J Arthropod-Borne Dis, March 2020, 14(1): 56–67 MR Shirzadi et al.: Impact of Environmental … 56 http://jad.tums.ac.ir Published Online: March 31, 2020 Original Article Impact of Environmental and Climate Factors on Spatial Distribution of Cutaneous Leishmaniasis in Northeastern Iran: Utilizing Remote Sensing Mohammad Reza Shirzadi1; Mohammad Javanbakht2; Hassan Vatandoost3,4; Nahid Jesri5; *Abedin Saghafipour6; Reza Fouladi-Fard7; Alireza Omidi-Oskouei6 1 Communicable Diseases Management Center, Ministry of Health and Medical Education, Tehran, Iran 2 Department of Remote Sensing and GIS, Faculty of Geography, Tehran University, Tehran, Iran 3 Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran 4 Department of Chemical Pollutants and Pesticides, Institute for Environmental Research, Tehran University of Medical Sciences, Tehran, Iran 5 Remote Sensing and GIS Centre, Shahid Beheshti University, Tehran, Iran 6 Department of Public Health, Faculty of Health, Qom University of Medical Sciences, Qom, Iran 7 Research Center for Environmental Pollutants, Qom University of Medical Sciences, Qom, Iran (Received 24 Jun 2018; accepted 10 Jun 2019) Abstract Background: Cutaneous leishmaniasis (CL) is a dermal and parasitic disease.. The aim of this study was to determine the effect of environmental and climate factors on spatial distribution of CL in northeastern Iran by utilizing remote sensing from 20 March 2016 to 19 March 2017. Methods: In this ecological study, the data were divided into two parts: The descriptive data on human CL cases were gathered from Communicable Diseases center of Iran. The remote sensing techniques and satellite imagery data (TRMM, MODIS-Aqua, MODIS-Terra and AMSR-2 with spatial resolution 0.25°, 0.05°, 5600m and 10km) of environ- mental and climate factors were used to determine the spatial pattern changes of cutaneous leishmaniasis incidence. Results: The incidence of CL in North Khorasan, Razavi Khorasan, and South Khorasan was 35.80 per 100,000 people (309/863092), 34.14 per 100,000 people (2197/6,434,501) and 7.67 per 100,000 people (59/768,898), respectively. The incidence of CL had the highest correlation with soil moisture and evapotranspiration. Moreover, the incidence of dis- ease was significantly correlated with Normalized Difference Vegetation Index (NDVI) and air humidity while it had the lowest correlation with rainfall. Furthermore, the CL incidence had an indirect correlation relation with the air tem- perature meaning that with an increase in the temperature, the incidence of disease decreased. Conclusion: As such, the incidence of disease was also higher in the northern regions; most areas of North Khorasan and northern regions of Razavi Khorasan; where the rainfall, vegetation, specific humidity, evapotranspiration, and soil moisture was higher than the southern areas. Keywords: Cutaneous leishmaniasis; Remote sensing; Climate; Iran Introduction Cutaneous leishmaniasis (CL) is considered a dermal and protozoan infectious disease which is caused by some species of Leishmania par- asite (1). The disease is more prevalent in many underdeveloped and developing countries (2). Cutaneous leishmaniasis is classified into two forms in terms of clinical symptoms and epide- miological characteristics: Zoonotic Cutaneous Leishmaniasis (ZCL) or Cutaneous Leishman- iasis due to Leishmania major (CLM) and An- throponotic Cutaneous Leishmaniasis (ACL) or Cutaneous Leishmaniasis due to Leishmania tropica (CLT). The vectors of CL are some spe- cies of female sand flies belonging to the genus Phlebotomus such as Ph. papatasi and Ph. ser- genti. Besides, reservoirs of disease are some wild rodents, domestic dogs and humans in ZCL and ACL, respectively (3). The globally recog- nized foci of the disease are located approximate- ly between 28–42 degrees of north latitude (4). *Corresponding author: Dr Abedin Saghafipour, E-mail: abed.saghafi@yahoo.com http://jad.tums.ac.ir/ mailto:abed.saghafi@yahoo.com J Arthropod-Borne Dis, March 2020, 14(1): 56–67 MR Shirzadi et al.: Impact of Environmental … 57 http://jad.tums.ac.ir Published Online: March 31, 2020 Cutaneous leishmaniasis is an endemic disease in tropical areas of the United States, Africa, the Indian subcontinent, and in the subtropical regions of southwest Asia (5). According to the WHO reports, CL has local transmission in 98 countries and over 350 million people are glob- ally at risk (5, 6). More than 20,000 cases of CL are reported annually in Iran, but the actual cases are estimated to be 4 to 5 times more than that figure (7, 8). Iran's geographic and climatic con- ditions are suitable for the growth of sand flies as vectors of ZCL, and rodents as reservoirs of disease (3, 9). This zoonotic disease is more prevalent in plain regions in central areas of Iran; such as Qom province (10) and in the old texture of the towns (11, 12). Nowadays, ZCL has en- demic foci in 17 provinces of 31 provinces in Iran, such as the three studied provinces (North Khorasan, Khorasan Razavi and South Khora- san) (13-15). Investigating the correlation be- tween climatic factors and incidence of the ar- thropod born diseases as applied epidemiologic studies can help epidemiologists in prevention and disease control, ultimately leading to taking preventive measures in vulnerable areas (16). In this regard, Salmon et al. (2012) studied the cli- mate change and the prevalence of leishmania- sis in Argentina. The findings of this study in- dicated that the prevalence of this disease has increased with nonlinear climate changes (17). Chamaillé et al. (2010) revealed that the disease prevalence is high in two regions; one region with low winter temperatures, 1042mm average annual rainfall and much forest cover and se- cond area with higher temperatures, lower rain- fall and less forest cover. They declared two re- gion groups probably responsible to the envi- ronment factors favored by the two sand fly vec- tors species; Ph. ariasi and Ph. perniciosus re- spectively (18). In addition, Gonzalez et al. stud- ied the relationship between climate change and risk of leishmaniasis in North America. The re- sults of the study showed that climate changes and increase in temperature provide a natural en- vironment and suitable breeding places for living vectors of this disease (19). In 2012, Tommy et al. conducted a standard multiple regression study to investigate the effect of climate factors on ZCL incidence in central Tanzania and showed that in case of rising rainfall as 1mm and a 1% increase in humidity from July to September, lead to an increase in incidence of the disease (20). Ghatee et al. in a study on role of envi- ronmental and climatic risk factors on the oc- currence of cutaneous leishmaniasis, found that some environmental and climatic factors includ- ing land cover, slope, elevation, close proximity to cattle sheds, rainfall, and temperature were the most effective factors (21). In addition, the Iranian medical entomologists also have studied on impact of environmental and climate factors on spatial distribution of CL using remote sens- ing (22, 23). Following the launch of the first meteorological satellites in the 1960s, and Land- sat-1 in 1972, the use of remote sensing in hu- man health studies have increased for more than four decades. The information received from satellites and their various sensors with the abil- ity to separate temporal and spatial distribution of data has created a new field in the scientific researches on human health. Several ecological indicators have been used in remote sensing re- lated to vector borne diseases, including Nor- malized Difference Vegetation Index (NDVI), near surface air and sea temperatures, soil mois- ture and cold cloudy periods. The term ‘remote sensing’ (RS) is a technique for diagnosis of ob- jects from afar (24). So, this study aimed for determining the impact of environmental and climatic factors on spatial distribution of CL in Northeastern Iran from March 2016 to March 2017 utilizing remote sensing. Materials and Methods Study area One of the main and confirmed foci of CL in Iran is the northeastern areas of the country (8). Therefore, the three provinces of North Khora- san (55°53′–58°20′ E and, 36° 37′-38°17′ N), Razavi Khorasan (35° 60' N–59° 15' E and, 36° 35' N–60° 25' E) and South Khorasan (57° 46´– http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 56–67 MR Shirzadi et al.: Impact of Environmental … 58 http://jad.tums.ac.ir Published Online: March 31, 2020 60° 57´ E and 30° 35 -́34° 14´ N) were selected as the study area of this research (Fig. 1). Ac- cording to the general census of population and housing in 2017, the totally residents in the study area was 8,066,491 people (North Khorasan, Razavi Khorasan and South Khorasan prov- inces had a population of 863092, 6434501 and 768898, respectively). These three provinces have an area of 28311, 118854, and 148669km2, re- spectively (North Khorasan, Razavi Khorasan and South Khorasan provinces). Study design The data used in this study included two parts: the field data related to the incidence of disease and remote sensing data in a one-year period (from 20 March 2016 to 19 March 2017). Estimation of various climatic components in large spatial scales has always been a frequent problem due to lack of availability of appropri- ate data. In recent years, a global database based on satellite estimates has reduced these prob- lems. In this research, various products of the Modus sensor and the Global Land Data As- similation System (GLDAS) were used. The GLDAS aims to produce hydrological and me- teorological parameters using the combination of ground-level models and satellite imagery with the aim of studying the changes in the en- ergy and water bill on the ground. Satellite im- agery data (TRMM, MODIS–Aqua, MODIS– Terra and AMSR-2 with spatial resolution 0.25°, 0.05°, 5600m and 10km) of environmental and climate factors were used to determine the spa- tial pattern changes of cutaneous leishmaniasis incidence. This system was developed jointly by the National Aeronautics and Space Admin- istration (NASA), the Goddard Space Flight Center (GSFC), the National Oceanic and At- mospheric Administration (NOAA), and the National Centers for Environmental Prediction (NCEP) (25). The parameters extracted from GLDAS included evapotranspiration, near sur- face temperature, rainfall, soil moisture and air humidity (Table 1). The GLDAS data has been used and evaluated in many scientific studies (26-28). Furthermore, the Normalized Differ- ence Vegetation Index (NDVI) and Modis da- ta were used in order to study variations in veg- etation. In addition, mean of climatic and envi- ronmental variables and cutaneous leishmania- sis incidence was evaluated (Table 2). Field data on CL disease is routinely collected from urban and rural health centers in these three provinces using standard epidemiological forms and re- ported to the Center for Disease Control and Prevention of the Ministry of Health and Med- ical Education of Iran. In order to investigate the spatial changes of the disease incidence, as well as the relationship between climatic and environmental factors and the incidence of CL, one-year data of this disease were taken from the CDC. Statistical analysis The data related to CL disease were entered into Excel software and the disease incidence was calculated. Also, Pearson correlation coef- ficient was used to determine the relationship between climatic and environmental factors and CL. The correlation coefficient is a value be- tween -1.0 and 1.0, positive correlation implies the presence of a direct relationship between two variables in which, when one variable increas- es as the other increases. As well as, negative correlation means there is a reverse change be- tween the two variables. The zero correlation, however, means that the variables are inde- pendent of each other. Correlation is significant at the 0.05 level. Results The incidence of CL in all three provinces was 25.66 per 100,000 people (2565/8,066,491). Also, CL incidence in North Khorasan, Ra- zavi Khorasan, and South Khorasan was 35.80 per 100,000 people (309/863092), 34.14 per 100,000 people (2197/6,434,501) and 7.67 per 100,000 people (59/768,898), respectively (Table 2 and Fig. 2). Spatial distribution of CL showed that the northern regions had a higher incidence than the southern ones. Therefore, the http://jad.tums.ac.ir/ https://www.google.com/url?sa=t&rct=j&q=&esrc=s&source=web&cd=1&cad=rja&uact=8&ved=0ahUKEwjN_8jP49nXAhWEbVAKHe7xAgUQFggkMAA&url=https%3A%2F%2Fwww.cdc.gov%2F&usg=AOvVaw347QtT6pi6CdNKfM8VFdw6 https://www.google.com/url?sa=t&rct=j&q=&esrc=s&source=web&cd=1&cad=rja&uact=8&ved=0ahUKEwjN_8jP49nXAhWEbVAKHe7xAgUQFggkMAA&url=https%3A%2F%2Fwww.cdc.gov%2F&usg=AOvVaw347QtT6pi6CdNKfM8VFdw6 J Arthropod-Borne Dis, March 2020, 14(1): 56–67 MR Shirzadi et al.: Impact of Environmental … 59 http://jad.tums.ac.ir Published Online: March 31, 2020 disease had a north to south trend which tend- ed to increase from south to the north. In terms of changes in the three provinces, the southern regions of North Khorasan and northern regions of Razavi Khorasan prov- inces had a high incidence. The southern re- gions of Razavi Khorasan Province and the whole region of South Khorasan had a lower incidence. Table 2 shows the mean of six cli- matic and environmental variables (rainfall, temperature, vegetation, specific humidity, evapotranspiration and soil moisture) in north- eastern provinces of Iran. The relationship be- tween climatic and environmental factors and incidence of CL was evaluated. Rain precipitation rate (mm) The results showed that the mean annual pre- cipitation in these three provinces was 15.08mm. The rate of change in average rainfall across these provinces showed a downward trend at a rate of 21.13 to 15.75 and 8.38mm in North Khorasan, Razavi Khorasan and South Khora- san, respectively (Table 2). The average annual rainfall in southern regions; all areas of South Khorasan, central and southern areas of Razavi Khorasan was lower than that in northern re- gions; most areas of North Khorasan and north- ern areas of Razavi Khorasan. So that North Khorasan Province had the highest rainfall dur- ing the year. The Razavi Khorasan Province al- so had different conditions; the northern areas of the province had specifically good rainfall, and the southern and western parts had a low- er rainfall than the northern parts. Furthermore, South Khorasan Province had a low rate of rainfall in most regions (Fig. 3a). There was a significant correlation between the incidence of CL and the precipitation mean (p= 0.046). According to the figures 2 and 3, it was also observed that the maximum precipitation areas were matched with the maximum incidence of the disease. Land surface temperature (ºC) The average temperature in all of these prov- inces was 35.9 °C. It was 42.67, 34.96 and 30.07° for the three provinces of South Khorasan, Ra- zavi Khorasan, North Khorasan and respective- ly. In this study, the trend of temperature de- creased from south to north areas. In terms of temperature conditions in the three studied prov- inces, North Khorasan Province had a lower av- erage temperature. The northern and northeast- ern parts of the Razavi Khorasan Province had lower temperatures than those in the southern and eastern parts of the province. South Khora- san Province residents had also experienced a different temperature in one year, and its south- ern and western parts had a higher temperature than the eastern and northern regions of the prov- ince (Fig. 3b). There was a correlation between incidence of CL and air temperature. It was ob- served that the incidence of disease had de- creased in southern regions with high temper- atures. Normalized Difference Vegetation Index (NDVI) Spatial variations in vegetation revealed that the northern regions; most areas of North Khora- san and northern regions of Razavi Khorasan had a better status than the southern regions (Fig. 3c). The NDVI was 0.11 in all studied provinces, while it was 0.8, 0.12 and 0.15 in South Khora- san, Razavi Khorasan and North Khorasan, re- spectively. The southern and western regions of Razavi Khorasan and all regions of South Khorasan Province had less vegetation. Sta- tistical analysis showed that there was a direct correlation between the trend of vegetation changes and the incidence of disease. Specific humidity (SH %) Spatial variations of specific humidity during this course indicated that the air humidity was low in most regions (Table 2). The highest SH was observed in northwest of North Khorasan Province. The northern parts of Razavi Khora- san Province had higher humidity. In the South Khorasan Province, the southwest areas were less humid (Fig. 3d). In total, the maximum mois- ture content was consistent with areas having the maximum incidence of disease. http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 56–67 MR Shirzadi et al.: Impact of Environmental … 60 http://jad.tums.ac.ir Published Online: March 31, 2020 Evapotranspiration (kg/ m2 -y) In this study, evapotranspiration had a north- west-southeast trend, showing a decreasing trend from northwest to south east (Table 2). The evapotranspiration of the North Khorasan Prov- ince was more than that of the other two prov- inces. In the province of Razavi Khorasan, the northern and eastern regions of the province had higher evapotranspiration than the southern and western regions. The spatial variations of evap- otranspiration in South Khorasan Province showed a low level of this index with most of the regions having low evapotranspiration (Fig. 3e). The comparison of evapotranspiration and spatial changes in the incidence of the disease showed that evapotranspiration was also an ef- fective factor in the incidence of this disease. Soil moisture (%) The spatial variation of soil moisture suggest- ed that the northern regions (most areas of North Khorasan and northern regions of Razavi Khora- san) had better conditions than the southern re- gions (Table 2). Soil moisture was specifically high in most parts of North Khorasan Province. In Razavi Khorasan Province, the northern and southern regions had higher rates of soil mois- ture than in the central regions of the province. Moreover, the soil moisture content reached the lowest level in southern Khorasan Province (Fig. 3f). There was also a significantly direct corre- lation between spatial variation of soil moisture and disease incidence (p= 0.007). Pearson Correlation Coefficient was used to study the relationship between every environ- mental and climatic factors and the incidence of the disease. Table 3 shows the Pearson corre- lation coefficient indices with the incidence of CL. Table 1. The characteristics of parameters extracted from GLDAS in this study Index Source Unit Spatial Resolution Precipitation rate TRMM mm 0.25° Land Surface Temperature MODIS - Aqua C 0.05° Normalized Difference Vegetation Index MODIS - Terra NDVI 5600m Specific humidity GLADS Model Kg kg-1 0.25° Evapotranspiration GLADS Model Kg m-2 s-1 0.25° Soil Moisture AMSR-2 % 10km Fig. 1. Location of the study area, northeastern Iran http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 56–67 MR Shirzadi et al.: Impact of Environmental … 61 http://jad.tums.ac.ir Published Online: March 31, 2020 Table 2. Mean of climatic and environmental variables and cutaneous leishmaniasis incidence in northeastern prov- inces of Iran from March 2016 to March 2017 Index North Khorasan Razavi Khorasan South Khorasan Total Precipitation rate (mm) 21.13 15.75 8.38 15.08 Land surface temperature (c º ) 30.07 34.96 42.67 35.9 Normalized Difference Vegetation Index (NDVI) 0.15 0.12 0.08 0.11 Specific humidity (Kg kg-1) x1e-3 4.64 4.12 3.73 4.16 Evapotranspiration (kg/ m2 -y) x1e-7 70.0 60.01 43.21 57.74 Soil moisture (%) 23.51 14.65 5.01 14.36 CL incidence/100,000 35.80 34.14 7.67 25.66 CL cases 309 2197 59 2565 Table 3. Pearson correlation coefficient indices with the incidence of Cutaneous leishmaniasis in northeastern Iran Index Correlation coefficient p- value Precipitation rate 0.239 0.046 Land surface temperature -0.322 0.028 Normalized Difference Vegeta- tion Index 0.314 0.032 Specific humidity 0.303 0.038 Evapotranspiration 0.465 0.001 Soil moisture 0.392 0.007 Fig. 2. Spatial distribution of cutaneous leishmaniasis in northeastern Iran http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 56–67 MR Shirzadi et al.: Impact of Environmental … 62 http://jad.tums.ac.ir Published Online: March 31, 2020 Fig. 3. Time averaged map of monthly rate of all environmental and climate factors in northeastern Iran Discussion The incidence of CL in North Khorasan, Ra- zavi Khorasan, and South Khorasan was 35.80, 34.14 and 7.67 per 100,000 people, respective- ly. The epidemiological studies on CL disease in Iran indicated that the majority of cases were reported in eastern, central, and southern prov- inces in the country (29). In addition, the inci- dence of CL in Iran were evaluated 27.5 per 100, 000 populations in 2011 (30). So, we can conclude that the CL incidence in two provinces out of 3 studied provinces; North Khorasan, Ra- zavi Khorasan was higher than the average in- cidence of the country. In the present study, the incidence of CL was highly correlated with soil moisture and evapotranspiration. In addition, there was a moderately positive relationship be- tween vegetation and humidity index with the incidence of the disease. Besides, the incidence of the disease had the lowest correlation with precipitation. In addition, there was also a sig- nificantly positive relationship between CL in- cidence and land surface temperature, so that the incidence of the disease decreased with the increasing temperature. In this study, there was a weak significant positive correlation between the incidence of CL and the mean of precipi- tation. It was also observed that the maximum precipitation areas were matched with the max- imum incidence of the disease. In contrast, Ente- zari and Eskandari have been found that there was an inverse correlation between climatic pa- rameters of rainfall and specific humidity with CL prevalence in Fars Province, southern Iran (31). It has already been proven that as rainfall http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 56–67 MR Shirzadi et al.: Impact of Environmental … 63 http://jad.tums.ac.ir Published Online: March 31, 2020 increases at the right level, it can usually ad- just air temperature and increases humidity. But, flood-causing rainfalls destroy the breeding plac- es of sand flies in addition to reducing their pop- ulations, leading consequently to a decrease in the incidence of the disease (32, 33). For ex- ample, the Ph. argentipes larvae, when exposed to monsoon floods in northern India, ascends the mud walls, and descend after the deposi- tion of water and the normalization of the con- ditions, but in other species, these floods lead to the death of the sand flies (34). In a study in French Guyana, it was observed that the pre- cipitation had a weak relationship with the CL incidence (35). In another study in Brazil, a di- rect correlation was found between incidence of disease and precipitation (36). In the present study, there was an inverse correlation between CL incidence and land surface temperature. It has been observed that the incidence of disease has decreased in southern regions with high tem- peratures. This finding is in contrast with the basic concepts about the disease. It had been previously proved that the growth of all spe- cies of sand flies occur at temperatures above 18 °C, which is the threshold temperature for their life (37). In general, the findings of vari- ous researchers show that the optimum tempera- ture for the development of their life stages be- fore maturation of sand flies is in range of 18– 28 °C (37). In an ecological study on phlebotom- ine sand flies in the Greek Aegean Islands showed that temperature preferences of them were 21–29 °C (38). It seems in addition to tem- perature, other environmental and climatic fac- tors are associated to the disease. In addition, adult sand flies activate during sunset and night when the land surface temperature is balanced and humidity rises. In this condition, the infected female phlebotomine sandflies can cause the transmission of Leishmania parasites into sus- ceptible hosts such as humans (39). In the pre- sent study, spatial distribution of vegetation re- vealed that the northern regions; most areas of North Khorasan and northern regions of Ra- zavi Khorasan had a better situation than the southern ones. Statistical analysis based on the NDVI showed that there is a direct correlation between vegetation changes and the incidence of disease. Contrary to the results of the pre- sent study, Mozafari et al. in a study comparing spatial distribution of disease cases with veg- etation status in Ardakan, central Iran, found that CL is more prevalent in areas with less veg- etation (40). Such differences in the results of various studies can indicate the impact of dif- ferent geographic locations on the CL incidence. Sometimes the effects of the same climatic pa- rameters will vary from one region to another. Vegetation is a function of temperature and hu- midity. The vegetation cover status and the CL incidence are affected by climatic factors (41). Vegetation can be increased under the influence of higher precipitation and lower temperatures. The situation also holds true about CL incidence. In addition, the incidence of CL disease also de- pends on sand flies’ density (3). Therefore, CL is indirectly affected by climatic factors. The incidence of the disease depends on a variety of factors in addition to the population of sand flies. For example, the change in population and the density of the disease reservoirs (rodents) can affect the incidence of disease (42). At the time of drought, the population of wild rodents approaching human settlements may increase. This situation, in turn, can lead to an increase in the population of rodents infected with Leish- mania parasite. So, the probability of blood- sucking of sand flies from these rodents rises as well as biting on humans and inoculation of the Leishmania parasite to humans (43, 44). Therefore, a vegetation index at a low level may ultimately lead to an increase in disease as well. The average specific humidity in the study area was 32.22%. The highest humidity was observed in North Khorasan and northern regions of Ra- zavi Khorasan. In general, areas with maximum moisture content were consistent with areas with the highest incidence of disease. The specific hu- midity is favorable for egg hatching, being be- tween 80–90% (45). Hesam-Mohammadi et al. also found that a specific humidity of 24.83– http://jad.tums.ac.ir/ https://www.ncbi.nlm.nih.gov/pubmed/?term=Hesam-Mohammadi%20M%5BAuthor%5D&cauthor=true&cauthor_uid=26114129 J Arthropod-Borne Dis, March 2020, 14(1): 56–67 MR Shirzadi et al.: Impact of Environmental … 64 http://jad.tums.ac.ir Published Online: March 31, 2020 36.33% was desirable for sand flies collected from Kashan district, Central Iran (46). Hence, in the present study area, climatic conditions are favorable for the activity of sand flies in terms of humidity, their biting habit on hosts such as humans and the transmission of CL disease. Alt- hough specific humidity is required in breed- ing places of sand flies, high moisture can make larvae migrate to other places (37). Mozafari et al. analyzed the role of biochemical factors (cli- matic factors affecting the life of living crea- tures) and the outbreak of CL in the Yazd-Ar- dakan plain, central Iran, using data from me- teorological data during the statistical period of 1997–2009. Their research showed that maxi- mum disease incidence occurs in the second half of the year, especially in autumn, and there is al- so a weak positive correlation between spe- cific humidity and incidence of the disease (40). In the present study, evapotranspiration has a northwest-southeast trend which de- creases from northwest to south east of all study areas. The comparison of evapotranspi- ration index with spatial distribution of dis- ease confirmed that evapotranspiration is also an important factor in CL incidence. Water movement in river beds can have an effective role in increasing evapotranspiration and con- sequently in increasing specific humidity, ul- timately leading to temperature modification. As such, North Khorasan with large rivers and streams characterized by sufficient evapotran- spiration, has provided suitable breeding places for the activities of sand flies as vectors of the disease. Previous studies have also proved the presence of infected female P. papatasi species with Leishmania major parasite in endemic ar- eas of North Khorasan Province (13). Spatial changes in the soil moisture indicate that the northern regions have more favorable condi- tions than the southern ones. In South Khora- san Province, the rate of soil moisture was al- so the lowest, which associated to the areas with the lowest incidence of the disease. Research- ers believe that rotten plants in the soil are the main source of food for sand flies larvae in na- ture since larvae cannot survive without water and moisture. The findings of the current study support the previous studies evaluating the ef- fect of soil moisture on the trend of the disease. In a study on the mapping of vulnerable areas of Kala-Azar disease using RS and GIS in parts of the Bihar Province of India, it was found that ponds, streams, irrigation canals, and rivers are directly interrelated and also very effective in maintaining soil moisture and subsoil levels with an average of 65–80% for the growth of larva and adult sand flies (47). Conclusion According to the findings, the incidence of disease was also higher in the northern regions; most areas of North Khorasan and northern re- gions of Razavi Khorasan; where the rainfall, vegetation, specific humidity, evapotranspiration, and soil moisture was higher than the southern studied areas. Acknowledgements The authors are grateful to the research dep- uty of Razavi Khorasan University of Medical Science. Ethical clearance was earned from the Institutional Ethics Committee of Razavi Khora- san University of Medical Sciences (KHRU. REC.1395.112). The authors declare that there is no conflict of interest. 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