Indian Journal of Pathology and Microbiology
Home About us Instructions Submission Subscribe Advertise Contact e-Alerts Ahead Of Print Login 
Users Online: 819
Print this page  Email this page Bookmark this page Small font sizeDefault font sizeIncrease font size

  Table of Contents    
Year : 2013  |  Volume : 56  |  Issue : 3  |  Page : 211-215
Clinical and histopathological characteristics of cutaneous Leishmaniasis in Sanliurfa City of Turkey including Syrian refugees

1 Department of Pathology, Medicine Faculty, Harran Universty, Sanliurfa, Turkey
2 Department of Dermatology, Medicine Faculty, Harran Universty, Sanliurfa, Turkey
3 Department of Pathology, Balikligol State Hospital, Sanliurfa, Turkey

Click here for correspondence address and email

Date of Web Publication24-Oct-2013


Background: The aim of our study was to investigate the clinical and histopathological characteristics of cutaneous leishmaniasis (CL) in the city of Sanliurfa in Turkey, where Syrian refugees also reside. Materials and Methods: At the Harran University Hospital outpatient clinics between 2012 and 2013, 54 CL cases, including 24 Syrian patients, underwent punch biopsy of the skin and/or a touch imprint. Patients in whom leishmania parasites were detected were included in the study. The clinical and histopathological data of the patients were obtained by a review of the patients' medical records. All the slides of each patient were re-evaluated histopathologically. Results: Fifty-four cases (mean age; 17 ± 12 years), consisting of 32 males (59.3%) and 22 females (40.7%), were examined. The most common site of involvement was the face (63%). The most common presentation was noduloulcerative lesions (57.4%). Histopathologically, the majority of the cases exhibited hyperkeratosis, follicular plugging of the epidermis, chronic inflammatory infiltration, leishmania amastigotes and non-caseating granulomatous inflammation in the dermis. Conclusion: CL presents with a wide spectrum of expression, both clinically and histologically, and may mimic other inflammatory and neoplastic diseases. The diagnosis of CL relies on the identification of leishmania amastigotes in either a direct smear of the lesion or in a tissue section.

Keywords: Cutaneous leishmaniasis, skin biopsy, Syrian refugees, touch imprint

How to cite this article:
Koçarslan S, Turan E, Ekinci T, Yesilova Y, Apari R. Clinical and histopathological characteristics of cutaneous Leishmaniasis in Sanliurfa City of Turkey including Syrian refugees . Indian J Pathol Microbiol 2013;56:211-5

How to cite this URL:
Koçarslan S, Turan E, Ekinci T, Yesilova Y, Apari R. Clinical and histopathological characteristics of cutaneous Leishmaniasis in Sanliurfa City of Turkey including Syrian refugees . Indian J Pathol Microbiol [serial online] 2013 [cited 2022 Dec 5];56:211-5. Available from:

   Introduction Top

Leishmaniasis is a vector-borne parasitic disease. It is caused by obligate intracellular protozoa of the Leishmania genus and transmitted to humans by the bite of female phlebotomine sand flies. [1] Depending on parasite- and host-related factors, the disease manifests as visceral, cutaneous or mucocutaneous forms. [2] Cutaneous leishmaniasis (CL), which is the most common form of leishmaniasis, is a notifiable disease in Turkey. The Health Ministry of the Turkish Republic has reported that the majority of CL cases (98%) have occurred in the cities of Sanliurfa, Osmaniye, Adana, Hatay, Mersin and Kahramanmaras, where CL disease is endemic. Sanliurfa Province in southeastern Anatolia, Turkey, is highly endemic for CL. [3],[4] Because of the civil war in Syria, Syrian refugees have migrated to Sanliurfa. Since then, the number of CL cases has dramatically increased. Following an elevation in the number of skin biopsies of Syrian patients diagnosed with CL at the Harran University Hospital Pathology department in Sanliurfa, we decided to evaluate the clinical spectrum and the histopathological characteristics of CL cases (54 patients, including 24 Syrian patients).

   Materials and Methods Top

In this retrospective study, 54 cases with leishmania amastigotes detected in a skin biopsy and/or a touch imprint were investigated. All the cases were diagnosed at the Department of Dermatology and Pathology in Harran University, Sanliurfa. The clinical histories of the patients were obtained by a review of the patients' medical records and an interview with the patients' dermatologist. The pathology reports, paraffin blocks and slides of 36 patients who had a skin biopsy were retrieved from the files and the archive of the pathology department. All the slides of each patient were re-evaluated histopathologically. In all cases, paraffin-embedded tissue sections 5-μm-thick were cut and stained with hematoxylin-eosin and Giemsa. Touch imprint preparations were stained with Giemsa in 32 cases. Statistical data were analyzed using the Statistical Package for Social Sciences (SPSS Inc., Chicago, IL, USA; version 11.5) software. The study was approved by the institutional ethics review board of XXX.

   Results Top

The clinical and histopathological data of 54 patients (32 male and 22 female), with an age range of 1-51 years and a mean (±standard deviation) age of 17 ± 12 years, were evaluated. Most of the patients were aged 0-20 years (66.7%) and few were >50 years (1.9%). A total of 70.4% of the cases were asymptomatic. The lesions were mostly painless, except when there was secondary bacterial infection. The most common symptom was itching. Pain was observed rarely. The lesions were most frequently located on the exposed parts of the body. The face was the most common site of involvement (34 patients, 63%), followed by the upper and lower extremities (14 patients, 25.9%) and multiple locations (31%). In six cases (11.1%), the lesions were present on parts of the body covered by clothing, such as the back, the abdomen and the gluteal region. Twenty-three patients (42.5%) had two or more lesions. The number of lesions ranged from one to five (mean: 1.63). The most common manifestation was noduloulcerative lesions [Figure 1] in 31 cases (57.4%), followed by papulonodular lesions [Figure 2] in 18 (33.3%) cases, vegetative lesions in two (3.7) cases, verrucous lesions in two (3.7%) cases and plaques [Figure 3] in one (1.9%) case. The duration of the lesions ranged from 1 month to 16 months, and the mean duration was 6.5 months. The size of the lesions ranged from 0.5 cm to 10 cm. The noduloulcerative cutaneous lesions were characteristically painless, with an exudative base and a raised margin, and they were frequently covered by a crust. In one patient, a malignant tumor was suspected because of atypical clinical findings, but cytology helped to diagnose leishmaniasis. All the cases were treated with intralesional and/or systemic antimonials. Clinical observations are ongoing in some of the patients. The histopathological examination of the lesions in 24 patients revealed leishmaniasis, and the results were suggestive of leishmaniasis in another patient. The histopathological studies showed epidermal and dermal changes in the 36 cases who had a biopsy. In the majority of the cases, the epidermis showed marked hyperkeratosis and follicular plugging. An ulcer was present in six cases, epidermal atrophy in 13 cases, liquefaction degeneration of the basal cell layer in seven cases, pseudoepitheliomatous hyperplasia in seven cases, intraepidermal parasites in one case and a crust in seven cases. The epidermal findings are shown in [Table 1]. In all cases, the dermis showed mononuclear dermal infiltration consisting of lymphocytes, histiocytes, plasma cells and, occasionally, eosinophil leukocytes. In 26 cases, granulomatous inflammation was seen [Figure 4], and six of these contained non-caseating necrosis. In eight cases with granulomatous inflammation, Langhans-type multinuclear giant cells were observed. No free zone between the epidermis and the dermal infiltration was present. The dermal findings are summarized in [Table 2]. The histopathological examination of the skin biopsies revealed leishmania amastigotes [Figure 5] in 24 patients who were given a diagnosis of CL. In 12 cases who received a diagnosis suggestive of leishmaniasis, parasites could not be identified microscopically, but amastigotes were shown using imprints. In 18 cases who had no skin biopsy, touch imprint preparations from the lesions were stained with Giemsa and revealed leishmania amastigotes [Figure 6].
Figure 1: Nodulo-ulcerative cutaneous lesions of cutaneous
leishmaniasis over left cheek

Click here to view
Figure 2: Erythematous papulonodules on the right arm

Click here to view
Figure 3: Erythematous plaque with surface ulcerati on and crusti ng
on the right cheek

Click here to view
Figure 4: Granulomatous infl ammati on is seen in dermis (Hematoxylineosin

Click here to view
Figure 5:

Click here to view
Figure 6: The large numbers of Leishmania amastigotes within the
macrophages in touch imprint preparati on (May Grunwald Giemsa x1000)

Click here to view
Table 1: Histological epidermal fi ndings of the CL cases

Click here to view
Table 2: Histological dermal fi ndings of the CL cases

Click here to view

   Discussion Top

CL is a centuries-old disease in Turkey where it is given different names such as Urfa boil, Antep boil, year boil, Halep boil, oriental sore and beauty scar. [3] It exhibits a wide spectrum of expression, both clinically and histologically. After a bite by an infected female phlebotomine sand fly, cutaneous lesions begin to develop on the exposed areas of the body. The lesions occur at the site of inoculation after an incubation period. Initially, the lesions are inflammatory erythematous papules, which turn into nodules and develop a crust in the center over the course of several weeks. Eventually, the center of the lesion ulcerates and the edges become raised. The lesions are often painless. Regional lymphadenopathy may occur. In 3-6 months, the lesions heal, leaving behind depigmented residual scars. [5] However, additional clinical presentations of CL have been described, including psoriasiform, eczematous, varicelliform, zosteriform, erysipeloid, lupoid, sporotrichoid, hyperkeratotic and warty forms. Because of the substantial variation in the manifestations of CL, it may be mistaken for either an inflammatory condition or a neoplasm (1). In a study by Saab et al. of 145 CL cases, they reported that 14.4% of the cases had a pre-biopsy clinical diagnosis other than CL. The pre-biopsy clinical diagnosis of the cases ranged from squamous cell carcinoma to deep fungal infection. [6] Bari et al. described unusual presentations of CL in 5.7% of the cases. [7] In a study by Bφer et al. that included 19 cases of CL, they described atypical clinical presentations of CL in 94.7% of the cases, ranging from malignant epithelial neoplasms to sarcoidosis. The clinical diagnosis was CL in only one case. [8] In another study, Ul Bari et al. reported that 6.3% of CL clinically resembled lupus vulgaris/lupus erythematosus. [9] In our study, the patients had one or more noduloulcerative cutaneous lesions, which were located predominantly on the patient's face or extremities. In only one patient, the clinical diagnosis was squamous cell carcinoma. The others were diagnosed as clinical CL.

Histopathologically, acute lesions are usually characterized by hyperkeratosis and acanthosis and, occasionally, epidermal atrophy, parakeratosis, follicular plugging, intraepidermal microabscesses, degeneration of the basal layer and pseudoepitheliomatous hyperplasia. Ulceration is frequently seen. In our study, ulceration was rare. Parasites are usually not found in the epidermis. We detected intraepidermal leishmania amastigotes in one case. The dermis contains a large number of lymphocytes, histiocytes and plasma cells. Rarely, the Grenz zone is evident. We did not observe the Grenz zone in the current study. Dermal necrosis may also be seen in CL cases when the parasites begin to accumulate within the histiocytes. [1] In chronic lesions, there can be a variable degree of epithelial hypertrophy and the dermis may contain large numbers of small non-caseating granulomas. Although abundant parasites are present inside macrophages in early lesions, it is difficult to detect parasites in older lesions. As a result of these factors, there is great variation in the histopathology of CL. [10],[11] Bφer et al. reported that the epidermis was unaltered in 37% of the cases and that parakeratosis, granulomas and nodular or diffuse infiltrates were frequently seen. Epidermal atrophy was rare in their cases. [8] In a histopathological analysis of samples from CL patients by Gumurdulu et al., they reported that hyperkeratosis, follicular plugging, liquefaction degeneration of the basal epidermal cell and non-caseating granulomatous inflammation were frequently seen and that ulceration, lesional crusts and acanthosis were rare. [12] Saab et al. reported that 45.6% of CL cases had atypical histopathological features, which showed marked irregular psoriasiform epidermal hyperplasia. [6] In our cases, liquefaction degeneration of the basal epidermal cell was rare and psoriasiform epidermal hyperplasia was absent. Moreover, the histopathological studies in the current study showed epidermal and dermal changes in all cases. The majority of the cases in the current study exhibited hyperkeratosis, follicular plugging of the epidermis, chronic inflammatory infiltration and non-caseating granulomatous inflammation in the dermis.

Although several methods can be used for the diagnosis of leishmaniasis, including serology, culture, molecular methods and inoculation into animals, clinical examination and histopathology and the detection of the parasites in smears obtained from the lesions are required for a definitive diagnosis. In chronic lesions, it is difficult to find any parasites on histopathological examination. [1] In a study by Gumurdulu et al. including 40 CL cases, they reported that the parasites were located in the dermis in all the cases. [12] Bφer et al. reported that 53% of the cases had parasites on the histopathological examination. (8). In a study by Schubach et al. including 88 CL cases, 30.2% of the patients had parasites on the histopathological examination. Leishmania parasites were detected in 28.2% of the patients using imprints, 43.4% using cultures, 41.4% using immunofluorescence and 58.5% using immunoperoxidase. [13] Rawlins et al. showed that 43.8% of the biopsy material from CL patients contained parasites. [14] In a study including 185 CL cases, Kubba et al. detected 50-80% of parasites by smear, 70% by biopsy and 50% by culture. [15] In our study, 66.7% of the patients had parasites on the histopathological examination. Leishmania parasites were identified in the remainder of the cases using imprints.

The differential diagnosis of CL consists of reactions to foreign bodies, fungal and mycobacterial infections, sarcoidosis, tumors, infected insect bites, impetigo and tropical and traumatic ulcers. [16],[17] For the differential diagnosis of other diseases, such as leprosy, paracoccidioidomycosis, tuberculosis and sporotrichosis, parasitological confirmation is essential, including the identification of the parasite. [13]

The choice and courses of treatment of CL depend on the causative species. Unfortunately, establishment of the species by culture is difficult and time consuming. The World Health Organization recommends intralesional or systemic antimonials for the treatment of CL according to the species and the clinical features. Generally, clinicians encountering CL cases treat patients without identification of the species, which is inferred from the epidemiology of the disease in the area. [18]

In conclusion, CL is a parasitic disease. It presents with a wide spectrum of expression, both clinically and histologically, and may mimic other inflammatory and neoplastic diseases. In a skin biopsy showing histiocytic infiltration and/or a granulomatous reaction, CL should be included in the differential diagnosis. A definitive diagnosis of CL relies on the identification of the parasite in lesional samples.

   References Top

1.Grayson W. Infectious Diseases of the Skin. In: Calonje E, Bren T, Lazar A, McKee PH, editors. McKee's Pathology of the Skin. 4 th ed. Philadelphia: Elsevier Saunders; 2012. p. 844-8.  Back to cited text no. 1
2.Paz C, Doumbia S, Keita S, Sethi A. Cutaneous leishmaniasis in Mali. Dermatol Clin 2011;29:75-8.  Back to cited text no. 2
3.Gürel MS, Yeºilova Y, Ölgen MK, Özbel Y. Cutaneous Leishmaniasis in Turkey. Turkiye Parazitol Derg 2012;36:121-9.  Back to cited text no. 3
4.Postigo JA. Leishmaniasis in the World Health Organization Eastern Mediterranean Region. Int J Antimicrob Agents 2010;36:62-5.  Back to cited text no. 4
5.Habif TP. Clinical Dermatology; a color guide to diagnosis and therapy. 5th ed. Philadelphia: Elsevier Saunders; 2010. p. 632.  Back to cited text no. 5
6.Saab J, Fedda F, Khattab R, Yahya L, Loya A, Satti M, et al. Cutaneous leishmaniasis mimicking inflammatory and neoplastic processes: A clinical, histopathological and molecular study of 57 cases. J Cutan Pathol 2012;39:251-62.  Back to cited text no. 6
7.Bari AU, Rahman SB. Many faces of cutaneous leishmaniasis. Indian J Dermatol Venereol Leprol 2008;74:23-7.  Back to cited text no. 7
[PUBMED]  Medknow Journal  
8.Böer A, Blödorn-Schlicht N, Wiebels D, Steinkraus V, Falk TM. Unusual histopathological features of cutaneous leishmaniasis identified by polymerase chain reaction specific for Leishmania on paraffin-embedded skin biopsies. Br J Dermatol 2006;155:815-9.  Back to cited text no. 8
9.Ul Bari A, Raza N. Lupoid cutaneous leishmaniasis: A report of 16 cases. Indian J Dermatol Venereol Leprol 2010;76:85.  Back to cited text no. 9
10.Convit J. Protozoan diseases of the skin. In: Elder D, editor. Lever's histopathology of the skin. 8th ed. Philadelphia: Lippincott Raven; 1997. p. 553-8.  Back to cited text no. 10
11.Samuelson J. Infectious Diseases. In: Cotran RS, Kumar V, Collins T, editors. Pathologic Basis of Disease. 6th ed. Philadelphia: W.B. Saunders; 1999. p. 329-402.  Back to cited text no. 11
12.Gumurdulu D, Ergin M, Tuncer I, Uzun S, Memisoglu H. Histopathological and clinical evaluation of the cutaneous leishmaniasis in Southern Anatolia, Turkey. Aegean Pathol J 2004;1:57-61.  Back to cited text no. 12
13.Schubach A, Cuzzi-Maya T, Oliveria AV, Sartori A, de Oliveira-Neto MP, Mattos MS, et al. Leishmanial antigens in the diagnosis of active lesions and ancient scars of American Tegumentary leishmaniasis patients. Mem Inst Oswaldo Cruz 2001;96:987-96.  Back to cited text no. 13
14.Rawlins SC, Tiwari T, Chadee DD, Validum L, Alexander H, Nazeer R et al. American cutaneous leishmaniasis in Guyana, South America. Ann Trop Med Parasitol 2001;95:245-51.  Back to cited text no. 14
15.Kubba R, Al-Gindan Y, El-Hassan AM, Omer AH. Clinical diagnosis of cutaneous leishmaniasis (oriental sore). J Am Acad Dermatol 1987;16:1183-9.  Back to cited text no. 15
16.Herwaldt BL. Leishmaniasis. Lancet 1999;354:1191-9.  Back to cited text no. 16
17.Hepburn NC. Cutaneous leishmaniasis. Clin Exp Dermatol 2000;25:363-70.  Back to cited text no. 17
18.Minodier P, Parola P. Cutaneous leishmaniasis treatment. Travel Med Infect Dis 2007;5:150-8.  Back to cited text no. 18

Correspondence Address:
Sezen Koçarslan
Department of Pathology, Medicine Faculty, Harran Universty, Yenisehir Campus, Sanliurfa 63000
Login to access the Email id

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0377-4929.120367

Rights and Permissions


  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]

  [Table 1], [Table 2]

This article has been cited by
1 Biophysical and ultrasonographic changes of acute Old World cutaneous leishmaniasis skin lesions in comparison with uninvolved skin: A possible tool for non-invasive early detection and treatment outcome assessment
Alireza Khatami, Taraneh Yazdanparast, Saman Ahmad Nasrollahi, Akram Miramin Mohammadi, Somayeh Yadangi, Ali Khamesipour, Martin Kassir, Alireza Firooz
Dermatologic Therapy. 2022;
[Pubmed] | [DOI]
2 Epidemiological and genetic characteristics of asymptomatic canine leishmaniasis and implications for human Leishmania infections in Egypt
Mai Abuowarda, Huda O. AbuBakr, Elshaimaa Ismael, Mohamed Shaalan, Mona A. Mohamed, Samira H. Aljuaydi
Zoonoses and Public Health. 2021; 68(5): 413
[Pubmed] | [DOI]
3 Diffuse cutaneous leishmaniasis and HIV co-infection: A case report and review of the literature
Ari A. Kassardjian, Kaitlyn M. Yim, Sina Rabi, Tom Z. Liang, Gene H. Kim, Maria T. Ochoa, Martin V. Sattah, Iris Z. Ahronowitz
Journal of Cutaneous Pathology. 2021; 48(6): 802
[Pubmed] | [DOI]
4 Cutaneous leishmaniasis in refugees from Syria: complex cases in Berlin 2015–2020
Andreas K Lindner, Joachim Richter, Maximilian Gertler, Marc Nikolaus, Gabriela Equihua Martinez, Kirsten Müller, Gundel Harms
Journal of Travel Medicine. 2020; 27(7)
[Pubmed] | [DOI]
5 The impact of refugees on leishmaniasis in Turkey: a new Syrian/Turkish Leishmania tropica population structure described by multilocus microsatellite typing (MLMT)
Mehmet Karakus,Zeynep Çizmeci,Semsi Nur Karabela,Bilgen Erdogan,Nuray Güleç
Parasitology Research. 2019; 118(9): 2679
[Pubmed] | [DOI]
6 Leishmaniasis in Istanbul; A new epidemiological data about refugee leishmaniasis
Zeynep Çizmeci,Mehmet Karakus,Semsi Nur Karabela,Bilgen Erdogan,Nuray Güleç
Acta Tropica. 2019; 195: 23
[Pubmed] | [DOI]
7 Clinical and epidemiological characteristics of cutaneous leishmaniasis in Sri Lanka
Devika Iddawela,Sanura Malinda Pallegoda Vithana,Dhilma Atapattu,Lanka Wijekoon
BMC Infectious Diseases. 2018; 18(1)
[Pubmed] | [DOI]
8 Physical Trauma among Refugees: Comparison between Refugees and Local Population Who Were Admitted to Emergency Department—Experience of a State Hospital in Syrian Border District
Yigit Duzkoylu,Salim Ilksen Basceken,Emrullah Cem Kesilmez
Journal of Environmental and Public Health. 2017; 2017: 1
[Pubmed] | [DOI]
9 Old World Cutaneous Leishmaniasis and Refugee Crises in the Middle East and North Africa
Rebecca Du,Peter J. Hotez,Waleed S. Al-Salem,Alvaro Acosta-Serrano,Sima Rafati
PLOS Neglected Tropical Diseases. 2016; 10(5): e0004545
[Pubmed] | [DOI]
10 Profile of illness in Syrian refugees: A GeoSentinel analysis, 2013 to 2015
Frank P. Mockenhaupt,Kira A. Barbre,Mogens Jensenius,Carsten S. Larsen,Elizabeth D. Barnett,William Stauffer,Camilla Rothe,Hilmir Asgeirsson,Davidson H. Hamer,Douglas H. Esposito,Philippe Gautret,Patricia Schlagenhauf
Eurosurveillance. 2016; 21(10)
[Pubmed] | [DOI]
11 Effect of the Syrian Civil War on Prevalence of Cutaneous Leishmaniasis in Southeastern Anatolia, Turkey
Rahime Inci,Perihan Ozturk,Mehmet Kamil Mulayim,Kemal Ozyurt,Emine Tugba Alatas,Mehmet Fatih Inci
Medical Science Monitor. 2015; 21: 2100
[Pubmed] | [DOI]
12 Severe ulcerative penile leishmaniasis – Importance of PCR-based diagnostics
V.G. Herbert,A. Böer-Auer,A. Brandenburg,T.M. Falk,I. Reiter-Owona,J.K. Rockstroh,K. Reich
Journal of Infection. 2015;
[Pubmed] | [DOI]
13 Natural Leishmania infection of Phlebotomus sergenti (Diptera: Phlebotominae) in an endemic focus of cutaneous leishmaniasis in Sanliurfa, Turkey
Samiye Demir,Mehmet Karakus
Acta Tropica. 2015; 149: 45
[Pubmed] | [DOI]


    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Email Alert *
    Add to My List *
* Registration required (free)  

    Materials and Me...
    Article Figures
    Article Tables

 Article Access Statistics
    PDF Downloaded127    
    Comments [Add]    
    Cited by others 13    

Recommend this journal