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Table of Contents
Year : 2021  |  Volume : 58  |  Issue : 1  |  Page : 47-53

Investigation of multiple infections with zoonotic pathogens of rodents in northern Vietnam

1 Joint Russian-Vietnamese Tropical Research and Technological Centre, Cau Giay, Hanoi, Vietnam
2 Joint Russian-Vietnamese Tropical Research and Technological Centre, Cau Giay, Hanoi, Vietnam; A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russia
3 National Institute of Malariology, Parasitology and Entomology, Nam Tu Liem, Hanoi, Vietnam

Date of Submission03-Sep-2019
Date of Acceptance16-Jan-2020
Date of Web Publication18-Nov-2021

Correspondence Address:
Le Thi Lan Anh
Joint Russian–Vietnamese Tropical Research and Technological Centre, No. 63, Nguyen Van Huyen, Nghia Do, Cau Giay, Hanoi
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0972-9062.321750

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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 Bartonella 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 infection 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.

Keywords: zoonotic diseases; Rickettsia; Leptospira; Bartonella; natural foci diseases; Indochina

How to cite this article:
Anh LT, Balakirev AE, Chau NV. Investigation of multiple infections with zoonotic pathogens of rodents in northern Vietnam. J Vector Borne Dis 2021;58:47-53

How to cite this URL:
Anh LT, Balakirev AE, Chau NV. Investigation of multiple infections with zoonotic pathogens of rodents in northern Vietnam. J Vector Borne Dis [serial online] 2021 [cited 2021 Nov 27];58:47-53. Available from: https://www.jvbd.org/text.asp?2021/58/1/47/321750

  Introduction Top

Zoonotic disease refers to diseases that are transmitted from animals to humans. Approximately 60% of all human infectious disease agents are zoonotic diseases by origin[1], and the most important reservoir species for these diseases include rodents[2] and some other wild mammals. Four of the most important tropical transmission zoonotic diseases in the world are caused by Rickettsia, Leptospira, Bartonella and Borrelia species. Rickettsial infections represent a major source of non-malarial febrile illnesses among residents of Southeast Asia and returning travellers from that region[3].

Rickettsioses are zoonotic infections transmitted to humans via the bites of infected ticks, fleas, mites, and lice[4]. In Vietnam, a low sero-prevalence of Rickettsia has been reported[4]; however, rickettsial DNA has been found in ticks[5] and rodents[6]. Leptospirosis, one of the important zoonotic pathogens that can be transmitted to humans through rodents[7] via cuts in the skin or by drinking leptospirosis-contaminated water, was first reported in 1930. The infection is believed to be endemic to Vietnam and other neighbouring countries such as Laos, Cambodia and Thailand, with seasonal peaks of incidence during the rainy season and outbreaks related to flooding events[8]. Leptospirosis is also considered the most common cause of acute fever of unknown origin in Vietnam, besides with rickettsial fever[9].

Bartonella is transmitted from animal reservoirs (rats, mice, cats, dogs, and bats) to humans through ectoparasite vectors such as fleas, ticks and lice. Bartonella infection has been reported in parts of eastern Asia such as China, Japan, Korea, Far East of Russia, and Taiwan and in south central Asia (Afghanistan, Bangladesh, India, and Nepal) and Southeast Asia (Indonesia, Philippines, Singapore, and Thailand)[10]. Although no human cases of Bartonella spp. infection have been reported to date in Vietnam, Bartonella spp. have been identified in febrile humans elsewhere in Southeast Asia[11] and are commonly found in rats in southern Vietnam[12].

Because the three zoonotic pathogens of Rickettsia, Leptospira, and Bartonella share the same primary reservoirs (rodents and other wild animals), the presence of multiple co-infections of these diseases is assumed. In Vietnam, some data have been reported about Rickettsia, Leptospira and Bartonella mono-infection in rodents[5],[6],[12],[13],[14], but these findings are sparse and are primarily focused in southern Vietnam. Furthermore, co-infection was not investigated or specifically mentioned. In this study, we investigated rodents that were trapped in three provinces of northern Vietnam. The prevalence of Rickettsia, Leptospira and Bartonella and multiple infections of these pathogens were investigated using real-time PCR. Our survey helps identify and warn of the risk of infections with these pathogens in humans in Vietnam and for travellers visiting the country.

  Material & Methods Top

Study sites and animal sampling

This study was performed as a series of independent expeditions in 2010, 2013, 2014, and 2018 in three provinces of northern Vietnam: Ha Giang province [Vi Xuyen (in 2014 and 2018) and Quan Ba districts (in 2013) and Ha Giang and Meo Vac towns (in 2010, 2014), with 88 animals collected]; Cao Bang [Trung Khanh and Thong Nong districts (in 2013), with 37 animals collected]; and Lao Cai [Sa Pa district (in 2013), with eight animals collected]. In the Ha Giang and Lao Cai provinces, trapping was performed with the help of the local people. Up to 150 living traps were placed per day; the captured animals were collected and processed in the field laboratory. The animals’ populations and densities in the study area were not determined; the focus in catching many animals was to maximise the number of examined rodents. Thus, the main biotopes surveyed were places where garbage accumulated and synanthropic species were concentrated in territory along rivers and streams, in addition to on/near rice fields and vegetable gardens adjacent to settlements; to a lesser extent, natural habitats were surveyed. In Cao Bang province, trapping was performed directly by one of the authors (AEB, up to 50 living traps were placed per day) mainly in forest biotopes with a focus on the wild species community; several other species (mainly squirrels) were also captured in the neighbouring forests by local residents and were acquired for examination. We followed guidelines of the American Society of Mammalogists for standard operating procedures (SOP) with wild rodents during the collection and handling of the animals used in this survey[15]. The animals were amalgamated by chloroform and sacrificed by cervical dislocation, bodies were packed individually in white dense tissue bags to prevent ectoparasites spread; after what they were weighed, measured and preliminarily classified based on morphology followed by they were sampled for total DNA.

The kidneys and livers were collected and stored fresh at -80°C (for some of the Ha Giang samples) or preserved with 96% alcohol and stored at -20°C (for the remainder of the Ha Giang samples and the Lao Cai and Cao Bang samples) until processing.

Total DNA extraction

A total of 133 tissues (liver and kidney) were available for DNA extraction. Small pieces of liver or liver and kidney tissues were sampled in the field and stored in 96% alcohol for DNA extraction. Total genomic DNA was extracted using a routine phenol/chloroform/proteinase K protocol[16],[17]. The DNA was further purified either by a DNA Purification Kit (Fermentas, Thermo Fisher Scientific Inc., Pittsburgh, PA) or by direct ethanol precipitation.

Real-time PCR with SYBR green fluorescence detection was performed using a Rotor-Gene Q (Qiagen) thermocycler with SYBR Green PCR Master Mix (Applied Biosystems) with target-specific primers. The threshold at 10 times the standard deviation of the fluorescence value of the baseline was setup for positive samples separation. The samples reached threshold value by 40 cycles considered as positive, all suspected positive results appeared near 40 cycles (37–39) were run one times additionally and treated as true-positive only if result was confirmed. Appropriate positive and non-template controls were included in each PCR reactions set (pair per 10 samples investigated), and post-amplification melting-curve analysis was performed at the end of each run to confirm the specificity of the reaction and checking for primer-dimer artifacts. Absolute levels of target DNA were calculated from a standard curve established using the DNA standards.

Detection of Rickettsia spotted fever group, Rickettsia typhi and Bartonella spp.

Real-time PCR targeting OmpB, the hypothetical protein gene 01310, and ITS genes was used for the detection of Rickettsia spotted fever group (SFG), Rickettsia typhi and Bartonella spp., respectively (in-house real-time PCR kits were made by the Research Institute of Epidemiology of the Federal Service on Customers’ Rights Protection and Human Well-being Surveillance, Moscow, Russia).

Detection of Leptospira

The real-time PCR kit AmpliSens® Leptospira-FRT (InterLabService Ltd.) (Research Institute of Epidemiology of the Federal Service on Customers’ Rights Protection and Human Well-being Surveillance, Moscow, Russia) targeting the 16S rRNA was used to screen the DNA samples for all Leptospira spp.

Ethical statement

This study was approved by Ethical Committee coded IRB-VN02017 which is certificated by Ministry of Health of Vietnam

  Results Top

Sample identifications and taxonomy used

The animals obtained in the field from 2010 to 2014 were specifically investigated in the laboratory as museum materials; the prepared skulls were evaluated with a binocular microscope, and the animals were genotyped by the Cyt b or COI genes and BLAST was run in the Gen-Bank database; and taxonomical attribution was directly assessed and followed the most recent taxonomy[18] and species ranges[19],[20],[21] in Indochina. The species attribution of rodents trapped in 2018 in Ha Giang province was unfortunately examined based only on morphology without molecular genetic attribution[22]. This creates known problems with the correct species attribution. Currently, R. rattus (Linnaeus, 1758) proper does not inhabit Indochina; however, until recently, this incorrect taxonomic attribution was widely used in the medical literature in the region. In fact, no individuals bearing the R1 mitochondrial haplogroup haplotype (genetic label of this species) are currently recorded in the GeneBank database from anywhere in continental Indochina out of several hundreds of sequences stored. The rats morphologically similar to this haplotype were usually called ‘Rattus haplogroupe IV’ due to the lack of an appropriate taxonomic name; these rats belong to the R. rattus species group but are not identical to R. rattus proper or a few other members of this group of species[20],[23]. Thus, the name R. cf. rattus used in this paper should be recognised as a ‘member of the R. rattus species group’.

The 133 small mammals investigated included 114 rats, 15 squirrels,one tree shrew (Tupaia belangeri), two ferret-badgers (Melogale moschata), and one lemur (Lepilemur edwardsi); 26 different species were identified. As shown in [Table 1], the most abundant species in this study was Rattus tanezumi (33.1%, 44 of 133 rodents), followed by R. cf. rattus (12%, 16 of 133 rodents) and Niviventer fulvescens (9.8%, 13 of 133 rodents). The other 23 species were Rattus norvegicus, R. andamanensis, R. sp., N. fulvescens, N. mekongis, N. niviventer, N. cf. confucianus, N. lotipes, Berylmys bowersi, Leopoldamys revertens, Mus musculus, M. sp., Rhizomys sinensis, Neotetracus sinensis, Callosciurus erythraeus, C. inornatus, Dremomys rufigenis, Petaurista alborufus, Hylopetes sp., T. belangeri, Melogale sp., Neotetracus sinensis, and L. edwardsi, which each comprised between 0.8% and 6.0% of the samples.
Table 1: General list of animals investigated and pathogens detected

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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 comprised 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 for each species of P. alborufus, R. norvegicus, B. bowersi, L. revertens, B. savilei, D. rufigenis, and Hylopetes sp. In general, of the 33 samples positive for Rickettsia SFG and R. typhi, 23 samples were obtained from Ha Giang province, 8 samples were obtained from Cao Bang province, and two samples were obtained from Lao Cai province.

According to the data presented here, we can confidently argue that there is a significant level of infection with Rickettsia in synanthropic species (genera Rattus and Bandicota members). However, for several wild non-synanthropic species represented in our sample set by only a few or even single individuals (rats of the genera Niviventer, Leopoldamys and Berylmys and various species of squirrels, even flying squirrels), a higher level of infection was also noted, primarily by Rickettsia SFG strains. This suggests a wide distribution of natural foci of this infection, not only in the agro-cultural landscape but also in nature.

Multiple infection with Rickettsia, Leptospira and Bartonella in rodents

To determine the co-infection rate of Rickettsia, Leptospira and Bartonella in rodents collected in northern Vietnam, and the multiple co-infections of these three common tropical zoonotic diseases, our 133 rodent samples were examined by real-time PCR. The prevalence of Rickettsia, Leptospira spp., and Bartonella spp. individual, double and triple co-infections was investigated simultaneously. The results indicated that Bartonella spp. showed the highest prevalence (42 out of 133 rodents, 31.6%) in all the investigated areas, including Ha Giang, Cao Bang and Lao Cai provinces. Most of the positive Bartonella spp. samples (25/42) were collected in Ha Giang province, whereas six positive samples were found in Lao Cai province and 11 were obtained in Cao Bang province [Figure 1]. Interestingly, similar to Rickettsia species, the positive cases for Bartonella spp. were primarily found in four species: R. tanezumi, N. fulvescens, R. rattus, and B. savilei. Of the 44 R. tanezumi trapped in Ha Giang province, 13 were positive for Bartonella. Of the 13 trapped N. fulvescens rodents, six were positive for Bartonella. Additionally, 4/16 trapped R. rattus were Bartonella positive, and 4/5 B. savilei were positive for Bartonella [Table 1]. As noted above, three of the species, namely, representatives of the genera Rattus and Bandicota, belong to the synanthropic fauna; however, N. fulvescens is one of the most abundant ‘background species’ and is widely distributed in a variety of natural forest ecosystems in northern Vietnam.
Figure 1: Distribution of patogens by locations in northern Vietnam.

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The real-time PCR results for Leptospira spp. presented in [Table 1] indicated that 24 of 133 rodents (18%) were positive for Leptospira, which included 22 rodents collected in Ha Giang province and only two rodents trapped in Cao Bang province. These positive samples belong to seven genera: R. rattus (7/24), R. tanezumi (11/24), B. bowersi (2/24), B. savilei (1/24), N. fulvescens (1/24), R. nitidus (1/24), and C. erythraeus (1/24).

The result of screening for double infections indicated that approximately 18.8% (25/133) of the samples were positive for two of the three pathogens. Of these samples, dual infection with Rickettsia and Bartonella and with Leptospira and Bartonella was found in 40% (10/25), followed by dual infection with Rickettsia and Leptospira, accounting for 20% (5/25) [Table 2]. After analysing the host reservoirs in these dual infection cases, a higher rate of dual infection was found in three synanthropic species: R. tanezumi, followed by R. cf. rattus and B. savilei. However, three cases of Rickettsia and Bartonella dual infection were detected in N. fulvescens, and one case each was detected in C. inornatus and N. huang [Figure 2].
Figure 2: Multiple infections of Rickettsia, Leptospira and Bartonella and host reservoirs in northern Vietnam.

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Table 2: Detection of multiple infections in northern Vietnam rodents and small animals

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This pattern of distribution of cases of joint co-infestation between synanthropic and non-synanthropic species may indicate a specific distribution of Rickettsia and Bartonella foci among species of wild fauna in the natural environment. The lack of material available does not allow us to analyse this phenomenon in detail. Obviously, more profound and extensive research should be aimed at screening not only the synanthropic but also the wild forest fauna of small mammals in the region of Southeast Asia. This becomes even more relevant because of the customs of Vietnam, where various species of rats and squirrels are a common object of hunting for human food consumption. Therefore, it is likely that the number of direct contacts with rodents and the contribution of wild species to cases of human infection of the agents investigated here are much greater when compared with regions where there are no such traditions. Conversely, the widespread co-infection among synanthropic species is quite obvious.

One single triple infection (0.75%) of Rickettsia, Leptospira and Bartonella was found in R. cf. rattus that was trapped in Ha Giang province. After analysing the results of the 25 dual infection samples, 20 cases were 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 reservoirs for the spread of infections.

  Discussion Top

Although multiple co-infections of zoonotic pathogens 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 small mammals are the main host reservoirs of several zoonotic pathogens.

The prevalence of Bartonella in rodents and other small mammals varies significantly in East and Southeast Asia, and the distribution of zoonotic agents may vary between countries and between regions in one country. For example, prevalence values of 6% have been reported in Jakarta[24], 8.7%–41.5% in Thailand[25],[26], 10.3% in Taiwan[27], and 25.5% in Laos[28]. Our data for the Rickettsia and Leptospira infection rate showed that 24.8% (33 of 133 rodents) were positive for Rickettsia, of which 5.3% was R. typhi and 19.5% was Rickettsia SFG; additionally, 24 rodents (18.1%) were positive for Leptospira. Some studies on Rickettsia, Leptospira and Bartonella have been reported previously in Vietnam, but they were sparse and mostly focused on the southern part of the country[5],[6],[12],[13],[14]. Furthermore, multiple infections of these pathogens have not yet been reported in Vietnam. This study shows that there is a higher risk of infection by Bartonella, Leptospira and Rickettsia from rodents in northern Vietnam. This may be due to differences in natural conditions and the composition of the fauna of north and south of Vietnam. The climate of southern Vietnam is typically tropical, while in the northern part of the country the climate is warm monsoon similar to that of the southern coastal regions of China. The rodents’ fauna also varies significantly, where the Indochinese fauna complex is widespread in the south, and the oriental fauna dominates in the northern regions. Till date there are no special studies on the prevalence of pathogens among the faunal geographical complexes of rodents in the region. In our study, 31.6% of rodents were positive for Bartonella (mostly among rats). If we compare this with the Bartonella infection rate for rats in southern Vietnam (14.9%), the level of infection is approximately two times lower than that of our study[14]. Conversely, in southern Vietnam, a higher level of Bartonella infection was found in bats (35%)[13], which were not evaluated in our study.

Of the 42 samples positive for Bartonella in this study, 25 were collected in Ha Giang province, 6 were collected in Lao Cai province, and 11 were collected in Cao Bang province. Thus, all three investigated areas showed a high prevalence of Bartonella in rodents, particularly Lao Cai province. Although only eight samples were collected in Lao Cai province, six of the eight (75%) were positive for Bartonella, with two (25%) showing dual infection with Rickettsia and Bartonella. The investigation of multiple infections of Leptospira, Bartonella, and Rickettsia in rodents collected in northern Vietnam identified 25 (18.8%) cases of dual infection of the three investigated pathogens. The most frequent combinations of dual infection were found for Rickettsia and Bartonella (40%) and for Leptospira and Bartonella (40%), followed by Rickettsia and Leptospira (20%). Only one triple infection (0.75% of the rodent population screened) of Rickettsia, Leptospira and Bartonella was found in the house rat R. cf. rattus. A molecular survey of multiple infections of Borrelia, Rickettsia, Bartonella, Babesia, Ehrlichia, Anaplasma, Francisella tularensis and Coxiella burnetiid in rodents and small mammals in Croatia indicated comparable levels of infection, with 21.5% of rodents infected with Leptospira and 12% infected with Bartonella. The dual and triple infection rates were reported as 10.7% and 2.9%, respectively[29]. In Peru, there was a higher prevalence of Bartonella infection than of Leptospira in rodents[22]. Conversely, a study of multiple infections of zoonotic pathogens, including three different hantavirus species, lymphocytic choriomeningitis virus, orthopox virus, Leptospira spp., Borrelia spp., Rickettsia spp., Bartonella spp., C. burnetii, and Toxoplasma gondii in rodents in Austria, reported double and triple infection rates of only 6.4% and 1.8%[30].

Herein, our observations indicate that rodents in northern Vietnam, particularly in Ha Giang and Cao Bang provinces, may host multiple zoonotic pathogens such as Leptospira, Rickettsia, including Rickettsia SFG and R. typhi, and Bartonella. Therefore, exposure to rodents contributes to an increased risk of zoonotic disease infection transmission from animals to humans.

  Conclusion Top

In summary, we collected 133 rodents and small animals from three provinces of northern Vietnam: Ha Giang, Cao Bang and Lao Cai. Three common zoonotic diseases (Rickettsia, Leptospira, and Bartonella) were found in Vietnam, and multiple infections of these pathogens were also reported. Among the three investigated pathogens, Bartonella had the highest infection rate and was primarily found in Ha Giang and Lao Cai provinces. Thus, our data indicate that synanthropic and wild rodents are the main reservoirs of zoonotic diseases in northern Vietnam. Further studies on these pathogens in nature and among the local people living in these areas should be performed.

Conflict of interest: None

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  [Figure 1], [Figure 2]

  [Table 1], [Table 2]


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