Journal of Global Infectious Diseases

ORIGINAL ARTICLE
Year
: 2017  |  Volume : 9  |  Issue : 4  |  Page : 146--150

Epidemiological trends of cutaneous leishmaniasis in Al-Madinah Al-Munawarah Province, Western Region of Saudi Arabia


Miskelyemen Abdelatti Elmekki1, Mogahid M Elhassan1, Hani A Ozbak2, Ilham T Qattan2, Satti M Saleh3, Ali H Alharbi3,  
1 Department of Clinical Laboratory Sciences, College of Applied Medical Sciences, Taibah University, Al-Madinah Al-Munawarah, KSA; Department of Medical Microbiology, College of Medical Laboratory Sciences, Sudan University of Science and Technology, Khartoum, Sudan, KSA
2 Department of Clinical Laboratory Sciences, College of Applied Medical Sciences, Taibah University, Al-Madinah Al-Munawarah, KSA
3 Department of medicine, Meeqat Hospital, Al-Madinah Al-Munawarah, KSA

Correspondence Address:
Dr. Miskelyemen Abdelatti Elmekki
Department of Clinical Laboratory Sciences, College of Applied Medical Sciences, Taibah University, Al-Madinah Al-Munawarah
KSA

Abstract

Objective: To investigate the epidemiological trends of cutaneous leishmaniasis (CL) in Al-Madinah Al-Munawarah, western region of KSA. Materials and Methods: Four hundred and sixty-seven parasitologically confirmed CL cases attending Al-Meeqat Hospital, Al-Madinah, during 2012–2015, were included in this study. Results: Both Saudi and non-Saudi nationals were infected, with the highest infection rate being among Saudis (68.7%). Males were more affected than females as 86.9% of the total CL cases were males. Moreover, CL was prevalent in all age groups with higher frequency among young adults and adolescents (23.1% and 22.7%, respectively). Interestingly, almost all the patients in the adolescent and child age groups were Saudis (96.2% and 93.5%, respectively). Considering geographical distribution, the highest percentage of the cases (40.5%) were from the northern parts of Al-Madinah province while the eastern parts reported the least infection rate (7.3%). Few cases (2.5%) were supposed to encounter the infection abroad. Additionally, the frequency of infection was found to follow a seasonal distribution. Regarding treatment, pentostam, ketoconazole, or cryotherapy were the treatment options usually used. Conclusion: CL is prevalent in Al-Madinah Al-Munawarah area and new foci are being introduced. Thus, detailed studies with large surveillances regarding vector and reservoir hosts in and around the area are needed.



How to cite this article:
Elmekki MA, Elhassan MM, Ozbak HA, Qattan IT, Saleh SM, Alharbi AH. Epidemiological trends of cutaneous leishmaniasis in Al-Madinah Al-Munawarah Province, Western Region of Saudi Arabia.J Global Infect Dis 2017;9:146-150


How to cite this URL:
Elmekki MA, Elhassan MM, Ozbak HA, Qattan IT, Saleh SM, Alharbi AH. Epidemiological trends of cutaneous leishmaniasis in Al-Madinah Al-Munawarah Province, Western Region of Saudi Arabia. J Global Infect Dis [serial online] 2017 [cited 2020 Sep 29 ];9:146-150
Available from: http://www.jgid.org/text.asp?2017/9/4/146/220407


Full Text

 Introduction



Old-world cutaneous leishmaniasis (CL), which occurs in Africa, Europe, Middle East, and Asia, is caused by Leishmania major, Leishmania tropica, and Leishmania infantum and is zoonotic with wild rodent/gerbil colonies representing the reservoir host. The estimated annual world incidence is around 1–1.5 million cases with over 100,000 new cases in the eastern Mediterranean region.[1] Some reports proved that L. tropica can also cause an anthroponotic form of CL.[2]

The transmission of leishmaniasis was observed to be focally associated with the parasite and the reservoir host distribution, which is in turn dependent on the ecology.[3] Domestication of the transmission cycle, urbanization, as well as introduction of agricultural projects into new areas are part of the environmental changes that can increase leishmaniasis incidence.[3],[4]

Phlebotomine sandflies, with over fifty species of genus Phlebotomus in the old world, and genus Lutzomyia in the new world, are the vector of leishmania that transmit disease to humans.[4]

Depending on the type and duration of the lesion, there is a variability of the clinical and histological spectrum in CL [5],[6] with the strain of parasite organism, host immunity, and other environmental factors contributing to this variation.[6],[7]

Regarding host immune response in CL, macrophages, although are the major site of parasite replication, are also responsible for parasites' killing.[8] However, it is well known in leishmaniasis that Th1 development through IL-12 leads to resistance, while the early production of IL-4 results in susceptibility.[9],[10]

Classical diagnosis of CL depends on the clinical features, microscopic examination of aspirate, skin biopsy, or scraping to identify the amastigotes (Leishman–Donovan [LD] bodies) or to culture the promastigote stage on specific media. However, all these methods are of low sensitivity.[11],[12] New methods with higher sensitivity and specificity have been introduced in the diagnosis field including serological and molecular techniques.[13],[14],[15]

Treatment of the most forms of CL is mainly by one of the pentavalent antimonials; sodium stibogluconate or meglumine antimonate. CL is mostly self–healing; however, treatment is needed in cases of severe disseminated lesions and in antropophilic transmission as in L. tropica infections. Reports included different regimens with several drugs. Stibocaptate, chloroquine, niridazole, rifampicin, and streptomycin [16] as well as cryotherapy or cryosurgery [17] were used. Some combination therapies were also tried.[18],[19] However, several studies regarding treatment were uncontrolled and not randomized, not taking into consideration all the factors and thus are not highly recommended.[20]

In Saudi Arabia, CL has been known for a long time and was considered of minor importance until 1975 when it was considered by the Saudi Ministry of Health as a disease that requires control.[21] Although declining of CL incidence in Al-Hassa in the eastern province of Saudi Arabia has been reported,[22] the disease is still endemic in different places of the kingdom,[22] and in the past 7 years, over 19,000 cases of CL have been reported. It is more common in males and appears to be more prevalent in adults.[23] Overall, it is found in equal percentages between Saudis and non-Saudis and is more prevalent in Al-Qassim area and least prevalent in Aljouf area.[23]

CL caused by L. major has been reported in many parts of Saudi Arabia, with Phlebotomus papatasi confirmed to be the vector, as in Al-Hasa area,[24] while CL caused by L. tropica is endemic in the southwestern part of the country [24],[25] with P. sergenti identified as the vector.[26],[27]

In Al-Madinah Al-Munawarah, both L. major and L. tropica were recently identified as the causative organisms of CL.[15]

 Materials and Methods



Study area and population

Al-Madinah Al-Munawarah is a region of Saudi Arabia, located on the country's west side, along the Red Sea coast. It coordinates a latitude of 25°0′N, a longitude of 39°30′E, and with an altitude of 1995 ft. It has an area of 151,990 km 2 and a population of 1,777,973 (2010 census), subdivided into seven governorates which include Medina, Al Hunakiyah, Mahd Al Thahab, Al-'Ula, Badr, Khaybar, and Yanbu Al Bahar. Medina has a hot desert climate; summers are extremely hot with daytime temperatures averaging about 40°C (104°F) with nights about 28°C (82°F). Temperatures above 45°C (113°F) are not unusual between June and September. Winters are milder, with temperatures from 12°C (54°F) at night to 24°C (75°F) in the day. There is very little rainfall, which falls almost entirely between November and May.

This descriptive, analytical, cross-sectional study was carried out by assessing all individuals who referred to the Meeqat Hospital (Al-Madinah Al-Munawarah, Saudi Arabia) due to suspected CL during 2012–2014.

Overall, 467 patients confirmed positive CL patients were included after being given their informed consents. The patients completed a special questionnaire for basic demographic data including age, sex, nationality, lesion type, time of incidence, diagnosis, and type of treatment prescribed.

Specimen collection and smear preparation

After cleaning the lesions and the adjacent skin around them, they were sterilized with disinfectant. After that, ~0.1 mL of sterile 0.9% saline was drawn into a 1.0–3.0 mL syringe with 23- to 27-gauge needle and the needle was inserted into the nodule or ulcer's margin and rotated gently several times. A small amount of saline was injected under the skin into the tissue, the needle was rotated while gentle suction was applied, and some tissue aspirate and freed tissue were withdrawn. The needle was withdrawn from the lesion, and part of the aspirate was discharged onto a clean glass microscope slide for smear preparation. After smears had dried completely, they were fixed with 100% methanol for 20–30 s, allowed to dry, and then stained with Giemsa for 20–30 min, CL was confirmed by the presence of Leishmania amastigotes (LD bodies) under the microscope.[28] Those with negative smears were excluded.

Statistical analysis

The SPSS statistical software package, version 16 (SPSS Inc., Chicago, IL, USA) was applied for the data analysis. Descriptive statistics were used to describe the basic features of the data in this study. Differences in categorical variables between groups were compared and analyzed using the Chi-square test. A two-sided P < 0.05 was considered statistically significant.

 Results



A total of 467 participants including both males and females and with different ages were diagnosed as smear positive for LD bodies between January 2012 and March 2015 [Table 1].{Table 1}

Both Saudi and different non-Saudi nationals were infected; 321 (68.7%) were Saudis and 146 (31.35) were residents of different Asian, African, and Arabian nationals who live in Al-Madinah Al-Munawarah area [Table 1]. This difference in percentage was statistically significant (P < 0.000).

Out of the 467 patients with confirmed CL, 406 (86.9%) were male and 61 (13.1%) were female with a difference that was statistically significant (P < 0.0001).

The 21–30 years' age group composed of the highest frequency (n = 108, 23.1%) of patients with CL while the lowest frequency of the infection was recorded in individuals with >50 years of age. The difference between age groups is highly statistically significant (P < 0.0001). Regarding gender and age distribution among Saudis and non-Saudis, the highest percentage of infected females was among Saudis (54/61, 88.5%) which is significantly higher than that in non-Saudis. Interestingly, 20/54 (37%) of the infected Saudi females are of the age group of 10 years and less and 36/54 (66.7%) are between 11 to 20 years of age. This is similar to previous findings from the KSA [22],[29] and from other parts of the world.[30],[31],[32],[33] Moreover, almost all the children (both males and females) in the two age groups mentioned above are Saudis (93.5% and 96.2%, respectively).

The surroundings of Al-Madinah Al-Munawarah region were divided into North, South, East, and West while the central part of the study area was considered as the city of Al-Madinah. Assessment of the prevalence of CL in the different parts around Al-Madinah Al-Munawarah revealed that, while the northern area had the highest number of infected individuals (n = 189; 40.5%), the lowest rate was observed in the eastern areas (n = 34; 7.3%) [Table 2]. The different towns, villages, and country sides where the patients were resident are shown in [Table 2]. Few patients, who were non-Saudis, and who were from known CL-endemic countries, were supposed to encounter the infection outside the KSA [Table 2]. The difference in the prevalence of CL between different geographical zones was highly statistically significant (P < 0.0001).{Table 2}

When the month of encountering the infection was taken into consideration, the highest frequency was observed from January to May [Figure 1], with another elevation in September.{Figure 1}

Regarding treatment, most of the cases were treated with standard dose (20 mg/kg/day for 21 days) of pentostam (n = 268, 57.4%) or ketoconazole with an oral dose of 10 mg/kg/day for 28 days (n = 191, 40.9%) while few (n = 8, 1.7%) with cryotherapy [Figure 2]. Treatment methods are dependent on the number and severity of the lesions, with the more severe lesions requiring systemic treatment and the mild ones can be treated with simple cryotherapy. In this study, the differences between frequencies of lesions, as reflected by methods of treatment, are highly statistically significant (P < 0.000).{Figure 2}

 Discussion



CL is well known in the old world since ancient times. In the KSA, CL was first reported in 1973 in the eastern province. However, in Al-Madinah Al-Munawarah, although many cases are annually reported, the epidemiology of CL has not been well studied.

The total number of patients was 467, 86.9% of them were male and 13.1% were female. The significant increase in infection among males could be explained by the nature of social life in the KSA. The men are responsible for work in the farms and outdoors while the women are not. Moreover, women are traditionally covering most parts of their bodies, thus being protected from sand flies; the parasite vector. This possibility is strengthened by the fact that 34% of the total infected females are young children of et al., 2013[22] in Al Hassa, eastern region of KSA, who found dominancy in CL cases among males. Moreover, a recent review study revealed a 77.5% infection rate of CL among males in the KSA.[29] Different studies from Ethiopia, Iran, Afghanistan, and Pakistan showed similar results.[30],[31],[32],[33] However, other studies from the KSA [34] and Africa [35] showed similar infection rate among males and females.

In this study, the most susceptible age group is the age group of 21–30 years, this finding is explained by the fact that this age group is the most active population in the community and that most of the labors are of this age group. This agrees with previous studies in Iran,[30] Kuwait,[36] and other parts of the world [37] that showed that this age group is exactly the one with the highest rate of infection. A review study from the KSA reported by the Saudi Ministry of Health during 2006–2011[29] also showed higher prevalence rate of CL among adults. However, another longitudinal study from the endemic area of Al Hassa, eastern region of KSA, revealed a trend of higher prevalence of infection among children [34]

Regarding the regional distribution, the highest rate of infection was recorded in the northern region of Al-Madinah Al-Munawarah. The geography of Al-Madinah Al-Munawarah is composed of three big valleys that join at the northwestern part of the holy city, resulting in provision of good ecological cover for the vector-breeding sites. Moreover, the northern provinces are composed of the major farming areas and most of the expatriates there are farmers who spend most of their time outdoors.

Regarding the distribution of CL according to the nationality, the majority of the cases was among Saudi nationals. However, the interesting fact was that most of the infected Saudis were in young age of [29] However, a previous study reported higher ratio of infection among Saudis during 2000–2002 which was later on reversed by a higher ratio for non-Saudi nationals, most of which were expatriates.[22] In an epidemiological study over a long period of time (more than 40 years) in 2004, Al-Tawfiq and AbuKhamsin [34] reported that almost all the CL cases were among Saudis (more than 98%). Hence, our results come into agreement with this study, although the infection rate among males and females was not equal as reported in that study and with a difference in the percentage of affected Saudi population which was 68.7% in this study. However, the difference from the other studies may be due to the fact that the vector has been found in new foci around the city, so increasing the infection rate among the original Saudi residents of Al-Madinah Al-Munawarah. In a study in Iran, the majority of CL patients were found to be Iranian in a known endemic area.[30]

Regarding the season of the highest frequency of infection, it was from February to May. This agrees with previous studies from the KSA [22],[34] and is thought to be dependent on the vector activity in this period of the year. Similar results of seasonal increased frequency were reported from Iran [30] and more recently reported from the nearby northwestern part of the kingdom.[38]

Most of the lesions were of the classic form and occur in the lower extremities and the majority of patients had more than one lesion on their bodies (312/467; 66.8%) and it is prevalent in both Saudi and non-Saudi patients. This finding agrees with the results of a longitudinal study from an endemic area of eastern region of the KSA.[22] Treatment options included pentostam as the drug of choice, ketoconazole, and cryotherapy, all of which are the usual prescription for CL treatment.[1]

 Conclusion



Both males and females in all age groups are susceptible to CL; however, most of the infected children are Saudis; this confirms a previous finding from the region.[20] Moreover, CL is not only prevalent in Al-Madinah Al-Munawarah, but is also emerging into new foci of the province which were not previously described as endemic, such as Almeleleh in the North, Yanbua' in the West, Alhanakeia in the East, and Abar Ali in the South. Thus, large-scale studies regarding vector and reservoir host are deeply needed, putting into account the seasonal distribution of the disease.

Acknowledgments

The authors acknowledge the staff members of Meeqat Hospital, Al-Madinah Al-Munawarah, KSA, for their help and support, and Dr. Elkhair Ibrahim Dafa'alla, Disease Vector Control Unit, Ministry of Health, Al-Madinah Al-Munawarah, KSA, for his advice.

Financial support and sponsorship

This project was supported by the Deanship of Scientific Research, Taibah University, Al-Madinah Al-Munawarah, KSA (Grant number 435/6103).

Conflicts of interest

There are no conflicts of interest.

References

1WHO Regional Publications, Eastern Mediterranean Series; 35, Manual for Case Management of Cutaneous Leishmaniasis in the WHO Eastern Mediterranean Region; 2014. ISBN: 978-92-9021-945-3 ISBN: 978-92-9021-946-0 (online) ISSN: 1020-041X
2Marty P, Le Fichoux Y, Pratlong F, Rioux JA, Rostain G, Lacour JP. Cutaneous leishmaniasis due to Leishmania tropica in a young Moroccan child observed in Nice, France. Trans R Soc Trop Med Hyg 1989;83:510.
3WHO. Control of the Leishmaniases. Report of a Meeting of the WHO Expert Committee on the Control of Leishmaniases, 22-26 March, 2010. WHO: Geneva: 2010. p. 5-88.
4Sutherst RW. Global change and human vulnerability to vector-borne diseases. Clin Microbiol Rev 2004;17:136-73.
5Bari AU, Rahman SB. Cutaneous leishmaniasis: An overview of parasitology and host-parasite-vector inter relationship. J Pak Assoc Dermatologists 2008;18:42-8.
6Mehregan DR, Mehregan DA, Mehregan AH. Histopathology of cutaneous leishmaniasis. Gulf J Dermatol Venereol 1997;4:1-9.
7Grevelink SA, Lerner EA. Leishmaniasis. J Am Acad Dermatol 1996;34(2 Pt 1):257-72.
8Birnbaum R, Craft N. Innate immunity and leishmania vaccination strategies. Dermatol Clin 2011;29:89-102.
9Scott P. The role of TH1 and TH2 cells in experimental cutaneous leishmaniasis. Exp Parasitol 1989;68:369-72.
10Himmelrich H, Launois P, Maillard I, Biedermann T, Tacchini-Cottier F, Locksley RM, et al. In BALB/c mice, IL-4 production during the initial phase of infection with leishmania major is necessary and sufficient to instruct Th2 cell development resulting in progressive disease. J Immunol 2000;164:4819-25.
11Goto H, Lindoso JA. Current diagnosis and treatment of cutaneous and mucocutaneous leishmaniasis. Expert Rev Anti Infect Ther 2010;8:419-33.
12Vega-López F. Diagnosis of cutaneous leishmaniasis. Curr Opin Infect Dis 2003;16:97-101.
13Zeyrek FY, Korkmaz M, Ozbel Y. Serodiagnosis of anthroponotic cutaneous leishmaniasis (ACL) caused by Leishmania tropica in Sanliurfa Province, Turkey, where ACL is highly endemic. Clin Vaccine Immunol 2007;14:1409-15.
14Yehia L, Adib-Houreih M, Raslan WF, Kibbi AG, Loya A, Firooz A, et al. Molecular diagnosis of cutaneous leishmaniasis and species identification: Analysis of 122 biopsies with varied parasite index. J Cutan Pathol 2012;39:347-55.
15El-Beshbishy HA, Al-Ali KH, El-Badry AA. Molecular characterization of cutaneous leishmaniasis in Al-Madinah Al-Munawarah province, western Saudi Arabia. Int J Infect Dis 2013;17:e334-8.
16Hawary GH. Studies on Cutaneous Leishmaniasis in Central Region of Saudi Arabia from 1972-1975. Proceeding of the Medical Symposium in Leishmaniasis; 22-24 March, 1980; Dammam, KSA. KSA: Ministry of Health; 1980. p. 73-8.
17Bassiouny A. Cryosurgery in cutaneous leishmaniasis. Br J Dermatol 1983;109:617-9.
18Alrajhi AA, Ibrahim EA, De Vol EB, Khairat M, Faris RM, Maguire JH. Fluconazole for the treatment of cutaneous leishmaniasis caused by leishmania major. N Engl J Med 2002;346:891-5.
19Pareek SS. Combination therapy of sodium stibogluconate and rifampin in cutaneous leishmaniasis. Int J Dermatol 1984;23:70-1.
20Al-Jaser MH. Treatment trends of cutaneous leishmaniasis in Saudi Arabia. Saudi Med J 2005;26:1220-4.
21Ministry of Health. Health Statistical Year Book. Saudi Arabia: Ministry of Health; 2006.
22Amin TT, Al-Mohammed HI, Kaliyadan F, Mohammed BS. Cutaneous leishmaniasis in Al Hassa, Saudi Arabia: Epidemiological trends from 2000 to 2010. Asian Pac J Trop Med 2013;6:667-72.
23Ministry of Health. Health Statistical Year Book. Saudi Arabia: Ministry of Health; 2012.
24El Hassan AM. Cutaneous Leishmaniasis in Al-Ahsa Oasis in Saudi Arabia and in Sudan: A comparative study. Saudi J Med Med Sci 2014;1:64-71.
25al-Zahrani MA, Peters W, Evans DA, Smith V, Ching Chin I. Leishmania infecting man and wild animals in Saudi Arabia 6. Cutaneous leishmaniasis of man in the South-West. Trans R Soc Trop Med Hyg 1989;83:621-8.
26Al-Zahrani MA, Peters W, Evans DA, Ching C, Smith IV, Lane RP. Phlebotomus sergenti, a vector of Leishmania tropica in Saudi Arabia. Trans R Soc Trop Med Hyg 1988;82:416.
27El-Beshbishy HA, Al-Ali KH, El-Badry AA. Molecular characterization of Leishmania infection in sand flies from Al-Madinah Al-Munawarah province, Western Saudi Arabia. Exp Parasitol 2013;134:211-5.
28Bensoussan E, Nasereddin A, Jonas F, Schnur LF, Jaffe CL. Comparison of PCR assays for diagnosis of cutaneous leishmaniasis. J Clin Microbiol 2006;44:1435-9.
29Zakai HA. Cutaneous leishmaniasis (CL) in Saudi Arabia: Current status. J Adv Lab Res Biol 2014;5:29-34.
30Karami M, Doudi M, Setorki M. Assessing epidemiology of cutaneous leishmaniasis in Isfahan, Iran. J Vector Borne Dis 2013;50:30-7.
31Birjees MK. Epidemiology of Cutaneous Leishmaniasis in Larkana District of Sindh Province with Particular Reference to Phlebotomine Sandflies: Public Health Division, National Institute of Health Islamabad, Pakistan; 2001.
32Morrone A, Pitidis A, Pajno MC, Dassoni F, Latini O, Barnabas GA, et al. Epidemiological and geographical aspects of leishmaniasis in Tigray, Northern Ethiopia: A retrospective analysis of medical records, 2005-2008. Trans R Soc Trop Med Hyg 2011;105:273-80.
33Adegboye OA, Kotze D. Disease mapping of leishmaniasis outbreak in Afghanistan: Spatial hierarchical Bayesian analysis. Asian Pac J Trop Dis 2012;2:253-9.
34Al-Tawfiq JA, AbuKhamsin A. Cutaneous leishmaniasis: A 46-year study of the epidemiology and clinical features in Saudi Arabia (1956-2002). Int J Infect Dis 2004;8:244-50.
35Bamba S, Gouba A, Drabo KM, Nezien D, Bougoum M, Guiguemdé TR. Trends in incidence of cutaneous leishmaniasis from 1999 to 2005 in Ouagadougou, Burkina. Med Trop (Mars) 2011;71:312.
36Al-Taqi M, Behbehani K. Cutaneous leishmaniasis in Kuwait. Ann Trop Med Parasitol 1980;74:495-501.
37Klaus SN, Frankenburg S, Ingber A. Epidemiology of cutaneous leishmaniasis. Clin Dermatol 1999;17:257-60.
38Haouas N, Amer O, Ishankyty A, Alazmi A, Ishankyty I. Profile and geographical distribution of reported cutaneous leishmaniasis cases in Northwestern Saudi Arabia, from 2010 to 2013. Asian Pac J Trop Med 2015;8:287-91.