Thematic Maps of the Impact of Urbanization and Socioeconomic Factors on the Distribution of the Incidence of Cutaneous Leishmaniasis Cases in Sefrou Province, Central North of Morocco (2007–2011)

Background Leishmaniases are vector-borne diseases with health risks. They cause a big health problem. These parasitic diseases are transmitted by the parasite of the genus Leishmania through sandflies. Objective The aim of this work is to study the distribution of the incidence of cutaneous leishmaniasis (CL) cases and the impact of urbanization and socioeconomic factors and their effects as leishmaniasis risk factors. Methods We conducted a retrospective study of CL cases collected at the level of Sefrou Province during the period from 2007 to 2011. The data was collected from registers of the Medical Delegation of Sefrou Province. The socioeconomic data, namely, the poverty rate, the popular density, and the type of environment (urban/rural) of Sefrou Province, were obtained from the High Commission for Planning. Statistical analysis was performed by SPSS software (version 20). The data were registered in a Microsoft Excel 2010 file. Statistical analysis was based on one-way analysis of variance (ANOVA), and then a correlation study was carried out (Pearson correlation). The results were considered significant when p was less than 0.05. The database was analyzed by QGIS 2.18, which is open source software. Results A total of 349 cases of CL were collected at Sefrou Province from 2007 to 2011. A percentage of 49% of the cases come from urban areas, while 51% of the cases come from rural areas. In the statistical analysis, the division of the incidence of CL cases was found to be significantly associated only with urbanization. For the other factors, the number of people or the poverty rate is not taken into account in the incidence dynamics. Conclusion This study may be useful for the implementation of future adequate measures and controls. Getting rid of leishmaniasis requires a comprehensive approach by acting on the sources of contamination through good continuous surveillance, appropriate management, effective vector control, and awareness-raising strategies.


Introduction
Leishmaniasis is a vector-borne disease caused by a flagellated protozoan of the genus Leishmania belonging to the family of Trypanosomatidae, which affects a variety of human and animal populations worldwide [1]. e epidemiology of leishmaniasis is very complex: 20 species of Leishmania are pathogenic to humans, and 30 species of sandflies are proven vectors in the world [2]. It is widespread in all continents with the exception of Oceania. Eighty-eight countries are affected in the Old World and twenty-two countries in the New World [3]. e global prevalence is estimated at 12 million human cases, with an annual incidence of 1.5 to 2 million new cases, and 350 million people would be exposed to the risk of Leishmania transmission [4].
is alarming situation is of paramount importance since Leishmania/HIV coinfections are frequent, and immunocompromised patients are much less controlled, which increases mortality [5]. In Morocco, leishmaniasis is endemic; the Ministry of Health has declared an annual average of 4,076.6 cases of cutaneous leishmaniasis (CL) and a hundred cases of visceral leishmaniasis (VL) in recent years [6]. In the majority of countries around the Mediterranean, leishmaniasis diseases represent entities of great clinical and epidemiological diversity and constitute a real health problem [7]. ey can be illustrated in three epidemiological entities: zoonotic cutaneous leishmaniasis (ZCL) with Leishmania major (L. major), anthroponotic cutaneous leishmaniasis (ACL) with Leishmania tropica (L. tropica), and VL with Leishmania infantum (L. infantum) [8]. e geographical position of Morocco is characterized by different ecological and bioclimatic conditions which can influence the diversity of vectors and consequently the distribution of the disease [9]. e choice of Province Sefrou as a study area is justified by its epidemic situation of leishmaniasis, as it is considered among the main foci, by means of its proximity to other important foci such as Taza [10], Sidi Kacem [11], and Errachidia [12]. Several entomological studies were pursued at the Province Sefrou that shows the presence of sandflies with a significant density [13][14][15]. e spread of cutaneous leishmaniasis disease is linked to various risk factors [16]; among these factors we notice the socioeconomic factors and the urbanization ones [17,18]. For several years, risk mapping has been used for several researches based on remote sensing and Geographic Information Systems (GIS). Indeed, these tools are of supreme interest with regard to epidemiological surveillance and the relationship between the spread of the disease and environmental factors [19][20][21]. For an effective control, it is necessary to establish a risk map of CL from different municipalities in Sefrou Province.
is work is a combination of the retrospective study and the risk factors for the distribution of CL: climate, urbanization, poverty, and population. e use of GIS allows us to draw up thematic maps identifying areas at risk. Cartographic analysis is very important to better elucidate the relationship between the distribution of CL disease and the factors of leishmaniasis risk. e aim of this present work is to study the epidemiological situation of this type of parasitosis, the distribution of the incidence, and the impact of urbanization and socioeconomic factors as leishmaniasis risk factors.

Materials and Methods
2.1. Study Zone. Sefrou Province (Central North of Morocco) covers an area of 3,520 km 2 with a predominantly rural population of 259,254 inhabitants. From a geographical point of view, it is limited to the south by the Boulemane and Ifrane Provinces, to the east by the Taza Province, to the north by the Fez prefecture, to the west by the Moulay Yacoub and El Hajeb Provinces, and to the northwest by the Taounate Province [22]. According to the municipal division, Sefrou Province has 5 municipalities and 18 rural communes. Most of these mountainous provinces are contaminated and considered as places of human CL [23].

Data Sources.
e data were collected from the registers of the health directorate of Sefrou Province. All cases of CL recorded on the survey forms were confirmed by parasitological diagnosis direct. CL patients with clinical lesions of CL were passively received during the study period at the local laboratory of the health center of Sefrou Province. [24]. e period of the study was four years, from 2007 to 2011. During this period, a total of 349 cases of CL were the subjects of a retrospective study. e socioeconomic data, namely, the poverty rate, the popular density, and the type of environment (urban/rural) of Sefrou Province, were obtained from the High Commission for Planning [25]. e incidence (I) of CL of each commune was calculated as follows: I � number of new cases of the disease in a given population total number of the population at risk of each commune . (1)

Data
Analysis. e data were registered in a Microsoft Excel 2010 file. Statistical analysis was based on one-way analysis of variance (ANOVA), and then the correlation study was carried out (Pearson correlation). e results were considered significant when p is less than 0.05. To achieve the objective of this study, it is essential to integrate the CL health data into a Geographic Information System in order to analyze its spatial distribution in the various municipalities of the Province of Sefrou. In this respect, the data processing was done by QGIS 2.18 software by the integration of Geographic Information System. Statistical analysis was performed with SPSS software (version 20).

Epidemiology of Leishmaniasis in Sefrou Province.
e temporary evolution of the incidence of CL revealed the endemic nature of this parasitosis in Sefrou Province. e study of the epidemiological situation in this Province during the period from 2007 to 2011 declared 349 cases of CL with an average of 5.77 per 100,000 inhabitants. In 2007, the incidence of CL cases was 17.35 per 100,000 population. is value decreased in 2008 to 10.03. From 2009, the incidence of cases increased with a peak in 2010 and decreased afterward ( Figure 1). is could be explained by the fact that the situation of this disease has become perturbing, which is linked to the appearance of new foci of transmission where the risk factors persist [16,26,27]. Also, the alarming epidemiological situation in 2010 witnessed better management of this public health problem, good awareness, and therefore greater treatment of patients. A cartographic study, on the same province, was able to show that during this year the rural areas were affected by a high rate of incidence (rural municipality of Tazouta and Ahl Sidi Lahcen) [16]. is result corroborates that of the Meknes Province [28] where the incidence varies in time and space; during the same period from 2009 to 2013, the incidence experienced a very marked development, which is justified by unhygienic environmental conditions which increase the risk of leishmaniasis by promoting the multiplication of vectors.
Statistical analysis of this result shows that there is no relationship between the distribution of cases and time (the p value is greater than 0.05).

e Impact of the Urbanization Factor on CL Disease in Sefrou
Province. According to the administrative division, Sefrou Province is made up of 24 communes, divided into 7 urban communes and 17 rural communes (Table 1) [25].
According to the census of CL cases, the disease occurs with high incidence in municipalities more than others. We found 49% of recorded cases of urban origin ( Figure 2) with a maximum incidence at El Menzel commune of 66.28 per 10,000 inhabitants. For rural municipalities, 51% of cases (177 cases) were reported with a maximum  . e analysis of variance revealed a statistically significant difference between the medium numbers of cases from one level of urbanization to another with a confidence rate of 95.0% (df � 1, F � 4.73, p � 0.041) Table 2. Accordingly, there is a significant effect between these two variables with a decision of 4.73%.
According to the literature, urbanization interests all continents and all countries [29].
is factor is closely linked to the massive migration to urban areas specifically in the outskirts of cities where there is a lack of waste management, which increases the reproduction of sandflies. In addition, urban CL of the Old World characterizes the anthroponotic type where transmission is carried out through a female sandfly infected with epidermis from one subject to another. is epidemic character is strictly linked to the density of sandflies and the human population. In addition, according to the World Health Organization [30], the phenomenon of urbanization increases the risk of transmission of leishmaniasis especially within an unimmunized population in rural areas. e lack of planning of cities in rural exodus and poor environmental hygiene conditions [31] increase the leishmaniasis risk and lead to favorable bioecological environments to the development of vectors [32][33][34]. Several studies reveal that urbanization   contributes to the increase in the incidence of ACL type [35,36]. ey also confirmed that the rural areas, where most leishmaniasis patients live, coexist in interresidential homes, or occupy dwellings, allow contact between humans and sandflies and subsequently ensure the circulation of the parasite [27,37].

e Impact of Socioeconomic Factors in Different Municipalities in Sefrou Province on the Distribution of the Incidence of CL Cases 3.3.1. Distribution of the Incidence of CL Cases according to the Population Factor of Sefrou Province.
According to the population census of Sefrou Province [25], the number of inhabitants is 259,254 (Table 3). e distribution of the incidence of CL according to the number of inhabitants of each municipality of Sefrou Province (Figure 3) shows that the municipalities with high incidence rate (Azzaba, Tazouta, El Menzel, and Ahl Sidi Lahcen) have a moderately small number of population.
is distribution of the incidence is not the same at the level of the other communes with low number of population where the incidence rate is low such as commune Ras Tabouda, Bir Tam Tam, and Bhalil. On the other hand, conversely, the commune of Sefrou with its overcrowded situation has been reported to have moderately low incidence (only 13.62 per 10,000 inhabitants) (Figure 3).
According to our result, the majority of municipalities with a high incidence rate are not overcrowded and of rural origin. In addition to the small number of population, the environmental characteristics of these environments make the situation more alarming, which leads to rapid dispersion of cases. Statistical analysis revealed that the distribution of the incidence of CL in this province is not linked to the number of inhabitants by municipality, but to the percentage of cases (Table 4). A positive correlation of 0.474 was confirmed by the normality tests of Kolmogorov-Smirnov (p � 0.003 < to 0.05) and Shapiro-Wilk (p � 0.001 < to 0.05), which reveals that the studied samples follow a normal distribution.
From 2007 to 2011, we observed that the number of cases increased with a peak in 2010. is peak could explain the success of the initiative and the management of the disease by the ministry and various authorities. e objectives of this program aim primarily to raise awareness among the population as well as intensifying mass screening activities in schools and localities at risk, following the recommendations of the response plan. erefore, the mentioned evolution of cases could be explained by the implementation of the strategy for the fight against this disease and the information campaigns conducted by the Ministry of Health according to the national plan for the fight against leishmaniasis, launched in 2009 530000 000000 540000 000000 550000 000000 560000 000000 570000 000000 580000 000000 590000 000000 600000 000000 610000 000000 620000 000000 530000 000000 540000 000000 550000 000000 560000 000000 570000 000000 580000 000000 590000 000000 600000 000000 610000 Interdisciplinary Perspectives on Infectious Diseases (Program of Integrated Management of Vector Control). In addition, the factor of the increasing density of the population and the propagation of favorable milieus to the multiplication of the vector could also have an effect on this situation [38]. Indeed, Old World anthroponotic cutaneous leishmaniasis (ACL) requires a reservoir which is humans [15]. is means that the parasite is transmitted from one subject to another through the bite of a peridomestic sandfly, once the infected subjects arrive to the endemic area. ereby, this can contribute to the extension of its geographical area. We can also explain that the municipalities which have several geographic (proximity to Fez) and economic advantages are highly attractive municipalities. In case of a contamination, overcrowd is directly associated with the high number of CL cases. Figure 4 shows the distribution of the incidence of CL cases according to the poverty rate of different municipalities in Sefrou Province. e    According to the descriptive analysis, it appears that the incidence of CL does not depend on the poverty rate. Indeed, at the level of the communes of Azzaba (76.21 per 10,000 inhabitants) and Tazouta (74.84 per 10,000 inhabitants), where the incidence is very high compared to the other communes, the poverty rate is ordered, respectively, as 20% and 17.5%, whereas at the level of the commune of El Menzel, poverty was only 9.6% despite the high incidence rate of 66.28 per 10,000 inhabitants (Figure 4). e statistical analysis of this result shows that there is no link between the distribution of the incidence of CL cases and the poverty rate at the level of Sefrou Province; this is justified by the p value with the order 0.55 which is greater than the significance level of 5% with a relatively very low correlation coefficient (p > 0.05, r � 0.13) ( Table 5).

Distribution of the Incidence of CL Cases according to the Poverty Factor of Sefrou Province.
According to the literature, socioeconomic factors such as poverty and lack of infrastructure seem to be among the main factors that lead to leishmaniasis [39,40]. In endemic areas, the leishmaniasis risk is strongly linked to the bad hygienic conditions of the environment [3]. Internal migration of the population for difficult economic reasons led to the establishment of peripheral areas of cities, which leads to favorable environments to the rapid spread of vectors. In addition, poverty rate is an indicator that entails bad nutrition, causing population to be more amenable to the pathogen [41]. Another study has shown that poverty can increase the risk of leishmaniasis due to poor hygienic conditions [41]. In our case, we were able to show another result; that is, poverty does not influence the distribution of the incidence of CL cases at the level of Sefrou Province but has an impact on the distribution of CL cases. A study in Quebec coincides with ours and it has been able to show that poverty does not explain the emergence of CL [42]. e same is true in Morocco, especially in Meknes Province, as the poverty rate of municipalities has no influence on the distribution of the epidemic [11].

Conclusion
Various factors can have an effect on the distribution of leishmaniasis.
is work emphasizes the effect of urbanization and socioeconomic risks on the distribution of cases of cutaneous leishmaniasis at the level of Sefrou Province. e use of GIS is an added value to the creation of thematic maps which function as CL risk maps. ese results must be taken into consideration in determining the risk zones for leishmaniasis and their risk factors in order to establish effective control strategies.

Data Availability
No data were used to support this study.

Conflicts of Interest
e authors declare that there are no conflicts of interest regarding the publication of this paper.