Advertisement
  • Loading metrics

Leptospira infection in rats: A literature review of global prevalence and distribution

Leptospira infection in rats: A literature review of global prevalence and distribution

  • Kenneth Boey, 
  • Kanae Shiokawa, 
  • Sreekumari Rajeev
PLOS
x

Abstract

Background

The role of rodents in Leptospira epidemiology and transmission is well known worldwide. Rats are known to carry different pathogenic serovars of Leptospira spp. capable of causing disease in humans and animals. Wild rats (Rattus spp.), especially the Norway/brown rat (Rattus norvegicus) and the black rat (R. rattus), are the most important sources of Leptospira infection, as they are abundant in urban and peridomestic environments. In this study, we compiled and summarized available data in the literature on global prevalence of Leptospira exposure and infection in rats, as well as compared the global distribution of Leptospira spp. in rats with respect to prevalence, geographic location, method of detection, diversity of serogroups/serovars, and species of rat.

Methods

We conducted a thorough literature search using PubMed without restrictions on publication date as well as Google Scholar to manually search for other relevant articles. Abstracts were included if they described data pertaining to Leptospira spp. in rats (Rattus spp.) from any geographic region around the world, including reviews. The data extracted from the articles selected included the author(s), year of publication, geographic location, method(s) of detection used, species of rat(s), sample size, prevalence of Leptospira spp. (overall and within each rat species), and information on species, serogroups, and/or serovars of Leptospira spp. detected.

Findings

A thorough search on PubMed retrieved 303 titles. After screening the articles for duplicates and inclusion/exclusion criteria, as well as manual inclusion of relevant articles, 145 articles were included in this review. Leptospira prevalence in rats varied considerably based on geographic location, with some reporting zero prevalence in countries such as Madagascar, Tanzania, and the Faroe Islands, and others reporting as high as >80% prevalence in studies done in Brazil, India, and the Philippines. The top five countries that were reported based on number of articles include India (n = 13), Malaysia (n = 9), Brazil (n = 8), Thailand (n = 7), and France (n = 6). Methods of detecting or isolating Leptospira spp. also varied among studies. Studies among different Rattus species reported a higher Leptospira prevalence in R. norvegicus. The serovar Icterohaemorrhagiae was the most prevalent serovar reported in Rattus spp. worldwide. Additionally, this literature review provided evidence for Leptospira infection in laboratory rodent colonies within controlled environments, implicating the zoonotic potential to laboratory animal caretakers.

Conclusions

Reports on global distribution of Leptospira infection in rats varies widely, with considerably high prevalence reported in many countries. This literature review emphasizes the need for enhanced surveillance programs using standardized methods for assessing Leptospira exposure or infection in rats. This review also demonstrated several weaknesses to the current methods of reporting the prevalence of Leptospira spp. in rats worldwide. As such, this necessitates a call for standardized protocols for the testing and reporting of such studies, especially pertaining to the diagnostic methods used. A deeper understanding of the ecology and epidemiology of Leptospira spp. in rats in urban environments is warranted. It is also pertinent for rat control programs to be proposed in conjunction with increased efforts for public awareness and education regarding leptospirosis transmission and prevention.

Author summary

The role of rodents in the transmission of many diseases, including leptospirosis, is widely known. Rats abundant in urban and peridomestic environments are the most important reservoirs and sources of Leptospira infection in humans and animals. Leptospirosis is a significant but neglected disease of humans and animals that is increasing in incidence in regions affected by natural disasters. This paper summarizes the global prevalence and distribution of Leptospira infection in rats and will add to the literature that supports research, education, and public awareness regarding leptospirosis transmission and prevention.

Introduction

Leptospirosis is a major zoonotic disease worldwide, having significant impact on both human and animal health [1, 2]. It is known to be the most widespread zoonosis in the world [3], affecting an estimated 1.03 million people and causing 58,900 deaths annually [4]. Leptospirosis can also cause major economic losses in livestock industries because of abortions and stillbirths in farm animals [2]. The disease is caused by pathogenic spirochete bacteria of the genus Leptospira, which consists of 22 known species (pathogenic, intermediate, and saprophytic) and is divided into more than 300 serovars [5]. Recently, 12 novel species of Leptospira have been isolated from tropical soils, suggesting a highly unexplored biodiversity in the genus [6].

Not only is leptospirosis a public health issue in developing countries, it has become an urban health problem in developed and industrialized countries, occurring in unsanitary environments in cities during periods of seasonal rainfall and flooding [7]. Leptospirosis is also associated with natural disasters, with large outbreaks occurring after hurricanes, typhoons, and floods in tropical regions [8].

A wide variety of mammals can act as reservoirs of Leptospira, harboring pathogenic Leptospira spp. in their renal tubules and then shedding them through urine, thus contaminating the environment [1]. Humans and other animals may be exposed to Leptospira spp. by direct or indirect contact with infected animals or through the contaminated environment such as soil or water [1, 9]. Vertical transmission from mother to fetus or neonate through transplacental or transmammary transmission, respectively, as well as through sexual transmission within species, may also occur [2].

Wild rats (Rattus spp.), especially the Norway/brown rat (Rattus norvegicus) and the black rat (R. rattus), are abundant in urban and peridomestic environments and are the most important known sources of Leptospira infection [1, 10]. Rats are chronic asymptomatic carriers of Leptospira spp., maintaining the spirochetes in their proximal renal tubules [11, 12]. They have also been reported to carry different pathogenic serovars of Leptospira spp. capable of causing disease in humans and other animals [13].

In this study, we focused on compiling and reviewing available data in the literature on global prevalence of Leptospira exposure and infection in rats, as well as comparing the global distribution of Leptospira spp. in rats with respect to prevalence, geographic location, methods of detection, diversity of serogroups/serovars, and species of rats.

Methods

Literature search

To find studies describing Leptospira prevalence in rats worldwide, a thorough literature search was conducted using PubMed (https://www.ncbi.nlm.nih.gov/pubmed) with search terms including but not limited to “((Leptospira) OR (Leptospirosis)) AND (Rats) AND (Prevalence),” “((Leptospira) OR (Leptospirosis)) AND (Rattus) AND (Prevalence),” “((Leptospira) OR (Leptospirosis)) AND (Rats) AND (Seroprevalence),” “((Leptospira) OR (Leptospirosis)) AND (Rattus) AND (Seroprevalence),” “((Leptospira) OR (Leptospirosis)) AND (Rodents) AND (Prevalence),” and “((Leptospira) OR (Leptospirosis)) AND (Rodents) AND (Seroprevalence),” without restrictions on publication date. In addition, a search was performed using internet-based search engines such as Google and Google Scholar using similar search terms to manually search for other relevant articles.

Inclusion and exclusion criteria

Titles and abstracts were initially screened against the inclusion criteria to determine their suitability to be included in this review. Abstracts were included if they described data pertaining to Leptospira spp. in rats (Rattus spp.) from any geographic region around the world, including reviews. Abstracts were excluded if they did not describe the prevalence of Leptospira spp. in rats or if they did not describe naturally occurring Leptospira infection in the rats. The full text documents were then assessed against specific inclusion criteria. Publications in languages other than English were excluded; however, such articles with an English abstract were included if they contained relevant data for extraction.

Data extraction

We extracted data including the authors, year of publication, geographic location, and methods of detection used from the articles retrieved. We also extracted information on the species of rat(s), sample size, and prevalence (any kind including sero/molecular/culture/other prevalence) of Leptospira spp. (overall and within each rat species) and information on species, serogroups, and/or serovars of Leptospira spp. detected if available. For cases in which mice or other rodents were also included in the study, we extracted only specific data regarding rats from the Rattus genus. We used a data extraction form to record the relevant data.

Results

Literature search

The database search retrieved 303 articles. Of these, 114 were rejected as duplicates, and 36 articles were excluded, as they did not have any information about Leptospira spp. in rats. Additionally, 29 articles that did not describe prevalence of Leptospira spp. in rats were excluded. Twelve publications in languages other than English were also excluded. However, six foreign language articles with an English abstract containing relevant data were included. Three articles describing prevalence of Leptospira spp. in laboratory rats, as well as four articles describing cases of human leptospirosis due to transmission from pet rats, were excluded for the purpose of this review; however, they will be discussed separately in this paper. In addition, 11 relevant articles were manually included through general internet-based searches, and a further 25 articles that reported Leptospira prevalence in different types of rodents or small mammals but had data on rats of the Rattus genus were included. In total, 145 articles published up until June 2018 were included in this literature review. Publication references are listed in S1 List.

Including articles in foreign languages (157 total), five articles were published before 1950, eight in 1951–1959, six in 1960–1969, five in 1970–1979, eleven in 1980–1989, seven in 1990–1999, 32 in 2000–2009, and 83 in 2010–2018. Half of the number of articles in foreign languages (9/18) were published earlier in time, between 1949 and 1970. The number of studies investigating Leptospira spp. in rats generally increased throughout the years and increased significantly in the last decade.

Geographic distribution of Leptospira prevalence

The publications retrieved reported relevant data from a total of 62 geographical locations (Fig 1; S1 Map). Data such as prevalence ranges and number of studies retrieved per geographic location are provided in Tables 18, grouped according to geographical continents or regions. Detailed data on prevalence and serogroup/serovar information from each publication can be found in S1 Table.

thumbnail
Fig 1. Geographic distribution of all 145 publications included in the literature review.

Map template obtained from OpenStreetMap.

https://doi.org/10.1371/journal.pntd.0007499.g001

thumbnail
Table 7. Summary of Leptospira prevalence in rats in Central America and the Caribbean.

https://doi.org/10.1371/journal.pntd.0007499.t007

The top five countries that were reported based on number of articles include India (n = 13), Malaysia (n = 9), Brazil (n = 8), Thailand (n = 7), and France (n = 6). Prevalence of Leptospira spp. in rats varied considerably. For example, two studies in Australia reported a very low prevalence of 1.7% [16] and 2.9% [15], and studies in China [31] and Ecuador [153] reported a similar prevalence of 3.0%. Several studies even reported zero prevalence of Leptospira spp. in rats, such as in Thailand [71], Madagascar [86], Tanzania [92], and the Faroe Islands [98]. Conversely, other studies reported a prevalence of more than 70%, such as in Brazil [137139, 142, 145], Mexico [120], Egypt [82], Réunion [88], and the Philippines [58].

The prevalence reported from the same country had significant variations as well. For example, in Hawaii, four studies reported a prevalence of 16.0% [22], 24.4% [20], 30.2% [21], and 53.3% [19]. However, there were also instances in which independent studies from the same geographic location reported a similar prevalence, such as in Trinidad, with three studies which reported a prevalence of 16.5% [133], 17.4% [131], and 20.5% [19]. In Malaysia, of the seven articles retrieved, one reported a prevalence of 3.1% [51], whereas the rest had a similar prevalence between 8% and 18% [50, 5357].

Methods of detecting for Leptospira exposure or infection

A wide variety of diagnostic methods used were reported (Table 9). The most common diagnostic methods used were microscopic agglutination test (MAT), polymerase chain reaction (PCR), and culture and isolation. The majority of the studies (n = 90) used only one method of detection, either MAT, PCR, culture, or others.

thumbnail
Table 9. Distribution of methods of detecting Leptospira spp. used by all studies.

https://doi.org/10.1371/journal.pntd.0007499.t009

Within the methods of PCR and culture, studies used several types of tissues and body fluids for the detection of Leptospira spp., with the most common being kidney and urine samples. Other samples utilized include blood, milk, liver, spleen, brain, lung, breast, and urinary bladder samples (Table 10). PCR target genes also varied, and the list of genes and the corresponding number of studies that used them can be found in Table 11. S2 Table illustrates all relevant data pertaining to diagnostic methods used, including the reported prevalence of Leptospira spp. in rats based on each specific method of detection.

thumbnail
Table 10. Distribution of samples used by studies that performed culture and/or PCR.

https://doi.org/10.1371/journal.pntd.0007499.t010

Geographic distribution of serovars

A large number of serovars have been reported across all the studies retrieved, representing different geographic locations and continents. For each of those geographic locations, the serovars reported are listed in Tables 18. Studies conducted in Asia reported the highest number of different serovars detected (n = 30), followed by studies conducted in South America (n = 28). A comparison of serogroups and serovars detected in all represented countries can be found in S3 Table.

Interestingly, serovar Ballum has been reported in all represented countries in Oceania: Australia [16], Fiji [17], Hawaii [1922], New Caledonia [23], and New Zealand [13, 24, 25], with the exception of Wallis and Futuna [26], which did not provide serovar information.

In Asia, frequently reported serovars include Icterohaemorrhagiae (reported in eight countries), Autumnalis, Javanica (reported in six countries), Australis, Canicola, Pomona, and Pyrogenes (reported in five countries). The most reported serovar in the Middle East was Icterohaemorrhagiae (reported in four countries), whereas the most reported serovar in Africa was Canicola (reported in three countries). In Europe, serovars Icterohaemorrhagiae and Sejroë were the most frequently reported serovars, detected in eight and three countries, respectively. Serovar Icterohaemorrhagiae was also the most frequently detected in North America, South America, and the Caribbean. Several serovars of the Icterohaemorrhagiae serogroup have been frequently reported in the Caribbean, including serovars Copenhageni, Icterohaemorrhagiae, and Mankarso. The most frequently reported serovar worldwide was Icterohaemorrhagiae, detected in 36 of 43 countries that provided serovar information.

Prevalence of Leptospira spp. in various species of rats (Rattus spp.)

Among all rat species sampled in all studies, R. norvegicus and R. rattus were the two most frequently sampled species (Tables 18). Studies representing countries in Asia reported the most diverse species of rats sampled, with other species such as R. exulans and R. argentiventer in Cambodia, Malaysia, Thailand, Laos, and Vietnam; R. tanezumi in Cambodia, Laos, Thailand, and Vietnam; and R. losea in China, Cambodia, Laos, and Thailand (Table 2). Studies from Malaysia reported many other rat species that were not identified and sampled in other countries, such as R. diardii, R. bowersi, R. muelleri, R. rajah, R. sabanus, R. tiomanicus, and R. whiteheadi.

Overall, 30.3% (4,829/15,917) of R. norvegicus, 17.8% (2,376/13,353) of R. rattus, 10.9% (344/3,143) of R. exulans, 19.3% (87/451) of R. argentiventer, 3.4% (15/435) of R. tanezumi, and 13.1% (18/137) of R. losea were reported to be positive for Leptospira spp. In general, R. norvegicus was largely found to have a higher prevalence than R. rattus within the same studies. However, the opposite was also reported—i.e., the prevalence of Leptospira spp. in R. rattus was higher than R. norvegicus within the same studies. For example, on Réunion Island, one study reported a prevalence of 38.5% (214/562) in R. rattus, whereas R. norvegicus had a prevalence of 30.6% (52/170) [89]. The same was reported in New Zealand [13, 25], with R. rattus having higher prevalences (33.3%–34.4%) than R. norvegicus (25.7%–25.9%). The prevalence of Leptospira spp. in the various rat species still varied greatly among all the studies. Detailed information about Leptospira prevalence in each rat species per study can be found in S4 Table.

Other studies involving laboratory or pet rats

We also found three studies pertaining to natural Leptospira infection in laboratory albino rat (R. norvegicus) colonies. Overall, relatively high prevalences were reported and could be a good discussion point. The three articles reported prevalences of 67.0% [156] (part 1), 26.9% [156] (part 2), 90.0% [157], and about 68.0% [158]. This demonstrated that Leptospira infection could even be endemic in laboratory colonies within controlled environments, most likely primarily caused by either carrier adult rats [156, 158] or infection from wild rats [158]. Most of the infections were caused by serovar Icterohaemorrhagiae [156, 158], but other serovars were also reported, such as serovar Javanica [157].

In addition, four European articles reported cases of human leptospirosis associated with transmission from pet rats, which were not included in this review. Two articles published in 2008 reported one case in 2006 in the UK [159] and another case in Germany (year not specified) [160]. L. interrogans serogroup Icterohaemorrhagiae was identified in both cases. An article published in 2012 in the Czech language reported three human patients treated for leptospirosis from 2005 to 2010 in Czech Republic, with likelihood that they acquired the infection from their pet rats [161]. Another article published in 2017 identified six human leptospirosis cases from 2009 to 2016 in Belgium and France, for which pet rodents were the source of infection [162]. Of the six cases, three were identified to be caused by serogroup Icterohaemorrhagiae and one by serogroup Sejroë.

Discussion

With rapid global urbanization and 68% of the world’s human population projected to be living in urban areas by the year 2050 (55% as of 2018) [163], in addition to the increasing loss of natural habitats, it is anticipated that the majority of human–wildlife interactions would transpire in these areas. Wild rats seem to benefit from urbanization and thrive in urban and peridomestic environments, leading to frequent human exposure to these species [164]. R. norvegicus and R. rattus have become ubiquitous in urban environments and are significant sources of many zoonotic pathogens that can result in mortality and morbidity in humans and animals, and leptospirosis is one of those important rat-associated zoonoses. Because of knowledge gaps in the ecology of rats in urban environments, urban rat control is largely ineffective [165]; thus, it is critical to acquire a deeper understanding of the ecological and demographical drivers of zoonotic pathogen transmission in urban environments [164]. In addition, knowing the prevalence of a specific rat-associated zoonosis in a geographic region is essential in targeted pathogen screening in order to reduce underdiagnoses and misdiagnoses.

In a broad perspective, significant information has been documented in almost every country included in this literature review. However, the results reveal findings consistent with the common knowledge that incidence of leptospirosis is higher in tropical or warm-climate countries compared with countries in temperate regions. Of the top five countries represented in terms of number of articles, four of them are in tropical regions: India, Malaysia, Brazil, and Thailand. However, more studies representing tropical countries were retrieved compared with those from temperate regions. Many of the studies conducted also reported prevalences based on small sample sizes, which might not be indicative of the true distribution of Leptospira spp. in those geographic locations. This could be because of the convenience sampling of rats in conjunction with other rodents or animals; nevertheless, data pertaining to the rat samples were extracted for this review. In addition, the actual number of rats and population density in the wild may vary considerably among all geographic locations, which might indirectly affect the differences in prevalence of Leptospira spp. Differences in rat species predominating in a certain region may also potentially contribute to the differences in prevalence, in which further research is necessary for evaluation.

Several studies revealed zero prevalence of Leptospira spp. in the rats, which might be due to a number of possible reasons. For some of those studies, it could be simply due to the small sample size, with less than 50 rat samples obtained in studies in South Korea [61, 63], Thailand [71], Mayotte [19], Canada [116], Austria [94], and Hungary [94]. Another reason could be due to climatic conditions, which resulted in zero prevalence reported in a study in the Faroe Islands, to which they concluded that it could either be too cold for Leptospira transmission or too cold for the maintenance of adequate densities of rats [98]. An article from Madagascar reported a prevalence of 0% despite having a relatively decent sample size, and it concluded that Leptospira spp. was likely not present in Madagascar [86]. However, a more recent article reported a prevalence of 40.0% [85], which could indicate a relatively recent change in geographical distribution of Leptospira spp. in Madagascar or that the methodology used in the earlier study was not optimal. A study done in Tanzania revealed zero prevalence in 384 rodents (including 320 rats), which is a notable finding, considering the rodents were sampled in areas known to have a high incidence of human leptospirosis. This might indicate that peridomestic rodents are not a major source of human infection in that area [92].

Prevalences reported by studies from the same country also varied, which could be because of reasons such as differences in methodology or sampling from different parts of that country. As seen in the Results section, methods of detecting for Leptospira spp. varied greatly among all the studies retrieved, which may have certain implications on detection sensitivity. Some diagnostic methods such as PCR and other molecular methods detect Leptospira nucleic acids, whereas serological methods such as MAT detect anti-Leptospira antibodies, which only indicates exposure to the bacterium and not necessarily a current infection. Moreover, such serological techniques possess a risk of cross-reaction; thus, their results should be interpreted with caution. PCR protocols, in general, are used for detecting pathogenic Leptospira spp., and isolation of infecting Leptospira strains followed by cumbersome serological methods are required for identifying the serovars, which is not pursued in many studies reported. In culture methods with the usage of dark-field microscopy for identification of spirochetes, there may be possibilities of human error or issues regarding ambiguity of results as well, with possible false positives or negatives. In addition, varied tissue samples were used among the publications retrieved, and some studies used only one type of tissue sample, whereas others used multiple types of samples, pooled or unpooled. There are also different sensitivities and specificities for each of the various diagnostic methods. All these factors could affect the detection of Leptospira spp., which may have contributed to the varied prevalences observed.

The diversity of serovars detected varied considerably among studies and geographic regions. This review revealed that studies conducted in Asia and South America detected the highest number of different serovars, which could have been influenced by several factors. Methodologies in general could influence this, with different methods of serovar characterization being used among the studies. In seroprevalence studies that used MAT, serovars not included in the diagnostic panel would not be detected and, thus, affect the study results. With Asia and South America being tropical regions, there could be plausible correlations with the large variety of serovars present. Factors to be considered are the higher incidence of Leptospira spp. in tropical regions and the relatively higher number of studies retrieved from Asia and South America, which could provide higher serovar diversity.

Several possible correlations with regard to geographic distribution of infecting serovars could be observed. Serovar Ballum could be the main infecting serovar in rats in Oceania, with all studies that provided serovar information having identified the presence of serovar Ballum. Serovar Sejroë was reported in European countries more than countries from other regions. Interestingly, most of the studies conducted in the Caribbean concurrently identified several serovars of the Icterohaemorrhagiae serogroup (serovars Copenhageni, Icterohaemorrhagiae, and Mankarso) more frequently than studies in other geographic regions. Overall, serovar Icterohaemorrhagiae was the most frequently reported serovar, identified in almost all represented geographic locations. In countries that did not report serovar Icterohaemorrhagiae, certain methodological factors discussed earlier in this section could be the reason for the absence. For example, in Australia, despite retrieving three articles, only one provided serovar information. However, the extremely low prevalence (1.7%) reported in that article meant that the true variety of serovars present may have been underestimated.

Comparing the two most common rat species sampled, reported Leptospira prevalence was generally higher in R. norvegicus than R. rattus. This may suggest a possible correlation with the species of rats and susceptibility of Leptospira infection. However, many of the studies use morphological characteristics and general appearance to determine the exact rat species and, thus, may cause inaccurate reporting of results. For a number of studies, rat species were not determined and reported, which may have certain implications. As there are many other species of small mammals and rodents that resemble rats, they may not be of the genus Rattus and, therefore, are not considered “true” rats. The taxonomy of rats has also changed throughout the years, and rats that were once known to be under the Rattus genus may not be classified as one in the present day. Twleve species reported by studies have been identified to be potentially not of the Rattus genus or are subspecies of R. rattus (S5 Table) [166, 167]. If such small mammals and rodents were misidentified as rats of the Rattus genus and reported in studies, this could be another reason for inaccurate reporting of results. In addition, some studies also combined the results of all rodents sampled, including mice and other rodents, and did not provide separate data and results for each type of animal. This caused inconsistencies in extraction of data from those articles. For future studies, inclusion of all information such as exact species of rats and the individual prevalence of each of those species will lower the inconsistency.

Our review also identified relatively high prevalences of Leptospira spp. in laboratory rat colonies within controlled environments, indicating primary carrier status in laboratory rats or inadvertent transmission and spillover infection from wild rats. In addition to possible interference with biomedical research, one of the main implications of high Leptospira prevalence in laboratory rat colonies is the zoonotic potential to laboratory animal caretakers, as evidenced by Natrajaseenivasan and Ratnam [157], who reported a very high seropositivity (91.0%) in animal house workers.

Several cases of human leptospirosis associated with transmission from pet rats demonstrate that wild rats are not the only sources of rodent-associated human infection. With the rising popularity of keeping rats as household pets, there may be concerns about pet rats being a potential source of human Leptospira infection, and exposure to infected pet rats could pose a significant public health risk.

Conclusions and recommendations

This review summarizes the literature on global prevalence and distribution of Leptospira infection in rats. Prevalence of Leptospira spp. varies widely, with a considerably high prevalence reported in many countries involving multiple rat species. This review also demonstrated several weaknesses to the current methods of detecting and documenting Leptospira prevalence in rats worldwide. As such, this necessitates a call for standardized protocols for the detection and reporting of such studies, especially pertaining to the diagnostic methods used. In addition, appropriate quality control programs using standardized region-specific diagnostic panels, as well as improvements in techniques for serovar differentiation, could be proposed. A deeper understanding of the ecology and epidemiology of Leptospira spp. in rats in urban environments is warranted. It is also pertinent for rat control programs to be implemented in conjunction with increased efforts for public awareness and education regarding leptospirosis transmission and prevention.

Key learning points

  • Prevalence of Leptospira infection in rats varies widely, with a considerably high prevalence reported in many countries involving multiple rat species.
  • Leptospira prevalence in rats is higher in geographical regions with tropical climates compared with regions with temperate climates.
  • Serovar Icterohaemorrhagiae is the most prevalent serovar reported in rats.
  • Weaknesses to the current methods of detecting and documenting Leptospira prevalence in rats necessitates a call for standardized protocols for reporting in such studies.
  • It is pertinent for rat control programs to be implemented in conjunction with increased efforts for public awareness and education regarding leptospirosis transmission and prevention.

Top five papers

  1. Desvars A, Cardinale E, Michault A. Animal leptospirosis in small tropical areas. Epidemiol Infect. 2011;139(2):167–88. Epub 2010/09/30. doi: 10.1017/S0950268810002074. PubMed PMID: 20875197.
  2. Hathaway SC, Blackmore DK. Ecological aspects of the epidemiology of infection with leptospires of the Ballum serogroup in the black rat (Rattus rattus) and the brown rat (Rattus norvegicus) in New Zealand. J Hyg (Lond). 1981;87(3):427–36. Epub 1981/12/01. PubMed PMID: 7310125; PubMed Central PMCID: PMCPMC2134120.
  3. de Faria MT, Calderwood MS, Athanazio DA, McBride AJ, Hartskeerl RA, Pereira MM, et al. Carriage of Leptospira interrogans among domestic rats from an urban setting highly endemic for leptospirosis in Brazil. Acta Trop. 2008;108(1):1–5. Epub 2008/08/30. doi: 10.1016/j.actatropica.2008.07.005. PubMed PMID: 18721789; PubMed Central PMCID: PMCPMC2596941.
  4. Himsworth CG, Jardine CM, Parsons KL, Feng AYT, Patrick DM. The Characteristics of Wild Rat (Rattus spp.) Populations from an Inner-City Neighborhood with a Focus on Factors Critical to the Understanding of Rat-Associated Zoonoses. PLoS ONE. 2014;9(3):e91654. doi: 10.1371/journal.pone.0091654.
  5. Ellis WA. Animal Leptospirosis. In: Adler B, editor. Leptospira and Leptospirosis. Berlin, Heidelberg: Springer Berlin Heidelberg; 2015. p. 99–137.

Supporting information

S1 Table. Summary of global Leptospira prevalence and serovar distribution.

https://doi.org/10.1371/journal.pntd.0007499.s001

(XLSX)

S2 Table. Summary of Leptospira prevalence by detection methods.

https://doi.org/10.1371/journal.pntd.0007499.s002

(XLSX)

S3 Table. Distribution of Leptospira serovars reported, sorted by continents.

https://doi.org/10.1371/journal.pntd.0007499.s003

(XLSX)

S4 Table. Summary of Leptospira prevalence by species of rats.

https://doi.org/10.1371/journal.pntd.0007499.s004

(XLSX)

S5 Table. Taxonomic synonymy of rat species reported in studies.

https://doi.org/10.1371/journal.pntd.0007499.s005

(DOCX)

S1 List. List of all 145 publications included in the literature review.

https://doi.org/10.1371/journal.pntd.0007499.s006

(DOCX)

S1 Map. Interactive map of the geographic distribution of all publications included in the literature review.

https://doi.org/10.1371/journal.pntd.0007499.s007

(HTML)

Acknowledgments

The authors would like to thank Grace Carr Benjamin and Ermine Cotton of the Stanley Mark Dennis Veterinary Library at Ross University School of Veterinary Medicine (St. Kitts, West Indies) for their assistance in the retrieval of full text articles for this study.

References

  1. 1. Haake DA, Levett PN. Leptospirosis in humans. Current topics in microbiology and immunology. 2015;387:65–97. Epub 2014/11/13. pmid:25388133.
  2. 2. Ellis WA. Animal Leptospirosis. In: Adler B, editor. Leptospira and Leptospirosis. Berlin, Heidelberg: Springer Berlin Heidelberg; 2015. p. 99–137.
  3. 3. Levett PN. Leptospirosis. Clinical microbiology reviews. 2001;14(2):296–326. Epub 2001/04/09. pmid:11292640.
  4. 4. Costa F, Hagan JE, Calcagno J, Kane M, Torgerson P, Martinez-Silveira MS, et al. Global Morbidity and Mortality of Leptospirosis: A Systematic Review. PLoS Negl Trop Dis. 2015;9(9):e0003898. Epub 2015/09/18. pmid:26379143.
  5. 5. Picardeau M. Virulence of the zoonotic agent of leptospirosis: still terra incognita? Nature reviews Microbiology. 2017;15(5):297–307. Epub 2017/03/07. pmid:28260786.
  6. 6. Thibeaux R, Iraola G, Ferres I, Bierque E, Girault D, Soupe-Gilbert ME, et al. Deciphering the unexplored Leptospira diversity from soils uncovers genomic evolution to virulence. Microbial genomics. 2018;4(1). Epub 2018/01/10. pmid:29310748.
  7. 7. Socolovschi C, Angelakis E, Renvoise A, Fournier PE, Marie JL, Davoust B, et al. Strikes, flooding, rats, and leptospirosis in Marseille, France. Int J Infect Dis. 2011;15(10):e710–5. Epub 2011/07/20. pmid:21767971.
  8. 8. Koizumi N, Muto M, Tanikawa T, Mizutani H, Sohmura Y, Hayashi E, et al. Human leptospirosis cases and the prevalence of rats harbouring Leptospira interrogans in urban areas of Tokyo, Japan. J Med Microbiol. 2009;58(Pt 9):1227–30. Epub 2009/06/17. pmid:19528143.
  9. 9. Murray GL. The molecular basis of leptospiral pathogenesis. Current topics in microbiology and immunology. 2015;387:139–85. Epub 2014/11/13. pmid:25388135.
  10. 10. Himsworth CG, Jardine CM, Parsons KL, Feng AYT, Patrick DM. The Characteristics of Wild Rat (Rattus spp.) Populations from an Inner-City Neighborhood with a Focus on Factors Critical to the Understanding of Rat-Associated Zoonoses. PLoS ONE. 2014;9(3):e91654. pmid:24646877
  11. 11. Sterling CR, Thiermann AB. Urban rats as chronic carriers of leptospirosis: an ultrastructural investigation. Vet Pathol. 1981;18(5):628–37. Epub 1981/09/01. pmid:7281461.
  12. 12. Thiermann AB. The Norway rat as a selective chronic carrier of Leptospira icterohaemorrhagiae. J Wildl Dis. 1981;17(1):39–43. Epub 1981/01/01. pmid:7253100.
  13. 13. Hathaway SC, Blackmore DK. Ecological aspects of the epidemiology of infection with leptospires of the Ballum serogroup in the black rat (Rattus rattus) and the brown rat (Rattus norvegicus) in New Zealand. J Hyg (Lond). 1981;87(3):427–36. Epub 1981/12/01. pmid:7310125.
  14. 14. Chakma S, Picard J, Duffy R, Constantinoiu C, Gummow B. A Survey of Zoonotic Pathogens Carried by Non-Indigenous Rodents at the Interface of the Wet Tropics of North Queensland, Australia. Transbound Emerg Dis. 2017;64(1):185–93. Epub 2015/04/25. pmid:25906923.
  15. 15. Dybing NA, Jacobson C, Irwin P, Algar D, Adams PJ. Leptospira Species in Feral Cats and Black Rats from Western Australia and Christmas Island. Vector Borne Zoonotic Dis. 2017;17(5):319–24. Epub 2017/04/25. pmid:28437186.
  16. 16. Milner AR, Wilks CR, Spratt DM, Presidente PJ. The prevalence of anti-leptospiral agglutinins in sera of wildlife in southeastern Australia. J Wildl Dis. 1981;17(2):197–202. Epub 1981/04/01. pmid:7241704.
  17. 17. Collings DF. Leptospira interrogans infection in domestic and wild animals in Fiji. N Z Vet J. 1984;32(3):21–4. Epub 1984/03/01. pmid:16031033.
  18. 18. Guernier V, Richard V, Nhan T, Rouault E, Tessier A, Musso D. Leptospira diversity in animals and humans in Tahiti, French Polynesia. PLoS Negl Trop Dis. 2017;11(6):e0005676. Epub 2017/06/29. pmid:28658269.
  19. 19. Desvars A, Cardinale E, Michault A. Animal leptospirosis in small tropical areas. Epidemiol Infect. 2011;139(2):167–88. Epub 2010/09/30. pmid:20875197.
  20. 20. Higa HH, Fujinaka IT. Prevalence of rodent and mongoose leptospirosis on the Island of Oahu. Public Health Rep. 1976;91(2):171–7. Epub 1976/03/01. pmid:822470.
  21. 21. Shimizu MM. Environmental and biological determinants for the prevalence of leptospirosis among wild small mammal hosts, island of Hawaii. Int J Zoonoses. 1984;11(2):173–88. Epub 1984/12/01. pmid:6534904.
  22. 22. Wong M, Katz AR, Li D, Wilcox BA. Leptospira infection prevalence in small mammal host populations on three Hawaiian islands. Am J Trop Med Hyg. 2012;87(2):337–41. Epub 2012/08/03. pmid:22855767.
  23. 23. Perez J, Brescia F, Becam J, Mauron C, Goarant C. Rodent abundance dynamics and leptospirosis carriage in an area of hyper-endemicity in New Caledonia. PLoS Negl Trop Dis. 2011;5(10):e1361. Epub 2011/11/01. pmid:22039557.
  24. 24. Carter ME, Cordes DO. Leptospirosis and other infections of Rattus rattus and Rattus norvegicus. N Z Vet J. 1980;28(3):45–50. Epub 1980/03/01. pmid:6930057.
  25. 25. Hathaway SC, Blackmore DK, Marshall RB. Leptospirosis in free-living species in New Zealand. J Wildl Dis. 1981;17(4):489–96. Epub 1981/10/01. pmid:7338970.
  26. 26. Theuerkauf J, Perez J, Taugamoa A, Niutoua I, Labrousse D, Gula R, et al. Leptospirosis risk increases with changes in species composition of rat populations. Naturwissenschaften. 2013;100(4):385–8. Epub 2013/03/29. pmid:23535996.
  27. 27. Ivanova S, Herbreteau V, Blasdell K, Chaval Y, Buchy P, Guillard B, et al. Leptospira and rodents in Cambodia: environmental determinants of infection. Am J Trop Med Hyg. 2012;86(6):1032–8. Epub 2012/06/06. pmid:22665613.
  28. 28. Kudo Y, Vansith K, Rin E, Uchida K, Kodama S, Fukui T, et al. Molecular Epidemiological Survey of Leptospira Infection of Wild Rodents in the Urban Settlement of Cambodia. Vector Borne Zoonotic Dis. 2018;18(3):144–50. Epub 2018/03/02. pmid:29494314.
  29. 29. Li S, Wang D, Zhang C, Wei X, Tian K, Li X, et al. Source tracking of human leptospirosis: serotyping and genotyping of Leptospira isolated from rodents in the epidemic area of Guizhou province, China. BMC microbiology. 2013;13:75. Epub 2013/04/04. pmid:23548108.
  30. 30. Yalin W, Lingbing Z, Hongliang Y, Jianmin X, Xiangyan Z, Xiaokui G, et al. High prevalence of pathogenic Leptospira in wild and domesticated animals in an endemic area of China. Asian Pac J Trop Med. 2011;4(11):841–5. Epub 2011/11/15. pmid:22078943.
  31. 31. Zhou J, Huang X, He H, Zhang X, Liu A, Yang T, et al. Epidemiological study on leptospirosa infection of host animals and healthy population in flood areas. Zhong Nan Da Xue Xue Bao Yi Xue Ban. 2009;34(2):99–103. Epub 2009/03/10. pmid:19270347.
  32. 32. Bojiraj M, Porteen K, Gunaseelan L, Sureshkannan S. Seroprevalence of Leptospirosis in Animals and Its Public Health Significance. Int J Livest Res. 2017;7(11):220–6.
  33. 33. Gangadhar NL, Rajasekhar M, Smythe LD, Norris MA, Symonds ML, Dohnt MF. Reservoir hosts of Leptospira inadai in India. Rev Sci Tech. 2000;19(3):793–9. Epub 2000/01/11. pmid:11107622.
  34. 34. Koteeswaran A. Seroprevalence of leptospirosis in man and animals in Tamilnadu. Indian J Med Microbiol. 2006;24(4):329–31. Epub 2006/12/23. pmid:17185869.
  35. 35. Kuriakose M, Paul R, Joseph MR, Sugathan S, Sudha TN. Leptospirosis in a midland rural area of Kerala State. Indian J Med Res. 2008;128(3):307–12. Epub 2008/12/05. pmid:19052343.
  36. 36. Lahiri MN. Studies on Leptospira Icterohaemorrhagiae in Rats in Bombay City. Ind Med Gaz. 1941;76(9):536–8. Epub 1941/09/01. pmid:29013710.
  37. 37. Natarajaseenivasan K, Boopalan M, Selvanayaki K, Suresh SR, Ratnam S. Leptospirosis among rice mill workers of Salem, South India. Jpn J Infect Dis. 2002;55(5):170–3. Epub 2002/12/27. pmid:12501258.
  38. 38. Natarajaseenivasan K, Vedhagiri K, Sivabalan V, Prabagaran SG, Sukumar S, Artiushin SC, et al. Seroprevalence of Leptospira borgpetersenii serovar javanica infection among dairy cattle, rats and humans in the Cauvery river valley of southern India. Southeast Asian J Trop Med Public Health. 2011;42(3):679–86. Epub 2011/06/29. pmid:21706947.
  39. 39. Parveen SM, Suganyaa B, Sathya MS, Margreat AA, Sivasankari K, Shanmughapriya S, et al. Leptospirosis Seroprevalence Among Blue Metal Mine Workers of Tamil Nadu, India. Am J Trop Med Hyg. 2016;95(1):38–42. Epub 2016/04/06. pmid:27044567.
  40. 40. Patil D, Dahake R, Roy S, Mukherjee S, Chowdhary A, Deshmukh R. Prevalence of leptospirosis among dogs and rodents and their possible role in human leptospirosis from Mumbai, India. Indian J Med Microbiol. 2014;32(1):64–7. Epub 2014/01/09. pmid:24399392.
  41. 41. Priya CG, Hoogendijk KT, Berg M, Rathinam SR, Ahmed A, Muthukkaruppan VR, et al. Field rats form a major infection source of leptospirosis in and around Madurai, India. J Postgrad Med. 2007;53(4):236–40. Epub 2007/12/22. pmid:18097111.
  42. 42. Sharma S, Vijayachari P, Sugunan AP, Sehgal SC. Leptospiral carrier state and seroprevalence among animal population—a cross-sectional sample survey in Andaman and Nicobar Islands. Epidemiol Infect. 2003;131(2):985–9. Epub 2003/11/05. pmid:14596541.
  43. 43. Vedhagiri K, Natarajaseenivasan K, Prabhakaran SG, Selvin J, Narayanan R, Shouche YS, et al. Characterization of leptospira borgpetersenii isolates from field rats (rattus norvegicus) by 16s rrna and lipl32 gene sequencing. Braz J Microbiol. 2010;41(1):150–7. Epub 2010/01/01. pmid:24031475.
  44. 44. Vimala G, Rani AM, Gopal VR. Leptospirosis in vellore: a clinical and serological study. Int J Microbiol. 2014;2014:643940. Epub 2014/07/23. pmid:25050124.
  45. 45. Sumanta H, Wibawa T, Hadisusanto S, Nuryati A, Kusnanto H. Genetic variation of Leptospira isolated from rats catched in Yogyakarta Indonesia. Asian Pac J Trop Med. 2015;8(9):710–3. Epub 2015/10/05. pmid:26433655.
  46. 46. Kawabata H, Sakakibara S, Imai Y, Masuzawa T, Fujita H, Tsurumi M, et al. First record of Leptospira borgpetersenii isolation in the Amami Islands, Japan. Microbiol Immunol. 2006;50(6):429–34. Epub 2006/06/21. pmid:16785714.
  47. 47. Kobayashi Y, Kusaba T, Ueki R. Isolation of Leptospira javanica from rats on Ishigaki Island. Am J Trop Med Hyg. 1972;21(3):342–4. Epub 1972/05/01. pmid:5025619.
  48. 48. Saito M, Villanueva SY, Masuzawa T, Haraguchi Y, Ita S, Miyahara S, et al. The usefulness of semi-solid medium in the isolation of highly virulent Leptospira strains from wild rats in an urban area of Fukuoka, Japan. Microbiol Immunol. 2015;59(6):322–30. Epub 2015/04/22. pmid:25890990.
  49. 49. Benacer D, Mohd Zain SN, Amran F, Galloway RL, Thong KL. Isolation and molecular characterization of Leptospira interrogans and Leptospira borgpetersenii isolates from the urban rat populations of Kuala Lumpur, Malaysia. Am J Trop Med Hyg. 2013;88(4):704–9. Epub 2013/01/30. pmid:23358635.
  50. 50. Benacer D, Mohd Zain SN, Sim SZ, Mohd Khalid MK, Galloway RL, Souris M, et al. Determination of Leptospira borgpetersenii serovar Javanica and Leptospira interrogans serovar Bataviae as the persistent Leptospira serovars circulating in the urban rat populations in Peninsular Malaysia. Parasit Vectors. 2016;9:117. pmid:26927873
  51. 51. Khairani-Bejo S, Oii SS, Bahaman AR. Rats: Leptospirosis Reservoir in Serdang Selangor Residential Area. Journal of Animal and Veterinary Advances. 2004;3(2):66–9.
  52. 52. Latifah I, Rahmat MS, Hayarti KB, Paramasvaran S, Azizah MR, Imran F, et al. Prevalence of leptospiral DNA among wild rodents from a selected area in Beguk Dam Labis, Segamat, Johor, Malaysia. Malays J Pathol. 2012;34(2):157–9. Epub 2013/02/22. pmid:23424779.
  53. 53. Latifah I, Abdul Halim A, Rahmat MS, Nadia MF, Ubil ZE, Asmah H, et al. Isolation by culture and PCR identification of LipL32 gene of pathogenic Leptospira spp. in wild rats of Kuala Lumpur. Malays J Pathol. 2017;39(2):161–6. Epub 2017/09/04. pmid:28866698.
  54. 54. Mohamed-Hassan SN, Bahaman AR, Mutalib AR, Khairani-Bejo S. Serological prevalence of leptospiral infection in wild rats at the National Service Training Centres in Kelantan and Terengganu. Trop Biomed. 2010;27(1):30–2. Epub 2010/06/22. pmid:20562810.
  55. 55. Mohamed-Hassan SN, Bahaman AR, Mutalib AR, Khairani-Bejo S. Prevalence of Leptospires in rats from selected locations in Peninsular Malaysia. Research Journal of Animal Sciences. 2012;6(1):12–25.
  56. 56. Pui CF, Bilung LM, Apun K, Su’ut L. Diversity of Leptospira spp. in Rats and Environment from Urban Areas of Sarawak, Malaysia. J Trop Med. 2017;2017:3760674. Epub 2017/03/30. pmid:28348601.
  57. 57. Smith CE, Turner LH, Harrison JL, Broom JC. Animal leptospirosis in Malaya: 3. Incidence in rats by sex, weight and age. Bull World Health Organ. 1961;24(6):807–16. Epub 1961/01/01. pmid:20604093.
  58. 58. Villanueva SY, Ezoe H, Baterna RA, Yanagihara Y, Muto M, Koizumi N, et al. Serologic and molecular studies of Leptospira and leptospirosis among rats in the Philippines. Am J Trop Med Hyg. 2010;82(5):889–98. Epub 2010/05/05. pmid:20439972.
  59. 59. Villanueva MA, Mingala CN, Gloriani NG, Yanagihara Y, Isoda N, Nakajima C, et al. Serological investigation of Leptospira infection and its circulation in one intensive-type water buffalo farm in the Philippines. Jpn J Vet Res. 2016;64(1):15–24. Epub 2016/06/29. pmid:27348885.
  60. 60. Kim HC, Klein TA, Chong ST, Collier BW, Usa M, Yi SC, et al. Seroepidemiological survey of rodents collected at a U.S. military installation, Yongsan Garrison, Seoul, Republic of Korea. Mil Med. 2007;172(7):759–64. Epub 2007/08/19. pmid:17691691.
  61. 61. O’Guinn ML, Klein TA, Lee JS, Richards AL, Kim HC, Ha SJ, et al. Serological surveillance of scrub typhus, murine typhus, and leptospirosis in small mammals captured at firing points 10 and 60, Gyeonggi province, Republic of Korea, 2001–2005. Vector Borne Zoonotic Dis. 2010;10(2):125–33. Epub 2009/05/01. pmid:19402761.
  62. 62. Rim BM, Rim CW, Chang WH, Kakoma I. Leptospirosis serology in Korean wild animals. J Wildl Dis. 1993;29(4):602–3. Epub 1993/10/01. pmid:8258863.
  63. 63. Sames WJ, Klein TA, Kim HC, Gu SH, Kang HJ, Shim SH, et al. Serological surveillance of scrub typhus, murine typhus, and leptospirosis in small mammals captured at Twin Bridges Training Area, Gyeonggi Province, Republic of Korea, 2005–2007. Mil Med. 2010;175(1):48–54. Epub 2010/01/30. pmid:20108842.
  64. 64. Denipitiya DT, Chandrasekharan NV, Abeyewickreme W, Hartskeerl RA, Hapugoda MD. Identification of cattle, buffaloes and rodents as reservoir animals of Leptospira in the District of Gampaha, Sri Lanka. BMC Res Notes. 2017;10(1):134. Epub 2017/03/24. pmid:28330498.
  65. 65. Gamage CD, Koizumi N, Muto M, Nwafor-Okoli C, Kurukurusuriya S, Rajapakse JR, et al. Prevalence and carrier status of leptospirosis in smallholder dairy cattle and peridomestic rodents in Kandy, Sri Lanka. Vector Borne Zoonotic Dis. 2011;11(8):1041–7. Epub 2011/02/03. pmid:21284522.
  66. 66. Della Rossa P, Tantrakarnapa K, Sutdan D, Kasetsinsombat K, Cosson JF, Supputamongkol Y, et al. Environmental factors and public health policy associated with human and rodent infection by leptospirosis: a land cover-based study in Nan province, Thailand. Epidemiol Infect. 2016;144(7):1550–62. Epub 2015/11/27. pmid:26607833.
  67. 67. Doungchawee G, Phulsuksombat D, Naigowit P, Khoaprasert Y, Sangjun N, Kongtim S, et al. Survey of leptospirosis of small mammals in Thailand. Southeast Asian J Trop Med Public Health. 2005;36:1516–1522. pmid:16610655
  68. 68. Jittimanee J, Wongbutdee J. Survey of pathogenic Leptospira in rats by polymerase chain reaction in Sisaket Province. J Med Assoc Thai. 2014;97 Suppl 4:S20–4. Epub 2014/05/24. pmid:24851560.
  69. 69. Kositanont U, Naigowit P, Imvithaya A, Singchai C, Puthavathana P. Prevalence of antibodies to Leptospira serovars in rodents and shrews trapped in low and high endemic areas in Thailand. J Med Assoc Thai. 2003;86(2):136–42. Epub 2003/04/08. pmid:12678151.
  70. 70. Wangroongsarb P, Saengsongkong W, Petkanjanapong W, Mimgratok M, Panjai D, Wootta W, et al. An application of duplex PCR for detection of Leptospira spp. and Orientia tsutsugamushi from wild rodents. Jpn J Infect Dis. 2008;61(5):407–9. Epub 2008/09/23. pmid:18806355.
  71. 71. Wongbutdee J, Jittimanee J. Detection of Leptospira in Rats Trapped from Households in Phraroj Village, Muang Sam Sip District, Ubon Ratchathani Province Using Polymerase Chain Reaction Technique. J Med Assoc Thai. 2016;99 Suppl 1:S17–21. Epub 2016/01/29. pmid:26817234.
  72. 72. Cosson JF, Picardeau M, Mielcarek M, Tatard C, Chaval Y, Suputtamongkol Y, et al. Epidemiology of Leptospira transmitted by rodents in Southeast Asia. PLoS Negl Trop Dis. 2014;8(6):e2902. pmid:24901706
  73. 73. Koma T, Yoshimatsu K, Yasuda SP, Li T, Amada T, Shimizu K, et al. A survey of rodent-borne pathogens carried by wild Rattus spp. in Northern Vietnam. Epidemiol Infect. 2013;141(9):1876–84. Epub 2012/11/02. pmid:23114204.
  74. 74. Loan HK, Van Cuong N, Takhampunya R, Kiet BT, Campbell J, Them LN, et al. How important are rats as vectors of leptospirosis in the Mekong Delta of Vietnam? Vector Borne Zoonotic Dis. 2015;15(1):56–64. Epub 2015/01/30. pmid:25629781.
  75. 75. Esfandiari B, Pourshafie MR, Gouya MM, Khaki P, Mostafavi E, Darvish J, et al. An epidemiological comparative study on diagnosis of rodent leptospirosis in Mazandaran Province, northern Iran. Epidemiol Health. 2015;37:e2015012. Epub 2015/03/17. pmid:25773440.
  76. 76. Lindenbaum I, Eylan E. Leptospirosis in Rattus norvegicus and Rattus rattus in Israel. Isr J Med Sci. 1982;18(2):271–5. Epub 1982/02/01. pmid:7068359.
  77. 77. Van der Hoeden J, Szenberg E. Leptospira Infections in Rats in Israel. Trop Geogr Med. 1964;16:377–84. Epub 1964/12/01. pmid:14265515.
  78. 78. Bezjak V, Thorburn H. Survey of rats (Rattus norvegicus) in Kuwait for the presence of Leptospira. Trop Geogr Med. 1983;35(1):33–6. Epub 1983/03/01. pmid:6612771.
  79. 79. Kalfayan BH. Leptospira icterohaemorrhagiae in rats of Beirut. Trans R Soc Trop Med Hyg. 1947;40(6):895–900. Epub 1947/07/01. pmid:20262311.
  80. 80. Sunbul M, Esen S, Leblebicioglu H, Hokelek M, Pekbay A, Eroglu C. Rattus norvegicus acting as reservoir of leptospira interrogans in the Middle Black Sea region of Turkey, as evidenced by PCR and presence of serum antibodies to Leptospira strain. Scand J Infect Dis. 2001;33(12):896–8. Epub 2002/03/01. pmid:11868761.
  81. 81. Foronda P, Martin-Alonso A, Del Castillo-Figueruelo B, Feliu C, Gil H, Valladares B. Pathogenic Leptospira spp. in wild rodents, Canary Islands, Spain. Emerg Infect Dis. 2011;17(9):1781–2. Epub 2011/09/06. pmid:21888829.
  82. 82. Samir A, Soliman R, El-Hariri M, Abdel-Moein K, Hatem ME. Leptospirosis in animals and human contacts in Egypt: broad range surveillance. Rev Soc Bras Med Trop. 2015;48(3):272–7. Epub 2015/06/25. pmid:26108004.
  83. 83. Freulon M, Aboubaker M, Marie JL, Drancourt M, Davoust B. Detection of Leptospira organisms in Rattus rattus of two islands in the Mozambique Channel: Europa and Juan-de-Nova. Bull Soc Pathol Exot. 2010;103(1):48–50. Epub 2010/01/26. pmid:20099052.
  84. 84. Halliday JE, Knobel DL, Allan KJ, de CB BM, Handel I, Agwanda B, et al. Urban leptospirosis in Africa: a cross-sectional survey of Leptospira infection in rodents in the Kibera urban settlement, Nairobi, Kenya. Am J Trop Med Hyg. 2013;89(6):1095–102. Epub 2013/10/02. pmid:24080637.
  85. 85. Rahelinirina S, Leon A, Harstskeerl RA, Sertour N, Ahmed A, Raharimanana C, et al. First isolation and direct evidence for the existence of large small-mammal reservoirs of Leptospira sp. in Madagascar. PLoS ONE. 2010;5(11):e14111. Epub 2010/12/03. pmid:21124843.
  86. 86. Ralaiarijaona RL, Bellenger E, Chanteau S, Roger F, Perolat P, Rasolofo Razanamparany V. Detection of leptospirosis reservoirs in Madagascar using the polymerase chain reaction technique. Arch Inst Pasteur Madagascar. 2001;67(1–2):34–6. Epub 2002/12/11. pmid:12471745.
  87. 87. Lagadec E, Gomard Y, Le Minter G, Cordonin C, Cardinale E, Ramasindrazana B, et al. Identification of Tenrec ecaudatus, a Wild Mammal Introduced to Mayotte Island, as a Reservoir of the Newly Identified Human Pathogenic Leptospira mayottensis. PLoS Negl Trop Dis. 2016;10(8):e0004933. Epub 2016/08/31. pmid:27574792.
  88. 88. Desvars A, Naze F, Benneveau A, Cardinale E, Michault A. Endemicity of leptospirosis in domestic and wild animal species from Reunion Island (Indian Ocean). Epidemiol Infect. 2013;141(6):1154–65. Epub 2012/09/25. pmid:22998941.
  89. 89. Guernier V, Lagadec E, Cordonin C, Le Minter G, Gomard Y, Pages F, et al. Human Leptospirosis on Reunion Island, Indian Ocean: Are Rodents the (Only) Ones to Blame? PLoS Negl Trop Dis. 2016;10(6):e0004733. Epub 2016/06/15. pmid:27294677.
  90. 90. Pagès F, Larrieu S, Simoes J, Lenabat P, Kurtkowiak B, Guernier V, et al. Investigation of a leptospirosis outbreak in triathlon participants, Reunion Island, 2013. Epidemiol Infect. 2016;144(3):661–9. Epub 2015/07/28. pmid:26211921.
  91. 91. Biscornet L, Dellagi K, Pages F, Bibi J, de Comarmond J, Melade J, et al. Human leptospirosis in Seychelles: A prospective study confirms the heavy burden of the disease but suggests that rats are not the main reservoir. PLoS Negl Trop Dis. 2017;11(8):e0005831. Epub 2017/08/29. pmid:28846678.
  92. 92. Allan KJ, Halliday JEB, Moseley M, Carter RW, Ahmed A, Goris MGA, et al. Assessment of animal hosts of pathogenic Leptospira in northern Tanzania. PLoS Negl Trop Dis. 2018;12(6):e0006444. Epub 2018/06/08. pmid:29879104.
  93. 93. Assenga JA, Matemba LE, Muller SK, Mhamphi GG, Kazwala RR. Predominant leptospiral serogroups circulating among humans, livestock and wildlife in Katavi-Rukwa ecosystem, Tanzania. PLoS Negl Trop Dis. 2015;9(3):e0003607. Epub 2015/03/26. pmid:25806825.
  94. 94. Heuser E, Fischer S, Ryll R, Mayer-Scholl A, Hoffmann D, Spahr C, et al. Survey for zoonotic pathogens in Norway rat populations from Europe. Pest Manag Sci. 2017;73(2):341–8. Epub 2016/06/15. pmid:27299665.
  95. 95. Collares-Pereira M, Korver H, Terpstra WJ, Santos-Reis M, Ramalhinho MG, Mathias ML, et al. First epidemiological data on pathogenic leptospires isolated on the Azorean islands. Eur J Epidemiol. 1997;13(4):435–41. Epub 1997/06/01. pmid:9258550.
  96. 96. Collares-Pereira M, Mathias ML, Santos-Reis M, Ramalhinho MG, Duarte-Rodrigues P. Rodents and Leptospira transmission risk in Terceira island (Azores). Eur J Epidemiol. 2000;16(12):1151–7. Epub 2001/08/04. pmid:11484805.
  97. 97. Krøjgaard LH, Villumsen S, Markussen MD, Jensen JS, Leirs H, Heiberg AC. High prevalence of Leptospira spp. in sewer rats (Rattus norvegicus). Epidemiol Infect. 2009;137(11):1586–92. Epub 2009/04/28. pmid:19393116.
  98. 98. Jensen PM, Magnussen E. Is it too cold for Leptospira interrrogans transmission on the Faroese Islands? Infect Dis (Lond). 2016;48(2):156–60. Epub 2015/10/08. pmid:26442766.
  99. 99. Rislakki V, Salminen A. Investigations of leptospirosis in rats in Finland. Acta Pathol Microbiol Scand. 1955;37(1):121–31. Epub 1955/01/01. pmid:14398273.
  100. 100. Aviat F, Blanchard B, Michel V, Blanchet B, Branger C, Hars J, et al. Leptospira exposure in the human environment in France: A survey in feral rodents and in fresh water. Comp Immunol Microbiol Infect Dis. 2009;32(6):463–76. Epub 2008/07/22. pmid:18639932.
  101. 101. Ayral F, Artois J, Zilber AL, Widen F, Pounder KC, Aubert D, et al. The relationship between socioeconomic indices and potentially zoonotic pathogens carried by wild Norway rats: a survey in Rhone, France (2010–2012). Epidemiol Infect. 2015;143(3):586–99. Epub 2014/05/20. pmid:24838220.
  102. 102. Ayral F, Zilber AL, Bicout DJ, Kodjo A, Artois M, Djelouadji Z. Distribution of Leptospira interrogans by Multispacer Sequence Typing in Urban Norway Rats (Rattus norvegicus): A Survey in France in 2011–2013. PLoS ONE. 2015;10(10):e0139604. Epub 2015/10/09. pmid:26447693.
  103. 103. Desvars-Larrive A, Pascal M, Gasqui P, Cosson JF, Benoit E, Lattard V, et al. Population genetics, community of parasites, and resistance to rodenticides in an urban brown rat (Rattus norvegicus) population. PLoS ONE. 2017;12(9):e0184015. Epub 2017/09/09. pmid:28886097.
  104. 104. Zilber AL, Belli P, Artois M, Kodjo A, Djelouadji Z. First Observation of Leptospira interrogans in the Lungs of Rattus norvegicus. Biomed Res Int. 2016;2016:9656274. Epub 2016/11/02. pmid:27800495.
  105. 105. Amaddeo D, Ieradi LA, Autorino GL, Perrella D. Leptospirosis in wild rodents living in urban areas (Rome—Italy). Proceedings of the I European Congress of Manvnalogy. 1996:105·14.
  106. 106. Pezzella M, Lillini E, Sturchio E, Ierardi LA, Grassi M, Traditi F, et al. Leptospirosis survey in wild rodents living in urban areas of Rome. Annali di igiene: medicina preventiva e di comunita. 2004;16(6):721–6. Epub 2005/02/09. pmid:15697001.
  107. 107. Vitale M, Di Bella C, Agnello S, Curro V, Vicari D, Vitale F. Leptospira interrogans survey by PCR in wild rodents coming from different urban areas of Palermo, Italy. Rev Cubana Med Trop. 2007;59(1):59–60. Epub 2007/01/01. pmid:23427420.
  108. 108. Vitale M, Agnello S, Chetta M, Amato B, Vitale G, Bella CD, et al. Human leptospirosis cases in Palermo Italy. The role of rodents and climate. Journal of infection and public health. 2018;11(2):209–14. Epub 2017/08/15. pmid:28802826.
  109. 109. Ferreira AS, Costa P, Rocha T, Amaro A, Vieira ML, Ahmed A, et al. Direct detection and differentiation of pathogenic Leptospira species using a multi-gene targeted real time PCR approach. PLoS ONE. 2014;9(11):e112312. Epub 2014/11/15. pmid:25398140.
  110. 110. Millán J, Cevidanes A, Chirife AD, Candela MG, Leon-Vizcaino L. Risk factors of Leptospira infection in Mediterranean periurban micromammals. Zoonoses and public health. 2018;65(1):e79–e85. Epub 2017/10/24. pmid:29058382.
  111. 111. Strand TM, Lohmus M, Persson Vinnersten T, Rasback T, Sundstrom K, Bergstrom T, et al. Highly Pathogenic Leptospira Found in Urban Brown Rats (Rattus norvegicus) in the Largest Cities of Sweden. Vector Borne Zoonotic Dis. 2015;15(12):779–81. Epub 2015/11/19. pmid:26579782.
  112. 112. Broom JC, Gibson EA. Infection rates of Rattus norvegicus with Leptospira icterohaemorrhagiae in Great Britain. I. A rural area in Carmarthenshire, Wales. J Hyg (Lond). 1953;51(3):416–25. Epub 1953/09/01. pmid:13096748.
  113. 113. Michna SW, Ellis W. The isolation of Leptospira belonging to the serogroup ballum from the kidneys of a brown rat (Rattus norvegicus). Res Vet Sci. 1974;16(2):263–4. Epub 1974/03/01. pmid:4830988.
  114. 114. Middleton AD. Leptospira icterohaemorrhagiae in Oxford Rats. J Hyg (Lond). 1929;29(2):219–26. Epub 1929/07/01. pmid:20475024.
  115. 115. Webster JP, Ellis WA, Macdonald DW. Prevalence of Leptospira spp. in wild brown rats (Rattus norvegicus) on UK farms. Epidemiol Infect. 1995;114(1):195–201. Epub 1995/02/01. pmid:7867738.
  116. 116. Allen SE, Ojkic D, Jardine CM. Prevalence of antibodies to Leptospira in wild mammals trapped on livestock farms in Ontario, Canada. J Wildl Dis. 2014;50(3):666–70. Epub 2014/05/09. pmid:24807356.
  117. 117. Himsworth CG, Bidulka J, Parsons KL, Feng AY, Tang P, Jardine CM, et al. Ecology of Leptospira interrogans in Norway rats (Rattus norvegicus) in an inner-city neighborhood of Vancouver, Canada. PLoS Negl Trop Dis. 2013;7(6):e2270. Epub 2013/07/03. pmid:23818996.
  118. 118. McKiel JA, Cousineau JG, Hall RR. Leptospirosis in Wild Animals in Eastern Canada With Particular Attention to the Disease in Rats. Can J Comp Med Vet Sci. 1961;25(1):15–8. Epub 1961/01/01. pmid:17649276.
  119. 119. Montes AS, Dimas JS, Preciado Rodriguez FJ. Rats and dogs: important vectors of leptospirosis in agricultural areas in Cuidad Guzman, Jalisco. Rev Cubana Med Trop. 2002;54(1):21–3. Epub 2005/04/26. pmid:15846935.
  120. 120. Panti-May JA, DE Andrade RRC, Gurubel-Gonzalez Y, Palomo-Arjona E, Soda-Tamayo L, Meza-Sulu J, et al. A survey of zoonotic pathogens carried by house mouse and black rat populations in Yucatan, Mexico. Epidemiol Infect. 2017;145(11):2287–95. Epub 2017/07/12. pmid:28689507.
  121. 121. Torres-Castro M, Guillermo-Cordero L, Hernandez-Betancourt S, Gutierrez-Ruiz E, Agudelo-Florez P, Pelaez-Sanchez R, et al. First histopathological study in kidneys of rodents naturally infected with Leptospira pathogenic species from Yucatan, Mexico. Asian Pac J Trop Med. 2016;9(2):145–7. Epub 2016/02/28. pmid:26919944.
  122. 122. Vado-Solis I, Cardenas-Marrufo MF, Jimenez-Delgadillo B, Alzina-Lopez A, Laviada-Molina H, Suarez-Solis V, et al. Clinical-epidemiological study of leptospirosis in humans and reservoirs in Yucatan, Mexico. Rev Inst Med Trop Sao Paulo. 2002;44(6):335–40. Epub 2003/01/18. pmid:12532218.
  123. 123. Easterbrook JD, Kaplan JB, Vanasco NB, Reeves WK, Purcell RH, Kosoy MY, et al. A survey of zoonotic pathogens carried by Norway rats in Baltimore, Maryland, USA. Epidemiol Infect. 2007;135(7):1192–9. Epub 2007/01/17. pmid:17224086.
  124. 124. Firth C, Bhat M, Firth MA, Williams SH, Frye MJ, Simmonds P, et al. Detection of zoonotic pathogens and characterization of novel viruses carried by commensal Rattus norvegicus in New York City. mBio. 2014;5(5):e01933–14. Epub 2014/10/16. pmid:25316698.
  125. 125. Li HY, Davis DE. The prevalence of carriers of Leptospira and Salmonella in Norway rats of Baltimore. Am J Hyg. 1952;56(1):90–1. Epub 1952/07/01. pmid:14933393.
  126. 126. Sulzer CR, Harvey TW, Galton MM. Comparison of diagnostic technics for the detection of leptospirosis in rats. Health Lab Sci. 1968;5(3):171–3. Epub 1968/07/01. pmid:4876436.
  127. 127. Taylor KD, Turner LH, Everard JD. Leptospires in Rattus spp. on Barbados. J Trop Med Hyg. 1991;94(2):102–3. Epub 1991/04/01. pmid:2023284.
  128. 128. Levett PN, Walton D, Waterman LD, Whittington CU, Mathison GE, Everard CO. Surveillance of leptospiral carriage by feral rats in Barbados. West Indian Med J. 1998;47(1):15–7. pmid:9619090
  129. 129. Keenan J, Sharma R, Dicker R, Rayner J, Stone D. Seroprevalence of Leptospira in rattus norvegicus in Grenada, West Indies. West Indian Med J. 2009;58(2):114–7. Epub 2009/03/01. pmid:21866595.
  130. 130. Rust JH. Leptospirosis in Puerto Rican wild rats. PR J Public Health Trop Med. 1948;24(2):105–12. Epub 1948/12/01. pmid:18111633.
  131. 131. Everard CO, Fraser-Chanpong GM, Bhagwandin LJ, Race MW, James AC. Leptospires in wildlife from Trinidad and Grenada. J Wildl Dis. 1983;19(3):192–9. Epub 1983/07/01. pmid:6644917.
  132. 132. Suepaul SM, Carrington CV, Campbell M, Borde G, Adesiyun AA. Serovars of Leptospira isolated from dogs and rodents. Epidemiol Infect. 2010;138(7):1059–70. Epub 2009/10/09. pmid:19811697.
  133. 133. Suepaul SM, Carrington CV, Campbell M, Borde G, Adesiyun AA. Seroepidemiology of leptospirosis in dogs and rats in Trinidad. Trop Biomed. 2014;31(4):853–61. Epub 2015/03/18. pmid:25776612.
  134. 134. Scialfa E, Bolpe J, Bardon JC, Ridao G, Gentile J, Gallicchio O. Isolation of Leptospira interrogans from suburban rats in Tandil, Buenos Aires, Argentina. Rev Argent Microbiol. 2010;42(2):126–8. Epub 2010/07/01. pmid:20589335.
  135. 135. Vanasco NB, Rossetti C, Sequeira G, Sequeira MD, Calderon G, Tarabla HD. First isolations of leptospires serogroup Ballum serovar arborea in Argentina. Vet Rec. 2000;147(9):246–7. Epub 2000/10/03. pmid:11014489.
  136. 136. Vanasco NB, Sequeira MD, Sequeira G, Tarabla HD. Associations between leptospiral infection and seropositivity in rodents and environmental characteristics in Argentina. Prev Vet Med. 2003;60(3):227–35. Epub 2003/08/06. pmid:12900160.
  137. 137. Costa F, Porter FH, Rodrigues G, Farias H, de Faria MT, Wunder EA, et al. Infections by Leptospira interrogans, Seoul virus, and Bartonella spp. among Norway rats (Rattus norvegicus) from the urban slum environment in Brazil. Vector Borne Zoonotic Dis. 2014;14(1):33–40. Epub 2013/12/24. pmid:24359425.
  138. 138. de Faria MT, Calderwood MS, Athanazio DA, McBride AJ, Hartskeerl RA, Pereira MM, et al. Carriage of Leptospira interrogans among domestic rats from an urban setting highly endemic for leptospirosis in Brazil. Acta Trop. 2008;108(1):1–5. Epub 2008/08/30. pmid:18721789.
  139. 139. de Oliveira D, Figueira CP, Zhan L, Pertile AC, Pedra GG, Gusmao IM, et al. Leptospira in breast tissue and milk of urban Norway rats (Rattus norvegicus). Epidemiol Infect. 2016;144(11):2420–9. Epub 2016/03/29. pmid:27019024.
  140. 140. Lilenbaum W, Ribeiro V, Martin E, Bispo V. Serologic study for detecting anti-Leptospira antibodies in Rattus norvegicus from Duque de Caxias, Rio de Janeiro, Brazil. Rev Latinoam Microbiol. 1993;35(4):357–80. Epub 1993/10/01. pmid:8066330.
  141. 141. Martins G, Lilenbaum W. The panorama of animal leptospirosis in Rio de Janeiro, Brazil, regarding the seroepidemiology of the infection in tropical regions. BMC Vet Res. 2013;9:237. Epub 2013/12/03. pmid:24289165.
  142. 142. Paixão MS, Alves-Martin MF, Tenorio Mda S, Starke-Buzetti WA, Alves ML, da Silva DT, et al. Serology, isolation, and molecular detection of Leptospira spp. from the tissues and blood of rats captured in a wild animal preservation centre in Brazil. Prev Vet Med. 2014;115(1–2):69–73. Epub 2014/04/08. pmid:24703251.
  143. 143. Pellizzaro M, Conrado FO, Martins CM, Joaquim SF, Ferreira F, Langoni H, et al. Serosurvey of Leptospira spp. and Toxoplasma gondii in rats captured from two zoos in Southern Brazil. Rev Soc Bras Med Trop. 2017;50(6):857–60. Epub 2018/01/18. pmid:29340468.
  144. 144. Santos AA, Figueira CP, dos Reis MG, Costa F, Ristow P. Heterogenic colonization patterns by Leptospira interrogans in Rattus norvegicus from urban slums. Braz J Microbiol. 2015;46(4):1161–4. Epub 2015/12/23. pmid:26691476.
  145. 145. Tucunduva de Faria M, Athanazio DA, Goncalves Ramos EA, Silva EF, Reis MG, Ko AI. Morphological alterations in the kidney of rats with natural and experimental Leptospira infection. J Comp Pathol. 2007;137(4):231–8. Epub 2007/11/13. pmid:17996544.
  146. 146. Correa JP, Bucarey SA, Cattan PE, Landaeta-Aqueveque C, Ramirez-Estrada J. Renal carriage of Leptospira species in rodents from Mediterranean Chile: The Norway rat (Rattus norvegicus) as a relevant host in agricultural lands. Acta Trop. 2017;176:105–8. Epub 2017/08/02. pmid:28760479.
  147. 147. Munoz-Zanzi C, Mason M, Encina C, Gonzalez M, Berg S. Household characteristics associated with rodent presence and Leptospira infection in rural and urban communities from Southern Chile. Am J Trop Med Hyg. 2014;90(3):497–506. Epub 2014/01/22. pmid:24445209.
  148. 148. Agudelo-Florez P, Londono AF, Quiroz VH, Angel JC, Moreno N, Loaiza ET, et al. Prevalence of Leptospira spp. in urban rodents from a groceries trade center of Medellin, Colombia. Am J Trop Med Hyg. 2009;81(5):906–10. Epub 2009/10/29. pmid:19861630.
  149. 149. Agudelo-Florez P, Arango JC, Merizalde E, Londono AF, Quiroz VH, Rodas JD. Serological evidence of Leptospira spp circulation in naturally-exposed rats (Rattusnorvegicus) in a Colombian urban area. Rev Salud Publica (Bogota). 2010;12(6):990–9. Epub 2011/10/28. pmid:22030686.
  150. 150. Calderón A, Rodriguez V, Mattar S, Arrieta G. Leptospirosis in pigs, dogs, rodents, humans, and water in an area of the Colombian tropics. Trop Anim Health Prod. 2014;46(2):427–32. Epub 2013/11/21. pmid:24254419.
  151. 151. Morales GA, Guzman VH, Beltran LE. Leptospirosis in Colombia: isolation of Leptospira spp. from the kidneys of brown rats (Rattus norvegicus) trapped on infected piggeries. Trop Anim Health Prod. 1978;10(2):121–3. Epub 1978/05/01. pmid:664013.
  152. 152. Romero-Vivas CM, Cuello-Perez M, Agudelo-Florez P, Thiry D, Levett PN, Falconar AK. Cross-sectional study of Leptospira seroprevalence in humans, rats, mice, and dogs in a main tropical sea-port city. Am J Trop Med Hyg. 2013;88(1):178–83. Epub 2012/11/15. pmid:23149584.
  153. 153. Barragan V, Chiriboga J, Miller E, Olivas S, Birdsell D, Hepp C, et al. High Leptospira Diversity in Animals and Humans Complicates the Search for Common Reservoirs of Human Disease in Rural Ecuador. PLoS Negl Trop Dis. 2016;10(9):e0004990. Epub 2016/09/14. pmid:27622673.
  154. 154. Johnson MA, Smith H, Joeph P, Gilman RH, Bautista CT, Campos KJ, et al. Environmental exposure and leptospirosis, Peru. Emerg Infect Dis. 2004;10(6):1016–22. Epub 2004/06/23. pmid:15207052.
  155. 155. Matthias MA, Ricaldi JN, Cespedes M, Diaz MM, Galloway RL, Saito M, et al. Human leptospirosis caused by a new, antigenically unique Leptospira associated with a Rattus species reservoir in the Peruvian Amazon. PLoS Negl Trop Dis. 2008;2(4):e213. Epub 2008/04/03. pmid:18382606.
  156. 156. Kallai L, Kemenes F, Vizy L. Studies on the Leptospira icterohaemorrhagiae infection of experimental rats. Acta Microbiol Acad Sci Hung. 1962;9:311–5. Epub 1962/01/01. pmid:13961958.
  157. 157. Natrajaseenivasan K, Ratnam S. An investigation of leptospirosis in a laboratory animal house. J Commun Dis. 1996;28(3):153–7. Epub 1996/09/01. pmid:8973012.
  158. 158. Nicolescu M, Borsai L, Alamita I. Leptospirosis in albino rats. Arch Roum Pathol Exp Microbiol. 1973;32(2):171–7. Epub 1973/06/01. pmid:4584313.
  159. 159. Gaudie CM, Featherstone CA, Phillips WS, McNaught R, Rhodes PM, Errington J, et al. Human Leptospira interrogans serogroup icterohaemorrhagiae infection (Weil’s disease) acquired from pet rats. Vet Rec. 2008;163(20):599–601. Epub 2008/11/18. pmid:19011247.
  160. 160. Guerra B, Schneider T, Luge E, Draeger A, Moos V, Loddenkemper C, et al. Detection and characterization of Leptospira interrogans isolates from pet rats belonging to a human immunodeficiency virus-positive patient with leptospirosis. J Med Microbiol. 2008;57(Pt 1):133–5. Epub 2007/12/11. pmid:18065682.
  161. 161. Džupová O, Smíšková D, Hůzová Z, Beneš J. Leptospirosis contracted from pet rats. Klin Mikrobiol Infekc Lek. 2012;18(5):156–9. Epub 2012/12/05. pmid:23208870.
  162. 162. Mori M, Bourhy P, Le Guyader M, Van Esbroeck M, Djelouadji Z, Septfons A, et al. Pet rodents as possible risk for leptospirosis, Belgium and France, 2009 to 2016. Euro surveillance: bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin. 2017;22(43). Epub 2017/11/02. pmid:29090679.
  163. 163. United Nations, Department of Economic and Social Affairs, Population Division. World Urbanization Prospects: The 2018 Revision [press release]. 2018 [cited 2019 May 15]. https://population.un.org/wup/Publications/Files/WUP2018-PressRelease.pdf.
  164. 164. Blasdell KR, Morand S, Perera D, Firth C. Association of rodent-borne Leptospira spp. with urban environments in Malaysian Borneo. PLoS Negl Trop Dis. 2019;13(2):e0007141. Epub 2019/02/28. pmid:30811387.
  165. 165. Parsons MH, Banks PB, Deutsch MA, Corrigan RF, Munshi-South J. Trends in urban rat ecology: a framework to define the prevailing knowledge gaps and incentives for academia, pest management professionals (PMPs) and public health agencies to participate. Journal of Urban Ecology. 2017;3(1).
  166. 166. National Center for Biotechnology Information [Internet]. NCBI Taxonomy Browser. [cited 2019 Apr 26]. https://www.ncbi.nlm.nih.gov/taxonomy.
  167. 167. Pagès M, Chaval Y, Herbreteau V, Waengsothorn S, Cosson JF, Hugot JP, et al. Revisiting the taxonomy of the Rattini tribe: a phylogeny-based delimitation of species boundaries. BMC evolutionary biology. 2010;10:184. Epub 2010/06/23. pmid:20565819.