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Imported Cutaneous Leishmaniasis Khan et al. Parasites Vectors (2019) 12:527 https://doi.org/10.1186/s13071-019-3771-6 Parasites & Vectors SHORT REPORT Open Access Imported cutaneous leishmaniasis: molecular investigation unveils Leishmania major in Bangladesh Md Anik Ashfaq Khan1, Rajashree Chowdhury1, Rupen Nath1, Sören Hansen2, Progga Nath3, Shomik Maruf1, Ahmed Abd El Wahed2* and Dinesh Mondal1* Abstract Background: The main clinical forms of leishmaniasis in Bangladesh are visceral leishmaniasis and post-kala-azar dermal leishmaniasis, which are caused by Leishmania donovani. Imported cutaneous leishmaniasis (CL) is emerging globally due mainly to increased human mobility. In recent years, several imported CL cases have also been reported in Bangladesh. Sporadic atypical cases of CL can be challenging for diagnosis and clinical management, while occur- rence of infection on a frequent basis can be alarming. We report of a case of a Bangladeshi temporary-migrant worker who, upon return, presented development of skin lesions that are characteristic of CL. Methods: A serum sample was collected and tested with an rK39 immunochromatographic test. Nucleic acid from skin biopsy derived culture sample was extracted and screened with a real-time PCR assay which targets the con- served REPL repeat region of L. donovani complex. The internal transcribed spacer 2 region of the ribosomal RNA gene cluster was amplifed and sequenced. Results: The suspect had a history of travel in both CL and VL endemic areas and had a positive rK39 test result. Based on clinical presentation, travel history and demonstration of the parasite in the skin biopsy, CL was diagnosed and the patient underwent a combination therapy with Miltefosine and liposomal amphotericin B. While typical endemic species were not detected, we identifed Leishmania major, a species that, to our knowledge, has never been reported in Bangladesh. Conclusions: Proper monitoring and reporting of imported cases should be given careful consideration for both clinical and epidemiological reasons. Molecular tests should be performed in diagnosis to avoid dilemma, and identif- cation of causative species should be prioritized. Keywords: Cutaneous leishmaniasis, Bangladesh, Leishmania major, Imported infection, Sequencing Background and visceral (VL) leishmaniasis. Te disease is endemic Leishmaniasis is a group of insidious infectious diseases in many parts of the world. Bangladesh belongs to the caused by species of the protozoan genus Leishmania endemic zones for VL as well as its skin complication transmitted through the bite of sand fies. It is classi- known as post-kala-azar dermal leishmaniasis (PKDL), fed into three clinical forms based upon the afected both of which are caused by Leishmania donovani. A tissue, namely cutaneous (CL), mucocutaneous (MCL) regional initiative for VL elimination, known as the regional kala-azar Elimination Programme (KAEP) have contributed to a remarkable decline in the incidence rate *Correspondence: [email protected]; [email protected] 1 Nutrition and Clinical Services Division, International Centre of VL cases over recent years in Bangladesh and other for Diarrhoeal Disease Research, Bangladesh, Dhaka, Bangladesh endemic regions of the Indian subcontinent; it is now 2 Division of Microbiology and Animal Hygiene, Georg-August-Universität approaching the maintenance phase of elimination [1]. Göttingen, Göttingen, Germany Full list of author information is available at the end of the article Patients afected by CL or MCL, on the other hand, are © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Khan et al. Parasites Vectors (2019) 12:527 Page 2 of 6 not usually found in Bangladesh, which might be due to he had been in to VL endemic areas of Bangladesh, and the absence of specifc transmitting vectors [2]. Te diag- was found positive by an rK39 rapid immunochromato- nostic and clinical practices are well-defned in the local graphic test (InBios International Inc., Seattle, Washing- health care centres for VL and PKDL, which is not the ton, USA). Te period since the lesion frst appeared was case for CL or MCL. Upon occurrence, the atypical dis- estimated to be three months, when he was working in ease forms may cause diagnostic and clinical dilemmas the Kingdom of Saudi Arabia (KSA), a country known to with respect to clinical presentation, cross-reaction in be endemic for CL. Physical examination revealed one serological tests, and treatment strategies [3, 4]. System- central depigmented ulcerated region surrounded by atic investigation of atypical cases and identifcation of several hyperkeratotic, plaque like, sharply demarcated, the causative Leishmania species are also important for painless papulonodular lesions (Fig. 1a) on his distal epidemiological reasons. Here, we report of a temporary- posteromedial aspect of the left forearm. Based on case migrant worker who was diagnosed with CL after his history and clinical examination, a provisional diagno- return to Bangladesh. We identifed L. major as the caus- sis of CL was made and lesional biopsy was obtained for ative agent. To our knowledge, this is the frst report of a parasitological confrmation. Maintaining aseptic con- L. major infected CL case in Bangladesh. ditions, a ~ 3.0 mm in diameter skin snip was collected with a scalpel from the nodular lesions followed by direct Methods microscopy of the Giemsa-stained thin biopsy smear, Case presentation which revealed large macrophages containing abundant A 40-year-old male was referred from the M.A.G Osmani intracellular and extracellular amastigotes (3+ para- Medical College Hospital, Sylhet to the Surya Kanta Kala- sitemia grade: 1–10 parasites/microscopic feld). One azar Research Center (SKKRC) hospital, Mymensingh in additional snip of a nodular lesion as well as pictures of October 2017 as a suspected case of CL, with multiple the lesions were collected following the patient’s consent. skin lesions on his left forearm. However, no other anom- Te patient received a combination therapy of liposo- aly such as fever, hepato-splenomegaly or mucosal lesion mal amphotericin B (AmBisome) at a dose of 20 mg/kg was observed. Te patient had no history of VL, although body-weight in four equally divided doses for four days. Fig. 1 Ulcerative lesion surrounded by nodules on the lower left arm of the patient, October 2017 to January 2018, SKKRC hospital, Mymensingh before treatment (a), fve days after treatment with 4 doses of AmBisome (b) and twelve weeks after treatment with Miltefosine (c) Khan et al. Parasites Vectors (2019) 12:527 Page 3 of 6 Tis was followed by an oral Miltefosine capsule for 12 sequences for Leishmania spp. with GENEIOUS v.9.1.6 weeks at a dose of 100 mg/day. Te combination therapy (Biomatters Ltd., Auckland, New Zealand) using the resulted in a remarkable improvement, demonstrated incorporated tree builder at default settings. by the dried up nodular crusts after fve days (Fig. 1b), and disappearance of nodules leaving atrophic scars Results with hypopigmented spots in the middle after 12 weeks Te RT-PCR assay did not result in a positive detection of (Fig. 1c). No major side-efect was reported during the L. donovani DNA in the culture sample. For identifcation follow-up visits and the patient did not return with any of Leishmania species, therefore, the PCR amplifed 400- relapse symptoms. bp segment of ITS2 spacer was sequenced. Te obtained sequence (Leish 17-832), which was assigned for species Parasite culture and DNA extraction identifcation using nucleotide BLAST search (NCBI), showed pairwise similarity of 99% to L. major reference Te additional skin snip (~ 3.0 mm in diameter) col- genome (GenBank: NC_007268) with a query cover of lected from a nodular lesion was inoculated into RPMI- 100%. In contrast, for the closest reference genome strain 1640 culture medium with 10% FBS supplemented with of L. infantum (GenBank: NW_004057905.1), the pair- penicillin-streptomycin. Two volumes each of stationary wise identity and query cover was 88% and 90%, respec- phase culture promastigotes were inactivated, stored in tively (Table 1). Te phylogenetic tree constructed for the bufer AL (Qiagen) at a 1:1 ratio and sent to the Emerging obtained ITS2 sequence showed that L. major, originat- Infections and Parasitology laboratory of International ing possibly from Iran, shares a common ancestral node Center for Diarrheal Disease Research (Dhaka, Bangla- with the test sequence in a single branch (Fig. 2). Te desh). DNA was extracted by using a QIAmp Blood DNA obtained nucleotide sequence was submitted to the Gen- Mini Kit (Qiagen). Bank database under the accession no. MK034756. Real‑time PCR and sequencing Discussion A TaqMan probe based real-time (RT)-PCR assay, In Bangladesh, VL and PKDL are prevalent in endemic which targets the conserved region of Leishmania REPL areas, whereas CL, a localized manifestation of nodu- repeats (L42486.1) of L. donovani complex, was carried lar or popular lesion with ulceration, is not regarded
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