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Assessing epidemiology of cutaneous leishmaniasis in Isfahan, Iran.

INTRODUCTION

Leishmaniasis, a major global health and economic issue, comprises a group of diseases caused by the protozoan parasites of the genus Leishmania. Transmission of leishmaniasis to mammals, including humans, requires the bite of female phlebotomine sandflies (1-3). Rodents serve as animal reservoir hosts of this disease and infected Rhombomys opimus, Meriones libycus and M. nesokia have been found in Isfahan Province (Iran) (4).

Clinical and epidemiological features of leishmaniasis vary depending upon the interactive impact of different factors such as parasites, hosts, vectors and the involved environment. Among three clinical forms (cutaneous, visceral, and mucocutaneous) of the disease, cutaneous leishmaniasis has the highest prevalence in the Middle East (2, 5). Despite remarkable advancements in disease control, leishmaniasis is still a major health concern. The World Health Organization (WHO) has, in fact, introduced leishmaniasis as the sixth most important disease in tropical and subtropical areas (6).

Two parasite species, i.e. Leishmania major and L. tropica, are responsible for most of the cases of CL. Urban (dry) CL is caused by L. tropica and has been reported in cities of Tehran, Shiraz, Mashhad, Nishabur, Kerman, Bam, Rafsanjan and Khomeyni Shahr (Iran) (7, 8). Rural (wet) CL, caused by L. major, has been found in vast areas of Iran including Isfahan, Sarakhs, Lotfabad, Khuzestan, Kashmar, Kashan, Damghan and Dehloran (9).

Although about 20,000 cases of the disease are annually reported from different areas of Iran, the actual rate has been estimated to be five times higher (10,11). The prevalence of leishmaniasis in different provinces of Iran ranges from 1.8 to 37.9%6. As the disease keeps appearing at new sites around the country, wide national and international investments and efforts have failed to eradicate it in Iran. Since unsuccessful health and social activities to control leishmaniasis have resulted in irreparable economic, social, and psychological damages, the cutaneous leishmaniasis control program in Iran has sought to identify the epidemiological characteristics of the disease at various sites (12-16).

Isfahan Province, located in the center of Iran on green plains of Zayandeh Rud River, has a high prevalence of CL. The present study aimed to review the epidemiology of this disease in the city of Isfahan (the capital of Isfahan Province).

MATERIAL & METHODS

This descriptive, analytical, cross-sectional study assessed all individuals (n = 1733) who referred to the Dermatology and Cutaneous Leishmaniasis Research Center (Isfahan, Iran) due to suspected CL during 2007-08. Overall, 1315 patients (75.9%) had positive leishmanin skin tests. After being examined by a physician in the health center, the patients provided informed consents and completed a special questionnaire including age, sex, occupation, lesion type, month and season of incidence, presumptive diagnosis, and type and duration of drug consumption. The lesion sites were then biopsied to confirm the diagnosis of leishmaniasis. Following fixation in methanol for 20-30 sec, the samples were stained with Giemsa (20-30 min). If Leishmania amastigotes were observed under the microscope, cutaneous leishmaniasis was confirmed and the patient's completed questionnaire was evaluated.

Finally, the collected data were analyzed using descriptive statistics and chi-square test in SPSS for Windows version 16.0 (SPSS Inc., Chicago, IL, USA). P-values < 0.05 were considered significant.

RESULTS

As indicated in Table 1, the prevalence of CL was assessed in northern, southern, eastern, western, and central Isfahan. While the northern area of the city had the highest number of infected individuals (n=800; 60.9%), the lowest rate was observed in southern areas (n=21; 1.6%). Out of 1315 people with leishmaniasis skin lesions, 812 (61.8%) were males, and 503 (38.2%) were females. Chi-square test showed a significant difference between the prevalence of the disease in men and women (p <0.01). The highest frequency (32.1%) of patients with cutaneous leishmaniasis was detected in 21-30 yr-old subjects. However, the disease was found to infect all the age groups (Table 2). The disease had the highest and lowest frequency among 21-30 and >59 yr-old individuals, respectively. Furthermore, >50% of samples with positive leishmanin test belonged to the individuals younger than 30 are of the most active group of the population due to their occupation, education, and activity.

Table 3 summarizes sites of lesions in different months and seasons of the year. As seen, most lesions occur in upper extremities (34.3%) and during fall (52.5%). Moreover, the majority of patients was Iranian (81.2%) and infected in fall (51.7%).

As Table 4 shows, the majority of patients (54%) had more than one lesion on their bodies. Moreover, the highest prevalence of multiple lesions was observed in fall (52.6%). Table 5 shows the prevalence of the usual (classic) and ususual clinical forms of cutaneous leishmaniasis among the patents in the city of Isfahan. As Table 6 shows, among various occupation, cutaneous leishmaniasis had the highest prevalence in students (18%). Finally, the most common treatment was intramuscular meglumine antimoniate (Glucantime) (24.5%) (Table 7).

DISCUSSION

Cutaneous leishmaniasis is seen in most provinces of Iran. It is an important health problem around the world particularly in Mediterranean and African countries and the Middle East. The spread of cutaneous leishmaniasis from endemic to non-endemic regions of Iran (due to environmental factors such as irregular immigration, demographic changes, development of agriculture, and water providing projects) and the consequent increase in the prevalence of the disease have imposed a considerable economic and health burden on the society (17, 18).

Almost all the cases of cutaneous leishmaniasis (90%) occur in only seven countries, i.e. Iran, Afghanistan, Algeria, Brazil, Peru, Syria, and Saudi Arabia (19). Iran not only has a high prevalence of the disease, but it is also a neighbor of Afghanistan and has close relationships and great deals of trading with Syria and Saudi Arabia. Apparently, such challenges increase the importance of the disease.

Numerous studies in different parts of the world have evaluated various aspects of cutaneous leishmaniasis. They have assessed epidemiological aspects of the disease by considering descriptive indices such as age, sex, occupation, and nationality (20). The present cross-sectional study tried to analyze the available statistics and demographic information to identify the relation of cutaneous leishmaniasis with epidemiological factors using 1315 patients during one year. We found most patients to be male. In a study in Shiraz and Qom (two cities in Iran) in 2008, 59.3% of the patients were male (21). Similarly, a study from Pakistan reported 56.6% of the patients with cutaneous leishmaniasis to be male (22). The very higher incidence of this disease in men compared to women can be justified by men comprising the majority of seasonal immigrants as work labor, working in open environments (farms and firms), wearing fewer parts of clothing than women, travelling more in deserts and wastelands, and having probably more contact with sandflies during evening and night. Enhancing the knowledge of seasonal workers who have to commute to endemic regions can reduce the contact rate with sandflies (15).

Most patients in the present study resided in the northern part of Isfahan. Borkhar (a city in the north of Isfahan) was the main disease site as it has suitable conditions for living and reproduction of disease reservoir. On the other hand, establishment of new residential and military zones and entrance of non-indigenous people have increased the prevalence of the disease and turned the city into a hyperendemic region. Natanz is another highly infected area in the north of Isfahan due to its active mice colonies. On the other hand, Agha-Ali-Abbas pantheon, which is located near Natanz, attracts many non-indigenous and sensitive pilgrims. These people can be easily infected during their visit since abundant haloxylon trees provide a great habitat for mice colonies. Previous studies have identified R. opimus and M. libycus in rodents of Natanz. Furthermore, mice infected with R. opimus and M. nesokia have been hunted in northern areas of Isfahan (13).

Four species of sandflies (Phlebotomus ansari, P. sergenti, P. caucasicus, and P. papatasi) have been recognized in human habitats of the five regions of Isfahan Province. Therefore, both urban and rural types of CL can occur in five regions of Isfahan. In addition, the activity of rodents (with R. opimus) in Isfahan reaches its peak during August-December (13, 17).

According to our findings, frequency of cutaneous leishmaniasis was significantly related with age. In general, adults who live near disease sites and work in endemic areas are at higher risk of infection (8).

While a study reported 51.1% of patients to the age 6-15 yr-old (23), another research found the highest prevalence among 16-50 yr old individuals (24). It can hence be concluded that rates of infection in different age groups depend upon the study location. In regions such as Isfahan with abundant reservoirs and vectors, people's high contact rate with them, and great number of natives, 5-6 yr old children are the most infected group (13, 17). Since 90% of the cases develop life-time immunity against the disease, it is very rare in adults and old people. However, in other parts of the country where the number of local people is low or the population is frequently altered, the disease can be seen in all age groups (25). The lesion site depends on many factors including the type of sandfly, social and cultural behavior of people, and climate. Most lesions in

the present study were in the upper extremities and face. It is clear that the body areas which are not covered are more exposed to bites of sandflies. Other studies in various parts of Iran have also suggested most lesions to occur in upper extremities, face, head, neck, and hands (26, 27.) Similar to previous research (17, 28), multiple lesions were more frequent than single lesions in our study. Multiple lesions can result from receiving infected bites at different times or insemination following scratching. They can also be found along lymphatic vessels or in people with underlying diseases such as acquired immune deficiency syndrome (AIDS), renal problems, and diabetes which attenuated the immune system (17). Rafati et al (21), Abbasi et al (29), and Hamzavi et al (30) found >60% of the patients to have more than one lesion on their bodies. Effects of CL on beauty and general and mental health of the patients necessitate more efficient measures to control and prevent the disease.

According to Table 8, the highest incidence of CL was observed in fall followed by summer. This finding can be justified considering the biology of vector sandflies, the main vectors in the studied area. Basically, CL in humans follows a seasonal pattern in regions where adult sandflies' growth is seasonal. In areas where adult sandflies develop in spring and early summer, new cases of CL usually appear at the end of summer or in fall (31). In contrast to our findings, a study in Pakistan (32) reported most cases of the disease in winter. Infections were found to depend on type of CL, prevalence of the vector, and disease reservoirs.

The majority of patients in this study were Iranian (82.2%). Although the incidence of first-time disease was the highest in fall, patients with a history of the disease had new lesions mostly in summer. Moreover, in our participants, classic forms of CL were more prevalent than non-classic forms. According to El-on et al (33), in Israel, secondary bacterial infections can be effective on both clinical forms of the disease and size of the cutaneous lesions.

In the current study, among various occupations, the highest prevalence of CL was detected in school and university students. Considering that Isfahan has a semi-arid and temperate climate, people spend hot summer nights outdoors and can thus be bitten by sandflies. On the other hand, most students aged 7-30 yr old and have not been infected by the disease; they comprise a high percentage of patients. However, Doroodgar et al (34) reported that CL had the highest prevalence among housewives in Kashan.

Intralesional glucantime, intramuscular glucantime, and simultaneous use of intramuscular and intralesional glucantime were the most common treatment modalities in all the age groups. However, since most patients had more than one lesion or had lesions on a sensitive part of their body (e.g. eyes, inside ears, nose, lips, and genitals) intramuscular glucantime was the most widely used treatment. A 20-day period of intramuscular glucantime (Specia, France) injections (20 mg/kg/day) seems to be the best method to treat CL in Iran and especially in Isfahan. The reasons include expansion of CL35, identifying different species of Leishmania due to the exclusive effect of fluconazole, itraconazole, and ketoconazole on L. major (22), lack of knowledge on the therapeutic effect of pentamidine (36, 37), and the recurrence of disease after treating with allopurinol (38, 39). Nevertheless, patients are recommended to be examined for the presence of cardiac, renal, hepatic and blood diseases before treating with glucantime.

CONCLUSION

According to our findings, the City of Isfahan is an important area with high CL infection rate in Isfahan Province and even in Iran. Although the number of recorded

cases of CL was 1315 in one year, the actual number can be much higher. This issue undoubtedly requires more accurate and comprehensive research. We also found gender, age, nationality, place of residence, and occupation to play major roles in the occurrence of the disease. Moreover, the disease was found to possess a seasonal pattern of incidence. More time and efforts have thus to be paid for increasing public awareness about transmission ways, prevention, and complications of infectious diseases, especially CL. Such efforts should be performed with more interaction between university hospitals and health centers in endemic and hyperendemic provinces. The importance of mass media and mass communication at the right time cannot be neglected in this regard.

ACKNOWLEDGEMENTS

The researchers would like to thank Dermatology and Cutaneous Leishmaniasis Research Center, Isfahan, Iran and its president, Dr Mohammad Ali Nilforoushzadeh. We are also grateful to the esteemed staff of the mentioned center, particularly Ms Leila Shirani Bidabadi (engineer and researcher), for their cooperation and advices.

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Correspondence to: Dr Monir Doudi, Department of Microbiology, Falavarjan Branch, Islamic Azad University, Falavarjan, Isfahan, Iran. E-mail: Monirdoudi@yahoo.com; Doudi@iaufala.ac.ir

Received: 27 September 2012 Accepted in revised form: 2 February 2013

Marziyeh Karami [1], Monir Doudi [2] & Mahbubeh Setorki [3]

[1] Young Researchers Club, Falavarjan Branch; [2] Department of Microbiology, Falavarjan Branch, Islamic Azad University, Falavarjan, Isfahan, Iran; [3] Department of Biology, Izeh Branch, Islamic Azad University, Izeh, Iran
Table 1. Frequency distribution of people with cutaneous leishmaniasis
(CL) based on their place of residence in Isfahan, Iran, during 2007-08

Location                Place of living

North      Zeynabieh, Borkhar, Meymeh, Shahin Shahr, Malek Shahr,
           Dolat Abad, Habib Abad, Khorzough, Dastjerd, Agha Ali
           Abbas, Narmi Emamzadeh, Gorgab, Natanz and Badrud
South      Sepahan Shahr, Baharestan, Mobarakeh, Shahreza, Zarrin
           Shahr, Dehaghan, Semirom and Margh-o-Mayar
East       Haftshouyeh, Jarghouyeh, Ziar, Khorasgan, North Bara'an,
           Ghahjaverestan, Mohammad Abad, Eshkavand, Gavart,
           Jolgeh, Ejieh, Varzaneh, Nuclear Plant and Shahid Beheshti
           Airport
West       Lenjan, Khomeini Shahr, Najaf Abad, Koushk, Falavarjan,
           Pirbakran, Zob Ahan Highway, Goldasht, Dorche, Jouzdan,
           Asghar Abad and Kahrizsang
Center     Areas around Kaveh Terminal, Sofeh Terminal, Zayanderoud
           Terminal, Jey Terminal, Imam Square, Imam Ali Square,
           Hetef, Neshat

Location   Population      People with CL n (%)   Total percentage

North      992             800 (60.9)             57.2

South      28              21 (1.6)               1.6

East       383             260 (19.8)             22.1

West       210             170 (12.9)             12.1

Center     120             64 (4.8)               6.9

Table 2. Frequency of cutaneous leishmaniasis in different age
groups of patients in Isfahan, Iran, during 2007-08

Age (yr)

< 10                  266 (20.2)
11-20                 235 (17.9)
21-30                 422 (32.1)
31-40                 149 (11.3)
41-50                 154 (11.7)
>50                   89 (6.8)

Total                 1315 (100)

Table 3. Frequency distribution of patients with cutaneous leishmaniasis
stratified based on months and seasons of occurrence and lesion site
(Isfahan, Iran, 2007-08)

Season    Month
                      Head and face (*)  Upper extremities (**)
                      n (%)              n (%)

Spring    April           5 (14.7)             14 (41.2)
          May            17 (29.3)             18 (31.1)
          June            8 (17.1)             18 (38.3)
Total                    30 (21.6)              50 (36)
Summer    July            8 (24.2)             10 (30.3)
          August         17 (18.7)             31 (34.1)
          September       33 (20)              59 (35.8)
Total                    58 (20.3)             100 (35)
Fall      October        25 (10.7)             90 (38.6)
          November       35 (13.5)             89 (34.4)
          December       26 (13.8)             59 (31.4)
Total                    86 (12.5)            238 (34.5)
Winter    January        17 (15.5)              32 (29)
          February        6 (14.3)             19 (45.2)
          March            9 (20)              19 (42.2)
Total                     32 (2.8)             70 (45.5)
Grand total (12 months   206 (15.8)           458 (34.4)

Season    Month       Lesion sites
                      Lower extremities ([dagger])
                      n (%)

Spring    April                 9 (26.5)
          May                   15 (25.9)
          June                  15 (31.9)
Total                           39 (28.1)
Summer    July                  10 (30.3)
          August                25 (27.5)
          September              28 (17)
Total                           63 (22.1)
Fall      October               31 (13.3)
          November               57 (22)
          December              48 (25.5)
Total                           136 (20)
Winter    January                33 (30)
          February              9 (21.4)
          March                 10 (22.2)
Total                           52 (33.8)

Grand total (12 months         290 (22.2)

Season    Month
                      More than one organ   Total
                      n (%)                 number

Spring    April            6 (17.6)          34 (100)

         May              8 (13.8)          58 (100)
          June             6 (12.8)          47 (100)
Total                      20 (14.4)        139 (100)
Summer    July             5 (15.2)          33 (100)
          August           18 (19.8)         91 (100)
          September        45 (27.3)        165 (100)
Total                      68 (23.8)        289 (100)
Fall      October          95 (40.8)        241 (100)
          November         78 (30.1)        259 (100)
          December         57 (30.3)        190 (100)
Total                     230 (33.8)        690 (100)
Winter    January          28 (25.5)        110 (100)
          February         8 (91.1)          42 (100)
          March            7 (15.6)          45 (100)
Total                      43 (100)         197 (100)
Grand total (12 months    361 (27.7)        1315 (100)

(*) Ear, forehead, eyes, cheeks, chin, and lips; (**) Neck, hand,
chest, abdomen, and waist; ([dagger]) Legs, buttocks, and genitals.

Table 4. Frequency distribution of patients with one or multiple
leishmaniasis lesions stratified based on
different months and seasons (Isfahan, Iran, 2007-08)

Season     Month       Patients with   Patients        Total
                       one lesion      with multiple   n (%)
                       n (%)           lesions n (%)

Spring     April         22 (2.5)        12 (1.7)       34 (2.6)
           May           36 (4.2)        19 (2.7)       58 (4.4)
           June          29 (3.3)        18 (2.5)       47 (3.6)
Total                     87 (10)        49 (6.9)      139 (10.6)
Summer     July          23 (3.8)        10 (1.4)       33 (2.6)
           August        50 (8.5)        41 (5.8)       91 (6.8)
           September      72 (12)        93 (13.1)     165 (12.7)
Total                   145 (24.3)      144 (20.3)     289 (22.1)
Fall       October        80 (12)       164 (22.8)     244 (17.9)
           November      99 (16.6)      160 (22.6)     259 (19.8)
           December      83 (13.9)       106 (15)      189 (14.5)
Total                   262 (42.5)      430 (60.4)     692 (52.6)
Winter     January        60 (10)        50 (7.1)      110 (8.4)
           February       24 (4)         18 (2.5)       42 (3.2)
           March         25 (4.2)        20 (2.8)       45 (3.5)

Total                   109 (18.2)       88 (12.4)     197 (15.1)

Grand total (12 months)  605 (46)        710 (54)      1315 (100)

Table 5. Frequency distribution of usual and unusual clinical forms
of cutaneous leishmaniasis in Isfahan, Iran during 2007-08

Forms (*)       Clinical forms           Number          Percentage
                                         of infected     of
                                         people          infection (**)

Usual form      Papule                        20             1.5
(Classic)       Nodule                        400           30.4
                Ulcer Keratosis               385           29.3
                More than one clinical        34             2.9
                All classical                 839           63.8
Unusual         Impetigo                      154           11.7
(Non-           Hyperkeratosis                36             2.7
classic)        Erysipeloid                   25             1.9
                Ecthyma                       18             1.3
                Warty                          7             0.5
                Sporotrichoid                  4             0.3
                Tumoral                        2             0.2
                Zostri                         8             0.6
                Volcano-shaped                200           15.2
                Lupoid                        16             1.2
                Plaque                         6             0.4
                All non-classical             476           36.2

Total number of patients                     1315            100

(*) According to Gramiccai & Gradoni (19); (**) Percentage of infection
has been calculated considering the total number of patients with
cutaneous leishmaniasis.

Table 6. Prevalence of cutaneous leishmaniasis among patients
with different occupations in Isfahan, Iran during 2007-08

Job title             Number        Percentage

Physicians            2             0.2
Engineers             3             0.3
Nurses                6             0.5
Employees             66            5
Military (*)          75            5.7
Students (**)         237           18
Drivers               55            4.2
Workers               217           16.4
Childern              214           16.3
Housekeepers          218           16.5
Retired               23            1.8
Farmers               33            2.5
Stockmen              4             0.4
Self-employed (+)     154           11.6
Unemployed            8             0.6
Total                 1315          100

(*) Soldiers, police officers, security guards, and patrol polices;
(**) School or university students; (+) Tailor, panel maker, cabinet
maker, quilter, sales person, fireman, chef, surveyor, shoemaker,
painter, draper, and butcher.

Table 7. Prevalence of common treatments of cutaneous leishmaniasis in
different months and seasons of the year (Isfahan, Iran, 2007-08)

Seasons    Months
                        Intralesional   Intramuscular   Intralesional
                        glucantime      glucantime      and
                                                        intramuscular
                                                        glucantime
Spring     April                             6               12
           May               30              12              25
           June              5               16              20
Total                        35              34              57

Summer     July              4               8               6
           August            30              15              12
           September         24              25              14
Total                        58              48              32

Fall       October           50              81              25
           November          54              54              28
           December          58              65              25
Total                       162             200              78

Winter     January           18              24              18
           February          4               8               4
           March             10              8               10
Total                        32              40              32
Grand Total (12 months)     287             322             199
                           (21.8)          (24.5)          (15.1)

Seasons    Months                       Treatment type
                        Ointments (*)   Herbal           Cryotherapy
                                        ointments (**)

Spring     April             2
           May               18              12               -
           June              14              18               -
Total                        34              30               -

Summer     July              2                8               -
           August            2               14               -
           September         6               12              2
Total                        10              34              2

Fall       October           4                8              2
           November          6                6               -
           December           -               8               -
Total                        10              22              2

Winter     January           14               6               -
           February          2               12               -
           March             6                2              2
Total                        22              20              2
Grand Total (12 months)      76              106             6
                            (5.8)           (8.1)           (0.4)

Seasons    Months
                        Freeze    Laser     More than    Withdrawn
                        therapy   therapy   one type     treatment

Spring     April                               15            6
           May             -         -         22            12
           June            -         -         18            19
Total                      -         -         55            37

Summer     July            -         -          2            10
           August          -         -         10            8
           September      2         1          18            15
Total                     2         1          30            33

Fall       October         -        1          24            22
           November        -        2          10            16
           December        -         -         28            18
Total                      -        3          62            56

Winter     January        2          -         10            8
           February       4          -          2            2
           March           -         -          -            11
Total                     6          -         12            21
Grand Total (12 months)   8         5          159          147
                         (0.6)     (0.3)      (12.1)       (11.1)

Seasons    Months       Total

Spring     April         41
           May          131
           June         110
Total                   282

Summer     July          40
           August        91
           September    119
Total                   250

Fall       October      217
           November     176
           December     202
Total                   595

Winter     January      100
           February      38
           March         49
Total                   187
Grand Total (12 months) 1315
                        (100)

(*) Paromomycin, chlorporomazine, miconazole, ketoconazole,
betamethasone, erythromycin, tetracycline, triamcinolone, calamine D,
acyclovir, fluconazole, trichloroacetic acid (TCA) ointments, and zinc
oxide; (**) Traditional herbal medicines like turmeric, garlic, thyme,
henna, yarrow, opium, and pomegranate peel extract; Figure in
parentheses indicate percentages.

Table 8. Prevalence of patients with cutaneous leishmaniasis stratified
based on season and month of infection, nationality, and history of the
disease (Isfahan, Iran, 2007-08)

Season     Month                   Previous infection
                                   Yes                  No.
                       Once        More than once       n (%)
                       n (%)       n (%)

Spring     April        2 (1.8)                          32 (2.7)
           May          5 (4.7)         1 (5.6)          53 (4.5)
           June         2 (8.1)         1 (6.5)          45 (3.7)
Total                   9 (8.5)         2 (2.1)         130 (10.9)

Summer     July         2 (1.8)         1 (6.5)          31 (2.6)
           August       15 (14)         3 (16.7)         78 (6.6)
           September   25 (23.3)        2 (11.1)         143 (12)
Total                  42 (38.8)        6 (33.4)        252 (21.2)

Fall       October      7 (6.5)         2 (11.1)        212 (17.8)
           November    18 (16.7)        4 (22.2)        241 (20.3)
           December     8 (7.4)         2 (11.1)        181 (15.3)
Total                  33 (30.7)        8 (44.4)        634 (53.4)

Winter     January     15 (13.8)           -             95 (7.9)
           February     3 (2.7)         1 (5.6)          39 (3.3)
           March        6 (5.6)         1 (5.6)          39 (3.3)
Total                  24 (22.2)        2 (2.1)         173 (14.5)
Grand total (12 months)108 (8.2)        18 (1.4)        1189 (90.4)

Season     Month                     Nationality
                       Iranian       Afghani         Other (*)
                       n (%)         n (%)           n (%)

Spring     April        29 (2.7)        5 (2.2)       1 (3.6)
           May          14 (1.3)        5 (2.2)          0
           June         53 (4.9)        6 (2.9)       1 (3.6)
Total                    96 (9)        16 (7.3)       2 (7.2)

Summer     July          32 (3)         1 (0.5)       1 (3.6)
           August       82 (7.7)        11 (5)        2 (7.2)
           September   137 (12.8)       31 (14)       3 (10.7)
Total                  251 (23.6)      43 (19.5)      6 (21.4)

Fall       October      193 (18)       44 (20.1)       7 (25)
           November    214 (20.1)      45 (20.4)      2 (7.2)
           December    145 (13.6)      43 (19.5)      5 (17.9)
Total                  552 (51.7)      132 (60)       14 (50)

Winter     January      94 (8.8)       16 (7.3)       1 (3.6)
           February     34 (3.2)        8 (3.7)       2 (7.2)
           March        40 (3.7)        5 (2.2)       3 (10.7)
Total                  168 (15.7)      29 (13.2)      6 (21.4)
Grand total (12 months)1067 (81.2)    220 (16.7)      28 (2.1)

Season     Month
                       All
                       nationalities
                       n (%)

Spring     April         35 (2.7)
           May           19 (1.4)
           June          60 (4.6)
Total                    114 (8.7)

Summer     July          34 (2.6)
           August        95 (7.2)
           September     171 (13)
Total                   300 (22.8)

Fall       October      244 (18.6)
           November     261 (19.8)
           December     193 (14.7)
Total                   698 (53.1)

Winter     January       111 (8.4)
           February      44 (3.3)
           March         48 (3.7)
Total                   203 (15.4)
Grand total (12 months) 1315 (100)

(*) Immigrants from Iraq, Pakistan, India, Malaysia, Bangladesh,
Turkey, and tourists from other countries.
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Author:Karami, Marziyeh; Doudi, Monir; Setorki, Mahbubeh
Publication:Journal of Vector Borne Diseases
Article Type:Report
Geographic Code:7IRAN
Date:Mar 1, 2013
Words:5217
Previous Article:Natural infection of wild caught Phlebotomus tobbi to Leishmania infantum in East Azerbaijan province, northwestern Iran.
Next Article:Molecular modeling, structural analysis and identification of ligand binding sites of trypanothione reductase from Leishmania mexicana.
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