• 1.

    Ergen EN, King AH, Tuli M, 2015. Cutaneous leishmaniasis: an emerging infectious disease in travelers. Cutis 96: E22E26.

  • 2.

    No authors, 2008. Etymologia: leishmaniasis. Emerg Infect Dis 14: 666.

  • 3.

    Bañuls AL, Hide MPF, 2007. Leishmania and the leishmaniases: a parasite genetic update and advances in taxonomy, epidemiology and pathogenicity in humans. Adv Parasitol 64: 1109.

    • Search Google Scholar
    • Export Citation
  • 4.

    Mathers CD, Ezzati M, Lopez AD, 2007. Measuring the burden of neglected tropical diseases: the global burden of disease framework. PLoS Negl Trop Dis 1: e114.

    • Search Google Scholar
    • Export Citation
  • 5.

    World Health Organization, 2015. OMS | Leishmaniasis. WHO, Vol. 375. Available at: http://www.who.int/mediacentre/factsheets/fs375/es/. Accessed December 5, 2017.

  • 6.

    Alvar J, Vélez ID, Bern C, Herrero M, Desjeux P, Cano J, Jannin J, den Boer M; WHO Leishmaniasis Control Team, 2012. Leishmaniasis worldwide and global estimates of its incidence. PLoS One 7: e35671.

    • Search Google Scholar
    • Export Citation
  • 7.

    Schwarz NG, Loderstaedt U, Hahn A, Hinz R, Zautner AE, Eibach D, Fischer M, Hagen RM, Frickmann H, 2017. Microbiological laboratory diagnostics of neglected zoonotic diseases (NZDs). Acta Trop 165: 4065.

    • Search Google Scholar
    • Export Citation
  • 8.

    Kevric I, Cappel MA, Keeling JH, 2015. New world and old world Leishmania infections: a practical review. Dermatol Clin 33: 579593.

  • 9.

    Espir TT, Guerreiro TS, Naiff Mde F, Figueira Lde P, Soares FV, da Silva SS, Franco AM, 2016. Evaluation of different diagnostic methods of American cutaneous leishmaniasis in the Brazilian Amazon. Exp Parasitol 167: 16.

    • Search Google Scholar
    • Export Citation
  • 10.

    Ertabaklar H, Özlem Çalışkan S, Boduç EES, 2015. Comparison of direct microscopy, culture and polymerase chain reaction methods for the diagnosis of cutaneous leishmaniasis. Mikrobiyol Bul 49: 7784.

    • Search Google Scholar
    • Export Citation
  • 11.

    Gomes CM et al. 2015. Accuracy of mucocutaneous leishmaniasis diagnosis using polymerase chain reaction: systematic literature review and meta-analysis. Mem Inst Oswaldo Cruz 110: 157165.

    • Search Google Scholar
    • Export Citation
  • 12.

    Lemrani M, Hamdi S, Laamrani A, Hassar M, 2009. PCR detection of Leishmania in skin biopsies. J Infect Dev Ctries 3: 115122.

  • 13.

    Vega-Lopez F, 2003. Diagnosis of cutaneous leishmaniasis. Curr Opin Infect Dis 16: 97101.

  • 14.

    Shirian S, Oryan A, Hatam G-R, Panahi SDY, 2014. Comparison of conventional, molecular, and immunohistochemical methods in diagnosis of typical and atypical cutaneous leishmaniasis. Arch Pathol Lab Med 138: 235240.

    • Search Google Scholar
    • Export Citation
  • 15.

    Hasnain G, Bashar A, Nath P, Ghosh P, Hossain F, Hossain SMD, 2015. Polymerase chain reaction in the diagnosis of visceral leishmaniasis recurrence in the setting of negative splenic smears. Am J Trop Med Hyg 94: 99101.

    • Search Google Scholar
    • Export Citation
  • 16.

    Nath-Chowdhury M, Sangaralingam M, Bastien P, Ravel C, Pratlong F, Mendez J, Libman M, Ndao M, 2016. Real-time PCR using FRET technology for old world cutaneous leishmaniasis species differentiation. Parasit Vectors 9: 255.

    • Search Google Scholar
    • Export Citation
  • 17.

    Sakkas H, Gartzonika C, Levidiotou S, 2016. Laboratory diagnosis of human visceral leishmaniasis. J Vector Borne Dis 53: 816.

  • 18.

    Mashayekhi-Ghoyonlo V, Kiafar B, Rohani M, Esmaeili H, Erfanian-Taghvaee MR, 2015. Correlation between socioeconomic status and clinical course in patients with cutaneous leishmaniasis. J Cutan Med Surg 19: 4044.

    • Search Google Scholar
    • Export Citation
  • 19.

    Accorsi S, Barnabas GA, Farese P, Padovese V, Terranova M, Racalbuto V, Morrone A, 2009. Skin disorders and disease profile of poverty: analysis of medical records in Tigray, northern Ethiopia, 2005–2007. Trans R Soc Trop Med Hyg 103: 469475.

    • Search Google Scholar
    • Export Citation
  • 20.

    Abass E, Kang C, Martinkovic F, Semião-Santos SJ, Sundar S, Walden P, Piarroux R, El Harith A, Lohoff M, Steinhoff U, 2015. Heterogeneity of Leishmania donovani parasites complicates diagnosis of visceral leishmaniasis: comparison of different serological tests in three endemic regions. PLoS One 10: e0116408.

    • Search Google Scholar
    • Export Citation
  • 21.

    Lopez M, Inga R, Cangalaya M, Echevarria J, Llanos-Cuentas A, Orrego C, Arevalo J, 1993. Diagnosis of Leishmania using the polymerase chain reaction: a simplified procedure for field work. Am J Trop Med Hyg 49: 348356.

    • Search Google Scholar
    • Export Citation
  • 22.

    Davies CR, Reithinger R, Campbell-Lendrum D, Feliciangeli D, Borges R, Rodriguez N, 2000. The epidemiology and control of leishmaniasis in Andean countries. Cad Saude Publica 16: 925950.

    • Search Google Scholar
    • Export Citation
  • 23.

    David CV, Craft N, 2009. Cutaneous and mucocutaneous leishmaniasis. Dermatol Ther 22: 491502.

  • 24.

    Davies CR, Llanos-Cuentas EA, Sharp SJ, Canales J, Leon E, Alvarez E, Roncal NDC, 1997. Cutaneous leishmaniasis in the Peruvian Andes: factors associated with variability in clinical symptoms, response to treatment, and parasite isolation rate. Clin Infect Dis 25: 302310.

    • Search Google Scholar
    • Export Citation
  • 25.

    Rohoušová I, Volf P, 2006. Sand fly saliva: effects on host immune response and Leishmania transmission. Folia Parasitol (Praha) 53: 161171.

    • Search Google Scholar
    • Export Citation
  • 26.

    Weigle KSN, 1996. Natural history, clinical evolution, and the host-parasite interaction in new world cutaneous leishmaniasis. Clin Dermatol 14: 433450.

    • Search Google Scholar
    • Export Citation
  • 27.

    Weigle KA, Santrich C, Martinez F, Valderrama L, Saravia NG, 1993. Epidemiology of cutaneous leishmaniasis in Colombia: a longitudinal study of the natural history, prevalence, and incidence of infection and clinical manifestations. J Infect Dis 168: 699708.

    • Search Google Scholar
    • Export Citation
  • 28.

    Martins AL, Barreto JA, Lauris JR, Martins AC, 2014. American tegumentary leishmaniasis: correlations among immunological, histopathological and clinical parameters. An Bras Dermatol 89: 5258.

    • Search Google Scholar
    • Export Citation
  • 29.

    Bensoussan E, Nasereddin A, Jonas F, Schnur LF, Jaffe CL, 2006. Comparison of PCR assays for diagnosis of cutaneous leishmaniasis. J Clin Microbiol 44: 14351439.

    • Search Google Scholar
    • Export Citation
  • 30.

    World Health Organization, 1990. Control of the leishmaniasis. Report of a WHO expert committee. World Health Organ Tech Rep Ser 793: 1158.

    • Search Google Scholar
    • Export Citation
  • 31.

    Suárez M, Valencia BM, Jara M, Alba M, Boggild AK, Dujardin J-C, Llanos-Cuentas A, Arevalo J, Adaui V, 2015. Quantification of Leishmania (Viannia) kinetoplast DNA in ulcers of cutaneous leishmaniasis reveals inter-site and intersampling variability in parasite load. PLoS Negl Trop Dis 9: 114.

    • Search Google Scholar
    • Export Citation
  • 32.

    Ramírez JR, Agudelo S, Muskus C, Alzate JF, Berberich C, Barker DVI, 2000. Diagnosis of cutaneous leishmaniasis in Colombia: the sampling site within lesions influences the sensitivity of parasitological diagnosis. J Clin Microbiol 38: 37683773.

    • Search Google Scholar
    • Export Citation
  • 33.

    Mikita K, Maeda T, Yoshikawa S, Ono T, Miyahira Y, Kawana A, 2014. The Direct Boil-LAMP method: a simple and rapid diagnostic method for cutaneous leishmaniasis. Parasitol Int 63: 785789.

    • Search Google Scholar
    • Export Citation
  • 34.

    Boelaert M, El-Safi S, Hailu A, Mukhtar MRS, 2008. Diagnostic tests for kala-azar: a multi-centre study of the freeze-dried DAT, rK39 strip test and KAtex in east Africa and the Indian subcontinent. Trans R Soc Trop Med Hyg 102: 3240.

    • Search Google Scholar
    • Export Citation
  • 35.

    de Assis TS et al. 2011. Multi-centric prospective evaluation of rk39 rapid test and direct agglutination test for the diagnosis of visceral leishmaniasis in Brazil. Trans R Soc Trop Med Hyg 105: 8185.

    • Search Google Scholar
    • Export Citation
  • 36.

    Pattabhi S et al. 2010. Design, development and evaluation of rK28-based point-of-care tests for improving rapid diagnosis of visceral leishmaniasis. PLoS Negl Trop Dis 4: pii: e822.

    • Search Google Scholar
    • Export Citation
  • 37.

    Verma S, Avishek K, Sharma V, Negi NS, Ramesh VSP, 2013. Application of loop-mediated isothermal amplification assay for the sensitive and rapid diagnosis of visceral leishmaniasis and post-kala-azar dermal leishmaniasis. Diagn Microbiol Infect Dis 75: 390395.

    • Search Google Scholar
    • Export Citation
  • 38.

    Mitropoulos P, Konidas P, Durkin-Konidas M, 2010. New world cutaneous leishmaniasis: updated review of current and future diagnosis and treatment. J Am Acad Dermatol 63: 309322.

    • Search Google Scholar
    • Export Citation
  • 39.

    Pace D, 2014. Leishmaniasis. J Infect 69 (Suppl 1): S10S18.

  • 40.

    Abdeladhim M, Kamhawi S, Valenzuela JG, 2014. What’s behind a sand fly bite? The profound effect of sand fly saliva on host hemostasis, inflammation and immunity. Infect Genet Evol 28: 691703.

    • Search Google Scholar
    • Export Citation
  • 41.

    Oré M et al. 2015. Outbreak of cutaneous leishmaniasis in Peruvian military personnel undertaking training activities in the Amazon basin, 2010. Am J Trop Med Hyg 93: 340346.

    • Search Google Scholar
    • Export Citation
  • 42.

    Carvalho BM, Rangel EF, Ready PDVM, 2015. Ecological Niche modelling predicts southward expansion of Lutzomyia (Nyssomyia) flaviscutellata (Diptera: Psychodidae: Phlebotominae), vector of Leishmania (Leishmania) amazonensis in South America, under climate change. PLoS One 10: e0143282.

    • Search Google Scholar
    • Export Citation
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

 

 

 

Prevalence of and Factors Associated with Negative Microscopic Diagnosis of Cutaneous Leishmaniasis in Rural Peru

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  • 1 Stony Brook University School of Medicine, Stony Brook, New York;
  • | 2 Thomas Jefferson University Hospital, Philadelphia, Pennsylvania;
  • | 3 US Naval Medical Research Unit No. 6, Lima, Peru;
  • | 4 University of Arizona, Tucson, Arizona;
  • | 5 School of Medicine, Universidad Peruana de Ciencias Aplicadas (UPC), Lima, Peru;
  • | 6 Universidad Peruana Cayetano Heredia, Lima, Peru;
  • | 7 Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland
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Cutaneous leishmaniasis is endemic to South America where diagnosis is most commonly conducted via microscopy. Patients with suspected leishmaniasis were referred for enrollment by the Ministry of Health (MoH) in Lima, Iquitos, Puerto Maldonado, and several rural areas of Peru. A 43-question survey requesting age, gender, occupation, characterization of the lesion(s), history of leishmaniasis, and insect-deterrent behaviors was administered. Polymerase chain reaction (PCR) was conducted on lesion materials at the Naval Medical Research Unit No. 6 in Lima, and the results were compared with those obtained by the MoH using microscopy. Factors associated with negative microscopy and positive PCR results were identified using χ2 test, t-test, and multivariate logistic regression analyses. Negative microscopy with positive PCR occurred in 31% (123/403) of the 403 cases. After adjusting for confounders, binary multivariate logistic regression analyses revealed that negative microscopy with positive PCR was associated with patients who were male (adjusted odds ration [OR] = 1.93 [1.06–3.53], P = 0.032), had previous leishmaniasis (adjusted OR = 2.93 [1.65–5.22], P < 0.0001), had larger lesions (adjusted OR = 1.02 [1.003–1.03], P = 0.016), and/or had a longer duration between lesion appearance and PCR testing (adjusted OR = 1.12 [1.02–1.22], P = 0.017). Future research should focus on further exploration of these underlying variables, discovery of other factors that may be associated with negative microscopy diagnosis, and the development and implementation of improved testing in endemic regions.

Author Notes

Address correspondence to Ryan Lamm, Thomas Jefferson University Hospital, 111 S. 11th St., Philadelphia, PA 19107. E-mail: ryan.lamm@jefferson.edu

Financial support: This work was supported by the United States Department of Defense Global Emerging Infections Surveillance and Response System (GEIS) work number [847705 82000 25GB B0016]. The sponsor had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Medical students (Ryan Lamm, Grace Perotta, and Meagan Murphy) received funding from Stony Brook University’s Global Health Scholarship to pay for their airfare and stay in Puerto Maldonado during the sample collection phase.

Copyright statement: Several authors of this manuscript are employees of the U.S. Government. This work was prepared as part of their 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.

Authors’ addresses: Ryan Lamm, Thomas Jefferson University Hospital, Philadelphia, PA, E-mail: ryan.lamm@jefferson.edu. Clark Alves, University of Arizona College of Medicine, Tucson, AZ, E-mail: calves@email.arizona.edu. Grace Perrotta, Meagan Murphy, Catherine Messina, and Jack Fuhrer, Stony Brook University School of Medicine, Stony Brook, NY, E-mails: grace.perrotta@stonybrookmedicine.edu, meagan.murphy@stonybrookmedicine.edu, catherine.messina@stonybrookmedicine.edu, and jack.fuhrer@stonybrookmedicine.edu. Juan F. Sanchez, Erika Perez, Luis Angel Rosales, Andres G. Lescano, Edward Smith, Hugo Valdivia, and Sarah-Blythe Ballard, Naval Medical Research Unit 6 (NAMRU-6), Bellavista, Peru, and Peruvian Navy Hospital, Lima, Peru, E-mails; chiroque@gmail.com, erikasofiaperez@gmail.com, larhpe@hotmail.com, willy.lescano@med.navy.mil, edward.s.smith121.fn@mail.mil, hvalrod@hotmail.com, and sarah.b.ballard2.mil@mail.mil.

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