Leprosy Associated with Atypical Cutaneous Leishmaniasis in Nicaragua and Honduras

Lucrecia Acosta Soto Sanatorio Fontilles, Alicante, Spain;
Universidad Miguel Hernández de Elche, Alicante, Spain;

Search for other papers by Lucrecia Acosta Soto in
Current site
Google Scholar
PubMed
Close
,
Nelson Caballero Asociación para el Desarrollo de los Pueblos (ADP), Nicaragua;

Search for other papers by Nelson Caballero in
Current site
Google Scholar
PubMed
Close
,
Lesny Ruth Fuentes Head of Leprosy Program, Choluteca, Honduras;

Search for other papers by Lesny Ruth Fuentes in
Current site
Google Scholar
PubMed
Close
,
Pedro Torres Muñoz Sanatorio Fontilles, Alicante, Spain;

Search for other papers by Pedro Torres Muñoz in
Current site
Google Scholar
PubMed
Close
,
Jose Ramón Gómez Echevarría Sanatorio Fontilles, Alicante, Spain;

Search for other papers by Jose Ramón Gómez Echevarría in
Current site
Google Scholar
PubMed
Close
,
Montserrat Pérez López Sanatorio Fontilles, Alicante, Spain;

Search for other papers by Montserrat Pérez López in
Current site
Google Scholar
PubMed
Close
,
Fernando Jorge Bornay Llinares Universidad Miguel Hernández de Elche, Alicante, Spain;

Search for other papers by Fernando Jorge Bornay Llinares in
Current site
Google Scholar
PubMed
Close
,
John L. Stanford University College London, London, United Kingdom;
Catriona Hargreaves Charitable Trust, Mill House, Claygate, Kent, United Kingdom

Search for other papers by John L. Stanford in
Current site
Google Scholar
PubMed
Close
,
Cynthia A. Stanford Catriona Hargreaves Charitable Trust, Mill House, Claygate, Kent, United Kingdom

Search for other papers by Cynthia A. Stanford in
Current site
Google Scholar
PubMed
Close
, and
Helen D. Donoghue University College London, London, United Kingdom;

Search for other papers by Helen D. Donoghue in
Current site
Google Scholar
PubMed
Close
Restricted access

In Central America, few cases of leprosy have been reported, but the disease may be unrecognized. Diagnosis is based on clinical criteria and histology. Preliminary field work in Nicaragua and Honduras found patients, including many children, with skin lesions clinically suggestive of atypical cutaneous leishmaniasis or indeterminate leprosy. Histology could not distinguish these diseases although acid-fast organisms were visible in a few biopsies. Lesions healed after standard antimicrobial therapy for leprosy. In the present study, patients, family members, and other community members were skin-tested and provided nasal swabs and blood samples. Biopsies were taken from a subgroup of patients with clinical signs of infection. Two laboratories analyzed samples, using local in-house techniques. Mycobacterium leprae, Leishmania spp. and Leishmania infantum were detected using polymerase chain reactions. Mycobacterium leprae DNA was detected in blood samples and nasal swabs, including some cases where leprosy was not clinically suspected. Leishmania spp. were also detected in blood and nasal swabs. Most biopsies contained Leishmania DNA and coinfection of Leishmania spp. with M. leprae occurred in 33% of cases. Mycobacterium leprae DNA was also detected and sequenced from Nicaraguan and Honduran environmental samples. In conclusion, leprosy and leishmaniasis are present in both regions, and leprosy appears to be widespread. The nature of any relationship between these two pathogens and the epidemiology of these infections need to be elucidated.

Author Notes

Address correspondence to Helen D. Donoghue, Centre for Clinical Microbiology, Division of Infection and Immunity, Royal Free Campus, University College London, London NW3 2PF, London, United Kingdom. E-mail: h.donoghue@ucl.ac.uk

Financial support: This work was mainly supported by the Directorate-General of cooperation for development and solidarity, the Regional Government of Valencia, Spain (Reference number: 3021/2007). The Sanatorio, Fontilles, Spain and the Catriona Hargreaves Charitable Trust, United Kingdom provided additional support. The funding bodies had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Authors’ addresses: Lucretia Acosto Soto, Carretera de Orba a Vall de Laguart, Fontilles, Alicante, Spain, and Universidad Miguel Hernández de Elche, Carretera de Valencia, San Juan, Alicante, Spain, E-mails: lacosta@fontilles.org or lacosta@umh.es. Nelson Caballero, Asociación para el Desarrollo de los Pueblos (ADP), Managua, Nicaragua, E-mail: nelcab64@hotmail.com. Lesney Ruth Fuentes, Head of Leprosy Program, Choluteca, Honduras, E-mail: lesnyr@yahoo.com. Pedro Torrez Muñoz, Jose Ramón Gómez-Echevarria, and Montserrat Pérez López, Fontilles Sanatorium, Carretera de Orba a Vall de Laguart, Fontilles, Alicante, Spain, E-mails: ptorres@fontilles.org, jrgomez@fontilles.org, and montse@perezlopez.com.es. Fernando Jorge Bornay-Llinares, Universidad Miguel Hernández de Elche, Carretera de Valencia, San Juan, Alicante, Spain, E-mail: f.bornay@umh.es. John L. Stanford and Cynthia A. Stanford, Catriona Hargreaves Charitable Trust, Mill House, Claygate, Kent, United Kingdom, E-mails: jandcstanford@btinternet.com and stanfordcynthia@gmail.com. Helen D. Donoghue, Centre for Clinical Microbiology, Division of Infection and Immunity, Royal Free Campus, University College London, London, United Kingdom, E-mail: h.donoghue@ucl.ac.uk.

  • 1.

    Britton WJ, Lockwood DN, 2004. Leprosy. Lancet 363: 12091219.

  • 2.

    Ridley DS, 1974. Histological classification and the immune spectrum of leprosy. Int J Lepr 34: 255273.

  • 3.

    Santos VS, de Mendonça Neto PT, Falcão Raposo OF, Fakhouri R, Reis FP, Feitosa VL, 2013. Evaluation of agreement between clinical and histopathological data for classifying leprosy. Int J Infect Dis 17: e189e192.

    • Search Google Scholar
    • Export Citation
  • 4.

    Talhari C, Talhari S, Penna GO, 2015. Clinical aspects of leprosy. Clin Dermatol 33: 2637.

  • 5.

    Bhatia AS, Katoch K, Narayanan RB, Ramu G, Mukherjee A, Lavania RK, 1993. Clinical and histopathological correlation in the classification of leprosy. Int J Lepr Other Mycobact Dis 61: 433438.

    • Search Google Scholar
    • Export Citation
  • 6.

    Lockwood DN, Sarno E, Smith WC, 2007. Classifying leprosy patients—searching for the perfect solution? Lepr Rev 78: 317320.

  • 7.

    Cortés SL, Rodríguez G, 2004. Leprosy in children: association between clinical and pathological aspects. J Trop Pediatr 50: 1215.

  • 8.

    World Health Organization, 2009. World Health Organization Factsheet. Available at: www.who.int./mediacentre/factsheets/fs375/en. Accessed August 5, 2017.

  • 9.

    World Health Organization, 2010. Control of the Leishmaniases. WHO Technical Report Series 949. Available at: http://whqlibdoc.who.int./trs/WHO_TRS_949_eng.pdf. Accessed August 5, 2017.

  • 10.

    Pan American Health Organization, 2017. Leishmaniases: Epidemiological Report of the Americas. Available at: http://iris.paho.org/xmlui/bitstream/handle/123456789/34112/leishmaniases_report_5_eng.pdf?sequence=5&isAllowed=y. Accessed August 5, 2017.

  • 11.

    Ponce C, Ponce E, Morrison A, Cruz A, Kreutzer R, McMahon-Pratt D, Neva F, 1991. Leishmania donovani chagasi: new clinical variant of cutaneous leishmaniasis in Honduras. Lancet 337: 6770.

    • Search Google Scholar
    • Export Citation
  • 12.

    Noyes H, Chance M, Ponce C, Ponce E, Maingon R, 1997. Leishmania chagasi: genotypically similar parasites from Honduras cause both visceral and cutaneous leishmaniasis in humans. Exp Parasitol 85: 264273.

    • Search Google Scholar
    • Export Citation
  • 13.

    Santos KE, Bermúdez J, López Lutz E, Alger J, Sierra M, Fajardo D, 2006. Clinical-epidemiologic study of atypical cutaneous leishmaniasis in Reitoca, an endemic zone in southern Honduras. Revista Médica de los Post Grados de Medicina UNAH 9: 4757.

    • Search Google Scholar
    • Export Citation
  • 14.

    Convit J, Ulrich M, Pérez M, Hung J, Castillo J, Rojas H, Viquez A, Ayaya LN, De Lima H, 2005. Atypical cutaneous leishmaniasis in central America: possible interaction between infectious and environmental elements. Trans R Soc Trop Med Hyg 99: 1317.

    • Search Google Scholar
    • Export Citation
  • 15.

    Belli A, García D, Palácios X, Rodriguez B, Valle S, Videa E, Tinoco E, Marin F, Harris E, 1999. Widespread atypical cutaneous leishmaniasis caused by Leishmania (L.) chagasi in Nicarágua. Am J Trop Med Hyg 61: 380385.

    • Search Google Scholar
    • Export Citation
  • 16.

    Zeledón R, Hidalgo H, Víquez A, Urbina A, 1989. Atypical cutaneous leishmaniasis in a semiarid region of north-west Costa Rica. Trans R Soc Trop Med Hyg 83: 786.

    • Search Google Scholar
    • Export Citation
  • 17.

    Agrela IF, Sánchez E, 2009. Prevalenia de la infección por Leishmania spp. en un area periurbana de Altagracia de Orituco, estado Guárico, Venezuela. Bol Malariol Salud Ambient 49: 111116.

    • Search Google Scholar
    • Export Citation
  • 18.

    Campos-Ponce M, Ponce C, Ponce E, Maingon RDC, 2005. Leishmania chagasi/infantum: further investigations on Leishmania tropisms in atypical cutaneous and visceral leishmaniasis foci in central America. Exp Parasitol 109: 209219.

    • Search Google Scholar
    • Export Citation
  • 19.

    Lizardo GA, Ponce C, Ponce E, Sierra M, 2008. Characterization of patients with atypical cutaneous leishmaniasis. Rev Med Hondur 76: 101107.

  • 20.

    World Health Organization, 2014. Global Leprosy Update, 2013; Reducing Disease Burden. Weekly Epidemiological Record. No. 36, Vol. 88, 389400. Available at: http://www.who.int/wer.

  • 21.

    Convit J, Ulrich M, Castillo J, De Lima H, Pérez P, 2006. Inorganic particles in the skin of inhabitants of volcanic areas of central America: their possible immunomodulatory influence in leishmaniasis and leprosy. Trans R Soc Trop Med Hyg 100: 734739.

    • Search Google Scholar
    • Export Citation
  • 22.

    Stanford JL, Stanford CA, Saidi KG, Dowlati Y, Weiss F, Farshchi Y, Madlener F, Rees RJW, 1989. Vaccination and skin test studies on the children of leprosy patients. Int J Lepr 57: 3844.

    • Search Google Scholar
    • Export Citation
  • 23.

    Plikaytis BB, Gelber RH, Shinnick TM, 1990. Rapid and sensitive detection of Mycobacterium leprae using a nested-primer gene amplification assay. J Clin Microbiol 28: 19131917.

    • Search Google Scholar
    • Export Citation
  • 24.

    Donoghue HD, Holton J, Spigelman M, 2001. PCR primers that can detect low levels of Mycobacterium leprae DNA. J Med Microbiol 50: 177182.

  • 25.

    Taylor GM, Donoghue HD, 2011. Multiple loci variable number tandem repeat (VNTR) analysis (MLVA) of Mycobacterium leprae isolates amplified from European archaeological human remains with lepromatous leprosy. Microbes Infect 13: 923929.

    • Search Google Scholar
    • Export Citation
  • 26.

    Schönian G, Nasereddin A, Dinse N, Schweynoch C, Schallig HDFH, Presber W, Jaffe CL, 2003. PCR diagnosis and characterization of Leishmania in local and imported clinical samples. Diagn Microbiol Infect Dis 47: 349358.

    • Search Google Scholar
    • Export Citation
  • 27.

    Cruz I et al.., 2013. An approach for interlaboratory comparison of conventional and real-time PCR assays for diagnosis of human leishmaniasis. Exp Parasitol 134: 281289.

    • Search Google Scholar
    • Export Citation
  • 28.

    Rodgers MR, Popper SJ, Wirth DF, 1990. Amplification of kinetoplast DNA as a tool in the detection and diagnosis of Leishmania. Exp Parasitol 71: 267275.

    • Search Google Scholar
    • Export Citation
  • 29.

    Belli A, Rodriguez B, Aviles H, Harris E, 1998. Simplified polymerase chain reaction detection of new world Leishmania in clinical specimens of cutaneous leishmaniasis. Am J Trop Med Hyg 58: 102109.

    • Search Google Scholar
    • Export Citation
  • 30.

    Fisa R, Riera C, Gállego M, Manubens J, Portús M, 2001. Nested PCR for diagnosis of canine leishmaniasis in peripheral blood, lymph node and bone marrow aspirates. Vet Parasitol 99: 105111.

    • Search Google Scholar
    • Export Citation
  • 31.

    Piarroux R, Azaiez R, Lossi AM, Reynier P, Muscatelli F, Gambarelli F, Fontes M, Dumon H, Quilici M, 1993. Isolation and characterization of a repetitive DNA sequence from Leishmania infantum: development of a visceral leishmaniasis polymerase chain reaction. Am J Trop Med Hyg 49: 364369.

    • Search Google Scholar
    • Export Citation
  • 32.

    Harris E, Kropp G, Belli A, Rodriguez B, Agabian N, 1998. Single-step multiplex PCR assay for characterization of new world Leishmania complexes. J Clin Microbiol 36: 19891995.

    • Search Google Scholar
    • Export Citation
  • 33.

    White C, Franco-Paredes C, 2015. Leprosy in the 21st century. Clin Microbiol Rev 28: 8094.

  • 34.

    Lima LN, Frota CC, Mota RM, Almeida RL, Pontes MA, Gonçalves H, Rodrigues LC, Kendall C, Kerr L, 2015. Widespread nasal carriage of Mycobacterium leprae among a healthy population in a hyperendemic region of northeastern Brazil. Mem Inst Oswaldo Cruz 110: 898905.

    • Search Google Scholar
    • Export Citation
  • 35.

    Pinho JD et al.., 2015. Presence of Mycobacterium leprae DNA and PGL-1 antigen in household contacts of leprosy patients from a hyperendemic area in Brazil. Genet Mol Res 14: 1447914487.

    • Search Google Scholar
    • Export Citation
  • 36.

    Araújo S, Lobato J, de Melo Reis É, Souza DOB, Gonçalves MA, Vieira Costa A, Goulart LR, Bernardes Goulart IM, 2012. Unveiling healthy carriers and subclinical infections among household contacts of leprosy patients who play potential roles in the disease chain of transmission. Mem Inst Oswaldo Cruz 107 (Suppl 1): 5559.

    • Search Google Scholar
    • Export Citation
  • 37.

    Romero-Montoya M, Beltran-Alzate JC, Cardona-Castro N, 2017. Evaluation and monitoring of Mycobacterium leprae transmission in household contacts of patients with Hansen’s disease in Colombia. PLoS Negl Trop Dis 11: e0005325.

    • Search Google Scholar
    • Export Citation
  • 38.

    Lavania M et al.., 2008. Detection of viable Mycobacterium leprae in soil samples: insights into possible sources of transmission of leprosy. Infect Genet Evol 8: 627631.

    • Search Google Scholar
    • Export Citation
  • 39.

    Turankar RP, Lavania M, Singh M, Sengupta U, Siva Sai KSR, Jadhav RS, 2016. Presence of viable Mycobacterium leprae in environmental specimens around houses of leprosy patients. Int J Med Microbiol 34: 315321.

    • Search Google Scholar
    • Export Citation
  • 40.

    Romero GA, de la Glória Orge Orge M, de Farias Guerra MV, Paes MG, de Oliveira Macêdo V, de Carvalho EM, 2005. Antibody response in patients with cutaneous leishmaniasis infected by Leishmania (Viannia) braziliensis or Leishmania (Viannia) guyanensis in Brazil. Acta Trop 93: 4956.

    • Search Google Scholar
    • Export Citation
  • 41.

    Azeredo-Coutinho RB, Matos DC, Nery JA, Valete-Rosalino CM, Mendonça SC, 2012. Interleukin-10-dependent down-regulation of interferon-gamma response to Leishmania by Mycobacterium leprae antigens during the clinical course of a coinfection. Braz J Med Biol Res 45: 632636.

    • Search Google Scholar
    • Export Citation
  • 42.

    Barnetson RS, Bryceson AD, 1978. Cutaneous leishmaniasis and leprosy. Trans R Soc Trop Med Hyg 72: 160163.

  • 43.

    Torealba J, Mendoza I, Ocanto T, Barroeta S, Mejia de Alejos MA, Bonfante-Garrido R, 1995. Concomitant cutaneous leishmaniasis and leprosy in Venezuela. Trans R Soc Trop Med Hyg 89: 69.

    • Search Google Scholar
    • Export Citation
  • 44.

    Raymond RW, McHugh CP, Kerr SF, 2010. Sand flies of Nicaragua: a checklist and reports of new collections. Mem Inst Oswaldo Cruz 105: 889894.

    • Search Google Scholar
    • Export Citation
  • 45.

    Lahiri R, Krahenbuhl J, 2008. The role of free-living pathogenic amoeba in the transmission of leprosy: a proof of principle. Lepr Rev 79: 401409.

    • Search Google Scholar
    • Export Citation
  • 46.

    Banerjee R, Banerjee B, Chaudhury S, Hati A, 1991. Transmission of viable Mycobacterium leprae by Aedes aegypti from lepromatous leprosy patients to the skin of mice through interrupted feeding. Lepr Rev 62: 21.

    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 66 66 25
Full Text Views 464 102 1
PDF Downloads 166 24 0
 
Membership Banner
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save