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164]

J Vector Borne Dis 58, March 2021, pp. 47–53

Investigation of multiple infections with zoonotic pathogens of rodents in


northern Vietnam
Le Thi Lan Anh1, Alexander E. Balakirev1, 2, Nguyen Van Chau3
Joint Russian–Vietnamese Tropical Research and Technological Centre, Cau Giay, Hanoi, Vietnam; 2A.N. Severtsov Institute of Ecology and
1

Evolution, Russian Academy of Sciences, Moscow, Russia; 3National Institute of Malariology, Parasitology and Entomology, Nam Tu Liem,
Hanoi, Vietnam

ABSTRACT

Background & objectives: Rodents are important reservoir hosts for several zoonotic pathogens such as Rickettsia,
Leptospira and Bartonella. Studies on the prevalence of zoonotic pathogens in Vietnam are data deficient, and there
is a scarcity of data on multiple co-infections of zoonotic pathogens to date. This study examined the prevalence of
Rickettsia spp., Leptospira spp., and Bartonella spp. and the co-infection of these pathogens in rodents captured in
three provinces of northern Vietnam - Ha Giang, Lao Cai and Cao Bang.
Methods: In total, 133 rodents of 25 species were screened for pathogen prevalence by real-time PCR.
Results: Very high infection rates were found for each pathogen, with 42 of 133 rodents (31.6%) positive for Barton-
ella and 33 of 133 (24.8%) positive for Rickettsia (5.3% were positive for Rickettsia typhi, and 19.5% were infected
with Rickettsia spotted fever group). Additionally, 24 rodents (18%) were positive for Leptospira. Double infec-
tion among these three pathogens was found in 26 of 133 rodents (18.8%), with the highest dual infection rates for
Rickettsia and Bartonella co-infection (40%) and Leptospira and Bartonella co-infection (up to 40%), followed by
Rickettsia and Leptospira co-infection (20% of animals investigated). One case of triple infection was documented
for a house rat (Rattus cf. rattus species group) trapped in Ha Giang province.
Interpretation & conclusion: Our survey indicates that rodents in northern Vietnam may host multiple zoonotic
pathogens simultaneously; thus, rodents contribute significantly to the increased risk of transmission of multiple
zoonotic infections from animals to humans.

Key words zoonotic diseases; Rickettsia; Leptospira; Bartonella; natural foci diseases; Indochina

INTRODUCTION ing countries such as Laos, Cambodia and Thailand, with


seasonal peaks of incidence during the rainy season and
Zoonotic disease refers to diseases that are transmitted outbreaks related to flooding events8. Leptospirosis is also
from animals to humans. Approximately 60% of all human considered the most common cause of acute fever of un-
infectious disease agents are zoonotic diseases by origin1, known origin in Vietnam, besides with rickettsial fever9.
and the most important reservoir species for these diseases Bartonella is transmitted from animal reservoirs (rats,
include rodents2 and some other wild mammals. Four of the mice, cats, dogs, and bats) to humans through ectoparasite
most important tropical transmission zoonotic diseases in vectors such as fleas, ticks and lice. Bartonella infection
the world are caused by Rickettsia, Leptospira, Bartonella has been reported in parts of eastern Asia such as China,
and Borrelia species. Rickettsial infections represent a ma- Japan, Korea, Far East of Russia, and Taiwan and in south
jor source of non-malarial febrile illnesses among residents central Asia (Afghanistan, Bangladesh, India, and Nepal)
of Southeast Asia and returning travellers from that region3. and Southeast Asia (Indonesia, Philippines, Singapore, and
Rickettsioses are zoonotic infections transmitted to hu- Thailand)10. Although no human cases of Bartonella spp.
mans via the bites of infected ticks, fleas, mites, and lice4. In infection have been reported to date in Vietnam, Bartonella
Vietnam, a low sero-prevalence of Rickettsia has been re- spp. have been identified in febrile humans elsewhere in
ported4; however, rickettsial DNA has been found in ticks5 Southeast Asia11 and are commonly found in rats in south-
and rodents6. Leptospirosis, one of the important zoonotic ern Vietnam12.
pathogens that can be transmitted to humans through ro- Because the three zoonotic pathogens of Rickettsia,
dents7 via cuts in the skin or by drinking leptospirosis-con- Leptospira, and Bartonella share the same primary res-
taminated water, was first reported in 1930. The infection ervoirs (rodents and other wild animals), the presence of
is believed to be endemic to Vietnam and other neighbour- multiple co-infections of these diseases is assumed. In
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48 J Vector Borne Dis 58, March 2021

Vietnam, some data have been reported about Rickettsia, The kidneys and livers were collected and stored fresh
Leptospira and Bartonella mono-infection in rodents5–6, at -80oC (for some of the Ha Giang samples) or preserved
12–14
, but these findings are sparse and are primarily fo- with 96% alcohol and stored at -20oC (for the remainder
cused in southern Vietnam. Furthermore, co-infection of the Ha Giang samples and the Lao Cai and Cao Bang
was not investigated or specifically mentioned. In this samples) until processing.
study, we investigated rodents that were trapped in three
provinces of northern Vietnam. The prevalence of Rickett- Total DNA extraction
sia, Leptospira and Bartonella and multiple infections of A total of 133 tissues (liver and kidney) were avail-
these pathogens were investigated using real-time PCR. able for DNA extraction. Small pieces of liver or liver
Our survey helps identify and warn of the risk of infec- and kidney tissues were sampled in the field and stored
tions with these pathogens in humans in Vietnam and for in 96% alcohol for DNA extraction. Total genomic DNA
travellers visiting the country. was extracted using a routine phenol/chloroform/protein-
ase K protocol16–17. The DNA was further purified either
MATERIAL & METHODS by a DNA Purification Kit (Fermentas, Thermo Fisher
Scientific Inc., Pittsburgh, PA) or by direct ethanol pre-
Study sites and animal sampling cipitation.
This study was performed as a series of independent Real-time PCR with SYBR green fluorescence detec-
expeditions in 2010, 2013, 2014, and 2018 in three prov- tion was performed using a Rotor-Gene Q (Qiagen) ther-
inces of northern Vietnam: Ha Giang province [Vi Xuyen mocycler with SYBR Green PCR Master Mix (Applied
(in 2014 and 2018) and Quan Ba districts (in 2013) and Biosystems) with target-specific primers. The threshold at
Ha Giang and Meo Vac towns (in 2010, 2014), with 88 10 times the standard deviation of the fluorescence value
animals collected]; Cao Bang [Trung Khanh and Thong of the baseline was setup for positive samples separation.
Nong districts (in 2013), with 37 animals collected]; and The samples reached threshold value by 40 cycles con-
Lao Cai [Sa Pa district (in 2013), with eight animals col- sidered as positive, all suspected positive results appeared
lected]. In the Ha Giang and Lao Cai provinces, trapping near 40 cycles (37–39) were run one times additionally
was performed with the help of the local people. Up to and treated as true-positive only if result was confirmed.
150 living traps were placed per day; the captured animals Appropriate positive and non-template controls were in-
were collected and processed in the field laboratory. The cluded in each PCR reactions set (pair per 10 samples
animals’ populations and densities in the study area were investigated), and post-amplification melting-curve anal-
not determined; the focus in catching many animals was ysis was performed at the end of each run to confirm the
to maximise the number of examined rodents. Thus, the specificity of the reaction and checking for primer-dimer
main biotopes surveyed were places where garbage ac- artifacts. Absolute levels of target DNA were calculated
cumulated and synanthropic species were concentrated in from a standard curve established using the DNA stan-
territory along rivers and streams, in addition to on/near dards.
rice fields and vegetable gardens adjacent to settlements;
to a lesser extent, natural habitats were surveyed. In Cao Detection of Rickettsia spotted fever group, Rickettsia
Bang province, trapping was performed directly by one typhi and Bartonella spp.
of the authors (AEB, up to 50 living traps were placed per Real-time PCR targeting OmpB, the hypothetical pro-
day) mainly in forest biotopes with a focus on the wild spe- tein gene 01310, and ITS genes was used for the detection
cies community; several other species (mainly squirrels) of Rickettsia spotted fever group (SFG), Rickettsia typhi
were also captured in the neighbouring forests by local and Bartonella spp., respectively (in-house real-time PCR
residents and were acquired for examination. We followed kits were made by the Research Institute of Epidemiology
guidelines of the American Society of Mammalogists for of the Federal Service on Customers’ Rights Protection
standard operating procedures (SOP) with wild rodents and Human Well-being Surveillance, Moscow, Russia).
during the collection and handling of the animals used in
this survey15. The animals were amalgamated by chloro- Detection of Leptospira
form and sacrificed by cervical dislocation, bodies were The real-time PCR kit AmpliSens® Leptospira-FRT
packed individually in white dense tissue bags to prevent (InterLabService Ltd.) (Research Institute of Epidemiol-
ectoparasites spread; after what they were weighed, meas- ogy of the Federal Service on Customers’ Rights Protec-
ured and preliminarily classified based on morphology tion and Human Well-being Surveillance, Moscow, Rus-
followed by they were sampled for total DNA. sia) targeting the 16S rRNA was used to screen the DNA
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Anh et al: Zoonotic pathogens in northern Vietnam 49

samples for all Leptospira spp. The animals obtained in the field from 2010 to 2014
were specifically investigated in the laboratory as muse-
Ethical statement um materials; the prepared skulls were evaluated with a
This study was approved by Ethical Committee coded binocular microscope, and the animals were genotyped by
IRB-VN02017 which is certificated by Ministry of Health the Cyt b or COI genes and BLAST was run in the Gen-
of Vietnam Bank database; and taxonomical attribution was directly
assessed and followed the most recent taxonomy18 and
RESULTS species ranges19–21 in Indochina. The species attribution
Sample identifications and taxonomy used of rodents trapped in 2018 in Ha Giang province was un-
Table 1. General list of animals investigated and pathogens detected
No. Rodent species N (samples Infection positive Percentage
investigated) Rickettsia SFG Rickettsia typhi Leptospira Bartonella in sampling
(%)
Insectivora, Soricidae
1 Neotetracus sinensis (Trouessart, 1909) 2 0 0 0 0 1.5
Scandentia, Tupaiidae
2 Tupaia belangeri (Wagner, 1841) 1 0 0 0 0 0.8
Primates, Lorisidae
3 Lepilemur edwardsi (Forbes, 1894) 1 0 0 0 1 0.8
Carnivora, Mustelidae
4 Melogale moschata (Gray, 1831) 1 0 0 0 0 0.8
Rodentia, Sciuridae
5 Hylopetes sp. 1 1 0 0 0 0.8
6 Petaurista alborufus (Milne-Edwards, 1870) 2 1 0 0 0 1.5
7 Callosciurus inornatus (Gray, 1867) 3 2 0 0 2 2.3
8 Callosciurus erythraeus (Pallas, 1779) 4 0 0 1 0 3.0
9 Dremomys rufigenis (Blanfird, 1878) 3 1 0 0 0 2.3
Spalacidae
10 Rhizomys sinensis (Gray, 1831) 1 0 0 0 0 0.8
Muridae
11 Bandicota savilei (Thomas, 1916) 5 1 0 1 4 3.8
12 Leopoldamys revertens (Robinson, Kloss, 1922) 3 1 0 0 0 2.3
13 Berylmys bowersi (Anderson, 1879) 4 1 0 2 2 3.0
14 Mus musculus (Linnaeus, 1758) 1 0 0 0 0 0.8
15 Mus sp. 1 0 0 0 0 0.8
16 Niviventer confucianus (Milne-Edwards, 1871) 1 0 0 0 1 0.8
17 Niviventer fulvescens (Gray, 1847) 13 3 1 1 6 9.8
18 Niviventer mekongis (Robinson and Kloss, 1922) 8 1 1 0 2 6.0
19 Niviventer lotipes (Allen, 1926) 5 0 0 0 2 3.8
20 Niviventer niviventer (Hodgson, 1836) 1 0 0 0 0 0.8
21 Rattus andamanensis (Blyth, 1860) 2 0 0 0 1 1.5
22 Rattus nitidus (Hodgson, 1845) 5 0 0 1 2 3.8
23 Rattus norvegicus (Berkenhout, 1769) 4 1 0 0 2 3.0
24 Rattus cf. rattus (Linnaeus, 1758) * 16 2 1 7 4 12.0
25 Rattus tanezumi (Temminck, 1844) 44 9 6 11 13 33.1
26 Rattus sp. 1 0 0 0 0 0.8
Total 133 24 9 24 42 100
Percentage of positive (%) 18.0 6.8 18.0 31.6
*The name R. cf. rattus used in this paper should be recognised as a ‘member of the R. rattus species group’.
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50 J Vector Borne Dis 58, March 2021

fortunately examined based only on morphology without for each species of P. alborufus, R. norvegicus, B. bowersi,
molecular genetic attribution22. This creates known prob- L. revertens, B. savilei, D. rufigenis, and Hylopetes sp. In
lems with the correct species attribution. Currently, R. rat- general, of the 33 samples positive for Rickettsia SFG and
tus (Linnaeus, 1758) proper does not inhabit Indochina; R. typhi, 23 samples were obtained from Ha Giang prov-
however, until recently, this incorrect taxonomic attribu- ince, 8 samples were obtained from Cao Bang province,
tion was widely used in the medical literature in the re- and two samples were obtained from Lao Cai province.
gion. In fact, no individuals bearing the R1 mitochondrial According to the data presented here, we can confi-
haplogroup haplotype (genetic label of this species) are dently argue that there is a significant level of infection
currently recorded in the GeneBank database from any- with Rickettsia in synanthropic species (genera Rattus
where in continental Indochina out of several hundreds and Bandicota members). However, for several wild
of sequences stored. The rats morphologically similar to non-synanthropic species represented in our sample set
this haplotype were usually called ‘Rattus haplogroupe by only a few or even single individuals (rats of the gen-
IV’ due to the lack of an appropriate taxonomic name; era Niviventer, Leopoldamys and Berylmys and various
these rats belong to the R. rattus species group but are not species of squirrels, even flying squirrels), a higher level
identical to R. rattus proper or a few other members of this of infection was also noted, primarily by Rickettsia SFG
group of species20, 23. Thus, the name R. cf. rattus used in strains. This suggests a wide distribution of natural foci
this paper should be recognised as a ‘member of the R. of this infection, not only in the agro-cultural landscape
rattus species group’. but also in nature.
The 133 small mammals investigated included 114
rats, 15 squirrels,one tree shrew (Tupaia belangeri), Multiple infection with Rickettsia, Leptospira and Bar-
two ferret-badgers (Melogale moschata), and one lemur tonella in rodents
(Lepilemur edwardsi); 26 different species were identi- To determine the co-infection rate of Rickettsia, Lep-
fied. As shown in table 1, the most abundant species in this tospira and Bartonella in rodents collected in northern
study was Rattus tanezumi (33.1%, 44 of 133 rodents), Vietnam, and the multiple co-infections of these three
followed by R. cf. rattus (12%, 16 of 133 rodents) and common tropical zoonotic diseases, our 133 rodent sam-
Niviventer fulvescens (9.8%, 13 of 133 rodents). The oth- ples were examined by real-time PCR. The prevalence
er 23 species were Rattus norvegicus, R. andamanensis, of Rickettsia, Leptospira spp., and Bartonella spp. indi-
R. sp., N. fulvescens, N. mekongis, N. niviventer, N. cf. vidual, double and triple co-infections was investigated
confucianus, N. lotipes, Berylmys bowersi, Leopoldamys simultaneously. The results indicated that Bartonella spp.
revertens, Mus musculus, M. sp., Rhizomys sinensis, Neo- showed the highest prevalence (42 out of 133 rodents,
tetracus sinensis, Callosciurus erythraeus, C. inornatus, 31.6%) in all the investigated areas, including Ha Giang,
Dremomys rufigenis, Petaurista alborufus, Hylopetes sp., Cao Bang and Lao Cai provinces. Most of the positive
T. belangeri, Melogale sp., Neotetracus sinensis, and L. Bartonella spp. samples (25/42) were collected in Ha
edwardsi, which each comprised between 0.8% and 6.0% Giang province, whereas six positive samples were found
of the samples. in Lao Cai province and 11 were obtained in Cao Bang
province (Fig. 1). Interestingly, similar to Rickettsia spe-
Detection of Rickettsia SFG and R. typhi in rodents
To examine the prevalence of two Rickettsia groups,
including Rickettsia SFG and R. typhi, 67 DNA samples
collected in Ha Giang province in 2018 and another 66
DNA samples of rodents trapped between 2010 and 2014
in Lao Cai and Cao Bang provinces were analysed by
real-time PCR. The results in table 1 show that among the
133 rodent tissue samples, 33 (24.8%) were positive for
Rickettsia, including Rickettsia SFG and R. typhi. Of these
samples, 26 (19.5%) were positive for Rickettsia SFG and
7 (5.3%) were positive for R. typhi. These samples com-
prised the following species: 14 rodents (42.4%) were R.
tanezumi, five rodents (15.2%) were N. fulvescens, three
rodents (9.1%) were R. cf. rattus, two rodents (6.1%) were
N. huang and C. inornatus each, and one rodent was found Fig. 1: Distribution of patogens by locations in northern Vietnam.
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Anh et al: Zoonotic pathogens in northern Vietnam 51

Table 2. Detection of multiple infections in northern Vietnam rodents and small animals
Multiple infections Rickettsia + Leptospira Leptospira + Bartonella Rickettsia + Bartonella Rickettsia + Leptospira + Bartonella
Number of positive samples 5 10 10 1
Percentage (%) 20 (5/25) 40 (10/25) 40 (10/25) 0.75 (1/133)

cies, the positive cases for Bartonella spp. were primar- of dual infection was found in three synanthropic species:
ily found in four species: R. tanezumi, N. fulvescens, R. R. tanezumi, followed by R. cf. rattus and B. savilei. How-
rattus, and B. savilei. Of the 44 R. tanezumi trapped in ever, three cases of Rickettsia and Bartonella dual infec-
Ha Giang province, 13 were positive for Bartonella. Of tion were detected in N. fulvescens, and one case each was
the 13 trapped N. fulvescens rodents, six were positive detected in C. inornatus and N. huang (Fig. 2).
for Bartonella. Additionally, 4/16 trapped R. rattus were This pattern of distribution of cases of joint co-infes-
Bartonella positive, and 4/5 B. savilei were positive for tation between synanthropic and non-synanthropic spe-
Bartonella (Table 1). As noted above, three of the spe- cies may indicate a specific distribution of Rickettsia and
cies, namely, representatives of the genera Rattus and Bartonella foci among species of wild fauna in the natural
Bandicota, belong to the synanthropic fauna; however, environment. The lack of material available does not al-
N. fulvescens is one of the most abundant ‘background low us to analyse this phenomenon in detail. Obviously,
species’ and is widely distributed in a variety of natural more profound and extensive research should be aimed
forest ecosystems in northern Vietnam. at screening not only the synanthropic but also the wild
The real-time PCR results for Leptospira spp. pre- forest fauna of small mammals in the region of Southeast
sented in (Table 1) indicated that 24 of 133 rodents (18%) Asia. This becomes even more relevant because of the
were positive for Leptospira, which included 22 rodents customs of Vietnam, where various species of rats and
collected in Ha Giang province and only two rodents squirrels are a common object of hunting for human food
trapped in Cao Bang province. These positive samples be- consumption. Therefore, it is likely that the number of
long to seven genera: R. rattus (7/24), R. tanezumi (11/24), direct contacts with rodents and the contribution of wild
B. bowersi (2/24), B. savilei (1/24), N. fulvescens (1/24), species to cases of human infection of the agents investi-
R. nitidus (1/24), and C. erythraeus (1/24). gated here are much greater when compared with regions
The result of screening for double infections indicated where there are no such traditions. Conversely, the wide-
that approximately 18.8% (25/133) of the samples were spread co-infection among synanthropic species is quite
positive for two of the three pathogens. Of these samples, obvious.
dual infection with Rickettsia and Bartonella and with One single triple infection (0.75%) of Rickettsia,
Leptospira and Bartonella was found in 40% (10/25), fol- Leptospira and Bartonella was found in R. cf. rattus that
lowed by dual infection with Rickettsia and Leptospira, was trapped in Ha Giang province. After analysing the
accounting for 20% (5/25) (Table 2). After analysing the results of the 25 dual infection samples, 20 cases were
host reservoirs in these dual infection cases, a higher rate obtained from Ha Giang province, 3 cases were obtained
from Cao Bang province, and two cases were obtained
from Lao Cai province. These observations indicate that
a high risk of pathogen infection was found in Ha Giang
province, and synanthropic rodents are the main reser-
voirs for the spread of infections.

DISCUSSION

Although multiple co-infections of zoonotic patho-


gens have not been specifically investigated and reported
in Vietnam, this area of study is very popular around the
world. Leptospira, Rickettsia, and Bartonella infections
are among the most frequent causes of undifferentiated
fever in tropical regions, including Vietnam. Rodents and
Fig. 2: Multiple infections of Rickettsia, Leptospira and Bartonella small mammals are the main host reservoirs of several
and host reservoirs in northern Vietnam. zoonotic pathogens.
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52 J Vector Borne Dis 58, March 2021

The prevalence of Bartonella in rodents and other and Leptospira (20%). Only one triple infection (0.75% of
small mammals varies significantly in East and Southeast the rodent population screened) of Rickettsia, Leptospira
Asia, and the distribution of zoonotic agents may vary and Bartonella was found in the house rat R. cf. rattus. A
between countries and between regions in one country. molecular survey of multiple infections of Borrelia, Rick-
For example, prevalence values of 6% have been reported ettsia, Bartonella, Babesia, Ehrlichia, Anaplasma, Fran-
in Jakarta24, 8.7%–41.5% in Thailand25–26, 10.3% in Tai- cisella tularensis and Coxiella burnetiid in rodents and
wan27, and 25.5% in Laos28. Our data for the Rickettsia and small mammals in Croatia indicated comparable levels
Leptospira infection rate showed that 24.8% (33 of 133 of infection, with 21.5% of rodents infected with Lepto-
rodents) were positive for Rickettsia, of which 5.3% was spira and 12% infected with Bartonella. The dual and
R. typhi and 19.5% was Rickettsia SFG; additionally, 24 triple infection rates were reported as 10.7% and 2.9%,
rodents (18.1%) were positive for Leptospira. Some stud- respectively29. In Peru, there was a higher prevalence
ies on Rickettsia, Leptospira and Bartonella have been of Bartonella infection than of Leptospira in rodents22.
reported previously in Vietnam, but they were sparse and Conversely, a study of multiple infections of zoonotic
mostly focused on the southern part of the country5–6, 12–14. pathogens, including three different hantavirus species,
Furthermore, multiple infections of these pathogens have lymphocytic choriomeningitis virus, orthopox virus,
not yet been reported in Vietnam. This study shows that Leptospira spp., Borrelia spp., Rickettsia spp., Bartonel-
there is a higher risk of infection by Bartonella, Lepto- la spp., C. burnetii, and Toxoplasma gondii in rodents in
spira and Rickettsia from rodents in northern Vietnam. Austria, reported double and triple infection rates of only
This may be due to differences in natural conditions and 6.4% and 1.8%30.
the composition of the fauna of north and south of Viet- Herein, our observations indicate that rodents in
nam. The climate of southern Vietnam is typically tropi- northern Vietnam, particularly in Ha Giang and Cao Bang
cal, while in the northern part of the country the climate is provinces, may host multiple zoonotic pathogens such as
warm monsoon similar to that of the southern coastal re- Leptospira, Rickettsia, including Rickettsia SFG and R.
gions of China. The rodents’ fauna also varies significant- typhi, and Bartonella. Therefore, exposure to rodents con-
ly, where the Indochinese fauna complex is widespread in tributes to an increased risk of zoonotic disease infection
the south, and the oriental fauna dominates in the north- transmission from animals to humans.
ern regions. Till date there are no special studies on the
prevalence of pathogens among the faunal geographical CONCLUSION
complexes of rodents in the region. In our study, 31.6% of
rodents were positive for Bartonella (mostly among rats). In summary, we collected 133 rodents and small ani-
If we compare this with the Bartonella infection rate for mals from three provinces of northern Vietnam: Ha Giang,
rats in southern Vietnam (14.9%), the level of infection is Cao Bang and Lao Cai. Three common zoonotic diseases
approximately two times lower than that of our study14. (Rickettsia, Leptospira, and Bartonella) were found in
Conversely, in southern Vietnam, a higher level of Bar- Vietnam, and multiple infections of these pathogens were
tonella infection was found in bats (35%)13, which were also reported. Among the three investigated pathogens,
not evaluated in our study. Bartonella had the highest infection rate and was primar-
Of the 42 samples positive for Bartonella in this study, ily found in Ha Giang and Lao Cai provinces. Thus, our
25 were collected in Ha Giang province, 6 were collected data indicate that synanthropic and wild rodents are the
in Lao Cai province, and 11 were collected in Cao Bang main reservoirs of zoonotic diseases in northern Vietnam.
province. Thus, all three investigated areas showed a high Further studies on these pathogens in nature and among
prevalence of Bartonella in rodents, particularly Lao Cai the local people living in these areas should be performed.
province. Although only eight samples were collected in
Lao Cai province, six of the eight (75%) were positive for Conflict of interest: None
Bartonella, with two (25%) showing dual infection with
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Correspondence to: Le Thi Lan Anh, Joint Russian–Vietnamese Tropical Research and Technological Centre, No. 63, Nguyen Van Huyen,
Nghia Do, Cau Giay, Hanoi, Vietnam.
Email: leanhbio@gmail.com

Revceived: 03 September 2019 Accepted in revised form: 16 January 2020

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