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Epidemiology of Cutaneous Leishmaniasis Outbreak, Waziristan, Pakistan.

Cutaneous leishmaniasis (CL), the most widespread form of leishmaniasis, caused by Leishmania tropica and L. major (1,2), has emerged as an endemic disease in Khyber Pakhtunkhwa, Pakistan (2-5), owing to frequent movement of internally displaced persons (IDPs) from Waziristan in response to surgical strikes and military operations against terrorists by Pakistani armed forces. Keeping in view the impact of the frequent outbreaks of CL in settled areas, we studied the prevalence of CL in war-affected North and South Waziristan, with the help of health department and local government authorities.

We surveyed 7,548 persons from the different endemic areas and collected samples from ulcerating skin lesions from 538 suspected CL patients, 244 in North Waziristan and 294 in South Waziristan, during April 2013-January 2015. To sort out the reservoir, we captured 72 rodents from different locations in Waziristan, such as around houses, in cornfields, and in wild plantations surrounding the houses of CL patients, and analyzed liver and spleen samples by PCR. In addition, we collected sand flies from within 1.5 km of CL patients' houses for molecular analysis (6). We determined the prevalence rate of CL by a formula described previously (7) and performed statistical analyses using statistical software SAS Enterprise Guide (version 4.2; SAS Institute, Cary, NC, USA) by univariate analysis of variance with statistical significance at p<0.05.

Prevalence according to sex was consistent with previous findings, indicating that CL infections were more prone to develop in males (Table) because of more social activity and interaction with IDPs, whereas females always remain covered because of Islamic rules and thus are less prone to sand fly bites. Agewise, we observed a higher prevalence rate in children 0-15 years of age (1.61%) compared with other age groups. Sand flies and rodents were also collected from different endemic villages; none of the trapped rodent samples tested positive for leishmaniasis, but samples from sand flies from 2 endemic villages of North Waziristan (Razmak and Shewa) and 1 endemic village of South Waziristan (Sreykhoray) tested positive by kinetoplast DNA PCR. Samples collected from domestic animals (sheep, goat, cattle, donkey, dogs, mules) were negative for leishmaniasis.

For this report, we performed internal transcribed spacer 1 PCR followed by restriction fragment length polymorphism analysis for identification of different species of Leishmania. For North Waziristan, we observed 63.0% of L. tropica and 8% of L. major specific bands by this analysis. Similarly, restriction fragment length polymorphism analysis of South Waziristan showed 54% L. tropica and 4% L. major specific bands. No L. infantum-positive cases were found in any human or animal (dog) samples. Moreover, different species of Phlebotomus and Sergentomya sand fly genera were identified in both North and South Waziristan; P. sergenti was the most abundant species, followed by P. papatasi. We reported leishmaniasis infection in 6 female P. sergenti sand flies. P. papatasi is also susceptible to carry L. tropica and is widely distributed in different parts of Pakistan, including Khyber Pakhtunkhwa Province (8). A previous team had reported L. infantum in 2 army personnel deployed in Waziristan, (9) but the present detailed study ruled out its presence.

We conclude that CL is prevalent in Waziristan and new cases are increasing day by day. The present study also confirms that L. tropica is the causative agent of CL in Waziristan. This study also confirmed that anthroponotic CL caused by L. tropica is the main causative agent of CL in Waziristan. All the patients whose specimens tested positive for L. major had a history of traveling to zoonotic CL endemic areas of Mezar Sharif (Afghanistan) and Sindh and Balochistan (Pakistan) (10). Because of limited access in the study area for security reasons, sampling could not be performed in other endemic parts of Waziristan, so further molecular epidemiologic studies on animal reservoirs and sand flies should be conducted in wider areas of Waziristan, including neighboring tribal and settled areas, to map the complete distribution of the disease.

A leishmaniasis control committee should be established by health authorities in association with the Ministry of Health. It is strongly recommended that proper recordkeeping and documentation systems for leishmaniasis be initiated by health authorities at the local, provincial, and national levels and be well maintained to identify leishmaniasis outbreaks so that control measures can be started in time. Further, IDP camps must be monitored regularly to minimize the risk that nonendemic areas will be exposed to the disease by infected IDPs.


We thank Relief International, Pakistan, for providing funding for conducting this study on the prevalence of leishmaniasis in Waziristan, Pakistan.

This study was conducted in the following institutions: Vector Borne Diseases Management Center, Department of Microbiology, Kohat University of Science and Technology, Kohat, KP, Pakistan; ANSES-French Agency for Health and Safety, Animal Health Laboratory, Leishmaniasis and Sandflies Team, Maisons-Alfort, France; and US Naval Medical Research Unit (NAMRU3), Cairo, Egypt.

Dr. Hussain is an associate professor and is in charge of the vector-borne diseases laboratory in the Department of Microbiology, Kohat University of Science and Technology, Khyber Pakhtunkhwa, Pakistan. His research interests include molecular characterization of Leishmania species in endemic areas of Pakistan.


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(2.) Hussain M, Munir S, Jamal MA, Ayaz S, Akhoundi M, Mohamed K. Epidemic outbreak of anthroponotic cutaneous leishmaniasis in Kohat District, Khyber Pakhtunkhwa, Pakistan. Acta Trop. 2017;172:147-55. j.actatropica.2017.04.035

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(4.) Hussain M, Munir S, Ayaz S, Khattak BU, Khan TA, Muhammad N, et al. First report on molecular characterization of Leishmania species from cutaneous leishmaniasis patients in southern Khyber Pakhtunkhwa province of Pakistan. Asian Pac J Trop Med. 2017;10:718-21. j.apjtm.2017.07.015

(5.) Hayat M, Ahmad I, Afaq U, Munir S, Anees M, Hussain T, et al. Prevalence and molecular diagnosis of cutaneous leishmaniasis in local population of Dir District, Khyber Pakhtunkhwa, Pakistan. Int J Pharm Sci Rev Res. 2013;21:359-64.

(6.) Parvizi P, Mauricio I, Aransay AM, Miles MA, Ready PD. First detection of Leishmania major in peridomestic Phlebotomus papatasi from Isfahan province, Iran: comparison of nested PCR of nuclear ITS ribosomal DNA and semi-nested PCR of minicircle kinetoplast DNA. Acta Trop. 2005;93:75-83. 10.1016/j.actatropica.2004.09.007

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(10.) van Thiel P-P, Leenstra T, de Vries HJ, van der Sluis A, van Gool T, Krull AC, et al. Cutaneous leishmaniasis (Leishmania major infection) in Dutch troops deployed in northern Afghanistan: epidemiology, clinical aspects, and treatment. Am J Trop Med Hyg. 2010;83:1295-300.

Address for correspondence: Shahzad Munir, Yunnan Agricultural University, Kunming 650201, China; email:

Mubashir Hussain, Shahzad Munir, Taj Ali Khan, Abdullah Khan, Sultan Ayaz, Muhammad Ameen Jamal, Irfan Ahmed, Sohail Aziz, Noha Watany, Mohamed Kasbari

Author affiliations: Kohat University of Science and Technology, Kohat, Pakistan (M. Hussain, S. Munir, T.A. Khan, A. Khan); Abdul Wali Khan University, Mardan, Pakistan (S. Ayaz); Yunnan Agricultural University, Kunming, China (S. Munir, M.A. Jamal, I. Ahmed); Khyber Medical University, Peshawar, Pakistan (S. Aziz); US Naval Medical Research Unit 3, Cairo, Egypt (N. Watany); French Agency for Health and Safety, Maisons-Alfort, France (M. Kasbari)

Table. Areawise prevalence of CL in Waziristan, Pakistan,
by microscopy and PCR

                                               samples, no.*

Area                    No. tested          Microscopy       PCR

North Waziristan
  Shewa                    966                  29           35
  Spinwam                  530                  17           21
  Mirali                   320                   6            7
  Edaky                    463                   9           11
  Darpakheil               450                  11           14
  Hasankheil               373                   9           11
  Dosali                   512                  19           24
  Miranshah                455                  15           17
  Razmak                   367                  14           16
  Subtotal                4,436                 129          156
South Waziristan
  Wanna                    412                  14           28
  Shekai                   463                  12           18
  Jandola                  516                  10           10
  Sra Roha                 253                   8           11
  Makeen                   169                   4            9
  Janata                   448                   6           11
  Sreykhoray               195                   6           12
  Kotkai                   755                  12           18
  Subtotal                3,112                 72           117
Total                     7,548                 201          273

                               CL prevalence, %

Area                    Microscopy              PCR

North Waziristan
  Shewa                3 ([dagger])       3.62 ([dagger])
  Spinwam             3.2 ([dagger])      3.96 ([dagger])
  Mirali                   1.87                2.18
  Edaky                    1.94                2.37
  Darpakheil               2.44           3.11 ([dagger])
  Hasankheil               2.41                2.94
  Dosali             3.71 ([dagger])      4.68 ([dagger])
  Miranshah          3.29 ([dagger])      3.73 ([dagger])
  Razmak             3.81 ([dagger])      4.35 ([dagger])
  Subtotal                 2.91           3.51 ([dagger])
South Waziristan
  Wanna                    3.39           6.79 ([dagger])
  Shekai                   2.59           3.88 ([dagger])
  Jandola                  1.93                1.93
  Sra Roha           3.16 ([dagger])      4.34 ([dagger])
  Makeen                   2.36           5.32 ([dagger])
  Janata                   1.33                2.45
  Sreykhoray         3.07 ([dagger])      6.15 ([dagger])
  Kotkai                   1.58                2.38
  Subtotal                 2.3            3.75 ([dagger])
Total                      2.66                3.61

* CL, cutaneous leishmaniasis.

([dagger]) Denotes statistically significant difference (p<0.05)
analyzed by [chi square] test. In South Waziristan, the highest
prevalence rate (6.79% by PCR), was found in Wanna district;
in North Waziristan, Dosali had the highest prevalence (4.68%
by PCR). However, South Waziristan showed a higher prevalence
rate, 3.75% (117/3,112), than North Waziristan's 3.51%
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Article Details
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Author:Hussain, Mubashir; Munir, Shahzad; Khan, Taj Ali; Khan, Abdullah; Ayaz, Sultan; Jamal, Muhammad Amee
Publication:Emerging Infectious Diseases
Geographic Code:9PAKI
Date:Jan 1, 2018
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