Skip to main content Accessibility help
×
Home

A survey of zoonotic pathogens carried by house mouse and black rat populations in Yucatan, Mexico

  • J. A. PANTI-MAY (a1), R. R. C. DE ANDRADE (a2), Y. GURUBEL-GONZÁLEZ (a3), E. PALOMO-ARJONA (a3), L. SODÁ-TAMAYO (a3), J. MEZA-SULÚ (a3), M. RAMÍREZ-SIERRA (a4), E. DUMONTEIL (a4) (a5), V. M. VIDAL-MARTÍNEZ (a6), C. MACHAÍN-WILLIAMS (a7), D. DE OLIVEIRA (a2), M. G. REIS (a2), M. A. TORRES-CASTRO (a8), M. R. ROBLES (a9), S. F. HERNÁNDEZ-BETANCOURT (a3) and F. COSTA (a2) (a10)...

Summary

The house mouse (Mus musculus) and the black rat (Rattus rattus) are reservoir hosts for zoonotic pathogens, several of which cause neglected tropical diseases (NTDs). Studies of the prevalence of these NTD-causing zoonotic pathogens, in house mice and black rats from tropical residential areas are scarce. Three hundred and two house mice and 161 black rats were trapped in 2013 from two urban neighbourhoods and a rural village in Yucatan, Mexico, and subsequently tested for Trypanosoma cruzi, Hymenolepis diminuta and Leptospira interrogans. Using the polymerase chain reaction we detected T. cruzi DNA in the hearts of 4·9% (8/165) and 6·2% (7/113) of house mice and black rats, respectively. We applied the sedimentation technique to detect eggs of H. diminuta in 0·5% (1/182) and 14·2% (15/106) of house mice and black rats, respectively. Through the immunofluorescent imprint method, L. interrogans was identified in 0·9% (1/106) of rat kidney impressions. Our results suggest that the black rat could be an important reservoir for T. cruzi and H. diminuta in the studied sites. Further studies examining seasonal and geographical patterns could increase our knowledge on the epidemiology of these pathogens in Mexico and the risk to public health posed by rodents.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      A survey of zoonotic pathogens carried by house mouse and black rat populations in Yucatan, Mexico
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      A survey of zoonotic pathogens carried by house mouse and black rat populations in Yucatan, Mexico
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      A survey of zoonotic pathogens carried by house mouse and black rat populations in Yucatan, Mexico
      Available formats
      ×

Copyright

Corresponding author

*Author for correspondence: J. A. Panti-May, Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán, Merida, Mexico. (Email: panti.alonso@gmail.com)

References

Hide All
1. Battersby, S, Hirschhorn, RB, Amman, BR. Commensal rodents. In: Bonnefoy, X, Kampen, H, Sweeney, K, eds. Public Health Significance of Urban Pests. Copenhagen: World Health Organization, 2008, pp. 387419.
2. Pimentel, D, Zuniga, R, Morrison, D. Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 2005; 52: 273288.
3. Himsworth, CG, et al. Rats, cities, people, and pathogens: a systematic review and narrative synthesis of literature regarding the ecology of rat-associated zoonoses in urban centers. Vector Borne and Zoonotic Diseases 2013; 13: 349359.
4. World Health Organization. Neglected tropical diseases (http://www.who.int/neglected_diseases/diseases/en/). Accessed 25 November 2016.
5. Sánchez-Montes, S, et al. Leptospirosis in Mexico: epidemiology and potential distribution of human cases. PLoS ONE 2015; 10: e0133720.
6. Carabarin-Lima, A, et al. Chagas disease (American trypanosomiasis) in Mexico: an update. Acta Tropica 2013; 127: 126135.
7. Mason, PR, Patterson, BA. Epidemiology of Hymenolepis nana infections in primary school children in urban and rural communities in Zimbabwe. Journal of Parasitology 1994; 80: 245250.
8. Mirdha, BR, Samantray, JC. Hymenolepis nana: a common cause of paediatric diarrhoea in urban slum dwellers in India. Journal of Tropical Pediatrics 2002; 48: 331334.
9. Thompson, RCA. Neglected zoonotic helminths: Hymenolepis nana, Echinococcus canadensis and Ancylostoma ceylanicum . Clinical Microbiology and Infection 2015; 21: 426432.
10. Hotez, PJ, et al. An unfolding tragedy of Chagas disease in North America. PLoS Neglected Tropical Diseases 2013; 7: e2300.
11. World Health Organization. Chagas disease in Latin America: an epidemiological update based on 2010 estimates. Weekly Epidemiological Record 2015; 90: 3344.
12. Waleckx, E, Gourbière, S, Dumonteil, E. Intrusive versus domiciliated triatomines and the challenge of adapting vector control practices against Chagas disease. Memorias do Instituto Oswaldo Cruz 2015; 110: 324338.
13. Lima, MM, et al. Investigation of Chagas disease in four periurban areas in northeastern Brazil: epidemiologic survey in man, vectors, non-human hosts and reservoirs. Transactions of the Royal Society of Tropical Medicine and Hygiene 2012; 106: 143149.
14. Pinto, CM, et al. Infection by trypanosomes in marsupials and rodents associated with human dwellings in Ecuador. Journal of Parasitology 2006; 92: 12511255.
15. Ko, AI, Goarant, C, Picardeau, M. Leptospira: the dawn of the molecular genetics era for an emerging zoonotic pathogen. Nature Reviews Microbiology 2009; 7: 736747.
16. Costa, F, et al. Global morbidity and mortality of leptospirosis: a systematic review. PLoS Neglected Tropical Diseases 2015; 9: e0003898.
17. Athanazio, DA, et al. Rattus norvegicus as a model for persistent renal colonization by pathogenic Leptospira interrogans . Acta Tropica 2008; 105: 176180.
18. Costa, F, et al. Influence of household rat infestation on Leptospira transmission in the urban slum environment. PLoS Neglected Tropical Diseases 2014; 8: e3338.
19. Costa, F, et al. Surveillance for leptospirosis in the Americas, 1996–2005: a review of data from ministries of health. Revista Panamericana de Salud Publica 2012; 32: 169177.
20. Nkouawa, A, et al. Cryptic diversity in hymenolepidid tapeworms infecting humans. Parasitology International 2016; 65: 8386.
21. Edelman, MH, et al. Hymenolepis diminuta (rat tapeworm) infection in man. American Journal of Medicine 1965; 38: 951953.
22. Baker, DG. Parasites of rats and mice. In: Baker, DG, ed. Flynn's Parasites of Laboratory Animals, 2nd edn. Iowa: Blackwell Publishing, 2007, pp. 303397.
23. Chero, JC, et al. Hymenolepis nana infection: symptoms and response to nitazoxanide in field conditions. Transactions of the Royal Society of Tropical Medicine and Hygiene 2007; 101: 203205.
24. Martínez-Barbabosa, I, et al. Infección por Hymenolepis diminuta en una estudiante universitaria. Revista Biomédica 2012; 23: 6164.
25. Bacigalupo, J. Infestation by Hymenolepis nana . Archivos Argentinos de Enfermedades del Apararato Disgestivo y Nutricion 1932; 7: 359364.
26. Luney, FW. Hymenolepis diminuta (rat tapeworm) in man. Canadian Medical Association Journal 1934; 30: 385386.
27. Guzman-Tapia, Y, Ramírez-Sierra, MJ, Dumonteil, E. Urban infestation by Triatoma dimidiata in the city of Mérida, Yucatán, México. Vector Borne and Zoonotic Diseases 2007; 7: 597606.
28. Dumonteil, E, et al. Geographic distribution of Triatoma dimidiata and transmission dynamics of Trypanosoma cruzi in the Yucatan peninsula of Mexico. American Journal of Tropical Medicine and Hygiene 2002; 67: 176183.
29. Vado-solís, IA, et al. Estudio de casos clínicos e incidencia de leptospirosis humana en el estado de Yucatán, México durante el período 1998 a 2000. Revista Biomédica 2002; 13: 157164.
30. Vado-Solís, I, et al. Clinical-epidemiological study of leptospirosis in humans and reservoirs in Yucatán, México. Revista do Instituto de Medicina Tropical Sao Paulo 2002; 44: 335340.
31. Torres-Castro, MA, et al. First molecular evidence of Leptospira spp. in synanthropic rodents captured in Yucatan, Mexico. Revue de Medecine Veterinaire 2014; 7–8: 213218.
32. Duarte-Zapata, L, Escalante-Triay, F, López-Novelo de Ceballos, M. Prevalencia de parasitosis intestinal en población de clase media de la ciudad de Mérida. Gaceta Medica de Mexico 1984; 120: 193197.
33. Rodriguez-Pérez, MA, et al. Lessons from a study in a rural community from southern Mexico: risk factors associated to transmission and reinfection of gastrointestinal parasites after albendazole treatment. Research and Reports in Tropical Medicine 2011; 2: 147153.
34. Panti-May, JA, et al. Infection levels of intestinal helminths in two commensal rodent species from rural households in Yucatan, Mexico. Journal of Helminthology 2015; 89: 4248.
35. Instituto Nacional de Estadística y Geografía. Inventario nacional de viviendas (http://www3.inegi.org.mx/sistemas/mapa/inv/Default.aspx?bi=1). Accessed 25 May 2013.
36. Panti-May, JA, et al. Population characteristics of human-commensal rodents present in households from Mérida, Yucatán, México. Manter Journal Parasite Biodiversity 2016; 5: 16.
37. Leary, S, et al. AVMA Guidelines for the Euthanasia of Animals: 2013 Edition. Schaumburg, Illinois: American Veterinary Medical Association, 2013, p. 102.
38. Moser, DR, Kirchhoff, LV, Donelson, JE. Detection of Trypanosoma cruzi by DNA amplification using the polymerase chain reaction. Journal of Clinical Microbiology 1989; 27: 14771482.
39. World Health Organization. Bench Aids for the Diagnosis of Intestinal Parasites, 4th edn. Geneva: World Health Organization, 2012, p. 20.
40. Chagas-Junior, AD, et al. An imprint method for detecting leptospires in the hamster model of vaccine-mediated immunity for leptospirosis. Journal of Medical Microbiology 2009; 58: 16321637.
41. Gómez Villafañe, IE, et al. Differences in population parameters of Rattus norvegicus in urban and rural habitats of central Argentina. Mammalia 2013; 77: 187193.
42. McDonald, JH. Handbook of Biological Statistics, 3rd edn. Baltimore, Maryland: Sparky House Publishing, 2014, p. 299.
43. Panti-May, JA, et al. Detection of Rickettsia felis in wild mammals from three municipalities in Yucatan, Mexico. Ecohealth 2015; 12: 523527.
44. Torres-Castro, MA, et al. First molecular evidence of Toxoplasma gondii in synanthropic rodents (Mus musculus and Rattus rattus) captured in Yucatan, Mexico. Revue de Medecine Veterinaire 2016; 169: 250255.
45. Andrade, LO, Andrews, NW. The Trypanosoma cruzi–host-cell interplay: location, invasion, retention. Nature Reviews Microbiology 2005; 3: 819823.
46. Zhang, L, Tarleton, RL. Parasite persistence correlates with disease severity and localization in chronic Chagas’ disease. Journal of Infectious Diseases 1999; 180: 480486.
47. Herrera, CP, et al. Genotype diversity of Trypanosoma cruzi in small rodents and Triatoma sanguisuga from a rural area in New Orleans, Louisiana. Parasites & Vectors 2015; 8: 19.
48. Galuppo, S, et al. Predominance of Trypanosoma cruzi genotypes in two reservoirs infected by sylvatic Triatoma infestans of an endemic area of Chile. Acta Tropica 2009; 111: 9093.
49. Zavala-Velázquez, J, et al. Infection by Trypanosoma cruzi in mammals in Yucatan, Mexico: a serological and parasitological study. Revista do Instituto de Medicina Tropical de Sao Paulo 1996; 38: 289292.
50. Hancke, D, Suárez, OV. Infection levels of the cestode Hymenolepis diminuta in rat populations from Buenos Aires, Argentina. Journal of Helminthology 2016; 90: 199205.
51. Mohd Zain, SN, Behnke, JM, Lewis, JW. Helminth communities from two urban rat populations in Kuala Lumpur, Malaysia. Parasites & Vectors 2012; 5: 47.
52. Milazzo, C, et al. Helminths and Ectoparasites of Rattus rattus and Mus musculus from Sicily, Italy. Comparative Parasitology 2003; 70: 199204.
53. Johnson, MAS, et al. Environmental exposure and leptospirosis, Peru. Emerging Infectious Diseases 2004; 10: 10161022.
54. Agudelo-Flórez, P, et al. Prevalence of Leptospira spp. in urban rodents from a groceries trade center of Medellín, Colombia. American Journal of Tropical Medicine and Hygiene 2009; 81: 906910.
55. Costa, F, et al. Patterns in Leptospira shedding in Norway rats (Rattus norvegicus) from Brazilian slum communities at high risk of disease transmission. PLoS Neglected Tropical Diseases 2015; 9: e0003819.
56. Foronda, P, et al. Pathogenic Leptospira spp. in wild rodents, Canary Islands, Spain. Emerging Infectious Diseases 2011; 17: 17811782.
57. Desvars, A, et al. Similarities in Leptospira serogroup and species distribution in animals and humans in the Indian Ocean island of Mayotte. American Journal of Tropical Medicine and Hygiene 2012; 87: 134140.
58. Bosseno, M-F, et al. Predominance of Trypanosoma cruzi Linage I in Mexico. J Clin Microbiol. 2002; 40: 627632.
59. Navone, GT, et al. Estudio comparativo de recuperación de formas parasitarias por tres diferentes métodos de enriquecimiento coproparasitológico. Parasitologia Latinoamericana 2005; 60: 178181.
60. Steinmann, P, et al. FLOTAC for the diagnosis of Hymenolepis spp. infection: proof-of-concept and comparing diagnostic accuracy with other methods. Parasitology Research 2012; 111: 749754.
61. Costa, F, 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 and Zoonotic Diseases 2014; 14: 3340.
62. Chagas-Junior, AD, et al. Detection and quantification of Leptospira interrogans in hamster and rat kidney samples: immunofluorescent imprints versus real-time PCR. PLoS ONE 2012; 7: 15.
63. Himsworth, CG, et al. An investigation of Bartonella spp., Rickettsia typhi, and Seoul Hantavirus in rats (Rattus spp.) from an inner-city neighborhood of Vancouver, Canada: is pathogen presence a reflection of global and local rat population structure? Vector Borne and Zoonotic Diseases 2015; 15: 2126.
64. Marangi, M, et al. Hymenolepis diminuta infection in a child living in the urban area of Rome, Italy. Journal of Clinical Microbiology 2003; 41: 39943995.

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed