Advertisement

EcoHealth

pp 1–11 | Cite as

Giardia Infection and Trypanosoma Cruzi Exposure in Dogs in the Bosawás Biosphere Reserve, Nicaragua

  • Amber F. Roegner
  • Miles E. Daniels
  • Woutrina A. Smith
  • Nicole Gottdenker
  • Laura M. Schwartz
  • James Liu
  • Amanda Campbell
  • Christine V. FiorelloEmail author
Original Contribution
  • 11 Downloads

Abstract

Indigenous Mayangna and Miskitu inhabit Nicaragua’s remote Bosawás Biosphere Reserve, located in the North Caribbean Coast Autonomous Region. They are sedentary horticulturists who supplement their diet with wild game, hunting with the assistance of dogs. To test whether hunting dogs increased the risk of human exposure to protozoal zoonotic neglected tropical diseases (NTDs), we sampled dogs from three communities varying in population size and level of contact with other communities. We screened dog feces (n = 58) for Giardia and Cryptosporidium DNA and sera (n = 78) for Trypanosoma cruzi antibodies and DNA. Giardia DNA was detected in 22% (13/58) of samples; sequencing revealed the presence of both zoonotic genotypes (assemblages A and B) and dog-specific genotypes (assemblages C and D). Giardia shedding was associated with community and age. Older dogs and those in the two, more accessible communities had greater odds of shedding parasites. Seroprevalence of T. cruzi antibodies, indicating prior exposure, was 9% (7/78). These results contribute to the limited literature on NTDs in indigenous populations, and suggest hunting dogs can both serve as sentinels of environmental NTDs and pose zoonotic risk for their owners and communities.

Keywords

Bosawás Domestic dogs Giardia Nicaragua Trypanosoma cruzi Indigenous health 

Notes

Acknowledgements

We thank U. Coleman, O. Dixon, F. Diaz-Santos, F. Gonzales, G. Gonzales, J. Foley, L. Hull, J. Koster, P. Rodriguez, C. Gonzales, J. Saucier, L. Faherty, K. Thomas, and L. Shender for technical and logistic assistance, the Campbell Pet Company for in-kind support, and three anonymous reviewers for valuable comments on the manuscript.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Approval

All applicable institutional and/or national guidelines for the care and use of animals were followed.

Supplementary material

10393_2019_1434_MOESM1_ESM.csv (4 kb)
S1Dataset. Original data for dogs in three communities of the Bosawás Reserve, Nicaragua, documenting exposure to or infection with Giardia, Cryptosporidium, and Trypanosoma cruzi. The first tab (“Giardia & Crypto”) includes results of 58 dogs tested via PCR for Giardia and Cryptosporidium. The second tab (“Giardia tables”) shows Giardia Assemblage information as well as summary tables and chi-square tests of location, sex, and age and logistic regression results for location. The third tab (“Chagas PCR”) shows results of 58 dogs tested via PCR for T. cruzi. The fourth and final tab (“Chagas serology”) shows results of two serologic tests performed on serum of dogs, the RAPID test performed on a small number of dogs, and confirmatory tests performed on those dogs returning positive results, as well as results of the confirmatory test performed at TVMDL performed (at a later date) on those dogs that were not tested initially with the RAPID test. (CSV 3 kb)

References

  1. Adell AD, Smith WA, Shapiro K, Melli A, Conrad PA (2014) Molecular epidemiology of Cryptosporidium spp and Giardia spp in mussels (Mytilus californianus) and California sea lions (Zalophus californianus) from central California. Applied Environmental Microbiology 80(24):7732–7740;  https://doi.org/10.1128/aem.02922-14 [October 3, 2014]CrossRefGoogle Scholar
  2. Aguirre AA (2009) Wild canids as sentinels of ecological health: a conservation medicine perspective. Parasites and Vectors 2(Suppl 1):S7;  https://doi.org/10.1186/1756-3305-2-s1-s7 CrossRefGoogle Scholar
  3. Alroy KA, Huang C, Gilman RH, Quispe-Machaca VR, Marks MA, Ancca-Juarez J, et al. (2015) Prevalence and transmission of Trypanosoma cruzi in people of rural communities of the high jungle of Northern Peru. PLoS Neglected Tropical Disease 9(5):e0003779;  https://doi.org/10.1371/journal.pntd.0003779 [Online May 2015]CrossRefGoogle Scholar
  4. Ballweber LR, Xiao L, Bowman DD, Kahn G, Cama VA (2010) Giardiasis in dogs and cats: update on epidemiology and public health significance. Trends in Parasitology 26(4):180–9;  https://doi.org/10.1016/j.pt.20https://doi.org/10.02.005 CrossRefGoogle Scholar
  5. Bouzid M, Halai K, Jeffreys D, Hunter PR (2015) The prevalence of Giardia infection in dogs and cats, a systematic review and meta-analysis of prevalence studies from stool samples. Veterinary Parasitology 207(3–4):181–202;  https://doi.org/10.1016/j.vetpar.2014.12.011 [Online December 27, 2014]
  6. Bryan HM, Darimont CT, Paquet PC, Ellis JA, Goji N, Gouix M, et al (2011) Exposure to infectious agents in dogs in remote coastal British Columbia: Possible sentinels of diseases in wildlife and humans. Canadian Journal of Veterinary Research 75(1):11–17.Google Scholar
  7. Cardinal MV, Castanera MB, Lauricella MA, Cecere MC, Ceballos LA, Vazquez-Prokopec GM, et al (2006) A prospective study of the effects of sustained vector surveillance following community-wide insecticide application on Trypanosoma cruzi infection of dogs and cats in rural Northwestern Argentina. American Journal of Tropical Medicine and Hygiene 75(4):753–761.CrossRefGoogle Scholar
  8. Chaves LF, Calzada JE, Rigg C, Valderrama A, Gottdenker NL, Saldaña A (2013) Leishmaniasis sand fly vector density reduction is less marked in destitute housing after insecticide thermal fogging. Parasites and Vectors 6: 164–177;  https://doi.org/10.1186/1756-3305-6-164 [Online June 6, 2013]
  9. Chiurillo MA, Crisante, G, Rojas, A, Peralta, A, Dias, M, Guevara, P, et al (2003) Detection of Trypanosoma cruzi and Trypanosoma rangeli infection by duplex PCR assay based on telomeric sequences. Clinical and Diagnostic Laboratory Immunology 10:775–779;  https://doi.org/10.1128/cdli.10.5.775-779.2003 Google Scholar
  10. Coura JR, Vinas PA, Junqueira AC (2014) Ecoepidemiology, short history and control of Chagas disease in the endemic countries and the new challenge for non-endemic countries. Memórias do Instituto Oswaldo Cruz 109(7):856–862;  https://doi.org/10.1590/0074-0276140236 [online October 21, 2014]
  11. Coura JR, Junqueira AC, Giordano CM, Funatsu RK (1994) Chagas’ disease in the Brazilian Amazon. I–A short review. Revista do Instituto de Medicina Tropical de São Paulo 36(4):363–368.Google Scholar
  12. Esch KJ, Petersen CA (2013) Transmission and epidemiology of zoonotic protozoal diseases of companion animals. Clinical Microbiology Review 26(1):58–85;  https://doi.org/10.1128/cmr.00067-12
  13. Fan CK, Su KE, Chung WC, Tsai YJ, Chiou HY, Lin CF, et al (1998) Seroprevalence of Toxoplasma gondii antibodies among Atayal aboriginal people and their hunting dogs in northeastern Taiwan. Japanese Journal of Medical Science 51(1):35–42.Google Scholar
  14. Feng Y, Xiao L (2011) Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clinical Microbiology Review 24(1):110–140;  https://doi.org/10.1128/cmr.00033-10
  15. Fiorello CF, Straub MH, Schwartz LM, Liu J, Campbell A, Kownacki AK, Foley JE (2017) Multiple-host pathogens in domestic hunting dogs in Nicaragua’s Bosawás Biosphere Reserve. Acta Tropica 167: 183–190;  https://doi.org/10.1016/j.actatropica.2016.12.020
  16. Fontanarrosa MF, Vezzani D, Basabe J, Eiras DF (2006) An epidemiological study of gastrointestinal parasites of dogs from Southern Greater Buenos Aires (Argentina): age, gender, breed, mixed infections, and seasonal and spatial patterns. Veterinary Parasitology 136(3):283–295;  https://doi.org/10.1016/j.vetpar.2005.11.012
  17. Fung HL, Calzada J, Saldaña A, Santamaria AM, Pineda V, Gonzalez K, et al (2014) Domestic dog health worsens with socio-economic deprivation of their home communities. Acta Tropica 135: 67–74;  https://doi.org/10.1016/j.actatropica.2014.03.010 [Online March 26, 2014]
  18. Gracey M, King M (2009) Indigenous health part 1: determinants and disease patterns. Lancet 374(9683):65–75;  https://doi.org/10.1016/s0140-6736(09)60914-4
  19. Gurtler RE, Cecere MC, Lauricella MA, Cardinal MV, Kitron U, Cohen JE (2007) Domestic dogs and cats as sources of Trypanosoma cruzi infection in rural northwestern Argentina. Parasitology 134(Pt 1):69–82;  https://doi.org/10.1017/s0031182006001259 [Online October 11, 2006]
  20. Gurtler RE, Cecere MC, Lauricella MA, Petersen RM, Chuit R, Segura EL, et al (2005) Incidence of Trypanosoma cruzi infection among children following domestic reinfestation after insecticide spraying in rural northwestern Argentina. American Journal of Tropical Medicine and Hygiene 73(1):95–103.CrossRefGoogle Scholar
  21. Himsworth CG, Skinner S, Chaban B, Jenkins E, Wagner BA, Harms NJ, et al. (2010a) Multiple zoonotic pathogens identified in canine feces collected from a remote Canadian indigenous community. The American Journal of Tropical Medicine and Hygiene 83(2):338–341;  https://doi.org/10.4269/ajtmh.2010.10-0137
  22. Himsworth CG, Jenkins E, Hill JE, Nsungu M, Ndao M, Thompson RC, et al (2010b) Emergence of sylvatic Echinococcus granulosus as a parasitic zoonosis of public health concern in an indigenous community in Canada. American Journal of Tropical Medicine and Hygiene 82(4):643–645;  https://doi.org/10.4269/ajtmh.2010.09-0686
  23. Hotez PJ, Bottazzi ME, Franco-Paredes C, Ault SK, Periago MR (2008) The neglected tropical diseases of Latin America and the Caribbean: a review of disease burden and distribution and a roadmap for control and elimination. PLoS Neglected Tropical Diseases 2(9):e300;  https://doi.org/10.1371/journal.pntd.0000300
  24. Koster J, Tankersley KB (2012) Heterogeneity of hunting ability and nutritional status among domestic dogs in lowland Nicaragua. Proceedings of the National Academy of Sciences, USA 109(8):E463–E70;  https://doi.org/10.1073/pnas.1112515109. [Online January 9, 2012]
  25. Koster JM (2008a) Hunting with dogs in Nicaragua: an optimal foraging approach. Current Anthropology 49(5):935–944.Google Scholar
  26. Koster J (2008b) The impact of hunting with dogs on wildlife harvests in the Bosawas Reserve, Nicaragua. Environmental Conservation 35(3):211–20;  https://doi.org/10.1017/S0376892908005055
  27. Lebbad M, Ankarklev J, Tellez A, Leiva B, Andersson JO, Svard S (2008) Dominance of Giardia assemblage B in Leon, Nicaragua. Acta Tropica 106(1):44–53;  https://doi.org/10.1016/j.actatropica.2008.01.004 [Online January 31, 2008]
  28. Morgan UM, Constantine CC, Forbes DA, Thompson RC (1997) Differentiation between human and animal isolates of Cryptosporidium parvum using rDNA sequencing and direct PCR analysis. Journal of Parasitology 83(5):825–830CrossRefGoogle Scholar
  29. Montenegro RA, Stephens C (2006) Indigenous health in Latin America and the Caribbean. Lancet 367(9525):1859–1869;  https://doi.org/10.1016/s0140-6736(06)68808-9
  30. Mundim MJ, Rosa LA, Hortencio SM, Faria ES, Rodrigues RM, Cury MC (2007) Prevalence of Giardia duodenalis and Cryptosporidium spp. in dogs from different living conditions in Uberlandia, Brazil. Veterinary Parasitology 144(3–4):356–359;  https://doi.org/10.1016/j.vetpar.2006.09.039 [November 16, 2006]
  31. Munoz-Antoli C, Pavon A, Marcilla A, Toledo R, Esteban JG (2011) Prevalence and molecular characterization of Cryptosporidium in schoolchildren from department of Rio San Juan (Nicaragua). Tropical Biomedicine 28(1):40–47.Google Scholar
  32. Nieto PD, Boughton R, Dorn PL, Steurer F, Raychaudhuri S, Esfandiari J, et al (2009) Comparison of two immunochromatographic assays and the indirect immunofluorescence antibody test for diagnosis of Trypanosoma cruzi infection in dogs in south central Louisiana. Veterinary Parasitology 165(3–4):241–247;  https://doi.org/10.1016/j.vetpar.2009.07.010 [July 15, 2009]
  33. Palma-Guzman R, Rivera B, Morales G (1996) Domestic vectors of Chagas’ disease in three rural communities of Nicaragua. Revista do Instituto de Medicina Tropical de São Paulo 38(2):133–140.CrossRefGoogle Scholar
  34. Pineda V, Saldana A, Monfante I, Santamaria A, Gottdenker NL, Yabsley MJ, et al (2011) Prevalence of trypanosome infections in dogs from Chagas disease endemic regions in Panama, Central America. Veterinary Parasitology 178(3–4):360–363;  https://doi.org/10.1016/j.vetpar.2010.12.043 [January 11, 2011]
  35. R Development Core Team (2017) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
  36. Read CM, Monis PT, Andrew Thompson RC (2004) Discrimination of all genotypes of Giardia duodenalis at the glutamate dehydrogenase locus using PCR-RFLP. Infection, Genetics and Evolution 4(2):125–130;  https://doi.org/10.1016/j.meegid.2004.02.001 [Online April 9, 2004]
  37. Rivera T, Palma-Guzman R, Morales W (1995) Seroepidemiological and clinical study of Chagas’ disease in Nicaragua. Revista do Instituto de Medicina Tropical de São Paulo 37(3):207–213.CrossRefGoogle Scholar
  38. Rossle NF, Latif B (2013) Cryptosporidiosis as threatening health problem: A review. Asian Pacific Journal of Tropical of Biomedicine 13(11):916–924;  https://doi.org/10.1016/s2221-1691(13)60179-3
  39. Ryan U, Cacciò SM (2013) Zoonotic potential of Giardia. International Journal of Parasitology 43(12):943–956;  https://doi.org/10.1016/j.ijpara.2013.06.001 [Online July 13, 2013].
  40. Saldaña A, Calzada, JE, Pineda V, Perea M, Rigg C, González K, et al (2015) Risk factors associated with Trypanosoma cruzi exposure in domestic dogs from a rural community in Panama. Memórias do Instituto Oswaldo Cruz 110(7):936–944;  https://doi.org/10.1590/0074-02760150284
  41. Schurer JM, Phipps K, Okemow C, Beatch H, Jenkins E (2015) Stabilizing dog populations and improving animal and public health through a participatory approach in Indigenous communities. Zoonoses Public Health 62(6):445–455;  https://doi.org/10.1111/zph.12173 [Online November 28, 2014]
  42. Schurer JM, Hill JE, Fernando C, Jenkins EJ (2012) Sentinel surveillance for zoonotic parasites in companion animals in indigenous communities of Saskatchewan. The American Journal of Tropical Medicine and Hygiene 87(3):495–498;  https://doi.org/10.4269/ajtmh.2012.12-0273 CrossRefGoogle Scholar
  43. Sequeira M, Espinoza H, Amador JJ, Domingo G, Quintanilla M, and de los Santos T (2010) Chagas disease in Nicaragua. Seattle, Washington: PATH; https://www.path.org/publications/files/TS_nicaragua_chagas_rpt.pdf [Accessed January 28, 2018]
  44. Smith JH (2003) Land-cover assessment of conservation and buffer zones in the BOSAWAS natural resource reserve of Nicaragua. Environmental Management 31(2):252–262;  https://doi.org/10.1007/s00267-002-2774-8
  45. Snelling WJ, Xiao L, Ortega-Pierres G, Lowery CJ, Moore JE, Rao JR, et al (2007) Cryptosporidiosis in developing countries. The Journal of Infection in Developing Countries 1(3):242–256.CrossRefGoogle Scholar
  46. Stephens C, Porter J, Nettleton C, Willis R (2006) Disappearing, displaced, and undervalued: a call to action for Indigenous health worldwide. Lancet 367(9527):2019–2028Google Scholar
  47. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology Evolution 30(12):2725–2729;  https://doi.org/10.1093/molbev/mst197 [Online October 16, 2013)
  48. Tenney TD, Curtis-Robles R, Snowden KF, Hamer SA (2014) Shelter dogs as sentinels for Trypanosoma cruzi transmission across Texas. Emerging Infectious Diseases 20(8):1323–1326;  https://doi.org/10.3201/eid2008.131843.
  49. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25(24):4876–4882.CrossRefGoogle Scholar
  50. Thompson RC, Reynoldson JA, Mendis AH (1993) Giardia and giardiasis. Advances in Parasitology 32:71–160.Google Scholar
  51. Titilincu A, Mircean V, Achelaritei D, Cozma V (2010) Prevalence of Cryptosporidium spp. in asymptomatic dogs by ELISA and risk factors associated with infection. Lucrări Ştiinłifice Medicină Veterinara XLIII(I):7–1;  https://doi.org/10.1155/2016/4591238 [Online January 3, 2016]
  52. Zeledon R, Marin F, Calvo N, Lugo E, Valle S (2006) Distribution and ecological aspects of Rhodnius pallescens in Costa Rica and Nicaragua and their epidemiological implications. Memórias do Institut Oswaldo Cruz 101(1):75–79;  https://doi.org/10.1590/s0074-02762006000100014

Copyright information

© EcoHealth Alliance 2019

Authors and Affiliations

  • Amber F. Roegner
    • 1
    • 5
  • Miles E. Daniels
    • 1
    • 2
  • Woutrina A. Smith
    • 1
  • Nicole Gottdenker
    • 3
  • Laura M. Schwartz
    • 4
  • James Liu
    • 4
    • 6
  • Amanda Campbell
    • 4
  • Christine V. Fiorello
    • 1
    • 7
    Email author
  1. 1.One Health Institute, School of Veterinary MedicineUniversity of CaliforniaDavisUSA
  2. 2.Institute of Marine SciencesUniversity of CaliforniaSanta CruzUSA
  3. 3.Department of Pathology, College of Veterinary MedicineUniversity of GeorgiaAthensUSA
  4. 4.Veterinary Medical Teaching Hospital, School of Veterinary MedicineUniversity of CaliforniaDavisUSA
  5. 5.School of Natural ResourcesUniversity of Nebraska-LincolnLincolnUSA
  6. 6.The Turtle ConservancyNew YorkUSA
  7. 7.Albuquerque BioParkAlbuquerqueUSA

Personalised recommendations