Leishmaniasis is prevalent in different parts of Asia, including Iraq, China, Saudi Arabia, Caucasus, Syria, Southeast Russia, Pakistan, Afghanistan, India and Iran [6,7]. About 12 million people in the world suffer from a variety of leishmaniasis every year, and nearly 400000 new cases of leishmaniasis have been reported in various parts of the world [8]. Approximately, 350 million people live in areas with the risk of leishmaniasis [9]. Nearly 20000 cases with leishmaniasis are reported annually in Iran; however, studies suggest that its actual incidence is 4 to 5 times are higher [8,10].
Cutaneous leishmaniasis does not lead to death in the majority of cases. It is an important issue due to the high prevalence of infected cases, disfiguring skin lesions which may remain for more than one year and the risk of permanent scar. One of the most important problems in controlling leishmaniasis, especially urban CL, is the simultaneous effect of several factors on the disease transmission. Diversity in the disease agent, the variety of vectors, the existence of human and animal reservoirs, differences in environmental conditions like climate, agriculture, and rainfall pattern, and also differences in human factors such as habits, living place, and occupation conditions can play an important role in the transmission or outcome of the infection [11]. Despite identification of the CL-causing parasites, its vector and transmission routes, and in-depth studies on the matter, the measures taken to control it has not been much effective and failed in developing an effective vaccine for the prevention of infection.
Dasht-e-Azadegan County is located in Khuzestan Province. The spread of CL from its neighbour endemic country, Iraq, has led to annual reports on infected cases in the county. According to the report by the Iranian Department of disease prevention and control, this disease has turned into an important health issue in the region. Over the past few years, Dasht-e-Azadegan County has gone through considerable geographic and demographic changes due to immigrant’s population enhancement, which have affected the prevalence of the CL. Therefore, it is necessary to have enough data on the present epidemiological situation of the CL to control the disease in the county. In this study, the relationship between the some risk factors and CL was assessed and the epidemiological and clinical conditions of CL were investigated in this county between 2014-2017.
Materials and Methods
A descriptive-analytical survey was conducted on CL patients from 2014 to 2017 in Dasht-e-Azadegan County. This study has been ethically approved by the Research Ethics Committee of the Ahvaz Jundishapur University of Medical Sciences, Iran (ID: AJUMS.REC.1397.629). This project was done in accordance with the ethical principles and the national norms and standard for conducting Medical research in Iran (Approval ID: IR.AJUMS.REC.1379.629/Approval Date: 2018-11-24). The confidentiality of the records of patients was assured. Informed consent was obtained from all the participants under study.
The population included all patients whose disease was confirmed through laboratory and clinical trials. People who did not have clinical signs and symptoms of CL and did not show Leishman bodies in laboratory samples were excluded from the study. The sampling of lesion secretions were performed and then was streaked on glass slide. After 20-25 minutes, the slides were stained with Giemsa and the microscope slides were visualised with 100 immersion lenses. The leishman-donovan bodies (amastigotes) were observed under light microscopy.
Data were collected by the means of a checklist. A checklist, made by researches, was completed for each patient, indicating age, sex, place of residence, month, occupation, diameter of the wound, result of culture from wound on media, medicinal regime, number and location of CL lesions.
Statistical Analysis
After collecting the data, data were analysed using SPSS 18, as well as descriptive statistics and chi-square and t-tests. Significance level was considered to be p<0.05.
Results
According to the findings, 1093 patients were identified between 2014 and 2017. In total, 582 patients were men (53.2%) and 511 patients were women (46.8%), out of which 209 women were housewives [Table/Fig-1]. The paired t-test suggested a significant relationship between the sex and prevalence of CL.
Frequency distribution of cutaneous leishmaniasis cases by age group, gender, occupation, lesion frequency, residential area, diameter of the wound, medicinal regimen, result of culture from wound in Dasht-e-Azadegan County, southwestern Iran (2014-2017).
| Variable/Year | | 2014 No (%) | 2015 No (%) | 2016 No (%) | 2017 No (%) | Total No (%) | p-value |
|---|
| Age group | 0-10 | 165 (38.2) | 131 (43.8) | 94 (35.6) | 33 (15.7) | 423 (38.7) | <0.01 |
| 11-20 | 114 (26.4) | 62 (20.7) | 56 (21.2) | 19 (19.3) | 251 (23.0) |
| 21-30 | 98 (22.7) | 71 (23.7) | 61 (23.1) | 18 (18.4) | 248 (22.7) |
| 31-40 | 30 (6.9) | 20 (6.7) | 29 (11.0) | 15 (15.3) | 94 (8.6) |
| ≥40 | 25 (5.8) | 15 (5.1) | 24 (9.1) | 13 (13.3) | 77 (7.0) |
| Gender | Male | 237 (54.9) | 153 (51.2) | 137 (51.9) | 55 (56.1) | 582 (53.2) | <0.05 |
| Female | 195 (45.1) | 146 (48.8) | 127 (48.1) | 43 (43.9) | 511 (46.8) |
| Occupation | Child (less than six-year-old) | 118 (27.3) | 94 (31.4) | 64 (24.2) | 227 (27.6) | 303 (27.7) | <0.02 |
| Student | 142 (32.9) | 91 (30.4) | 73 (27.7) | 23 (23.5) | 329 (30.1) |
| Housewife | 73 (16.9) | 57 (19.1) | 57 (21.6) | 22 (22.4) | 209 (19.1) |
| Farmer | 6 (1.4) | 4 (1.3) | 3 (1.1) | 3 (3.1) | 16 (1.5) |
| Worker | 27 (6.2) | 31 (10.4) | 35 (13.3) | 10 (10.2) | 103 (9.4) |
| Unemployed | 24 (5.6) | 6 (2.0) | 15 (5.7) | 6 (6.1) | 51 (4.7) |
| Self-employment and government employee | 42 (9.7) | 16 (5.4) | 17 (6.4) | 7 (7.1) | 82 (7.5) |
| Lesion frequency | 1 | 254 (58.8) | 160 (53.6) | 166 (62.9) | 52 (53.1) | 632 (57.8) | <0.001 |
| 2 | 67 (15.5) | 67 (22.4) | 43 (16.3) | 21 (21.4) | 198 (18.1) |
| 3 | 48 (11.1) | 30 (10.0) | 23 (6.7) | 11 (11.2) | 112 (10.2) |
| ≥4 | 63 (14.6) | 42 (14.0) | 32 (12.1) | 14 (14.3) | 151 (13.8) |
| Residential area | Urban | 274 (63.4) | 193 (64.5) | 167 (63.3) | 63 (64.3) | 697 (63.8) | <0.01 |
| Rural | 158 (36.6) | 106 (35.5) | 97 (36.7) | 35 (35.7) | 396 (36.2) |
| Lesion site | Hand | 177 (41.0) | 123 (41.1) | 88 (38.2) | 37 (37.8) | 426 (38.9) | <0.05 |
| Leg | 101 (23.4) | 71 (23.7) | 74 (28.0) | 24 (24.5) | 270 (24.7) |
| Face | 94 (21.8) | 64 (21.4) | 59 (22.3) | 17 (17.3) | 234 (21.4) |
| Trunk | 13 (3.0) | 7 (2.3) | 15 (5.7) | 3 (3.1) | 38 (3.5) |
| Hand and Leg | 14 (3.2) | 7 (2.3) | 9 (3.4) | 5 (5.1) | 35 (3.2) |
| leg and Face | 5 (1.2) | 4 (1.3) | 3 (1.1) | 2 (2.0) | 14 (1.3) |
| Hand and Face | 17 (3.9) | 15 (5.0) | 6 (2.3) | 6 (6.1) | 44 (4.0) |
| Hand, Leg and Face/Trunk | 11 (2.5) | 8 (2.7) | 10 (3.8) | 4 (4.1) | 33 (3.0) |
| Diameter of the wound | ≤1 cm | 389 (90.0) | 280 (93.6) | 245 (92.8) | 96 (98.0) | 1010 (92.4) | <0.001 |
| ≥2 cm | 43 (10.0) | 19 (6.4) | 19 (7.2) | 2 (2.0) | 83 (7.6) |
| Result of culture from wound | Positive | 419 (97.0) | 298 (99.7) | 263 (99.6) | 98 (100.0) | 1078 (98.6) | <0.001 |
| Negative | 13 (3.0) | 1 (0.3) | 1 (0.4) | 0 (0.0) | 15 (1.4) |
| Medicinal Regimen1,2 | Cryotherapy and Topical Injection | 224 (51.9) | 239 (79.9) | 260 (98.5) | 84 (85.7) | 807 (73.8) | <0.001 |
| Systemic Injection | 0 (0.0) | 1 (0.3) | 3 (1.1) | 0 (0.0) | 4 (0.4) |
| Topical Injection | 207 (47.9) | 59 (19.7) | 0 (0.0) | 14 (14.3) | 280 (25.7) |
| Traditional | 1 (0.2) | 0 (0.0) | 1 (0.4) | 0 (0.0) | 1 (0.1) |
| Total | | 432 (100) | 299 (100) | 264 (100) | 98 (100) | 1093(100) | |
1Regimen: A regimen is a regulated plan of medical treatment, designed to give a positive result; 2Meglumine antimoniate was given for systematic and topical therapy
The oldest and youngest patients were 91-year-old and one-year-old, respectively. Investigation into the disease prevalence showed that the age group of below 10-year-old accounted for the majority of patients with 423 cases (38.7%), followed by 11-20-year-old with 251 cases (23%). On the other hand, the age group of older than 40 years with 77 cases (7%) accounted for the least number of patients. The non-parametric chi-square test showed a significant relationship between the prevalence of the disease and age group [Table/Fig-1].
Findings showed that urban areas accounted for the majority of cases with 697 patients (63.8%) [Table/Fig-1]. The t-test showed a significant relationship between the prevalence of the disease and place of residence.
According to occupation groups, students followed by children (less than six-year-old) accounted for the majority of cases with active lesions with the incidence rates of 30.1% and 27.7% respectively [Table/Fig-1]. The chi-square test showed no significant difference between the prevalence of CL among male and female students; whereas, it showed a significant difference between different job groups. Based on the lesion site, hands with 426 (38.9%) and legs with 270 (24.7%) cases, presented the most affected body parts. The chi-square test showed a significant difference between the anatomic sites of the lesions and the prevalence of CL.
The prevalence rate varied according to the months. In February with 260 cases (23.8%) and January with 254 cases (23.2%) represented the highest incidence rates; however, after this it showed a downward trend and reached 1.1% in July [Table/Fig-2]. The highest prevalence rate was observed in the winter with 649 cases (59.4%). The lowest prevalence rate was observed in the summer (7.2%) [Table/Fig-2]. The non-parametric chi-square test showed a significant relationship between the prevalence of the disease and season.
Frequency distribution of cutaneous leishmaniasis cases by month and season in Dasht-e-Azadegan County, Southwestern Iran (2014-2017).
| Season | Year | 2014 No (%) | 2015 No (%) | 2016 No (%) | 2017 No (%) | Total No (%) | p-value |
|---|
| Spring | April | 2 (0.5) | 20 (6.7) | 18 (6.8) | 12 (10.4) | 52 (4.8) | <0.001 |
| May | 5 (1.2) | 3 (1.0) | 9 (3.4) | 11 (13.5) | 28 (2.6) |
| June | 3 (0.7) | 0 (0.0) | 7 (2.7) | 3 (12.3) | 13 (1.2) |
| Summer | July | 1 (0.2) | 5 (1.7) | 3 (1.1) | 3 (9.6) | 12 (1.1) |
| August | 9 (2.1) | 6 (2.0) | 4 (1.5) | 8 (6.2) | 27 (2.5) |
| September | 5 (1.2) | 13 (4.3) | 13 (4.9) | 9 (7.7) | 40 (3.7) |
| Autumn | October | 10 (2.3) | 23 (7.7) | 9 (3.4) | 11 (5.8) | 53 (4.8) |
| November | 23 (5.3) | 30 (10.0) | 13 (4.9) | 10 (8.5) | 76 (7.0) |
| December | 60 (13.9) | 36 (12.0) | 31 (11.7) | 16 (6.9) | 143 (13.1) |
| Winter | January | 111 (25.7) | 82 (27.4) | 46 (17.4) | 15 (6.9) | 254 (23.2) |
| February | 131 (30.3) | 51 (17.1) | 78 (29.5) | 0 (5.8) | 260 (23.8) |
| March | 72 (16.7) | 30 (10.0) | 33 (12.5) | 0 (6.5) | 135 (12.4) |
Results showed that 92.4% of the patients had a lesion with a diameter of 1 cm or smaller and 7.6% had a lesion with a diameter of 2 cm or larger [Table/Fig-1]. Findings showed a significant relationship between the lesion size and selection of the therapeutic regime (p<0.001), that 73.8% of patients with 1 cm lesion received intralesional injection and cryotherapy.
According to the findings, 632 patients (57.8%) had one lesion and 13.8% of the patients had four or more than four lesions [Table/Fig-1]. The mean number of lesions in the participants was 2.05.
Data analysis showed a significant relationship between the number of lesions and treatment choice. The majority of patients with more than one lesion received the intralesional injection of meglumine antimoniate and cryotherapy; whereas, the patients with more than three lesions received the systematic treatment with meglumine antimoniate.
Discussion
This research showed that the CL is endemic and prevalent in Dasht-e-Azadegan County. The age group of 1-10-year-old accounted for the majority of patients (38.7%). Results of present study were consistent with previous studies conducted in Kerman [12] and Fars [13] Provinces. The highest prevalence rate of CL was observed in the age group of older than 20-year-old in Fars Province [14], Hamadan County [15] and Badrood City [16] and Kashan County [17].
The highest prevalence rate in Brazil [18] and Pakistan [19] was observed in the age group of 10-30-year-old. This difference can be due to the endemicity of CL to Dasht-e-Azadegan County. This is because the prevalence rate of CL follows an upward trend in people aged below 15-year-old in endemic areas, and then starts decreasing due to acquired immunity, making children and students more vulnerable than other occupational groups. Housekeepers are primarily women, hence are prone to CL.
Culture, behaviour, job and dressing code of different Iranian ethnic groups have made males more vulnerable to CL. In studies in Iran and Ganaveh [20,21], the prevalence of the disease was reported higher among males. Results of this study were inconsistent with those of Reithinger R et al., in Kabul [22] and Akhavan AA et al., in a new focus of southern Iran [22,23]. The higher prevalence of CL among males which can be attributed to factors such as working of the majority of males as seasonal migrant workers, working in an open environment, greater the contact of men with infection sources, wearing less clothes than women, being more active in abandoned areas and deserts and increased risk of being bitten in the evening and night [24]. In addition, job travels to endemic areas could have been an important role in the transmission of CL to men.
Findings showed that the majority of patients in this study were urbanites. Studies conducted in Badrood [16] and Hamadan [15] produced results similar to the current study. It is worth noting that regarding the ratio of rural to urban population, the prevalence rate can differ in different counties. In some areas, due to easy access to urban health centres and more sensitivity of the urbanites to the disease, CL is reported less common among villagers. In addition, inadequate environmental health-related measures, farming livestock around the home and the lack of a suitable sewage system, specifically in the marginal areas, which result in an increase in the number of infected phlebotomine sand flies, have caused more reported CL cases in urban areas.
Results showed that hands and legs were the most exposed body parts. In a study conducted in Kermanshah, hands and legs accounted for 47% and 19% of the infected sand fly bite sites, respectively [25]. Moreover, hands and legs accounted for the majority of the sand fly bite sites in Arsanjan County [26]. This may be because of hands and legs are more exposed body parts; therefore, it is recommended that these parts should be covered as much as possible. The application of window and door mesh or insecticide-impregnated mosquito net is also recommended. The frequency of lesions in infected patients, involvement of the most uncovered body parts, and its irreparable complications in terms of appearance highlight its control and prevention.
One of the most important factors influencing CL is climate, which depends on season and month of the year. In this study, winter, followed by spring accounted for the majority of CL cases. On the other hand, its seasonal dispersion pattern in Dasht-e-Azadegan clearly confirms the indigenous transmission of the disease. The first and second half of the year accounted for the most active period of phlebotomine sand flies and the highest incidence rate, respectively. In epidemiological studies, the highest prevalence of CL in other parts of the country was observed in spring and winter, which is consistent with the findings of the current study [27].
Findings of the current study showed that the number of lesions differed in the infected patients and ranged between 1 and 14. The majority of patients (57.8%) had only one lesion. In addition, 65.4% and 46% of the patients in Hamadan County and Badrood City had more than one lesion [15,16]. In Kashan County, only 35.9% of the patients had more than one lesion [17].
In Pakistan, 44% and 24% of the patients had one and two lesions, respectively [19]. The reason behind multiple wounds could be due to the biting procedure of sand flies as these insects perform several bites for each stage of the biting. The other reason for the existence of various wounds could be the abundance of infected sand flies in one area.
The recommended treatment in Iran is the injection of meglumine antimoniate, application of cryotherapy, or the combination of both. Due to spontaneous wound healing, sometimes it is recommended that small wounds should not be treated. Gonzalez U et al., recommended informing patients about the spontaneous healing and the lack of sufficient evidence on the treatment effectiveness before administration of the CL therapy [28]. Different studies in the Eastern Mediterranean Region and Asia have reported an improvement following an intralesional injection of meglumine antimoniate in more than 90% of cases [29,30].
Cutaneous leishmaniasis in patients with intact immune system can be treated topically or intramuscularly, but transplant patients with disseminated leishmaniasis should be hospitalised and treated with combined systemic long-term drugs. The present case was treated with glucantim and Amphotericin B [31]. It is important to monitor the presence of CL in each region and to know the epidemiology and distribution of this disease in the endemic areas. The results of the present study are useful for prevention of CL.
Limitation
The limitation of this study was that the type of parasite was not identified through molecular studies. The strong point is a widespread assessment during several years of CL epidemiology in Dasht-e-Azadegan.
Conclusion
According to the present study the average annual prevalence of CL was found to be 273.25 per 100000 populations (1093 divided by 4-mean annual population in this county in period study was 100000 people) in Dasht-e-Azadegan County. Meantime, the findings of this study showed that CL is spreading southwestern Iran. Dasht-e-Azadegan is an example of the establishment of a focus of CL, through unplanned urban and agricultural development, movement of infected persons and to increases in people and sand fly populations. It is proposed that health authorities should do active screening, follow-up and raise the knowledge about the CL transmission, control and prevention.
It is also recommended to manage more descriptive-analytical studies to determine the role of socioeconomic factors such as population dynamics, development, human behaviour and poverty. Further epidemiological investigations should be conducted to assess the Leishmania infection and its associated risk factors.
1Regimen: A regimen is a regulated plan of medical treatment, designed to give a positive result; 2Meglumine antimoniate was given for systematic and topical therapy