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Trending Topics in Escherichia coli

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Trending
Topics in
Escherichia
coli Research
The Latin American Perspective
Second Edition
Trending Topics in Escherichia coli Research
Alfredo G. Torres
Editor

Trending Topics
in Escherichia coli Research
The Latin American Perspective

Second Edition
Editor
Alfredo G. Torres
Department of Microbiology and Immunology
University of Texas Medical Branch
Galveston, TX, USA

ISBN 978-3-031-29881-3    ISBN 978-3-031-29882-0 (eBook)


https://doi.org/10.1007/978-3-031-29882-0

© The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature
Switzerland AG 2016, 2023
This work is subject to copyright. All rights are solely and exclusively licensed by the Publisher, whether
the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of
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The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland
Foreword

The knowledge of the biology of the Escherichia coli species began at the end of the
nineteenth century when the species was first described and named Bacterium coli
commune by Theodor Escherich. Some strains belonging to this species were soon
identified by the same discoverer as potential cause of urinary tract and intestinal
infections in the subsequent 10 years, shortly before the species was renamed
after him.
The knowledge of the organism lagged until after World War II when W. H. Ewing,
from the communicable diseases center of Atlanta in the USA, observed that “In a
large number of otherwise unexpected epidemics of diarrheal disease of infants,
certain Escherichia coli serotypes are recovered”. This observation raised a certain
interest, and in the subsequent years, the reports of E. coli infections associated with
both intestinal and extraintestinal disease accumulated in the low- and high-income
countries, respectively, and the studies on the mechanisms of interaction between
these bacteria and the human host hinted at the extraordinary plasticity of this spe-
cies in deploying adhesion and invasion mechanisms as well as in producing toxins.
In the 1980s, the identification of a new pathogenic group of E. coli, Shiga toxin-­
producing E. coli (STEC), was determined to be the cause of severe forms of gastro-­
intestinal infections to humans and as the cause of hemolytic uremic syndrome
(HUS) in childhood, mostly preceded by diarrhea. This discovery boosted again the
microbiologists to study the organism and to decide to look deeper into the evolu-
tion of the pathogenic strains belonging to the E. coli species, gave pediatricians
treating children with HUS better tools to characterize their patients and study the
epidemiology and pathophysiology of the STEC infections and STEC-induced
hemolytic uremic syndrome (STEC-HUS), and stimulated researchers from various
backgrounds and all over the world to unravel the habits of these intriguing patho-
gens and their relation to disease. It was with the diffusion of polymerase chain
reaction and, later, of genomics that the understanding of how diverse and plastic
this species was made a quantum leap.

v
vi Foreword

As a matter of fact, the quick and sensitive detection of the genes associated to
virulence allowed an easier attribution of the E. coli strains isolated from the differ-
ent forms of illness to the different pathogenic types and permitted a deeper knowl-
edge of their circulation into their natural reservoirs, eventually shedding light on
their potential to expose and cause disease to humans and animals. At the same
time, the ability to delve into the phylogenesis brought the researchers to describe
the dynamics that led the different E. coli pathotypes and serotypes to diversify into
subpopulations with more potential to harm and cause disease.
The ability to completely sequence the genome of the pathogenic E. coli strains
permitted to determine the size of the core genome of the E. coli species, which is
largely used as a base for the strain typing, and to define the accessory genome,
conveying all the determinants linked to pathogenicity and conferring traits favoring
the survival and persistence of the species into countless niches.
One of the latest discoveries concerning the extreme plasticity of the E. coli spe-
cies is related with its talent for spreading mobile genetic elements conveying viru-
lence genes and generating cross-pathotype or hybrid strains. The first example of a
hybrid pathotype with a shuffled virulence repertoire was the Shiga toxin-producing
enteroaggregative E. coli (Stx-producing EAEC). Such a hybrid combination of
virulence features was first identified in an STEC strain of serogroup O111 associ-
ated with a small outbreak of hemolytic uremic syndrome (HUS) in France at the
beginning of the 1990s and followed 20 years later by the infamous O104:H4 strain
that caused in 2011 the largest outbreak occurred in Europe and the most severe
STEC epidemic ever reported. Retrospectively, similar strains of other serogroups
have been described in several sporadic cases and small outbreaks of infections in
Japan, Italy, and Northern Ireland.
The emergence of the Stx-producing EAEC seems to be linked to the acquisition
of an Stx-converting phage by an enteroaggregative E. coli strain, which is largely
supported by the high capacity of bacteriophages to infect E. coli and spread their
load of transduced genes, including the Stx-coding ones. Whole genome sequenc-
ing allowed the researchers to discover that, beside the Stx-producing EAEC, hybrid
combinations of virulence determinants can be found in E. coli strains belonging all
the E. coli pathotypes. Of public health impact are the Stx-producing ETEC and the
STEC with the virulence genes repertoire of extraintestinal pathogenic E. coli, often
isolated from severe forms of HUS with bacteremia, to mention a few of these.
The emergence of STEC strains with virulence genes of other E. coli pathotypes,
raise the point of how STEC, are to be identified. As a matter of fact, the ability of
Stx-phages to move between strains together with their wide diffusion in the reser-
voirs and the environment makes any E. coli potentially an STEC and suggests that
this pathotype could be considered an association of two organisms, a pathogenic
E. coli and an Stx-phage.
Even though more than 130 years have passed since its discovery, the species
E. coli continues to represent a public health problem around the world with new
groups of pathogenic strains continuously emerging. Their extreme genomic plas-
ticity generates new variants and pathotypes that prompt researchers to carry out
new studies and research to understand the extraordinary adaptability of this species.
Foreword vii

This book represents the most up-to-date collection of ideas and data produced
by scientists from Latin America and will certainly be the starting point for further
new knowledge to be produced by the global scientific community.

Stefano Morabito
European Reference Laboratory for E. coli
Microbiological food safety and food borne
diseases unit. Food safety, Nutrition,
and Veterinary Public Health Department
Istituto Superiore di Sanità
Roma, Italy
Nicole van de Kar
Department of Pediatric Nephrology, Radboud Institute
for Molecular Life Sciences, Amalia Children’s Hospital
Radboud University Medical Center
Nijmegen, The Netherlands
January 24, 2023
Preface

“You are the Petri dish to Escherichia coli, and it could be your friend or your foe”.

Pathogenic Escherichia coli infections remain a major global public health issue in
Latin America and around the globe, and despite efforts to combat human and ani-
mal infections, these bacteria remain associated with disease and significant mor-
bidity. In the Americas, the need to understand this pathogen and to tackle all the
challenges that E. coli infections posed to the medical, veterinary, research com-
munities and population at large resulted in the establishment of the Latin American
Coalition for E. coli Research (LACER). This regional scientific group was created
in 2009 to promote and expand the research efforts in the Americas using the One
Health model, to support and expand quality science within Latin American coun-
ties, to prepare the next generation of scientist-physicians and research investiga-
tors, and to work together with the community to translate regional scientific
findings into products improving the well-being of the population suffering from
E. coli infections. By 2023, the LACER group has grown to become a multidisci-
plinary network of more than 70 research groups in Latino America and the USA,
working on different aspects of pathogenic E. coli, including, but not restricted to,
epidemiology, pathogenesis, vaccine and therapeutic design and testing, public
health, surveillance, and clinical bacterial isolation and treatment.
One of the key missions of the LACER community is to disseminate their scien-
tific findings in the form of manuscripts, invited commentaries, social media post,
books, and interviews. As part of the efforts to bring the knowledge about these
bacteria to the students, researchers, and the community in general, the first book by
the LACER network was published in 2010 and entitled Pathogenic Escherichia
coli in Latin America. The central theme of this book was to present the current
understanding of the Latin American research community about pathogenic E. coli,
featuring comprehensive analysis of the most common categories of E. coli associ-
ated with diarrheal illness, as well as outlining prospects for future research in the
region. The second book was published in 2016 and entitled Escherichia coli in the
Americas. The theme of this book included a series of chapters written by Latin
American experts, covering basic concepts regarding the different categories of

ix
x Preface

E. coli, including their environmental niche, virulence mechanisms, host reservoir,


and disease outcomes, as well as diagnosis, vaccine development, and treatment.
This second book was written to target trainees and students learning about the
basic and clinical aspects of E. coli pathogenesis, but also providing information to
experts around the globe who wish to learn more about this pathogen and the public
health impact these bacteria is having in the Americas.
As the LACER network gained maturity with several consolidated research
groups who are driving novel research projects in the Latin American region, as
well as the presence of new investigators initiating their independent research
careers and laboratories, it was decided that it was time again to publish a book
displaying the talent of all these scientists and their recent research findings. This
third book is entitled Trending Topics in Escherichia coli Research. The Latin
American Perspective, and it represents a collection of chapters that have unique
characteristics: they are written by a multidisciplinary group of experts, and they all
emphasize research progress performed in the Latin American region. Many of the
topics included in this book are novel because they represent new areas of research
in the region including priority areas such as the One Health challenge to under-
stand E. coli isolated in the Americas as well as the need to monitor emergence of
antibiotic resistant strains. The other chapters present recent progress on under-
standing virulence of different pathogenic E. coli strains and their association with
human or animal infections or their presence in the environment. More specialized
chapters included in the book discussed the importance of phages in the lifestyle of
E. coli or the role of Shiga toxin and its effect on the central nervous system. Other
topics discussed the interactions of these bacteria with fresh produce and beef con-
sumption and the need of microbial risk assessments to predict food contamination
and increase prevention. Finally, the book also includes new areas of research
emerging in the Latin American region, such as the need to understand the associa-
tion of E. coli with intestinal microbiota and the emergence of hybrid pathogenic
E. coli strains. All these research advances required complete analysis of the E. coli
genomes to understand their pathogenic profiles and to help in the development of
novel therapeutic approaches.
As we continue advancing the goals of the LACER network for the benefit of the
Latin American community, we must keep in mind that the best approach to tackle
the challenges that we have in this region is to use One Health principles, because
they can help us assess the interdisciplinary interaction and interdependence
between health and wellbeing in a constantly changing environment. We must con-
tinue using these principles to encourage sustainable collaborative partnerships and
to promote optimal health for people, animals, plants, and the environment of the
Latin American region, information that can be exported to the whole world. In
Latin America, despite the concept still being discussed among health professionals
and educators, we have been incorporating several of the One Health initiatives in
the LACER goals.
LACER has become a network that is recognized by microbiological and other
scientific societies in Latin America and by E. coli investigators worldwide as a
group that has created a model that combines unique talent, expertise, and
Preface xi

collaborative attitudes that makes the group stronger together than apart. It is my
hope that this book motivates students and trainees to join LACER and become the
next generation of researchers in Latin America.

Galveston, TX, USA Alfredo G. Torres


January 12, 2023
Contents

1 WHO Critical Priority Escherichia coli in Latin America:


A One Health Challenge for a Post-Pandemic World��������������������������    1
Nilton Lincopan, Danny Fuentes-Castillo, Maria Espinoza-Muñoz,
Fernando Gonzales-Zubiate, Edgar Gonzales-Escalante,
Lenin Maturrano, Rafael Vignoli, Jose Di Conza,
and Gabriel Gutkind
2 Recent Progress on Enterotoxigenic E. coli (ETEC)
and Antibiotic Resistance in Pathogenic E. coli������������������������������������   33
Enrique Joffré, Jeannete Zurita, Carla Calderon Toledo,
and Sergio Gutiérrez-Cortez
3 New Concepts on Domestic and Wild Reservoirs
and Transmission of E. coli and Its Environment ��������������������������������   55
Adriana Bentancor, Ximena Blanco Crivelli, Claudia Piccini,
and Gabriel Trueba
4 New Molecular Mechanisms of Virulence and Pathogenesis
in E. coli����������������������������������������������������������������������������������������������������   79
Fernando Navarro-García, Antonio Serapio-Palacios,
Bertha González-­Pedrajo, Mariano Larzábal, Nora Molina,
and Roberto Vidal
5 Bovine Reservoir of STEC and EPEC: Advances
and New Contributions���������������������������������������������������������������������������� 107
Nora Lía Padola, Vinicius Castro, Analía Etcheverría,
Eduardo Figueiredo, Rosa Guillén, and Ana Umpiérrez
6 Phages and Escherichia coli�������������������������������������������������������������������� 129
Paula M. A. Lucchesi, Leticia V. Bentancor, Alejandra Krüger,
Edgar González-Villalobos, and José Molina-López

xiii
xiv Contents

7 Insights into Animal Carriage and Pathogen Surveillance


in Latin America: The Case of STEC and APEC �������������������������������� 149
Nicolás Galarce, Fernando Sánchez, Indira Kudva,
Erika N. Biernbaum, Terezinha Knöbl, and André B. S. Saidenberg
8 
Shiga Toxin and Its Effect on the Central Nervous System ���������������� 177
Alipio Pinto, Ana Beatriz Celi, and Jorge Goldstein
9 Relevance of Escherichia coli in Fresh Produce Safety������������������������ 205
Juan J. Luna-Guevara, Magaly Toro, Christian Carchi-Carbo,
Juan L. Silva, and M. Lorena Luna-Guevara
10 Quantitative Microbial Risk Assessment of Hemolytic
Uremic Syndrome due to Beef Consumption:
Impact of Interventions to Reduce the Presence
of Shiga Toxin-­Producing Escherichia coli�������������������������������������������� 229
Victoria Brusa, Mariana Cap, Gerardo Leotta, Marcelo Signorini,
and Sergio Vaudagna
11  Updated Overview on the Resistance and Virulence of UPEC������ 249
An
Edwin Barrios-Villa, Luciana Robino Picón,
Rodolfo Bernal Reynaga,
and Margarita María de la Paz Arenas-Hernández
12 Interactions of Pathogenic Escherichia coli
with Gut Microbiota�������������������������������������������������������������������������������� 277
Elizabeth Miliwebsky, María Ángela Jure, Mauricio J. Farfan,
and Marina Sandra Palermo
13 Emergence of Hybrid Escherichia coli Strains�������������������������������������� 295
Tânia Aparecida Tardelli Gomes, Ana Carolina de Mello Santos,
Rodrigo Tavanelli Hernandes, Monica Yurley Arias-Guerrero,
Ana Elvira Farfán-García, and Oscar G. Gómez-Duarte
14 Genomic Analysis of Pathogenic Escherichia coli Strains
in Latin America�������������������������������������������������������������������������������������� 317
Isabel Chinen, Carolina Carbonari, Natalie Weiler Gustafson,
Cindy Fabiola Hernández Pérez, Bruna Fuga,
and Narjol González-Escalona
15 
Therapeutic Options for Diarrheagenic Escherichia coli �������������������� 339
Alejandro Balestracci, Daniela Luz, Flavia Sacerdoti,
Maria Marta Amaral, Oscar G. Gómez-Duarte,
and Roxane Maria Fontes Piazza

Index������������������������������������������������������������������������������������������������������������������ 361
Contributors

Maria Marta Amaral Universidad de Buenos Aires, Facultad de Ciencias


Médicas, Departamento de Ciencias Fisiológicas. Laboratorio de Fisiopatogenia,
Buenos Aires, Argentina
CONICET – Universidad de Buenos Aires. Instituto de Fisiología y Biofísica
Bernardo Houssay (IFIBIO Houssay), Buenos Aires, Argentina
Margarita María de la Paz Arenas-Hernández Posgrado en Microbiología,
Centro de Investigación en Ciencias Microbiológicas, Instituto de Ciencias,
Benemérita Universidad Autónoma de Puebla, Puebla, Puebla, Mexico
Monica Yurley Arias-Guerrero Instituto de Investigaciones Masira, Facultad de
Ciencias Médicas y de la Salud, Universidad de Santander, Bucaramanga, Colombia
Alejandro Balestracci Unidad de Nefrología, Hospital General de Niños Pedro de
Elizalde, Ciudad Autónoma de Buenos Aires, Argentina
Edwin Barrios-Villa Universidad de Sonora, Departamento de Ciencias Químico
Biológicas y Agropecuarias, Caborca, Sonora, Mexico
Adriana Bentancor Universidad de Buenos Aires, Facultad de Ciencias
Veterinarias, Microbiología, CABA, Argentina
Leticia V. Bentancor Instituto de Estudios para el Desarrollo Productivo y la
Innovación (IDEPI), Universidad Nacional de José C. Paz (UNPaz), José C. Paz,
Pcia, Buenos Aires, Argentina
Rodolfo Bernal Reynaga Unidad de Investigaciones en Salud Pública “Dra.
Kaethe Willms,” Facultad de Ciencias Químico-Biológicas, Universidad Autónoma
de Sinaloa, Culiacán, Sinaloa, Mexico
Erika N. Biernbaum Food Safety and Enteric Pathogens Research Unit, National
Animal Disease Center, Agricultural Research Service, United States Department
of Agriculture, Ames, IA, USA
Oak Ridge Institute for Science and Education, Oak Ridge, TN, USA

xv
xvi Contributors

Ximena Blanco Crivelli Universidad de Buenos Aires, Facultad de Ciencias


Veterinarias, Microbiología, CABA, Argentina
Victoria Brusa IGEVET – Instituto de Genética Veterinaria “Ing. Fernando
N. Dulout” (UNLP-CONICET LA PLATA), Facultad de Ciencias Veterinarias,
Universidad Nacional de La Plata, Buenos Aires, Argentina
Carla Calderon Toledo Unidad de Microbiología Ambiental, Instituto de Biología
Molecular y Biotecnología (IBMB), Carrera de Biología, Universidad Mayor de
San Andrés, La Paz, Bolivia
Mariana Cap Instituto Tecnología de Alimentos, INTA, Buenos Aires, Argentina
Instituto de Ciencia y Tecnología de Sistemas Alimentarios Sustentables (UEDD
INTA-CONICET), Buenos Aires, Argentina
Carolina Carbonari Servicio Fisiopatogenia, Instituto Nacional de Enfermedades
Infecciosas – ANLIS “Dr. Carlos G. Malbrán”, Buenos Aires, Argentina
Christian Carchi-Carbo Institute of Nutrition and Food Technology, University
of Chile, Santiago, Chile
Vinicius Castro Department of Biological Science, University of Lethbridge
(ULETH), Lethbridge, AB, Canada
Ana Beatriz Celi Universidad de Buenos Aires, Facultad de Medicina,
Departamento de Ciencias Fisiológicas, Buenos Aires, Argentina
Universidad de Buenos Aires-CONICET, Instituto de Fisiología y Biofísica
“Houssay” (IFIBIO), Laboratorio de Neurofisiopatología, Buenos Aires, Argentina
Isabel Chinen Servicio Fisiopatogenia, Instituto Nacional de Enfermedades
Infecciosas – ANLIS “Dr. Carlos G. Malbrán”, Buenos Aires, Argentina
Jose Di Conza Facultad de Farmacia y Bioquímica, Instituto de Investigaciones en
Bacteriologia y Virología Molecular, Universidad de Buenos Aires, Buenos Aires,
Argentina
Maria Espinoza-Muñoz Hospital Seguro Social Universitario,
Cochabamba, Bolivia
Analía Etcheverría Universidad Nacional del Centro de la Provincia de Buenos
Aires, Facultad Ciencias Veterinarias, Departamento Sanidad Animal y Medicina
Preventiva- CIVETAN, Tandil, Buenos Aires, Argentina
Mauricio J. Farfan Departamento de Pediatría y Cirugía Infantil, Facultad de
Medicina, Universidad de Chile, Santiago, Chile
Ana Elvira Farfán-García Instituto de Investigaciones Masira, Facultad de
Ciencias Médicas y de la Salud, Universidad de Santander, Bucaramanga, Colombia
Eduardo Figueiredo Departamento de Alimentos e Nutrição, Universidade
Federal de Mato Grosso, Cuiabá, Mato Grosso, Brazil
Contributors xvii

Danny Fuentes-Castillo Departamento de Patología y Medicina Preventiva,


Facultad de Ciencias Veterinarias, Universidad de Concepción, Chillán, Chile
Bruna Fuga Departamento Microbiologia, Instituto de Ciências Biomédicas, São
Paulo, Brazil
Nicolás Galarce Escuela de Medicina Veterinaria, Facultad de Ciencias de la Vida,
Universidad Andrés Bello, Santiago, Chile
Jorge Goldstein Universidad de Buenos Aires, Facultad de Medicina,
Departamento de Ciencias Fisiológicas, Buenos Aires, Argentina
Universidad de Buenos Aires-CONICET, Instituto de Fisiología y Biofísica
“Houssay” (IFIBIO), Laboratorio de Neurofisiopatología, Buenos Aires, Argentina
Tânia Aparecida Tardelli Gomes Laboratório Experimental de Patogenicidade
de Enterobactérias, Disciplina de Microbiologia, Departamento de Microbiologia,
Imunologia e Parasitologia, Escola Paulista de Medicina, Universidade Federal de
São Paulo, São Paulo, SP, Brazil
Oscar G. Gómez-Duarte International Enteric Vaccine Research Program,
Division of Pediatric Infectious Diseases, Department of Pediatrics, State University
of New York at Buffalo, Buffalo, NY, USA
Division of Pediatric Infectious Diseases, Department of Pediatrics, State University
of New York (SUNY) at Buffalo, Buffalo, NY, USA
Edgar Gonzales-Escalante Facultad de Medicina, Universidad de Piura,
Lima, Peru
Fernando Gonzales-Zubiate Escuela de Ciencias Biológicas e Ingeniería,
Universidad Yachay Tech, San Miguel de Urcuquí, Ecuador
Narjol González-Escalona Division of Microbiology, Office of Regulatory
Science, Food and Drug Administration, Silver Spring, MD, USA
Bertha González-Pedrajo Departamento de Genética Molecular, Instituto de
Fisiología Celular, Universidad Nacional Autónoma de México, Mexico City, Mexico
Edgar González-Villalobos Laboratorio de Patogenicidad Bacteriana, Unidad de
Hemato-oncología e investigación, Hospital Infantil de México “Federico Gómez”,
Facultad de Medicina UNAM, México City, México
Rosa Guillén Instituto de Investigaciones en Ciencias de la Salud, Universidad
Nacional de Asunción, San Lorenzo, Paraguay
Sergio Gutiérrez-Cortez Unidad de Microbiología Ambiental, Instituto de
Biología Molecular y Biotecnología (IBMB), Carrera de Biología, Universidad
Mayor de San Andrés, La Paz, Bolivia
Gabriel Gutkind Facultad de Farmacia y Bioquímica, Instituto de Investigaciones
en Bacteriologia y Virología Molecular, Universidad de Buenos Aires, Buenos
Aires, Argentina
xviii Contributors

Rodrigo Tavanelli Hernandes Departamento de Ciências Químicas e Biológicas


(Setor de Microbiologia e Imunologia), Instituto de Biociências, Universidade
Estadual Paulista (UNESP), Botucatu, SP, Brazil
Cindy Fabiola Hernández Pérez Centro Nacional de Referencia de Plaguicidas y
Contaminantes – SENASICA, Ciudad de México, Mexico
Enrique Joffré Department of Microbiology, Tumor and Cell Biology (MTC),
Karolinska Institutet, Stockholm, Sweden
María Ángela Jure Cátedra de Bacteriología. Instituto de Microbiología Luis
C. Verna. Fac. de Bioquímica, Qca y Fcia. Universidad Nacional de Tucumán, San
Miguel de Tucumán, Argentina
Terezinha Knöbl Department of Pathology, School of Veterinary Medicine and
Animal Science – University of São Paulo (FMVZ-USP), São Paulo, SP, Brazil
Alejandra Krüger Universidad Nacional del Centro de la Provincia de Buenos
Aires (UNCPBA), Facultad de Ciencias Veterinarias, CISAPA, Tandil, Pcia. Buenos
Aires, Argentina
Centro de Investigación Veterinaria de Tandil (CIVETAN), UNCPBA-­CICPBA-­
CONICET, Tandil, Pcia. Buenos Aires, Argentina
Indira Kudva Food Safety and Enteric Pathogens Research Unit, National Animal
Disease Center, Agricultural Research Service, United States Department of
Agriculture, Ames, IA, USA
Mariano Larzábal Instituto de Agrobiotecnología y Biología Molecular INTA-­
CONICET, Hurlingham, Buenos Aires, Argentina
Gerardo Leotta Instituto de Ciencia y Tecnología de Sistemas Alimentarios
Sustentables (UEDD INTA-CONICET), Buenos Aires, Argentina
Nilton Lincopan Departamento de Microbiologia, Instituto de Ciências
Biomédicas, Universidade de São Paulo, São Paulo, Brazil
Paula M. A. Lucchesi Universidad Nacional del Centro de la Provincia de Buenos
Aires (UNCPBA), Facultad de Ciencias Veterinarias, CISAPA, Tandil, Pcia. Buenos
Aires, Argentina
Centro de Investigación Veterinaria de Tandil (CIVETAN), UNCPBA-­CICPBA-­
CONICET, Tandil, Pcia. Buenos Aires, Argentina
Juan J. Luna-Guevara College of Food Engineering, Faculty of Chemical
Engineering, Meritorious Autonomous University of Puebla, Puebla, Mexico
M. Lorena Luna-Guevara College of Food Engineering, Faculty of Chemical
Engineering, Meritorious Autonomous University of Puebla, Puebla, Mexico
Daniela Luz Laboratório de Bacteriologia, Instituto Butantan, São Paulo, SP, Brazil
Contributors xix

Lenin Maturrano Facultad de Medicina Veterinaria, Universidad Nacional Mayor


de San Marcos, Lima, Peru
Elizabeth Miliwebsky Servicio Fisiopatogenia, Departamento de Bacteriología,
Instituto Nacional de Enfermedades Infecciosas” Carlos G. Malbrán”, CABA,
Argentina
Nora Molina Centro Universitario de Estudios Microbiológicos y Parasitológicos,
Facultad de Ciencias Médicas, Universidad Nacional de La Plata, Buenos Aires,
Argentina
José Molina-López Laboratorio de Patogenicidad Bacteriana, Unidad de Hemato-­
oncología e investigación, Hospital Infantil de México “Federico Gómez”, Facultad
de Medicina UNAM, México City, México
Fernando Navarro-García Department of Cell Biology, Centro de Investigación
y de Estudios Avanzados, Mexico City, Mexico
Nora Lía Padola Universidad Nacional del Centro de la Provincia de Buenos
Aires, Facultad Ciencias Veterinarias, Departamento Sanidad Animal y Medicina
Preventiva- CIVETAN, Tandil, Buenos Aires, Argentina
Marina Sandra Palermo Instituto de Medicina Experimental (IMEX) CONICET-­
Academia Nacional de Medicina, CABA, Argentina
Roxane Maria Fontes Piazza Laboratório de Bacteriologia, Instituto Butantan,
São Paulo, SP, Brazil
Claudia Piccini Departamento de Microbiología, Instituto de Investigaciones
Biológicas Clemente Estable, Montevideo, Uruguay
Alipio Pinto Universidad de Buenos Aires, Facultad de Medicina, Departamento
de Ciencias Fisiológicas, Buenos Aires, Argentina
Universidad de Buenos Aires-CONICET, Instituto de Fisiología y Biofísica
“Houssay” (IFIBIO), Laboratorio de Neurofisiopatología, Buenos Aires, Argentina
Luciana Robino Picón Universidad de la Republica, Facultad de Medicina,
Instituto de Higiene, Departamento de Bacteriologia y Virologia,
Montevideo, Uruguay
Flavia Sacerdoti Universidad de Buenos Aires, Facultad de Ciencias Médicas,
Departamento de Ciencias Fisiológicas. Laboratorio de Fisiopatogenia, Buenos
Aires, Argentina
CONICET – Universidad de Buenos Aires. Instituto de Fisiología y Biofísica
Bernardo Houssay (IFIBIO Houssay), Buenos Aires, Argentina
André B. S. Saidenberg Department of Pathology, School of Veterinary Medicine
and Animal Science – University of São Paulo (FMVZ-USP), São Paulo, SP, Brazil
xx Contributors

Fernando Sánchez Departamento de Medicina Preventiva Animal, Facultad de


Ciencias Veterinarias y Pecuarias, Universidad de Chile, Santiago, Chile
Ana Carolina de Mello Santos Laboratório Experimental de Patogenicidade de
Enterobactérias, Disciplina de Microbiologia, Departamento de Microbiologia,
Imunologia e Parasitologia, Escola Paulista de Medicina, Universidade Federal de
São Paulo, São Paulo, SP, Brazil
Antonio Serapio-Palacios Michael Smith Laboratories, University of British
Columbia, Vancouver, BC, Canada
Marcelo Signorini Instituto de Investigación de la Cadena Láctea (IdICaL)
(CONICET-INTA), EEA Rafaela, INTA, Santa Fe, Argentina
Juan L. Silva Department of Food Science and Technology, Mississippi State
University, Starkville, MS, USA
Magaly Toro Joint Institute for Food Safety and Applied Nutrition, University of
Maryland, College Park, MD, USA
Institute of Nutrition and Food Technology (INTA), University of Chile,
Santiago, Chile
Gabriel Trueba Instituto de Microbiología, Colegio de Ciencias Biológicas y
Ambientales, Universidad San Francisco de Quito, Vía Interoceánica y Diego de
Robles, Cumbayá, Quito, Ecuador
Ana Umpiérrez Departamento de Microbiología, Instituto de Investigaciones
Biológicas Clemente Estable, Montevideo, Uruguay
Sergio Vaudagna Instituto Tecnología de Alimentos, INTA, Buenos Aires,
Argentina
Instituto de Ciencia y Tecnología de Sistemas Alimentarios Sustentables (UEDD
INTA-CONICET), Buenos Aires, Argentina
Roberto Vidal Instituto de Ciencias Biomédicas, Universidad de Chile,
Santiago, Chile
Rafael Vignoli Departamento de Bacteriología y Virología, Facultad de Medicina,
Universidad de la República, Montevideo, Uruguay
Natalie Weiler Gustafson Laboratorio Central de Salud Pública, Ministerio de
Salud Pública y Bienestar Social, Asunción, Paraguay
Jeannete Zurita Unidad de investigaciones en Biomedicina. Zurita y Zurita
Laboratorios, Facultad de Medicina, Pontificia Universidad Católica del Ecuador,
Quito, Ecuador
Chapter 1
WHO Critical Priority Escherichia coli
in Latin America: A One Health Challenge
for a Post-Pandemic World

Nilton Lincopan, Danny Fuentes-Castillo, Maria Espinoza-Muñoz,


Fernando Gonzales-Zubiate, Edgar Gonzales-Escalante, Lenin Maturrano,
Rafael Vignoli, Jose Di Conza, and Gabriel Gutkind

Chapter Summary The dissemination of carbapenem-resistant and third genera-


tion cephalosporin-resistant pathogens, classified as priority pathogens by the World
Health Organization (WHO), is a critical issue that is no longer restricted to hospital
settings. In this regard, in Escherichia coli, resistance to these last resort β-lactam
antibiotics is mediated by the production of carbapenemases and extended-­spectrum
beta-lactamases (ESBLs). In South American countries, several types of ESBLs
have been detected, including TEM-, SHV-, and CTX-M-type variants (e.g.,
­CTX-­M-­2, -3, -8, -9, -14, -15, -27, -55, -65). However, CTX-M has been the most

N. Lincopan (*)
Departamento de Microbiologia, Instituto de Ciências Biomédicas, Universidade de São
Paulo, São Paulo, Brazil
e-mail: lincopan@usp.br
D. Fuentes-Castillo
Departamento de Patología y Medicina Preventiva, Facultad de Ciencias Veterinarias,
Universidad de Concepción, Chillán, Chile
M. Espinoza-Muñoz
Hospital Seguro Social Universitario, Cochabamba, Bolivia
F. Gonzales-Zubiate
Escuela de Ciencias Biológicas e Ingeniería, Universidad Yachay Tech,
San Miguel de Urcuquí, Ecuador
E. Gonzales-Escalante
Facultad de Medicina, Universidad de Piura, Lima, Peru
L. Maturrano
Facultad de Medicina Veterinaria, Universidad Nacional Mayor de San Marcos, Lima, Peru
R. Vignoli
Departamento de Bacteriología y Virología, Facultad de Medicina, Universidad de la
República, Montevideo, Uruguay
J. Di Conza · G. Gutkind
Facultad de Farmacia y Bioquímica, Instituto de Investigaciones en Bacteriologia y Virología
Molecular, Universidad de Buenos Aires, Buenos Aires, Argentina

© The Author(s), under exclusive license to Springer Nature 1


Switzerland AG 2023
A. G. Torres (ed.), Trending Topics in Escherichia coli Research,
https://doi.org/10.1007/978-3-031-29882-0_1
2 N. Lincopan et al.

widespread ESBL group. Endemic status of CTX-M-positive E. coli strains in the


region is associated with the successful expansion of international clones belonging
to sequence types (STs) ST2, ST10, ST38, ST44, ST58, ST90, ST115, ST131,
ST155, ST167, ST224, ST354, ST410, ST457, ST517, ST648, and ST711, which
are shared between human and animal (pets, wildlife, and food-producing) hosts,
and polluted aquatic environments. Regarding carbapenem resistance, the increased
frequency of reports on carbapenemases in Latin America shows that they have suc-
cessfully spread, becoming endemic in some countries, such as Argentina, Colombia,
and Brazil. In this respect, carbapenem-resistant E. coli belonging to global ST10,
ST48, ST90, ST131, ST155, ST167, ST224, ST349, ST354, ST457, ST502, ST648,
ST730, and ST744 clones have been isolated from humans, in association with the
production of KPC-2 or NDM-1 carbapenemases. After the COVID-19 pandemic, a
major concern has been the appearance of more virulent and resistant E. coli strains.
The convergence of wide resistome and virulome is contributing to the persistence
and rapid spread of international high-risk clones of critical priority E. coli at the
human-animal-environmental interface, which must be considered a One Health
challenge for a post-pandemic scenario. Here, we present updated information on
the status of WHO critical priority E. coli in Latin America.

1.1 Introduction

The dissemination of oximino-cephalosporins and/or carbapenem-resistant E. coli


is a major public health concern worldwide, no longer restricted to hospital settings.
E. coli and other clinically relevant Gram-negative bacteria have developed several
mechanisms of resistance, including the production of β-lactamases, efflux pumps,
and porin mutations. However, most clinical and epidemiologically relevant resis-
tance mechanisms are the production of extended-spectrum β-lactamases (ESBLs)
and carbapenemases, whose genes rapidly spread by horizontal gene transfer. In
2017, the WHO published the global priority list of antibiotic-resistant bacteria to
guide research, discovery, and development of new antibiotics (Tacconelli et al.
2018). In this list, ESBL-producing and carbapenem-resistant E. coli are included
as a critical priority.
Historically, oximino-cephalosporins became available for clinical use in South
America in the early 1980s. In 1988 and 1989, first ESBLs were reported in
Argentina and Chile, in clinical Klebsiella pneumoniae strains carrying blaSHV-2 and
blaSHV-5 genes, respectively. In 1992, production of CTX-M-2 ESBL was reported in
Salmonella enterica serovar Typhimurium in Argentina. Currently, CTX-M has
been the most widespread ESBL group in this region, and although ESBLs in human
samples are most studied, ESBLs in food, livestock, companion animal, and envi-
ronmental samples have been prevalent. CTX-M-producing E. coli clones ST131
and ST10 are the most widespread clones found in South America, and migratory
species of birds have been identified as reservoirs. On the other hand, CTX-M-2 and
CTX-M-8 have been identified in E. coli from poultry and chicken meat samples,
1 WHO Critical Priority Escherichia coli in Latin America: A One Health… 3

supporting that ESBL-producing E. coli strains have also adapted to the agribusi-
ness sector (Fig. 1.1).
At the end of the 1980s, imipenem was the first carbapenem available for clinical
use in Latin American countries, and although surveillance studies began to report
imipenem resistance, almost 20 years after its introduction, the first report of a
member of the Enterobacterales order producing a carbapenemase was found related

Fig. 1.1 Distribution and sources of extended-spectrum beta-lactamase (ESBL)- and/or


carbapenemase-­producing Escherichia coli in South America
4 N. Lincopan et al.

to production of the IMP-1 metallo-beta-lactamase (MBL) by a clinical K. pneu-


moniae strain in Brazil. Nowadays, production of KPC-2 serine-carbapenemase has
been the main mechanism of carbapenem resistance in E. coli, with NDM-1 rapidly
emerging among isolates from Argentina and Brazil (García-Betancur et al., 2021).
Therefore, the rapid spread of critical priority pathogens in South America is wor-
rying, considering the dimension of the continent, diversity of international trade,
livestock production, and human travel.

1.1.1 Critical Priority E. coli in Brazil

Resistance to third generation cephalosporins is a particularly significant issue in


Brazil. Although occurrence of ESBL producers was early documented in 1997, in
private and public tertiary hospitals located in Rio de Janeiro and São Paulo
(Sampaio and Gales 2016), the first molecular studies were published in 2000
(Bonnet et al. 2000), evidencing predominance of CTX-M ESBL variants, and
describing the emergence of the novel CTX-M-8 enzyme, in strains other than
E. coli, from Rio de Janeiro. Currently, CTX-M enzymes are the most prevalent
among E. coli strains, becoming endemic in clinical settings (Table 1.1).
In 2001, two blaCTX-M genes encoding β-lactamases of pI 7.9 and 8.2 were impli-
cated in resistance to broad-spectrum cephalosporins. While the blaCTX-M-9 gene was
observed in the E. coli strain Rio-7, a novel CTX-M-encoding gene, designated
blaCTX-M-16, was identified in the E. coli strain Rio-6 (Bonnet et al. 2001). Interestingly,
both strains were isolated in 1996, whereas a study published in 2012, revealed that
CTX-M-2- and CTX-M-59-producing E. coli were already associated with human
infections in 2000. While E. coli strains producing CTX-M-14 and CTX-M-15 were
isolated in 2006 (Cergole-Novella et al. 2010), the novel CTX-M-8 emerged in
E. coli in 2008, 8 years after its first identification in 1996 (Bonnet et al. 2000;
Peirano et al. 2011). After 2016, CTX-24-, CTX-M-27-, and CTX-M-55-positive
E. coli strains were isolated from human infections, denoting an epidemiological
change, following a global trend (Table 1.1).
Among human isolates of CTX-M-producing E. coli circulating in Brazil, viru-
lent clones belonging to global ST131, ST410, ST127, and ST354 have been identi-
fied. In this regard, the emergence of the ST131 C1-M27 high-risk extraintestinal
pathogenic lineage is of critical concern (Soncini et al. 2022). In fact, this lineage
has been recently identified in sea food and vegetable samples (Fernandes et al.
2020; Lopes et al. 2022).
Dissemination of CTX-M E. coli beyond hospital walls is another public health
concern in Brazil. In this respect, CTX-M-8 E. coli were initially identified in live-
stock in 2010 (Aizawa et al. 2014). However, the main problem has been the occur-
rence of CTX-M-2-, CTX-M-8-, CTX-M-15-, and CTX-M-55-producing E. coli in
poultry, since Brazil is the world’s largest poultry exporter and third largest pro-
ducer (https://brazilianfarmers.com/category/discover/poultry/). Strikingly, interna-
tional lineages of CTX-M-positive E. coli belonging to ST58, ST90, ST131, ST155,
1 WHO Critical Priority Escherichia coli in Latin America: A One Health… 5

Table 1.1 Characteristics of WHO critical priority E. coli circulating at the human-animal-food-­
environmental interface in Brazil and Argentina

Country Source ESBL Carbapenemase MLST Year References


Brazil Human CTX-M-9, – 1996 Bonnet et al.
CTX-M-16 (2001)
Human CTX-M-2 – 2000 Queiroz
et al. (2012)
Human CTX-M-59 ST34 2000 Queiroz
et al. (2012)
Human CTX-M-2 ST533 2001 Minarini
et al. (2007)
Human SHV-5 ST528 2001 Minarini
et al. (2007)
Human CTX-M-2 ST62, ST127, 2003– Berman et al.
ST167, ST359, 2008 (2014)
ST362, ST405,
ST652
Human SHV-5 – 2005 Dropa et al.
(2015)
Human CTX-M-14, – 2006 Cergole-­
CTX-M-15 Novella et al.
(2010)
Human CTX-M-15 ST998 2006 Berman et al.
(2014)
Human – KPC-2 – 2008 Carvalho-­
Assef et al.
(2010)
Human CTX-M-15 ST131, ST410 2008– Peirano et al.
2009 (2011)
Human CTX-M-8 – 2008– Peirano et al.
2009 (2011)
Human CTX-M-15 KPC-2 ST502 – Almeida
et al. (2012)
Human CTX-M-14 ST127 2009 Berman et al.
(2014)
Human CTX-M-2, ST354 2015 Conceição-­
CTX-M-15 Neto et al.
(2017)
Human CTX-M-2, KPC-2 ST90 2013 Fuga et al.
14, 15 (2022)
Human – KPC-2 ST648 2013 Fuga et al.
(2022)
Human – NDM-1 – 2013 Campos
et al. (2015)
Human – NDM-1 ST707 2014 Fuga et al.
(2022)
Human – KPC-2 ST744 2014 Dalmolin
et al. (2017)
(continued)
6 N. Lincopan et al.

Table 1.1 (continued)

Country Source ESBL Carbapenemase MLST Year References


Human – KPC-2 ST167 2015 Conceição-­
Neto et al.
(2017)
Human – KPC-2 ST224 2015 Fuga et al.
(2022)
Human – KPC-2 ST457 2015 Fuga et al.
(2022)
Human CTX-M-24 KPC-2 ST354 2016 Dias et al.
(2022)
Human – NDM-1 ST155 2016 Fuga et al.
(2022)
Human CTX-M-24, ST354, ST131 2016– Soncini et al.
CTX-M-27 2019 (2022)
Human CTX-M-8, ST117 2017 Fernandes
CTX-M-55 et al. (2018a)
Human – NDM-1 ST744, ST349 2017 Fuga et al.
(2022)
Human CTX-M-15 KPC-2 ST648 2017 Fuga et al.
(2021)
Human – NDM-1 ST48, ST167 2018 Fuga et al.
(2022)
Human KPC-2 2509 2019 Fuga et al.
(2022)
Food-­ CTX-M-8 ST224, 2010 Aizawa et al.
producing ST2179, (2014)
animal ST2308
(buffalo)
Food-­ CTX-M-2 ST93, ST155, 2011– Ferreira et al.
producing ST2309 2012 (2014a)
animal
(chicken)
Food-­ CTX-M-8 ST155, 2012 Ferreira et al.
producing ST1011, (2014b)
animal ST2197,
(chicken) ST2929
Food-­ CTX-M-15 ST224, ST410, 2012 Silva et al.
producing ST1284 (2016)
animal
(swine)
Food-­ CTX-M-2 – 2012 da Silva
producing et al. (2017)
animal
(Turkey)
(continued)
1 WHO Critical Priority Escherichia coli in Latin America: A One Health… 7

Table 1.1 (continued)

Country Source ESBL Carbapenemase MLST Year References


Food-­ CTX-M-55 ST457, ST453, 2013– Cunha et al.
producing ST117, ST1706 2016 (2017)
animal
(broiler)
Food-­ CTX-M-15 ST90 2014 Sartori et al.
producing (2017)
animal (calf/
cow)
Food-­ CTX-M-2 ST443 2014 Palmeira
producing et al. (2018)
animal
(cattle)
Food-­ CTX-M-2 ST57, ST1158, 2019 Dos Anjos
producing ST2369, et al. (2022)
animal ST10064
(poultry)
Food-­ CTX-M-8 ST106, ST117, 2019 Dos Anjos
producing ST345, ST2179 et al. (2022)
animal
(poultry)
Food-­ CTX-M-15 ST224 2019 Dos Anjos
producing et al. (2022)
animal
(poultry)
Food-­ CTX-M-55 ST58, ST93, 2019 Dos Anjos
producing ST131,ST155, et al. (2022)
animal ST162, ST224,
(poultry) ST295,ST366,
ST1485,
ST2607
Food-­ SHV-12 ST93 2019 Dos Anjos
producing et al. (2022)
animal
(poultry)
Companion CTX-M-15 ST2179 2012 Leigue et al.
animal (2015)
(horse)
Companion CTX-M-2 ST371, ST457, 2012 Melo et al.
animal (dog, ST155, ST457 (2018)
cat)
Companion CTX-M-8 ST58, ST372, 2012 Melo et al.
animal (dog) ST2541 (2018)
Companion CTX-M-9 ST10, ST3395 2012 Melo et al.
animal (dog) (2018)
(continued)
8 N. Lincopan et al.

Table 1.1 (continued)

Country Source ESBL Carbapenemase MLST Year References


Companion CTX-M-15 ST90 2012 Melo et al.
animal (dog) (2018)
Companion CTX-M-16 ST3267 2012 Melo et al.
animal (dog) (2018)
Companion CTX-M-8 ST711 2012 Fernandes
animal et al. (2018b)
(horse)
Companion CTX-M-8 ST224 2015 Silva et al.
(cat) (2018)
Companion CTX-M-2, ST648 2017 Fernandes
animal (cat) CTX-M-15 et al. (2018c)
Companion CTX-M-15 KPC-2 ST648 2017 Sellera et al.
animal (dog) (2018b)
Synanthropic CTX-M-8 ST359 2012 Borges et al.
animal (2017a)
(pigeon)
Wildlife CTX-M-8 – 2010– Borges et al.
(wild bird) 2012 (2017b)
Wildlife CTX-M-2 ST744 2016 Sellera et al.
(fish) (2018a)
Wildlife CTX-M-55 ST746 2016 Sellera et al.
(fish) (2018a)
Wildlife CTX-M-55 ST212, ST744 2017– De Carvalho
(vulture, owl, 2018 et al. (2020)
coati)
Wildlife CTX-M-2 ST58 2017– De Carvalho
(coati) 2018 et al. (2020)
Wildlife CTX-M-15 ST1251 2017– De Carvalho
(coati) 2018 et al. (2020)
Wildlife CTX-M-2 ST1158 2017– De Carvalho
(vulture) 2018 et al. (2020)
Wildlife CTX-M-14 ST38 2017– De Carvalho
(vulture) 2018 et al. (2020)
Wildlife – NDM-1 ST156 2018 Wink et al.
(penguin) (2022)
Wildlife CTX-M-8 ST131 2018– Ewbank
(seabirds) 2019 et al. (2022a)
Wildlife SHV-12 ST177 2018– Ewbank
(frigatebirds) 2019 et al. (2022a)
Wildlife CTX-M-55 ST11350 2018– Ewbank
(frigatebirds) 2019 et al. (2022a)
(continued)
1 WHO Critical Priority Escherichia coli in Latin America: A One Health… 9

Table 1.1 (continued)

Country Source ESBL Carbapenemase MLST Year References


Wildlife CTX-M-8 ST58 2019 Fuentes-­
(merganser) Castillo et al.
(2021)
Wildlife CTX-M-2 ST648 2020 Ewbank
(frigatebird) et al. (2022b)
Wildlife – NDM-1 ST162 2020 Sellera et al.
(whale) (2022)
Captive CTX-M-65 ST156 2017 Rueda
animal (giant Furlan et al.
anteater) (2019)
Captive CTX-M-8 ST410 2018 Furlan et al.
animal (2020)
(elephant)
Food (meat) CTX-M-2 – 2006 Warren et al.
(2008)
Food CTX-M-15 – 2010– Botelho et al.
(chicken 2011 (2015)
carcasses)
Food CTX-M-2 – 2011 Casella et al.
(chicken (2015)
meat)
Food CTX-M-8 – 2013 Casella et al.
(chicken (2015)
meat)
Food CTX-M-15 ST345 2014 Casella et al.
(chicken (2017)
meat)
Food (sea CTX-M-27 ST38, ST131 2016 Fernandes
food) et al. (2020)
Food CTX-M-15 ST38, ST648, 2016 Lopes et al.
(vegetable) ST14012 (2021a)
Food (sea CTX-M-14 ST4012 2016– Bueris et al.
food) 2017 (2022)
Food CTX-M-55 ST117 2016– Soncini et al.
(chicken and 2019 (2022)
pork meat)
Food CTX-M-44 – – Iark et al.
(chicken (2018)
meat)
Food CTX-M-27 KPC-2 ST131 2019 Lopes et al.
(vegetable) (2022)
Environment CTX-M – 2008 Chagas et al.
(hospital (2011)
wastewater)
(continued)
10 N. Lincopan et al.

Table 1.1 (continued)

Country Source ESBL Carbapenemase MLST Year References


Environment CTX-M-15 ST4401 2009 Dropa et al.
(sewage) (2016)
Environment CTX-M-8 ST4445, 2009 Dropa et al.
(sewage) ST4402, (2016)
ST4403
Environment CTX-M-2, – 2012– Conte et al.
(wastewater) CTX-M-5, 2013 (2017)
CTX-M-8,
CTX-M-9,
CTX-M-­
15,SHV-12
Environment CTX-M-2, – 2012– Conte et al.
(superficial CTX-M-3, 2013 (2017)
water) CTX-M-8,
CTX-M-9,
CTX-M-15,
Environment CTX-M-15 ST617 2012– Nascimento
(urban lake) 2013 et al. (2017)
Environment CTX-M-8 ST58 2017 Sacramento
(mangrove) et al. (2018)
Environment CTX-M-15 ST131 2019 Lopes et al.
(agricultural (2021b)
soil)
Argentina Human CTX-M-2, – ST131 2010 Rincón Cruz
CTX-M-14, et al. (2013)
CTX-M-15
Human – KPC-2 – 2010 Anchordoqui
et al. (2015)
Human CTX-M-15 KPC-2 ST131 2011– De Belder
2014 et al. (2018)
Human CTX-M-2, KPC-2, KPC/ ST10, ST131 2012, Sanz et al.
CTX-M-15 OXA-439, 2014– (2022)
KPC-2/ 2017
OXA-163,
IMP-8,
VIM-­1,NDM-1
Human CTX-M-2, – – 2012– Faccone
CTX- 2018 et al. (2020)
M-­9/14,
CTX-
M-­8/25,
CTX-
M-­1/15,
PER-2
Human – NDM-1 – 2014 Martino
et al. (2019)
(continued)
1 WHO Critical Priority Escherichia coli in Latin America: A One Health… 11

Table 1.1 (continued)

Country Source ESBL Carbapenemase MLST Year References


Human CTX- KPC-2 ST131 2015– Figueroa-­
M-­9/14 2016 Espinosa
et al. (2019)
Human – IMP-8 – 2016 Elena et al.
(2018)
Human – NDM-5 – 2018 Costa et al.
(2021)
Human – KPC-2 ST730 2019 Álvarez et al.
(2022)
Human CTX-M-14 OXA-232 – 2020 Garcia et al.
(2022)
Food-­ CTX-M-2, – 2014 Dominguez
producing CTX-M-14 et al. (2017,
animal 2018)
(poultry)
Food-­ CTX- ‘ ST95, ST131 2017 Faccone
producing M-­8/25, et al. (2019)
animal CTX-
(swine) M-­1/15,
CTX-M-2,
CTX-
M-­9/14,
PER-2
Companion CTX-M-2, – – 2014 Rumi et al.
animal (dog, CTX-M-14, (2019)
cat) CTX-M-15
Wildlife CTX-M-14 – – 2012 Liakopoulos
(kelp gulls) CTX-M-2 et al. (2016)
Food CTX-M-2 – – 2017– Rumi et al.
(minced 2018 (2021b)
meat)
Environment CTX-M-2 – – 2018 Ghiglione
(wastewater) et al. (2019,
2020)
Environment CTX-M – – 2021– Gonzalez
(lake, 2022 et al. (2022)
sediment/
water)

ST224, and ST410 seem to have adapted to the production chain of chicken and
other foods. Indeed, since 2006, CTX-M-2-, CTX-M-8-, CTX-M-14, CTX-M-15-,
and CTX-M-55-positive E. coli strains of ST38, ST345, ST117, ST648, or ST4012
have been increasingly identified in chicken and pork meat and vegetables
(Table 1.1).
Companion animals and wildlife have also been colonized or infected by ESBL-­
producing E. coli. Since 2012, surveillance studies have documented the occurrence
12 N. Lincopan et al.

of E. coli producing CTX-M-2, CTX-M-8, and CTX-M-15 belonging to ST10,


ST58, ST90, ST224, and ST648 in dogs, cats, and horses, whereas those CTX-M
variants, CTX-M-14 and CTX-M-55 ESBLs, have been identified among E. coli of
ST38, ST58, ST131, ST410, and ST648 isolated from samples collected in wild
animals. To monitor the impact of antimicrobial resistance on the environment, the
role of wildlife as bioindicators or sentinels has begun to be studied, because most
Brazilian urban areas with aquatic environments have been anthropogenically
impacted. As such, E. coli strains producing CTX-M-2, CTX-M-8, or CTX-M-15
have been isolated from sewage, wastewater, and surface water. Of note, E. coli
CTX-M-8/ST58 and CTX-M-15/ST13 have been isolated from mangrove and agri-
cultural soil samples.
The increased frequency of reports on carbapenemases in this country shows that
they have successfully spread. While KPC-2 has an endemic status, production of
NDM-1 is becoming frequent. From the first description, in 2010, of KPC-2 in
E. coli (D’Alincourt Carvalho-Assef et al. 2010), lineages related to ST90, ST167,
ST224, ST354, ST457, ST649, and ST744 have acquired the blaKPC-2 gene
(Table 1.1), producing severe infections in hospital settings. Specifically, E. coli
KPC-2/ST648 has persisted since 2013, and recently it has expanded to veterinary
medicine, causing the first case of fatal infection in a dog (Sellera et al. 2018b).
Moreover, E. coli ST131 co-producing KPC-2 and CTX-M-27 has been detected in
fresh vegetables. In human medicine, NDM-1 metallo-β-lactamases have been suc-
cessfully incorporated by E. coli lineages of ST48, ST155, ST167, ST349, ST707,
and ST744, from 2013 (Table 1.1). Of concern, NDM-1-producing E. coli belong-
ing to ST156 and ST162 have been identified in marine wildlife, representing an
emerging ecological threat to marine ecosystems, since anthropogenic pollution and
infectious diseases have been the most notorious threats for vulnerable and endan-
gered species.

1.1.2 Critical Priority E. coli in Argentina

Even if resistance of third generation cephalosporins (TGC) was originally due to


the presence of TEM and SHV mutants with an extended spectrum activity, or de-­
repression of chromosomal AmpCs, CTX-M-2 was (after emerging in different
Salmonella serotypes) the first and most prevalent ESBL for decades, in different
microorganisms such as E. coli (Rossi et al. 1995; Radice et al. 1994). A prior
manuscript summarizes early dissemination reports in different meetings previously
unpublished (Radice et al. 2002).
A 1-month-period prospective study conducted in 2000 from public hospitals in
Buenos Aires clearly displayed CTX-M-2 as the most prevalent ESBL produced by
E. coli and other Enterobacterales (Quinteros et al. 2003). The same conclusion was
obtained after analyzing consecutive isolates from the same year in a single hospital
in Posadas, Misiones (Quiroga et al. 2008). Since then and assuming the endemic
presence of this enzyme, no interventions were aimed at preventing emergence and
1 WHO Critical Priority Escherichia coli in Latin America: A One Health… 13

dissemination of other ESBLS (and their accompanying resistance) until a multi-


center survey, carried out in 2010, with 15 hospitals from three regions, showed an
increased prevalence of ESBL-producing enterobacteria, due to an accumulation of
CTX-M-2 still in circulation in addition to CTX-M-15 and to a lesser extent CTX-­
M-­14 emergence, which was observed in E. coli isolates (some belonging already to
ST131) (Sennati et al. 2012). Marchisio et al. found that outpatient urine cultures in
two health institutions from Santa Fe city rendered only a single TGC-resistant
E. coli isolate (1.6%) due to the presence of plasmidic CMY-2 (Marchisio et al.
2015). A previous multicenter prospective study conducted for 3 months of 2009
detected 0.9% of pAmpC enzymes in enterobacteria, with CMY-2-producing E. coli
as the most prevalent (Cejas et al. 2012).
A prospective study of TGC-resistant E. coli isolates recovered from January
2013 to March 2015 at the Hospital Regional de Ushuaia, Tierra del Fuego prov-
ince, displayed CTX-M-1/15 (54%) as the most prevalent ESBL followed by CTX-­
M-­9/14 (25%) and CTX-M-2 (17%) (Gramundi et al. 2022). A similar study
including all clinically relevant Enterobacterales isolated in December 2012 and
April 2013, from infected patients in four health institutions at Santa Fe city,
revealed that TGC resistance in the recovered E. coli (n = 16) was due to CTX-M-2
(n = 5), CTX-M-9/14 (n = 4), CTX-M-1/15 (n = 3), CMY-2 (n = 3), and PER-2
(n = 1) (Marchisio et al. 2021).
Even if no resistance mechanisms are analyzed, electronic reports from the
national surveillance program show almost TGC resistance levels in E. coli (18% in
2010 to 20 or 23.4% in 2021) (Vigilancia Nacional de la Resistencia a los
Antimicrobianos Argentina, Tendencia 2010–2021 – Red WHONET, visited
2022-12-01 (http://antimicrobianos.com.ar/category/resistencia/whonet/analisis-­
de-­ram/). From the same report, TGC resistance among community-onset E. coli
urinary tract infections was 8% in 2020, with strong differences accordingly to age
and sex (15% in elder males).
Regarding carbapenemases, after the initial isolation of KPC-positive Citrobacter
freundii and K. pneumoniae in early 2007, an electronic emergency report was
transmitted by the national reference center (ANLIS), reinforced in June 2010, after
an 800% increase was observed as compared with the number of isolates submitted
for confirmation from the previous year (Alerta Epidemiológica, 2010, http://anti-
microbianos.com.ar/category/alerta/, visited 2022-12-01). The in vivo horizontal
dissemination of blaKPC-2 was promptly documented between E. coli and K. pneu-
moniae from a single patient (Anchordoqui et al. 2015). Even though KPC-­
producing E. coli are not frequent, they were described in a prospective study from
Argentina’s patients (2011–2014), including some from the high-risk ST131 clone
(De Belder et al. 2018).
By 2013, NDM-1 MBLs had emerged among Enterobacterales (Alerta
Epidemiológica, 2013, http://antimicrobianos.com.ar/category/alerta/, visited
2022-12-01). A few years later, a new variant, NDM-5, was described in an ExPEC
recovered from an old female patient (Costa et al. 2021), and this enzyme is cur-
rently becoming more frequently isolated. A retrospective study on 71
carbapenemase-­producing ExPEC across Argentina was conducted (Sanz et al.
14 N. Lincopan et al.

2022), where a plethora of combined mechanisms were described. More relevant


combinations of beta-lactamases are highlighted in (Table 1.1).
A recent comparison of nosocomial resistance rates modifications comparing
isolates before (2018) and during the COVID-19 (2021) pandemic showed signifi-
cant increase of non-susceptible rates to imipenem (1.1% vs 2.3%), meropenem
(MER, 1.0% vs 1.9%), and ciprofloxacin (CIP, 38.5% vs 41.7%). However, some
antibiotics showed a small decrease: gentamicin (GEN, 16.8% vs 15.2%), trime-
thoprim/sulfamethoxazole (TMS, 47.4% vs 44.5%), and colistin (COL, 1.3% vs
0.8%); or no modification: tigecycline (TIG, 22.6%), piperacillin-tazobactam (PTZ,
16.4%), and amikacin (AKN, 1.8%) (Lucero et al. 2022).
ESBL-positive nosocomial E. coli were highly resistant to CIP (83.6%) and
TMS (69.7%), whereas resistance to GEN (34.6%) and PTZ (33.9%) was less
observed, as well as low resistance rates to fosfomycin (FOS, 5.5%), AKN (4.4%),
COL (2.2%), and TIG (0.6%). Among carbapenem-resistant E. coli (CREC), 63.5%
displayed a MER MIC greater than or equal to 16 mg/L which are not suitable for
synergy. These strains were highly resistant to TMS (60.0%), CIP (57.3%), GEN
(45.4%), and AKN (31.9%), whereas the low resistance level to FOS (7.5%), COL
(2.0%), and TIG (0%) indicated that these drugs were still suitable (in combination)
for treatment of the infections produced by E. coli.
According to the information from WHONET, 26% of CREC produced KPC
enzyme, 21% MBL, 3% OXA-48 like, 1% MBL+ KPC, and the remaining 49% of
strains were not completely characterized (some of them were ESBL and imperme-
able). Trend of carbapenemases was varying between both pre-COVID-19 (2018)
and COVID-19 (2021): 59.5% KPC and 35.7% MBL versus 45.5% KPC and 46.5%
MBL. OXA-48-type increased from 0% to 7.4%. Lastly, among mcr-1-positive
E. coli of this period, 41.8% produced ESBL (most of them CTX-M) and only 2
isolates carbapenemases (1 KPC and 1 NDM).
Regarding animals and environment ecosystems, in a systematic review and
meta-analysis recently conducted (Prack McCormick et al. 2022), antimicrobial
resistance to all agents evaluated was observed for E. coli isolates in food-producing
animals, except for carbapenems and glycylcyclines. MCR-1-producing E. coli was
described in most of niches analyzed in Argentina recovered from gulls, chicken,
pigs, dogs, aquatic environment, and sediment of a lake (Table 1.1); whereas identi-
cal IncI2 plasmids have been reported in some of these mcr-1-positive E. coli
(Quiroga et al. 2019). The mcr-1.5 variant was detected in plasmids of E. coli iso-
lates recovered from human samples, from healthy chicken on commercial farms,
and from diarrheic piglets and healthy fattening pigs (Dominguez et al. 2019).
E. coli recovered from local companion animals display resistance patterns simi-
lar to local human strains (Rumi et al. 2021a). E. coli was one of the most frequently
isolated species in both cats and dogs. Interestingly, the values found for cefotaxime
(CTX)-resistant E. coli were like those reported in human isolates from Argentinian
hospitals (18.3%). In this country, resistance to third generation cephalosporins in
pet isolates is due to ESBL and plasmid-mediated AmpC enzymes (Rumi et al.
1 WHO Critical Priority Escherichia coli in Latin America: A One Health… 15

2019), with predominance of CTX-M-2, CTX-M-14, CTX-M-15, and CMY-2 beta-


lactamases. In a systematic review of the status of ESBLs in E. coli conducted in
South America, Argentina was one of the countries with the second highest research
contributions (Bastidas-Caldes et al. 2022a). Therefore, since ESBLs producing
E. coli are widely distributed at the human-animal-food-­environmental interface
across Argentina, there is a need to increment studies to strengthen multi-sectoral
antimicrobial resistance research and surveillance.

1.1.3 Critical Priority E. coli in Uruguay

The first report of ESBL-producing E. coli in Uruguay comes from isolates obtained
from children admitted to the pediatric hospital with diarrhea between 1991 and
1993. Of 68 EPEC isolates obtained between October 1990 and April 1993, 13
(19.1%) carried blaPER-2 (Vignoli et al. 2005). Subsequent studies, however, have
shown that the importance of Diarrheagenic E. coli (DAC) as a reservoir of ESBL-­
encoding genes would not be a problem today (Peirano et al. 2018; Mota et al. 2020).
Regarding extra-intestinal E. coli clinical isolates, the main ESBL detected in
both adults and pediatric population were CTX-M-15 (55–60%), followed by CTX-­
M-­2 (15–20%) and CTX-M-9 (12–15%) (Vignoli et al. 2016; García-Fulgueiras
et al. 2011; Garcia-Fulgueiras et al. 2017). Comparable results were found in stool
samples from patients admitted to the ICU (Bado et al. 2016). As of 2017, sporadic
cases of clinical isolates of E. coli carrying ESBL (CTX-M-15) or class C plasmid
β-lactamase pAmpC (CMY-2), co-carriers of the colistin resistance gene mcr-1,
have been reported (Papa-Ezdra et al. 2020).The high-risk clones related to this
resistance belonged to the sequence types of ST 131, ST405, and ST10 (Vignoli
et al. 2016; Bado et al. 2016; Papa-Ezdra et al. 2020).
For critical priority E. coli in animals, resistance to oximino-cephalosporins in
bovine feces has been detected in 1–2% of the animals studied, finding the ESBL
CTX-M-14 and CTX-M-15 (Umpiérrez et al. 2017; Cóppola et al. 2020). In the
case of poultry, resistance has been reported in 17.4% of the animals studied, with
the most frequently resistant mechanisms detected being CMY-2, followed by
CTX-M-2, CTX-M-8, SHV2, and CTX-M-55 (Cóppola et al. 2020) (Fig. 1.1).
Interestingly, some of these enzymes, such as CTX-M-8, CMY-2, and CTX-M-55,
were detected in 1-day-old chicks imported from Brazil, which suggests a source of
resistance entry into the country (Coppola et al. 2022).
Finally, the highest levels of resistance were observed in pig breeding, where
resistance to oximino-cephalosporins was detected in the feces of 72% of the ani-
mals studied. In this population, the main β-lactams detected were CTX-M-8, fol-
lowed by CMY-2, SHV-12, and to a lesser extent CTX-M-14 and CTX-M-15
(Cóppola et al. 2020).
16 N. Lincopan et al.

1.1.4 Critical Priority E. coli in Chile

Although WHO critical priority E. coli and its impact are widely recognized in
Chile, reports of these pathogens are still scarce. Epidemiological surveillance in
the community is conducted by the Public Health Institute (Instituto de Salud
Pública, ISP) of Chile, which works as the reference center for the confirmation of
resistant pathogens sent by hospitals throughout the country. On the other hand,
E. coli carrying ESBL or carbapenemases detected in domestic animals, wildlife,
food, vegetables, and water are not reported to the ISP, leading to a lack of knowl-
edge on dissemination through the different transmission routes. In human medi-
cine, detection of ESBL- or carbapenemase-producing E. coli became relevant after
the 2000s. The first reports using phenotypic tests made it possible to establish that
there were ESBL-producing E. coli causing septicemia in cancer patients (Rabagliati
et al. 2009). Then, investigations using molecular analyses showed that CTX-M-­
type enzymes were the main β-lactamases in E. coli isolated from clinical samples
(Wozniak et al. 2012); and specifically, enzymes from the CTX-M-1, CTX-M-2,
and CTX-M-9 groups and SHV-like were carried (García et al. 2011; Elgorriaga-­
Islas et al. 2012; Wozniak et al. 2012; Álvarez et al. 2018; Pavez et al. 2019)
(Fig. 1.1).
Regarding carbapenemases, KPC-2-producing E. coli belonging to the ST378
lineage has been reported among a multispecies outbreak of carbapenem-resistant
bacteria in a patient admitted to a hospital coronary care unit (Wozniak et al. 2021).
Currently, hospitals in Chile must notify to the ISP the presence of carbapenem-­
resistant bacteria; these records show that E. coli carry carbapenemases of KPC,
NDM, and VIM types among nosocomial infections. Furthermore, the co-­production
of KPC + VIM has already been found in E. coli. However, carbapenemases are
more common in other species as Klebsiella spp., Acinetobacter spp., and
Pseudomonas aeruginosa (ISP 2022).
In domestic animals, a study reports the presence of CTX-M-1 and CTX-M-14
and PER-2 β-lactamases in E. coli isolated from hospitalized cats and dogs (Moreno
et al. 2008). Subsequently, a study described the presence of E. coli carrying
enzymes of groups CTX-M-1, CTX-M-2, CTX-M-8, CTX-M-9, and CTX-M-25 in
dogs from the Chacabuco province in the Metropolitan Region of central Chile
(Benavides et al. 2021). The same study reports E. coli harboring β-lactamases of
the groups CTX-M-1 and CTX-M-2, and SHV-like among livestock samples (cat-
tle, pigs, sheep, and chickens). Sporadically, ESBL-producing E. coli causing uri-
nary tract infections in dogs and horses are detected in the Veterinary Microbiology
Laboratory of the University of Concepción in Chillán. Until now, no carbapenemase-­
producing E. coli has been reported in Chilean domestic animals.
In wildlife, studies on ESBL-producing E. coli began to be conducted in 2009 in
migratory birds (Hernandez et al. 2013), detecting CTX-M-1, CTX-M-15, CTX-­
M-­ 3, and CTX-M-14 enzymes among E. coli isolated from fecal samples of
Franklin’s gulls in Con-Con and Talcahuano coasts. In the same species, but in
Antofagasta, northern Chile, another study reports the presence of E. coli harboring
1 WHO Critical Priority Escherichia coli in Latin America: A One Health… 17

enzymes of the CTX-M-2, CTX-M-3, CTX-M-15, and CTX-M-22 groups (Báez


et al. 2015) (Fig. 1.1). Both studies reported ESBL genes in various lineages includ-
ing the high-risk clones ST10 and ST131.
Wildlife rescue and rehabilitation centers have been important components of
epidemiological surveillance on WHO critical priority pathogens in wild animals
(Fuentes-Castillo et al. 2019, 2020). In fact, CTX-M-8-producing E. coli were
detected in two owl species (rufous-legged owl and Magellanic horned owl).
Subsequently, international clones of E. coli ST162, ST602, ST1196, and ST1485
carrying CTX-M-14, CTX-M-55, or CTX-M-65 ESBL were detected in Andean
condors admitted at two wildlife rehabilitation centers. Carbapenemase-producing
E. coli in wild birds were reported in Franklin’s gulls (Ahlstrom et al. 2022). In this
regard NDM-5 MBL was detected in E. coli strains belonging to ST345, ST744,
and ST1178.
In the center of the country, E. coli harboring CTX-M genes were detected in the
Claro and Lontue rivers, in Maule Region, a large area with agricultural activity
(Díaz-Gavidia et al. 2021). The same study revealed the presence of CTX-M-­
producing E. coli in parsley and lettuce ready for human consume. In contrast, stud-
ies that looked for STEC in samples from cattle and pigs found no association of
E. coli strains carrying Shiga toxin with the presence of ESBL or carbapenemase
(Galarce et al. 2021; Sánchez et al. 2021).

1.1.5 Critical Priority E. coli in Ecuador

In Ecuador, the first report of ESBL-producing E. coli was in 2009, from the screen-
ing of samples collected from patients with intra-abdominal infections. In this study,
the presence of E. coli expressing CTX-M-3 and CMY-2 β-lactamases was reported
(Hawser et al. 2012). Nowadays, Ecuador is the country with the second highest
number of human detections of ESBLs-producing E. coli. The high occurrence of
ESBL producers has been associated with a high prevalence of CTX-M-1, CTX-­
M-­15, and CTX-M-55 variants, with CTX-M-15 being most common in clinical
isolates (Bastidas-Caldes et al. 2022a; Delgado et al. 2016; Chiluisa-Guacho et al.
2018; Hawser et al. 2012; Nordberg et al. 2013; Ortega-Paredes et al. 2016, 2020a;
Soria Segarra et al. 2018; Zurita et al. 2019) (Fig. 1.1). In healthy carriers, CTX-­
M-­55 has been a prevalent variant (Bastidas-Caldes et al. 2022a; Calderón et al.
2022; Salinas et al. 2021). In a study performed between 2013 and 2014, in three
high-complexity teaching hospitals in Quito, analysis of ESBL-producing E. coli
from bloodstream infections revealed the emergence of the CTX-M-15-producing
E. coli ST131-B2 clone, representing an important public-health problem, because
this multi-resistant clone is considered highly virulent, and a vehicle for the propa-
gation of antimicrobial resistance genes (Zurita et al. 2019). Other epidemiologi-
cally valuable information of this study was the description of CTX-M-15-positive
E. coli ST10, ST23, ST46, ST168, ST354, ST405, and ST6548, as well as CTX-­
M-­14-producing E. coli strains belonging to ST14, ST23, and ST405. In this study,
18 N. Lincopan et al.

the authors reported the emergence of the CTX-M-27/ST131 global E. coli clone
(Zurita et al. 2019).
Poultry products have been the most important source of animal protein
(CONAVE, 2021, https://conave.org/informacion-­sector-­avicola-­publico/), and
because of the overuse of antibiotics in their breeding, they are perfect reservoirs of
antibiotic-resistant microorganisms. In the case of food-producing animals, most of
the studies have presented data of E. coli from poultry (Hedman et al. 2019; Ortega-­
Paredes et al. 2020a; Vinueza-Burgos et al. 2019). In this respect, a study on chicken
samples and carcasses collected from farms and markets, between 2017 and 2018,
in Quito, showed the occurrence and predominance of CTX-M-55 and CTX-M-65
among ESBL-producing E. coli strains (Ortega-Paredes et al. 2020a).
In companion animals, E. coli isolates producing CTX-M-type ESBLs have been
more prevalent in canines (Albán et al. 2020; Bastidas-Caldes et al. 2022a; Ortega-­
Paredes et al. 2019; Salinas et al. 2021). Interestingly, a surveillance study con-
ducted in Quito revealed that E. coli strains from children and domestic animals
shared the same blaCTX-M allelic variants, whereas the most prevalent ESBL genes
were CTX-M-55 and CTX-M-65, which were found in isolates from children, dogs,
and chickens (Salinas et al. 2021) (Fig. 1.1).
In food, the occurrence of epidemic clones of E. coli ST131, ST162, ST410, and
ST744, producing CTX-M-8, CTX-M-14, CTX-M-15, CTX-M-24, CTX-M-55, or
CTX-M-65 ESBLs, in ready-to-eat street food samples has alerted that street food
is a possible way to spread harmful multidrug-resistant E. coli strains in the com-
munity (Zurita et al. 2020). Moreover, reports in the city of Ambato and Riobamba
showed the presence of E. coli expressing SHV and CMY genes in ready-to-eat
street food samples and fresh vegetables (Barragán-Fonseca et al. 2022; Tubón et al.
2022). Of public health concern has been the detection of ESBL-producing E. coli
in alfalfa, leaf lettuce, and parsley/cilantro samples, in a municipal market in Quito,
in 2015 (Ortega-Paredes et al. 2018). In this regard, the hyperepidemic CTX-M-15-­
producing E. coli clone ST410-A was reported for the first time in fresh vegetables,
alerting regarding the health risk that this could pose, since vegetables and fruits are
usually consumed raw. In the same study, the authors identify CTX-M-15-producing
E. coli strains belonging to ST44 in leaf lettuce, alfalfa, and parsley/cilantro sam-
ples (Ortega-Paredes et al. 2018). Noteworthy, a recent investigation by these
authors also confirmed the presence of CTX-M-15-producing E. coli ST44 in the
polluted Machángara River, where most of the wastewater of Quito city is dis-
charged directly through sewage drainage (Ortega-Paredes et al. 2020b).
Additionally, water samples collected from points with domestic and industrial
activities, and animal rearing, irrigation, domestic, and recreational purposes were
positive for CTX-M-15-producing E. coli of ST10, ST46, ST162, ST167, ST457,
ST1140, and ST1711, and CTX-M-18-, CTX-M-29-, and CTX-M-65-producing
E. coli of ST10, ST362, and ST394, respectively, highlighting the high potential of
polluted urban rivers as sites of emergence and sources of spread of critical priority
E. coli. Furthermore, predominance of CTX-M-15 in E. coli isolates supports the
establishment of this variant in the city, and its aquatic dissemination through the
sewage to the environment (Ortega-Paredes et al. 2020b). Moreover, CTX-M-55,
1 WHO Critical Priority Escherichia coli in Latin America: A One Health… 19

CTX-M-65, and CTX-M-15 have been confirmed in produce and irrigation water
across different provinces of Ecuador (Bastidas-Caldes et al. 2022b; Montero et al.
2021). Regarding carbapenemase-producing E. coli, during a surveillance study of
colonized patients, first KPC-positive E. coli strains were identified in 2016, from
inguinal and perineal swab cultures performed in ICU patients, in Guayaquil (Soria-­
Segarra et al. 2020).

1.1.6 Critical Priority E. coli in Bolivia

In Bolivia, E. coli is one of the most clinically important pathogens, and during the
last decade an important dissemination of CTX-M-type ESBL has been observed
(Fig. 1.1), despite being a country with very few published data, restricted to clini-
cal settings. The first description of E. coli strains producing the CTX-M-2 ESBL
was reported in 2002, in fecal samples of healthy children from the Bolivian Chaco,
denoting the role that commensal E. coli isolates could play as potential reservoirs
of these clinically relevant resistance mechanisms (Pallecchi et al. 2004). Three
years later, a survey carried out among members of the same healthy population
revealed that fecal carriage of E. coli strains resistant to broad-spectrum cephalo-
sporins was remarkably increased compared to that observed in the same settings in
2002, with the emergence of CTX-M-15-producing E. coli being documented
(Pallecchi et al. 2007). Another survey conducted in 2011, in the same setting,
reported a relentless increase of resistance to ciprofloxacin and broad-spectrum
cephalosporins, with occurrence of CTX-M-1-, CTX-M-2-, and CTX-M-9-type
producing E. coli (Bartoloni et al. 2013). CTX-M-2 was replaced by CTX-M-15
and CTX-M-65. In 2015, it was reported that widespread dissemination of CTX-­
M-­65 was related to the polyclonal spreading of an IncI1 sequence type 71 (ST71)
epidemic plasmid (Riccobono et al. 2015). Analysis of clinical isolates recovered
between 2010 and 2014, from culture of urinary tract infections, resulted in the
identification of CTX-M-15-positive E. coli belonging to the international ST131
(Bartoloni et al. 2016).
In Cochabamba, a molecular survey that includes clinical samples recovered
from different health centers, during 2012–2013, reported a high prevalence of the
CTX-M-1 group among E. coli isolates (Saba Villarroel et al. 2017). More recently,
emergence of CTX-M-8-positive E. coli and occurrence of CTX-M-1 and CTX-­
M-­9 producers was reported in school-age children from Indigenous communities
of the Chaco, where the consumption of antibiotics is limited (Boncompagni
et al. 2022).
Regarding aquatic environments, the presence of CTX-M-3-producing E. coli
was reported in the Choqueyapu River in La Paz, from a sample collected in 2013.
Interestingly, although ST648, ST410, and ST162 were identified, only E. coli of
ST162 carried the blaCTX-M-3 ESBL gene, indicating the possibility of antibiotic
resistance transfer from the environment to the community (Guzman-Otazo
et al. 2019).
20 N. Lincopan et al.

1.1.7 Critical Priority E. coli in Peru

In the same way as in other Latin American countries, in Peru, CTX-M-type ESBL
producers have been predominant, mainly CTX-M-15 (Medina-Pizzali et al. 2022;
Yauri-Condor et al. 2020; Alcedo et al. 2022; Palma et al. 2017; Benavides et al.
2022; Ymaña et al. 2022) (Fig. 1.1). The first E. coli strains producing CTX-M-15
or CTX-M-2 were isolated, in 2002, from fecal swab specimens taken from healthy
children living in Yurimaguas and Moyobamba (Pallecchi et al. 2004). Later, a sur-
vey conducted in 2005, among the same members of a healthy population of chil-
dren, revealed the emergence of CTX-M-14 and CTX-M-24 (CTX-M-9 group) in
commensal E. coli strains (Pallecchi et al. 2007). Moreover, E. coli isolates causing
bacteremia in children from Lima carried a variety of ESBL-encoding genes,
including blaSHV-12, blaCTX-M-15, blaCTX-M-2, and blaCTX-M-65. However, predominance of
blaCTX-M-15 was confirmed (Palma et al. 2017). In urinary tract infections, a preva-
lence near to 55.0% of ESBL production, associated with CTX-M among E. coli
isolates has been observed in public hospitals (Marcos-Carbajal et al. 2021), includ-
ing the Peruvian jungle departments (León-Luna et al. 2021).
In animal hosts, ESBL-producing E. coli have been isolated in fecal samples col-
lected from wild common vampire bats and livestock near Lima, where molecular
analyses revealed that most of this resistance resulted from the production of CTX-­
M-­15, with CTX-M-14-, CTX-M-15-, and CTX-M-26-postive E. coli belonging to
ST2, ST356, ST466, and ST779 being isolated from cows; CTX-M-15 producers of
ST2, ST422, ST472, ST721, ST305, and ST716 from bats; and CTX-M-14- and
CTX-M-15-producing clones ST2, ST21, ST716, ST849, ST850, and ST851 recov-
ered from pigs (Benavides et al. 2018). A more recent survey revealed the occur-
rence of CTX-M-3, CTX-M-14, CTX-M-15, CTX-M-55, and CTX-M-65 among
commensal E. coli ST10, ST117, ST155, ST156, ST162, ST167, ST410, ST602,
ST617, ST648, ST744, ST1049, ST1485, and ST2197 isolated from vampire bats
and livestock (Benavides et al. 2022). Strikingly, CTX-M E. coli of ST2 and ST17
are shared between wild birds and livestock (Benavides et al. 2018, 2022). CTX-M-­
producing E. coli has also been isolated in poultry farms in Ica, highlighting a criti-
cal need for effective policy development and antimicrobial stewardship interventions
in poultry production (Dávalos-Almeyda et al. 2022). In companion animals, CXT-­
M-­8-producing E. coli ST5259 has been identified in feces collected from dog
(Medina-Pizzali et al. 2022).
In environmental settings, in a study performed between 2016 and 2017, a CTX-­
M-­3-producing E. coli was recovered from drinking water sample obtained from a
rural Andean household from Cajamarca (Larson et al. 2019). More recently, CTX-­
M-­55 E. coli ST227 was also isolated from drinking water (Medina-Pizzali et al.
2022). Regarding carbapenemases, in humans, occurrence of these enzymes in
E. coli has been restricted to identification of NDM-1 in a ST155 clone isolated
from a urine culture of an elderly patient with pancreatic cancer, in 2017 (Tamariz
et al. 2018). Worryingly, the blaKPC-3 gene was identified in one market chicken iso-
late of E. coli ST10, in 2018, in Lima (Murray et al. 2021).
1 WHO Critical Priority Escherichia coli in Latin America: A One Health… 21

1.2 Conclusions

E. coli resistant to broad-spectrum cephalosporins and carbapenems antibiotics,


classified as a critical priority by the WHO, have successfully disseminated beyond
the hospital settings, and are now being identified in the environment, and in pets,
food-producing, and wild animals, in South America. Molecular surveillance has
significantly improved the ability to investigate the spread and emergence of clones
at the human-animal-food-environment-animal interface. In this regard, studies
conducted in Latin American countries have confirmed the occurrence of CTX-M
(2, 3, 8, 9, 14, 15, 27, 55, 65)-producing E. coli strains belonging to international
sequence types (STs) ST2, ST10, ST38, ST44, ST58, ST90, ST131, ST155, ST162,
ST167, ST224, ST354, ST362, ST394, ST405, ST410, ST457, ST602, and ST648.
They have been identified from humans, animals, and plant sources in Argentina,
Bolivia, Brazil, Chile, Ecuador, Peru, and Uruguay. On the other hand, E. coli pro-
ducing KPC-2 or NDM-1 carbapenemases, belonging to the ST10, ST48, ST90,
ST131, ST155, ST167, ST354, ST457, ST502, ST648, ST730, and ST744 have
disseminated in humans, in Argentina, Brazil, and Peru, whereas E. coli ST156,
ST162, ST345, ST648, ST744, and ST1178 producing KPC-2, NDM-1, or NDM-5
have emerged in animal infections in Chile and Brazil. Anthropogenic actions and
accelerated urbanization seem to contribute to this phenomenon, where endangered
species such as iconic birds (e.g., Andean condor), whales, and marine turtles are
now colonized or infected by WHO critical priority pathogens genomically related
to hospital bacteria. The rapid spread of critical priority pathogens in South America
is worrying, considering the dimension of the continent, diversity of international
trade, livestock production, and human travel, becoming a challenge within a One
Health perspective that must be monitored, in the current post-pandemic scenario.

References

Ahlstrom CA, Woksepp H, Sandegren L, Mohsin M, Hasan B, Muzyka D, Hernandez J, Aguirre


F, Tok A, Söderman J, Olsen B, Ramey AM, Bonnedahl J (2022) Genomically diverse car-
bapenem resistant Enterobacteriaceae from wild birds provide insight into global patterns of
spatiotemporal dissemination. Sci Total Environ 824:153632
Aizawa J, Neuwirt N, Barbato L, Neves PR, Leigue L, Padilha J, Pestana de Castro AF, Gregory L,
Lincopan N (2014) Identification of fluoroquinolone-resistant extended-spectrum β-lactamase
(CTX-M-8)-producing Escherichia coli ST224, ST2179 and ST2308 in buffalo (Bubalus buba-
lis). J Antimicrob Chemother 69(10):2866–2869
Albán MV, Núñez EJ, Zurita J, Villacís JE, Tamayo R, Sevillano G, Villavicencio FX, Calero-­
Cáceres W (2020) Canines with different pathologies as carriers of diverse lineages of
Escherichia coli harbouring mcr-1 and clinically relevant β-lactamases in central Ecuador. J
Glob Antimicrob Resist. 22:182–183
Alcedo K, Ruiz J, Ochoa TJ, Riveros M (2022) High prevalence of blaCTX-M in fecal commensal
Escherichia coli from healthy children. Infect Chemother 54(1):59–69
Almeida AC, de Sá Cavalcanti FL, Vilela MA, Gales AC, de Morais MA Jr, Camargo de Morais
MM (2012) Escherichia coli ST502 and Klebsiella pneumoniae ST11 sharing an IncW plasmid
22 N. Lincopan et al.

harbouring the bla(KPC-2) gene in an Intensive Care Unit patient. Int J Antimicrob Agents
40(4):374–376
Álvarez J, Rojas Á, Carvajal C, Revello J, Meza P, Guggiana P, García P, Labarca J (2018)
Evaluation of susceptibility and response to therapy with piperacillin-tazobactam in patients
with infections caused by Escherichia coli with extended-spectrum β-lactamase (ESBL) CTX-­
M. Rev Chil Infectol 35(4):343–350
Álvarez VE, Allende NG, Massó MG, Piekar M, Campos J, Fox B, Gambino AS, Fernández-­
Canigia L, Quiroga MP, Centrón D (2022) Replacement of KPC-producing pandemic lineages
and dissemination of plasmids associated to antimicrobial resistance determinants during inpa-
tient’s hospitalization. J Glob Antimicrob Resist S2213–7165(22):00245–00244
Anchordoqui MS, De Belder D, Lucero C, Rapoport M, Faccone D, Rodriguez A, Di Martino
A, Martino F, Herrero I, Pasteran F, Corso A, Gomez SA (2015) In vivo horizontal dissem-
ination of the blaKPC-2 gene carried on diverse genetic platforms among clinical isolates of
Enterobacteriaceae. J Glob Antimicrob Resist. 3(3):210–213
Bado I, Gutierrez C, Garcia-Fulgueiras V, Cordeiro NF, Araújo Pirez L, Seija V, Bazet C, Rieppi
G, Vignoli R (2016) CTX-M-15 in combination with aac(6')Ib-cr are the most prevalent
mechanisms of resistance between both Escherichia coli and Klebsiella pneumoniae including
ST258 in an ICU from Uruguay. J Glob Antimicrob Resist. 6:5–9
Báez J, Hernández-García M, Guamparito C, Díaz S, Olave A, Guerrero K, Cantón R, Baquero
F, Gahona J, Valenzuela N, Del Campo R, Silva J (2015) Molecular characterization and
genetic diversity of ESBL-producing Escherichia coli colonizing the migratory Franklin's gulls
(Leucophaeus pipixcan) in Antofagasta, North of Chile. Microb Drug Resist 21(1):111–116
Barragán-Fonseca G, Tubón J, Calero-Cáceres W (2022) Data on antibiogram and resistance genes
of Enterobacterales isolated from fresh vegetables in Ecuador. Data Brief 42:108249
Bartoloni A, Pallecchi L, Riccobono E, Mantella A, Magnelli D, Di Maggio T, Villagran AL, Lara
Y, Saavedra C, Strohmeyer M, Bartalesi F, Trigoso C, Rossolini GM (2013) Relentless increase
of resistance to fluoroquinolones and expanded-spectrum cephalosporins in Escherichia coli:
20 years of surveillance in resource-limited settings from Latin America. Clin Microbiol Infect
19(4):356–361
Bartoloni A, Sennati S, Di Maggio T, Mantella A, Riccobono E, Strohmeyer M, Revollo C,
Villagran AL, Pallecchi L, Rossolini GM (2016) Antimicrobial susceptibility and emerging
resistance determinants (blaCTX-M, rmtB, fosA3) in clinical isolates from urinary tract infec-
tions in the Bolivian Chaco. Int J Infect Dis 43:1–6
Bastidas-Caldes C, Romero-Alvarez D, Valdez-Vélez V, Morales RD, Montalvo-Hernández
A, Gomes-Dias C, Calvopiña M (2022a) Extended-spectrum beta-lactamases producing
Escherichia coli in South America: asystematic review with a one health perspective. Infect
Drug Resist 15:5759–5779
Bastidas-Caldes C, Ochoa J, Guerrero-Latorre L, Moyota-Tello C, Tapia W, Rey-Pérez JM, Baroja
MI (2022b) Removal of extended-spectrum beta-lactamase-producing Escherichia coli, ST98,
in water for human consumption by black ceramic water filters in low-income Ecuadorian
highlands. Int J Environ Res Public Health 19(8):4736
Benavides JA, Shiva C, Virhuez M, Tello C, Appelgren A, Vendrell J, Solassol J, Godreuil S,
Streicker DG (2018) Extended-spectrum beta-lactamase-producing Escherichia coli in
common vampire bats Desmodusrotundus and livestock in Peru. Zoonoses Public Health
65(4):454–458
Benavides JA, Salgado-Caxito M, Opazo-Capurro A, González Muñoz P, Piñeiro A, Otto Medina
M, Rivas L, Munita J, Millán J (2021) ESBL-producing Escherichia coli carrying CTX-M
genes circulating among livestock, dogs, and wild mammals in small-scale farms of central
Chile. Antibiotics (Basel) 10(5):510
Benavides JA, Godreuil S, Opazo-Capurro A, Mahamat OO, Falcon N, Oravcova K, Streicker
DG, Shiva C (2022) Long-term maintenance of multidrug-resistant Escherichia coli carried by
vampire bats and shared with livestock in Peru. Sci Total Environ 810:152045
1 WHO Critical Priority Escherichia coli in Latin America: A One Health… 23

Berman H, Barberino MG, Moreira ED Jr, Riley L, Reis JN (2014) Distribution of strain type and
antimicrobial susceptibility of Escherichia coli isolates causing meningitis in a large urban set-
ting in Brazil. J Clin Microbiol 52(5):1418–1422
Boncompagni SR, Micieli M, Di Maggio T, Mantella A, Villagrán AL, Briggesth Miranda T,
Revollo C, Poma V, Gamboa H, Spinicci M, Strohmeyer M, Bartoloni A, Rossolini GM,
Pallecchi L (2022) Relevant increase of CTX-M-producing Escherichia coli carriage in school-­
aged children from rural areas of the Bolivian Chaco in a three-year period. Int J Infect Dis
121:126–129
Bonnet R, Sampaio JL, Labia R, De Champs C, Sirot D, Chanal C, Sirot J (2000) A novel CTX-M
beta-lactamase (CTX-M-8) in cefotaxime-resistant Enterobacteriaceae isolated in Brazil.
Antimicrob Agents Chemother 44(7):1936–1942
Bonnet R, Dutour C, Sampaio JL, Chanal C, Sirot D, Labia R, De Champs C, Sirot J (2001) Novel
cefotaximase (CTX-M-16) with increased catalytic efficiency due to substitution Asp-240--
>Gly. Antimicrob Agents Chemother 45(8):2269–2275
Borges CA, Maluta RP, Beraldo LG, Cardozo MV, Guastalli EAL, Kariyawasam S, DebRoy C,
Ávila FA (2017a) Captive and free-living urban pigeons (Columba livia) from Brazil as carriers
of multidrug-resistant pathogenic Escherichia coli. Vet J 219:65–67
Borges CA, Cardozo MV, Beraldo LG, Oliveira ES, Maluta RP, Barboza KB, Werther K, Ávila
FA (2017b) Wild birds and urban pigeons as reservoirs for diarrheagenic Escherichia coli with
zoonotic potential. J Microbiol 55(5):344–348
Botelho LA, Kraychete GB, Costa e Silva JL, Regis DV, Picão RC, Moreira BM, Bonelli RR (2015)
Widespread distribution of CTX-M and plasmid-mediated AmpCβ-lactamases in Escherichia
coli from Brazilian chicken meat. Mem Inst Oswaldo Cruz 110(2):249–254
Bueris V, Sellera FP, Fuga B, Sano E, Carvalho MPN, Couto SCF, Moura Q, Lincopan N (2022)
Convergence of virulence and resistance in international clones of WHO critical priority
Enterobacterales isolated from Marine Bivalves. Sci Rep 12(1):5707
Calderón D, Cárdenas PA, Prado-Vivar B, Graham JP, Trueba G (2022) A longitudinal study of
dominant E. coli lineages and antimicrobial resistance in the gut of children living in an upper
middle-income country. J Glob Antimicrob Resist 29:136–140
Campos JC, da Silva MJ, dos Santos PR, Barros EM, Pereira Mde O, Seco BM, Magagnin CM,
Leiroz LK, de Oliveira TG, de Faria-Júnior C, Cerdeira LT, Barth AL, Sampaio SC, Zavascki
AP, Poirel L, Sampaio JL (2015) Characterization of Tn3000, a transposon responsible for
blaNDM-1 dissemination among enterobacteriaceae in Brazil, Nepal, Morocco, and India.
Antimicrob Agents Chemother 59(12):7387–7395
Carvalho-Assef AP, Leão RS, da Silva RV, Ferreira AG, Seki LM, Asensi MD, Marques EA (2010)
Escherichia coli producing KPC-2 carbapenemase: first report in Brazil. Diagn Microbiol
Infect Dis 68(3):337–338
Casella T, Rodríguez MM, Takahashi JT, Ghiglione B, Dropa M, Assunção E, Nogueira ML,
Lincopan N, Gutkind G, Nogueira MC (2015) Detection of blaCTX-M-type genes in complex
class 1 integrons carried by Enterobacteriaceae isolated from retail chicken meat in Brazil. Int
J Food Microbiol 197:88–91
Casella T, Cerdeira LT, Fernandes MR, Souza TA, Haenni M, Madec JY, Lincopan N, Nogueira
MCL (2017) Draft genome sequence of a CTX-M-15-producing Escherichia coli ST345 from
commercial chicken meat in Brazil. J Glob Antimicrob Resist 9:124–125
Cejas D, Fernández Canigia L, Quinteros M, Giovanakis M, Vay C, Lascialandare S, Mutti D,
Pagniez G, Almuzara M, Gutkind G, Radice M (2012) Plasmid-encoded AmpC (pAmpC) in
Enterobacteriaceae: epidemiology of microorganisms and resistance markers. Rev Argent
Microbiol 44(3):182–186
Cergole-Novella MC, Guth BE, Castanheira M, Carmo MS, Pignatari AC (2010) First description
of bla(CTX-M-14)- and bla(CTX-M-15)-producing Escherichia coli isolates in Brazil. Microb
Drug Resist 16(3):177–184
24 N. Lincopan et al.

Chagas TP, Seki LM, Cury JC, Oliveira JA, Dávila AM, Silva DM, Asensi MD (2011)
Multiresistance, beta-lactamase-encoding genes and bacterial diversity in hospital wastewater
in Rio de Janeiro, Brazil. J Appl Microbiol 111(3):572–581
Chiluisa-Guacho C, Escobar-Perez J, Dutra-Asensi M (2018) First detection of the CTXM-15-­
producing Escherichia coli O25-ST131 pandemic clone in Ecuador. Pathogens 7(2):42
Conceição-Neto OC, Aires CAM, Pereira NF, da Silva LHJ, Picão RC, Siqueira BN, Albano
RM, Asensi MD, Carvalho-Assef APD (2017) Detection of the plasmid-mediated mcr-1
gene in clinical KPC-2-producing Escherichia coli isolates in Brazil. Int J Antimicrob Agents
50(2):282–284
Conte D, Palmeiro JK, da Silva NK, de Lima TM, Cardoso MA, Pontarolo R, Degaut Pontes FL,
Dalla-Costa LM (2017) Characterization of CTX-M enzymes, quinolone resistance determi-
nants, and antimicrobial residues from hospital sewage, wastewater treatment plant, and river
water. Ecotoxicol Environ Saf 136:62–69
Cóppola N, Freire B, Umpiérrez A, Cordeiro NF, Ávila P, Trenchi G, Castro G, Casaux ML, Fraga
M, Zunino P, Bado I, Vignoli R (2020) Transferable resistance to highest priority critically
important antibiotics for human health in Escherichia coli strains obtained from livestock feces
in Uruguay Front. Vet Sci 7:588919
Coppola N, Cordeiro NF, Trenchi G, Esposito F, Fuga B, Fuentes-Castillo D, Lincopan N, Iriarte
A, Bado I, Vignoli R (2022) 2022 imported one-day-old chicks as Trojan horses for multidrug-­
resistant priority pathogens Harboring mcr-9, rmtG and extended-spectrum β-lactamase genes.
Appl Environ Microbiol 88(2):e0167521
Costa A, Figueroa-Espinosa R, Gaudenzi F, Lincopan N, Fuga B, Ghiglione B, Gutkind G, Di
Conza J (2021) Co-occurrence of NDM-5 and RmtB in a clinical isolate of Escherichia coli
belonging to CC354 in Latin America. Front Cell Infect Microbiol 11:654852
Cunha MP, Lincopan N, Cerdeira L, Esposito F, Dropa M, Franco LS, Moreno AM, Knöbl T
(2017) Coexistence of CTX-M-2, CTX-M-55, CMY-2, FosA3, and QnrB19 in extraintes-
tinal pathogenic Escherichia coli from poultry in Brazil. Antimicrob Agents Chemother
61(4):e02474–e02416
da Silva KC, Cunha MP, Cerdeira L, de Oliveira MG, de Oliveira MC, Gomes CR, Lincopan N,
Knöbl T, Moreno AM (2017) High-virulence CMY-2- and CTX-M-2-producing avian patho-
genic Escherichia coli strains isolated from commercial turkeys. Diagn Microbiol Infect Dis
87(1):64–67
Dalmolin TV, Castro L, Mayer FQ, Zavascki AP, Martins AF, Lima-Morales D, Barth AL (2017)
Co-occurrence of mcr-1 and blaKPC-2 in a clinical isolate of Escherichia coli in Brazil. J
Antimicrob Chemother 72(8):2404–2406
Dávalos-Almeyda M, Guerrero A, Medina G, Dávila-Barclay A, Salvatierra G, Calderón M,
Gilman RH, Tsukayama P (2022) Antibiotic use and resistance knowledge assessment of per-
sonnel on chicken farms with high levels of antimicrobial resistance: a cross-sectional survey
in Ica, Peru. Antibiotics (Basel) 11(2):190
De Belder D, Lucero C, Rapoport M, Rosato A, Faccone D, Petroni A, Pasteran F, Albornoz E,
Corso A, Gomez SA (2018) Genetic diversity of KPC-producing Escherichia coli, Klebsiella
oxytoca, Serratia marcescens, and Citrobacter freundii isolates from Argentina. Microb Drug
Resist 24(7):958–965
de Carvalho MPN, Fernandes MR, Sellera FP, Lopes R, Monte DF, Hippólito AG, Milanelo L,
Raso TF, Lincopan N (2020) International clones of extended-spectrum β-lactamase (CTX-­
M)-producing Escherichia coli in peri-urban wild animals, Brazil. Transbound Emerg Dis
67(5):1804–1815
Delgado DY, Barrigas ZP, Astutillo SG, Jaramillo AP, Ausili A (2016) Detection and molecular
characterization of β-lactamase genes in clinical isolates of Gram-negative bacteria in Southern
Ecuador. Braz J Infect Dis 20(6):627–630
Dias JB, Soncini JGM, Cerdeira L, Lincopan N, Vespero EC (2022) MDR Escherichia coli carrying
CTX-M-24 (IncF[F-:A1:B32]) and KPC-2 (IncX3/IncU) plasmids isolated from community-­
acquired urinary tract infection in Brazil. Braz J Infect Dis 26(6):102706
1 WHO Critical Priority Escherichia coli in Latin America: A One Health… 25

Díaz-Gavidia C, Barría C, Rivas L, García P, Alvarez FP, González-Rocha G, Opazo-Capurro


A, Araos R, Munita JM, Cortes S, Olivares-Pacheco J, Adell AD, Moreno-Switt AI (2021)
Isolation of ciprofloxacin and ceftazidimer Enterobacterales from vegetables and river water is
strongly associated with the season and the sample type. Front Microbiol 12:604567
Dominguez JE, Figueroa Espinosa RA, Redondo LM, Cejas D, Gutkind GO, Chacana PA, Di Conza
JA, Fernández-Miyakawa ME (2017) Plasmid-mediated colistin resistance in Escherichia coli
recovered from healthy poultry. Rev Argent Microbiol 49(3):297–298
Dominguez JE, Redondo LM, Figueroa Espinosa RA, Cejas D, Gutkind GO, Chacana PA, Di
Conza JA, Fernández Miyakawa ME (2018) Simultaneous carriage of mcr-1 and other anti-
microbial resistance determinants in Escherichia coli from poultry. Front Microbiol 9:1679
Dominguez JE, Faccone D, Tijet N, Gomez S, Corso A, Fernández-Miyakawa ME, Melano RG
(2019) Characterization of Escherichia coli carrying mcr-1-plasmids recovered from food ani-
mals from Argentina. Front Cell Infect Microbiol 9:41
Dos Anjos AM, Châtre P, Métayer V, Drapeau A, Pillonetto M, Penkal ML, Lopes JK, Beirão BCB,
Madec JY, de Macedo REF, Haenni M (2022) Escherichia coli ST224 and IncF/blaCTX-M-55
plasmids drive resistance to extended-spectrum cephalosporins in poultry flocks in Parana,
Brazil. Int J Food Microbiol 380:109885
Dropa M, Balsalobre LC, Lincopan N, Matté GR, Matté MH (2015) Complex class 1 integrons
harboring CTX-M-2-encoding genes in clinical Enterobacteriaceae from a hospital in Brazil. J
Infect Dev Ctries 9(8):890–897
Dropa M, Lincopan N, Balsalobre LC, Oliveira DE, Moura RA, Fernandes MR, da Silva QM,
Matté GR, Sato MI, Matté MH (2016) Genetic background of novel sequence types of CTX-­
M-­8- and CTX-M-15-producing Escherichia coli and Klebsiella pneumoniae from public
wastewater treatment plants in São Paulo, Brazil. Environ Sci Pollut Res Int 23(5):4953–4958
Elena A, Cejas D, Magariños F, Jewtuchowicz V, Facente A, Gutkind G, Di Conza J, Radice M
(2018) Spread of clonally related Escherichia coli Strains Harboring an IncA/C1 plasmid
encoding IMP-8 and its recruitment into an unrelated MCR-1-containing isolate. Antimicrob
Agents Chemother 62(6):e02414–e02417
Elgorriaga-Islas E, Guggiana-Nilo P, Domínguez-Yévenes M, González-Rocha G, Mella-­
Montecinos S, Labarca-Labarca J, García-Cañete P, Bello-Toledo H (2012) Prevalencia del
determinante de resistencia plasmídica a quinolonas aac(6′)-Ib-cr en cepas de Escherichia coli
y Klebsiella pneumoniae productoras de BLEE aisladas en diez hospitales de Chile. Enferm
Infecc Microbiol Clin 30(8):466–468
Ewbank AC, Fuentes-Castillo D, Sacristán C, Cardoso B, Esposito F, Fuga B, de Macedo EC,
Lincopan N, Catão-Dias JL (2022a) Extended-spectrum β-lactamase (ESBL)-producing
Escherichia coli survey in wild seabirds at a pristine atoll in the southern Atlantic Ocean,
Brazil: first report of the O25b-ST131 clone harboring blaCTX-M-8. Sci Total Environ 806(Pt
2):150539
Ewbank AC, Fuentes-Castillo D, Sacristán C, Esposito F, Fuga B, Cardoso B, Godoy SN, Zamana
RR, Gattamorta MA, Catão-Dias JL, Lincopan N (2022b) World Health Organization critical
priority Escherichia coli clone ST648 in magnificent frigatebird (Fregata magnificens) of an
uninhabited insular environment. Front Microbiol 13:940600
Faccone D, Moredo FA, Giacoboni GI, Albornoz E, Alarcón L, Nievas VF, Corso A (2019)
Multidrug-resistant Escherichia coli harbouring mcr-1 and blaCTX-M genes isolated from swine
in Argentina. J Glob Antimicrob Resist. 18:160–162
Faccone D, Rapoport M, Albornoz E, Celaya F, De Mendieta J, De Belder D, Lucero C, Gomez
S, Danze D, Pasteran F, Corso A, Mobilizable Colistin Resistance Group (2020) Plasmidic
resistance to colistin mediated by mcr-1 gene in Escherichia coli clinical isolates in Argentina:
a retrospective study, 2012–2018. Rev Panam Salud Publica 44:e55
Fernandes MR, Sellera FP, Moura Q, Souza TA, Lincopan N (2018a) Draft genome sequence of
a CTX-M-8, CTX-M-55 and FosA3 co-producing Escherichia coli ST117/B2 isolated from
an asymptomatic carrier. J Glob Antimicrob Resist. 12:183–184. https://doi.org/10.1016/j.
jgar.2018.01.015
26 N. Lincopan et al.

Fernandes MR, Cerdeira L, Silva MM, Sellera FP, Muñoz M, Junior FG, Azevedo SS, Power P,
Gutkind G, Lincopan N (2018b) Novel mcr-5.3 variant in a CTX-M-8-producing Escherichia
coli ST711 isolated from an infected horse. J Antimicrob Chemother 73(12):3520–3522
Fernandes MR, Sellera FP, Moura Q, Gaspar VC, Cerdeira L, Lincopan N (2018c) International
high-risk clonal lineages of CTX-M-producing Escherichia coli F-ST648 in free-roaming cats,
South America. Infect Genet Evol 66:48–51
Fernandes MR, Sellera FP, Cunha MPV, Lopes R, Cerdeira L, Lincopan N (2020) Emergence of
CTX-M-27-producing Escherichia coli of ST131 and clade C1-M27 in an impacted ecosystem
with international maritime traffic in South America. J Antimicrob Chemother 75(6):1647–1649
Ferreira JC, PenhaFilho RA, Andrade LN, Berchieri A Jr, Darini AL (2014a) Detection of chromo-
somal bla(CTX-M-2) in diverse Escherichia coli isolates from healthy broiler chickens. Clin
Microbiol Infect 20(10):O623–O626
Ferreira JC, Penha Filho RA, Andrade LN, Berchieri A Jr, Darini AL (2014b) IncI1/ST113 and
IncI1/ST114 conjugative plasmids carrying blaCTX-M-8 in Escherichia coli isolated from
poultry in Brazil. Diagn Microbiol Infect Dis 80(4):304–306
Figueroa-Espinosa R, Costa A, Cejas D, Barrios R, Vay C, Radice M, Gutkind G, Di Conza J
(2019) MALDI-TOF MS based procedure to detect KPC-2 directly from positive blood culture
bottles and colonies. J Microbiol Methods 159:120–127
Fuentes-Castillo D, Farfán-López M, Esposito F, Moura Q, Fernandes MR, Lopes R, Cardoso B,
Muñoz ME, Cerdeira L, Najle I, Muñoz PM, Catão-Dias JL, González-Acuña D, Lincopan N
(2019) Wild owls colonized by international clones of extended-spectrum β-lactamase (CTX-­
M)-producing Escherichia coli and Salmonella Infantis in the Southern Cone of America. Sci
Total Environ 674:554–562
Fuentes-Castillo D, Esposito F, Cardoso B, Dalazen G, Moura Q, Fuga B, Fontana H, Cerdeira L,
Dropa M, Rottmann J, González-Acuña D, Catão-Dias JL, Lincopan N (2020) Genomic data
reveal internationa llineages of critical priority Escherichia coli harbouring wide resistome in
Andean condors (Vultur gryphus Linnaeus, 1758). Mol Ecol 29(10):1919–1935
Fuentes-Castillo D, Navas-Suárez PE, Gondim MF, Esposito F, Sacristán C, Fontana H, Fuga B,
Piovani C, Kooij R, Lincopan N, Catão-Dias JL (2021) Genomic characterization of multidrug-­
resistant ESBL-producing Escherichia coli ST58 causing fatal colibacillosis in critically endan-
gered Brazilian merganser (Mergus octosetaceus). Transbound Emerg Dis 68(2):258–266
Fuga B, Cerdeira L, Moura Q, Fontana H, Fuentes-Castillo D, Carvalho AC, Lincopan N (2021)
Genomic data reveals the emergence of an IncQ1 small plasmid carrying blaKPC-2 in
Escherichia coli of the pandemic sequence type 648. J Glob Antimicrob Resist. 25:8–13
Fuga B, Sellera FP, Cerdeira L, Esposito F, Cardoso B, Fontana H, Moura Q, Cardenas-Arias A,
Sano E, Ribas RM, Carvalho AC, Tognim MCB, de Morais MMC, Quaresma AJPG, Santana
ÂP, Reis JN, Pilonetto M, Vespero EC, Bonelli RR, Cerqueira AMF, Sincero TCM, Lincopan
N (2022) WHO critical priority Escherichia coli as one health challenge for a post-pandemic
scenario: genomic surveillance and analysis of current trends in Brazil. Microbiol Spectr
10(2):e0125621
Furlan JPR, Gonzalez IHL, Ramos PL, Stehling EG (2020) International high-risk clone of
multidrug-resistant CTX-M-8-producing Escherichia coli C-ST410 infecting an elephant
(Loxodonta africana) in a zoo. J Glob Antimicrob Resist. 22:643–645
Galarce N, Sánchez F, Escobar B, Lapierre L, Cornejo J, Alegría-Morán R, Neira V, Martínez V,
Johnson T, Fuentes-Castillo D, Sano E, Lincopan N (2021) Genomic epidemiology of Shiga
toxin-producing Escherichia coli isolated from the livestock-food-human interface in South
America. Animals (Basel) 11(7):1845
García CP, Rubilar PC, Vicentini HD, Román GJC, León CE, Muñoz CG, Domínguez YM,
González RG, Bello TH, Labarca LJ (2011) Caracterización clínica y molecular de b­ acteriemias
causadas por enterobacterias productoras de β -lactamasas de espectro extendido: 2004–2007.
Rev Chil Infectol 28(6):563–571
Garcia JF, Nastro M, Dabos L, Campos J, Traglia G, Ocampo CV, Famiglietti A, Rodriguez CH,
Vay CA (2022) Molecular and phenotypic characterization of a multidrug-resistant Escherichia
coli coproducing OXA-232 and MCR-1.1 in Argentina. Microb Drug Resist 28(5):511–516
1 WHO Critical Priority Escherichia coli in Latin America: A One Health… 27

García-Betancur JC, Appel TM, Esparza G, Gales AC, Levy-Hara G, Cornistein W, Vega S, Nuñez
D, Cuellar L, Bavestrello L, Castañeda-Méndez PF, Villalobos-Vindas JM, Villegas MV (2021)
Update on the epidemiology of carbapenemases in Latin America and the Caribbean. Expert
Rev Anti-Infect Ther 19(2):197–213
García-Fulgueiras V, Bado I, Mota I, Robino L, Cordeiro NF, Varela A, Algorta G, Gutkind G,
Ayala JA, Vignoli R (2011) Extended spectrum β-lactamases and plasmid mediated qQui-
nolone resistance in Enterobacterial clinical isolates in the paediatric hospital of Uruguay. J
Antimicrob Chemother 66(8):1725–1729
Garcia-Fulgueiras V, Araujo L, Bado I, Cordeiro NF, Mota MI, Laguna G, Algorta G, Vignoli
R (2017) 2017 Allodemic distribution of plasmids co-harbouring blaCTX-M-15/aac(6′)-Ib-­
cr/qnrB in Klebsiella pneumoniae is the main source of extended-spectrum β-lactamases in
Uruguay’s paediatric hospital. J Glob Antimicrob Resist. 9:68–73
Ghiglione B, Brunetti F, Figueroa R, Santiago Bispo da Silva J, Pepe Razzolini MT, Di Conza J,
Gutkind G, Power P, Dropa M (2019) Community raw sewage effluent as a reservoir of resis-
tance genetic determinants in Buenos Aires, Argentina. ASM Microbe 2019. San Francisco,
USA. June 2019
Ghiglione B, Haim S, Penzotti et al (2020) Genomic characterization of multidrug-resistant
Enterobacteriaceae isolated from wastewater reveals the circulation of emerging pathogens
as a source of KPC-2 dissemination in Argentina. GW4 AMR symposium 2020. Bristol, UK
Gonzalez MJ, Ghiglione B, Figueroa-Espinosa R, Gonzalez SM, Rojas Molina F, Di Conza
JA (2022) Calidad bacteriológica y perfil de resistencia de aislamientos de Escherichia coli
en ecosistemas acuáticos circundantes a la ciudad de Santa Fe. XX Jornadas Argentinas de
Microbiología. 7–8 septiembre 2022
Gramundi I, Albornoz E, Boutureira M, Rapoport M, Gomez S, Corso A, Castro G, Faccone D
(2022) Characterization of third generation cephalosporin-resistant Escherichia coli clinical
isolates from Ushuaia, Argentina. Rev Argent Microbiol S0325–7541(22):00059–00051
Guzman-Otazo J, Gonzales-Siles L, Poma V, Bengtsson-Palme J, Thorell K, Flach CF, Iñiguez
V, Sjöling Å (2019) Diarrheal bacterial pathogens and multi-resistant enterobacteria in the
Choqueyapu River in La Paz, Bolivia. PLoS One 14(1):e0210735
Hawser SP, Bouchillon SK, Hoba DJ, Badal RE, Hackel MA, Lascols CA, Villegas MV, Rossi F
(2012) Low frequency of ertapenem-resistant intraabdominal isolates of Escherichia coli from
Latin America: susceptibility, ESBL-occurrence, and molecular characterisation (SMART
2008–2009). J Chemother 24(1):6–11
Hedman HD, Eisenberg JNS, Vasco KA, Blair CN, Trueba G, Berrocal VJ, Zhang L (2019) High
prevalence of extended-spectrum beta-lactamase ctx-m-producing Escherichia coli in small-­
scale poultry farming in rural Ecuador. Am J Trop Med Hyg 100(2):374–376
Hernandez J, Johansson A, Stedt J, Bengtsson S, Porczak A, Granholm S, González-Acuña
D, Olsen B, Bonnedahl J, Drobni M (2013) Characterization and comparison of extended-­
spectrum β-lactamase (ESBL) resistance genotypes and population structure of Escherichia
coli isolated from Franklin's gulls (Leucophaeuspipixcan) and humans in Chile. PLoS One
8(9):e76150
Iark ADS, Koga V, Vespero EC, Takayama Kobayashi RK, Moreira R, de Oliveira TC (2018) First
report of CTX-M-44 in Escherichia coli isolated from chicken meat produced in Brazil. J
Infect Dev Ctries 12(4):284–285
Instituto de Salud Pública de Chile (ISP) (2022). Infecciones asociadas a la atención en salud.
Retrieved from https://vigilancia.ispch.gob.cl/app/iaas
Larson A, Hartinger SM, Riveros M, Salmon-Mulanovich G, Hattendorf J, Verastegui H, Huaylinos
ML, Mäusezahl D (2019) Antibiotic-resistant Escherichia coli in drinking water samples from
rural Andean households in Cajamarca, Peru. Am J Trop Med Hyg 100(6):1363–1368
Leigue L, Warth JF, Melo LC, Silva KC, Moura RA, Barbato L, Silva LC, Santos AC, Silva
RM, Lincopan N (2015) MDR ST2179-CTX-M-15 Escherichia coli co-producing RmtD
and AAC(6′)-Ib-cr in a horse with extraintestinal infection, Brazil. J Antimicrob Chemother
70(4):1263–1265
Another random document with
no related content on Scribd:
The genealogical tree from Kane to Kahiko contains O ka papa mookuauhau mai a Kane mai a h
twenty-nine generations and from Wakea to iwakaluakumamaiwa hanauna; a mai a Wake
Kamehameha seventy-five generations. By adding the Kamehameha, he kanahikukumamalima han
generations before Wakea with those after him we have ka hanauna mamua aku o Wakea, hookahi h
one hundred and fourteen generations. We cannot, hanauna. Aka, aole nae e hiki ke hoomaopo
however, ascertain whether this is so, nor can we say that pololei keia mau papa mookuauhau. Pela na
this genealogical tree is correct. This, however, is what is moolelo o Kualii.
shown in the history of Kualii.

There are several genealogical trees in connection with He nui na mookuauhau e pili ana i keia mook
this genealogy of kings; the following is one of them: ka papa kuauhau malalo:

HUSBAND. WIFE. CHILD. KANE. WAHINE.


Kapapaiakea. Kauhihi. Hinakapeau. O Kapapaiakea. O Kauhihi.
Hinakapeau. Ukunohunohu. Ukunaopiopi. O Hinakapeau. O Kunohunohu.
Ukunaopiopi. Maakuanana. Kalei. O Ukunaopiopi. O Maakuanana.

Kaiakea.

Kalei. Kaeelekoha. Moanakea. Kalei. O Kaeelekoha.

Hulukeeaea.

Hauii.
Kaiakea. Kaehokumanawa. Kaiakea. Kaehokumanawa.
Hauee.

Moanakea. Kauakahikuaana. Kanehoalani. Moanakea. Kauakahikuaana.


Iwikauikauanui. Kauakahikuaana. Hauonunaholoholo. Iwikauikauanui. Kauakahikuaana.
Hulekeeaea. Kahakuakea. Hauiikaiapokahi. Hulukeeaea. Kahakuakea.

Uliuli.

Hauiikaiapokahi. Wahineikapeakapu. Hauiikaiapokahi. Wahineikapeakapu.

Maihea.

Uliuli. Kaukeano. Uliuli.


Kahakapolani. Kahakapolani.
Maihea. Mehameha. Maihea.

Uliuli. Niau. Kahiko. Uliuli. Niau.


Kahiko. Kupulanakehau. Wakea. Kahiko. Kupulanakehau.

In this genealogical tree there are eleven generations Ma keia papa kuauhau, he umikumamakahi
from Kapapaiakea 310 to Wakea. It is, however, told that Kapapaiakea mai a hiki ia Wakea. Ua oleloia
the genealogical tree to which Kane is the head, and the mookuauhau o Kane, a me ka papa kuauhau
genealogical tree of Kapapaiakea, were handed down by Oahu nei poe malama kuauhau ia, a ua ikeia
those who had the keeping of the Oahu genealogy, and ma ka moolelo o Kualii. A o ka mookuauhau
these divisions are seen in the history of Kualii; and the ia Wakea, mai a Wakea a hiki ia Kamehame
genealogical tree from Opuukahonua 311 to Wakea and malama kuauhau ia. A ua ike ia pela ia papa
from Wakea to Kamehameha had been handed down by moolelo o Moikeha. Aka o ka mea i ike mau
the Hawaii genealogy keepers, and this genealogical tree mookuauhau mai a Wakea mai a hiki ia Kam
is seen in the history of Moikeha. But the genealogical mea i olelo ia e Kalauwalu, a me kekahi poe
tree that is commonly seen these days is the one from a ma ka hoomaopopo ana i ka oiaio o na ma
Wakea to Kamehameha as told by Kalauwalu and other aole he akaka; aka, ma ka nana ana i ka ma
genealogy keepers. mookuauhau me he mea la, ua kaawale ko M
kaawale ko Kauai. Aka, o ko Molokai mooku
In trying to ascertain the truth of the different divisions of malama ana a ko Molokai poe kuauhau, ua o
these genealogical trees one is left in doubt as to their Hookumukahonua ke kupuna mua o ko Haw
correctness, but in looking them over one cannot help ma ka manao ana o ka poe kakaolelo, mai a
seeing that each island had a separate tree, the Maui one hookumu ana o ka hanauna alii.
being different from that of Kauai. Molokai’s genealogy
differs again. In the records kept by the Molokai
genealogist it is stated that Hookumukahonua was the
progenitor of the royal family of Hawaii, but in the opinion
of historians they generated from Wakea.

CHAPTER V. MOKUNA V.

THE BATTLES OF KUALII AND THE NA HOOUKA KAUA A KUALII, A


BATTLE GROUNDS. KAUA.

The battle on the plains of Keahumoa at Honouliuli, Ewa, Ua oleloia ma ka Mokuna I ka hoouka kaua a
is described in Chapter I. In looking over the history of Keahumoa, i Honouliuli, ma Ewa, a i ka nana
Kualii related in that chapter, it is thought to have been the Kualii ma kela mokuna, ua manaoia oia ka h
last battle in which he took part, for in Chapter II it is Kualii. No ka mea, ma ka Mokuna II, ua olelo
shown that Kauai was simply given over by its king to mai o Kauai e ko Kauai alii ia Kualii; nolaila,
Kualii, whereby the whole group from Hawaii to Niihau mai Hawaii a Niihau. Pela i manao ia ai, oia
was united [under him]. Therefore it is believed that was Kualii. [409]
Kualii’s final contest. [408]

The first battle on Oahu in which Kualii took part where a O ka hoouka kaua mua a Kualii i hoomaka a
general war was had, was the one fought on Kawaluna, oia ka hoouka kaua ana iluna o Kawaluna m
the heights above Waolani, 312 where a great slaughter oia ka luku nui ana i ula pu ai ke pili o Keana
took place that reddened the pili grass of Keanakamano. moolelo o ia kaua ana:
The history of that battle is told as follows:

Oahu had four kings just prior to the time of Kakuhihewa; Eha mau alii o Oahu mamua aku o Kakuhihe
Lonohulimoku was the king of Koolaupoko; Lonohulilani oia ke alii o Koolaupoko; a o Lonohulilani, oia
was the king of Koolauloa and Waialua; Lonokukaelekoa me Waialua; o Lonokukaelekoa, oia ke alii o
was the king of Waianae and Ewa; and Lonoikaika was Lonoikaika, oia ke alii o Kona, mai Moanalua
the king of Kona, from Moanalua to Maunalua. While
Kualii was residing at Kalehuawehe, in Waikiki, at a time Aka, o Kualii i kona manawa ma Waikiki, iaia
when he was about to attain the age of manhood, he Kalehuawehe, iloko o kona mau la e hookan
began to be dissatisfied with the king of Kona district, pono ole iho la kona manao i ko Kona nei ali
because his immediate attendants often complained of ponoi o Kualii, ua kaniuhu mau lakou no ko l
mea, hele aku la ua mau kahu nei o Kualii, a
being oppressed and would come to him with the me ka i aku: “Ina no hoi paha ka waawaa o k
following remarks: ikaika i ke kaua, ola nei mau iwi; aole, o ka w
lilo o ka hoounauna ino i na ’lii e, hele a ukiu
“If your muscular body was only that of a fearless warrior hoi, paeha oe, kai no ko koa i ka wa kamalii,
these bones would indeed be saved: but no, your strength ka he koa ia no ka wa kamalii.” I aku o Kualii
is worthless. Here we are being ordered roughly by the la ia oukou ka hua e hooikaika ai, he mau la
different chiefs which is so degrading and angers us. In
your younger days you could beat everybody whom you
fought against. Being so fearless in your childhood days,
one would think it would continue; yet alas, it was only the
fearlessness of youth.” Kualii replied: “There will be
fighting then, since you have found the cause why I
should urge it. A few days hence the pili grass will be
reddened.” 313

On the expiration of the days during which the temple on A pau na la o ke kapu heiau iluna o Kawalun
Kawaluna was dedicated, 314 the following night the army aku la ke kaua a Lonoikaika iluna o Keanaka
of Lonoikaika arrived on Keanakamano, as word had oleloia e Lonoikaika, ua kipi o Kualii. A oia no
been carried to Lonoikaika that “Kualii has rebelled.” This na koa ma ke kula o Keanakamano. No ka m
was the reason why the soldiers slept that night on the ana ia Kawaluna, aole i kupono ia ia Kualii.
plains of Keanakamano, Kualii in dedicating the temple on
Kawaluna had overstepped himself. Very early that Ma ka pili o ke ao, hoala aku la o Kualii i kon
morning Kualii aroused his father Kauakahiakahoowaha: “E! Auhea oe, hoalaia
Kauakahiakahoowaha 315 with the words: “Say, Where art ua puni kakou i ke kaua, eia malalo mai o ka
thou? Rouse up the men, we are now surrounded by the ma Koolau mai kekahi kaua, a eia malalo o W
enemy; there is one army below us, there is another army kaua; hookahi wale no pali i koe o Waolani; n
from Koolau and there is still another one from Waialua; na kanaka, a e hoakoakoa mai, no ka mea, u
there is but one pali left, that of Waolani, therefore you ke kaua.”
must rouse up the men and get them together as I am
I aku la o Kauakahiakahoowaha: “Pehea i m
ready for the battle.” Kauakahiakahoowaha replied: “How
kakou i ke kaua?” I aku o Kualii: “Ke hai mai
do you know that we are surrounded by the enemy?”
ko ke ao, no ka mea, ua olelo ae la ke alii o L
Kualii spoke up: “The night tells me that there will be war kakou, no ko kakou kii ana mai nei e kapu he
in the day time, for the king, Lonoikaika, has remarked, No ka mea, he akua nui ka mea nana e kapu
that we have rebelled against him, because we have
I aku o Kauakahiakahoowaha: “Auhea oe e K
come here to dedicate this temple on Kawaluna, thus
mai la ka po ia oe he kaua ko ke ao ana ae,
taking upon ourselves something which only a great god
nei hoi oe, hookahi pali i koe aole i paa i ke k
has power to do.” Kauakahiakahoowaha replied: “Say,
ko’u manao, ma ia pali kakou e holo aku ai i
Kualii, since the night has told you that there will be war
ma Waikiki.” I aku la o Kualii: “Heaha ka mea
during the day and you say there is left us but one more
aku auanei pakele ina he kaua no keia no ko
pali, that of Waolani, my idea is this: let us escape by way
no paha a he make, e make ana no, a ina no
of that pali this early morning and return to Waikiki.” Kualii
ola ana no.” [411]
replied: “Why should we run? Do you suppose that we
would be saved by escaping? If we are to die in this
battle, running will not save us, we would indeed die; and
if we are to live, we will surely live.” [410]

Kauakahiakahoowaha again asked: “What are we to do I aku la o Kauakahiakahoowaha, me ka nina


then?” Kualii replied: “Let us remain and fight them.” kakou?” I aku la o Kualii: “E noho kakou e ka
Kauakahiakahoowaha remarked: “If you want to fight, you Kauakahaikahoowaha: “Ina i makemake oe i
may do so, but as for myself I am going to look for a way aka, owau nei la, e imi ana wau i ko’u wahi e
of escaping.” Kualii then said: “You must not go; remain Kualii: “Mai hele oe, noho iho pela, ina e hele
where you are; if you go, I may not be able to see you, for wau e ike aku ia oe, make e mai oe i ke kaua
you might get killed by mistake; it is best that you stay noho mai oe a make pu iloko o ke kaua a Lo
with me and let us die together in this battle against
Lonoikaika if need be.”

This conversation with his father took up a good part of A no ia mea, ua lilo loa ko Kualii manawa i ke
Kualii’s time and the day grew brighter. When it became makuakane ma keia mea a malamalama loa
broad daylight, Kualii looked forth and behold the pili aku auanei ka hana o Kualii, he ula pu wale
grass was red with men; the pili grass of Keanakamano pili, ua pani ia iho ke pili o Keanakamano paa
was entirely covered with men. Kualii at this time covered manawa, hiamoe iho la o Kualii, aole nae he
himself over as though asleep; he was not, however, mea e maopopo ai i kona makuakane a me k
really asleep, but he did this to show his father and their pololei ka olelo a Kualii ia wanaao. I na kana
men that he had indeed spoken the truth that early Kauakahiakahoowaha e hiamoe ana, lohe ae
morning. While the men and Kauakahiakahoowaha were uwauwa ma kuahiwi mai, ma kahi e kokoke m
sleeping they heard a great commotion from the Nolaila, hikilele ae la o Kauakahiakahoowaha
mountain, somewhere near Kawaluna. hana, e hoonoho ana ke kaua; i kiei aku ka h
Kauakahiakahoowaha was therefore startled and looking e pii ana ke kahi maha o ke kaua i Puuiwa; e
around he saw that the enemy was already formed for Koolau kaua i Kaniakapupu, a o kekahi maha
battle. When he looked down the bottom of Waolani, one mai aia ma ka pali o Kalihi, ke pii aku nei hoi
wing of the army was climbing Puuiwa; the army from Kona aku nei kaua a hookui me ko Koolau ka
Koolau was coming down Kaniakapupu, while one of the Kualii.
wings of the army from Koolau was already on the Kalihi
cliffs, and still another wing from Kona was coming up
soon to meet the army from Koolau, whereby Kualii would
be entirely surrounded.

When Kauakahiakahoowaha saw this he called out to A ike ae la o Kauakahiakahoowaha i keia me


Kualii: “Say, where are you? Are you to continue sleeping, Kualii: “E, auhea oe? He moe mai ka kau, eia
when here we are surrounded by the enemy?” When kaua?” A no keia mea, pane ae la o Kualii m
Kualii heard this he spoke from within the bed clothes that pulou ana: “I aha auanei ka’u pono e ala ae a
covered his head: “What can I do by getting up? There is a’u pono, o ka noho iho no a hiki mai ka luku
only one thing for me to do, that is, to remain where I am make e hele aku ai; oia e, he wahi hapa kana
till the slaughter gets here. What have we on hand to fight olelo, e pono ai ke hele aku i ke kaua. Malia
them with when we can see for ourselves that they have keia kaua.”
no end of men on their side. On the other hand it is
entirely within reason that this battle is not intended for
us.”

That morning a messenger was seen coming as though Ia kakahiaka, ike ia aku la kekahi luna i hoou
sent by Lonoikaiaka. He approached Kualii and said: Lonoikaika mai, a hele aku la a halawai me K
“There is going to be a battle today.” When Kualii heard “He kaua ko keia la.” A lohe o Kualii i keia ole
the messenger he replied: “Why did they send you? If you aku la i ka luna: “I hoouna ia mai la no hoi oe
wish to make war come and do so, I shall not prevent it. paha e makemake no ke kaua, aole a’u hana
You know well enough that I have not as yet acquired the mai la no ia aole wau i a’o i ke kaua; a i mea
art of warfare. All would have been well if there was ana ia Oahu nei a puni e kii mai ia’u e kaua a
reason for this. With all this lack of reason, still you come ina la he hala kekahi; me ia hala ole no ka, o
and make war on a mere youngster whose bones are not luku i ke kamalii aole i oo ka iwi. E hoi oe a o
even matured. You go back and ask Lonoikaika what is kuu hewa.” I mai o Hema ka luna: “Ua lohe a
my fault.” Hema, the messenger, replied: “I have heard of ana o ka heiau nau e kapu, aole ka i kupono
your fault. It is the fact that you dedicated the temple, akua ka ka mea nana e kapu keia heiau.” I a
taking upon yourself something only a god has the right to aku ia Lonoikaikaole, na’u e kapu keia heiau
do.” Kualii replied: “Go back and tell Lonoikaikaole 316 that
I have the right to dedicate this temple.”

Hema thereupon returned to the king and reported as Hoi aku la o Hema, a olelo aku la i ke alii: “I i
follows: “Kualii told me to come back and tell you the mai au a olelo aku ia oe, penei oia i olelo ma
following words: ‘Go back and tell Lonoikaikaole that I Lonoikaikaole, na’u e kapu keia heiau.’ A pe
have the right to dedicate this temple.’ ” When Lonoikaika mai nei ia’u.” A lohe o Lonoikaika i keia olelo
heard what Hema had to say, he became very angry and manawa, aole o kana mai a ka huhu o Lonoi
remarked: “Is this youngster who is still so young that he ka oia wahi keiki ma’i lewalewa ko’u mea na
has no knowledge of what shame is, going to be the one ikaika ole. A heaha la hoi kana.”
to tell me that I am [412]not strong enough? Well, we’ll see
about it.” Lonoikaika then sent Hema to hasten and inform
the army from Koolau to bring the wings of the armies
together so as to surround Kualii.

When the armies were ready to begin the conflict, Kualii Hoouna aku la o Lonoikaika ia Hema e holo
looked about him and saw that the different armies were kaua mai, e hui na holo o na kaua, e hoopun
closing in on him, and the grass was so thickly covered ke kaua, ia manawa, nana aku la o Kualii e h
with men that it was dried up from the tramping; he then pau, ua owela ka nahele; alaila ninau ae la o
remarked to his own personal attendant, Maheleana: kona kahu ponoi: “E, auhea oe? I nei kakahia
“Say, where are you? This morning you must learn how to koa.” I aku o Maheleana: “Aole e ku ka ikaika
fight and how to be brave.” Maheleana replied: “One poai mai nei ka ohu mauka a makai, ma o a
cannot show his strength against such odds. The rain “Elua kaua, elua o Kane laua o Kanaloa, ku
clouds are encircling from above, from sea-ward and from no ia o ia nui i ka hee.” I ke kaua e hoopuni a
all sides.” Kualii spoke up: “There are two of us as Kane ae la oia i ka heiau e pule ai, a i ka pau o ka
and Kanaloa are also two. Let us then make a stand and hana o Maheleana, ua kokoke loa ke kaua. I
you will see these numbers flee.” While the armies were o Kualii i kana laau palau ia Manaiakalani, a
closing around Kualii he entered the temple to pray. At the Maheleana, me ka i aku: “Eia kuu laau palau
close of Kualii’s prayer Maheleana looked and lo, the iloko o ke kaua a Lonoikaika.”
enemy was close upon them. Kualii then reached for his
war club Manaiakalani 317 and handed it to Maheleana with
the remark: “Here is my war club, go out and enter into
the army of Lonoikaika.”

As directed by Kualii, Maheleana went forth and began E like me ka Kualii olelo, puka ae la oia a luk
the slaughter of the people with such courage that the palau, a hee aku la ke kaua ma kona alo pon
enemy retired from before him and ran directly toward Lonoikaika; na lakou i hee, hee na kaua a pu
Lonoikaika. When these people withdrew the whole of the ka pali o Waolani, hiolo aku la lakou me he il
enemy retreated, those on the pali of Waolani fell over like aku la o Kualii a pau loa na ’lii ma ko Lonoika
pebbles down the pali. Kualii then slew almost all the na kanaka make me he pauku laau la, ka he
chiefs on Lonoikaika’s side. The dead bodies were strewn kaua ana; a lanakila ae o Kualii ma ia hoouk
around like logs of wood, so great was the number of hoouka kaua mua a Kualii, a lilo ae la ia Kua
those that were killed in this battle. Kualii was therefore Moanalua a Maunalua. Mahope iho o ia man
victorious in this his first battle and he became the owner i Kailua ma Koolaupoko, a malaila oia i noho
of all the land from Moanalua to Maunaloa. Shortly after nui o Kalanihale.
this Kualii went and lived in Kailua, Koolaupoko, in a great
palace called Kalanihale.
Sometime after this, Kualii and Maheleana, his personal I kekahi manawa mahope mai, ao ae la o Ku
attendant and fellow companion in battle, took lessons in Maheleana, kona kahu, a hoa kaua pu hoi, i
learning the art of using the war club, and he took Kahai lawe ae la oia ia Kahai, a me Malanaihaehae
and Malanaihaehae to be his chief warriors. They all ao iho la lakou nei i na mea kaua a pau a ma
studied the different arts of warfare until they were quite mahope iho, holo ae la o Kualii me kona mau
proficient. Shortly after this Kualii and his chief warriors ka manao e loaa ia lakou ka laau palau no la
sailed for Kauai, being desirous of procuring certain kinds hele ana, ua loaa ko lakou makemake, a hoi
of war clubs. 318 On this tour they were able to obtain what mau laau palau la, a kapa aku la o Kualii i ka
they wanted and returned with their new weapons. Kualii Hulimokualana.
named his war club Hulimokualana. 319

On their return from Kauai, Kualii desired to land at Hoi mai la o Kualii mai Kauai mai a pae ma K
Kamaile, Waianae, but upon arrival there he found that hoi, ua hoonoho mua ia ke kaua e ko Waiana
the place was already prepared for battle under the ko Koolauloa alii mai me kona kaua. E kali a
command of the chief of Waianae and Ewa, the Koolau mai Kauai mai, alaila o ka hoomaka no ia e k
chief and his army had also arrived there and all were
waiting for Kualii’s return from Kauai when they would
engage him.

While out at sea some distance from land Kualii, by his A waena moana, ike e no o Kualii ua puni o W
supernatural powers, knew beforehand that Waianae was hoomoemoe. Ia manawa, olelo aku la o Kua
surrounded by an army which was waiting for him. So he laua me Maheleana: “E, ua paa uka o Waian
remarked to Malanaihaehae and Maheleana: “Say, no ia kakou a pae o ka hoomaka no ia o ka l
Waianae is surrounded by an army that is ready to fight ike e no o Kualii i keia mau mea ma kona an
us as soon as we make a landing.” Before Kualii had mamua o kona holo ana i Kauai, ua kauoha
sailed for Kauai he ordered his men to come and meet e imi mua mai, ke [415]hiki aku i na la e hoi ak
him at Waianae upon his [414]return from Kauai, but when mai. Aka, ia Kualii ma i pae aku ai ma Kama
Kualii and his fellow travelers arrived outside of Kamaile kaua; a no ia mea, lana iho la na waa iloko o
they saw the place surrounded by an army. Upon seeing ia po. Ia kakahiaka ana ae, i nana aku auane
this they laid off in their canoes all that day and night. In ua uhi ia mai ke pili o Kamaile e na kanaka.
the morning when Kualii looked he saw the pili grass of
Kamaile was completely covered by the people.

While on the canoes that morning Kualii, upon seeing the Iluna no o na waa ma ia kakahiaka, pane ak
people, addressed them in the following words: “You no makemake kaua me Kualii, ihea e kaua ai?”
doubt want to fight Kualii, but where will the battle be?” “Pae no na waa i uka nei, o ke kaua no ia.” I
The people from the shore replied: “As soon as the kakou iuka o Kalena, ilaila e kaua ai. Ina ia n
canoes land the fighting will commence.” Kualii answered moana loa no e hele ai na waa, o Molokai ke
back: “Let us go to Kalena and fight there. If you insist on a Kualii, iuka o Kalena e kaua ai, ae aku la k
fighting here the canoes will continue by sea and land at nolaila, pae aku la lakou iuka, o Kualii, o Mah
Molokai.” Because of this request of Kualii to go to Kalena Malanaihaehae. Hele aku la lakou mauka a n
and there fight, the chiefs of Waianae consented because po a ao ae, ma ke kakahiakanui, o ka hoouk
it was but a reasonable request. Kualii, Maheleana and ma Kalena, i ke kula o Haleauau ma Lihue. M
Malanaihaehae therefore came ashore and proceeded by ekolu mano ka nui; a ma ko Kualii aoao hoi,
land to Malamanui. All that night both sides took a long o ka hee iho la no ia o na alii o Waianae a m
rest; but early in the morning the fighting commenced at la o Kualii ia hoouka kaua ana o Kalena.
Kalena on the plains of Haleauau, at Lihue. On the one
side there were twelve thousand men, while on Kualii’s
side there were but three men, and yet the armies of the
chiefs of Waianae and Koolauloa were routed. Kualii
named this the battle of Kalena.

A few days after this three more battles were fought, at A ma kekahi mau la ae, he mau hoouka kaua
Malamanui, Pulee and Paupauwela. These were the Pulee, a ma Paupauwela, oia ka hoouka nui
greatest of the battles fought by Kualii in all the Oahu mamua o na hoouka kaua a pau ma Oahu n
contests. Sometime after he had conquered the whole of manawa mahope mai o kona ai ana ia Oahu
Oahu he heard that there was a battle in Hilo, Hawaii; he kaua ma Hilo i Hawaii; nolaila, hele aku la oia
therefore made up his mind to make a trip to Hawaii with mau pukaua. A lohe o Haalilo, ua hiki aku o
his chief warriors. When Haalilo heard that Kualii had Laupahoehoe, alaila, hoomakaukau ae la oia
arrived at Laupahoehoe he immediately prepared for war, la o Kualii i Peahi ma Hilo, halawai koke ae l
so that when Kualii reached Peahi in Hilo he ran into o ka hoomaka iho la no ia o ke kaua, a lanak
Haalilo and the battle commenced. It was of but short aku la na ’lii o Puna, ua hee o Haalilo, hee ho
duration and Kualii was victorious. When the chiefs of mau alii.
Puna heard that Haalilo was beaten they too fell back.

Shortly after this word was brought to Kualii at Hilo that A mahope iho o ia manawa, hiki aku ka lohe
the chiefs of Oahu had again risen against him and were na ’lii o Oahu nei. Ia manawa, hoi mai la o K
ready to dispute his title as king of Oahu. Upon hearing ma Oahu nei, ua pau loa na kanaka a pau m
this Kualii returned from Hilo to Oahu and found upon his Waianae kahi i noho ai, ua hui ae la na ’lii mu
arrival that all the people, together with the rebellious me ka manao lokahi, e kipi aku ia Kualii. A n
chiefs, had gone to Waianae to hold a council of war with Kualii, aia na ’lii a pau malalo o Waianae; no
the one set purpose of fighting him. When Kualii heard me kona mau pukaua, a hiki lakou malaila, i
that all the chiefs were gathered at Waianae, he continued hana, he mea e ka nui o na kanaka. A o ka h
on with his chief warriors for that place. Upon arrival at the ia, a lanakila iho la o Kualii ma ia hoouka ana
seat of war they looked and saw that the rebellious chiefs a Kualii ma i ka nui i make ma ia hoouka ana
had indeed a very large army. No time was lost, however, Kalapo, a nui no hoi na kupapau malalo o El
for the battle immediately commenced, and again Kualii ia kekahi mau lalani mele ma ka haku ana a
was victorious. After the battle Kualii and his chief warriors me ke ano o ia hoouka kaua ana malaila, a p
looked over the battle ground and saw that a very large
number of men had been killed, so much so that the
waters of Kalapo were dammed and a large number of
dead bodies were strewn below Eleu. Because of this
great victory certain lines of mele were composed by his
attendants which read as follows:

A battle for Ku, He kaua na Ku,


Beating his enemy on the heights of Kawaluna. E uhau ana iluna o Kawalu
Where, where is the battle field Ihea, ihea la ke kahua,
Where the warrior is to fight? Paio ai o ke koa-a?
On the field of Kalena, 5 I ka i kahua i Kalena, 5
At Manini, at Hanini, I Manini, i Hanini
Where was poured the water of the god I ninia i ka wai akua,
At Kahana, at Malamanui; I Kahana i Malamanui
On the heights of Kapapa, at Paupauwela, Ka luna o Kapapa, i Paupa
Where they lean and rest; 10 I ka hilinai i ke kalele, 10
At the hala trees of indolent Halahalanui, [416] Ka hala o Halahalanui maa
At the ohia grove of Pule-e, Ke kula ohia ke Pule-e, [417
The god of Lono, of Makalii, Ke ’kua o Lono o Makalii
The fragrant branch of the Ukulonoku, Ka lala aalao Ukulonoku,
Mayhap from Kona, from Lihue, 15 No Kona paha, no Lihue. 15
For the day at Maunauna, No ka la i Maunauna,
For the water at Paupauwela; No ka wai i Paupauwela,
Growing low at Nepee, I ulu haa lilo i Nepee,
At the slaughter of Aui, A ka hauna o Aui.
Where the priests joined in the battle. 20 Kokomo kahuna i kakua laa
Ku is arrayed in his feather cloak, Komo Ku i kona ahuula,
The sun-lighted rain in the heavens, Ka wela o ka ua i ka lani,
The sun at Kauakahihale. Ka la i Kauakahihale,
Red is the leaf of the mamane, Ula ka lau o ka mamane,
The koaie of Kauai; 25 Ke koaie o Kauai; 25
The sea grass has been stripped by Ku— He pili kai ihi ia e Ku,
The waving [grass] of Kamaile; Ka aloalo o Kamaile,
The towering surf of Maihiwa, Ka nalu kakala o Maihiwa,
Which dammed up the waters of Halapo. Pania ka wai i Halapo,
The breaking up is below at Eleu, 30 Ka naha ilalo o Eleu. 30
The rain is drawn away to the sky, Huki kaua a moa i ka lani,
Like a full retreat from the mountain; Me he hee nui no kuahiwi;
It must be the defeat of Hilo by Puna, Ka hee ana o Hilo ia Puna,
There at Hilo is Peahi. Aia ma Hilo Peahi;
Red is the water of Paupauwela, 35 Ula ka wai i Paupauwela, 3
From the slain at Malamanui, Ke kilau o Malamanui,
The slain on the ridge at Kapapa. Ka moo kilau i Kapapa.
The tidings reached Haalilo Kui ka lono ia Haalilo,
Your younger brother is beaten. Kaua aku la ko kaina;
Haalilo is sore at heart, 40 Hahai Haalilo i ka manawa
For Ku has left but few of the priests; I kai muku kahuna ia Ku;
They are beaten by Ku, I la ka mawa ia Ku,
The children of Haalilo. I keiki a Haalilo.
Here is Malanaihaehae, Eia Malanaihaehae,
Offspring of mischief-making Niheu, 45 Kama a Niheu kalohe, 45
The dammer of the waters of Kekeuna. Ke pani wai o Kekuna,
A prodigy among the people. He mee nei no ke kanaka,
He is girding on his robe, Ke pu nei i ka aahu,
He is whirling his weapon [in the air], Ke lapa nei i ka laau,
The war club is caught in his robe. 50 Ka laulau o ka aahu, 50
Here is Haalilo, Eia Haalilo-e!—
Ku is indeed king. O Ku no ke alii.

CHAPTER VI. MOKUNA VI.

RELATING TO KUALII’S TRIP TO HAWAII. NO KA HOLO HOU ANA O KU

Sometime after the battles spoken of in Chapter V were Mahope mai o kela mau hoouka kaua ana i o
fought, where Kualii maintained his title of king of Oahu, V, a me ko Kualii lanakila ana, a pau ka hoop
after the land matters were satisfactorily arranged, he alaila, holo hou aku la o Kualii i Hawaii, a ma
again set sail for Hawaii and landed in Hilo where he took liuliu kona noho ana malaila, alaila, kui aku la
up his residence for some time. While there word was Molokai, ua kaua aku a kaua mai a pono ole
brought to him of wars on Molokai, where several pitched No ka mea, o na ’lii o Koolau o Molokai, ua m
battles had been fought and the chiefs were in conflict e lilo Kekaha ia lakou, mai Kawela a Maamo
with one another all the time. The cause of all the trouble ke kumu o ko lakou manao nui ana i kela wa
was this: The chiefs on the Koolau side of Molokai were ’lii o Kekaha, a nolaila i kipi ai na ’lii o Moloka
anxious to get possession of Kekaha, a stretch of country
from Kawela to Maamomi; and the reason why these
chiefs were so desirous of getting possession of this
section of country was on account of the fishing. But the
chiefs of Kekaha, knowing the value of these fishing
grounds, were determined to hold on to them; so this
determination on their part caused a general internal
conflict at this time.

When Kualii heard of this general conflict on Molokai, he A no keia mea, lohe ae la o Kualii i keia kaua
left Hilo and set sail for Molokai. On the way Kualii aku la oia ia Hilo, a holo mai la i Molokai. Hik
touched at Honokawai in Kaanapali, Maui, where a chief Honokawai, i Kaanapali ma Maui, ua puka a
by the name of Paepae arrived at the same time. This Kanapaali ia manawa. O ua Paepae nei, oia
Paepae was one of the chiefs of Kekaha, and the reason manawa. A o ke kumu o kona hiki ana i Mau
why he had come to Maui was to enlist Kauhi, one of the kekahi alii o Maui, he keiki ua o Kauhi na Ka
chiefs of Maui, to come to their aid. This Kauhi was the Kamalalawalu. Ia Paepae i hiki mai ai ma Ka
son of Kauhiakama, the younger brother of Kamalalawalu. lohe ae la oia o Kualii keia, ua hiki aku ma K
Upon Paepae’s arrival at Kaanapali he was told that Kualii oia e ike maopopo ia Kualii, no ka mea ua ka
had already arrived there. Upon hearing this he went to ikaika, a oia wale no ke kumu o ko Paepae h
ascertain whether it was really the Kualii who was noted maopopo. [419]
for his great strength. That was the sole purpose of
Paepae’s visit to see and be assured that it was Kualii.
[418]

When Paepae saw for himself that it was indeed Kualii he A ike aku la o Paepae o Kualii io keia, nolaila
decided there and then to abandon his first idea of manao mua e kii ia Kauhi. A no keia mea, ho
enlisting Kauhi’s aid, and left in haste for Kekaha to notify aku la i kekahi mau alii o Kekaha, o Kualii ke
the chiefs of his discovery and to ask their consent to the Kaunakahakai, aia na ’lii a pau o Kekaha ma
change in the programme. Upon his arrival at Kaunakakai hoomakaukau ana no ka hoouka kaua ke hik
he found that all the chiefs of Kekaha had gone to Paepae i hiki aku ai ma Kalamaula, ike mai l
Kalamaula preparing for another battle to commence Paepae; a no ia mea, nana mai la na ’lii i ka
upon the arrival of Kauhi. But when Paepae arrived at olelo.
Kalamaula the chiefs saw that Paepae had returned alone
and so were anxious to hear what he had to say about his
mission.

When Paepae came up to the chiefs he was asked: A halawai o Paepae me na ’lii ninau mai la la
“Where is Kauhi, the chief?” Paepae replied: “I left here Kauhi?” I aku la o Paepae: “Ua hele aku nei
with my mind fully made up to procure Kauhi, but upon my Kauhi, aka, halawai koke aku nei wau me ke
arrival at Kaanapali I met Kualii, the king of Oahu, so I ma Kaanapali, nolaila hoi mai nei wau e hai a
returned to inform you of this fact and to urge upon you to ia Kualii e lawe mai ma ko kakou aoao, o lilo
try and enlist him on our side, else the Koolau chiefs will Koolau mau alii.” A no ia mea, hoolale hou n
get him first.” When the chiefs heard this they urged upon
Paepae to again set sail, and also sent Kapolei, daughter a hoouna pu aku la ia Kapolei ke kaikamahin
of Keopuolono, to entertain Kualii. Early that morning hoolealea ia Kualii.
Paepae reached Kaanapali, but to his surprise found that
Kualii had already left for Molokai at dawn.

Upon hearing that Kualii had already left for Molokai, he Ma ia wanaao no hiki aku la o Paepae i Kaan
boarded his canoes again and returned in haste. While in o Kualii ia wanaao no i Molokai. A lohe o Pae
mid-channel he saw the flapping of the sails of canoes Kualii, hoi hou mai la no oia, a iwaena moan
inside of the reef at Kamalo, so Paepae followed in. kilepalepa ana ka pea o ka waa, maloko o ku
Before the several things in Kualii’s canoes could be malaila no o Paepae i hiki mai ai. Aole i pau
taken ashore and before the canoes could be hauled on Kualii i ka lawe i uka, e hekau ana no i kai no
the beach, Paepae arrived and moored his canoe at the ana o Paepae a hekau pu na waa me ko Kua
stern of Kualii’s canoes. Without further delay Paepae told
Kualii the object of his errand in the following words: “I Ia manawa, hoomaka koke no o Paepae e h
have come to entreat you to come to our rescue. The ai ia Kualii, me ka i aku: “I kii mai nei wau ia
chiefs of Koolau have taken up arms against us with the Aia na ’lii la o Koolau, ua kipi mai nei ia mako
intention of taking away from us our lands from Kawela to Koolau mau alii, e lilo ko makou mau aina m
Maamomi. Because of this desire on their part we have a nolaila, ua kue aku a kue mai makou e noh
had several disputes and a battle is about to commence. no koe; ua hoomaka mua iho nei no nae i ke
A minor engagement has already taken place, however, in makou, o ka nui o na ’lii aia iluna o Maunaloa
which we were beaten. The majority of the chiefs are
encamped on the top of Maunaloa.”

When Kualii heard this he immediately gave his consent A lohe o Kualii i keia olelo o ka ae koke no ia
and the canoes were again put to sea and they set sail for kau ma Kaunakahakai, a kukakuka ae la me
Kaunakakai where they arrived in due time. A council was ana, o ka hele koke iho la no ia, maluna o na
then held by the chiefs, at the close of which they set out. mauka na ’lii o Molokai me Kualii, a hiki ma M
The men were embarked on the canoes, while the kau aku la o Kualii ma me na ’lii maluna o na
Molokai chiefs and Kualii went by land until they reached Kalaupapa.
Maamomi, where Kualii and the chiefs took the canoes
and set sail for Kalaupapa.

When the chiefs of Koolau heard that the war was to be I ka lohe ana aku o na ’lii o Koolau ua hiki ak
carried into Kalaupapa, the war canoes were put out from Kalaupapa, nolaila holo mai la na waa kaua
Halawa and from all the Koolau side to go to battle. But Koolau a puni no ka hoouka kaua. Aka, ua h
Kualii and his chief warriors, Maheleana and me kona mau pukaua me Maheleana a me M
Malanaihaehae, with two other warriors had already kekahi mau pukaua e ae elua. A make pio ih
encountered the chiefs residing at Kalaupapa and had ma Kalaupapa ia manawaa. A hiki mai la kek
defeated these chiefs. But other chiefs of Koolau and Koolau a mai Kona mai kekahi mau alii me n
Kona with their men arrived soon after this who were no ka hoouka kaua i na ’lii o Kekaha. Aka i k
prepared to continue the battle against the chiefs of alaila ua oi aku ko Paepae ikaika a me kona
Kekaha. In this battle Paepae was very conspicuous both pukaua a Kualii. A lanakila ae la o Kualii ma
in strength and bravery, so much so that he and his force Molokai a puni, a lilo ae la ka aina ia Paepae
surpassed the chief warriors of Kualii. When Kualii and his
followers were victorious over all the chiefs of Molokai all Aka, aole me ka luku i ka laau palau kela lan
the lands on the Koolau side came into Paepae’s ka luku ana a Kualii me ka maka o ke koi ana
possession. This victory was not, however, gained inoa, he koi pohaku. A penei ka moolelo o ka
through the use of the war clubs, but through the use of ka maka o ke koi. [421]
Kualii’s stone axe named Haulanuiakea. Following is the
story of the destruction of the enemy by Kualii with the
blade of the axe. [420]

While Kualii and his followers were floating in their canoes Ia Kualii ma e lana ana ma kahi one i Kalaup
over the sand bar at Kalaupapa the soldiers from Koolau a lalau i ka waa o Kualii e hoopio, he mau ka
swam out to the canoes of Kualii with the intention of auamo ae la i na waa o Kualii. Ia wa, ku ae la
capturing them; there were some forties in number. When a hili iho la me ka maka o ke koi ma kekahi a
they got to the canoes they took hold of them and lifted aku la kekahi waa i lalo oiai ua amo ia na wa
them onto their shoulders. While this was being done Malanaihaehae, ua pau na kanaka o kekahi
Kualii rose with his axe in hand and swung it along one ku ae la ua Malanaihaehae nei, a lalau mai la
side of the canoes killing those on that side, which caused lima e paa ana, a oki iho la ma kekahi aoao,
the canoes to lean toward that side as the canoes were kanaka i ka make, a haule iho la na waa i ke
then on the shoulders of the men. When Malanaihaehae mamua.
saw that the people on one side of the canoes were all
slain, he rose and reached for the axe which was being
held in Kualii’s hand and swung it along the other side of
the canoes, which slew all the people on that side; and
the canoes again fell on even keel in the sea and floated
as before.

Not very long after this some more of the enemy came Aole no i liuliu, hiki hou mai la no he mau kan
along, equal in number to those that had been slain, and nui me na kanaka mua i make, a lawe ae la
again lifted up the canoes of Kualii just as the others had iluna e like me ka auamo mua ana no a kela
done, without any signs of fear, although the others were mai i keia poe e make ana. Ia manawa, luku
floating around dead. Again the axe was used with deadly maka o ke koi, a lanakila hou ae la no o Kua
effect and again Kualii and his followers were victorious Haulanuiakea. Pela mau no ka luku ana a pa
by the use of the blade of Haulanuiakea. This was kept up make. A i ka hoouka kaua hope loa ana ma
until the whole army was slain. la o Kualii i ka luku ia Paepae me Malanaiha
Paepae maluna o na koa a pau. A mahope i
At the final battle which was fought at Pelekunu, Kualii left Pelekunu, ku aku ai o Paepae a olela kaena
the fighting to Paepae and Malanaihaehae. Again Paepae me ka i aku: “Ua pau oukou i ka lukuia e ka l
showed his quality by routing the whole army. After this
great slaughter at Pelekunu, Paepae stood up in the Ia huaoleio, alaila akahi no lakou a lohe o Ku
canoe and spoke to the people in a boastful manner manawa, haawi ae la na ’lii o Koolau i ka ain
saying: “You are all slain by the war club of Kualii.” At Kualii. A ma keia kaua ana, o keia ke kaua i
these words the people were for the first time made aware lalani mele o ko Kualii inoa i hoike ia ma ka M
of the fact that it was Kualii that had killed their men. The hai ana malalo iho penei:
chiefs of Koolau then gave up to Kualii the whole of
Molokai. It was this battle that a few lines of the Kualii
mele speaks of in Chapter I, which run as follows:

Kuku, Aa, O Kuku, o Aa,


Haulanuiakea the axe, O Haulanuiakea ke koi.
Paepae, Manau his wife. O Paepae o Manau ka wahin
They brought forth Kanaenae that dwells on the mountain, Hanau ka naenae noho kuam
The Hinihini that sings on the high mountain. 5 Ka hinihini kani kuaola; 5
Broken on the front seat of the canoe, Hakina iho i ka wae mua o k
That is [Molokai] torn asunder, Ua naha ke ’na.
Deserted by Kanaloapuna, Haalele aku Kanaloapuna,
Kanaloawaia, Kanaloawaia,
[There is] death if you run toward the mountains; 10 Make holo uka, 10
[There is] death if you run toward the sea. Make holo kai.
Luukia is suffering headache, Hoonalulu ana Luukia,
Made sick by the unpleasant sensation of pregnancy Hoopailua i ka iloli,
Conceiving the child. I ke kauhua o ke kamaiki.
The ieie is conceived that creeps in the forest, 15 Hanau ka ieie hihi i ka nahel
Makaaulii was his wife O Makaaulii kana wahine.
Which brought forth the lupua and laulama Hanau ka lupua me ka laulam
Like unto the bushy stock of Lono, Ku i ke opu o Lono,
Kapolei was the wife. O Kapolei ka wahine.
Kukaikaina behind the spider, 20 O Ku ka i aina i hope ka lana
Of Kukonaihoae, O Kukonaihoae,
Ku of the rising sea. O Ku o ke kai malielie
Like unto a dancing sea is Ku; Me he kai e haa aku ana o K
Here is the woman that hides, Eia ka wahine peeki
Covered by the dust of Keaau, 25 Uhi lepo o Keaau, 25
The calabash of kneaded earth. Ka umeke hoowalina lepo
Like unto the leaf of the sugar-cane is the path. Me he haka la ke ala.
Here is the company of travelers, Eia na huakai hele
The slippery road that makes men fall, Alanui ka kanaka.
Which softened the dirt of Mahiki, 30 Wali ai ka lepo o Mahiki 30
Being trodden down by the foot. I ka paala a ka waewae.

In this mele the battles fought by Kualii as related in this Ma keia mele, ua haiia na hoouka kaua ana
chapter are spoken of. After Kualii had made a new keia Mokuna. A pau ka Kualii hooponopono
division of the lands, he then left Paepae and Manau his aku la oia ia Paepae, a me Manau kana wah
wife in charge of the island of Molokai subject to his aimoku o Molokai malalo o Kualii. A hoi mai
further pleasure. Kualii then returned to Oahu and went to noho ma Kailua, Koolaupoko, maloko o kona
live in Kailua, Koolaupoko, in his palace called Kalanihale. Kalanihale. [423]
[422]

CHAPTER VII. MOKUNA VII.

KUALII’S RETURN TO OAHU FROM HOI O KUALII I OAHU MAI MO


MOLOKAI.

After Kualii completed the redivision of the lands of Mahope iho o ka pau o ka Kualii hooponopo
Molokai, those pertaining to the chiefs as well as to the me ka hooponopono ana i na ’lii a me na kan
people, he returned to Oahu accompanied by his Kualii i Oahu me kona mau hoa hele, kana m
companions, his chief warriors. Upon arriving from ana mai a Kualii mai Molokai mai, a noho ma
Molokai he proceeded on his way to Kailua where he nae ka pono o ka noho ana o na kanaka a m
found that the chiefs and people were all living in peace. manawa mahope mai o ka noho ana ma Oah
After residing on Oahu for some time Kualii again set out o Kualii i Hawaii a noho hou ma Hilo, oia ke
for Hawaii and again took up his residence in Hilo, this ma Hilo.
being the third time that he decided to go and live there. Noho iho la o Kualii ma Hilo ia manawa, a he
After Kualii had been living in Hilo for some time word was mai, lohe hou aku la no ua o Kualii he kaua m
brought to him that war had broken out on Lanai, caused keiki a Kauhiakama, no ka mea, ua kipi mai
by Kauhi, son of Kauhiakama; the chief of Lanai having keiki a Kauhiakama kekahi kuhina o Kamala
taken up arms against the son of Kauhiakama, one of moolelo o ke kaua ana. I kekahi manawa, he
Kamalalawalu’s ministers. Following is the story of this Haloalena, a o ka puni punahele a ua alii la,
battle: manawa e hiki aku ai ka auhau manu a ke a
ka luna a ua alii nei ka hele e kala aku i ka o
Haloalena, the chief of Lanai, was considered a very good me kona makemake. A penei e kala hele aku
ruler. His great favorite pastime was the collection of the
skeletons of birds. When the chief’s bird tax was about
due it was the usual custom of the agents to go out and
proclaim the chief’s wishes. Following was the
proclamation announced by the agents:

Tomorrow cook the food. Apopo-e, kahu ke-o.


The following day, Ia po iho a ao a-e,
[Is] the snaring of birds for the king. He hoohei manu na ke alii-e.
Pick the feathers off the birds, E hukihuki ka hulu o ka ma-nu,
Pick all the meat, E lawe ka io a pa-u,
Be careful with the bones lest you break them. E malama i ka iwi o ha-i;
If the bones are broken and you are a chief of a district Ina i hai ka iwi o-ka manu, a he
You shall no longer be a district chief; E pau kona aimoku a-na;
If you are a chief of an ahupuaa 320 Ina he alii aiahupua-a,
You shall no longer be chief of that ahupuaa; E pau kona aiahupuaa a-na.
If it be a common farmer who breaks the bones of the Ina he lopa ka mea i hai ka iwi o
bird, He make kona ho-pe.
Death shall be his portion.

This was the king’s constant proclamation to the people in Penei ke alii e kala aku ai imua o na kanaka,
order that they be informed of his law. After a person has ke alii kanawai. Aia a pau ka ke kanaka hana
cleaned the skeleton of a bird it is then carried into one of lawe ia aku la e kukulu maloko o kekahi mau
the king’s warehouses and there made to stand. These mau manu iwi wale no, i lawe ia ka io a pau,
skeletons are picked clean of their meat and are stood up iloko o ka halau. Aia a makaukau ko ke alii m
in rows in their storehouses. After the king’s wishes are la ke kanaka i ke alii e hele mai e nana i na h
carried out he is then sent for to come and look at the manawa a ke alii e hele aku ai e nana i ke ku
skeletons. After looking through one house he would go to maloko o ka halau; aia a pau ae kana nana a
the next one and inspect the skeletons in that house. This aiaila komo aku ana he halau hou; a pela e m
was Haloalena’s usual way of passing his time. After Haloalena. I ka pau ana ae o ka ke alii maka
inspection the king would retire to his house. la ke alii i ka hale.

Once upon a time Kauhi happened to be in Lanai and saw Aia a lohe o Kauhi ua hoi o Haloalena i ka ha
the king returning to his house one day after inspecting aku ai o Kauhi iloko o ka hale manu a Haloa
his skeletons. Kauhi then went into Haloalena’s hili aku la i na manu iwi, a pau loa i ka ulupa
storehouses with long poles and knocked down all the ai a pau na halau manu o ke alii o Lanai. Ia m
skeletons from their places, and he kept this up until he nana na halau manu iwi ua pau i ka haihai ia
had gone through all the storehouses of the chief of Lanai. mai la o Haloalena a ninau mai i ke keiki a K
When the king heard that Kauhi had entered the kapu [425]o oe?” Alaila hai aku la o Kauhi me
storehouses and had destroyed all his skeletons he sent koa la: “Na Kauhiakama.” Olelo hou aku la o
for the son of Kauhiakama and asked him: “Whose Kauhiakama no oe i olelo mai e haihai i kuu
mischievous son [424]art thou?” Kauhi answered without Alaila olelo mai o Kauhi: “Aole i olelo mai o K
fear: “Kauhiakama’s.” Haloalena again asked him: “Was it mai e haihai i ko mau halau manu. Aka, eia k
Kauhiakama that told you to destroy all my skeletons?” ia’u, e hele mai au e kolohe, a e koa hoi, oia
Kauhi replied: “Kauhiakama did not tell me to destroy the mai ia’u; a nolaila la hele mai nei au e kolohe
skeletons in your storehouses, but what he told me was to kipi ana o na ’lii o Lanai me ko Maui, me ka m
come and act in a mischievous manner and to be Lanai aole malalo o na ’lii o Maui. No ka mea
fearless. This was all he told me; therefore I came and alii o Lanai, malalo no lakou o Kamalalawalu
acted mischievously.” This was the cause of the hostilities
between the king of Lanai and the king of Maui, and the
reason why the king of Lanai wanted to be independent
and not be any longer under the king of Maui. At this time
the chiefs of Lanai were under the control of
Kamalalawalu, king of Maui.

When Kualii heard of this proposed war he set sail from A lohe o Kualii i keia haunaele kaua, ia mana
Hilo and first touched at Kaupo where he found that the mai Hilo mai a hiki ma Kaupo, ua pau mai na
Maui chiefs had gone to Lanai. Upon hearing this Kualii lohe o Kualii ua pau na ’lii o Maui i Lanai, no
continued on his way to Lanai and landed at Wailehua. a pae i Wailehua. I nana aku auanei ka hana
Upon his arrival at this place Kualii saw a fleet of war mai ana na waa kaua o Lanai i Kekaa. A o K
canoes in Kekaa. Kamalalawalu at this time was on Lanai kela me kona puali alii i Lanai e kali ana ia H
with his army waiting for the return of Haloalena when the alaila hoouka ke kaua. Aka, no ka lohe ana o
fight would commence. When Haloalena heard that Kualii ana o Kualii i keia kaua ana, nolaila i kali ai n
was on his way to this war he decided to wait with his fleet Kekaa. I kekahi la ae, kui aku la ka lono o Ku
of war canoes at Kekaa. On the next day the news of noho ma Wailehua; ia manawa no ke kii ana
Kualii’s arrival at Wailehua was carried to Haloalena. Kualii e lawe e kaua aku ia Kamalalawalu.
Immediately upon hearing this he started off to meet Kualii
and entreat him to take up his cause and fight
Kamalalawalu.

That night Kualii and the chiefs of Lanai sailed under the Ia po iho holo aku la o Kualii me ko Lanai ma
lee side of Kaena as directed by the people who were ka holo ana, e like me ke alakai a na kamaai
acquainted with the place. All that night until the next day hoomoana mua na waa o Kualii i kai o Mane
Kualii’s canoes were moored along the beach at Manele. Kamalalawalu elele, hoouna ia aku la oia e h
[In the meantime Kamalalawalu was still waiting for
Haloalena.] After a time Kamalalawalu grew anxious and Ma ia hele ana, ike aku la o Hinau e lana ma
sent for his messenger Hinau and instructed him to make ma i Manele, a i ka ike ana aku a Hinau, he m
a circuit of Lanai. When Hinau arrived at Manele he saw nolaila, hookokoke loa aku la o Hinau e ike le
Kualii’s fleet of canoes moored there, and according to aole i ike ia o Haloalena me Kualii, ma na ho
their appearance judged them to be war canoes. Upon Haloalena, a ma na waa hoi ka ike ana ia Ku
making this discovery Hinau drew closer with the intention
of ascertaining if they were Haloalena’s. He did not,
however, see Haloalena and Kualii, but by the paddlers he
recognized Haloalena’s canoes, and by the shape and
appearance of the others he was positive they belonged
to Kualii.

Upon making this last discovery Hinau returned to Nolaila hoi aku la o Hinau a hai aku la ia Kam
Kamalalawalu and informed him of what he had seen in ike ai, me ka i aku: “Holo aku nei au ma Mau
the following words: “I ran by way of Maunalei to Kaena aole au i ike iki i ke alii, hele hou mai au a hik
without seeing the king. From this last place I continued to au, he mau waa ke lana mai ana, he waa an
Manele and there I saw some canoes moored along the kaua. Alaila hele loa aku la au e ike pono, ao
beach which had the appearance of war canoes. Upon nona na waa, aka, o na hoewaa o ke alii ka’u
making this discovery I drew closer so as to ascertain me ko Haloalena mau hoewaa, a o kekahi m
their true character. I did not, however, see the chiefs who waa o Kualii, aole nae au i ike ia Kualii.”
owned the canoes, but I saw the king’s paddlers; they
appeared to me to be Haloalena’s men, and the other
canoes looked like those of Kualii. I did not, however, see
Kualii.”

When Kamalalawalu heard Hinau speak of Kualii, he A lohe o Kamalalawalu i ka olelo a Hinau no
immediately sent for some soldiers and ordered them to ae la o Kamalalawalu i kekahi mau koa, e kii
go and bring Kualii. When Kauhi heard the orders given to ana nae ka Kauhi i ka huaolelo kena no keka
the soldiers he thereupon set out and ran to Manele to puka aku la o Kauhi a holo aku la ma Manele
meet Kualii without receiving any orders from me kona kena ole ia aku e Kamalalawalu. Ak
Kamalalawalu to do so, but took it upon himself to be the ke kii e ia Kualii.
first person to bring Kualii. When Kauhi arrived at the
place where the canoes moored he first looked for Ia Kauhi i hiki aku ai ma kahi a Kualii ma e la
Haloalena’s canoes and upon ascertaining which canoes hekauia na waa iuka. Aka, o ua Kauhi nei, ia
were his, this mischievous son of Kauhiakama unfastened e hekau ana na waa, nana pono ae la ia, a ik
the rope that held Haloalena’s canoes [426]to the shore Haloalena, alaila wehe ae la ua keiki kolohe
and dropped it in the sea. At this time a strong breeze was ke kaula hekau o na waa o Haloalena a kiola
blowing and the canoes were carried out to sea, leaving pa ana nae ka makani ia manawa, ua hele lo
Kualii’s canoes by themselves at their mooring place. haalele mai la i ke kaulike pu ana me Kualii.
Kauhi next took up the rope which held Kualii’s canoes to
A o ko Kualii mau waa hoi, lawe ae la keia i k
the shore and pulling on it drew them toward him and
a hukihuki mai la i ke kaula hekau, a kau aku
when near he jumped aboard, approached Kualii and sat
Kualii, hele aku la ua o Kauhi, a noho iho la i
on his lap. By the action of the boy Kualii knew he was a
Ia wa, maopopo ae la ia Kualii he keiki koloh
mischievous fellow and therefore asked him: “Whose
aku oia: “Nawai ke kupu o oe?” Olelo aku la
mischievous son art thou?” Kauhi replied:
Kauhiakama.” Olelo hou o Kualii me ka ninau
“Kauhiakama’s.” Kualii again asked him: “Did Kauhiakama
no oe i olelo mai e hele mai a noho iluna o k
tell you to come and sit on my lap?” Kauhi replied: “Yes,
“Ae, nana no i olelo mai ia’u e noho iluna ou.
he told me to sit on your lap.”

Because of these positive replies made by Kauhi, Kualii A no keia olelo a Kauhi, manao ae la o Kuali
made up his mind to go to Kauhiakama and ask him pololei aku ia Kauhiakama. Alaila holo pu ak
directly on the matter. Kualii then set off with Kauhi on Kauhi, a hiki aku la i o Kamalalawalu, ninau a
their way to meet Kamalalawalu. Upon coming up to Kauhiakama: “Nau no anei keia keiki o Kauh
Kamalalawalu and his company, Kualii turned to Kauhiakama: “Ae, na’u ponoi.” Ninau hou ak
Kauhiakama and asked him: “Is this your son Kauhi?” i olelo aku, e hele ae e noho iluna o kuu uha
Kauhiakama replied: “Yes, my own son.” Kualii again “Aole au i olelo aku ia keiki wahahee, e hele
asked him: “Was it you who told him to come and sit on ke alii.” I mai la o Kualii: “Ka! I olelo ae nei, n
my lap?” Kauhiakama replied: “I did not tell that deceitful iluna o’u.” I aku o Kauhiakama: “E nani ke ke
boy to go and sit on your lap, O King.” Kualii remarked: na keiki kolohe.” Kii ia aku la o Kauhi, a hiki m
“He told me that you had told him to sit on my lap.” Kauhiakama kona makuakane, ninau ia aku
Kauhiakama then replied: “What a deceitful boy; send for oiaio anei ua olelo aku nei oe i ke alii (Kualii)
that mischievous boy.” Kauhi was then sent for and he hele e noho iluna o ka uha o ke alii?” I mai o
was brought in the presence of Kauhiakama his father aku la ka makuakane: “Nani ke keiki wahahe
and was then asked: “Say, Kauhi, is it true that you told ka’u olelo ana aku ia oe pela?”
the king (Kualii) that it was I that had instructed you to go
and sit on his lap?” Kauhi replied: “Yes, you told me to do
it.” The father then said: “You are indeed a deceitful boy.
When did I tell you to do such a thing?”

Kauhi then answered his father without fear: “Here is what I mai o Kauhi me ka makau ole i kona makua
you told me. While I was teasing the boys and was pulling ia’u. Ia’u e paeha ana i na kamalii, a e uhuki
up our newly planted fields till you had about enough of mahinaai a kaua, a ana oe i kuu kolohe, olelo
my mischievous capers, you then spoke to me in the ke ana ia oe e ke keiki i ke kolohe; e aho e h
following words: ‘At last I am sick and tired of your capers; kolohe ai, ilaila e ku ai kau kolohe.’ Pela mai
the best thing for you to do is to go and behave this way in i hele aku ai e kolohe ia Kualii.”
the presence of the king, there you can cut as much of
your capers as you like.’ These were your very words to
me, and that is the reason why I acted the way I did to the
king.”

Because Kauhi spoke the way he did to his father, Kualii A no keia olelo a Kauhi pela i kona makuaka
made up his mind that Kauhi had in him the makings of a o Kualii he kanaka koa o Kauhi, alaila, lawe a
brave soldier, and thereupon took him as one of his koa nona; a lilo ae la o Kauhi i pukaua nui no
soldiers. In course of time Kauhi proved to be what Kualii Maheleana a me Malanaihaehae.
had predicted of him and was made his chief warrior, even
over Maheleana and Malanaihaehae.

The battle prepared by Haloalena was declared off by Aka, o ke kaua i hoomakaukau mua ia e Hal
Kualii, and Lanai once more came under the rule of aku la o Kualii ia kaua ana, a hui hou ae la m
Kamalalawalu. Shortly after this, Kualii returned to Oahu A hoi aku la o Kualii i Oahu, lawe pu ae la ia
taking Kauhi along with him.

CHAPTER VIII. MOKUNA VIII.

THE BATTLE FOUGHT BY KUALII AT KE KAUA ANA A KUALII I


KALAKOA.

In most of the battles fought by Kualii it was customary for He mea mau i na hoouka kaua ana a pau a K
him to accompany his soldiers. But later on when Kualii me na koa. Aka, no ko Kualii ike ana aku i ko
saw that his soldiers were proficient and that they showed makaukau, a ikaika no hoi, nolaila, hookuu a
great strength he decided to let them go to war by ke kaua o kona mau koa wale. He nui na kau
themselves, while he stayed behind at Kailua. But kona mau koa, noho no nae oia ma Kailua. A
nevertheless, his soldiers usually told him the time and [429]na koa o Kualii ka hele aku e hai i ke alii
place the battles were to be fought, so as to keep the king ai ke kaua, a me ke kahua hoi kahi e hoouka
informed. This was the [428]practice regularly observed. alii. A pela mau no ka hana ana. Aka, hele a
Kualii, however, often went to witness these battles makaikai i ke kaua a kona mau koa, me kona
without the knowledge of his soldiers. In these secret nae o kona manawa e hele ana e nana i ke k
tours of his, he always took part in the battles against his oia i ke kanaka, a lawe mai i ka ahuula. Pela
enemies and carried away the feather cloaks. Kualii often hele ai i na kaua, aka, he mea haohao nae ia
went out to battle in this secret way and the soldiers were a hoomaka iho ka hoouka ana o na kaua o n
puzzled at certain things they saw which they were not o Kualii ma kela aoao kahi i luku aku ai i ke k
able to unravel. Every time an engagement occurred ia nei poe kaua. Aia a pau ka hoouka ana o
Kualii was there, fighting those who were opposed to his ka oili a keia kanaka me ka ahuula mailoko a
men. At the close of the battle the men would then see puka aku la no ia hele ana, hoi aku la i Kailua
some one come out of the conflict bearing a feather cloak
who would disappear on the way to Kailua. It was no one
else but Kualii.

After a while Kualii’s soldiers became very anxious to A no ka uluhua mau o na koa o ua o Kualii i
know who this person was that always came out from the nei me ka ahuula, nolaila manao ae la na ko
ranks of the enemy carrying a feather cloak on his arm. i ike ai lakou i keia kanaka koa e puka nei ma
So the soldiers made up their minds to seize him, so that kaua. Ua nui na hoouka kaua ana i hala i kom
they would be able to find out who this brave soldier was. ole ia. A nolaila, ua ninau wale iho kona mau
Several battles were fought after this where Kualii joined keia? Owai la?” Nolaila, kukakuka ae la na k
in without being recognized by his men, and the soldiers hana ia aku nona.
began to question amongst themselves: “Is it possible that
this is indeed Kualii? Who can it be?” The soldiers
therefore held a council to decide what must be done to
him.

One early morning just before dawn Kualii set out from I kekahi kakahiaka ma ka manawa e molehu
Kailua; leaving Kaneohe he went by sea and the sea was no o Kualii mai Kailua mai; a hiki ma Kaneoh
dried up. When Kualii arrived at Kahaluu that same ke kai, maloo ke kai. A hoea oia i Kahaluu, m
morning he was seen by a certain boy at Kualoa. The boy manawa ike mai la kekahi keiki i Kualoa, ma
resided at Kaoio Point. Upon seeing Kualii the boy noho ai. I aku la ua keiki nei i ke kupunawah
remarked to his grandmother: “Say, how swiftly that man kanaka e holo mai nei maloko o ke kai.” I aku
runs along the sea.” The grandmother replied: “Watch him “Nana pono ia aku, aole na he kanaka e; o k
closely; it cannot be anybody else; it must be the king, aku la ka moopuna: “Aia a hiki mai ke alii, ala
Ku.” The grandson then remarked: “When the king arrives mahope.” I aku ke kupunawahine: “A ina i ma
I am going to follow him.” The grandmother replied: “If you hanai, e paa aku oe i ka wahi opae me ka pe
are thinking of following your lord you must carry along hele kela a alawa iho mahope, malia o ike i k
these shrimps wrapped in ti-leaf together with the king’s oe, alaila hai aku oe. Mai hele hookokoke ak
fan. It is possible that the king may look behind him and iluna o ke alii, a mai hele oe ma ko ia la malu
see the fan and would like to know who you are; then aka o ke alii; hoomamao ike mai oe.”
make yourself known to him. Don’t go near him, however;
your shadow may pass over the king; and don’t go on his
lee side for you may step over the king’s shadow, but
keep at a little distance away from him.”

Just as the grandmother concluded her instructions Kualii Pau no hoi ka ke kupunawahine olelo ana, h
passed by. The boy then followed. Kualii kept on running o lakou nei. Ia manawa, ukali pu aku la ua ke
and passed Kaaawa, then along and over Makaua and as Kualii, a hala o Kaaawa, a ae iluna o na Mak
he was going up the rise from which place you can see e nana aku ai ia Kahana. I alawa iho auanei
Kahana, Kualii looked behind and saw a boy following ana keia keiki mahope o ia nei. I iho la ke ali
him. The king then remarked: “I see there is a boy mahope.” A no ka makemake ole o Kualii e u
following me.” As the king did not wish to be followed for auanei kana hele ana i ke kaua; nolaila, holo
fear that his intention of going to battle might be known, me ka manao o ke one o Kahana kahi e pau
he ran much faster with the idea that when they reached nei.
the sands of Kahana he would outrun the boy. When
Kualii reached the sands of Kahana he then ran at great
speed along the sea, with the boy close behind; when A hiki o Kualii i ke one o Kahana, holo mama
Kualii got on the other side of Kahana which adjoins kai, o ke keiki aku no mahope; a hiki o Kualii
Punaluu he looked around and saw the boy still close Kahana e pili aku ai me Punaluu, i alawa iho
behind him. The king then remarked to himself: “Surely kau aku ana no ke keiki mahope ona. Ia man
this boy is a fast runner.” Passing Punaluu, Kaluanui and ana o Kualii i kona mama, a hala o Punaluu,
up the summit of Kaipapau, the boy kept on following iluna o Kaipapau, i alawa mai auanei o Kuali
close behind till the king reached Waimea; Kualii keiki nei mahope. I iho la ke alii: “He oi ka ho
continued down the slope and sat down on the other side Pela ka uhai holo ana o ua keiki nei mahope
of the Waimea stream; but the boy remained on this side Waimea. Iho aku la o Kualii a ma kela aoao o
at a place called Piliaama where he sat down, as the sun keiki nei pili aku la ma keia aoao ma kahi i ol
had now risen. The boy wanted to get nearer to the king, malaila [431]oia i noho ai, no ka mea ua puka
but was afraid his shadow might pass over him, so he keiki nei e hookokoke aku i kahi a ke alii e no
concluded to stay where he was. [430] keia o ae ke aka o ua keiki nei iluna o ke alii,
keiki nei malaila.

While they were at Waimea, Kualii looked and saw that Ia laua me Kualii malaila, nana aku la o Kual
the boy was holding his fan; he then watched the boy to peahi o ua o Kualii e ua keiki nei; kali aku la
see if he would use it, but the boy did not, because he o ke keiki, aole oia i peapeahi, no ka mea ua
knew that the fan belonged to the king. Had the king seen ke alii ka peahi. Ina e ike aku o Kualii i ua ke
the boy use the fan the boy would have been killed. After ua peahi nei, ina ua make ua keiki nei. A liuli
waiting for a while the king called for the boy and the boy alaila, kahea aku la o Kualii i ke keiki, a hele
stood up and went over to meet the king. The king then alii. Ninau aku la ke alii: “Nawai i haawi mai i
asked him: “Who gave you that fan?” The boy answered: la ua keiki nei: “Na ko kahu no.” Ninau mai la
“Your honored servant.” Kualii again asked the boy: hele ana oe i hea?” I aku la ke keiki: “I ukali m
“Where are you going to?” The boy replied: “I am following hou aku ke alii: “Ina holo au a hopu i ka ahuu
the king.” The king again asked him: “If I should run and la ke keiki: “Hopu no au i ka ahuula.” I hou a
grab hold of a feather cloak, would you grab one too?” hopu au i ke kanaka, hopu no oe?” “Ae, hopu
The boy answered: “I would grab a feather cloak too.” keiki. A no keia mea, manao ae la o Kualii, h
Kualii again asked him: “If I should seize hold of a man,
would you seize one too?” “Yes, I would seize one too,”
replied the boy. After hearing the boy answer all his
questions, Kualii made up his mind that this must be a
very brave boy.

Upon their arrival at Lihue they heard that the two armies Ma ia hele ana a laua nei a hiki iuka o Lihue,
were encamped at Kalakoa, so they kept right on and hoomoana ke kaua i Kalakoa. A nolaila, hele
went into the battle. This is known as the battle of iloko o ke kaua, oia ke kaua i olelo ia o Kuka
Kukaniloko. When they drew close to the enemy, Kualii hookokoke aku ai, komo aku la o Kualii iloko
entered into the thickest part of the fight with the boy komo pu aku la no hoi me ua keiki nei.
behind him. Kualii, upon entering into the fight, left his
own men far behind him, but he and the boy kept on with A hala na koa ponoi o Kualii mahope o laua,
the desire of again encountering the enemy at Paia where ke kaua a Paia. Ike aku la o Kualii i ke alii e a
another battle was being fought. Upon reaching Paia, ahuula, hopu aku la o Kualii i ka ahuula a law
Kualii saw the opposing king dressed in a feather cloak. lawe mai ai i ka ahuula, hopu aku la no hoi u
Kualii then drew near to the other king and after killing him manamana lima iki a lawe mai la, lalau aku la
seized the feather cloak and took it. While Kualii was kekahi pepeiao o ua kanaka nei no nona ka
carrying off the feather cloak the boy cut off one of the
man’s small fingers and took it. The boy also cut off one of
the man’s ears and took it.
After getting the feather cloak Kualii returned with the idea Hoi mai la o Kualii me ka manao aole e hiki m
that the boy would not be able to follow him out of the hoi ana o Kualii me ka manao oia wale no ke
fight. While Kualii was on his way to Kailua with the idea aka, i alawa ae ka hana o Kualii i hope, e he
that he was all by himself, he thought he would look mahope ona. Nolaila, kali iho la ua o Kualii a
behind him; when he did, he saw to his surprise that the hiki ana mai, ninau aku la ke keiki: “Pehea oe
boy was still behind him. When Kualii saw the boy mau no.” Ninau aku la hoi o Kualii; “Auhea h
following he stopped and waited for the boy to come up to la ke keiki: “Ia oe no i lawe mai ai i ka ahuula
him. When the boy got up to him, the boy asked him: manamana lima iki me kekahi pepeiao.”
“How are you?” Kualii replied: “Just as usual.” Kualii then
asked the boy: “Where is your man?” The boy replied:
“When you took the feather cloak, I took the small finger
and one of his ears.”

When the boy made this answer, Kualii made up his mind A no keia olelo a ke keiki, manao ae la o Kua
that this must be a brave lad. They then resumed their Nolaila, hoi aku la laua a hiki ma ka lae o Ka
journey until they reached Kaoio Point at Kualoa, where la i ka malo i kona kahu. A haawi lilo ia mai u
the king asked his servant for his malo. Upon receiving it keiki, a hoahume pono aku la no o Kualii i ka
he gave it to the boy to be his own, and he fastened it to hoi aku la laua a hiki ma Kailua, Koolaupoko
the boy with his own hands. 321 They then returned to ai ma ka hale, hoonoho iho la o Kualii i ua ke
Kailua in Koolaupoko. noho oe maanei, e hele au imua, aia kani ma
okoa kou mea nana e kii mai.” Alaila, hoi aku
While they were approaching near the houses, Kualii told aku la imua, a mahope kani ana ka pahu. Kii
the boy to stay where he was. “You stay here while I go [433]
on ahead to the mua. 322 When you hear the beating of the
drum, then someone will come and bring you along.” With
these words Kualii went on and entered the mua. Soon
after this the boy heard the beating of the drum and saw
someone coming for him. [432]

CHAPTER IX. MOKUNA IX.

SUPPLEMENTARY. HE PAKUI.

The Royal Kolowalu Statute. 323—This was the best law O ke Kanawai Niaupio Kolowalu. O ke kanaw
during the reign of Kualii Kuniakea loa i ke au o ka noho aupuni ana o Kualii Ku
Kuikealaikauaokalani. 324 It was strict, unvarying and Kuikealaikauaokalani, he paa, he luli ole he o
always just. It was for the care and preservation of life; it pomaikai, o ka hele o ka elemakule ame ka l
was for the aged men and women to lie down in the road o ka kokua i ka poe mahiai ame ka poe lawa
with safety; it was to help the husbandmen and the poe malihini, o ka hanai i ka poe pololi i ka a
fishermen; to entertain (morally) strangers, and feed the kanaka he pololi au i ka ai, e hanai aku i ka a
hungry with food. If a man says, “I am hungry for food,” mai, a hoohiki mai i ke kanawai ma kona wa
feed [him] with food, lest he hungers and claims his rights laa kela ai ma ke kanawai, aole e hiki i ka me
by swearing the kolowalu law by his mouth, whereby that ua lilo ma ke kanawai, o ka uku ka pono. E m
food becomes free, so that the owner thereof cannot nana e hoohiki i ke kanawai o pili ia ia ke kan
withhold it; it is forfeited by law. It is better to compensate. ke kanawai o ka Moi me ka hewa ole, aia ma
He who swears must observe the law faithfully, lest he be hoopai. Ina he makaha wale i ka hai ai, a i ka
accountable to the law of the king which he has sworn to maluna o ka mea nana i lawe wale i ke kana
observe, 325 and the punishment be upon him. If it is kaumaha. O ke kanaka lawelawe a he kanak
simple robbery of others’ food, or of others’ property, then kauia e keia kanawai, ua hookuuia oia mai k
severe punishment shall be meted out to the person who lawehala hoi. O ka pololei o kona kanawai am
violated the law. A transgressor, 326 or one who is about to malama ana i ke aupuni, ua malama mai ke
die, is, under the application of this law exonerated of his kona ola ana, a nona ke ola kaulana ma ka m
death or other penalty. Through the uprightness of his kahiko. No ka Moi alii o Oahu, ua ola oia i na
[Kualii’s] law, and the honesty with which he administered me umikumalima makahiki. Ua hele a kolopu
the government, God preserved him, so that he lived a haumakaiole, a palalauhala, a kauikapuanea
long life, and his is that notable life spoken of in the aumaka make oia ma Kailua i Koolaupoko i k
annals of the ancient people, of the king of Oahu, who mau makahiki o ke ola ia. Ua ana he 175.
lived four times forty and fifteen years. In the last stage of
life he was bent with age and withered, with the eyes
reddened and bedimmed; and was carried about in a
netting. He died at Kailua, in Koolaupoko, in a.d. 1730, in
the one hundred and seventy-fifth year of his life.

Kualii is thus shown to have lived to an extremely old age,


and to have possessed unusual strength and vigor
throughout. Fornander, in his Polynesian Race, Vol. II,
pages 283–4, furnishes the following additional legendary
data and characteristic final of this eminent worthy:

“It is related that when Kualii was upwards of ninety years


old, Peleioholani arrived one time from Kauai on a visit to
his father on Oahu. Without endorsing the details of the
legend, it suffices to say that a quarrel arose between
father and son; that the latter assaulted the former, and a
scuffle ensued in which the old man, getting the grip of the
lua 327 on his son, handled him so severely that, when
released from the paternal grasp, he started at once for
Kauai, and never revisited Oahu until after his father’s
death.

“Kailua, in Koolaupoko, seems to have been the favorite


residence of Kualii, and there he died at a very advanced
age. Shortly before his death he called his trustiest kahu
and friend to his side and strictly enjoined upon him the
duty of hiding his bones [434]after death, so that mortal
man should never get access to them or be able to
desecrate them. When Kualii was dead, and the body,
according to custom, had been dissected and the flesh
burned, the kahu carefully wrapped the bones up in a
bundle and started off, as everybody thought, to hide
them in some cave, or sink them in the ocean. Instead of
which, he repaired to a lonely spot and there pounded up

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