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Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy Toxicon 53 (2009) 454–459 Contents lists available at ScienceDirect Toxicon journal homepage: www.elsevier.com/locate/toxicon Epidemiological and clinical survey of scorpionism in Khuzestan province, Iran (2003) Delavar Shahbazzadeh a, *, Aref Amirkhani b, Navid Dinparast Djadid a, Shahla Bigdeli c, Abolfazl Akbari d, Hamed Ahari a, Hossein Amini a, Rouhullah Dehghani e a Biotechnology Research Center, Pasteur Institute of Iran, Pasteur Sq., Pasteur St., P.O. Box: 131694-3551, Tehran, Iran Department of Epidemiology, Pasteur Institute of Iran, Tehran, Iran c Public Health Center of Khuzestan Province, Ahvaz, Iran d Razi Vaccine Research & Serum Development Institute, 31975/148 Karaj, Iran e Department of Environmental Health, Kashan University of Medical Sciences, Kashan, Iran b a r t i c l e i n f o a b s t r a c t Article history: Received 9 June 2008 Received in revised form 31 December 2008 Accepted 9 January 2009 Available online 19 January 2009 Epidemiological and clinical survey of scorpion envenomation was carried out by statistical method of stratified cluster random sampling in Khuzestan, the southern province of Iran, cross-sectionally. We analyzed 12,150 cases recorded in Emergency Unit of the hospitals of six cities in Khuzestan province during the year 2003. The prevalence rate of human scorpion stings in the province is 3.1/1000 inhabitants. The percentage of prevalence in selected cities was as follows: Masjed-Soleiman (27.1%), Ramhormoz (26.6%), Izeh (15.3%), Shush (12%), Baghmalek (11.7%), and Behbahan (7.3%). The scorpions, responsible for the majority of stings in Khuzestan province of Iran were identified as 53.3% yellow (Mesobuthus eupeus, Hottentotta saulcyi, Odonthobuthus doriae and Hemiscorpius lepturus), and 17.4% black (Androctonus crassicauda and Hottentotta schach), and 29.3% unknown colors. Most stings occurred throughout the year, however, the highest and lowest frequency occurs in June (16.0%) and February (0.6%), respectively. Nocturnal envenomations (60.9%) were more common than diurnal (39.1%), and 39.3% of stings were on the hands and 37.3% on the feet. Most envenomings were mild (74.5%) that all evolved to cure, except for three deaths. Envenomation was characterized by local pain (63.3%), erythema (10.1%), vomiting (1.3%), restlessness (0.6%), hyperthermia (0.5%), sweating (0.4%), and spasmic (0.3%). With respect to the outcoming results, scorpionism in Khuzestan province of Iran is a public health problem, which needs to be monitored carefully by the government. Ó 2009 Elsevier Ltd. All rights reserved. Keywords: Epidemiology Scorpion envenoming Ramhormoz Izeh Baghmalek Behbahan Masjed-Soleiman Shush Khuzestan Province Iran 1. Introduction In Khuzestan, a southwestern province of Iran, as in numerous tropical areas nearby the Persian Gulf region, envenomation by scorpion stings is a major public health problem, particularly in children (Mirdehghan and Motlagh, 2001). There are more than 23 scorpion species in Iran, in which six species are dangerous, medically * Corresponding author. Tel./fax: þ98 21 648 0780. E-mail address: [email protected] (D. Shahbazzadeh). 0041-0101/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.toxicon.2009.01.002 important and responsible for envenomings (Vachon, 1966). Except for one species of Hemiscorpius lepturus, others belong to the Buthidae family and include Androctonus crassicauda, Hottentotta saulcyi, Hottentotta schach, Odontobuthus odonturus, and Mesobuthus eupeus (Radmanesh, 1990a,b; Akbari et al., 1997; Fet et al., 2000; Bucherl, 1971). Envenomations are characterized by various symptoms such as pain, sweating, fever and hypertension. The venom of Buthidae family has neurotoxic effects (Radmanesh, 1990b; Mirdehghan and Motlagh, 2001), and H. lepturus Author's personal copy D. Shahbazzadeh et al. / Toxicon 53 (2009) 454–459 with cutaneous reaction. In most severe cases, hematuria due to hematolytic effect of H. lepturus venom was reported (Radmanesh, 1998; Pipelzadeh et al., 2007). In Iran, serotherapy has been one of the major therapeutic measures used in the treatment of scorpion envenoming for the last 30 years (Akbari et al., 1997; Latifi and Tabatabai, 1979). The dose of choice for the antivenom and the administration protocol are based on the instructions advised by the manufacturer or by the National Expert Committee, which mainly includes physicians, engaged in scorpion envenomation treatment. Information on envenomation accidents in Khuzestan province is scarce and very little is known about the rate of scorpion stings in different areas of this province (Mirdehghan and Motlagh, 2001; Radmanesh, 1990a,b, 1998; Pipelzadeh et al., 2007). The current study was designed in order to investigate the demographic and clinical features of scorpion envenomation, the amount of antivenom required for treatments, and revision of current protocols. To achieve this goal, questionnaire was distributed to the Emergency Units of selected hospitals from six cities in the province during the year 2003. Statistical analyses were performed on the collected data. 2. Materials and methods 2.1. Study area and population Due to its high envenomation frequency reports among 30 provinces in Iran, Khuzestan, a southern province with the population of 3,972,309 consisting 6.6% of the whole country population was selected for the purpose of this study. The study was carried out on the data obtained from the six major cities in the province which were selected by stratified cluster random sampling method. The selected cities were as follows. Shush (183,409 inhabitants), Ramhormoz (146,364), Masjed-Soleiman (237,418), Izeh (179,337), Baghmalek (105,504), and Behbahan (170,694). 2.2. Data collection and recording process Questionnaire containing information on the envenoming accidents was distributed to the designated hospitals in the selected cities. The questionnaire contained information about the city where the incident was recorded, the date and place of the accident (inside or outside home, at work, etc.), the site of scorpion stung, as well as the age and sex of the injured, the signs and/or symptoms recorded at the time when patients admitted to the Emergency Units; possible known species of the scorpion; and measures taken by the Emergency Units for every envenomed individuals. The time between the sting and administration of antivenom and the amount of antivenom given to each patient was also recorded. 2.3. Patients A total of 12,150 cases of scorpion envenomed patients were documented in Emergency Units of the selected hospitals which were responsible for admission of envenomed patients from both the rural and urban areas. 455 2.4. Use of antivenom Most patients included in this study (7782 out of 12,150) received scorpion polyvalent antivenom. The antivenom is prepared by Razi Vaccine and Serum Research Institute in Karaj, Iran, through injecting the horses with a pool of venoms collected from six different scorpions including: A. crassicauda, H. saulcyi, H. schach, O. doriae, M. eupeus and H. lepturus. This antivenom is usually presented in the vials of 5 ml. 2.5. Statistics Data in the completed questionnaires were analyzed by EPI-info2007 research statistical software (www.cdc.gov/ epiinfo). 3. Results The 12,150 questionnaires related to the cases of reported scorpionism were collected during 2003 (Fig. 1). The accidents were reported from six cities located in different parts of the province, which were selected by stratified cluster random sampling method (Fig. 2). The percentage of reported cases was as follows: Masjed-Soleiman (Bistodo-e-Bahman hospital) 27.1%, Ramhormoz (Imam Khomeini hospital) 26.6%, Izeh (Shohada and Hefdah-e-Shahrivar hospitals) 15.4%, Shush (Nezamafi hospital) 12.0%, and Baghmalek (Tabatabaee hospital) 11.7%. It is estimated that the prevalence rate of scorpion envenomation in Khuzestan province is 3.1 cases/1000 inhabitants per year. It is notable that the accidents were occurred yearround. However, about 90% of the accidents took place in the warmest months of the year (April–October). While, although scarce, there were cases (2.5%) that detected even during the seasons in which scorpion activity is lower (December-March). There were no significant differences between sexes of envenomated individuals (52.3% female; 47.7% male). The highest incidence rate of the scorpion stings fell in the group aged 6–45 years, which was significantly different (P < 0.05) from those recorded for the other age groups. Housewives and students were under high risk for envenomation (63.3%) than those of farmers and workers (9.4%). On admission to hospital, identification of scorpion species was difficult by the information provided via the patients and or their guardians, however, a description of the scorpion’s color was obtained in 6209 (53.3%) cases as yellow and 2025 (17.4%) cases as black. About 91.5% of the individuals stung were occurred indoor, which may be in accordance with the synanthropic behavior of these scorpions in the region. The frequency of stings in feet and legs (37.3%), hands and arms (39.3%) was clearly different from those in bodies (16.8%) and head and necks (6.5%). Most stings were happened during the night (6 p.m.–6 a.m.) which is in accordance with the nocturnal behaviors of scorpions involved. Clinical signs and/or symptoms were reported in 44.8% of the accidents. Local symptoms were more frequent than systemic. The signs which more frequently reported were Author's personal copy 456 D. Shahbazzadeh et al. / Toxicon 53 (2009) 454–459 Time elapsed between stings and admission at emergency unit (hour): <3 3-6 >6 Site of sting: Hand Foot Body Head & Neck Place of sting: Inside building Outside building Time of sting (in 24 hours period): 0-6 6-12 12-18 18-24 Previous sting(s): Scorpion Snake Colour: Black Yellow Unknown Local name: Tosan (Mesobuthus eupus) Goadim (Hemiscorpius lepturus) Other Asymptomatic Symptomatic Pain Edema Vomiting Hyperthermia Sweating Spasmic Semi-consciousness Necrosis Tachycardia Restlessness Other (specify):_____________ Hemoglobinuria test IDP*(specify) Antiserum therapy Positive Previous receipt: Yes No Skin test: + Route of injection: I.V. I.M. Amount of Injection: 1-5 ml > 5 ml Sensitiveness: Allergy Shock Other Treatment Negative 1st test (at admission): 2nd test(after 6 hours): 3rd test (after 12 hours): 4th test (after 24 hours): Antihistamin Coricosteroid non-Narcotic-analgesic Antibiotic Other (specify): _____________________________________________ ________________________________________________________________ Conclusion Clinical data Scorpion data Condition of sting General information City:_________ Hospital: ____________ Date: ____________ Serial No.: ______ Last name:______________________ First name: ___________________ Sex: M F Age: Weight: Occupation: ____________________ Home Address:___________________________________________________ Phone: ______________________________ Discharged hospitalized Death Comments: ----------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------Name and sign of physician: ___________________________Date:_________ *Intensive degree of positive (IDP): 1. (1+) 2. (2+) 3. (3+) 4. (4+) Fig. 1. Questionnaire sample for the epidemiological survey of scorpion envenomation in Khuzestan province of Iran. pain (63.3%), and edema (10.1%). Neurological symptoms like spasm (0.3%) were also observed, while central symptoms like hyperthermia (0.5%), sweating (0.4%), vomiting (1.3%), restlessness (0.6%) were less frequently reported. Other reported symptoms such as tachycardia, semi-consciousness, and local necrosis (0.1%) were also observed. All patients were received medical treatments several hours after the sting. As depicted in Table 1, the history of previous treatment with antivenom was given by 997 (9.0%) cases. Most patients (64.0%) received the antivenom within 3 h after sting, reaching 77.5% up to 6 h, and the remaining 2647 (22.5%) patients were treated by antivenom after 6 h. About 97.6% of total patients were administered antivenom via intramuscular injection. However, a total of 4074 cases did not receive antivenom. Allergic reactions to antivenom, in the form of skin rash, were observed in 0.4% of cases and anaphylaxis shock (due to the horse origin antibodies in serum) occurred in just three cases. Most patients received 1–5 ml of antivenom; however, the dose was increased 2–3 folds according to the clinical presentation in 339 (4.4%) cases. Hemoglobinuria was observed in 1763 (14.5%), in which 145 (8.2%) cases showed positive result even after 24 h. The intensive degree of hemoglobinuria was reported in 1193 envenomed patients, among those 15 cases were with high degree of hemoglobinuria. During the study period, three patients reported dead after being stung by scorpions. Two cases in Izeh city; one, a 13-year-old girl envenomed by H. lepturus at 2 a.m., with local necrosis in hand, and 3þ intensive degree hemoglobinuria. She received scorpion antivenom and blood transfusion, then for further treatment dispatched to the capital hospital and died at 2 p.m. due to the heart failure Author's personal copy D. Shahbazzadeh et al. / Toxicon 53 (2009) 454–459 occurred in Masjed-Soleiman which was a 3-year-old boy, who stung by unknown black scorpion at 2:30 a.m., in the neck, transferred to the hospital and in spite of receiving medical cares and scorpion antivenom died due to the respiratory failure at 6 a.m. 2 4. Discussion 3 1 4 IRAQ 5 Ahvaz 6 Persian Gulf Fig. 2. Study areas in Khuzestan province of Iran: (1) Shush, (2) MasjedSoleiman, (3) Izeh, (4) Baghmalek, (5) Ramhormoz, and (6) Behbahan. before arriving to the hospital. The second case, was a 75year-old woman who was stung by unknown scorpion sting with local necrosis in groin (most probably due to H. lepturus), with 4þ intensive degree of hemoglobinuria, received scorpion antivenom and blood transfusion, died after 3 days of hospitalization due to hematuria. One death Table 1 Frequency of the patients’ records based on different variables encountered in the designed questionnaire completed in study areas of Khuzestan province. No. % Antiserum receipt Antiserum previous receipt Antiserum allergy 7782 997 28 64.0 9.0 0.4 Elapsed time between sting and receive antiserum <3 h 3–6 h >6 h 7693 1417 2647 65.4 12.1 22.5 Route of injection I.M. I.V. 7598 184 97.6 2.4 Amount of injection 1–5 c.c. >5 c.c. Skin reaction Shock 7356 339 13 3 95.6 4.4 0.2 – Hemoglobinuria 1st test (6 h) 2nd test (12 h) 3rd test (24 h) 1276 342 145 72.4 19.4 8.2 718 273 187 15 60.2 22.9 15.7 1.3 Intensive degree of hemoglobinuria 1þ 2þ 3þ 4þ 457 Scorpion envenomation is a major public health problem in developing countries especially in tropical and subtropical regions (Mahadevan, 2000; Osnaya-Romero et al., 2001; Ozkan et al., 2006; Radmanesh, 1990a,b, 1998; Mazzei de Davila et al., 1997; Ghalim et al., 2000). In southern regions of Iran, especially in Khuzestan province, as in numerous tropical countries, envenomation by scorpion stings is a major public health problem. Khuzestan province, neighboring with Iraq in west and Persian Gulf in south has mild winters, with average January temperatures ranging from 7 C to 18 C (45 F–64 F), very humid and hot in summer, with temperature exceeding 48 C (119 F) during July in the interior areas. The study of scorpion fauna in Khuzestan indicates that there are at least 12 scorpion species in Khuzestan from which 10 species belong to Buthidae family, one to Scorpionidae and one species to Liochelidae (Prendini, 1802; Vachon, 1966; Farzanpay, 1987; Sissom, 1998; Fet et al., 2000). Buthidae scorpions in Khuzestan province include: A crassicauda, Apistobuthus petrygocercus, Hottentotta leptochelys, H saulcyi, H schach, Compsobuthus mattheinsseni, M. eupeus, O. odonturus, Orthochirus scrobiculosus and Razianus zarudnyi (Akbari et al., 1997). There is also Scorpio maurus from Scorpionidae, and H. lepturus, previously included in the family Scorpionidae (Lourenco, 2001), which has recently been re-classified into the family Liochlidae (Solegland and Fet, 2003). The black scorpions (A. crassicauda and H. schach) and the yellow scorpions (M. eupeus, H. saulcyi, O. doriae and H. lepturus) are the most dangerous scorpions in Iran and are responsible for the majority of stings in Khuzestan province (Akbari et al., 1997; Radmanesh, 1990a, 1998; Mirdehghan and Motlagh, 2001). To our knowledge the current study is the first epidemiological survey that covers the whole province. In this present year-round clinical survey in 2003, a number of 12,150 scorpions stung patients, were cross-sectionally studied by stratified cluster random sampling method. The designed questionnaire distributed in the province which was completed by the physicians in the Emergency Unit of each designated hospitals within the cities located in the cluster which are known for their high percentage of scorpionisms reported in the province. The cities of Shush, Masjed-Soleiman, Izeh, Baghmalek, Ramhormoz, and Behbahan in Khuzestan province were selected as clusters. Based on the previous epidemiological data available in this province, the total of 36,463 scorpion sting cases (April 1990–July 1996) were referred to Abuzar hospital in Ahvaz, with a mean of 5100 stings per year and totally 61 deaths (Radmanesh, 1998). In other report, 26,397 patients have been recorded with 32 deaths during a 5-year period from 1993 to 1997 (Pipelzadeh et al., 2007). Also, Mirdehghan and Motlagh (2001) reported 28,296 scorpionism during Author's personal copy 458 D. Shahbazzadeh et al. / Toxicon 53 (2009) 454–459 1995–2000, in which 11,318 (40%) were children, 1316 cases were hospitalized and 62 died. These studies were performed by using the collected data from one or two major referral hospitals of Abuzar and Golestan in city of Ahvaz, the capital of Khuzestan province. Our finding confirms the morbidity rate in published data; however, the mortality was less than those reported in the previous works. This might be due to the improved efficacy of the local antivenom, and regional education programs carried out by local health clinics in both rural and urban areas. Scorpion stings mostly occurred indoors (7074 cases), from which 38% were recorded in housewives and 30% in school students with the age groups of 6–20 (36%), and 21– 45 (42%). About 55% of the patients had no clinical signs, but the rest showed local signs and symptoms. The most frequent symptom of scorpion envenomation was pain (63%), edema (10%), and restlessness (1%). The signs and symptoms in this study which are in local and systemic levels are in accordance with other Buthidae scorpion envenomations (Dehesa-Davila and Possani, 1994; FreireMaia, 1990; Freire-Maia and Campos, 1987; Freire-Maia et al., 1994; Mazzei de Davila et al., 1997). It can also be pointed out that our data show that there were no significant differences between sexes across all age groups in Khuzestan province, which is in agreement with the other report (Pipelzadeh et al., 2007). Feet and hands accounted for 76% of the stings, a frequency not very different from those reported by other authors worldwide (de Roodt et al., 2003; Chowell et al., 2006; Ozkan et al., 2006). The type of scorpion species responsible for the stings in Khuzestan province is unclear, and this is due to the lack of knowledge of physicians on the type of the scorpion, and unavailability of scorpions in most accidents. The most venomous of all types of scorpions in the region is H. lepturus which is categorized as yellow scorpion that contributes to 10–12% of morbidity and 95% of all mortalities in scorpion stung patients (Mirdehghan and Motlagh, 2001; Radmanesh, 1990a, 1998; Pipelzadeh et al., 2007). This scorpion can induce severe hemolysis and gross hematuria in children from a few hours to 6 days after sting, and results in renal failure development following hemolysis (Radmanesh, 1990a), and another report from Iran shows that the venom of H. lepturus produced hemolysis of red blood cells in a concentration-dependent and duration-of-exposure manner, with 100% of hemolysis produced after 24 h following exposure to 40 mg/ml of venom (Pipelzadeh et al., 2006). In our study, local necrosis was reported in 7 cases out of 4485 patients with clinical symptoms due to the sting of H. lepturus. It seems that by local necrosis appearing in the patients stung by H. lepturus, the systemic dysfunction begins and results in renal failure, which is discussed by other authors. Radmanesh (1990a,b) showed that renal toxicity is one of the serious systemic effects of H. lepturus which, if not treated early by administration of polyvalent antivenom or other medical treatments, can progress to severe renal and cardio-respiratory failures. Mirdehghan and Motlagh (2001) also shown that out of 28,296 cases of scorpion stings in Khuzestan province during 5 years, 11,318 patients were children in which 1316 have been hospitalized due to hemoglobinuria and needed renal dialysis. In the present study 1763 patients showed hemoglobinuria, from these 187 cases with 3þ, and 15 cases with 4þ intensive degrees were present, and it can be the result of H. lepturus sting. One female patient (75 years old) died with hematuria stung with unspecified yellow scorpion, most probably due to H. lepturus, the only scorpion which causes renal failure and hematuria. Based on our knowledge, Buthidae scorpions cannot induce renal failure. It is not known how H. lepturus venom causes hemolysis, whether by cell wall damage or by disturbance of different enzyme systems (Radmanesh, 1990a). According to the present study most physicians in Khuzestan province prescribe the following treatments for scorpion envenomed patients: antihistamines 4962 (43.8%), corticosteroids 4612 (40.8%), antibiotics 555 (4.9%), and non-narcotic analgesics 634 (5.6%). Our data show that 64% patients received a dose equaling to 1–5 ml serum of antivenom and 2.8% received more than 5 ml, from which only 0.5% of the patients showed allergic reaction, indicating the efficacy of the antivenom and its selection as the best choice for treatment of the scorpion stings. However, how it covers all features leading to the failure of treatment and rare death of the patients are not clear and cannot be verified based on our current knowledge. It is clear that the current treatment protocol needs to be modified and doctors advised to use antivenom only by intravenous route, in the future. In conclusion, this study shows that scorpion envenomation in Khuzestan province of Iran is a real public health problem especially in summer times and in the rural areas. The treatment consists of a combination of symptomatic conventional protocols and antivenom therapy. Due to the presence and involving of more than one scorpion species in the stings in each study in cluster areas of Khuzestan province, the quantification of venom antigens in body fluids of stung patients, by the development of immunoassay methods, is a crucial matter to evaluate the severity of envenomation by scorpions. Based on the previous studies, it is possible to identify the type of scorpion venom in the sera of stung patients in each area by developing a specific immunoenzyme assay kit (Krifi et al., 1998; Ghalim et al., 2000). The outcoming results of this study could be useful for other similar geographical and zoological areas within Iran and neighboring countries that have common fauna of scorpions in this region. Furthermore, this data may be applied in joint collaborative studies on scorpions of Eastern Mediterranean regions. Acknowledgements This research was supported by the project No. 183 of Institute Pasteur of Iran. We thank Dr. M. Moghisi and Dr. N. Ajang, Center for Diseases Management and Control (CDMC), Ministry of Health and Medical Education, Iran for useful consultancies and to Dr. M. H. Modarresi, Director, Pasteur Institute of Iran for his continuous support. Conflict of interest The authors have no conflict of interest to disclose. Author's personal copy D. Shahbazzadeh et al. / Toxicon 53 (2009) 454–459 References Akbari, A., Tabatabei, S.M., Hedayat, A., Modir Roosta, H., Alizadeh, M.H., Kamalzare, M., 1997. 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