J Arthropod-Borne Dis, September 2016, 10(3): 272–281 MR Aflatoonian et al.: A Review of Impact of … 272 http://jad.tums.ac.ir Published Online: January 06, 2016 Review Article A Review of Impact of Bam Earthquake on Cutaneous Leishmaniasis and Sta- tus: Epidemic of Old Foci, Emergence of New Foci and Changes in Features of the Disease Mohammad Reza Aflatoonian 1, *Iraj Sharifi 2, Bahnaz Aflatoonian 1, Mohammad Reza Shirzadi 3, Mohammad Mahdi Gouya 4, Alireza Kermanizadeh 5 1Research Center of Tropical and Infectious Diseases, Kerman University of Medical Sciences, Kerman, Iran 2Leishmaniasis Research Center, Kerman University of Medical Sciences, Kerman, Iran 3Zoonoses Department, Center for Disease Control, Ministry of Health and Medical Education, Tehran, Iran 4Center for Disease Control, Ministry of Health and Medical Education, Tehran, Iran 5Cutaneous Leishmaniasis Control Center, Bam University of Medical Sciences, Kerman, Iran (Received 4 Jan 2014; accepted 3 Feb 2015) Abstract Background: Global findings indicate that incidence rate of cutaneous leishmaniasis (CL) has significantly in- creased during the past decade, as documented in many countries. This review was aimed to evaluate the trend of CL cases in terms of demographic and clinical characteristics during a decade after the earthquake (2003–2012) com- pared to the corresponding period before the earthquake in Bam (1993–2003). Methods: Direct smear preparations along with different intrinsic methods were used for detection and identification of the causative agents. Results: Overall, 20999 cases of CL have occurred during the last 20 years (1993–2012), 6731 cases before and 14268 cases after the earthquake (P< 0.001). Conclusions: Following a major earthquake, several risk factors could activate epidemics of cutaneous leishmaniasis in old foci and induce emerging foci in new areas. Keywords: Cutaneous leishmaniasis, Disaster, Earthquake, Iran Introduction Leishmaniasis is estimated to cause the ninth largest disease burden in terms of mor- bidity and mortality among infectious dis- eases and is largely neglected in tropical and sub-tropical countries (WHO 2009). Cutaneous leishmaniasis (CL) represents an important public health concern of considerable magni- tude in many parts of the world, especially in Africa, Indian Subcontinent, Eastern and Southern Mediterranean Regions and coun- tries of the Middle East including Iran (WHO 2010). Both types of CL are present in different parts of Iran. Leishmania major, the causative agent of zoonotic CL (ZCL), and L. tropica, the cause of anthroponotic CL (ACL), are endemic in various districts of Iran (Shirzadi and Gouya 2012). Phleboto- mus papatasi and P. sergenti are the prin- cipal sand fly vectors, respectively, for the aforementioned CL diseases (Nadim and Af- latoonian 1995, Rassi et al. 2008). They im- pose an enormous medical and socio-eco- nomic impact here, although they are a cause of global concern. CL has the potential to spread within the cities and across borders. ACL is prevalent in Kerman Province, par- *Corresponding author: Dr Iraj Sharifi, E -mail: iraj.sharifi@yahoo.com J Arthropod-Borne Dis, September 2016, 10(3): 272–281 MR Aflatoonian et al.: A Review of Impact of … 273 http://jad.tums.ac.ir Published Online: January 06, 2016 ticularly in the city of Bam (Sharifi et al. 2011a). Global findings have shown that inci- dence rate of CL cases has significantly in- creased during the past decade (Alvar et al. 2012), as documented in Iran (Shirzadi and Gouya 2012) and across the world (Reyburn et al. 2003, Kolaczinski et al. 2004, WHO 2010, Ready 2011, Alvar et al. 2012, Ocampo et al. 2012). Several contributing factors play an im- portant role in increasing CL disease which include inadequate vector and reservoir con- trol, urbanization, ecological changes, natu- ral disasters, population movement, poor sanitation and garbage disposal system, hu- man behavioral risk factors and resistance to standard drugs (Daszk et al. 2001, Desjeux 2001, Macpherson 2005, Croft et al. 2006). All of these changes can lead to favor epi- demic, emergence and spread of CL. Natural disasters including earthquakes, tsunamis, floods and cyclones can create suitable conditions for increased incidence of infectious diseases and cause epidemics (Dye and Wolpert 1988, Desjeux 2001, Bay- ramgurler et al. 2002, Smith 2005, Shultz et al. 2005, Sharifi et al. 2011b, Kouadio et al. 2012, Zhang et al. 2013). Iran is prone to natural disasters such as earthquake. Fol- lowing natural disasters, particularly after earthquakes, various risk factors in favor of diseases will be created, which in turn pro- vide a suitable condition for breeding the vector and thus transmission of the causative agent. Other confounding factors have con- tributed to the occurrence of new outbreaks and emergence of CL after disasters in sev- eral countries (Ashford 2000, Daszak et al. 2001, Patz et al. 2000, Fazaeli et al. 2009, Fakoorziba et al. 2010). During the period after the earthquake, the population of Bam has significantly in- creased mainly due to various occupational opportunities related to the large-scale con- struction works and new project develop- ment, which caused massive movement of contractors and labor forces (Sharifi et al. 2011c). According to the official report, about 60,000 new comers, mostly males and from non-CL endemic regions (non-immune) arrived to the area and consequently resulted in increased incidence rate. The aim of the present review was to evaluate trend of CL cases in terms of de- mographic and clinical characteristics during 10 years after the earthquake (2003–2012) compared to the corresponding period before the earthquake in Bam (1993–2003). Fur- thermore, we wanted to analyze the impact of control measures applied post disaster in Bam, which would serve as a model for planning future control strategies and public health measures not only in our country but also in other foci of endemic CL as well as epidemics. Materials and Methods Scope of this study The review of literature was disappoint- ing as there was no comprehensive study re- ported. We therefore looked at the opera- tional aspects of ACL case-management, prevention and control measures that could be undertaken in disaster situation in an en- demic focus of ACL. In addition, their pos- sible impact on reduction of the CL disease was assessed. Therefore, in this review, epi- demic of old foci and emergence of new foci in Bam district following the earthquake were reviewed. Since field trials of single and multiple doses of killed L. major plus BCG vaccine candidate against ACL (Sharifi et al. 1998a) had been conducted prior to the earthquake (1993–1998), we had very good information about the epidemiology of ACL, prior to the earthquake of 2003 which gave us good background information to compare the post-earthquake situation. The trained and knowledgeable team of personnel cre- ated for the vaccine studies, were the basis J Arthropod-Borne Dis, September 2016, 10(3): 272–281 MR Aflatoonian et al.: A Review of Impact of … 274 http://jad.tums.ac.ir Published Online: January 06, 2016 on which a CL clinic (CLC) for cutaneous leishmaniasis control was established which is still functioning. Therefore, in addition to using existing published studies, registered data on passive and active case-detections, were extracted, analyzed and presented. Study area This study was carried out in district of Bam, 180 km south to the city of Kerman, center of Kerman Province, southeast of Iran (Fig. 1). Bam is located 1000 m above the sea level along the Zagros mountain range. A massive earthquake struck the city of Bam and the neighboring areas on 26th December 2003. The affected population was 250,000, 100,000 in urban and 150,000 in rural areas. The magnitude of this earthquake was 6.6 on the Richter scale, leaving 30,000 death, 30,000 injured, 60,000 homeless and dam- aging over 90% of the city's infrastructures including medical and health facilities, caus- ing l0 million tons of mud and rubbles (Abolghasemi et al. 2006). Special attention was paid to ensure rap- id recovery and rehabilitation of public health services. The city was divided to 12 zones by national and provincial health sys- tems to facilitate accessibility of the popula- tion to essential health services and strength- en the medical supply chain. Simultaneously, a disease surveillance system was promptly established in the affected areas for deliver- ing primary health care (PHC), even though the magnitude of destruction was enormous. However, it took two years to reconstruct the health and medical system following the earthquake. Approximately 30,000 people from the Province of Kerman and additional 30,000 individuals from other provinces of the country arrived at the city for various occupational purposes. Cutaneous leishmaniasis clinic In Bam, CL is a notified disease and its surveillance has long been integrated into the health system. The clinic was officially es- tablished in 2005 (two years after the earth- quake) and used as a headquarters to coordi- nate and control various activities involved in the post- earthquake era including training personnel, health education, diagnosing and identifying cases, active and passive case- finding, implementing vector control measures, eliminating stray dogs, treating patients and referring non- healing cases to the provincial health clinic in Afzalipour University Hospi- tal in Kerman, center of Kerman Province. A national control program was developed by National Center for Disease Control Of- fice, Zoonoses Department, and several Med- ical Universities of Ministry of Health (MoH). Case definition and identification Skin scraping tissues were obtained from the periphery of lesions using a scalpel and sterile blade. The clinical materials were used for direct smear preparation and microscopic examination, culture and further identifica- tion by immunological methods, PCR or char- acterization by isoenzyme (Sharifi et al. 1997, Sharifi et al. 1998b, Sharifi et al. 2011a). Personal protection measures Dressing of lesions and stick insect re- pellents such as diethyl toluamide (Deet) to skin or clothing to reduce man-vector con- tact was applied. Face-to-face health educa- tion program of the population at risk and re- training of health personnel were in high pri- ority. A large-scale deltamethrin-impreg- nated screens and curtains were assessed in high-risk areas in the city of Bam (Afla- toonian and Sharifi 2011, Noazin et al. 2013). Environmental management The activities included improving housing conditions, sanitation of temporary camps, land clearance around dwellings and insecti- cide spraying, particularly in high-risk areas, to eliminate potential sand fly breeding sites. About 10 million tons of mud and rubbles were removed. J Arthropod-Borne Dis, September 2016, 10(3): 272–281 MR Aflatoonian et al.: A Review of Impact of … 275 http://jad.tums.ac.ir Published Online: January 06, 2016 Vector incrimination So far, four main studies have been car- ried out on distribution of vectors and their implication in transmission of ACL in Bam before (Nadim et al. 1995) and after the earth- quake (Aghasi and Sharifi 2003, Aghaei Af- shar et al. 2011, Aghaei Afshar et al. 2013). Treatment of patients Pantavalent antimonials are the first choice medicines for treating all forms of leishman- iasis in global terms. In Bam, meglumine antimoniate (Glucantime) was given intra- muscularly (IM), intralesionally or sometimes intravenously (IV). Combination therapy be- tween meglumine antimoniate and cryother- apy (liquid nitrogen) or along with the se- cond line drugs (allopurinol) was used main- ly for treating ACL resistant forms (Esfan- diarpour and Dabiri 2007, Sharifi et al. 2010). Results Epidemic of anthroponotic cutaneous leish- maniasis in the city of Bam All the cases (20540 patients) were iden- tified by direct smear preparation method and overall 150 random cases by intrinsic techniques including 14 cases by immuno- logical and 9 patients by biochemical meth- ods before the earthquake and 253 cases by molecular methods (conventional or nested- PCR) after the earthquake. Various methods revealed that all species (100%) were L. tropica after the earthquake, except for the cases identified before the earthquake which were predominantly L. tropica (90%) and was at low frequency (≤10%) L. major. ACL due to L. tropica has been endemic in city of Bam since ancient times (Nadim and Aflatoonian 1995). According to the da- ta gathered in the last 20 years (1993–2012), 20999 cases of ACL have occurred, 6731 cases before and 14268 cases after the earth- quake (P< 0.001) during a similar time (Fig. 2). Over the same time, ACL incidence has steadily risen from 1.2% in 1993 to 2.5 % in the peak epidemic in 2006. There was a sig- nificant excess of incidence rate (P< 0.001) among the cases during the two times before and after the earthquake (Fig. 2). Most of the cases occurred in females (53.4%) and then in males (46.6%) 10 years before the earthquake. In contrast, proportion of females (43.7%) to males (56.3%) was reversing (Fig. 2) 10 years after the earth- quake (P< 0.001). The majority of CL cases was recorded in individuals of <20 years old 10 years before the earthquake (mean age, 17 years), whereas this proportion changed in the corresponding period after the earth- quake (Fig. 3) and there was a gradual shift of infection toward older individuals (mean age of 25 years). Anatomical distributions of lesions were considerably different during these two time periods, face (60%) was the most site of in- volvement in the 10 years before the earth- quake while location of involvement signifi- cantly changed to hands (59%) in the years after the earthquake (P< 0.001). Severity of diseases in terms of the number of lesions significantly changed before and after the earthquake (P< 0.05) (Sharifi et al. 2014). Duration of the CL disease sharply de- creased from 10.8 months to 6.1 months (P< 0.001) in the years after the earthquake. Ma- jority of the cases originally came from four old zones before the earthquake, whereas in the period after the earthquake, the cases were distributed throughout the 12 zones within the city of Bam (Fig. 1). Epidemic of anthroponotic cutaneous leish- maniasis in adjacent districts A newly established focus of ACL with low endemicity occurred following the earth- quake in the rural areas of Mohammadabad County, Jiroft District, adjacent to Dehbakri County, bordering Bam District (Poursmaelian et al. 2010). Originally, seven cases sporadi- cally emerged between 1997 and 2002 prior J Arthropod-Borne Dis, September 2016, 10(3): 272–281 MR Aflatoonian et al.: A Review of Impact of … 276 http://jad.tums.ac.ir Published Online: January 06, 2016 to the earthquake. The cases sharply in- creased to 181 patients after 2003 to peak in 2006 and become endemic, thereafter. The overall prevalence rate was 5.3%, 6.2% in females and 4.5% in males, resulting in a significant gender difference (P< 0.05). Most of the lesions were single and on the face (47%) followed by hands and legs (39%). Nested-PCR showed L. tropica, the only causative parasite. Emergence of anthroponotic cutaneous leish- maniasis following the earthquake south- ern villages of Bam A newly emerging focus of ACL was identified in southern villages (Nazamshahr County) of Bam District (Aflatoonian et al. 2013). Overall, 1.2% of the inhabitants were infected (0.5% active and 0.7% scars) and females were more significantly infected (1.7%) than males (0.8%) (P= 0.003). All the age groups were equally affected. Most of the lesions were on the face and majority of them had single lesion. Most of the cases appeared from 2006 to 2008 during the CL epidemic in the city of Bam. PCR indicated L. tropica as the causative agent. Northwestern villages of Bam Another epidemic of ACL due to L. tropi- ca occurred in rural areas of Dehbakri Coun- ty, North West of Bam District (Sharifi et al. 2011c). Again, all the age groups were af- fected although patients ≤10 years of age showed the highest rate of infection (P= 0.0001). The overall prevalence rate was 5.3%, 6.3% in females and 4.3% in males. Out of 204 cases, 1.8% had active sores and 3.5% showed scars with a significant difference between the genders (P= 0.005). Of the lesions, 47% were on the face and 77.9% had one lesion. The incidence gradually increased 2004– 2005 but grew exponentially 2006–2008. Vector susceptibility test Baseline susceptibility tests were carried out on field-collected strains of P. papatasi and P. sergenti and tested using WHO im- pregnated papers with DDT 4% and del- tamethrin 0.05% in the endemic focus of disease in Dehbakri County during 2010. LT50 values of DDT4% and deltamethrin 0.05% against P. papatasi were 20.6 and 13.6 min, respectively. The same data for P. sergenti ranged between 21.8 and 17.7 min (Aghaei Afshar et al. 2011). The impact and outcome indicators following residual spray- ing with deltamethrin were assessed in a new focus of CL in Dahbakri (Bam). Incidence of the disease was significantly decreased (3.7 vs. 8.5). There was a significant difference between the treatment and control areas on blood fed and gravity of sand flies. The re- sults clearly indicated that indoor residual spraying caused a significant decline of den- sity, blood fed and gravity of vectors, result- ing in a sharp reduction of disease incidence (Aghaei Afshar et al. 2013). Cost of treatment and prevention In a descriptive cross-sectional survey, data about treatment and prevention costs of 5320 CL patients during the two years of epidemic (2006 and 2007) were analyzed (Aflatoonian et al. 2009). The per capita treat- ment cost was estimated to be US$ 48, which showed a significant difference in terms of cost effectiveness as compared with the pa- tients in other CL endemic countries. It seems that the implementation of preventive measures had a negligible effect on the ACL control strategy (Aflatoonian et al. 2010). The au- thors concluded that establishment of CLC in Bam reduced the disease costs and pro- vided an efficient, free and easy accessible service for the patients after the earthquake. This experience could be a suitable model to be used in a similar disaster situation in other parts of the world. J Arthropod-Borne Dis, September 2016, 10(3): 272–281 MR Aflatoonian et al.: A Review of Impact of … 277 http://jad.tums.ac.ir Published Online: January 06, 2016 Fig. 1. Distribution of cutaneous leishmaniasis before (A) and after (B) the earthquake in Bam District Fig. 2. Distribution and incidence of anthroponotic cutaneous leishmaniosis cases in Bam before and after the earthquake by year (1993–2012) Fig. 3. Mean age distribution of anthroponotic cu- taneous leishmaniosis cases in Bam before and af- ter the earthquake by year (1993–2012) Discussion Global data indicate that CL is spreading and extending its range to new foci, espe- cially after major natural and anthropogenic environmental changes (Daszak et al. 2001, Alvar et al. 2012). Such changes can activate various risk factors and lead to alterations in the density and range of vector and reservoir population, thereby enhancing accessibility of humans to infected sand fly bites (Patz et al. 2000, Desjeux 2001). The review of data indicate that majority of the CL cases oc- curred in male individuals of higher ages in the period after the earthquake. The reason was mainly due to arrival of sensitive male labor forces to the city of Bam for various positions, which was created after the earth- quake (Sharifi et al. 2011b). Similar risk fac- tors have contributed major roles to the emerging epidemics of CL or other infec- tious diseases in Iran and abroad (Dye and Wolpert 1988, Bayramgurler et al. 2002, Shultz et al. 2005, Smith 2005, Fazaeli 2009, Fakoorziba et al. 2010, Kouadio et al. 2012, Zhang et al. 2013). Despite implementation of comprehensive control measures ACL occurred in several localities within the district of Bam. However, J Arthropod-Borne Dis, September 2016, 10(3): 272–281 MR Aflatoonian et al.: A Review of Impact of … 278 http://jad.tums.ac.ir Published Online: January 06, 2016 such control approaches have not adequately been evaluated. Although, large impregnated curtains and screens were assessed in several places within the city of Bam. Significant effectiveness of these control measures was observed. In addition, the impact and out- come indicators following application of re- sidual spraying with deltamethrin were eval- uated in a new emerging focus of ACL in Dahbakri County, North-West of Bam dis- trict. The incidence rate was significantly decreased (Aghaei Afshar et al. 2013). Most of the cases occurred in non- indigenous in- dividuals who arrived to the affected areas from neighboring districts and various prov- inces of the country, after the earthquake. Majority of whom were non- immune labors and contractors who traveled from non- CL endemic areas to the city of Bam where CL infection was endemic (Fig. 1). The incidence of CL was in order of 3- fold in non- local population during the peak epidemic (2006) compared to the indigenous residents (Afla- toonian and Sharifi 2010). While the incidence of disease was relatively stable in local resi- dents, it rose gradually from 2005 to 2007 in the city of Bam (Sharifi et al. 2011b). Conclusions The findings presented herein strongly suggested that, following the earthquake, major risk factors were created which were associated with epidemics and emergences of CL in Bam district and adjacent areas. Such precipitating determinants included suitable environmental conditions, poor hy- gienic conditions, individual and behavioral changes and arrival of non-immune popula- tion. These factors could activate epidemics of old foci and induce new emerging foci. Epidemiological and clinical features of the disease in terms of gender, age, location, se- verity and duration of the lesions signifi- cantly changed after the earthquake. Proper surveillance, followed by prompt diagnosis and subsequent treatment, should be extend- ed to all areas with high risk in order to pre- vent and control epidemics and/ or emer- gences of ACL, particularly in endemic foci after a major natural disaster. Acknowledgements We thank all the partners and authors who contributed information and added to the scientific merits of this work. We would also like to thank the personnel in Bam Health System, cutaneous leishmaniasis clin- ic and Kerman Leishmaniasis Research Cen- ter for their extensive work during the last two decades. The authors declare that there is no conflict of interests. References Abolghasemi H, Radfar MH, Khatami M, Saghafi Nia M, Amid A, Briggs S (2006) International medical response to a natural disaster: lessons learned from the Bam earthquake experience. Prehosp Disaster Med. 21: 141–147. Aflatoonian MR, Sharifi I, Fekri AR (2009) Evaluation of the cost-effectiveness of cutaneous leishmaniasis treatment after the earthquake. J Kerman Univ Med Sci. 4: 365–373. Aflatoonian MR, Sharifi I, Abbasi R, Ranjbar L (2010) To evaluate the cost of pre- vention on incidence of cutaneous leishmaniasis due to earthquake in Bam. Iran J Epidemiol. 6: 32–38. Aflatoonian MR, Sharifi I (2010) prevalence rate of cutaneous leishmaniasis in Bam district during 20 years (1988– 2007). J Kerman Univ Med Sci. 17 (4): 297–306. Aflatoonian MR, Sharifi I (2011) The epi- demiology of cutaneous leishmania- sis in the city and suburb of Bam in J Arthropod-Borne Dis, September 2016, 10(3): 272–281 MR Aflatoonian et al.: A Review of Impact of … 279 http://jad.tums.ac.ir Published Online: January 06, 2016 2010: active case-finding, treatment and health education of the school children. Iran J Epidemiol. 7: 52–57. Aflatoonian MR, Sharifi I, Poursmaelian S, Hakimi-Parizi M, Ziaali N (2013) The emergence of anthroponotic cu- taneous leishmaniasis following the earthquake in southern villages of Bam district, southeastern Iran, 2010. J Arthropod-Borne Dis. 7: 8–14. Aghasi M, Sharifi I (2003) Survey of the fauna and monthly activity of the sand fly as the vector of the cutane- ous leishmaniasis in the city of Bam. J Kerman Univ Med Sci. 10: 85–91. Aghae Afshar A, Rassi Y, Sharifi I, Abai MR, Oshaghi MA, Yaghoobi-Ershadi MR, Vatandoost H (2011) Suscepti- bility status of Phlebotomus papatasi and P. sergenti (Diptera: Psychodi- dae) to DDT and Deltamethrin in a focus of cutaneous leishmaniasis af- ter earthquake strike in Bam, Iran. Iran J Arthropod-Borne Dis. 5: 32–41. Aghaei Afshar A, Vatandoost H, Sharifi I, Rassi Y, Abai MR, Oshaghi MA, Yaghoobi-Ershadi MR, Rafizadeh S (2013) First determination of impact and outcome indicators following in- door residual spraying (IRS) with deltamethrin in a new focus of an- throponotic cutaneous leishmaniasis (ACL) in Iran. Asian Pac J Trop Dis. 3: 5–9. Akhavan AA, Yaghoobi-Ershadi MR, Hasibi F, Jafari R, Abdoli H, Arandian MH, Soleimani H, Zahraei-Ramazani AR, Mohebali M, Hajjaran H (2007) Emer- gence of cutaneous leishmaniasis due to Leishmania major in a new focus of southern Iran. Iran J Arthropod- Borne Dis. 1: 1–8. Alvar J, Velez ID, Bern C, Herrero M, Desjeux P, Cano J, Jannin J, Boer M (2012) Leishmaniasis worldwide and global estimates of its incidence. PLoS One. 7: e 35671. Ashford RW (2000) The leishmaniasis as emerging and reemerging zoonoses. Int J Parasit. 30: 1269–1281. Bayramgürler D, Bilen N, Namli S, Altinaş L, Apaydin R (2002) The effects of 17 August Marmara earthquake on patient admittances to our dermatol- ogy department . J Eur Aca Dermatol Venereol. 16: 249–245. Croft SL, Sunder S, Fairlamb AH (2006) Drug resistance in leishmaniasis. Clin Microbiol Rev. 19: 111–126. Daszak P, Cunningham AA, Hyatt AD (2001) Anthropogenic environmental changes and the emergence of infec- tious diseases in wildlife. Acta Trop. 78: 103–116. Desjeux P (2001) The increase in risk factors for the leishmaniasis worldwide. Trans Roy Soc Trop Med Hyg. 95: 239–243. Dye C, Wolpert DM (1988) Earthquakes, influenza and cycles of Indian kala- azar. Trans Roy Soc Trop Med Hyg. 82: 843–850. Esfandiarpour I, Dabiri SH (2007) Treatment of cutaneous leishmaniasis recidi- vans with a combination of allopuri- nol and meglumine antimoniate: a clinical and histologic study. Int J Dermatol. 46: 848–852. Fakoorziba MR, Baseri A, Eghbal F, Rezaee S, Azizi K, Moemenbellah-Fard (2010) Post-earthquake outbreak of cutane- ous leishmaniasis in a rural region of southern Iran. Ann Trop Med Parasi- tol. 104: 521–528. Fazaeli A, Fouladi B, Sharifi I (2009) Emer- gence of cutaneous leishmaniasis in a border area at south-east of Iran: an epidemiological survey. J Vector Borne Dis. 46: 36–42. Kolaczinski J, Brooker S, Reyburn H, Row- land M (2004) Epidemiology of an- throponotic cutaneous leishmaniasis J Arthropod-Borne Dis, September 2016, 10(3): 272–281 MR Aflatoonian et al.: A Review of Impact of … 280 http://jad.tums.ac.ir Published Online: January 06, 2016 in Afghan refugee camps in north- west Pakistan. Trans Roy Soc Trop Med Hyg. 98: 373–378. Kouadio Ik, Aljunid S, Kamigaki T, Ham- mad K, Oshitani H (2012) Infectious diseases following natural disasters: prevention and control measures. Exp Rev Anti Infect Ther. 10: 95–104. Macpherson CNL (2005) Human behaviour and the epidemiology of parasitic zo- onoses. Int J Parasitol. 35: 1319–1331. Nadim A, Aflatoonian MR (1995) Anthro- ponotic cutaneous leishmaniasis in Bam, southeast Iran. Iran J Publ Health. 24: 15–24. Nadim A, Motabar M, Houshmand B, Key- ghobadi K, Aflatoonian MR (1995) Evaluation of pyrethroid impregnated bednets for control of anthroponotic cutaneous leishmaniasis in Bam (Is- lamic Republic of Iran). World Health Organization /Leish/95.37 Geneva. Noazin S, Shirzadi MR, Kermanizadeh A, Yaghoobi-Ershadi MR, Sharifi I (2013) Effect of large-scale installation of deltamethrin-impregnated screens and curtains in Bam, a major focus of an- throponotic cutaneous leishmaniasis in Iran. Trans Roy Soc Trop Med Hyg. 107(7): 444–450. Ocampo CB, Ferro MC, Cadena H, Gongora R, Pérez M, Valderrama-Ardila CH (2012) Environmental factors associ- ated with American cutaneous leish- maniasis in a new Andean focus in Colombia. Trop Med Int Health. 17: 1309–1317. Patz JA, Graczyk TK, Geller N, Vittor AY (2000) Effects of environmental chang- es on emerging parasitic diseases. Int J Parasitol. 30: 1395–1405. Poursmaelian S, Mirzaei M, Sharifi I, Zarean M (2010) The prevalence of cutane- ous leishmaniasis in the city and sub- urb of Mohammadabad, Jiroft district and identification of parasite species by nested-PCR, 2008. J Kerman Univ Med Sci. 18: 218–227. Rassi Y, Abai MR, Javadian E, Rafizadeh S, Imamian H, Mohebali M, Fateh M, Hajjaran H, Ismaili K (2008) Molec- ular data on vectors and reservoir hosts of zoonotic cutaneous leish- maniasis in central Iran. Bull Soc Path Exot. 101: 425–428. Ready PD (2011) Leishmaniasis emergence in Europe (a review article). Availa- ble at: http:// www. eurosurveillance. Reyburn H, Rowland M, Mohsen M, Khan B, Davies C (2003) The prolonged epidemic of anthroponotic cutaneous leishmaniasis in Kabul, Afghanistan: bringing down the neighborhood. Trans Roy Soc Trop Med Hyg. 97: 170–176. Sharifi I, Ardehali S, Motazadian H, Afla- toonian MR (1997) Identification and characterization of Leishmania isolates in school children in Bam, southeast- ern Iran. Iran J Med Sci. 22: 82–88. Sharifi I, Fekri AR, Aflatoonian MR, Khamesipour A, Nadim A, Mousavi MR, Momeni AZ, Dowlati Y, Godal T, Zicker F, Smith PG, Modabber F (1998a) Randomized vaccine trial of single dose of killed Leishmania ma- jor plus BCG against anthroponotic cutaneous leishmaniasis in Bam, Iran. Lancet. 351: 1540–1544. Sharifi I, Fekri AR, Aflatoonian MR, Khamesipour A, Mahboudi F, Dow- lati Y, Nadim A, Modabber F (2010) Leishmaniasis recidivans among school children in Bam, South-east Iran, 1994– 2006. Int J Dermatol. 49: 557–561. Sharifi F, Sharifi I, Zarean M, Hakimi Parizi M, Aflatoonian MR, Fasihi Harandi M, Zahmatkesh R, Mashayekhi M, Kermanizadeh AR (2011a) Spatial distribution and molecular identifica- tion of Leishmania species from en- demic foci of south-eastern Iran. Iran J Arthropod-Borne Dis, September 2016, 10(3): 272–281 MR Aflatoonian et al.: A Review of Impact of … 281 http://jad.tums.ac.ir Published Online: January 06, 2016 J Parasitol. 7: 45–52. Sharifi I, Nakhaei N, Aflatoonian MR, Ha- kimi Parizi M, Fekri AR, Safizadeh H, Shirzadi MR, Gooya MM, Khamesi- pour A, Nadim A (2011b) Cutaneous leishmaniasis in Bam: a comparative evaluation of pre- and post- earth- quake years (1999–2008). J Publ Health. 40: 49–56. Sharifi I, Poursmaelian S, Aflatoonian MR, Ardakani RF, Mirzaei M, Fekri AR, Khamesipour A, Parizi MH, Harandi MF (2011c) Emergence of a new fo- cus of anthroponotic cutaneous leish- maniasis due to Leishmania tropica in rural communities of Bam district after the earthquake, Iran. Trop Med Int Health. 16: 510–513. Sharifi I, Aflatoonian MR, Aflatoonian B, Kermanizadeh A (2014) The se- verity of cutaneous leishmaniasis be- fore and after the earthquake in Bam, southeastern Iran. J Parasit Dis. (DOI 10.1007/s12639-014-0435-5). Shirzadi MR, Gouya MM (2012) National Guidelines for Cutaneous Leishmani- asis Surveillance in Iran. Ministry of Health and Medical Education, Zo- onoses Control Department, Tehran Iran. Shultz JM, Russell J, Espinel Z (2005) Epi- demiology of tropical cyclones: the dynamics of disaster, disease, and de- velopment. Epidemiol Rev. 27: 21–35. Smith AW (2005) Tsunami in south Asia: what is the risk of post- disaster in- fectious disease outbreaks. Ann Acad Med Singapore. 34: 625–631. World Health Organization (2009) Leish- maniasis: background information. A brief history of the disease. Available at: www.who.int /leishmaniasis/en. World Health Organization (2010) Control of the leishmaniasis. Report of a Meeting of the WHO Export Com- mittee on the Control of Leishmaniasis, WHO Technical Report Series 949, Geneva. Zhang S, Lu Z, Liu H, Xindong Xiao, Zongguo Zhao, Genshu Bao, Jian Han, Tao Jing, Gen Chen (2013) In- cidence of Japanese encephalitis vis- ceral leishmaniasis and malaria be- fore and after the Wechuan earth- quake, in China. Acta Trop. 1: 85–89.