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Variability of Cutaneous Leishmaniasis Lesions Is Not Associated with Genetic Diversity of Leishmania tropica in Khyber Pakhtunkhwa Province of Pakistan
Nazma Habib Khan
Nazma Habib Khan
Department of Immunology & Infection, Faculty of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine, London, United Kingdom;
Department of Zoology, University of Peshawar, Peshawar, Khyber Pakhtunkhwa, Pakistan;
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Department of Zoology, University of Peshawar, Peshawar, Khyber Pakhtunkhwa, Pakistan;
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Martin S. Llewellyn
Martin S. Llewellyn
Department of Pathogen Molecular Biology, Faculty of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine, London, United Kingdom;
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Gabriele Schönian
Gabriele Schönian
Institute of Microbiology and Hygiene, Chariteì-University Medicine Berlin, Hindenburgdamm, Berlin, Germany
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Colin J. Sutherland
Colin J. Sutherland
Department of Immunology & Infection, Faculty of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine, London, United Kingdom;
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Leishmania tropica is the causative agent of cutaneous leishmaniasis in Pakistan. Here, intraspecific diversity of L. tropica from northern Pakistan was investigated using multilocus microsatellite typing. Fourteen polymorphic microsatellite markers were typed in 34 recently collected L. tropica isolates from Pakistan along with 158 archival strains of diverse Afro-Eurasian origins. Previously published profiles for 145 strains of L. tropica originating from different regions of Africa, Central Asia, Iran, and Middle East were included for comparison. Six consistently well-supported genetic groups were resolved: 1) Asia, 2) Morroco A, 3) Namibia and Kenya A, 4) Kenya B/Tunisia and Galilee, 5) Morocco B, and 6) Middle East. Strains from northern Pakistan were assigned to Asian cluster except for three that were placed in a geographically distant genetic group; Morocco A. Lesion variability among these Pakistani strains was not associated with specific L. tropica genetic profile. Pakistani strains showed little genetic differentiation from strains of Iraq, Afghanistan, and Syria (FST = 0.00–0.06); displayed evidence of modest genetic flow with India (FST = 0.14). Furthermore, genetic structuring within these isolates was not geographically defined. Pak–Afghan cluster was in significant linkage disequilibrium (IA = 1.43), had low genetic diversity, and displayed comparatively higher heterozygosity (FIS = −0.62). Patterns of genetic diversity observed suggest dominance of a minimally diverse clonal lineage within northern Pakistan. This is surprising as a wide clinical spectrum was observed in patients, suggesting the importance of host and other factors. Further genotyping studies of L. tropica isolates displaying different clinical phenotypes are required to validate this potentially important observation.
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Author Notes
Financial support: This work was supported by “Faculty Development Program (FDP)” scholarship awarded by Higher Education Commission, Pakistan to NK.
Authors’ addresses: Nazma Habib Khan, Department of Zoology, University of Peshawar, Peshawar, Khyber Pakhtunkhwa, Pakistan, E-mail: nazma@upesh.edu.pk. Martin S. Llewellyn, Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, United Kingdom, E-mail: martin.llewellyn@glasgow.ac.uk. Gabriele Schönian, Institute of Microbiology and Hygiene, Chariteì-University Medicine Berlin, Hindenburgdamm, Berlin, Germany, E-mail: gabriele.schoenian@t-online.de. Colin J. Sutherland, Department of Immunology and Infection, Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom, E-mail: colin.sutherland@lshtm.ac.uk.
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1.
Nagill R, Kaur S, 2011. Vaccine candidates for leishmaniasis: a review. Int Immunopharmacol 11: 1464–1488.
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2.
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3.
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4.
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7.
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8.
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-
9.
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11.
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12.
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13.
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14.
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-
15.
Rowland M, Munir A, Durrani N, Noyes H, Reyburn H, 1999. An outbreak of cutaneous leishmaniasis in an Afghan refugee settlement in north-west Pakistan. Trans R Soc Trop Med Hyg 93: 133–136.
-
16.
Noor SM, Hussain D, 2004. Cutaneous leishmaniasis in Sadda, Kurram agency, Pakistan. J Pak Assoc Dermatol 14: 114–117.
-
17.
Marco JD et al. 2006. Multilocus enzyme electrophoresis and cytochrome B gene sequencing-based identification of Leishmania isolates from different foci of cutaneous leishmaniasis in Pakistan. Am J Trop Med Hyg 75: 261–266.
-
18.
Khan NH, Bari AU, Hashim R, Khan I, Muneer A, Shah A, Wahid S, Yardley V, O’Neill B, Sutherland C, 2016. Cutaneous leishmaniasis in Khyber Pakhtunkhwa province of Pakistan: clinical diversity and species-level diagnosis. Am J Trop Med Hyg 95: 1106–1114.
-
19.
Bari AU, Rahman SB, 2008. Many faces of cutaneous leishmaniasis. Indian J Dermatol Venereol Leprol 74: 23–27.
-
20.
Bari AU, Raza N, 2010. Lupoid cutaneous leishmanisis: a report of of 16 cases. Indian J Dermatol Venereol 76: 85.
-
21.
Raja KM, Khan AA, Hameed A, Rahman SB, 1998. Unusual clinical variants of cutaneous leishmaniasis in Pakistan. Br J Dermatol 139: 111–113.
-
22.
Shamsuddin S, Mengal JA, Gazozai S, Mandokhail ZK, Kasi M, Muhammad N, 2006. Atypical presentation of cutaneous leishmaniasis in native population of Baluchistan. J Pak Assoc Dermatol 16: 196–200.
-
23.
Bari AU, 2006. Epidemiology of cutaneous leishmaniasis. J Pak Assoc Dermatol 16: 156–162.
-
24.
Rahman S, Abdullah FH, Khan JA, 2009. The frequency of old world cutaneous leishmaniasis in skin ulcers in Peshawar. J Ayub Med Coll Abbottabad 21: 72–75.
-
25.
Alam MZ, Kuhls K, Schweynoch C, Sundar S, Rijal S, Shamsuzzaman AK, Raju BV, Salotra P, Dujardin JC, Schonian G, 2009. Multilocus microsatellite typing (MLMT) reveals genetic homogeneity of Leishmania donovani strains in the Indian subcontinent. Infect Genet Evol 9: 24–31.
-
26.
Bulle B et al. 2002. Practical approach for typing strains of Leishmania infantum by microsatellite analysis. J Clin Microbiol 40: 3391–3397.
-
27.
Jamjoom MB, Ashford RW, Bates PA, Kemp SJ, Noyes HA, 2002. Towards a standard battery of microsatellite markers for the analysis of the Leishmania donovani complex. Ann Trop Med Parasitol 96: 265–270.
-
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Ochsenreither S, Kuhls K, Schaar M, Presber W, Schonian G, 2006. Multilocus microsatellite typing as a new tool for discrimination of Leishmania infantum MON-1 strains. J Clin Microbiol 44: 495–503.
-
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