Leptospirosis in Humans, Animals and the Environment—A “One Health” Perspective

A special issue of Tropical Medicine and Infectious Disease (ISSN 2414-6366). This special issue belongs to the section "One Health".

Deadline for manuscript submissions: closed (10 November 2021) | Viewed by 37942

Special Issue Editors


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Guest Editor
1. Institut de Recherche pour le Développement, iEES-Paris, 75005 Paris, France
2. Faculty of Veterinary Technology, Kasetsart University, 10900 Bangkok, Thailand
Interests: disease ecology; eco-epidemiology; environmental health; leptospirosis; melioidosis; neglected tropical diseases; phylogenetics and evolution; zoonoses; One Health; antimicrobial resistance

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Guest Editor
Unité Epidémiologie et de Recherche Clinique, Institut Pasteur de Madagascar, B.P. 1274, Ambatofotsikely, 101 Antananarivo, Madagascar
Interests: epidemiology; leptopsirosis; rickettsiosis; tunga penetrans; zoonoses; acute undifferentiated fever; One Health; (veterinary) public health; implementation research; burden of disease

Special Issue Information

Dear Colleagues,

As we start a new decade, there is a legitimate and compelling agreement upon the need for multidisciplinary research on infectious diseases in order to tackle the increasing complexity of epidemics related to global and local changes such as climate change, biodiversity loss, urbanization or deforestation. These social and environmental changes associated with emerging or reemerging threats to human and animal health have triggered a growing interest for Planetary Health, EcoHealth, and One Health. The concept of One Health, an interdisciplinary approach stressing connections between human, animal, and environmental health, gained momentum after the SARS and avian influenza pandemics, and more recently with the spread of antimicrobial-resistant pathogens, where the need for a multisectoral approach continues to be emphasized.

Leptospirosis is a bacterial zoonosis, i.e. affecting both humans and animals, and among the most widespread diseases in subtropical and tropical countries. Leptospira spp., the causative agent of the disease, is acquired directly through contact with urine or aborted tissues of infected animals, or indirectly through contact with a contaminated environment. Animal reservoirs contaminate soil and water, which are especially important compartments of the epidemiological cycle during times of heavy rainfall and flooding.

Effective control of leptospirosis requires knowledge of the animal and environmental reservoirs of infection and of any spatiotemporal variability in order to assess the populations and places at risk and to identify the best control strategies. This entails the collaboration of scientists, physicians, veterinarians, ecologists, policy makers, planners, regulators, public and animal health officials, and environmental health officers—hence the application of a “One Health” approach.

To achieve this multidisciplinary goal, information on the diversity, ecology, and virulence of the bacteria Leptospira is being collected not only from humans, but also animals and the environment. Methods such as molecular epidemiology, -omics, mathematical modeling, GIS or risk analysis have been applied to better link the different compartments involved in the epidemiological cycle of leptospirosis in various settings.

This Special Issue will bring together studies that provide novel and comprehensive evaluations of the local epidemiology of leptospirosis in a changing environment. One Health studies investigating the nexus between human health, animal health, and the environment in order to enhance surveillance and control are particularly welcome, as well as studies investigating unknown reservoirs of infection, or using original methodologies to address the risk of infection.

Dr. Vanina Guernier
Dr. Anou Dreyfus
Guest Editor

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Keywords

  • Leptospirosis
  • Zoonoses
  • Environmental health
  • Risk mapping
  • Veterinary epidemiology
  • Neglected tropical diseases
  • One Health

Published Papers (10 papers)

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Research

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9 pages, 291 KiB  
Article
Tracking Animal Reservoirs of Pathogenic Leptospira: The Right Test for the Right Claim
by Yann Gomard, Koussay Dellagi, Steven M. Goodman, Patrick Mavingui and Pablo Tortosa
Trop. Med. Infect. Dis. 2021, 6(4), 205; https://0-doi-org.brum.beds.ac.uk/10.3390/tropicalmed6040205 - 30 Nov 2021
Cited by 6 | Viewed by 2654
Abstract
Leptospirosis is the most prevalent bacterial zoonosis worldwide and, in this context, has been extensively investigated through the One Health framework. Diagnosis of human leptospirosis includes molecular and serological tools, with the serological Microscopic Agglutination Test (MAT) still being considered as the gold [...] Read more.
Leptospirosis is the most prevalent bacterial zoonosis worldwide and, in this context, has been extensively investigated through the One Health framework. Diagnosis of human leptospirosis includes molecular and serological tools, with the serological Microscopic Agglutination Test (MAT) still being considered as the gold standard. Mammals acting as reservoirs of the pathogen include species or populations that are able to maintain chronic infection and shed the bacteria via their urine into the environment. Animals infected by Leptospira are often identified using the same diagnosis tool as in humans, i.e., serological MAT. However, this tool may lead to misinterpretations as it can signal previous infection but does not provide accurate information regarding the capacity of animals to maintain chronic infection and, hence, participate in the transmission cycle. We employ in this paper previously published data and present original results on introduced and endemic small mammals from Indian Ocean islands to show that MAT should not be used for the identification of Leptospira reservoirs. By contrast, serological data are informative on the level of exposure of animals living in a specific environment. We present a sequential methodology to investigate human leptospirosis in the One Health framework that associates molecular detection in humans and animals, together with MAT of human samples using Leptospira isolates obtained from reservoir animals occurring in the same environment. Full article
11 pages, 946 KiB  
Article
Evolution of Public Health Prevention of Leptospirosis in a One Health Perspective: The Example of Mahasarakham Province (Thailand)
by Jaruwan Viroj, Claire Lajaunie and Serge Morand
Trop. Med. Infect. Dis. 2021, 6(3), 168; https://0-doi-org.brum.beds.ac.uk/10.3390/tropicalmed6030168 - 17 Sep 2021
Cited by 2 | Viewed by 3102
Abstract
Leptospirosis is an endemic disease with moderate to high incidence in Mahasarakham province, Thailand. The present study was designed to assess the policy implementation mission regarding leptospirosis prevention and control from the national level to the local administrative levels, through a One Health [...] Read more.
Leptospirosis is an endemic disease with moderate to high incidence in Mahasarakham province, Thailand. The present study was designed to assess the policy implementation mission regarding leptospirosis prevention and control from the national level to the local administrative levels, through a One Health perspective. A qualitative study was conducted, using documentation review, individual in-depth interviews with public health officers, local government officers, livestock officers who developed policy implementation tools or have responsibilities in leptospirosis prevention and control. The results show that Thailand has progressively developed a leptospirosis prevention and control policy framework at the national level, transferring the responsibility of its implementation to the local level. The province of Mahasarakham has decided to foster cooperation in leptospirosis prevention and control at the local level. However, there are insufficient linkages between provincial, district and sub-district departments to ensure comprehensive disease prevention activities at the local level concerning leptospirosis patients and the whole population. Full article
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17 pages, 3839 KiB  
Article
Agro-Environmental Determinants of Leptospirosis: A Retrospective Spatiotemporal Analysis (2004–2014) in Mahasarakham Province (Thailand)
by Jaruwan Viroj, Julien Claude, Claire Lajaunie, Julien Cappelle, Anamika Kritiyakan, Pornsit Thuainan, Worachead Chewnarupai and Serge Morand
Trop. Med. Infect. Dis. 2021, 6(3), 115; https://0-doi-org.brum.beds.ac.uk/10.3390/tropicalmed6030115 - 28 Jun 2021
Cited by 7 | Viewed by 4937
Abstract
Leptospirosis has been recognized as a major public health concern in Thailand following dramatic outbreaks. We analyzed human leptospirosis incidence between 2004 and 2014 in Mahasarakham province, Northeastern Thailand, in order to identify the agronomical and environmental factors likely to explain incidence at [...] Read more.
Leptospirosis has been recognized as a major public health concern in Thailand following dramatic outbreaks. We analyzed human leptospirosis incidence between 2004 and 2014 in Mahasarakham province, Northeastern Thailand, in order to identify the agronomical and environmental factors likely to explain incidence at the level of 133 sub-districts and 1982 villages of the province. We performed general additive modeling (GAM) in order to take the spatial-temporal epidemiological dynamics into account. The results of GAM analyses showed that the average slope, population size, pig density, cow density and flood cover were significantly associated with leptospirosis occurrence in a district. Our results stress the importance of livestock favoring leptospirosis transmission to humans and suggest that prevention and control of leptospirosis need strong intersectoral collaboration between the public health, the livestock department and local communities. More specifically, such collaboration should integrate leptospirosis surveillance in both public and animal health for a better control of diseases in livestock while promoting public health prevention as encouraged by the One Health approach. Full article
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10 pages, 2737 KiB  
Article
Exposure and Carriage of Pathogenic Leptospira in Livestock in St. Croix, U.S. Virgin Islands
by Hannah M. Cranford, Marissa Taylor, Andrew Springer Browne, David P. Alt, Tammy Anderson, Camila Hamond, Richard L. Hornsby, Karen LeCount, Linda Schlater, Tod Stuber, Leah De Wilde, Valicia J. Burke-France, Esther M. Ellis, Jarlath E. Nally and Bethany Bradford
Trop. Med. Infect. Dis. 2021, 6(2), 85; https://0-doi-org.brum.beds.ac.uk/10.3390/tropicalmed6020085 - 24 May 2021
Cited by 6 | Viewed by 5041
Abstract
From 2019–2020, the Virgin Islands Department of Health (VIDOH) investigated potential animal reservoirs of Leptospira spp., the pathogenic bacteria that cause leptospirosis. We examined Leptospira exposure and carriage in livestock on the island of St. Croix, United States Virgin Islands (USVI). We utilized [...] Read more.
From 2019–2020, the Virgin Islands Department of Health (VIDOH) investigated potential animal reservoirs of Leptospira spp., the pathogenic bacteria that cause leptospirosis. We examined Leptospira exposure and carriage in livestock on the island of St. Croix, United States Virgin Islands (USVI). We utilized the microscopic agglutination test (MAT) to evaluate the sera, and the fluorescent antibody test (FAT), real time polymerase chain reaction (rt-PCR), and bacterial culture to evaluate urine specimens from livestock (n = 126): 28 cattle, 19 goats, 46 pigs, and 33 sheep. Seropositivity was 37.6% (47/125) with agglutinating antibodies to the following serogroups identified: Australis, Djasiman, Icterohaemorrhagiae, Ballum, Sejroe, Cynopteri, Autumnalis, Hebdomadis, Pomona, Canicola, Grippotyphosa, and Pyrogenes. Urine from 4 animals (4.0%, 4/101) was positive by rt-PCR for lipL32: 2 sheep, 1 goat, and 1 bull. Sequencing of secY amplicons identified L. interrogans in 1 sheep and 1 bull. Livestock in USVI harbor pathogenic Leptospira bacteria and could play a role in the zoonotic cycle of leptospirosis. Full article
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13 pages, 4282 KiB  
Article
Potentially Pathogenic Leptospira in the Environment of an Elephant Camp in Thailand
by Somjit Chaiwattanarungruengpaisan, Wasinee Thepapichaikul, Weena Paungpin, Kanokwan Ketchim, Sarin Suwanpakdee and Metawee Thongdee
Trop. Med. Infect. Dis. 2020, 5(4), 183; https://0-doi-org.brum.beds.ac.uk/10.3390/tropicalmed5040183 - 06 Dec 2020
Cited by 3 | Viewed by 2430
Abstract
Leptospira is the causative agent of leptospirosis, a globally emerging zoonotic disease. The infection is commonly acquired through contact with the contaminated environment. To extend the knowledge on environmental source of leptospirosis, we investigated the presence of Leptospira in an elephant camp setting [...] Read more.
Leptospira is the causative agent of leptospirosis, a globally emerging zoonotic disease. The infection is commonly acquired through contact with the contaminated environment. To extend the knowledge on environmental source of leptospirosis, we investigated the presence of Leptospira in an elephant camp setting where the interaction between humans, animals, and the shared environment occur particularly when engaging in recreational activities. In this study, a total of 24 environmental samples were collected from an elephant camp area in western Thailand. All samples were processed for Leptospira isolation using the EMJH medium. The identification of Leptospira species was carried out by partial 16S rRNA and secY gene sequencing. Of those 24 samples, 18 samples (75%) were culture-positive for Leptospira. The recovered leptospires were mostly derived from water and soil sampled from a river and a mud pond, the main areas for recreational activities. The majority of the isolates were classified into “Pathogens” clade (89%, 16/18) and more than half of the isolates (61%, 11/18) contained species of the “Saprophytes” clade. Notably, two soil isolates from the river beach sampling area were found to contain leptospiral DNA with high similarity to the pathogenic L. interrogans and L. santarosai. The evidence of diverse Leptospira species, particularly those belonging to the “Pathogens” clade, suggest that the shared environments of an elephant camp can serve as potential infection source and may pose a risk to the elephant camp tourists and workers. Full article
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12 pages, 1599 KiB  
Article
Low Prevalence of Leptospira Carriage in Rodents in Leptospirosis-Endemic Northeastern Thailand
by Panadda Krairojananan, Janjira Thaipadungpanit, Surachai Leepitakrat, Taweesak Monkanna, Elizabeth W. Wanja, Anthony L. Schuster, Federico Costa, B. Katherine Poole-Smith and Patrick W. McCardle
Trop. Med. Infect. Dis. 2020, 5(4), 154; https://0-doi-org.brum.beds.ac.uk/10.3390/tropicalmed5040154 - 30 Sep 2020
Cited by 7 | Viewed by 2872
Abstract
Leptospirosis is a neglected zoonotic disease affecting mostly the world’s tropical regions. The rural people of northeastern Thailand suffer from a large number of leptospirosis infections, and their abundant rice fields are optimal rodent habitats. To evaluate the contribution of diversity and carriage [...] Read more.
Leptospirosis is a neglected zoonotic disease affecting mostly the world’s tropical regions. The rural people of northeastern Thailand suffer from a large number of leptospirosis infections, and their abundant rice fields are optimal rodent habitats. To evaluate the contribution of diversity and carriage rate of pathogenic Leptospira in rodent reservoirs to leptospirosis incidence, we surveyed rodents, between 2011 and 2012, in four provinces in northeastern Thailand with the highest incidence rates of human leptospirosis cases. We used lipL32 real-time PCR to detect pathogenic Leptospira in rodent kidneys, partial 16S rRNA gene sequencing to classify the infecting Leptospira species, and whole 16S rDNA sequencing to classify species of isolated Leptospira. Overall prevalence of Leptospira infection was 3.6% (18/495). Among infected rodents, Bandicotaindica (14.3%), Rattusexulans (3.6%), and R. rattus (3.2%) had renal carriage. We identified two pathogenic Leptospira species: L. interrogans (n = 15) and L. borgpetersenii (n = 3). In addition, an L. wolffii (LS0914U) isolate was recovered from the urine of B. indica. Leptospira infection was more prevalent in low density rodent populations, such as B. indica. In contrast, there was a lower prevalence of Leptospira infection in high density rodent populations of R. exulans and R. rattus. Full article
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10 pages, 676 KiB  
Article
Detection of Pathogenic Leptospires in Water and Soil in Areas Endemic to Leptospirosis in Nicaragua
by Byron Flores, Karla Escobar, José Luis Muzquiz, Jessica Sheleby-Elías, Brenda Mora, Edipcia Roque, Dayana Torres, Álvaro Chávez and William Jirón
Trop. Med. Infect. Dis. 2020, 5(3), 149; https://0-doi-org.brum.beds.ac.uk/10.3390/tropicalmed5030149 - 18 Sep 2020
Cited by 6 | Viewed by 3098
Abstract
In Nicaragua, there are ideal environmental conditions for leptospirosis. The objective of this investigation was to detect pathogenic and saprophytic leptospires in water and soil samples from leptospirosis-endemic areas in Nicaragua. Seventy-eight water and 42 soil samples were collected from houses and rivers [...] Read more.
In Nicaragua, there are ideal environmental conditions for leptospirosis. The objective of this investigation was to detect pathogenic and saprophytic leptospires in water and soil samples from leptospirosis-endemic areas in Nicaragua. Seventy-eight water and 42 soil samples were collected from houses and rivers close to confirmed human cases. Leptospira spp was isolated in Ellinghausen–McCullough–Johnson–Harris (EMJH) culture medium with 5-fluororacil and positive samples were analyzed through PCR for the LipL32 gene, specific for pathogenic leptospires (P1 clade). There were 73 positive cultures from 120 samples, however only six of these (5% of all collected samples) were confirmed to be pathogenic, based on the presence of the LipL32 gene (P1 clade). Of these six pathogenic isolates, four were from Leon and two from Chinandega. Four pathogenic isolates were obtained from water and two from soil. This study proved the contamination of water and soil with pathogenic leptospires, which represents a potential risk for public health. Full article
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8 pages, 392 KiB  
Article
Relationship between Physicochemical Characteristics and Pathogenic Leptospira in Urban Slum Waters
by Daiana de Oliveira, Vladimir Airam Querino, Yeonsoo Sara Lee, Marcelo Cunha, Nivison Nery Jr., Jr., Louisa Wessels Perelo, Juan Carlos Rossi Alva, Albert I. Ko, Mitermayer G. Reis, Arnau Casanovas-Massana and Federico Costa
Trop. Med. Infect. Dis. 2020, 5(3), 146; https://0-doi-org.brum.beds.ac.uk/10.3390/tropicalmed5030146 - 16 Sep 2020
Cited by 3 | Viewed by 2690
Abstract
Leptospirosis, a zoonosis caused by pathogenic Leptospira, primarily affects tropical, developing regions, especially communities without adequate sanitation. Outbreaks of leptospirosis have been linked with the presence of pathogenic Leptospira in water. In this study, we measured the physicochemical characteristics (temperature, pH, salinity, [...] Read more.
Leptospirosis, a zoonosis caused by pathogenic Leptospira, primarily affects tropical, developing regions, especially communities without adequate sanitation. Outbreaks of leptospirosis have been linked with the presence of pathogenic Leptospira in water. In this study, we measured the physicochemical characteristics (temperature, pH, salinity, turbidity, electrical conductivity, and total dissolved solids (TDS)) of surface waters from an urban slum in Salvador, Brazil, and analyzed their associations with the presence and concentration of pathogenic Leptospira reported previously. We built logistic and linear regression models to determine the strength of association between physicochemical parameters and the presence and concentration of Leptospira. We found that salinity, TDS, pH, and type of water were strongly associated with the presence of Leptospira. In contrast, only pH was associated with the concentration of the pathogen in water. The study of physico-chemical markers can contribute to a better understanding of the occurrence of Leptospira in water and to the identification of sources of risk in urban slum environments. Full article
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13 pages, 919 KiB  
Article
Optimization of Culture Protocols to Isolate Leptospira spp. from Environmental Water, Field Investigation, and Identification of Factors Associated with the Presence of Leptospira spp. in the Environment
by Udomsak Narkkul, Janjira Thaipadungpanit, Prapaporn Srilohasin, Preeraya Singkhaimuk, Metawee Thongdee, Somjit Chaiwattanarungruengpaisan, Panadda Krairojananan and Wirichada Pan-ngum
Trop. Med. Infect. Dis. 2020, 5(2), 94; https://0-doi-org.brum.beds.ac.uk/10.3390/tropicalmed5020094 - 05 Jun 2020
Cited by 12 | Viewed by 3796
Abstract
The successful culture of Leptospira spp. from the environment is challenging. Here, we optimized the isolation of Leptospira spp. from water samples spiked with different species and initial concentrations of this organism. The time periods between water sampling and the isolation process were [...] Read more.
The successful culture of Leptospira spp. from the environment is challenging. Here, we optimized the isolation of Leptospira spp. from water samples spiked with different species and initial concentrations of this organism. The time periods between water sampling and the isolation process were varied (0, 2, and 4 weeks). Bacterial cultures were observed under a microscope, and cultures were graded for cell density, weekly, for 12 weeks. Most pathogenic Leptospira spp. were difficult to culture under all conditions. All conditions of water samples spiked with novel species of Leptospira subclade P1 were culture positive within 2 weeks. For Leptospira subclade P2, storing samples for 2 weeks prior to isolation resulted in more successful isolation compared with isolation after other storage conditions. For subclade S1, all samples with initial bacterial concentrations of more than 103 colonies/mL, under all storage conditions, were successfully cultured. These results suggest that storing contaminated water samples for 2 to 4 weeks in the dark at an ambient temperature prior to culturing can improve the isolation of Leptospira spp. from the samples. We implemented this protocol and collected water samples from natural sources accessed by both humans and animals. Leptospira spp. was identified in 32% (35/109) of water samples. The animal species using a water source influenced the likelihood of water samples being contaminated with Leptospira spp. Cultures of Leptospira spp. from environmental samples can provide useful information for understanding the complex interactions between humans, animals and the environment in the transmission of leptospirosis. Full article
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Review

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22 pages, 1691 KiB  
Review
Of Mice, Cattle, and Men: A Review of the Eco-Epidemiology of Leptospira borgpetersenii Serovar Ballum
by Marie Moinet, David A. Wilkinson, Danielle Aberdein, James C. Russell, Emilie Vallée, Julie M. Collins-Emerson, Cord Heuer and Jackie Benschop
Trop. Med. Infect. Dis. 2021, 6(4), 189; https://0-doi-org.brum.beds.ac.uk/10.3390/tropicalmed6040189 - 20 Oct 2021
Cited by 8 | Viewed by 3847
Abstract
In New Zealand (NZ), leptospirosis is a mostly occupational zoonosis, with >66% of the recently notified cases being farm or abattoir workers. Livestock species independently maintain Leptospira borgpetersenii serovar Hardjo and L. interrogans serovar Pomona, and both are included in livestock vaccines. The [...] Read more.
In New Zealand (NZ), leptospirosis is a mostly occupational zoonosis, with >66% of the recently notified cases being farm or abattoir workers. Livestock species independently maintain Leptospira borgpetersenii serovar Hardjo and L. interrogans serovar Pomona, and both are included in livestock vaccines. The increasing importance in human cases of Ballum, a serovar associated with wildlife, suggests that wildlife may be an overlooked source of infection. Livestock could also act as bridge hosts for humans. Drawing from disease ecology frameworks, we chose five barriers to include in this review based on the hypothesis that cattle act as bridge hosts for Ballum. Using a narrative methodology, we collated published studies pertaining to (a) the distribution and abundance of potential wild maintenance hosts of Ballum, (b) the infection dynamics (prevalence and pathogenesis) in those same hosts, (c) Ballum shedding and survival in the environment, (d) the exposure and competency of cattle as a potential bridge host, and (e) exposure for humans as a target host of Ballum. Mice (Mus musculus), rats (Rattus rattus, R. norvegicus) and hedgehogs (Erinaceus europaeus) were suspected as maintenance hosts of Ballum in NZ in studies conducted in the 1970s–1980s. These introduced species are distributed throughout NZ, and are present on pastures. The role of other wildlife in Ballum (and more broadly Leptospira) transmission remains poorly defined, and has not been thoroughly investigated in NZ. The experimental and natural Ballum infection of cattle suggest a low pathogenicity and the possibility of shedding. The seroprevalence in cattle appears higher in recent serosurveys (3 to 14%) compared with studies from the 1970s (0 to 3%). This review identifies gaps in the knowledge of Ballum, and highlights cattle as a potential spillover host. Further studies are required to ascertain the role that wild and domestic species may play in the eco-epidemiology of Ballum in order to understand its survival in the environment, and to inform control strategies. Full article
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