Leishmaniasis in the United States military veterinary patient population

Lauren M. Seal US Army Veterinary Corps, Public Health Activity, Fort Carson, CO

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Sara B. Mullaney Department of Chemistry and Life Science, US Military Academy, West Point, NY

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Sheldon G. Waugh US Army Public Health Center, Aberdeen Proving Ground, MD

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Abstract

OBJECTIVE

To describe the presence of Leishmania infection within the animal population receiving care from US Army Veterinary Services.

ANIMALS

629 canine, feline, and equine patients of US Army Veterinary Services from 2014 to 2017.

PROCEDURES

Personnel at the US Army Public Health Center ran a query within the Remote Online Veterinary Record system using previously validated search terms (eg, liesh, leish, and lesh) and returned data on any patient for which the master problem list included those terms. Next, a query was run to identify all leishmaniasis testing. Records identified by queries were reviewed manually, and data were collected on patient signalment, indication for and type of testing, location of testing, and previous locations or country of the patient.

RESULTS

Only dogs (n = 378), not cats or horses, had been tested for leishmaniasis, 54 (14.3%) of which tested positive for Leishmania infection. More specifically, 39 of 104 (37.5%) privately owned dogs tested positive, compared with 15 of 274 (5.6%) government-owned dogs. Overall, 186 dogs had no clinical signs, 12 (6.5%) of which tested positive. Forty-four of the 54 (81%) test-positive dogs were located in or had traveled to an endemic area.

CLINICAL RELEVANCE

The prevalence of leishmaniasis in the various subpopulations of dogs suggested the need for additional prevalence studies. Many animals travel in and out of the US, and repeated introduction of Leishmania spp could lead to this vector-borne disease becoming endemic in the US animal and human populations. Consequently, US veterinarians need to ensure proper testing and follow-up to protect one health.

Abstract

OBJECTIVE

To describe the presence of Leishmania infection within the animal population receiving care from US Army Veterinary Services.

ANIMALS

629 canine, feline, and equine patients of US Army Veterinary Services from 2014 to 2017.

PROCEDURES

Personnel at the US Army Public Health Center ran a query within the Remote Online Veterinary Record system using previously validated search terms (eg, liesh, leish, and lesh) and returned data on any patient for which the master problem list included those terms. Next, a query was run to identify all leishmaniasis testing. Records identified by queries were reviewed manually, and data were collected on patient signalment, indication for and type of testing, location of testing, and previous locations or country of the patient.

RESULTS

Only dogs (n = 378), not cats or horses, had been tested for leishmaniasis, 54 (14.3%) of which tested positive for Leishmania infection. More specifically, 39 of 104 (37.5%) privately owned dogs tested positive, compared with 15 of 274 (5.6%) government-owned dogs. Overall, 186 dogs had no clinical signs, 12 (6.5%) of which tested positive. Forty-four of the 54 (81%) test-positive dogs were located in or had traveled to an endemic area.

CLINICAL RELEVANCE

The prevalence of leishmaniasis in the various subpopulations of dogs suggested the need for additional prevalence studies. Many animals travel in and out of the US, and repeated introduction of Leishmania spp could lead to this vector-borne disease becoming endemic in the US animal and human populations. Consequently, US veterinarians need to ensure proper testing and follow-up to protect one health.

Introduction

Leishmania is a genus of vector-borne protozoa that causes new infections in up to 1.2 million people annually, making it the ninth largest individual infectious disease burden globally.1 Leishmaniasis, the associated disease, is endemic in 98 disease-reporting countries and disproportionally affects lower-income populations in Asia, Africa, and Latin America, earning the World Health Organization classification of a Neglected Tropical Disease.1 The protozoa can cause 3 forms of disease in humans: visceral (kala-azar), cutaneous, and mucocutaneous. The species causing the infection (eg, Leishmania infantum or chagasi, Leishmania donovani, and Leishmania braziliensis), its route of infection, and the immune response of the host all play a role in determining the clinical presentation of an individual.2 The most common route of transmission is a sand fly bite, either Lutzomyia spp or Phlebotomus spp, depending on the location. Additional, less common routes, including venereal transmission, vertical transmission (ie, from mother to offspring), and dog bites, warrant further scrutiny, as they may indicate a public health risk that has not been previously identified.3,4

Leishmaniasis is not currently endemic in the US, but cases of infection do occur. Multiple cases have been identified within the Department of Defense (DOD) animal population, including a retired military working dog (MWD).5 Animals can serve as sentinels for emerging vector-borne diseases entering the US (eg, West Nile Virus in birds in 19996), so it is important to monitor the occurrence of emerging vector-borne diseases in animals. Increases in the incidence or prevalence of leishmaniasis in animals could precede an increase in human cases, but no current estimates are available regarding the prevalence of Leishmania infection in US animal populations.

Leishmaniasis is a disease of great concern for the US military, and as military members continue to deploy to and be stationed in Leishmania-endemic areas, diagnoses in this population have increased. In a 2002 Morbidity and Mortality Weekly Report, the CDC recognized 22 cases of leishmaniasis in US service members who had deployed to Asia.7 Another study8 revealed a 2.1% infection rate during a 2004 survey of 15,549 deployed military personnel. A third study9 in 2019 found that 19.5% of 200 asymptomatic service members tested were positive for Leishmania infection. Thus, evaluation of the presence of leishmaniasis among privately owned animals (POAs) and government-owned animals (GOAs) would provide valuable information to both the Military Health System and the US public health community. The prevalence of leishmaniasis among animals within the DOD can serve as an indicator of the prevalence of disease in humans and allow researchers and public health professionals to observe and prevent future outbreaks.

The goal of the study reported here was to establish an epidemiological baseline of Leishmania cases in the DOD veterinary patient population. Specifically, we sought to evaluate the presence of Leishmania infection within Remote Online Veterinary Record (ROVR), the electronic medical records system for > 540,000 animals that receive care at DOD-owned veterinary treatment facilities (VTFs) globally. The animals in this population include GOAs as well as pets owned by service members. This specific animal population is likely at higher risk for Leishmania infection than the general US pet population because of the greater likelihood of global travel and diverse countries of origin, both of which include endemic areas.

Materials and Methods

Animals

A query of the ROVR system was performed to identify any of the following search terms in the master problem lists (MPLs) for all patients, which included dogs, cats, and horses: liesh, leish, and lesh (which would also identify any words containing these terms, such as leishmaniasis). All queries included any patient record from the implementation of ROVR (April 2014) through January 1, 2018. The MPL was entered into an animal patient’s record by the health-care provider in either free-text form or by selection of terms from a standard list. Use of the MPL varied by provider. Inclusion of Leishmania in the MPL indicated that the provider deemed the animal had leishmaniasis from a previous diagnosis or from the provider’s own clinical determination.

Next, a query was performed to identify all patients with record of a leishmaniasis test, including serum antibody titer measurement, patient-side antibody testing, PCR assay, and cytologic or histologic evaluation. Afterward, each individual patient record was reviewed to determine the indication for testing, test result, demographic information, current patient disposition, and travel history. Animals were included in the study if leishmaniasis was included in the MPL or there was evidence that a test for Leishmania infection had been performed. If no test result or discussion of testing could be found during the review, that patient was excluded from additional analysis.

Results

A total of 629 animals’ medical records met the criteria for record review. Of these, 251 (40.0%) animals were excluded because their records did not include test results, notes of Leishmania testing, or files from outside clinics to provide test results. Of the remaining 378 animals, 21 had leishmaniasis listed in their MPL (with or without test results in ROVR) and 357 had test results in ROVR. All tested animals were dogs.

Of the 378 dogs, 54 (14.3%) tested positive for Leishmania infection. These 54 dogs included 41 (76%) males and 13 (24%) females with a median age of 5 years (range, 1 to 18 years). The most common breed was German Shepherd Dog (15/54 [28%]). Fourteen of the 54 dogs that tested positive for Leishmania infection also tested positive for Trypanosoma cruzi infection, but so few had follow-up testing recorded that it was impossible to explore these results further.

Various types of tests were used to screen for or diagnose Leishmania infection (Table 1). Of the 378 dogs tested, 104 (27.5%) were recorded as POAs at the time of testing, of which 39 (37.5%) tested positive for Leishmania infection. A total of 274 (72.5%) dogs were recorded as GOAs, of which 15 (5.6%) tested positive.

Table 1

Results of tests for Leishmania infection for 378 dogs receiving care from the US Army Veterinary Services from 2014 through 2017 by the type of test performed.

Type of test* No. of dogs tested No. (%) positive
PCR assay 33 2 (6)
Immunofluorescence assay 325 46 (14)
Biopsy or fine-needle aspirate specimen evaluation 4 3 (75)
Patient-side ELISA 13 0 (0)
Unknown 3 3 (100)

*If ≥ 2 types of tests yielded different results (with 1 result being positive), the dog was counted among the number of positive dogs for the type of test that was positive. If ≥ 2 types of tests yielded the same result, the dog was counted among those considered positive by the less common test.

The indication for testing included wellness (presumably as a screening test; n = 186 [49.2%]) and illness (87 [23.0%]) or was unknown (105 [27.8%]). Of these dogs, 12 (6.5%), 30 (34.5%), and 12 (11.4%), respectively, had positive test results. In clinically normal dogs, Leishmania tests were often conducted as part of a semiannual examination (required for MWDs), a requirement for upcoming travel, or a requirement due to the dog having been adopted from or having traveled to an endemic area. In ill dogs, signs of disease included lethargy, decreased appetite, recurrent dermatologic disease, and enlarged lymph nodes. In situations when the reason for testing was unknown, most often the testing could not be associated with a specific examination or medical note that would indicate the cause for testing.

Of the 54 dogs that tested positive for Leishmania infection, 44 (81%) were in an endemic region or area at the time of diagnosis or had a documented history of travel to an endemic area (Figure 1). Ten dogs had no documented history of travel. Of those 10 dogs, 3 were POAs at the time of testing, and 1 was from the DOD MWD Breeding and Consignment Program, meaning it was bred by the program at Lackland Air Force Base, Texas. The remaining 6 dogs were owned by US Customs and Border Protection and had been purchased within the US.

Figure 1
Figure 1

Maps showing the geographic distribution of dogs receiving care from the US Army Veterinary Services from 2014 through 2017 that had positive results of testing for Leishmania infection. Blue shading indicates locations in which Leishmania infection was diagnosed. Numbers correspond to the number of cases of infection in those locations. Values in black represent dogs with no history of travel documented in the medical records, and values in gold represent dogs with a history of travel. *In Texas, 7 dogs had a documented history of travel and 6 others did not. Maps courtesy of Dr. Sheldon Waugh, US Census Bureau; used with permission.

Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.21.05.0226

Discussion

The present study provided new information relevant to the military veterinary and human medical communities. First and foremost, 10 Leishmania-positive dogs had no history of travel in their medical records. This finding suggested a need for more research to better understand infection within the US. Findings also indicated that a majority (44/54 [81%]) of Leishmania-positive dogs in this study had a documented history of travel to an endemic area or were in an endemic area when diagnosed. In other words, most cases of Leishmania infection were acquired in an endemic area. If this study represented the GOA and POA animal populations as a whole, prevention of most Leishmania infections could be directed toward limiting travel, testing animals prior to travel or on return from an endemic area, and using approved preventive products that protect against sand flies.

Our findings may also have indicated a greater risk of Leishmania infection within the ROVR population than previously appreciated. In a study10 reported in 2007, Leishmania testing of serum samples (immunofluorescence assay [IFA]; n = 32) and tissue samples (PCR assay; 36) from 64 MWDs stationed in the Mediterranean basin yielded no positive results.

The present study was not without limitations. One important limitation was the relatively small number of animals represented: only 378 dogs out of 540,000 animals in the ROVR population. As a result, no statistical analysis was possible and the generalizability of the findings is unclear. Findings did support the need for active surveillance for leishmaniasis in the ROVR population because animals seen by US Army Veterinary Services travel and deploy to endemic areas. Once there is a better understanding of leishmaniasis in this specific population, it can be determined whether more active surveillance in the general US animal population is necessary. Second, potentially 251 test results were not entered into the electronic medical records. The missing test results should be the subject of additional study, as they could substantially affect results of the present study. Third, the travel data had some limitations in that we were unable to confirm whether some of the dogs without a documented travel history were purchased overseas. For this reason, we could not confirm the number of positive dogs within the study that were infected within the US. Such confirmation must be a goal of future studies because of its importance to public health.

Other limitations concerned the specific diagnostic tests used in the study. A considerable number of dogs tested positive via IFA testing with a positive cutoff value of 1:128 (tested at a US confirmatory laboratory), while others were tested with a cutoff value of 1:50 (tested at a European confirmatory laboratory), creating challenges in interpreting positive results. In addition, many of the dogs with positive results of IFA were not retested, so it was impossible to confirm whether they were actively infected with L infantum. An additional major limitation of the testing used was the fact that dogs tested by IFA were only tested for L infantum, which means that we may have missed dogs infected with Leishmania mexicana and other Leishmania spp. Furthermore, Leishmania spp have cross-reactivity on IFA with the protozoan T cruzi, the causative agent of American trypanosomiasis, also known as Chagas disease. Chagas disease has become a concern in the MWD community, as it has an expanded geographic distribution throughout Texas. As a result, the US military routinely tests MWDs for Chagas disease. Because cross-reactivity can occur between these 2 protozoa, positive IFA results can be challenging to interpret, especially for individuals with nonspecific clinical signs or no evidence of clinical disease. Multiple studies have been conducted in attempts to evaluate this cross-reactivity with a wide range of results. One study11 found that 50% of animals experimentally infected with T cruzi tested positive for Leishmania spp on IFA or ELISA. Another study12 of 2 commercially available tests for Chagas disease found cross-reactivity rates of 18% (ELISA Chagas III) and 20% (Gold ELISA Chagas) in humans known to have Leishmania infection. These findings, along with the frequency with which MWDs are tested for Chagas disease, exacerbated the challenges of results interpretation for animals in the present study that tested positive for both infections. Very few of those animals had any additional testing recorded in ROVR. Although it was more likely that they were infected with T cruzi and the leishmaniasis test produced a false-positive result, further testing would be required to determine true infection status. Additional diagnostic testing (specifically for amastigotes in blood or tissue samples) must be performed for animals with a positive IFA result to determine whether the infection is due to Leishmania spp, T cruzi, or both. The results of the present study are valuable to the DOD veterinary and human medical communities in that they indicate a need for additional research, but our results should be interpreted with caution given the aforementioned limitations.

Overall, screening tests in the present study identified Leishmania infection in 6.5% of tested clinically normal dogs. It is important to consider that this population, if routinely tested, could serve as a sentinel for the presence of leishmaniasis cases in the US. Also noteworthy is that this study confirmed that animal travel is a method by which Leishmania spp are introduced to the US animal population, and there is reason to believe that repeated introduction of the protozoa is a threat to public health. Data presented here supported the need for additional, active surveillance for Leishmania spp within the companion animal population, specifically among POAs and GOAs. Although POAs and GOAs are not the only companion animals that travel globally, they can be more closely monitored as a subpopulation of the entire domestic animal population.

The presence of 135 globally distributed DOD-owned VTFs with a centrally managed electronic health record system (ie, ROVR) creates an opportunity to monitor diseases in this population. The life cycle of Leishmania spp demonstrates the close interconnections among humans, animals, vectors, and the environment. To fully understand and prevent leishmaniasis, a collaborative approach modeling the one-health concept is necessary. It is crucial for the medical community to recognize the risk of Leishmania infection within domestic human and animal populations and to initiate effective preventive measures to protect them. Veterinarians working in DOD-owned VTFs should be educated in the identification of leishmaniasis in companion animals, diagnosis of previous or active infection through appropriate testing, and accurate documentation of findings in the patient medial record. Human medical providers and veterinarians colocated on DOD installations should communicate regularly about all zoonotic diseases within their respective populations and develop collaborative plans for disease mitigation. A unique opportunity exists to harness the GOA and POA population for sentinel surveillance and to integrate a one-health approach to mitigate the potential domestic spread of leishmaniasis.

Acknowledgments

The authors declare that there were no conflicts of interest.

The views expressed in this publication are those of the authors and do not necessarily reflect the official policy or position of the US Department of the Army, US Department of Defense, or US Government.

The authors thank the US Army Public Health Center and the Remote Online Veterinary Record staff for their help in gathering and analyzing the data.

References

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    Naucke TJ, Lorentz S. First report of venereal and vertical transmission of canine leishmaniosis from naturally infected dogs in Germany. Parasit Vectors. 2012;5:67. doi:10.1186/1756-3305-5-67

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    Naucke TJ, Amelung S, Lorentz S. First report of canine leishmaniosis through bite wounds from a naturally infected dog in Germany. Parasit Vectors. 2016;9(1):256. doi:10.1186/s13071-016-1551-0

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    Mody RM, Lakhal-Naouar I, Sherwood JE, et al. Asymptomatic visceral Leishmania infantum infection in US soldiers deployed to Iraq. Clin Infect Dis. 2019;68(12):20362044.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Killian JW. The impact of leishmaniasis on military working dogs with Mediterranean basin exposure. US Army Med Dep J. 2007;2007(Jul–Sep):1725.

    • Search Google Scholar
    • Export Citation
  • 11.

    Zanette MF, Felix de Lima VM, Laurenti ND, et al. Serological cross-reactivity of Trypanosoma cruzi, Ehrlichia canis, Toxoplasma gondii, Neospora caninum and Babesia canis to Leishmania infantum chagasi tests in dogs. Rev Soc Bras Med Trop. 2014;47(1):105107.

    • Crossref
    • Search Google Scholar
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  • 12.

    Daltro RT, Leony LM, Freitas NEM, et al. Cross-reactivity using chimeric Trypanosoma cruzi antigens: diagnostic performance in settings where Chagas disease and American cutaneous or visceral leishmaniasis are coendemic. J Clin Microbiol. 2019;57(8):e0076219. doi:10.1128/JCM.00762-19

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Figure 1

    Maps showing the geographic distribution of dogs receiving care from the US Army Veterinary Services from 2014 through 2017 that had positive results of testing for Leishmania infection. Blue shading indicates locations in which Leishmania infection was diagnosed. Numbers correspond to the number of cases of infection in those locations. Values in black represent dogs with no history of travel documented in the medical records, and values in gold represent dogs with a history of travel. *In Texas, 7 dogs had a documented history of travel and 6 others did not. Maps courtesy of Dr. Sheldon Waugh, US Census Bureau; used with permission.

  • 1.

    Alvar J, Vélez ID, Bern C, et al. Leishmaniasis worldwide and global estimates of its incidence. PLoS One. 2012;7(5):e35671. doi:10.1371/journal.pone.0035671

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2.

    Roberts LJ, Handman E, Foote SJ. Science, medicine, and the future: leishmaniasis. BMJ. 2000;321(7264):801804.

  • 3.

    Naucke TJ, Lorentz S. First report of venereal and vertical transmission of canine leishmaniosis from naturally infected dogs in Germany. Parasit Vectors. 2012;5:67. doi:10.1186/1756-3305-5-67

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4.

    Naucke TJ, Amelung S, Lorentz S. First report of canine leishmaniosis through bite wounds from a naturally infected dog in Germany. Parasit Vectors. 2016;9(1):256. doi:10.1186/s13071-016-1551-0

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5.

    Scruggs JL, Weber KA. Pathology in Practice. J Am Vet Med Assoc. 2017;251(12):13911393.

  • 6.

    Murray KO, Mertens E, Despres P. West Nile Virus and its emergence in the United States of America. Vet Res. 2010;41(6):67. doi:10.1051/vetres/2010039

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    CDC. Cutaneous leishmaniasis in US military personnel—Southwest/Central Asia, 2002–2003. MMWR Morb Mortal Wkly Rep. 2003;52(42):10091012.

    • Search Google Scholar
    • Export Citation
  • 8.

    Beaumier CM, Gomez-Rubio AM, Hotez PJ, Weina PJ. United States military tropical medicine: extraordinary legacy, uncertain future. PLoS Negl Trop Dis. 2013;7(12):e2448. doi:10.1371/journal.pntd.0002448

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Mody RM, Lakhal-Naouar I, Sherwood JE, et al. Asymptomatic visceral Leishmania infantum infection in US soldiers deployed to Iraq. Clin Infect Dis. 2019;68(12):20362044.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Killian JW. The impact of leishmaniasis on military working dogs with Mediterranean basin exposure. US Army Med Dep J. 2007;2007(Jul–Sep):1725.

    • Search Google Scholar
    • Export Citation
  • 11.

    Zanette MF, Felix de Lima VM, Laurenti ND, et al. Serological cross-reactivity of Trypanosoma cruzi, Ehrlichia canis, Toxoplasma gondii, Neospora caninum and Babesia canis to Leishmania infantum chagasi tests in dogs. Rev Soc Bras Med Trop. 2014;47(1):105107.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Daltro RT, Leony LM, Freitas NEM, et al. Cross-reactivity using chimeric Trypanosoma cruzi antigens: diagnostic performance in settings where Chagas disease and American cutaneous or visceral leishmaniasis are coendemic. J Clin Microbiol. 2019;57(8):e0076219. doi:10.1128/JCM.00762-19

    • Crossref
    • Search Google Scholar
    • Export Citation

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