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1.
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Raoult D, Birtles RJ, Montoya M, Perez E, Tissot-Dupont H, Roux V, Guerra H, 1999. Survey of three bacterial louse-associated diseases among rural Andean communities in Peru: prevalence of epidemic typhus, trench fever, and relapsing fever. Clin Infect Dis 29: 434–436.
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Travassos J, Rodrigues PM, Carrijo L, 1949. Tifo Murino em São Paulo: Identificação da Rickettsia mooseri Isolada de um Caso Humano. Available at: https://www.scienceopen.com/document?vid=03867a14-fb15-4153-809e-287f5ef40ce9. Accessed October 16, 2018.
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Hadad E, Pirogovsky A, Bartal C, Gilad J, Barnea A, Yitzhaki S, Grotto I, Balicer RD, Schwartz E, 2006. An outbreak of leptospirosis among Israeli troops near the Jordan River. Am J Trop Med Hyg 74: 127–131.
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Seroprevalence and Risk Factors for Rickettsia and Leptospira Infection in Four Ecologically Distinct Regions of Peru
Gabriela Salmon-Mulanovich
Gabriela Salmon-Mulanovich
U.S. Naval Medical Research Unit No. 6, Callao, Peru;
Universidad Peruana Cayetano Heredia, Lima, Peru;
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Universidad Peruana Cayetano Heredia, Lima, Peru;
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Mark P. Simons
Mark P. Simons
U.S. Naval Medical Research Unit No. 6, Callao, Peru;
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Carmen Flores-Mendoza
Carmen Flores-Mendoza
U.S. Naval Medical Research Unit No. 6, Callao, Peru;
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Steev Loyola
Steev Loyola
U.S. Naval Medical Research Unit No. 6, Callao, Peru;
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María Silva
María Silva
U.S. Naval Medical Research Unit No. 6, Callao, Peru;
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Matthew Kasper
Matthew Kasper
Armed Forces Health Surveillance Center, Silver Spring, Maryland;
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Hugo R. Rázuri
Hugo R. Rázuri
U.S. Naval Medical Research Unit No. 6, Callao, Peru;
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Luis Enrique Canal
Luis Enrique Canal
U.S. Naval Medical Research Unit No. 6, Callao, Peru;
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Mariana Leguia
Mariana Leguia
U.S. Naval Medical Research Unit No. 6, Callao, Peru;
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Daniel G. Bausch
Daniel G. Bausch
U.S. Naval Medical Research Unit No. 6, Callao, Peru;
Tulane School of Public Health and Tropical Medicine, New Orleans, Louisiana;
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Tulane School of Public Health and Tropical Medicine, New Orleans, Louisiana;
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Allen L. Richards
Allen L. Richards
Viral and Rickettsial Diseases Department, Naval Medical Research Center, Silver Spring, Maryland
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Rickettsia and Leptospira spp. are under-recognized causes of acute febrile disease worldwide. Rickettsia species are often placed into the spotted fever group rickettsiae (SFGR) and typhus group rickettsiae (TGR). We explored the antibody prevalence among humans for these two groups of rickettsiae in four regions of Peru (Lima, Cusco, Puerto Maldonado, and Tumbes) and for Leptospira spp. in Puerto Maldonado and Tumbes. We also assessed risk factors for seropositivity and collected serum samples and ectoparasites from peri-domestic animals from households in sites with high human seroprevalence. In total, we tested 2,165 human sera for antibodies (IgG) against SFGR and TGR by ELISA and for antibodies against Leptospira by a microscopic agglutination test. Overall, human antibody prevalence across the four sites was 10.6% for SFGR (ranging from 6.2% to 14.0%, highest in Tumbes) and 3.3% for TGR (ranging from 2.6% to 6.4%, highest in Puerto Maldonado). Factors associated with seroreactivity against SFGR were male gender, older age, contact with backyard birds, and working in agriculture or with livestock. However, exposure to any kind of animal within the household decreased the odds ratio by half. Age was the only variable associated with higher TGR seroprevalence. The prevalence of Leptospira was 11.3% in Puerto Maldonado and 5.8% in Tumbes, with a borderline association with keeping animals in the household. We tested animal sera for Leptospira and conducted polymerase chain reaction (PCR) to detect Rickettsia species among ectoparasites collected from domestic animals in 63 households of seropositive participants and controls. We did not find any association between animal infection and human serostatus.
Author Notes
Financial support: The study was funded by U.S. DoD Global Emerging Infections Surveillance and Response System, work unit 847705 82000 25GB B0016.
Disclosure: The views expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Department of the Navy, Department of Defense, or the U.S. government. Some authors are or were military service members and employees of the U.S. government. This work was prepared as part of their official duties. Title 17 U.S.C. §105 provides that “Copyright protection under this title is not available for any work of the United States Government.” Title 17 U.S.C. §101 defines a U.S. government work as a work prepared by a military service member or employee of the U.S. government as part of that person’s official duties. The study protocol was approved by the Naval Medical Research Unit-6 Institutional Review Board (Protocol No. NAMRU6.2013.0002) in compliance with all applicable Federal regulations governing the protection of human subjects. The experiments reported herein were conducted in compliance with the Animal Welfare Act and in accordance with principles set forth in the “Guide for the Care and Use of Laboratory Animals,” Institute of Laboratory Animals Resources, National Research Council, National Academy Press, 2011. This study was approved via Resolucion Directoral No. 297-2015-SERFOR/DGGSPFFS by the Forestry and Wild Fauna Service, Peruvian Ministry of Agriculture.
Authors’ addresses: Gabriela Salmon-Mulanovich, Department of Virology and Emerging Infections, Naval Medical Research Unit No. 6, Callao, Peru, Facultad de Salud Pública y Administración, Universidad Peruana Cayetano Heredia, Lima, Peru, and Ingeniería Biomédica, Pontificia Universidad Católica del Perú, Lima, Peru, E-mail: gsalmonm.veid@gmail.com. Mark P. Simons, Wound Infections, Naval Medical Research Unit No. 6, Silver Spring, MD, E-mail: mark.p.simons.mil@mail.mil. Carmen Flores-Mendoza, Department of Entomology, Naval Medical Research Unit No. 6, Callao, Peru, E-mail: carmen.flores.fn@mail.mil. Steev Loyola and María Silva, Department of Virology and Emerging Infections, Naval Medical Research Unit No. 6, Callao, Peru, E-mails: steev.loyola@gmail.com and maritasilva71@gmail.com. Matthew Kasper, Department of Bacteriology, U.S. Naval Medical Research Unit No. 6, Lima, Peru, E-mail: matthew.r.kasper2.mil@mail.mil. Hugo R. Rázuri, Division of Clinical Epidemiology, Research Institute of the McGill University Health Centre, Montreal, Canada, and Department of Virology and Emerging Infections, Naval Medical Research Unit No. 6, Callao, Peru, E-mail: hugorazuri@gmail.com. Luis Enrique Canal, Department of Bacteriology, Naval Medical Research Unit No. 6, Callao, Peru, E-mail: enrique.a.canal.fn@mail.mil. Mariana Leguia, Department of Virology and Emerging Infections, Naval Medical Research Unit No. 6, Callao, Peru, and Vicerrectorado de Investigación, Pontificia Universidad Catolica del Peru, Lima, Peru, E-mail: mariana.leguia@gmail.com. Daniel G. Bausch, Department of Virology and Emerging Infections, Naval Medical Research Unit No. 6, Callao, Peru, School of Public Health and Tropical Medicine, Tulane University School of Public Health and Tropical Medicine, New Orleans, LA, Public Health England London Region, UK Public Health Rapid Support Team, London, United Kingdom, and London School of Hygiene and Tropical Medicine, UK Public Health Rapid Support Team, London, United Kingdom, E-mail: daniel.bausch@phe.gov.uk. Allen L. Richards, Department of Viral and Rickettsial Diseases, Naval Medical Research Center, Silver Spring, MD, E-mail: allen.l.richards.civ@mail.mil.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Nicholson WL, Paddock CD, 2016. Rickettsial (spotted & typhus fevers) & related infections (Anaplasmosis & Ehrlichiosis). 2016 Yellow Book. Travelers’ Health. New York, NY: CDC. Available at: https://wwwnc.cdc.gov/travel/page/2018-yellow-book-about. Accessed April 20, 2017.
-
2.
Parola P, Paddock CD, Raoult D, 2005. Tick-borne rickettsioses around the world: emerging diseases challenging old concepts. Clin Microbiol Rev 18: 719–756.
-
3.
Labruna MB et al. 2011. Rickettsioses in Latin America, Caribbean, Spain and Portugal. Rev MVZ Córdoba 16: 2435–2457.
-
4.
Labruna MB, 2009. Ecology of Rickettsia in South America. Ann N Y Acad Sci 1166: 156–166.
-
5.
Labruna MB, Whitworth T, Bouyer DH, McBride J, Camargo LMA, Camargo EP, Popov V, Walker DH, 2004. Rickettsia bellii and Rickettsia amblyommii in Amblyomma ticks from the state of Rondônia, western Amazon, Brazil. J Med Entomol 41: 1073–1081.
-
6.
Blair PJ et al. 2004. Characterization of spotted fever group rickettsiae in flea and tick specimens from northern Peru. J Clin Microbiol 42: 4961–4967.
-
7.
Jiang J, Blair PJ, Felices V, Moron C, Cespedes M, Anaya E, Schoeler GB, Sumner JW, Olson JG, Richards AL, 2005. Phylogenetic analysis of a novel molecular isolate of spotted fever group rickettsiae from northern Peru: Candidatus Rickettsia andeanae. Ann N Y Acad Sci 1063: 337–342.
-
8.
Raoult D, Birtles RJ, Montoya M, Perez E, Tissot-Dupont H, Roux V, Guerra H, 1999. Survey of three bacterial louse-associated diseases among rural Andean communities in Peru: prevalence of epidemic typhus, trench fever, and relapsing fever. Clin Infect Dis 29: 434–436.
-
9.
Blair PJ et al. 2004. Evidence of rickettsial and Leptospira infections in Andean northern Peru. Am J Trop Med Hyg 70: 357–363.
-
10.
Ramal AC, Díaz DE, López TJ, 2007. Rickettsiosis, enfermedad emergente en Loreto. Evidencia sexológica de 20 casos. Rev Peru Med Exp Salud Publica 24: 99–100.
-
11.
Travassos J, Rodrigues PM, Carrijo L, 1949. Tifo Murino em São Paulo: Identificação da Rickettsia mooseri Isolada de um Caso Humano. Available at: https://www.scienceopen.com/document?vid=03867a14-fb15-4153-809e-287f5ef40ce9. Accessed October 16, 2018.
-
12.
Hidalgo M et al. 2013. Flea-borne rickettsioses in the north of Caldas province, Colombia. Vector Borne Zoonotic Dis 13: 289–294.
-
13.
Sihuincha MM, Anaya FE, Carranza VV, Durand VS, 2006. Evidencia serológica de la presencia de rickettsias del grupo de la fiebre manchada en la Amazonía del Perú. Rev Peru Med Exp Salud Publica 23: 284–287.
-
14.
Forshey BM et al. 2010. Epidemiology of spotted fever group and typhus group rickettsial infection in the Amazon basin of Peru. Am J Trop Med Hyg 82: 683–690.
-
15.
Ramadass P, Jarvis BDW, Corner RJ, Penny D, Marshall RB, 1992. Genetic characterization of pathogenic Leptospira species by DNA hybridization. Int J Syst Bacteriol 42: 215–219.
-
16.
Yasuda PH, Steigerwalt AG, Sulzer KR, Kaufmann AF, Rogers F, Brenner DJ, 1987. Deoxyribonucleic acid relatedness between serogroups and serovars in the family Leptospiraceae with proposals for seven new Leptospira species. Int J Syst Bacteriol 37: 407–415.
-
17.
Kocher C et al. 2016. Rickettsial disease in the Peruvian Amazon basin. PLoS Negl Trop Dis 10: e0004843.
-
18.
Perez J, Brescia F, Becam J, Mauron C, Goarant C, 2011. Rodent abundance dynamics and leptospirosis carriage in an area of hyper-endemicity in New Caledonia. PLoS Negl Trop Dis 5: e1361.
-
19.
Bharti AR et al. 2003 Leptospirosis: a zoonotic disease of global importance. Lancet Infect Dis 3: 757–771.
-
20.
Johnson MA et al. 2004. Environmental exposure and leptospirosis, Peru. Emerg Infect Dis 10: 1016–1022.
-
21.
Hadad E, Pirogovsky A, Bartal C, Gilad J, Barnea A, Yitzhaki S, Grotto I, Balicer RD, Schwartz E, 2006. An outbreak of leptospirosis among Israeli troops near the Jordan River. Am J Trop Med Hyg 74: 127–131.
-
22.
World Health Organization, 2003. Human Leptospirosis: Guidance for Diagnosis, Surveillance and Control. Available at: http://www.who.int/iris/handle/10665/42667. Accessed April 20, 2017.
-
23.
Barcellos C, Sabroza PC, 2000. Socio-environmental determinants of the leptospirosis outbreak of 1996 in western Rio de Janeiro: a geographical approach. Int J Environ Health Res 10: 301–313.
-
24.
Barcellos C, Sabroza PC, 2001. The place behind the case: leptospirosis risks and associated environmental conditions in a flood-related outbreak in Rio de Janeiro. Cad Saúde Pública 17: S59–S67.
-
25.
Sejvar J et al. 2003. Leptospirosis in “eco-challenge” athletes, Malaysian Borneo, 2000. Emerg Infect Dis 9: 702–707.
-
26.
Lau CL, Smythe LD, Craig SB, Weinstein P, 2010. Climate change, flooding, urbanisation and leptospirosis: fuelling the fire? Trans R Soc Trop Med Hyg 104: 631–638.
-
27.
Céspedes ZM, Balda JL, González QD, Tapia LR, 2006. Situación de la leptospirosis en el Perú 1994–2004. Rev Peru Med Exp Salud Publica 23: 56–66.
-
28.
Céspedes ZM, Ormaeche MM, Condori P, Balda JL, Glenny AM, 2003. Prevalencia de leptospirosis y factores de riesgo en personas con antecedentes de fiebre en la Provincia de Manu, Madre de Dios, Perú. Rev Peru Med Exp Salud Publica 20: 80–185.
-
29.
Céspedes ZM et al. 2004. Leptospirosis: una enfermedad zoonótica hiperendémica en la provincia de Coronel Portillo. Ucayali, Perú. Rev Peru Med Exp Salud Publica 21: 62–70.
-
30.
Forshey BM et al. for the NMRCD Febrile Surveillance Working Group, 2010. Arboviral etiologies of acute febrile illnesses in western South America, 2000–2007. PLoS Negl Trop Dis 4: e787.
-
31.
Binder WD, Mermel LA, 1998. Leptospirosis in an urban setting: case report and review of an emerging infectious disease. J Emerg Med 16: 851–856.
-
32.
Alarcón-Villaverde JO, Romani-Romani F, Tejada RA, Wong-Chero P, Céspedes-Zambrano M, 2014. Leptospirosis seroprevalence and associated features in rice farmers of tropical region of Peru. Rev Peru Med Exp Salud Pública 31: 195–203.
-
33.
Leal-Pinedo JM, Linares-Palomino R, 2005. The dry forests of the Biosphere Reserve of Northwestern (Peru): tree diversity and conservation status [in Spanish]. Caldasia 27: 195–211.
-
34.
Tinoco YO et al. 2017. Burden of influenza in 4 ecologically distinct regions of Peru: household active surveillance of a community cohort, 2009–2015. Clin Infect Dis 65: 1532–1541.
-
35.
Linares HD, Quispe JSG, 2018. Diversidad, dominancia y distribución arbórea en Madre de Dios, Perú. Rev For Perú 33: 4–23.
-
36.
Razuri H et al. 2012. Population-based active surveillance cohort studies for influenza: lessons from Peru. Bull World Health Organ 90: 318–320.
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37.
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