J -Borne Dis, March 2019, 13(1): 104–115 O Ozkan and ME Alcigir: A Comparative …

Original Article A Comparative Pathomorphological Findings Between abdullahbayrami and (: ) Envenomation in Rabbit Model

*Ozcan Ozkan1; Mehmet Eray Alcigir2

1Çankırı Karatekin University, Çankırı, Turkey 2Department of Pathology, Kirikkale University, Faculty of Veterinary Medicine, Kirikkale, Turkey

(Received 15 May 2017; accepted 23 Dec 2018)

Abstract Background: The aim of study was to compare macroscopical and histopathological findings between venoms be- longing to two scorpion species, Androdoctonus crassicauda, and the newly discovered Leirus abdullahbayrami. Methods: The used in this experimental study were fifteen New Zealand bred rabbits. Three groups were constituted as group I (L. abdullahbayrami group, n= 6), group II (A. crassicauda group, n= 6) and group III (control group, n= 3). The animals in the L. abdullahbayrami group and the A. crassicauda group were envenomed through an intravenous route. The rabbits were monitored for the first 24h following the envenomation. The animals dead within that time period were examined and all animals were sacrificed and standard necropsy process was performed at 24h. Results: The pathomorphological findings from group I were found to be more severe than those observed in group II. The venom from the newly identified L. abdullahbayrami has a greater effect than the venom from the A. crassicauda. Moreover, as this was a rabbit modeling study, the L. abdullahbayrami might pose the most serious health threat to infants in particular due to their smaller body weight. Conclusion: These findings will provide a better understanding of envenomation of human beings in terms of the possible consequences of scorpion toxication on the organs.

Keywords: Leirus abdullahbayrami; Androctonus crassicauda; Venom; Pathomorphology; Rabbit

Introduction

In many parts of the world, millions of Africa, India, and the Middle Eastern countries people are stung by various scorpion species because those areas have scorpion species with yearly. These stings can result in death, par- the most potent venoms as they are classified as ticularly in children (1, 2). This is because of neurotoxic, hemotoxic, cardiotoxic, nephrotox- the serious health problems that result, such as ic, and myotoxic (3-5). cardiovascular, respiratory, and/or neurologic In Turkey, the most hazardous complications. Nowadays, despite advances in are the yellow scorpion, Leiurus abdul- medical science, scorpion envenomation cas- lahbayrami, which is endemic in Southeast- es still continue to be a current public health ern Anatolia, and a black scorpion, Androcto- problem all over the world, including in Tur- nus crassicauda, commonly found in South- key. Scorpions are considered to be life-threat- eastern Anatolia and in a part of Eastern Ana- ening venomous animals. Arguably, the med- tolia (Fig. 1) and neighbouring countries ical knowledge of the scorpion's species is most Iran, Iraq and Syria (2, 5-7). critical for the scorpion species that are typi- Furthermore, in these regions, the species cally found in Mexico, the middle and northern are responsible for the most deadly cases, par- regions of South America, North and South ticularly those involving children. According- 104 *Corresponding author: Dr Ozcan Ozkan, E-mail: [email protected] http://jad.tums.ac.ir Published Online: April 27, 2019

J Arthropod-Borne Dis, March 2019, 13(1): 104–115 O Ozkan and ME Alcigir: A Comparative …

ly, these scorpion species are described as med- following a venom injection (20-22). In enven- ically significant to both the world and to Tur- omations from different scorpion species, the key (1, 3, 5, 7). lungs, heart, liver, intestines, and pancreas were In the toxicokinetic studies, radiolabeled documented as the most affected organs in ad- venom from the L. quinquestriatus and venom dition to the recently described effects on the from the A. crassicauda scorpion have reached brain following a Leiurus envenomation (23- the maximum value of total plasma radioac- 27). tivity in less than two minutes after a subcu- As a result of the effect of scorpion venom, taneous injection and begin distribution with- different clinical tables have reported varying in four to seven minutes after the injection with effects from localized signs to more serious au- a half-life of between 4–21h. At that time, the tonomic and neurologic findings as well as fatal degree of the clinical symptoms depends on cases due to multisystem organ failure. Ac- the amount of venom circulating in the body cording to medical records from Turkey, most (7-9). deaths were caused by the results of cardiopul- A low venom dose triggers an adrenergic monary complications, such as myocarditis and effect while high scorpion venom concentra- acute pulmonary edema following a scorpion’s tions result in venom cholinergic symptoms. sting (1, 2, 7). The venom results in an excessive acetylcho- In animal models, scorpion envenomation line (Ach) release or a decrease in the destruc- symptoms were similar to those described by tion of Ach, which is acting on the postgan- the clinical findings in humans. Therefore, to glionic nerve endings. Thus, cholinergic activ- mimic human victims, especially children, rab- ity begins. On the other side, catecholamine is bits were chosen as the animal model for ex- released into the peripheral sympathetic nerve perimental scorpion envenomation to mimic endings from the adrenal medulla in response a natural sting accident. Thus, in this study, to the venom. Then, an autonomic storm begins different pathomorphological findings devel- because of the renin secretion by the alpha ad- oped by two scorpion venoms were revealed renergic receptor. The receptor stimulation out L. abdullahbayrami and A. crassicauda, plays a significant role because it increases which species were most encountered in south- blood pressure and ultimately results in the east region of Turkey and also were showed pathogenesis of pulmonary edema. Addition- L. abdullahbayrami having unusual harmful ally, it causes an inflammatory reaction in the effects onto several organs during long term. vital organs (8, 10-13). Scorpion envenomation has been reported to mainly culminate in a syndrome of fuel-en- Materials and Methods ergy deficiency. This situation develops as a deficiency during the usage of existing meta- Scorpions Origin bolic substrates. As an aftermath, a failure oc- Scorpions were collected using an ultra- curs within vital organs including a multi-or- violet lamp at night in the Sanliurfa and Ga- gan system deficiency that can lead to death ziantep Provinces, southeastern part of Tur- (14, 15). The main reason for this failure is the key. The animals were kept in plastic boxes triggering of an inflammatory response cascade at the Department of Entomology, Faculty of that results in a release of several mediators, Veterinary Medicine, Ankara. The scorpions such as prostaglandins, cytokines, and nitric ox- were received fresh water daily and fed crick- ide, and an infiltration of inflammatory cells ets or cockroaches weekly. (16-19). The highest venom concentrations can be found in the kidneys, liver, heart, and lungs 105 http://jad.tums.ac.ir Published Online: April 27, 2019 J Arthropod-Borne Dis, March 2019, 13(1): 104–115 O Ozkan and ME Alcigir: A Comparative …

Scorpion venom and the median lethal dium Pentobarbital injection (100mg/kg Intra- dose (LD50) venous route) were done and then cervical dis- The venom of scorpions was milked by location were performed for each one. Necrop- electrical stimulation of 24 Volt. The venoms sy process was done systematically and all or- were added sterile double-distilled water, dis- gans and tissues were examined routinely. Le- solved and centrifuged at 14000rpm for 15 sions were photographed. For histopathologi- min at 4 °C. Supernatant was dissolved in PSS. cal examination, tissue samples were taken sys- The median lethal doses (LD50) of the scor- tematically from each organ in 10% buffered pions were determined as in previous studies formalin. After fixation for 48h, tissue samples (28, 29). were processed routinely through alcohol and xylol series and mounted in paraffin. Processed Animals tissues were embedded in paraffin wax. Five- This study was conducted on 15 of healthy micron thickness-sections were cut from par- New Zealand rabbits 12 months old of both affin blocks and Haematoxylin-Eosin (H and sexes and between 2.4±0.1kg body weight for E) staining method. this experiment. The rabbits were fed with a special rabbit pellet diet ad libitum until en- Results venomation. The animals were kept in room temperature set to 19±1 °C and with 12h light/ Macroscopical Findings 12h dark schedule. The experimental protocol In all groups, cadavers were well-fed, and was approved by the local Laboratory Animal rigor mortis did not happen. However, the Ethics Committee. After 24h all animals were blood in group I was lately clotted in contrast subjected to euthanasia for macroscopical and to the other groups. Conjunctiva was hyper- histopathological findings. emic in two of the animals from group I. The gut walls were thickened and filled with a yel- Experimental envenomation of the animals lowish content in all of the members of group The animals were envenomed by the ven- I and II. The liver, kidneys, and lungs were con- om of L. abdullahbayrami in group I (GI, n: gested in all members of both groups I and II. 6), and the venom of A. crassicauda in group However, there was haemorrhagia that hap- II (GII, n: 6). Finally, three rabbits were se- pened in the kidneys in the members of group lected as a control group and will be referred II, and also atrophia and capsular contraction to as GIII. The venoms (2xLD50 for both) were in the spleen was noticed in all animals within injected into the marginal ear vein by intrave- group II. In group I, a meningeal vessel was nous (IV) route after dissolving the venoms congested in one animal. In contrast, none of within 0.5mL PSS. For control group, any en- these macroscopical findings were evident in venomation was not performed. 0.9% Physi- the animals of group III. ological saline solution only was administrated to rabbits of this group. The animals were mon- Histopathological Findings itored and kept in individual cages up to 24h Heart following the injections because the deaths were Myocardiocytes in some areas were degen- not shown during first 24h of critical period. erated or partly necrotic in the members of group I. There was a hyalinosis in appearance Histopathological Examination in the degenerated myocardiocytes in the group After providing sedation by xylazine (10 I. Haemorrhagia between cardiomyocytes was mg/kg Intramuscular route) and ketamine hy- formed in two animals from group I and four drochloride (5mg/kg intramuscular route), So- 106 http://jad.tums.ac.ir Published Online: April 27, 2019 J Arthropod-Borne Dis, March 2019, 13(1): 104–115 O Ozkan and ME Alcigir: A Comparative …

animals from group II. However, there was fo- Central Nervous System cal mononuclear cell infiltration in one animal Lesions on the central nervous system from group II. There were no changes in con- were predominantly seen in group I. Menin- trol group. geal and parenchymal vessels were severely hyperemic in one animal of group I. Stratum Lungs pyramidal cells of the brain often seemed to All veins and vessels were hyperemic in have lost their nuclear chromatin in almost members from group I. Furthermore, there was all foci. Perivascular mononuclear cell infil- edema in all of the animals in group I. Micro- tration was observed in substantia alba of the haemorrhagies were noticed in three of the cerebrum within one of the animals in group members of group I and all of the members I. In the cerebellum, cytoplasms and nuclei of group II. BALT hyperplasia was noted in of Purkinje cells generally degenerated in one member of group I and all of the mem- both groups of animals. Moreover, some of bers of group II. It was not encountered with the cells were necrotic in group I animals, any findings in control group. seen in Fig. 2 and Fig. 3A–F. However, there were no conspicuous findings in the control Kidneys group in terms of any of these organ. In the kidneys, there was hyperemia in all vessels and glomerules in all animals from Gastrointestinal system group I, there were no such findings in the Regarding the intestinal lesions, in group group II animals. On the other hand, vacuolar I, lymphocyte-plasma cell infiltration was and hydropic degeneration in tubular epitheli- noted in three animals, and neutrophil leuco- um were common findings for members of the cyte infiltration was evident in one animal in first group except for one of group I animals. the duodenum. In the group II, lymphocyte There is no any changes in control group. and macrophage infiltrations were seen in the jejunum as well as the duodenum in two Liver of the animals. In addition, aggregate lym- Hepatocytes contained vacuoles in different phoid follicles were hyperplasic in three an- sizes in their cytoplasm and degenerated nuclei imals from group I. There were no findings in especially the periphery of lobules for all an- in the stomach of any of the members of imals from the first two groups. In some an- group I in contrast to the focal periarteriolar imals of group II, reticular degeneration was haemorrhagia noted in one animal from also noted in addition to those findings. Ad- group II. In control group, there were no any ditionally, mononuclear cell infiltrations in the pathologies. portal field were evident in the group I find- ings and in all animals of group II. Finding in control group in terms of this organs were un- remarkable.

Spleen Although no prominent findings were observed in animals of group II, focal follic- ular necrosis and haemorrhagia were noted in each animal of group I. Finding in control group in terms of this organ were unremark- able. 107 http://jad.tums.ac.ir Published Online: April 27, 2019 J Arthropod-Borne Dis, March 2019, 13(1): 104–115 O Ozkan and ME Alcigir: A Comparative …

Fig. 1. The distribution of the black colored scorpion is the Androdoctonus crassicauda (black dots), and a yellow colored scorpion the species (red dots) are found in Hatay, Kilis, Sanliurfa, Mardin, Gaziantep provinces of the Southeastern Anatolia as shown map of Turkey. The scorpions were captured in Gaziantep and Sanliurfa

Fig. 2. A. Vacuolar degeneration (arrows), periphery of lobules, liver, x100, H and E. B. Hyperemia (asterisks), glomerules and capillary vessels, kidney, x100, H and E. C. Vacuolar degeneration (arrows), kidney, x400, H and E. D. Haemorrhagia (arrows), lung, x100, H and E. E. Necrosis in myocardiocytes (arrows), x100, H and E. F. Degeneration (arrows) and necrosis (arrowhead) in Purkinje cells x100, H and E 108 http://jad.tums.ac.ir Published Online: April 27, 2019 J Arthropod-Borne Dis, March 2019, 13(1): 104–115 O Ozkan and ME Alcigir: A Comparative …

Fig. 3. A. Focal lymphocytes in propria mucosa (arrows), duodenum, x100, H and E. B. Focal mononüklear cell infiltration (asteriks) in portal region and vacuolar degeneration in hepatocytes (oklar), liver, x100, H and E. C. Hydropic degeneration in tubul epitheliums (arrows), kidney, x100, H and E. D. Haemorrhagia (arrows), lung, x100, H and E. E. Focal lymphocyte infiltration (arrow), heart, x100, H and E. F. Degenerative and necrotic changes (arrows), cerebellum, x100, H and E

Discussion

Scorpion envenomation continues to be a clinical table has shown localized symptoms global problem despite some national measures at the sting site up to a significantly severe taken by authorities in various countries. Re- generalized envenomation (7, 11, 28). garding the the clinical symptoms, the degree In Turkey, the scorpion sting is very com- of the envenomation depends on some factors mon in the provinces of Southeastern Anato- related to the scorpion such as the species and lia and Eastern Anatolia due to social and ge- the size of the scorpion as well as the number ographical factors. In these areas, the scorpion of stings, the content of the venom, and the sting cases have been reported as coming from amount of venom injected. Another factor as- both the yellow colored scorpion, which is the sociated with a patient’s prognosis include the L. abdullahbayrami, and a black colored scor- patient’s health status, the part of the body that pion, which is the A. crassicauda species. In has been stung, the patient’s body mass, and addition, scorpions have been the main animal the patient’s age. After the sting, the symptoms responsible for medically important enven- of envenomation can be evident within a few omation cases (5, 11-13). minutes, and maximum severity is usually In the Kilis Province, southeastern Turkey, achieved within five hours. Consequently, the recently, acute pulmonary edema and cardio 109 http://jad.tums.ac.ir Published Online: April 27, 2019 J Arthropod-Borne Dis, March 2019, 13(1): 104–115 O Ozkan and ME Alcigir: A Comparative …

myopathy were due to the excessive catechol- diomyopathy and acute pulmonary edema were amine release that resulted from a sympathetic caused by severe envenomation, especially overstimulation in an 11-yr-old male child fol- among small children or infants because of their lowing an L. abdullahbayrami stung (7). An- smaller body weight (7). Namely, following other study conducted at the Sanliurfa Chil- envenomation, an acute failure leads to multi- dren’s Hospital reported on a patient with symp- organ system deficiency among the vital or- toms that included fever, hypersalivation, my- gans, which leads to death (14, 15), especially driasis, tachycardia, lethargic, and respiratory within the heart and lungs. After acute enven- distress during admission time. Later, this pa- omation, a cardiac dysfunction occurred, and tient had to be intubated because of pulmonary as a result of this cardiac failure, the formation edema and myocarditis. Another girl had neu- of edema and hemorrhages happened in the rological signs similar to the first victim as well lungs (8, 9, 33). Thrombosis of cardiac vessels, as anisocoria and seizure. Two girls, ages 2-yr- endothelial cells of those vessels, edema, and old and 4-yr-old, had pulseless ventricular tach- necrosis in cardiac muscle cells were all ob- ycardia and died (13). In the province of Hatay served during the 24h following envenomation in the Southeast Anatolia region, the patients (33). In another acute envenomation study with were categorized according to the color of the A. australis hector, LD50 of the venom resulted scorpion that had stung them as yellow (54.2%) in myocardial necrosis and degeneration. Neu- and black (28.7%). Two children passed away trophil leucocyte and mononuclear cell infil- due to cardiac and respiratory complications tration in the interstitium of myocardium were resulting from a scorpion sting (30). In this noted within the first 24h period in mice as same province, a 4-yr-old boy died because of well. Suppurative bronchopneumonia, focal pulmonary edema (31). Furthermore, in Adıya- haemorrhagia, and fibrin deposits are found in man Province, the patients were categorized the lungs of the mice. Cardiac edema, myocar- by the color of the scorpion as well with black dial haemorrhagia, degeneration and necrosis consisting of 40% of the cases and yellow re- were also detected with envenomation attribut- sulting in 60% of the cases (12). One of these ed to Centuroides sculpturatus venom (34). In patients died due to cardiac and respiratory ar- another study that experimented with LD50 rest. 50.8% of their scorpion cases were A. doses of Mesobuthus eupeus envenomation on crassicauda stings (5). Additionally, four of rabbits, several important consequences pro- the deaths in children were caused by the A. gressed including myocardial necrosis, focal crassicauda species, and only one was caused haemorrhage, thrombus formation and inflam- by an L. abdullahbayrami (32). Especially in mation in myocardium and the endocardium children, similar findings have been shown in surfaces of the heart and lungs (35). In our previous studies concerning these two important study, more serious fatal findings, such as hy- scorpion species. These scorpions were respon- peremia, edema, and haemorrhage, were evi- sible for serious medical cases and deaths in dent in the lungs. Degeneration and necrosis Turkey as well. Therefore, our study aimed to in the myocardiocytes occurred within the rab- determine and compare the pathological ef- bits in group I envenomated with L. abdul- fects of the venom based on an animal model. lahbayrami. However, BALT hyperplasia and The L. abdullahbayrami scorpion venom- microhemorrhage were encountered in the induced potassium and sodium voltage-gated lungs and focal mononuclear cell infiltration ion channels and then led to excessive cate- in heart in the rabbits envenomated with A. cholamine release due to the over stimulation crassicauda. Leiurus abdullahbayrami trig- of the sodium and potassium ion channels. gered a more acute reaction especially in re- As a result of the catecholamines storm, car- gards to the cardiopulmonary system within the 110 http://jad.tums.ac.ir Published Online: April 27, 2019 J Arthropod-Borne Dis, March 2019, 13(1): 104–115 O Ozkan and ME Alcigir: A Comparative …

first 24h as compared to another type of ven- gestion were encountered in both the spleen and oms documented in several previous studies. the pancreas (36). In our study, no other prom- Therefore, the results obtained from these study inent findings were evident. However, focal groups were found to parallel the findings of follicular necrosis and haemorrhagia were both previous studies which also examined the ef- noted in all of the animals in group I. The ven- fects that occur within the first 24h following om of the L. abdullahbayrami might be more a scorpion sting. effective since it triggered an inflammatory re- Some deaths in humans and animals were action. related to the effect of the venom on the kid- In relation to the gastrointestinal system, neys. The scorpion toxin caused hyperemia and edema and mildly necrosis have occurred in degenerative-necrotic changes in the tubules the guts of these envenomed animals. On the and glomeruli. This situation resulted in acute other hand, no inflammatory changes were ev- renal failure (2, 33, 34, 36, 37). Even an enven- ident even though there were severe microscop- omation attributed to a Hemiscorpius lepturus ical changes noted, such as gastrointestinal scorpion can sometimes result in a uremic syn- haemorrhagia, necrosis, and inflammation (33, drome in a child (38). In an acute envenomation 36). In our study, in group I, inflammatory re- from M. eupeus, congestion in the vessels and actions was evident in some of the animals glomeruli of the envenomated animals has been from both groups. Additionally, aggregate lym- reported. In our study, group I animals en- phoid follicles were found hyperplasic in three venomated with L. abdullahbayrami showed animals of group I. There were no findings in similar important damages, including vascular the stomach of any of the members from group congestion and degenerative changes in tubules, I, which was in contrast to the focal periarte- as compared to group II animals envenomat- riolar haemorrhagia found in one of the animals ed by the venom of the A. crassicauda. from group II. These findings correlated with On the other hand, certain studies conduct- the previous findings (36). In our study, the ed in association with particularly both acute most significant findings in almost all organs as well as sub-acute envenomation have prov- were mostly hyperemia, focal haemorrhagia, en that venom of the M. eupeus species can and mononuclear cell infiltrations as was in- promptly effect animals within 30min up to dicated in several previous studies. Such results three to five hours later by resulting in con- have been reported as a result of inflammatory gestion within the central and portal vein of responses under influence of the variety of cy- the liver and in interstitial vessels (35). In sub- tokines as reported in previous reports (18, 24, acute envenomation caused by the C. sculp- 25). In our study, the acute findings belonging turatus’s venom, the liver of rats was affect- to L. abdullahbayrami envenomation were ed within two hours and up to five days after found to be more severe than the A. crassi- the envenomation. In the livers of envenomat- cauda envenomation because it caused much ed animals, congestion of central veins, hy- more of an inflammatory reaction within the dropic degeneration, and single cell necrosis first 24h. In this sense, the newly identified of hepatocytes was also observed (34, 38). In L. abdullahbayrami venom had more of an ef- our study, the findings were observed in both fect than the A. crassicauda venom. experimental groups. However, mononuclear Additionally, many studies have reported cell infiltrations in the portal field were also on this inflammatory responses following en- noted in all of the animals of group II. The last venomation. Among them, leucocytosis has finding is a different finding as compared to been mentioned as occurring in the hours fol- previous reports. Apart from the findings with- lowing envenomation (14, 18, 25, 39, 40). In in the vital organs, milder findings such as con- the present study, mononuclear cell infiltrations 111 http://jad.tums.ac.ir Published Online: April 27, 2019 J Arthropod-Borne Dis, March 2019, 13(1): 104–115 O Ozkan and ME Alcigir: A Comparative …

were more evident in several organs, especial- L. abdullahbayrami has resulted in more severe ly among the Leirus sp. group. The Leirus lesions when compared to the A. crassicauda. envenomation resulted in an ongoing or final Especially, findings were evident in both the stage of acute inflammatory reaction. On the vital parenchymatous organs, such as the heart, other hand, the main affected organs included lungs, liver, kidneys, as well as other organs, the lungs, liver, intestine, and pancreas, respec- such as the brain, spleen, gastrointestinal sys- tively (22-26). However, some important find- tem, during the first 24h. In addition, the lesions ings in the kidneys and the central nervous sys- were more related to vascular changes and de- tems were also evident in our study, which was generative-necrotic changes in envenomated an- less likely to be mentioned in prior documents imals with L. abdullahbayrami. Thus, some cy- except for the most recent document (27). The tokines might have change the immune re- inflammation might be a long-term effect from sponse of the animals against the preservation the two types of venom. Particularly, another of body homeostasis. This situation might be reason for multiple organ disfailure was the hy- more related to the degrees of toxic components dropic-vacuolar degeneration in parenchyma- of mentioned scorpion species. In this regard, tous organs. It has been previously associated therapeutic strategy against envenomation by with the loss of function of the Na-K ATPase several scorpion species and course of toxi- pump (15, 27, 41, 42). This situation could be cation might be changed during critical first further clarified by examining several fractions 24h-period. of these venoms that target one or more vital cells such as those from the liver, kidneys and Acknowledgements also the cerebellum rather than simply focus- ing on the most prominent vital organs of the No financial support was received for this heart and the lungs. Hence, we think that the study. The authors declare that there is no hepatocytes, tubular epitheliums, and Purkinje conflict of interests. cells were more affected based on the findings of this current study. In our study, the main acute findings were mainly hyperemia, haem- References orrhagia and degenerative-necrotic changes in the aforementioned vital organs. The period of 1. Yılmaz F, Arslan ED, Demir A, Kavalci C, experimentation for this study was longer as Durdu T, Yılmaz MS, Yel C, Akbulut S compared to other envenomation studies. Find- (2013) Epidemiologic and clinical char- ings from this study related to the other organs acteristics and outcomes of scorpion sting besides just the two vital organs have been in the southeastern region of Turkey. Ulus made more evident due to the longer time that Travma Acil Cerrahi Derg. 19(5): 417– allowed these effects from both types of ven- 422. oms to be noticed. In addition, histopatholog- 2. Shahbazzadeh D, Amirkhani A, Djadid ND, ical findings might change according to the type Bigdeli S, Akbari A, Ahari H, Amini H, of scorpion venom and the envenomation meth- Dehghani R (2009) Epidemiological and od for an organism. clinical survey of scorpionism in Khuzestan Province, Iran (2003). Tox- Conclusion icon. 53: 454–459. 3. Bavani MM, Rafinejad J, Hanafi-Bojd AA, Leirus abdullahbayrami and A. crassicauda Oshaghi MA, Navidpour S, Dabiri F, Ba- venoms cause to more slight findings beyond dakhshan M, Ghorbani E, Bagheri M simply resulting in death for rabbits. However, (2017) Spatial Distribution of Medically 112 http://jad.tums.ac.ir Published Online: April 27, 2019 J Arthropod-Borne Dis, March 2019, 13(1): 104–115 O Ozkan and ME Alcigir: A Comparative …

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