Department of Public Health Science

Health Systems and Policy Research group

Centre for Research on Health Care in Disasters
Erasmus Mundus Master program Public Health in Disasters
Degree Project, 20 Credits

Risk Factors for Leptospirosis in Urban Flooding

A Literature Review

Author:
Melanie Mann

First Supervisor:
Johan von Schreeb
Department of Public Health Sciences, Karolinska Institutet, Stockholm

Co-Supervisor:
Roy Nobhojit
Tata Institute of Social Sciences, Mumbai

Examiner:
Kim Brolin
Department of Public Health Sciences, Karolinska Institutet, Stockholm

Date of Submission:
June 16th, 2015
 Declaration

Hereby I, Melanie Mann declare that this thesis entitled

Risk Factors for Leptospirosis in Urban Flooding
is my own work.

All sources of information reported by others are indicated in the list of references in accordance
with the guidelines.

Melanie Mann
Signature: _________________________________________________________
(Students signature)

Total word count: 12742

I, ___________________________________________approve this thesis for submission.

(Supervisors signature)

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 Content
Abstract................................................................................................................................................4
Abbreviation........................................................................................................................................5

1. Background......................................................................................................................................6
1.1 Leptospirosis Overview.................................................................................................................6
1.1.1 Manifestation.....................................................................................................................6
1.1.2 Transmission......................................................................................................................7
1.1.3 Diagnosis...........................................................................................................................7
1.1.4 Treatment...........................................................................................................................8
1.2. Leptospirosis and Flooding..........................................................................................................9
1.3 Leptospirosis and Rapid Urbanization........................................................................................10

2. Aim and Objectives........................................................................................................................11

3. Methods.........................................................................................................................................12
3.1 Design............................................................................................................................12
3.2 Search............................................................................................................................12
3.3 Eligibility Criteria..........................................................................................................12
3.4 Study Selection..............................................................................................................13
3.5 Study Characteristics.....................................................................................................14
3.6 Synthesis of Results.......................................................................................................15

4. Results............................................................................................................................................15
4.1 Environmental Factors...................................................................................................16
4.2 Human Factors...............................................................................................................20
4.3 Socio-Economic Factors................................................................................................22

5. Discussion......................................................................................................................................25
6. Limitations.....................................................................................................................................32
7. Recommendations for Future Work...............................................................................................33
8. Conclusion.....................................................................................................................................35

9. Acknowledgements........................................................................................................................37
10. References....................................................................................................................................38
11. Appendix......................................................................................................................................43

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Risk Factors for Leptospirosis in Urban Flooding
A Literature Review

Abstract
Aims

This literature review aims to explore main risk factors that favor contracting leptospirosis in the
event of urban flooding.

Methods

A extensive literature search, with set inclusion and exclusion criteria was conducted. Findings from
a final selection of 18 papers were analyzed, grouped and compared in detail using the PRISMA
protocol for systematic literature reviews.

Results & Discussion

Risk factors for leptospirosis in urban flooding can be divided into environmental, human and socio-
economic risk factors. Statistical significant factors include proximity of household to contaminated
water, contact with host or contaminated water, presence of inadequate drainage system, poor refuse
management, lack of protective clothing as well as poverty. Validity and reliability of these findings
are limited due to random as well as systematic error in several studies. Small sample size and re-
sponse bias were the main influencing factors for such error.

Conclusion

More region specific quality research is needed to fully understand the complex epideminology of
leptospirosis. Improved water, sewer and sanitation systems, investment in health promotion and
waste management as well as eradication of poverty might not only reduce leptospirosis during urban
flooding but also prevent morbidity and mortality from other water- and vector-borne diseases. Risk
factors highlighted in this review have the potential to support future guidelines for diagnosis and act
as epidemiological determinants for leptospirosis infection for health service provider. GIS and other
modelling approaches are promising future methods to identify risk zones that point to the source of
infections such as leptospirosis during urban flooding.

Keywords:
Leptospirosis, Flood, Slum, Risk Factor, Urban

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 Abbreviations

ARF Acute Renal Failure

BMC Bombay Multiprincipal Corporation
CI Confident Interval
DFY Doctors For You
ELISA Enzyme Linked Immunosorbent Assay
GIS Geographic Information System
ICU Intensive Care Unit
IgM Immunoglobulin M
LIC Low Income Country
MAT Miller Analogies Test
MCAT Micros-capsule Agglutination Test
MCGM Municipal Corporation of Greater Mumbai
NGO Non-Governmental Organization
NTD Neglected Tropical Diseases
OR Odds Ratio
P P-Value
PPP Purchasing Power Parity
PRISMA Preferred Reporting Items for Systematic Reviews and Meta-Analyses
PSD Preliminary Situation Definition
UNICEF United Nations International Children Emergency Fund
WHO World Health Organization

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 1. Background
1.1 Leptospirosis Overview

Leptospirosis also known as seven-day fever and cane cutters disease is an infectious zoonotic
disease caused by the pathogenic bacteria leptospires resulting in acute febrile illness (4).
Leptospirosis occurs worldwide but has most commonly been reported in tropical and subtropical
regions with hot and humid climate conditions as well as in relation to high levels of rainfall and
seasonal flooding (5-11). Animals such as rats and canine seem to be the major host for this disease
(12). The bacteria is found in and spread by animal urine (5). Direct transmission from animal to
human is rare whereas indirect transmission through infected water and soil is common as leptospires
bacteria can live for a long time in damp and moist reservoirs (13). Once leptospires have entered the
body and have caused infection, case fatality can range from >5% to 30%. For the majority of cases
lower estimates are common. Only a small number of cases (515%) develop Weils disease which is
the severe form of leptospirosis (14). Weils disease is associated with major complications and case
fatality can reach up to 40% (12). When looking at the worldwide occurrence of leptospirosis,
currently available reports estimate incidences to range from 1/100.000 per year in temperate
climates to 10-100/100.000 per year in humid climates. During outbreaks incidences can reach over
100/100.000 per year (15). Although in many areas of the world leptospirosis has been described as
endemic as well as has been recognized as a common disaster-related infection (16) occurrence of
the disease yet is not well documented, meaning that the number of human cases worldwide is not
known precisely.

1.1.1 Clinical Manifestation

There are over 200 pathogenic leptospirosis strains which make clinical manifestation highly
variable. Some strains generally tend to cause mild disease, while others severe disease. However,
there are no strain-specific presentations of infection and any strain may cause mild or severe disease
in different hosts. It can be differentiated between anicteric leptospirosis and icteric leptospirosis.
After an incubation period of 2-21 days, the onset of anicteric leptospirosis is abrupt and is
characterized by mild influenza like symptoms such as fever, headache, severe myalgia and chills
with rigors, (4, 5, 15, 17). The symptoms are prominent for 4 to 7 days during the first stage called
septicemic phase. The second stage (immune phase) of anicteric leptospirosis is preceded by a one

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to three-day asymptomatic period and coincides with
Leptospirosis Case Definition
the appearance of IgM antibodies. After that, the
second stage lasts from 4 to 30 days and is A suspected leptospirosis case involves
a person presenting with acute febrile
accompanied by reoccurring fever. Mild aseptic illness; headache, myalgia and prostra-
meningitis is very common during this stage until the tion; associated with any of the follow-
ing symptoms: conjunctival suffusion;
leptospires are cleared from the blood (4, 17). Icteric meningeal irritation; anuria, oliguria,
leptospirosis also called Weils syndrome is the more or proteinuria; jaundice; hemorrhage
(from intestines; lung bleeding often no-
severe form of disease and characterized by symptoms torious); cardiac arrhythmia or failure;
such as hepatic, renal and vascular dysfunction. Even skin rash; a history of exposure to in-
fected animals or an environment con-
though clinical manifestations vary in terms of severity taminated with infected animal urine.
and symptomatology, Weils syndrome likewise
(World Health Organization 2010)
anicteric leptospirosis is bi-phasic and similar
symptoms such as fever, jaundice and azotemia have been reported. Fever appears in the first phase
whereas azotemia, oliguria and anuria commonly occur during the second stage of illness (4).
Although only a small proportion of patients diagnosed with leptospirosis develop Weils disease, in
about 16%-40% of the cases it causes acute renal failure (ARF) if not treated (5, 17). Clinically as
well as epidemiological leptospirosis mimics other diseases such as dengue, typhoid, tuberculosis,
influenza, pneumonia, encephalitis, typhus fever, poliomyelitis, rickettsiosis, glandular fever,
brucellosis, malaria, viral hepatitis as well as hantavirus infections (17-20). Due, to an overlap of
many neglected tropical diseases (NTDs) unrecognized co-infections often occur which in turn
creates a multiple burden of disease for the population in those regions where tropical diseases are
prevalent (21).

1.1.2 Transmission
Leptospirosis is usually transmitted through abrasions or cuts in the skin or via mucus membranes
(17). More specifically, the bacteria is presumed to enter directly into the bloodstream or lymphatic
system via the conjunctiva or the nasopharyngeal mucosa. It is believed that transmission when drink-
ing or inhalation of contaminated water following immersion is also possible (4, 14). Infection rarely
follow animal bites. Direct transmission between humans is very uncommon and has only been found
in relation to sexual intercourse (12) and through giving breast milk to infants or children (17).

1.1.3 Diagnosis
To date no easy to perform or accurate diagnostic tool to detect leptospirosis has been developed
(22). Together with a current limited understanding of the mechanisms of parthenogenesis and the

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fact that leptospirosis mimics many other diseases, this leads to many cases being misdiagnosed
and/or undiagnosed (15, 17, 23). For patients developing severe leptospirosis, prediction of disease
severity at the onset of the illness based on clinical features alone is almost impossible. Even though
several promising approaches to rapid diagnosis have been developed, laboratory blood test are often
essential in order to make full diagnosis (17). Miller Analogies Test (MAT) is regarded as gold
standard for diagnosis but also requires technical expertise and maintenance of multiple live serovars
(15). In many settings where leptospirosis is endemic resources for such tests are extremely limited
and often unavailable to populations most at risk of contracting leptospirosis (24, 25). Because of
this, clinicians not only use less accurate tools but also often solely rely on their clinical judgment
which in turn might result in under-diagnosis of infection as presentations may overlap as infection
progresses and co-infections may exist. These factors make clinical diagnosis particularly in the
tropics and sub-tropics difficult, where co-infections such as dengue and other hemorrhagic fevers
are common (15, 23). Shortcomings regarding diagnosis as well as adequate monitoring of disease,
serve as a threat to underestimation as well as overestimation of the real risk connected with the
spread of infections caused by leptospira (5). As prompt diagnosis and early initiation of antibiotic
therapy are essential for preventing disease progression, diagnostic focus in recent years has not only
relied on the potential bio markers that could serve as early warnings for severe disease (23) but also
on public health determinants and risk factors that might increase the possibility of contracting
leptospirosis (12).

1.1.4 Treatment
Leptospirosis is a potentially serious but treatable disease. Mild versions of leptospirosis are mostly
treated with oral antibiotics such as amoxicillin, ampicillin, doxycycline or erythromycin (12)
whereas intravenous penicillin (6 million IU/day for 8 days) is the gold standard treatment for the
severe form of leptospirosis (4, 26). Although vaccinations have been developed in countries such as
China, France and Cuba (27), they are not widely used due to the serovar-specificy of leptospirosis
(17). Doxycycline which is used in high risk and endemic regions for short-term chemo-prophylaxis
(4) cannot prevent leptospirosis but may be valuable for reduction of morbidity and mortality during
outbreaks (26). Although antibiotic treatment does not reverse tissue and organ damage, early
administration of intravenous penicillin has been shown to reduce mortality and the duration of
illness in severe leptospirosis cases (4). In most cases where leptospirosis is suspected, early
antibiotic therapy is initiated without confirmed diagnosis, adding to the problem of under-reporting
(17).

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Leptospirosis has been described as a worldwide public health problem, and has also been directly
related to events of flooding (5-11) as well as indirectly to urbanization and slum dwellings (18, 28).
The magnitude of the problem in tropical and subtropical regions has been largely attributed to cli-
matic and environmental conditions but also to the great likelihood of contact with a leptospira con-
taminated environment caused by, for example, flooding, local agricultural practices and poor hous-
ing, water, sanitation and waste disposal, all of which give rise to many sources of infection (28).
Such conditions are predominantly found in low income countries and informal settlements and
therefore need significant attention (10).

1.2 Leptospirosis and Flooding

With floods being the most common type of global disaster (18), responsible for almost half of all
victims of natural disasters and for economic losses of nearly US $ 50 billion a year (29), they serve
not only as a threat to property and infrastructures but also to human health (23, 29). Flooding events
are expected to increase in frequency and intensity due to climatic changes such as rising sea levels,
elevation in subsurface water and more frequent and extreme precipitation events (18, 30). Together
with predicted increases in temperatures and humidity, outbreaks of water-borne diseases are antici-
pated to increase in frequency and intensity and so a higher health burden of infectious diseases from
floods can be expected in the near future (2, 23). Tropical as well as sub-tropical regions are expected
to be predominantly affected by such adverse climate changes (18). Environmental drivers such as
floods, monsoons as well as typhoons not only disrupt infrastructure and public health services they
also cause increased exposure to animal hosts and to precarious situations of lack of clean water and
basic sanitation (18, 23, 28), consequently increasing the risk of the spread of diseases, the occurrence
of outbreaks (10, 18, 23) and urban epidemics (10, 31, 32), including leptospirosis (5-9). Several
studies have found that leptospirosis incidences increase between two and eight-fold as a result of
flooding (18, 33, 34) which demonstrates the clear link between leptospirosis incidences and flooding
(10, 23). (18) Numerous outbreaks of leptospirosis have been reported following extreme weather
events, in geographically diverse areas around the world (10-21). Highly populated areas with sub-
optimal drainage (i.e. urban slums) and low-lying areas have been found to be most at risk (10).
Natural hazards, such as flooding are proven to cause the greatest harm in combination with existing
problems and vulnerability factors such as overpopulation, demographic imbalance, poor govern-
ance, endemic poverty, and lack of infrastructure (18, 23). Many tropical regions that are most vul-
nerable to flooding also host the majority of the most vulnerable populations (18). Thus in recent
years the importance of preventative measures with regards to risk reduction has been highlighted,

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suggesting that through systematic efforts to analyze and manage the causal factors of the hazard, the
severity of a disaster can tremendously be reduced (35).

1.3 Leptospirosis and Rapid Urbanization

Rapid urbanization and urban poverty have led to the dramatic growth of slum settlements throughout
low and middle-income countries in the last few years (10) creating an important determinant for the
emerge of zoonotic diseases such as leptospirosis (21). Although in the past studies looking at lepto-
spirosis focused mainly on occurrence in populations working in occupations that favor contact with
contaminated soil or water in rural areas (10) recent studies have indicated that leptospirosis cases
equally seem to cluster in urbanized areas, particularly slum settlements (6, 36, 37). It is estimated
that presently close to one billion (14%) of the world's population live in slum areas and that this
population continues to expand at rates of 10% per year, reaching a total of 20% of the worlds
population by 2020 (18, 38). This accounts for 33% of the total urban population living in low and
middle income countries. Typically, urban slums are densely populated informal settlements with
high rates of poverty and inadequate access to health services, education, water, and sanitation facil-
ities (39). Overcrowding, open sewers and accumulated refuse create the ideal breeding grounds for
disease transmission and clustering of disease due to vectors including mosquitoes, flies, rodents,
and dogs (21, 36, 40). Moreover one-half of the urban population in developing countries currently
lack piped water, waste collection, paved roads, Vulnerability
sewers and storm water drains (41). Such environ-
Vulnerability can be defined as the
ments are highly vulnerable to floods, and other diminished capacity of an individual, group
disaster, making associated water-borne diseases or community to anticipate, cope with, resist
and recover from the impact of a natural or
such as leptospirosis a concern not only during man-made hazard(UNISDR 2009)
rainy season (10, 18, 36). It has been estimated that
Factors that influence such capacities
urbanization can potentially magnify flooding in- include physical, social, economic and
tensity by ten-fold (6). Thus with the increasing risk psychological characteristics and
circumstances. Such define the level of
of flooding and continuing urbanization in devel- resilience and ability of people to recover
oping countries, these areas are believed to experi- from a hazard (1). Vulnerability which is
associated with socio-economic factors, in
ence an upsurge in the scale and severity of lepto- combination with potential hazards, such as
spirosis epidemics. Such trends are further magni- flooding create a level of risk; a probability
of developing disease (2).
fied due to high levels of vulnerability among slum
inhabitants. Poor coping capacity to mitigate the hazard increase their vulnerability to diseases, in-
cluding infection from leptospires (18).

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In order to allow a comprehensive public health response to urban leptospirosis cases and outbreaks
during flooding, non-biomedical factors that increase exposure and lead to epidemic transmission of
disease need to be understood (12, 36, 42). Only then can mitigation capacities of an individual as
well as community be determined and prevention, surveillance and mitigation strategies can be de-
veloped in the future (38, 39). At present, several studies looking at clinical manifestation and sero-

Risk Factors prevalence of leptospirosis have been carried out, but very few
efforts have been made to identify underpinning public health
Risk Factors are any attribute,
characteristic or exposure of an determinants and risk factors, which are ought to give insight
individual that increases the in identifying and understanding the factors responsible for
likelihood of developing a dis-
ease or injury transmission of the disease (24, 38). A first step therefore will
be to analyze the results of leptospirosis risk factors found in
(World Health Organization 2015)
previous literature and studies. Information from these studies
might help identify areas specific to leptospirosis transmission, highlight gaps in study design and
execution as well as might point to priority needs of the population at risk particularly in relation to
urban flooding (43). To be able to arrive at a reasonable and defensible decision from the scientific
information already presented, a literature will be performed that explores the main risk factors that
favor leptospirosis infection in the event of urban flooding.

2. Aims & Objectives

Aim: To explore main risk factors that favor contracting leptospirosis in

the event of urban flooding

Objectives:
1. To systematically review literature that explores risk factors that favor contracting
leptospirosis in urban flooding
2. To distinguish, group and list risk factors that favor contracting leptospirosis in an event of
urban flooding.
3. To discuss gaps in the literature and explore measures that have been take and/or should be
taken to reduce exposure to risk factors that favor contracting leptospirosis in urban flooding.

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 3. Methods
3.1 Design

To facilitate understanding and appraisal of the review methods, as well as the detection of
modifications to methods and allow transparency of the process, the PRISMA protocol was used
(44).

3.2 Search

A comprehensive literature search including databases of Science Direct, SCOPUS, PubMed, Web
of Science, EBSCO, Research Gate and Primo Central was performed for relevant articles. The
search was tailored to keywords such as leptospirosis OR leptospira OR leptospires in title or
abstract AND risk factor* AND flood* in all fields. Bibliographies of cited literature as well as
gray literature were also searched.

3.3 Eligibility Criteria

Papers included in this literature review were restricted to studies:

published in English and German within the last 20 years (1995 2015)
providing information on risk factors
reporting on leptospirosis in humans only
conducted in urban setting
following or during flooding events

The search was not restricted to any particular study design to allow for a thorough investigation of
the subject. As the research topic choose has not received much attention yet and only a limited
number of studies have been conducted, including all study designs also ensured that a substantial
amount of valid studies were included in the review. Papers dealing with human leptospirosis, that
were specifically investigating clinical manifestations and symptoms that are associated with
leptospirosis were excluded from the literature review but included as information source for the
background and discussion section. Papers that were not able to be retrieved in full or were double
entries were also not included. The majority of the papers that had to be excluded after the initial
database search were studies of leptospirosis infections found predominantly in canine but also
included studies on goats, sheep, pigs, sea lions, deer, and rats. Such accounted for almost half of all
the studies found in the initial search.
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 3.4 Study Selection

There were 387 studies in the original search after the application of the exclusion criteria. These
studies were predominantly found in databases of Science Direct and SCOPUS. In order to filter
articles further all title and abstracts were read through independently by the author, and relevant
papers were identified to determine the relevance to the research topic. After the initial search, a total
of 52 full papers were read. Such contained cohort, cross sectional, ecological, and case-control
studies as well as literature reviews and non-randomized controlled trials. These sources were
screened for a well described methodology, which should address the research question stated and
allow the repeatability of the study. Further sources were screened for an adequate sample size and
an accurate statistical analysis which includes the presentation of OR, CI and P-values to indicate
significance, generalizability and transferability of findings.

One study on epidemiological risk factors of urban leptospirosis in North Chennai, India had to be
excluded from this review. Although environmental risk factors had been established, only a
summary of this work was available, no references were provided and the details of the study design
were unclear, leading to exclusion. Another study of leptospirosis in children following flooding in
an urban slum in Mumbai also was
not included. This hospital - based
Peer-Reviewd Did not meet
prospective study lacked a detailed Papers (from Inclusion Criteria:
study design and while looking at Database Search): 676
symptoms of children infected by 1063
leptospirosis it did not explore
related risk factors and so did not fit
the inclusion criteria. The same was Potential Excluded due to
found for one study conducted in appropriate studies Selection Criteria:
Guyana which investigated an
(Abstract read): 387 335
outbreak following flooding by
studying hospital register. This
study served as good background
information but was not included in Studies read in full: Key Studies included
52 in Final Review: 18
the paper analysis as it did not
explore underlying risk factors of
the outbreak.

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 3.5 Study Characteristics

Out of the 52 articles screened in depth 23 were directly or indirectly related to flooding (monsoon,
or heavy rain season) whereas 9 did not present any correlation to flooding. 20 out of the 52 did not
provide any findings regarding risk factors in relation to flooding or outbreak of leptospirosis and so
were solely used as background information and/or source for additional considerations in relation
to leptospirosis. The final selected peer-reviewed articles fulfilling all inclusion criteria were 18
papers. More than 50% of the papers reviewed where published in the last four years and provide
recent data.

Chart 1 presents the different study designs represented in the final selected papers which were used
for this review. Case-control (39%) and cohort study (17%) designs were the main study designs
represented in the different articles, whereas 11% applied a cross-sectional design. Only one study
was a clinical non-randomized controlled trial and one ecological study respectively. Literature
reviews were represented with 4 articles (22%) and often included studies which were included in
this paper. 21 was the mean number of studies included in in the literature reviews that were reviewed
in relation to leptospirosis in urban flooding and so is slightly higher than the number of studies
included in this review. The majority of studies included in this paper were conducted in Central and
South America (55,6%), 40% were in Brazil. The rest of the studies were found to be conducted in
India (16,7%) as well as South East Asia and Asian Pacific region (22,2%) including Australia. More

Chart 1: Study Design Distribution

5,5% Non-RCT
17%
22% Literature Review
5,5%
Cross-Sectional
Case-Control
11%
Ecological
39%
Cohort

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than one third (38,9%) of the 18 studies included were conducted in 2014 and no study was older
than 15 years. A detailed summary showing characteristics and findings in relation to risk factors of
each study included in this review can be found in Appendix 11.1.

3.6 Synthesis of Results

To analyze all articles and studies included after the final selection, the PRISMA protocol was used
(see Appendix 11.2). This protocol provides an extensive checklist for evaluating the quality and
rigor of studies and so allows for a systematic literature review and meta-analysis. Checklist items
that were provided in this protocol were used to analyze and value the different research sections in
each study. Studies were first screened for their quality and eligibility, checking for a clearly defined
hypothesis and appropriate methodology and research design that is able to answer the research ques-
tion. Further the sampling as well as data collection process was tested for its appropriateness by
looking at possible ethical issues or biases that were encountered. Statistical significance of findings
were analyzed by looking at effect estimates, confidence intervals, odds ratios and P-values. Findings
from such efforts were compared across studies to be able to draw conclusion on which studies might
offer most valid data in relation to leptospirosis in urban flooding.

In order to organize the literature review, similarities of studies were grouped by themes and
differences were highlighted and discussed. Such themes were environmental factors, human factors
and socio-economic factors. Under such themes information was grouped by similarity of variables.
This method was used as it has been proven to be most effective in highlighting findings in relation
to the chosen research topic as well as points out strength and weaknesses of each study (45).

4. Results

Results presented in this paper are grouped into themes of environmental, human and socio-economic
factors. Whereas environmental risk factors explain physical factors favoring contracting
leptospirosis in peoples direct surroundings, human factors refer to personal risk behavior within a
study sample. Socio-economic factors, sometimes grouped under environmental factors, include
occupational factors, income as well as education level. Environmental, human as well as socio-
economic factors are often tightly interlinked and influence each other in a community or among a
sample. Understanding the risk factors, within and between these themes, might be important to
facilitate disease prevention and health promotion measures (24).

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 4.1 Environmental Risk Factors

Environmental factors in the context of this paper are defined by all physical, chemical, and
biological factors external to a person that can potentially affect health (46). According to the World
Health Organization (WHO) (47) environmental factors such as inadequate water supply, excreta
disposal facilities, sanitation facilities, poor hygiene, food storage and consumption as well as the
climate, influence the spread of communicable diseases that are likely to cause epidemics.
Particularly the household environment is believed to be an important transmission determinant in
the urban slum settings (2, 36).

One of the main environmental risk factor associated with leptospira infection risk has been found to
be the proximity of residence to open sewers (6, 10, 38, 48). Felzemburgh et al found association
with an odds ratio (OR) of 21.6 and confident interval (CI) between 7.831.1 for distance of residence
to an open sewer (m) and primary infection (10). Likewise Sarkar et al (48), although not presenting
any P-values, reported matched OR of 5.15, 95% and CI ranging from 1.8014.74 and described
proximity to open sewer as an independent and strongest factor associated with illness. Reis et al who
had similar findings found that, infection risk increased as distances from an open sewer or refuse
deposit decreased, suggesting that households which are situated closer to these foci have a higher
degree of environmental contamination with leptospira (6). Such result is further supported by
Kamath et al who found in a recent study conducted in India that the presence of drainage within
15m radius of the home was statistically significant for an increased risk of leptospirosis (P=0,02)
(38).

Four studies included in this review found that in addition to deficiencies such as presence of open
sewers near the household, the presence of rats in close proximity to individuals and or the household
were independent risk factors for both mild and severe leptospirosis infection (6, 38, 48, 49). Sighting
rats was the major independent risk factor in three studies. In a study from Reis et al, subjects who
reported sighting two or more rats in the household environment had increased risk of acquiring
leptospira antibodies (6). A significant association was also found in the study by Bhardwaj et al
indicating leptospirosis being associated to sighting rats at home or at the workplace (OR = 4.95,
95% CI 1.53-16.05, P < 0.05). In the study by Bhardwaj et al the risk of occurrence of leptospirosis
was found to be 4.95 times higher among those who reported constant presence of rats in their
household compared to those who did not (49). Similar findings were reported by Sarkar et al. In this

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study a higher proportion of cases reported sighting five or more rats compared with control subjects
(41% versus 18%; OR = 4.49, 95% CI = 1.57-12.83) (48). Although sighting five or more rats was
an independent risk factors for leptospirosis on the one hand, reported contact with rats or other
potential reservoirs, including mice and dogs on the other hand was not observed to be significantly
associated with disease acquisition (48). Similarly non-significance with regard to proximity to
domestic animals or contact with domestic animals was found in Indonesia (24). However, this is
contrasted by the results from Keenan et al who in a study conducted in Jamaica in 2010 found that
cases were significantly more likely than controls to have contact with rodents (OR = 3.52 (95% CI
= 1.339.36, P = 0.01) (50). Controls in this study were individuals without reported clinical
leptospirosis, who resided in the same neighborhood as a case during the study period. Controls were
matched (1:n) to cases on neighborhood and age (10 years). Case definitions for cases varied
between suspected cases and confirmed cases. Suspected cases were defined as any person that
presented fever and had any one of the following symptoms: myalgia, conjunctival suffusion, anuria
or oliguria and/or proteinuria, jaundice, hemorrhages with a history of exposure to flood water or
mud. Confirmed cases were defined as suspected case of leptospirosis with paired sera samples
showing positive results (ELISA IgM titer value > 20 IU) (49, 50). In the study by Maciel et al as
well as Vanasco et al cases were defined by the presence of a four-fold rise in the MAT titer (36)
whereas in the study by Kamath et al the laboratory test that determined cases remained unclear.

Besides immediate vector related exposure other studies explore the relationship between living in
proximity to bodies of water or in low laying areas and the risk of leptospirosis infection. Prab-
hakaran et al found this to have a significant association among urban dwellers (P<0.0001) (51)
whereas Vanasco et al identified risk factors for leptospirosis to be residence in an urban center
(34). The strength of association was the highest for people also exposed to stagnant water (51). A
study conducted in Salvador, Brazil also found that workplace exposure to contaminated environ-
mental sources and occupational contact to sewer water (matched OR 2.46, 95% CI 1.045.11,
P<0,001), flood-water (P<0,001), or mud (matched OR 3.71, 95% CI 1.3510.17, P<0,005) were
found to be independent risk factors for acquiring disease (48).

While Sarkar et al were looking at workplace exposure Ashford et al studied household factors. They
found that having an indoor household water source was more frequent among non-infected than
infected people (193 [40.1%] versus 15 [17.7%]) and was associated with significant protection (OR
0.32, 95% CI 0.18-0.60, P<0.0002). This factor remained independently associated with protection

17 | P a g e
against leptospirosis when multivariable backward logistic regression analysis was applied (OR ad-
justed 0.42, 95% CI 0.22-0.80) (52). Besides water, sanitation and drainage facilities were also seen
as important epidemiological risk factors as found by Loganathan et al. According to their findings
95,5% of the study sample which acquired leptospirosis had poor sanitation facilities and 78,8%
inadequate drainage facilities (11) . Closely related factors such as living in close proximity to accu-
mulated trash (OR = 4.31, 95% CI 1.41-14.76, P < 0.05) (49) and the presence of drainage and gar-
bage within a 15 meter radius of houses had OR of 3.69 and 2.42 respectively (P=0,013) (38) and
was found to be significantly associated with leptospirosis by Bhardwaj et al and Kamath et al.

Additional environmental factors such high temperatures (28-32 degrees Celsius) and increased
humidity due to climate change have also been linked to the distribution and population size of
disease vectors (11, 47) and so similarly have been associated with prolonged bacterial survival and
expansion of the geographical areas in which leptospires are commonly found (18). With a predicted
rise of global temperatures by 1.45.8 C by the year 2100 (53) likewise incidences of leptospirosis
anticipated to increase (18).

Another finding was that in the study by Sarkar et al. more than 90% of the serovars isolated from
patients belonged to one serogroup called Icterohae morrhagiae, commonly associated with rattus
species reservoirs (48). Similarly Felzemburgh et al found that in his study outbreak of Leptospiro-
sis was due to transmission of the single serovar, L. interrogans serovar Copenhageni. Both
serovars have been associated with rattus species reservoirs.

Members of the genus Rattus are native to temperate and tropical continental Asia. Most of the 20 species in the rattus group live in
lowland and montane rainforests, scrublands, agricultural and fallow fields, and human structures. They occupy habitats including
sandy flats, open grasslands, and grassy areas within forest, heaths, savannas, and tropical rainforests. Out of the 20 species there are
11 species whose relationships are unresolved (Encyclopedia Britannica 2015).

18 | P a g e
 Chart 2: Variation of CI and OR among Environmental Factors
CI (95%)

15

10

0
Proximity to Sighting Rats Sighting Rats Contact with Living close to Having a Contact with Contact with
open Sewer (Bhardwaj (Sarker 2002) Rodents accumulated Indoor Water Sewer Water Flood Water
(Sarkar 2002) 2008) (Keenan 2010) trash Source (Sarkar 2002) (Sarkar 2002)
(Bhardwaj (Ashford 2000)
-5
2008)

When comparing the CI and OR across studies under this theme it becomes clear that variations of
CI and OR are relatively small among the environmental Risk factors that were found to be associated
with leptospirosis. Apart from the study by Ashford et al which found a protective factor for
leptospirosis all other studies mentioning environmental factors can be regarded as homogeneous, as
CI overlap. The estimates of proximity of open sewer made by Sarkar et al are more positive than
the estimates made of other variables. When comparing OR across studies it can be said that on
average people who were exposed to environmental risk factors such as proximity to open sewer,
sighting and having contact with rats as well as having contact with sewer and flood water are four
times more likely to be infected with leptospirosis.

19 | P a g e
 4.2 Human Risk Factors

In comparison to environmental factors, human risk factors are determinants that are internal to a
person including behavioral factors as well as personal characteristics such as age and gender. Risk
behaviors are often directly linked to low socio-economic status and place participants in exposure
to potentially contaminated environment (10).

Besides behavioral factors also gender and age were found to be correlated to primary as well as
secondary infection of leptospirosis. Such factors were, however, only found to be significant in 4
out of 18 studies. Felzemburgh et al in example found that young adults with 1534 years of age (OR
10.82, 95% CI, 1.3885.08) have increased risk for secondary infection whereas male gender was
associated with primary infection (OR 2.88, 95% CI, 1.405.91) (10). While a study by Vanasco et
al identified risk factors of acquiring leptospira antibodies to be age >30 years and male gender re-
spectively (34), Prabhakaran et al found contrary to Vanasco et al findings that age groups between
10-20 were most at risk to acquire infection (51). Likewise Reis et al found association with gender,
though age was not particularly specified and only referred to as increasing age (6).

Human factors besides gender and age that have been found to be favorable for contracting leptospi-
rosis are behaviors that increases exposure to the contaminated environment, particularly contami-
nated water sources and flood water. Such risk behaviors include prolonged exposure of skin, that
presents cuts or abrasions, to contaminated water or mud (38, 49, 54, 55), walking barefoot (OR =
10.34, 95% CI 5.09-21.31, P < 0.001) and taking a bath in floodwater (P = 0.0039) (38, 49, 52) and
were significantly related to acquiring leptospirosis. In the study by Bhardwaj (49) it was observed
that the risk of occurrence of leptospirosis was found to be close to five times higher among those
who walked barefoot in floodwater compared to those who did not (adjusted OR= 4.95, 95% CI 2.22-
11.06, P < 0.001). Whereas Keenan et al describes walking barefoot as non-significant in his study
(50), Loganathan et al found that 85,5% of patients infected with leptospirosis shared a history of
walking barefoot (11). In a study conducted in India in 2007/8 it was pointed out that significant
association between leptospirosis and contact with contaminated soil or water if cut or wound in body
parts are present (OR of 6.05; 95% CI: 2.09-15.3, P=0,001) (38). Although Chusri et al similarly
found significant association between skin wound and leptospirosis, they point out that such associ-
ation only accounts for severe skin disruption, such as laceration wounds (P=0,04) (56). Kamath et
al additionally highlights that individual hygiene and water handling such as boiling of water before
drinking, avoidance of open ground defecation, avoidance of bathing at highly risk areas such as
streams and rivers and protective measures against rodent contact seem to be protective against the

20 | P a g e
disease. Those findings are supported by findings from Allwood et al who also found that poor refuse
management (P<0,01) is an important determinant for contracting leptospirosis (57). Preventative
measures such as wearing boots while working as well as washing hands with soap after work were
found to be factors that are protective against leptospiral infection (24, 25).

Several behavioral factors are also supported by Ashford et al and Bhardwaj et al who found that
infected people were significantly more likely to have washed clothes (P<0.0104) or taken a bath
(P<0.0039) in a river or brook (49, 52) or spent more than four days in cleaning activities respectively
(adjusted OR = 2.64, 95% CI 1.18-5.89, P < 0.05) (49). Individuals who were exposed to those risks,
found to be 2.64 times more likely to contract leptospirosis compared to those who have not been
exposed to such (46).

Chart 3: Variation of CI and OR among Human Factors

CI (95%)
85
80
75
70
65
60
55
50
45
40
35
30
25
20
15
10
5
0
-5 Age (15-34) Male Gender Walking Barefoot Walking Barefoot Contact with flood > 4 days spent in
(Felzemburgh 2014)(Felzemburgh 2014) (Bhardwaj 2008) (Ramachandra water + skin cut cleaning activities
2014) (Ramachandra (Bhardwaj 2008)
2014)

When comparing OR across studies under this theme it can be said that on average people who were
exposed to human risk factors such as walking barefoot, >4 days spend in cleaning activities as well
as contact with flood water are six times more likely to be infected with leptospirosis. As all variables
in studies which presented CIs have overlapping CIs human factors can be regarded as homogeneous.

21 | P a g e
 4.3 Socio-Economic Risk Factors
Socio-economic factors as mentioned above refer to structural factors that influence peoples health.
As such, income, employment, food security, nutritional status, education and literacy, social support
as well as access to services such as health care can be regarded as socio-economic factors. Such
determine peoples socio-economic status within a society and serve as a direct measure for poverty
and vulnerability (58). Socio-economic status is an important determinant of the likelihood that in-
dividuals and populations execute risk behavior and/or are exposed to environmental risk factors
which directly as well as indirectly impact their health (58).

Although mentioned as an important factor in relation to vulnerability in flooding as well as the

transmission of communicable diseases, socio-economic factors have only limited representation in
studies that look at leptospirosis in urban flooding. Only three studies explored factors such as illit-
eracy, per capita household income as well as unsatisfied basic needs (2, 6, 10). Felzemburgh et al
study found that an increase of the daily per capita household income by $1 per person per day de-
creased the odds of primary infection by 50% (OR 0.54 for an 95% CI, 0.300.98) (10). In addition,
socio-economic variables which included illiteracy (P=0,00), low per capita household income
(P=0,00), were found to be risk factors for primary leptospirosis infection in the study by Bacallao et
al (2014) (2). While Bacallao et al explored socio-economic variables related to leptospirosis and
found that extreme poverty is influential factor for acquiring leptospirosis (P=0,00) (2), Reis et al
highlights the association between per capita income and the presence of the disease (6). In this study,
Reis et al define socio-economic status as greater unsatisfied basic needs for quality of the household
and for sanitary services, higher extreme poverty and illiteracy rates and distinguish it from risk given
by environmental factors (2). In Bacallao et al study extreme poverty is also explained as unsatisfied
basic need which is defined by housing conditions, access to sanitary services and access to education.
Another study conducted in Jamaica similarly discusses socio-economic factors in relation to access
to and or availability of information services and education and found that knowledge of leptospirosis
was protective against contracting leptospirosis (OR 0.39; 95% CI = 0.160.93, P = 0.03) (50). Alt-
hough this might highlight the value of public health education in the region Allwood et al showed
that despite over 80% of respondent in his study being aware that rodents and dogs can spread lepto-
spirosis, 45% could not see a connection between open dumping and rodent infestations of their
homes (57).

Besides the awareness factors, occupational factors have furthermore been highlighted in three stud-
ies included in this review. It was found that certain occupational groups are more at risk than others.
22 | P a g e
Such include in the study by Loganathan et al, people who work in sewers, cane or rice fields (11).
In the study by Keenan et al likewise people who were engaged in outdoor labor such as farming
were associated with higher risk of contracting leptospirosis (OR = 5.30 (95% CI = 1.4119.92, P =
0.01) (50). Occupational factors, such as work that involved garbage collection, contact with sewage
water and cleaning an open sewer, were moreover associated with increased risk for infection in
univariate analyses in the study conducted in Brazil by Felzemburgh et al (10).

Chart 4: Variation of CI and OR among Socio-Economis Factors

20

CI (95%)

15

10

0
Increase in PPP by $1 per person/day Knowledge of Leptospirosis (Keenan Outdoor Labor (Keenan 2010)
(Felzembough 2014) 2010)

-5

OR and CI of variables grouped under the socio-economic theme display two protective factors for
leptospirosis in urban flooding: Increase In PPP by one Dollar per person per day and knowledge of
leptosirosis. Chances of leptospirosis infection increase by a fivefold when being involved with
outdoor labour.

Besides case control, cohort and cross sectional studies, which were the main study designs found in
this review, also one ecological study was included. Such was conducted by Bacallao in Nicaragua
in 2014. The ecological study design used in this work examined the relationship between exposure
and outcome on population-level rather than individual-level which is useful for generating hypoth-
eses but also makes it difficult to detect complicated exposure-outcome relationships (59). It has been
highlighted by Piantadosi et al that due to the multidimensional factors that seem to be contributing
to the likelihood of contracting leptospirosis, ecological studies may be a better approaches compared

23 | P a g e
to other study designs, to study exposures that impact health of slum communities in different regions
in the world.

In addition to study results presented above, four literature reviews have also been included in this
paper. The reviews explored factors such as climate change, urbanization and particularly flooding.
Lau et al in his review from 2010 found that the combination of climate change, urbanization and
flooding will likely drive an increase in the overall incidence as well as the frequency of outbreaks
of leptospirosis. Thus as well as due to the complex epidemiology of leptospirosis, ecological ap-
proaches are required to understand disease patterns at local, regional and global levels. He further
highlights that in order to build local coping capacities and to mitigate hazard intensity it will be vital
to understand environmental drivers of leptospirosis (18). Sakundarno et al major finding when re-
viewing the literature on leptospirosis in the Asian-Pacific Region was that most indonesian commu-
nity-based human leptospirosis risk factor studies only used rapid test procedures for diagnosis rather
than a recognized test, such as MAT. This was believed to be due to unavailability and inaccessibility
of gold standard tests. He therefore conclusively suggests to firstly invest in accurate diagnostic tools
and make them available and secondly to gather reliable information on risk factors for leptospirosis
infection in order to develop effective prevention and control programs (24). Baqir et al who explore
common infections during acute and sub-acute phase of flooding events found that leptospirosis in
line with other infectious diseases such as malaria and respiratory infection are causing public health
issues that are related to weak infrastructure, resource limitation and lack of awareness among the
population at risk (5). Alderman et al explore in their review of 35 epidemiological studies the impact
of floods on human health (23) They likewise Baqir et al did group findings into categories. Such
categories include short-term and long term health outcomes of floods. Under short term health out-
comes and communicable diseases, leptospirosis was discussed. Their findings, however, draw a
wider picture of the impact of flooding and highlight environmental factors as the leading risk for
vulnerability to floods and diseases. Such environmental determinants according to Alderman et al
are often caused by underlying socio-economic factors such as urban poverty. They therefore pro-
motes investment into strengthening capacities and improving mitigation measures to be able to re-
duce vulnerability. Out of the four literature reviews included only one, Lau et al review is solely
concerned with Leptospirosis in urban flooding.

In summary it can be said that main risk factors that are associated with leptospirosis can be grouped
into three subgroups. Environmental risk factors, human risk factors and socio-economic risk factors.

24 | P a g e
Although environmental, human and socio-economic risk factors have been distinguished in this re-
view, strong correlation between them are common and combined exposure is likely to increase the
risk of contracting leptospirosis.

5. Discussion
Several factors might contribute to the fact that slum communities seem more vulnerable to disease
outbreaks during flooding. First, houses in slum areas are often built on land with poor quality soil
and with a high susceptibility to flooding (6, 51). During the event of flooding and also heavy rains
contaminated animal urine is washed out of the soil and often passes directly into surface water or
persists in mud (12, 54). The exposure of humans to such contaminated water and mud increases the
risk of transmission of leptospirosis (51). Inadequate flooring was found to be a risk factor in a study
by Bacallao (P=0,00) (2), increasing contact with flood water which is infected, thus increasing the
risk of leptospirosis transmission (6, 18, 37) Second, during the rainy season sewages and drainages
get blocked and overflow leading to environmental contamination and making proximity to open
sewers a factor to be favorable for acquiring leptospirosis (6, 38, 47). Lastly, after floodwater has
subsided leptospires can survive in humid soils for up to six months, giving concern to potential long
term exposure following floods (60). Moreover, after floods, drainage material contaminated with
rodent urine may also collect on roads, creating a potential source of infection (5). During flooding
leptospires gets dispersed through flood water and the redistribution of rodent population to higher
grounds (37) and so often spread to areas that are distant from the source of contamination. This
increases the potential for the agents contact with population groups with no previous contact with
the bacteria. Although many studies found that people living closer to the foci are more likely to be
infected , due to flooding, a shift in this seropositivity can be predicted and should be considered in
future studies (43, 49).

Due to the fact that several studies found that infections of leptospirosis is not necessary related to
direct contact with rodents, but rather clustered around households in slum communities (36, 48) it
becomes clear that the household environment and flood and vector related factors might be one of
the major determinant for leptospirosis transmission in an urban setting. Identification of risk factors
such as residential proximity to an open sewer and household rat infestation support those findings
and indicate the likelihood of peri-domiciliary transmission of leptospirosis. Besides household fac-
tors also work related exposure was noted favoring leptospira transmission in slum communities,

25 | P a g e
work related exposures may equally contribute to infection. Differences which have been drawn be-
tween workplace and peri-domiciliary environment, however, are often not distinguishable as in in-
formal settlements such as the one in Salvador, Brazil, workplace for informal employment is often
located within the same areas where the study subjects reside (36). This in turn means that if envi-
ronmental risk factors are tackled household as well as workplace risk might be reduced.

Improper water storage, which was seen as one of the risk factors associated with leptospirosis
throughout several study areas, is a common practice in communities where water supply from the
National Water Commission is unreliable. This lack of access may lead to people using unsafe water
as main source for water, particularly during the rainy seasons and after natural disasters. Ways to
either improve National Water Commission service or to inform practices and provide the population
with appropriate storage containers should be considered in the future to reduce exposure. Due to the
fact that leptospires are susceptible to chlorine (61), further promotion of chlorine tablets might re-
duce the chance of transmission in the longer term. Besides water management, poor refuse disposal
practices were identified as a major risk factor for acquiring leptospirosis. In several studies poor
refuse disposal seemed to be linked to the limited availability of municipal collection services. Even
though good refuse storage practices were observed in most of the households, many of the residents
also appeared to be practicing open dumping on or near their premises as a means of final disposal.
This strongly indicates lack of community resources to dispose of refuse. The presence of garbage,
waste and sewage not only might be an excellent breeding ground for rodents, but also might block
drainage systems and so exacerbate flooding risk. From this it becomes clear that together with poor
sanitation, inadequate waste management and lack of safe water are major problems in urban slum
communities particularly in developing countries. As findings highlight such environments are di-
rectly related to poor health, such areas are likely to be also more susceptible to the spread infections
such as leptospirosis.

Another area that was highlighted in the results was that knowledge of leptospirosis seemed to have
protective function against contracting leptospirosis. While Allwood et al found that the majority of
the respondents in their study had some knowledge of leptospirosis, a large proportion, including
people who had a history of leptospirosis did not see the connection between open dumping and
rodent infestation and also did not believe that leptospirosis causes a risk for their health. This might
show that communities within the study area might not be aware of the exact transmission route and
associated risk factors of leptospirosis. It might also indicate that while a relatively high level of
knowledge about leptospirosis existed, this does not seem to alter behavioral changes. This could,

26 | P a g e
however, be due to infrastructural barriers. Barriers to behavioral change could be that trash cans are
located far from home of most residents and services are not available to transport the refuse. Besides,
residents who cleaned sewers might have no protective clothing readily available that could keep
them safe from contact with the bacteria. It must be stated that in the event of disaster or flooding
although residents might be aware that contact with floodwater is an important risk factor for trans-
mission of leptospirosis, contact might be unavoidable (39). This highlights that knowledge will only
be useful if structures are in place that enable to put the knowledge into practice. Unfortunately this
is often not the case in deprived areas such as informal settlements.

Besides human and socio-economic factors, the environment seems to be a vital factor in the spread
of leptospirosis as well as in determining the vulnerability of an area to flood, factors such as com-
position of the soils and their drainage characteristics may also serve as a risk for the disease trans-
mission (42). Soil with impeded drainage may be a relevant factor for leptospirosis occurrence.
Therefore, it has been highlighted that Geographical Information System (GIS) analysis and spatial
statistics might be useful to explore spatial patterns as well as the intricate dynamics of disease de-
terminants and associated effects on health (18, 37). Such geographical clustering of risk factors
might be useful to identify communities which may be at risk due to their environmental conditions,
but have not had a history of leptospirosis. In the study by Reis et al (6) GIS and modeling approaches
identified that cases geographically clustered in areas of poor sanitation and flooding during periods
of heavy rainfall. (37). The application of such systems in the future therefore might be useful to
define risk areas and tailor intervention more effectively and efficiently.

After an extensive analysis of all studies included in this review, it becomes clear that several meth-
odological biases have been present. Such might not only have negatively influences on the accuracy
of the findings but also might have led to non-transferability and limitations in overall validity and
reliability of the studies.

Small sample size was one of the major limitations of most of the studies included in this review.
The small sample size and matched design in Keenan et al study made it difficult to detect significant
findings among variables with larger OR. Equally in Allwood et al study small sample size seem to
have affected multivariate analysis which in turn made it not fully possible to relate findings to urban
flooding. With less than 30 cases included, the sample size in the study conducted by Chusri et al
was the smallest among all studies reviewed in this paper. Precise estimates of specific risks might
have therefore been limited. A high non-response rate which led to exclusion of previously defined

27 | P a g e
cases was apparent among sample in the study by Ramat et al. This is believed to be due to the strict
exclusion criteria, which caused each individual who migrated in or out at least one month before the
disease appeared and any suspected case and people having a history of any other viral disease such
as dengue, to be excluded from the study. Out-migration was also the leading factor for a 21% non-
response rate in the follow-up study by Felzemburgh et al. This meant that a significant number of
cases, which could have led to different study outcomes, were missed. Similar issues where recorded
in Brazil in 2002 where Sarkar et al was unable to investigate in 20% of their originally sample size
due to change of residence, high mortality among cases (8%) and/or the random selection method
which was applied. To overcome such response biases Allwood et al in their study included local
community health inspectors which were familiar with the communities to help collect interviews.
This led to high response rates and minimization of sampling or systematic bias. The design although
mainly relying on self-reporting also incorporated elements of observational data, which was used
for variables such as waste disposal, water supply and general sanitation.

Although small sample size impacts negatively on validity as well as generalizability of findings,
household factors found in Maciel et al study might still be relevant to the large slum population
residing in other developing countries. Since slum populations are often subjected to similar condi-
tions of poverty and social marginalization transferability of risk factors still might be possible. Sim-
ilarly Felzemburgh et al acknowledges in their study that even though limitations might have oc-
curred as their study was performed in only a single slum community in Brazil, most slum commu-
nities around Brazil have the same features of poverty, climate, poor environment and inadequate
access to services. Findings might therefore be highly relevant and generalizable for Brazil or at least
several regions within Brazil. Kamath et al supports this view in his study conducted in India and
highlights that cultural practice and environmental factors are the same within different states of India
making generalizability at least to a larger population possible.

Moreover, several studies in this review only give limited information on the data collection process.
In example Bhardwaj et al, even though explaining the process of data analysis in their study suffi-
ciently, only extremely limited information is given on the initial steps of data collection. Equally
shortcoming where found as several studies which did not include nor explain their study limitations
(51). Leaving out valuable information regarding the study process and its limitations makes it ex-
tremely difficult to value the findings of the research, but more importantly might mean that the
reliability of the study is hampered. As all studies which are included in this review made use of
interviews, surveys or questionnaires recall bias could have occurred. The length of time between

28 | P a g e
onset of disease and conduction of interview may have caused a general problem of remembering
exposure to possible risk factors. Likewise the personal ability to recall exposures could have varied
between case and control individuals, which again introduces recall bias and so limits validity and
reliability of findings (38, 48, 50). Interviewers in the study by Keenan et al for example were in-
formed about the disease status of the interviewee before conducting the interview, raising the pos-
sibility of introducing interviewer effects by asking probing questions differently for cases than con-
trols. Although sampling bias is likely to have occurred, studies such Bhardwaj et al, Keenan et al
Pabhakar et al and Sarkar et al ought to avoid confounding and tried to ensure comparability between
cases and controls by matching controls for sex and or age.

When comparing statistical findings in those studies that present OR and CI it becomes clear that
especially confidence intervals reported show an extremely wide range, indicating wide variation
within the sample. This is most likely due to the small sample size, which does not allow for con-
clusion regarding correlation between the tested variables (62). Large variations might also be re-
lated to the differences in underlying conditions of social deprivation, environmental degradation
and climate where urban slum communities are situated. Greater homogeneity of findings can be
observed when comparing environmental factors. Here, confidence intervals are found in the range
of 1,04 -16,5. Odds ratios, apart from the variable of having an indoor water source which was
protective, center around a score of 5,0. This narrow variation indicates that correlation between
tested variables might be strong, therefore true. Out of all studies which included odds ratios in
their design, most presented odds ratio that are adjusted (48, 49, 57). However, two studies only
presented unadjusted OR for some variables (34, 51). This means that other factors might not have
been taken into account when looking at the relationship between the dependent as well as inde-
pendent variable. Confounding variables are particularly important factors that should be consid-
ered when studying a topic that is not yet well understood and appears multifactorial, such as lepto-
spirosis. In order to describe the significance of the findings of a study, P-value needs to be pre-
sented. More than 55% of the studies included in this review do not present and P-values. Felzem-
burgh et al for example does not include any P-value in their study and therefore significance of
proximity to open sewer as well as age and male gender cannot be proven significant as they could
have appeared by chance. Bacallao et al, describe P-value as significant in their study, but display it
as P=0.00 for several variables. As such, finding is not possible to have occurred, it is assumed that
an error in displaying only up to the second decimal place has occurred instead. Presumably signifi-
cance becomes clear when looking at the 3rd or 4th decimal place. This, however, is not possible
for the reader and therefore serves as major limitation of this study.
29 | P a g e
Shortcomings among statistical findings could additionally have occurred during the sample selec-
tion process due to limitations during the diagnosis procedure of leptospirosis. Misdiagnosis of the
disease during the sample selection process could have occurred in studies such as Chusri et al and
Bhardwaj et al which used tests to define leptospirosis cases that were not regarded as gold standard
such as ELISA or MCAT. The lack of applying gold standard test in those studies could be due to
financial constraints and access to tools as reported in Surat, India, where facilities to carry out MAT
were not available and so limited the accuracy of diagnosis (49). Financial constrains equally meant
that in the study by Kamath et al controls were not tested to confirm non-infection. In the study by
Chusri, which used MCAT instead of MAT tools, cases who were infected by different serovars or
were tested after one week after infection could have been misdiagnosed in this study. MCAT has
been shown to be highly sensitive and gives positive results earlier in the course of leptospirosis,
compared to MAT or ELISA. MCAT titres reach their peak at the 7th day after infection and then
gradually decline whereas MAT tires increase up to the 14 th day. MCAT is also not able to detect the
same antibodies against some serovars (63). Misdiagnosis might have furthermore occurred in a
study conducted in Brazil in 2008. This study screened participants for only one specific serovar
called Copenhageni. This was the only serovar believed to be prevalent in the area. Two previous
study from 2000 also indicated that endemic transmission of leptospirosis in the slum setting in Brazil
might be largely due to circulation of a single serogroup (10, 48). Such findings, however, have not
been verified and presence of different serovars might be possible. Therefore, screening for one
serovar only might cause great biases by ignoring the possibility of the existence of other serovars
within one area. Although other studies might have screened for more than one serovar (18, 19, 23,
48), other water- and vector-borne infections that are common after flooding and might mimic lepto-
spirosis symptoms were often also not investigated. Infections, such as malaria, dengue and
chikungunya fever, however, could have coexisted and so worsened progress of disease. In turn this
could have had falsified the overall findings. Due to the fact that misdiagnosis is still a big issue
following outbreaks or leptospirosis investigation conducted in low-income countries (LIC) Chusri
et al suggested to initiate mass medication if patients present leptospirosis symptoms (56). However,
mass antibiotic prophylaxes in order to avoid or reduce occurrence of leptospirosis appears rather
dangerous, considering the vast number of symptoms associated with leptospirosis and the already
massive problem of antibiotic resistance, worldwide.

Conclusion made in relation to factors associated with urban instead of rural areas that have been
flooded might have been limited in Allwood et al study as less than 40% of the households enrolled
in their study were from urban or peri-urban areas. Ashford et al, who similarly to Allwood et al

30 | P a g e
conducted a cross-sectional study in Central America on the other hand had 78.8% of the sample
population living in urban households. Therefore, findings from Ashford et al are more likely to have
presented variables that correlate with urban flooding than findings from Allwood et al where the
majority of the sample was found to be from urban areas.

Several studies included report on leptospirosis in rural areas and so conclusion made cannot be
translated to an urban setting. Out of the four literature reviews included only one, Lau et al review
is solely concerned with leptospirosis in urban flooding. Their review, however, does not include a
methodology nor did they review leptospirosis solely in urban flooding. This indicates that current
literature reviews relating the topic of leptospirosis in urban flooding either have not been able to
draw sound conclusion on urban flooding or have not been able to provide a sound methodology that
would support the validity of their findings.

When looking at studies included in this review it becomes clear that studies which applied a cross
sectional design might not be able to draw conclusions about causes as they are descriptive in their
nature and therefore more likely to generate hypothesis instead of assessing exposures. Studies such
as Felzemburgh et al and Reis et al which make use of a cohort design allow for a more accurate
collection of exposure information and might be able to determine multiple effects of single exposure
compared to the cross sectional studies included in this review. Accuracy, however, only can be
secured in this design if the sample size is large. Whereas Felzemburgh includes a cohort of 2003
people and Reis et al a cohort of 3171, Gaynor only includes 271 respectively, indicating reduced
accuracy of findings in Gaynors et al study. Although cohort studies are ought to be more likely to
establish causality than case control studies, case control studies, which represent the majority of
study designs included in this review, are described to assess exposures and are believed to be a
reliable design for testing for multiple risk factors associated with a disease. Therefore, cohort studies
that include a large sample such as Felzemburgh et al and Reis et al as well as large case control
studies seem to be the most suitable designs for exploring the risk factors associated with
leptospirosis. In regions where the etiology of leptospirosis is unknown or sparsely reported,
however, ecological studies might be the best design as they generate hypothesis and are more likely
to detect wider environmental and socio-economic factors for diseases that are not yet well
understood.

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 Dr Ravikant Singh, founder of Doctors For You (DFY), a NGO serving slum communities in
Mumbai, India since 2011 explains his experiences with leptospirosis and associated public
health implication during flooding in his community:

Ravikant explains that in Mumbai cases of leptospirosis that have been reported are very low and
that he only saw leptospirosis cases during the 2006 flooding when he was working at KEM
Hospital. He remembers that people coming to the clinic were mostly Municipal Corporation of
Greater Mumbai (MCGM) employees, particularly people who were responsible for cleaning the
sewers as well as slum dwellers. Among such, highest disease prevalence was recorded as they
were directly exposed to the contaminated environment he believes. Unplanned urbanization was
seen as a factor that causes an increase in water and vector-borne diseases including
gastrointestinal diseases, malaria, dengue and leptospirosis. Particularly slum settlements here
in Mumbai, so Ravikant, are very congested, densely populated and lack sufficient and clean
water supply and sanitation facilities.

I have not seen any cases reported in people coming from higher economic class.

In addition to this he noticed that especially in slum communities but also compound areas, rat
population is very high. Similarly waste disposal is very poor in Mumbai, especially disposal of
food items, making it a perfect living environment for rats. Because of the poor organic waste
management and state of sewage lines, in an event of flooding all the water gets mixed together
with the rat urine. If people then are walking barefoot through such floodwater, or with a cut, they
can get infected.

In order to control diseases such as leptospirosis he believes that urbanization needs to be

planned, sewer systems need to be improved and accumulated waste needs to be managed more
efficiently in order to reduce underlying risk factors that lead to increased rat population and
environmental contamination. In addition to this, he suggests that improvements in safety
measures for staff cleaning sewers and disposing waste as well as public awareness might be
useful to mitigate risk in the future.
(Dr. Ravikant Singh, DFY, Mumbai, India 2015) (3)

6. Limitations
While there is an established body of literature on rural leptospirosis in relation to farming and lep-
tospires found in canine and other domestic animals, there are only few published studies and papers
available concerning leptospirosis in human in urban flooding. This, meant that this literature review
was reliant on a limited number of studies concerning the wider field of leptospirosis and associated
risk factors. While every effort was made to include and present a vast picture of the literature on this
subject, not all studies that might have been relevant were retrievable through the databases and
therefore were not possible to be included in this report. On a positive note, however, it can be argued
that due to the limited amount of research and original studies conducted in this field of research, the
possibility of selection bias for this review is minor.

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Investigations into leptospirosis in relation to urban flooding only have been made in recent years.
Although this might highlight the current relevance of leptospirosis outbreaks during urban flooding,
it might also make it difficult to draw conclusions regarding changes in the prevalence of the disease,
exposure to risk factors and the development of leptospirosis over longer periods of time.

Due to word limitations it was not possible to explore each question set by the PRISMA protocol in
detail, but rather use those questions to highlight the main strengths and weaknesses of each study
included in this review as well as explore most interesting findings in more depth. Limitations with
regard to the literature analysis and decision making during the actual review were also present due
to the fact that this project only had one reviewer. Presentation of the variation of the CI and OR
among risk factors is not an attempt of a detailed meta-analysis but rather a means to display find-
ings and their strength of association with leptospirosis across studies in order to identify limitation
within the study design.

Several limitations are identified relate to the size of the studies included in this review, the lack of
direct comparability between some of the studies, their generalizability and limitations associated
with the study designs. Some of the studies explored were carried out in localities including a small
sample; hence the findings may have limited generalizability. The strength of associations of the
studied risk factors, expressed as the odds ratio, are sufficiently presented in most case-control
studies, although some only present unadjusted OR which on their own do not allow to calculate
confounding variables that might have influenced findings. Although a majority of the studies pre-
sents statistical data, more than half of the studies included in this review did not provide P-values
that could ensure statistical significance. Due to the fact that random as well as systematic error oc-
curred in several studies conclusion drawn from such might have limited value and did not allow
for sound conclusions regarding significance or risk factors presented.

7. Recommendations for Future Work

Due to the fact that the body of research that has explored leptospirosis in urban flooding is relatively
small, further research is needed to grasp the whole picture of leptospirosis. Future studies need to
acknowledge the complex epidemiology of leptospirosis and therefore should target each effort to
the region specific needs and vulnerabilities. Ongoing monitoring in the post-disaster phase is essen-
tial for assessing the long-term impacts of leptospirosis following flooding and therefore should be
promoted. Risk factors explored in this review might help to determine vulnerabilities associated
33 | P a g e
with leptospirosis and so might help tailor public health initiatives and policy changes effectively.
Risk factors found in this review could be incorporated in guideline documents that set out guidelines
for diagnosis and management of leptospirosis. Such factors can in line with clinical factors serve as
epidemiological determinants for infection and so might support detection of the disease.

Future efforts must focus on multidimensional approaches incorporating environmental, human and
socio-economic factors in the prevention and control of leptospirosis. With regard to environmental
risk factors rodent control, including rodent trapping and the use of poison has been one of the most
common recommendation to minimize exposure to leptospirosis (48). Although investment in rodent
control is recommended (64, 65), in order to reduce exposure to the host many strategies are costly,
time-consuming and their effectiveness have not been evaluated nor validated for slum areas. Wider
public health initiative that look at improvement of living conditions, waste disposal, water storage
and sanitation seem more promising in reducing exposure to risk factors and additionally might also
serve as control for other major infectious diseases such as dengue and malaria as they target under-
lying factors that lead to increased vector populations. Preventative public health measures must first
and foremost include improved water and sanitation facilities as well as better access to health facil-
ities. These measures need to go hand in hand with efficient waste management in risk areas. Invest-
ing in adequate water supplies as well as solid waste management, is essential in preventing outbreaks
of vector-borne diseases (65) Such initiatives should focus on waste composting, recycling, and other
sustainable modalities that create a safer environment. In order to increase public health surveillance
as well as to facilitate appropriate response during a disaster, identification of risk zones will be
beneficial for identifying the source of infection. The application of GIS and modeling approaches
can be helpful in understanding the distribution of the disease within one area or country as well as
predicting future disease burden as a result of environmental change. Such information when shared
with stakeholder, local as well as national authorities can be used as valuable and dynamic infor-
mation to pinpoint and project high-risk locations and hot-spots for epidemics.

Besides improvements made to the environment, health education and awareness raising among
health personnel as well as the population residing in vulnerable areas should be promoted. Frontline
health workers could be explored as a channel for disseminating education at community level. Ap-
propriate public health messages combined with improved surveillance programs for the detection of
disease should be introduced as part of flood emergency preparedness. These should include infor-
mation on hygiene practices, protective clothing, water handling as well as risk factors associated
with skin cuts or abrasions. Although educative measures might be useful, awareness and knowledge

34 | P a g e
might not translate into taking appropriate precautions and actions during emergencies if tools or
structures that would allow for mitigation of exposure are not made available to the public. Therefore,
stakeholders at community and state level should consider for example providing sewer workers with
appropriate protective clothing, residents with sufficient amounts of soap, to secure a safe water
source and to have structures in place that are accessible and able to detect and treat infection. As
chlorine tablets are highly effective against nearly all water-borne pathogens investment and promo-
tion of the use of such tablets as affordable disinfectant for drinking water should be extended. Fur-
ther research is required to investigate into occupational factors such as informal employment and
work conditions associated with urban poverty that influence contact with contaminated environ-
ments. Although mass drug administration to prevent outbreaks in endemic regions is encouraged
due to the multidimensional nature of leptospirosis outbreaks in the past (56) the threat of antibiotic
resistance should be considered before engaging in any chemo-prophylaxis or mass drug administra-
tion campaign.

Investment in laboratory facilities and trained staff might be useful to ensure correct diagnosis, de-
pending on the prevalence of leptospirosis within the country. With regard to public health, focus on
practical tools that. It might also be efficient to invest in the development of accurate diagnostic tests
and practical tools that can detect and distinguish water-borne disease such as leptospirosis during
flooding. Though, this might help reduce and limit disease risk and outbreaks, such tests, however,
need to be made accessible and affordable for communities, to allow for fast and easy detection and
the control of this disease in the future (66).

8. Conclusion
Leptospirosis is a bacterial infectious zoonotic disease which is predominantly found in hot and hu-
mid climate zones. Although the epidemiology of leptospirosis is still poorly understood, leptospiro-
sis has been found to be related to urban flooding. Driving factors seem to be rapid urbanization as
well as climate change. Several studies in the last 15 years have investigated into risk factors that are
associated with leptospirosis. Although such risk factors are highly interlinked they can be grouped
into environmental, human as well as socio-economic risk factors.

Risk factors that are statistically significant with regard to the environment include proximity to open
sewer, presence of and contact with rats in household or workplace as well as being exposed to stag-
nant water (sewer water or flood water) and living in close proximity to trash. Protective factors

35 | P a g e
include having an indoor household water source. Statistical significant factors found in relation to
human risk factors comprise of walking barefoot and the presences of cuts or wounds, particularly
severe skin disruptions and lacerating wounds. Poor refuse management and repeated engagement in
cleaning activities in a river or brook were also significantly associated with leptospirosis in urban
flooding. Socio-economic factors are explained in relation poverty and significant factors include
illiteracy and low per capita household income. Knowledge of leptospirosis was significantly protec-
tive against leptospirosis and was found to stand in direct relation to access to and availability of
information services and education.

Although the household and close peri-domicilary environment remain the major determinants of
leptospirosis transmission in urban setting, areal shifts in seropositivity should be considered during
flooding due to redistribution of rodent population as well as flow of contaminated floodwater to
areas where leptospirosis has not been detected before. Although knowledge of leptospirosis was
found to be protective factors, such knowledge might not translate into action during flooding events
if infrastructural barriers exist that would allow for behavior change. This is particularly an issue in
relation to refuse management, sanitation, availability of protective clothing as well as access to
health services. This literature revealed that most studies exploring leptospirosis in urban flooding
suffer from a small sample size and the lack of statistical significance. This indicates wide variations
within the samples and makes valid conclusions in relation to risk factors related to urban flooding
difficult. Shortcomings among statistical findings might also have occurred due to limitation during
the diagnosis process. Lack of availability and/or access to diagnostic tests that allow gold standard
might have led to underreporting as well as several misdiagnosis.

Whereas selection bias might have been the major limitation in case control studies, response bias
was the main limitation in cohort studies. Application of a matched design helped reduce such bias.
Several studies lack a sufficient methodology in their design. This negatively affects repeatability
and reliability. Large scale cohort studies as well as ecological approaches might be able to provide
most reliable data on risk factors of leptospirosis in urban flooding. Ecological studies are able to
generate hypothesis for wider environmental and socio-economic factors for diseases that are not yet
well understood whereas cohort studies are more likely to establish causality.

This review moreover highlights that future efforts need to emphasize multidimensional approaches
that incorporate environmental, human and socio-economic factors. Such efforts predominantly
should focus on refuse management, water supply and sanitation improvements as well as should be

36 | P a g e
aimed at tackling the underlying factors of absolute poverty. Additional quality research that
acknowledges the complex epidemiology of leptospirosis and targets efforts to each region specific
needs and vulnerabilities is needed to respond to future flooding more effectively.

In order to increase public health surveillance as well as to facilitate appropriate response during a
disaster, identification of risk zones will be beneficial for identifying the source of infection. The
application of GIS and modeling approaches can be helpful in understanding the distribution of the
disease within one area or country as well as predicting future disease burden as a result of environ-
mental change by pinpointing high-risk locations and hot-spots for epidemics. The application of
such systems in the future therefore might be useful to tailor intervention more effectively and effi-
ciently.

Risk factor found in this review might help with the identification of areas and regions specific to
leptospirosis transmission and also highlight gaps and priority needs of the population at risk. Such
information could be used by stakeholders as part of disaster management efforts to improve the
timeliness of emergency response, to provide an evidence base for planning and allocating disaster
management and public health resources such as local capacities, and to target interventions aimed
at reducing infection risk during flooding and so reduce overall burden of disease from leptospirosis.

9. Acknowledgements
First and foremost I would like to thank my supervisors Johan von Schreeb and Roy Nobhojit for
continuous feedback and valuable suggestions regarding the content and design of this work. Further
I like to express my gratitude to Siddarth Daniels David, Annu Baranwal and Ankit Anand, as well
as the other researcher attending the research meetings who gave comments and suggestions that
helped improve my work even further. A special thanks goes to Doctors For You who were incredible
hosts and facilitated the opportunity for me to work in an area that was directly related to my research
topic. Particular gratitude needs to be expressed to the president of Doctors For You, Doctor Ravikant
Singh who gave me the opportunity to be involved in several projects that allowed me to grow
personally as well as professionally. Beyond this I want to thank all my course mates who have not
only given great suggestion for improvements but also have been great emotional support.

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59. Piantadosi S. Ecological biases. American Journal of Epidemiology. 1994;139:761-8.

60. Sulong MR, Shafei MN, Yaacob NA, Hassan H, Daud A, Moham-ad WMZW, et al. Risk
Factors Associated with Leptospirosis among Town Service Workers International Medical Journal.
2011;18:83-8.

61. Gayer M, Connolly MA. Chapter 5: "Communicable Disease Control After Disasters" in
Public Health Consequences of Disasters. Oxford: Oxford University Press; 2005.

62. Higgins JPT, Green S. Cochrane Handbook for Systematic Reviews of Interventions 2011.

63. Sehgal SC, Vijayachari P, Subramaniam V. Evaluation of leptospira micro capsule

agglutination test (MCAT) for serodiagnosis of leptospirosis. Indian Jounal of Medical Research.
1997;106:504-7.

64. Costa F, Ribeiro G, Felzemburgh R, Santos N, Reis R. Influence of Household Rat Infestation
on Leptospira Transmission in the Urban Slum Environment. PLoS Neglected Tropical Diseases.
2014;8(12).

65. Kouadio IK, Aljunid S, Kamigaki T, Hammad K, Oshitani H. Infectious diseases following
natural disasters: prevention and control measures. Expert Review of Anti-Infective Therapy.
2012;10(1):95-104

66. Dechet AM, Parsons M, Rambaran M, Mohamed-Rambaran P, Florendo-Cumbermack A,

Persaud S, et al. Leptospirosis Outbreak following Severe Flooding: A Rapid Assessment and Mass
Prophylaxis Campaign; Guyana, January-February 2005. PLoS ONE. 2012;7(7).

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 11. Appendix
11.1 List of studies included in the Literature Review
Study Name Author Study Location Sample Risk Factors
Type & Year Size
Human Socio-Economic Environmental
Single dosage of Chusri A non- 2014 614 Having a laceration - exposure to flood
doxycycline for et al randomize Thailand wound more than 3 h per
prophylaxis against d day
leptospiral infection and controlled
leptospirosis during trial
urban flooding in
southern Thailand: A
non-randomized
controlled trial
Knowledge, cross- 2014 91 improper storage of - poor refuse
perceptions, and sectional, Jamaica househol water for domestic management
environmental risk Interviews ds purposes
factors among Jamaican
households with a
history of leptospirosis
Risk Factors for Sakunda Literature 2014 19 presence or owning of - flooding, contact
Leptospirosis rno et al Review Indonesia articles domestic animal, with stagnant
Infection in Humans (Asian swimming in rivers, water or flood
and pacific fishing in the streams or water, and taking a
Implications for Public region) rivers, contact with bath or washing in
Health domestic animal tissues the river
Intervention in or urine, and using
Indonesia and the Asia- stream or river water as
Pacific Region a source of drinking
water. Lack of personal
hygiene
Floods and human Alderma Literature 2012 35 highly populated Socio-economic flooding
health: A systematic n, et al Review China & articles areas with suboptimal status
review Australia drainage (i.e. urban
slums)
low-lying areas
Infectious diseases in Baqir et Literature 2012 - Contact with - Increased vector
the aftermath of al review Pakistan contaminated sources, population
monsoon flooding in Walking barefoot
Pakistan
A Case Control Study to Bhardw Case 2006 315 (62 Walking barefoot in - contact of their
explore the Risk Factors aj et al Control Surat cases, floodwater, bathing in injured part with
for acquisition of Study India 253 age floodwater, sighting of flood water,
Leptospirosis in Surat (questionn and sex rats, Living in close constant presence
City after Flood aire) matched proximity to of rats in their
controls) accumulated trash, more household
than four days spend in
cleaning activities
Risk factors associated Prabhak case 2014, 1851 building workers, - people living in
with rural and urban aran et control India (621 keeping a dog in the house dwelling
epidemics al study cases, house, exposed to near water bodies,
of leptospirosis in 1230 stagnant water low lying area
Tiruchirappalli District control
of Tamilnadu, India Age
matched
)
Kamath population 2014, 256 (116 using well-water for - presence of
Studying Risk Factors
et al -based Udupi, cases, drinking purpose, drainage and
Associated with Human
case- India 140 presence of rodents and garbage within 15
Leptospirosis
control control) seeing more than five m radius of
rats per day at home or houses, however,
work place, ,contact direct contact with
with contaminated soil, water or mud
presence of cut or during work,
wound in body parts in taking a bath in
contact with water or the river or stream
mud after work

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 Clinical characteristics Vanasco Case 2008 645 (182 be age >30 years, male - contact with
and risk factors of et al control Argentina cases gender, residence in an contaminated
human leptospirosis in study 463 urban center, occupation surface water and
Argentina control) in rural settings, work- flooding prior to
(19992005) related exposure to the onset of
livestock, illness, extended
contact with
floods in the
recent years
Household Maciel Case 2008, 74 lack of refuse collection - open sewers, poor
Transmission of et al control Salvador, househol services, and sighting of rainwater drainage
Leptospira Infection in Brazil ds (22 rats in the household systems and
Urban Slum cases 52 environment associated
Communities controls) flooding,
Leptospirosis on Oahu: Gaynor Cohort 2007, 271 Open wound (foot) - Exposure to flood
an Outbreak Associated et al Study Hawaii water
With Flooding of a (Internet
University Campus Survey)
Asymptomatic Infection Ashford Cross- 2000 El 566 Private well and Owning a radio, dwellings without
and Risk Factors for et al sectional Sauce, river/lake/spring water lower socio adequate floors,
Leptospirosis in survey Nicaragua sources, washed clothes economic status outdoor household
Nicaragua or taken a bath in a river water source,
or brook
Prospective Study of Felzemb Cohort 2014 2003 1534 years of age, illiteracy, per Household
Leptospirosis urgh et Study Salvador Male gender, illiteracy, capita household flooding during
Transmission in an al Brazil low per capita income rainy periods,
Urban Slum household income, proximity to open
Community: Role of contact with mud, waste sewer, and
Poor Environment in sewage water, or three-dimensional
Repeated Exposures to garbage, and cleaning distance of
the Leptospira Agent an open sewer, work residence to the
that involved garbage lowest point in the
collection valley and open
waste sewers
Population-based case- Sarkar Case- 2000 226 (101 urban poverty, proximity of
control investigation of et al. Control Salvador cases, occupational residence to open
risk factors for Study Brazil 125 con- contact with sewers, sighting
leptospirosis during an trols) contaminated five or more rats,
urban epidemic environment
(sewer water,
flood water,
mud)
Risk Factors for Clinical Keenan retrospecti 2010 132 (43 contact with rodents knowledge of -
Leptospirosis from et al ve case- Jamaica cases 89 leptospirosis was
Western Jamaica control controls) protective
study

Climate change, flood- Lau et al Literature 2010 10 Heavy rainfall, flooding, - -

ing, urbanization and Review Australia Studies hot and humid climate,
leptospirosis: fuelling Exposre to animals,
the fire? Poor sanitation and
inadequate waste
disposal
Socioeconomic Factors Bacallao Ecological 2014 32 access to sanitary unsatisfied basic lower
and Vulnerability to et al Study Nicaragua municip services, In dwellings needs socioeconomic
Outbreaks of alities without adequate floors status, higher
Leptospirosis in (1001 extreme poverty
Nicaragua cases) and illiteracy rates
Impact of Environment Reis et Cohort 2008 3171 Age, male gender, per capita in- sighting of rats in
and Social Gradient on al Study Salvador come, occupa- the workplace
Leptospira Infection in (communit Brazil tions that entail environment,
Urban Slums y based contact with con- distance of
survey) taminated envi- household to the
ronments nearest open sewer

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11.2 PRISMA 2009 Checklist

Section/topic # Checklist item

TITLE

Title 1 Identify the report as a systematic review, meta-analysis, or both.

ABSTRACT

Structured summary 2 Provide a structured summary including, as applicable: background; objectives; data sources; study eligi-
bility criteria, participants, and interventions; study appraisal and synthesis methods; results; limitations;
conclusions and implications of key findings; systematic review registration number.

INTRODUCTION

Rationale 3 Describe the rationale for the review in the context of what is alreadyknown.

Objectives 4 Provide an explicit statement of questions being addressed with reference to participants, interventions,
comparisons, outcomes, and study design (PICOS).

METHODS

Protocol and registration 5 Indicate if a review protocol exists, if and where it can be accessed (e.g., Web address), and, if avail-
able, provide registration information including registration number.

Eligibility criteria 6 Specify study characteristics (e.g., PICOS, length of followup) and report characteristics (e.g.,
years considered, language, publication status) used as criteria for eligibility, giving rationale.

Information sources 7 Describe all information sources (e.g., databases with dates of coverage, contact with study au-
thors to identify additional studies) in the search and date last searched.

Search 8 Present full electronic search strategy for at least one database, including any limits used, such
that it could be repeated.

Study selection 9 State the process for selecting studies (i.e., screening, eligibility, included in systematic review, and,
if applicable, included in the metaanalysis).

Data collection process 10 Describe method of data extraction from reports (e.g., piloted forms, independently, in duplicate) and
any processes for obtaining and confirming data from investigators.

Data items 11 List and define all variables for which data were sought (e.g., PICOS, funding sources) and any as-
sumptions and simplifications made.

Risk of bias in individ- 12 Describe methods used for assessing risk of bias of individual studies (including specification of
ual studies whether this was done at the study or outcome level), and how this information is to be used in any
data synthesis.
Summary measures 13 State the principal summary measures (e.g., risk ratio, difference in means).

Synthesis of results
Risk of bias across studies
14 Describe the methods of handling data and combining results of studies, if done, including measures of
2
consistency
) (e.g., I for each metaanalysis.
15 Specify any assessment of risk of bias that may affect the cumulative evidence (e.g., publication
bias, selective reporting within studies).

Additional analyses 16 Describe methods of additional analyses (e.g., sensitivity or subgroup analyses, meta-regression), if
done, indicating which were prespecified.

RESULTS

Study selection 17 Give numbers of studies screened, assessed for eligibility, and included in the review, with reasons for
exclusions at each stage, ideally with a flow diagram.

Study characteristics 18 For each study, present characteristics for which data were extracted (e.g., study size, PICOS, follow-up
period) and provide the citations.

Risk of bias within studies 19 Present data on risk of bias of each study and, if available, any outcome level assessment (see item 12).

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 Results of individual studies 20 For all outcomes considered (benefits or harms), present, for each study: (a) simple sum-
mary data for each intervention group (b) effect estimates and confidence intervals, ideally
with a forest plot.
Synthesis of results 21 Present results of each meta-analysis done, including confidence intervals and measures of consistency.

Risk of bias across studies 22 Present results of any assessment of risk of bias across studies (see Item 15).

Additional analysis 23 Give results of additional analyses, if done (e.g., sensitivity or subgroup analyses, meta-regression [see Item
16]).
DISCUSSION

Summary of evidence 24 Summarize the main findings including the strength of evidence for each main outcome; consider their
relevance to key groups (e.g., healthcare providers, users, and policy makers).

Limitations 25 Discuss limitations at study and outcome level (e.g., risk of bias), and at review-level (e.g., incom-
plete retrieval of identified research, reporting bias).

Conclusions 26 Provide a general interpretation of the results in the context of other evidence, and implications for future
research.

FUNDING
Funding 27 Describe sources of funding for the systematic review and other support (e.g., supply of data); role of
funders for the systematic review.

11.3 List of Risk Factors (summary after initial screening of articles)

Human (lifestyle/behavioral) Environment (Physical, chemical & biological) Socio-Economic
- Walking barefoot - Living in a low lying area - Illiteracy
- Contact with flood water - Living near water bodies - low per capita
- Use of surface water - Presence of garbage within 15m radius of house household income
- Non-use of soap - High temperatures (28-32 degrees) and humid - high extreme
- Having a skin cut or abrasion environments poverty
- Ingestion of contaminated water - Overcrowding - low education level
- Swimming in freshwater pools - Presence of stray dogs and/or rats - Lack of knowledge
- Improper water storage and collection - Presence of rats in household about leptospirosis
for domestic purposes - Prolonged exposure of the skin to contaminated - Occupational
- Age of 15-34 / Male gender water contact with animal
- Cleaning open sewer - Spending more than 4 hours a day in cleaning excreta
- Bathing and/or washing clothes in activities - No or insufficient
contaminated water sources - Presence of poor refuse disposal practices access to sanitary
- Contact with mud, sewage water, - Flooding of household services and piped
garbage - Proximity of place of residence to the nearest open water
- Contact with rats waste sewer - Poor rainwater
- Having a antecedent of cholera or - Number of rats sighted in workplace and/or drainage systems
dengue household
- Keeping dogs in the house
Combination of risk factors increases risk

11.4 Interview Questions

After having explained the purpose of this short interview and the way the information will be used
in this project verbal consent was taken. The interviewee agreed to the interview and that the
organization name as well as that his position within the organization will be mentioned in this
paper.

1. Hi, Dr. Ravikant, please tell me a bit about yourself.

My name is Dr. Ravikant Sigh. I started an organization called Doctors For You (DFY) in August

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2002 together with a few of my colleges and other students. DFY has two health centers of which
both serve slum communities in Mumbai. Before that, I used to work in KM Hospital as a general
practitioner but my specialization now is public health so my concern is more with the control and
prevention of diseases.

2. What do you know about Leptospirosis? Incidences? Symptoms? Diagnosis? Treatment?

I have not been working directly with Lepto cases since the last outbreak, 7 years ago. We have
seen all ICU cases of Lepto in our emergency department during my residency days in KEM
hospital though. I dont remember the exact diagnostic tools or treatment procedure which were
used for Leptospirosis. As far as I remember treatment was mainly symptomatic treatment.

3. Do you think Leptospirosis outbreaks are related to flooding?

Actually if you ask me, yes. During the 2006 flooding in Mumbai we have seen most Leptospirosis
cases. Otherwise reported cases have been very low. People coming to the clinic were mostly
coming from certain areas within the city. BMC employees, particularly people who are responsible
for cleaning the sewers were reported to have been infected, as they are obviously more exposed to
the contaminated environment. The cases reported were not age nor gender specific.

4. Do you think Leptospirosis outbreak are related to urbanization?

Yes definitely because there is so much unplanned urbanization. And this is not only causing Lepto
but even more though high increase in diarrheal cases and malaria. Particularly slum communities
here in Mumbai are very congested, densely populated and lack sufficient and clean water supply
and sanitation facilities. So most cases I have seen are coming from those slum areas only. I have
not seen any cases reported by people coming from higher economic class. All of the cases I know
of have come from the slum community and lower socio economic class.

5. So you already mentioned Environmental as well as Socio-economic factors which seem to

be related to Leptospirosis but what would you see as Human/Behavioral Factors that might
cause a risk?

The one thing I noticed in Mumbai is, especially in slum communities but also compound areas,
that the rat population is very high. Waste disposal is very poor especially disposal of food items,
making it a perfect living environment for rats. In fact people are even given 5 to ten rupees if they
hand over rats to the BMC (Bombay Multiprincipal Corporation). Because of the poor organic
waste management and state of sewage lines in an event of flooding all the water gets mixed
together with the rat urine. If people then are walking barefoot through such floodwater, or with a
cut, they can get infected.

6. What do you think are preventative measures that should be taken to control spread of such
diseases?

We just have to plan urbanization and improve the sewage system as well as waste management.
Also the rat population needs to be controlled. There needs to be more safety measures in place,
especially for the staff cleaning sewers and disposing waste. More general public awareness might
also be useful. Education is useful because people should know that its dangerous to walk barefoot
during flooding and monsoon season. People should also be informed about proper waste disposal
as due to the amount of wastage the rat population keeps on increasing.

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11.5 Internship Report
Mumbai, which is home to one of the largest slums in the world, also has a history of Leptospirosis
outbreaks following flooding and therefore served as the perfect place to investigate into risk factors
that favor Leptospirosis during urban flooding. During my five week stay between April and Mai
2015 I was involved with Tata Institute of Social Sciences as well as a local non-governmental
organization (NGO) that offers health services to local slum communities as well as is involved in
disaster response efforts in the state of Maharashtra, Bihar, Assam and the region of Kashmir. The
objectives of this internship were to get a contextual insight into risk factors that might favor
contracting Leptospirosis and to explore possible local limitations that might hinder the reduction of
such risk factors.

Before my departure to Mumbai, Dr Roy Nobhojit had already established contacts to Doctors For
You and so I was able to have a Skype call and arrange a meeting with the president and founder of
this NGO in the first week of my arrival. During the meeting we finalized the scope my involvement
and set days on which I would be joining Doctors For You in their offices near the slum. My major
focus were to support DFY with their efforts in the community and particularly with disaster related
projects which are still running. During my first few days I visited both of their health facilities, met
staff and got introduced to their work. In the coming week I was able to accompany Doctors For You
to their outreaches in the local slum. During such, I was not only able to observe living conditions of
people living in informal settlements in Mumbai but also to assist in a vaccination campaign
facilitated by Doctors For You.

During my second week of internship a devastating earthquake hit Nepal. This caused that my efforts
regarding Leptospirosis were put on hold. I joined the response team from Doctors For You and
developed preliminary situation definition (PSD) documents and initial assessment reports that
served to inform extend and possible impact of the disaster to the team. Moreover I conducted inter-
view about current DFY efforts in the Nepal Response for local newspaper

I partnered with Siddarth a researcher from Tata Institute to assess the situation in Nepal and advice
DFY on possible support that could be provided and possible projects that could be developed as part
of their Nepal response. From such efforts we developed a checklist that helped doctors to collect
basic primary data out in the field. Such data was meant to inform baseline data changes following
the earthquake and to tailor response in the coming weeks.

Besides disaster response efforts I finalized a proposal for the set-up of a national nutrition platform
that offers opportunities for capacity building, guidance, international standards, information sharing
and dissemination with regards to nutritional needs in emergencies such as natural as well as man-
made disaster. This platform is designed to build structures that enable long term involvement, ca-
pacity building & support for already existing schemes, projects & organizations under the nutrition
cluster as well as interested parties who seek to develop effective response capacities in emergencies
and disaster. Structures are ought to facilitates coordinated response to disaster at national level. The
alarming Nutritional Status of India has been highlighted by UNICEF, who seems eager to support
this project.

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Besides getting to know and sharing information with researchers from Tata Institute and doctors
and disaster manager from Doctors For You I was able to form bonds with extremely interesting and
knowledgeable people and so grow personally as well as professionally.

With regards to my thesis and research, weekly research meetings, which were held every Thursday
at the Institute, allowed me to present my ideas, ask questions and discuss progress. It further gave
me the opportunity to explore other peoples work and take part in research debates regarding topics
such as informed consent for clinical trial as well as findings from interventions executed in Assam
state following flooding and Kashmir region during conflict.

At the end of my stay I conducted a small interview asking the founder of Doctors For You about his
experience of and concerns about Leptospirosis in Mumbai during urban flooding. This short inter-
view should serve as a additional note that allows for personal contextual information with regards
to Leptospirosis during urban flooding.

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