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Year : 2022  |  Volume : 67  |  Issue : 3  |  Page : 311
The clinical phenotypes of cutaneous leishmaniasis in central and Southwest Regions of Yemen

1 Department of Dermatology, Faculty of Life Sciences and Medicine, King's College London, SE1 9RT, London, UK
2 Department of Dermatology, Rutgers New Jersey Medical School, New Jersey, United States
3 Department of Dermatology, Faculty of Medicine and Health Sciences, Taiz University, Taiz, Yemen

Date of Web Publication22-Sep-2022

Correspondence Address:
Ahlam M Muthanna
Department of Dermatology, Faculty of Life Sciences and Medicine, King's College London, SE1 9RT, London
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijd.ijd_81_22

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Background: Cutaneous leishmaniasis (CL) is endemic in Yemen. CL displays a spectrum of typical and atypical morphologies yet understudied in the central and southwest regions of Yemen. Aims and Objectives: To identify the typical and atypical clinical phenotypes of CL in the central and southwest regions of Yemen. Materials and Methods: A survey of 145 patients who visited Prof. Al-Qubati Clinic in Taiz between 2010 and 2015, was conducted. Results: Children and residents of the rural areas were at high risk of exposure to the insect vector. The typical phenotype was single (67%), facial (58%) and ulcerated nodule (35%). Other usual phenotypes were small ulcers (21.4%) and non-ulcerative papules and nodules (21%). Unusual phenotypes constituted 12% of the cohort and included psoriasiform, eczematous, erysipeloid, lupoid, verrucous, large ulcerative, leishmania recidivens, satellite, granulomatous infiltrative and hyperkeratotic plaques. Mucous membrane involvement was evident in 10.6% and was also polymorphic. Conclusion: CL has many morphologic patterns in central and southwest regions of Yemen, some are clinically deceptive.

Keywords: Cutaneous leishmania, phenotypes, risk factors, unusual/atypical, usual/typical

How to cite this article:
Muthanna AM, Malhomme HD, Schwartz RA, Al-Qubati YA. The clinical phenotypes of cutaneous leishmaniasis in central and Southwest Regions of Yemen. Indian J Dermatol 2022;67:311

How to cite this URL:
Muthanna AM, Malhomme HD, Schwartz RA, Al-Qubati YA. The clinical phenotypes of cutaneous leishmaniasis in central and Southwest Regions of Yemen. Indian J Dermatol [serial online] 2022 [cited 2022 Sep 29];67:311. Available from:

   Introduction Top

Cutaneous leishmaniasis (CL) is a major public health problem in Yemen and leaves a mutilating scar triggered by untreated disease or corrosive chemicals practiced by some traditional healers in Yemen.[1] Clinically, CL is a polymorphic disease.[2] The ulcerated nodule “dry type”, typical of L. tropica species, and more ulcerative lesions “wet type”, caused by L. major, are the classic leishmania phenotypes in Old World leishmaniasis.[2] Atypical phenotypes are not uncommon, but make the diagnosis challenging because of the wide range of disease mimickers.[2],[3] It is important that physicians become aware of the atypical presentation of CL in endemic areas to avoid missing the diagnosis and treatment delay, which can result in severe mutilation.[4] There is some variation in the histopathological reaction in different clinical morphologies presentation [Table 1].
Table 1: Histopathological correlation with the varied morphological presentation

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Studies from Yemen proved that the disease is endemic in all regions.[5],[6],[7],[8],[9] The first case was reported from the north region in 1933.[10] In a series of studies from the same region, the typical phenotype was a localized ulcerative nodule and atypical morphologies ranged from erysipeloid, verrucous plaques, infiltrated plaques with scaly surface, infiltrated indurated granulomatous plaques, induration of the whole face, lichenoid plaques, nodulo-tumorous plaques, sporotrichoid to the recurrent variant of CL, Leishmania recidivens.[5],[11],[12]

The disease was also documented in the southwest and central regions. First cases were documented in Taiz and Tihama in 1986.[13] Al-Qubati[14] reported a prevalence of 143 and 183 per 100,000 between 1987–1993 and 2007–2009,[9] respectively, from these areas. Muqbel described 82 cases from Lahj in 2012.[6] However, clinical morphologies were less studied from these regions of Yemen. In this study, we focus more on the spectrum of clinical phenotypes of CL in patients residing in the central and southwest regions of Yemen. This the first study that identifies a wide range of CL clinical morphologies from the region understudy.

   Materials and Methods Top

This is a clinic-based survey of CL patients who visited YAQ Clinic, based in Taiz City, for treatment during 2010–2015. The following data were collected from 145 patients: (a) sociodemographic data: age, gender, city of residence, (b) history of contact with CL patients and (c) distribution pattern and clinical phenotypes. Photos were taken from patients after obtaining consent. Diagnosis was based on the long duration of the lesions (1 month or more), coming from, or visiting an endemic leishmania area, clinical picture and identifying the amastigotes using Slit Skin Smear (SSS) stained with Giemsa. This method was proved to be highly sensitive in confirming CL in Yemen with sensitivity rate of 95.3%.[5] Skin biopsy was taken in unusual cases. Culture on Novy–MacNeal–Nicolle (NMN) medium and PCR tests were not available in our setting. The data was then analyzed using descriptive frequencies. The ethics committee is obtained on 13/3/2007.

   Results Top

Sociodemographic characteristics

More than half of the patients, 100 (69.5%), were residing in highland governorates in the southwest and central regions: Taiz 69 (48%), Ibb 31 (21.5%), Lahj 35 (24.3%), Dale'a 3 (2.1%), Abyan 1 (0.7%). Less patients, 5 (3.5%) were from the north: Sana'a 1 (0.7%), Thamar 2 (1.4%) and Raymah 2 (1.4%). All patients were Yemenis. Both females and males were infected at a similar rate, 71 (49%) and 74 (51%), respectively. CL was more common in children between 1 and 14 years, 75 (52.3%); followed by adults between 15 and 45 years, 55 (37.9%); and the lowest frequency, 12 (8.3%), was recorded in those aged >45 years.

Majority of the CL cases were living in rural areas, working as agriculturists and rearing animals such as cattle and dogs either in the basement or within few metres from their houses. When asked about living with the patients who had CL, 59 (43.7%) reported positive contacts and 76 (56.3%) denied contact with CL patients.

Distribution pattern and clinical phenotypes

Most of the patients in our study had single lesions, 97 (67%). Patients with multiple lesions, 48 (33%) had between 2–12 lesions; 29 patients had 2 lesions; 1 patient had 7 and another had 12 lesions. Most lesions in our study (n = 111) measured between 0.5 and 4 cm in diameter, with a median size of 2 cm. Lesions were widely distributed on all body areas in our cohort. There were 234 lesions in total. Most lesions were on the face, 136 (58%), followed by upper limbs, 53 (22.6%), lower limbs, 42 (18%) and lastly on the trunk, 3 (1.3%). On the face, there were 111 lesions on cheeks and other facial areas. Less lesions, 25 lesions (10.6%), were on mucous membranes.

CL displayed a wide spectrum of clinical phenotypes in our cohort [Flow Chart 1]. The typical phenotype in our study was centrally ulcerated nodules 35% (n = 82) [Figure 1]a,[Figure 1]b,[Figure 1]c,[Figure 1]d. In some patients, lesions ulcerated because of traditional healer interventions and not due to the disease itself, making the lesion look unusually large, ulcerative and crusty [Figure 1]c. Few patients had slightly eroded papules and nodules [Figure 1]e,[Figure 1]f,[Figure 1]g,[Figure 1]h mimicking acne [Figure 1]f,[Figure 1]g,[Figure 1]h. Ulcers were recognized in 21.4% (n = 50) [Figure 2]a and [Figure 2]b. Few patients had multiple ulcers [Figure 2]c and [Figure 2]d. One infant developed three small ulcers arranged on a straight line, reflecting the breakfast–lunch–dinner pattern of insect bite on the face [Figure 2]c.
Figure 1: (a) Classic dry type CL on the temple with firm margin and central ulceration “volcano sign”. (b) Mother and two children with classic multiple dry type CL. (c) Dry type but with extensive ulceration induced by corrosive substances applied by traditional healers. (d) Moderate size ulcerative, keratotic, dry nodules and plaque. (e-f) Slightly eroded nodules. (g and h) Non-ulcerted granuolmatous nodules and papules

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Figure 2: (a and b) Wet type CL. (c and d) Multiple wet type CL

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Lesions on mucous membranes showed less obvious features than those on skin [Figure 3]. In our study, 25 lesions (10.6%) were on mucous membranes: lips, nose, eyelids and ear. Lesions on lips resulted in diffuse lip swelling [Figure 3]a,[Figure 3]b, localized lip swelling [Figure 3]c, and localized erosions and ulcerations [Figure 3]d. CL on ear and eyelid resembled a furuncle [Figure 3]e,[Figure 3]f. On the nose, lesions caused extensive erosions with dry and serous crusting resembling lupus pernio or impetigo contagiosa [Figure 3]g.
Figure 3: (a and b) Diffuse lip swelling. (c and d) Localized lip ulceration and erosion. (e and f) Furuncle like lesion. (g) Erosions along the nasal margin with dry and serous crusts

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Atypical phenotypes constituted 12% (n = 28) in our survey. These were in the form of well-defined and large ulcerative plaques which were primary lesions in some cases [Figure 4]a and [Figure 4]b, but were sometimes secondary to corrosive substances commonly applied by traditional healers to treat leishmania in rural areas, resulting in large ulcers with thick adherent crusts [Figure 4]c,[Figure 4]d,[Figure 4]e. Large and infiltrative granulomatous plaques appeared more on extremities [Figure 4]f,[Figure 4]g,[Figure 4]h. Other atypical morphologies were psoriasiform plaques [Figure 4]i, discoid eczematous plaques [Figure 4]j, ill-defined facial plaques that mimicked atypical mycobacterial infections and lupus vulgaris [Figure 4]k and [Figure 4]l, facial lupoid plaques [Figure 5]a,[Figure 5]b,[Figure 5]c, verrucous plaques phenotype on the lower limbs [Figure 5]d and [Figure 5]e and erysipeloid phenotype [Figure 5]f. A 7-year-old girl was seen with recurrent leishmania, leishmania recidivens, which appeared as active crusts and scaling at the margin of a healed leishmania scar [Figure 5]g. The 12-year-old girl in [Figure 1]b developed localized spread of CL in the form of satellite, small, red papules around the primary ulcer on the nose [Figure 5]h. This primary ulcer was covered with a black eschar most due to traditional healer manipulation. Diagnosis was challenging in these cases; skin biopsy confirmed the diagnosis and ruled out other diseases.
Figure 4: (a and b) Primary well-defined large ulcerative plaques. (c–e) Large ulcers with thick adherent crusts secondary to corrosive substances. (f–h) Granulomatous plaques. (i and j) Papulo-squamous plaques. (k and l) Ill-defined plaques vegetative plaques

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Figure 5: (a–c) Lupoid phenotype CL. (d and e) Verrucous phenotype. (f) Erysiploid phenotype. (g) Leishmania recidivens. (h) Satellite phenotype, obvious small papules scattered around the larger ulcerated manipulated nodule on the nose

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   Discussion Top

Based on our findings, rural communities, families with CL-affected members and children were the populations at the highest risk of developing leishmania. Young children were affected more than individuals aged >14 years, which is consistent with the findings from studies in Taiz,[15],[16] Al-Bayda,[8] Thamar[17] and Hajjah,[18] where prevalence among children was 62.1%, 57.2%, 76.3% and 60%, respectively. In Yemen, majority of CL patients are reported from rural areas.[8],[15] The environmental and housing conditions in these areas are the important risk factors for Leishmania spread.[8],[15],[19]

Based on our findings, the commonest phenotype in the southwest and central regions of Yemen was single, localized, facial, localized and centrally ulcerated nodule “dry type”. Previous studies from the southwest region recognized a similar phenotype at a rate between 58% and 70%.[6],[12],[15],[16] This phenotype was also prevalent in the northern part of Yemen.[5],[11],[12] The second most common morphology in our cohort was the ulcerative phenotype “wet type” and were not detected until now in the north or other Yemeni regions.[5] Atypical phenotypes similar to our study were also described from the northern region of Yemen.[11],[18] However, there were less atypical phenotypes in our study compared to the northern region where phenotypes such as sporotrichoid, L.recidivens and disseminated CL were also documented.[5]

Nodules with a keratotic surface was not a common morphology in our cohort or other Yemeni regions. These phenotypes were well described from Pakistan.[12] In few patients, leishmania nodules were unexpectedly very small and non-ulcerative, mimicking acne nodules, sarcoidosis and granulomatous reactions to insect bites [Figure 1]e,[Figure 1]f,[Figure 1]g,[Figure 1]h. Similar phenotype was identified in the Old and New CL world, Mediterranean Basin and the United States, respectively.[20],[21]

Leishmania recidivens, also known as recurrent leishmania, is evident on an old leishmania scar.[22] We had one patient with this variant. This phenotype was also documented from the northern region.[5] Verrucous CL was documented on the lower limbs of a pregnant women in Syria and South America.[23],[24] However, in our cohort this phenotype was found on the lower limbs in two male adults. These phenotypes are not uncommon in L. tropica countries.[2] The chronicity, clinical morphology and granulomatous histological features of atypical phenotypes may lead to misdiagnosis with other infectious and non-infectious granulomatous diseases such as lupus vulgaris, tuberculoid leprosy, lupus erythematous, and sarcoidosis.[4]

Lesions on mucous membrane were also polymorphic in our study and had wide mimickers: chronic actinic cheilitis, chronic granulomatous cheilitis and squamous cell carcinoma. Phenotypes on mucous membrane in our survey were similar to those in northern region.[5],[11]


The study was conducted in a private clinic, while the affected population reside in rural areas. Hence, only CL in patients who can afford transportation expenses from the rural areas to the city, which is significantly costly, were studied. Due to poverty, affected population in rural areas access traditional healers for CL treatment. So, we might have missed a large proportion of affected individuals thus making our results less generalizable. We recommend that CL surveys are conducted in rural areas under study so that people can access health services, thus making study results more generalizable from these areas and are comparable to other Yemeni regions.

Financial support and sponsorship

This research received no funding from any research organization. It was conducted by the clinicians working in the clinic as part of their interests in doing research on Cutaneous Leishmaniasis.

Conflicts of interest

There are no conflicts of interest.

   References Top

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

  [Table 1]


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