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More than 20 species of pathogenic protozoan parasites of the genus Leishmania are known to cause a group of diseases called leishmaniasis with different clinical spectrums ranging from self-healing cutaneous leishmaniasis to lethal visceral disease [1]. The different species of Leishmania are transmitted by the bite of a female phlebotomine sandfly. Amastigotes liberated from host cells in the insect’s gut transform into promastigotes, which reproduce there and are introduced into a new host when sandfly feeds again [2]. The disease is distributed in 98 countries worldwide, and around 1.3 million new cases, with an estimated 20,000 to 40,000 deaths, are reported annually [3]. Leishmaniasis is endemic in Iraq, where both forms of the disease, cutaneous (Baghdad boil) and visceral (Kala-azar), are found. Leishmaniasis was reported from the eastern provinces of Diyala, Wasit, Missan, and Basrah [4]. Cutaneous leishmaniasis (CL) is prevalent across the whole of Iraq except for in 3 northeastern provinces, and is transmitted by Phlebotomus papatasi and P. sergenti species of sandfly [5]. Two types of CL were reported in Iraq, a zoonotic type caused by L. major and an anthroponotic type caused by L. tropica [6]. In 2000 and 2001 there were 955 and 625 cases of CL respectively, down from 8779 cases in the peak year 1992. Cases of anthroponotic cutaneous leishmaniasis (ACL) predominantly occur in the suburbs of large cities, zoonotic cutaneous leishmaniasis (ZCL) is more widespread and occurs mostly in rural areas, especially in the northern and southern provinces of Iraq [7]. In 2008 there was a large outbreak of CL, with 300 cases being reported from Qadisiyah province [8].

Leishmania cycles between sand flies, reservoir hosts, and humans for the zoonotic type, and between sand flies and humans for the anthroponotic type. Human infections with CL are based on the ecological relationship between human activities and vector– reservoir systems [9]. The prevalence and seasonal tendency of leishmaniasis as a vector-borne disease is likely influenced by climate changes, mostly in temperate zones where increased average temperatures might extend the breeding seasons of the existing sand fly species, or facilitate the establishment of invasive tropical or subtropical species, or both, collectively allowing transmission of diseases in regions where low temperatures previously prevented sandfly over-wintering [10]. Iraq shows various climatic, geographic, and population aspects, some of which may be contributory to the incidence of leishmaniasis. The present study was, therefore, designed to determine the prevalence of cutaneous leishmaniasis (CL) and to demonstrate the association of CL with age, sex, and season.

Materials and methods
Data collection

Data from 7112 patients from all 18 provinces (Figure 1), admitted to Iraqi hospitals from 2011 to 2013 were gathered by Communicable Diseases Control Center (CDC), Ministry of Health, Baghdad, Iraq. These patients were clinically diagnosed with cases of CL and the infection confirmed by one or more methods such as the rK-39 strip test, microscopic examination, and indirect fluorescent antibody test. For each patient, their sex and the season when the case was identified were recorded. Patient age was classified into one of four groups: Group 1: <1-year-old, Group 2: 1–4 years old, Group 3: 5–14 years old, Group 4: 15–45 years old, Group 5: >45 years old. The precise residential address of each patient was recorded from the patients’ hospital files. The data enabled us to determine the provinces the patients were from.

Figure 1

Map of Iraq showing its 18 provinces. Permission to use the map granted by kind courtesy of MemNav. (Source: https://i2.wp.com/www.memnav.com/im/Iraq_map.jpg)

By contrast with the data for patients with CL from the broader Iraqi population, the later was classified based on demographic and environmental criteria. Total population, rural population, urban population, elevation, total annual rainfall and annual mean temperature for three consecutive years (2011–2013), were derived from Central Statistical Organization annual reports for each province [11].

Statistical analysis

Differences in occurrence were examined among sexes and age groups using chi-square tests. Spearman’s correlation coefficient was used for analyzing the effects of spatial, climate, and population factors on CL incidence. Both analyses were conducted using the Statistical Package for the Social Sciences for Windows (version 16, SPSS Inc). P < 0.05 was considered significant.

Results

A total of 7112 CL cases surveyed were reported from 2011–2013. During this time, there was a 44.6% overall decrease in the number of CL positive cases, from 2978 in 2011 to 1648 in 2013. Table 1 shows the sex and age distribution of the CL patients. There were significant differences in occurrence between different age groups (P < 0.05). Cases of CL were largely reported among those aged 15–45 years old. Approximately 8% of patients were <1-year-old. Generally, men and boys were at higher risk for CL than women and girls. Significant differences were noticed between sexes (P < 0.0001). Analyses of age and sex relationships indicated no significant differences (P < 0.05) in prevalence among male and female individuals in the 2 youngest young age groups. However, difference approached significance for the 5–14 age group, and was significant for the 2 oldest age groups.

Sex and age of 7112 patients in Iraq with cutaneous leishmaniasis for the years 2011–2013

201120122013Total
n%n%n%number%
Male174158.5146959.194157.1415158.4
Female123741.5101740.970742.9296141.6
<1 y1685.62349.419411.85968.4
1–4 y83928.228611.526716.2139219.6
5–14 y90530.460724.436722.3187926.4
15–45 y81927.591736.959636.2233232.8
>45 y2478.344217.822413.691312.8
<1 y, male1093.71084.31076.53244.6
<1 y, female592.01265.1875.32723.8
1–4 y, male45915.41455.81489.075210.6
1–4 y, female38012.81415.71197.26409.0
5–14 y, male50717.032713.220412.4103814.6
5–14 y, female39813.428011.31639.984111.8
15–45 y, male48116.257823.335621.6141519.9
15–45 y, female33811.433913.724014.691712.9
>45 y, male1454.931112.51267.65828.2
>45 y, female1023.41315.7985.93314.7

Figure 2 shows the distribution of CL cases among the provinces of Iraq. Cases of CL were reported in 17 of 18 provinces. CL was not reported in patients from Dohuk. Most cases were reported in the neighboring provinces of Diyala and Salahuddin. Approximately a third (n = 2674; 37.6%) of all cases were from these 2 provinces, each of which showed more than 1100 cases for the consecutive years 2011–2013. Elevation, total annual rainfall, and rural population had no significant association with occurrence of the disease. However, the most cases (n = 5968, 83.9%) were reported in lowland provinces with an elevation ≤51 m above sea level. About half of the cases (n = 3310; 46.5%) were reported in provinces that had annual rainfall of more than 190 mm (Diyala, Salahuddin, and Ninevha). About two thirds of cases (n = 4958; 69.7%) occurred in provinces with a rural population of 35.5%–51.6% (Salahuddin, Muthanna, Diyala, Anbar, Babil, Qadisiyah, Ninevha, Wasit, and Dhiqar).

Figure 2

The distribution of cutaneous leishmaniasis among the Iraqi provinces for the years 2011–2013.

Figure 3 shows the seasonal distribution of CL. More than half of all cases (n = 4330; 60.9%) for the years 2011–2013, were identified during winter (January and February), with a peak seen in February (n = 2220 cases).

Figure 3

The seasonal distribution of cutaneous leishmaniasis in Iraq for the years 2011–2013

Discussion

Cutaneous leishmaniasis, caused by L. tropica and L. major, is endemic in Iraq and has caused relatively recent outbreaks [4, 5]. A common name of the disease, Baghdad boil, suggests the disease has a long history in the region [12]. Therefore, the high number of cases recorded was not unexpected. There were 1648 cases of CL recorded in 2013 down from 2978 cases in 2011; this was likely because of the efforts of both the World Health Organization and the Iraqi Ministry of Health. Most cases were detected in men and boys, and the sex differences are more pronounced in older age groups. These differences are likely because men and boys are more likely to be exposed during outdoor activities [13]. Some investigators believe that the sex hormone levels may also affect the establishment and the course of some parasitic diseases, making male individuals more likely to be sensitive to the protozoan infectious agent [14]. Our findings are consistent with the other studies in Iraq [6, 15]. The overall incidence of CL is greater among people who are 5–14 and 15–45 years old. These age groups are the school and work age groups in Iraq for both sexes and they are more likely to participate in outdoor activities and be exposed to sandfly-associated environmental conditions than individuals from other age groups. Further, L. tropica infections result in the development of life-time immunity [16], which may contribute to lower incidence in the oldest age groups [17]. Recently, in some parts of Iraq the population is frequently altered so the disease can be seen in all age groups.

There are many factors that play critical roles in the incidence and distribution of CL in different parts of Iraq particularly in Diyala and Salahuddin, which showed the highest number of cases. These factors are the presence of animal reservoirs for ZCL, and the use of clay to build some of the houses in villages in these areas [15]. Clay maintains a sufficient level of moisture in the sand fly larval habitat so these houses facilitate sand fly breeding. The majority of CL cases occurred in provinces with a more rural population, these provinces have large agricultural areas that attract and harbor many species of insects, and the human population in these regions work mainly on farms where they are potentially more exposed to insect bites [18].

The majority of CL cases were noticed in provinces with low mean elevation. The level of elevation has an apparent effect on vector density. This finding is consistent with previous observations [19], which showed that most CL patients were from the dry and intermediate zones of the low-altitude areas. Landscapes with low elevations and with moderate or low annual rain falls and humidity are likely to be good for vegetation growth, which in turn allows maintenance and even expansion of the population of sand fly hosts. This scenario can potentially increase the infected sand fly numbers and thus the possibility of CL cases [20].

CL cases were more abundant in winter, with a peak in February. The incidence of infection then started to decline from April and reaches its lowest in July and August. This variation in seasonal peak could be the result of the existence of various dominant reservoir species in these areas particularly for ZCL, and the activity of the sand flies. The sand fly season in Iraq is from April through November and peaks in September–October. The incubation period of Leishmania is typically between 2–6 months. When the sand fly bites a host in September or October, cases would become apparent in January or February [21].

This study has reported some initial data on the demographic and environmental correlates of CL. Such work is importance for making informed decisions regarding the assessment of possible management methods for the control of CL in Iraq.

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