J Arthropod-Borne Dis, March 2017, 11(1): 166–170 T Hazratian et al.: Pharyngeal Myiasis Caused … 166 http://jad.tums.ac.ir Published Online: March 14, 2017 Case Report Pharyngeal Myiasis Caused by Sheep Botfly, Oestrus ovis (Diptera: Oestridae) Larva, Tabriz, East Azarbaijan Province, Iran: a Case Report *Teimour Hazratian 1, Ali Tagizadeh 2, Mohammad Chaichi 3, Madineh Abbasi 1 1Departement of Parasitology, School of Medicine, Tabriz University of Medical Sciences, Tabriz, Iran 2Departement of Emergency Medicine, School of Medicine, Tabriz University of Medical Sciences, Tabriz, Iran 3Departement of Infectious and Tropical Diseases, School of Medicine, Tabriz University of Medical Sciences, Tabriz, Iran (Received 18 Dec 2014; accepted 3 Aug 2016) Abstract Myiasis is caused by the larvae of flies infesting animal or human tissues and organs. This report aims to present a case of pharyngeal myiasis caused by the larvae of Oestrus ovis (Diptera: Oestridae). A 55-yr old drug addict living in the Shahindeje village of Western Azerbaijan Province, northwestern Iran was referred to the Emam Reza Hospi- tal in Tabriz, having a medical history of Chronic Obstructive Pulmonary Disease (COPD) and hospitalized due to respiratory distress, 20 days ago. He was intubated with a mechanical ventilator (MV) because of his respiratory distress condition. There was an evidence of the presence of pulmonary nodules in his lungs following diagnosis, and a CT scan revealed a cavity in his lung. During the nasogastric intubation procedure, a larva was seen emerging from the patient’s mouth by one of the staff of the intensive care unit of the hospital. A laboratory diagnosis was per- formed in the Entomology Department of the School of Medicine, Tabriz University of Medical Sciences. Interest- ingly, larvae of O. ovis were identified and confirmed following the laboratory proceedings. Keywords: Myiasis, Pharyngeal myiasis, Oestrus ovis, Iran Introduction Propounded by Hope in 1840, myiais orig- inated from a Greek word known as “Miya” which means fly (Sharma et al. 2008). Myiasis is a term used to describe a medical condi- tion in which the tissues and organs of human or animals are infested by the larvae of flies (Masoodi et al. 2000). These fly larvae peri- odically obtain food from their hosts’ dead or living tissues, body fluids or directly ingest solid food (Laner and Crosskey 1993), which may result in various clinical manifestations. The sheep nasal botfly, O. ovis, is one of the remarkable causative agents of human myia- sis (Verstrynge and Foets 2004). The family Oestridae encompasses a wider range of spe- cies in which the larvae of all included spe- cies are obligate parasites of domestic ani- mals or wildlife. Unexpected intrusion of human tissues by a number of these parasites gives rise to se- vere pathological consequences. The devel- opment of Oestrinae larvae occur in the naso- pharyngeal cavities of a host of mammalian species. First-stage larvae of O. ovis are de- posited by the females into the nostrils of sus- ceptible domestic mammals. Though uncom- mon, the larvae are occasionally transferred into the eyes, the mouth, or the external ear of man, especially in people who are in close con- tact with sheep and goats. Notably, patients complain being hit in the eye by a wandering insect or object. In critical situations, migra- tion of the larvae to the nasal cavities ensues, leading to an abscess formation, pain and head- ache. In human nasal cavities, the growth of fly larvae into a third stage hardly occurs. When *Corresponding author: Dr Teimour Hazratian, E-mail: hazratiant@tbzmed.ac.ir J Arthropod-Borne Dis, March 2017, 11(1): 166–170 T Hazratian et al.: Pharyngeal Myiasis Caused … 167 http://jad.tums.ac.ir Published Online: March 14, 2017 these larvae spread to the throat, swallowing of food becomes challenging, however these symptoms do not last long (Richard and Cross- key 1996). Classification of myiasis may be accom- plished in two wasy, entomological or clini- cal. In Entomology, myiasis is classified ac- cording to the parasitic characteristics of the fly larvae. These include obligatory, faculta- tive and accidental parasitic fly larvae. Clini- cally, however, myiasis is classified based on the anatomical region in which infestation oc- curs (Langan et al. 2004). Key examples of the clinical classifications include ophthalmomy- iasis (Janbakhsh et al. 1977), Urogenital myiasis (Jdalayer et al. 1978), Orbit myiasis (Khata- minia et al. 1999), Pharyngeal myiasis (Karimi and Vahidi 1999), Ear myiasis (Talari et al. 2002), Auricular myiasis (Tirgary et al. 1977), Oral mucosa myiasis (Hakimi and Yazdi 2002) and wound myiasis (Talari et al. 2004). In ad- dition, clinical classification of myiasis may be described as primary or secondary. Rarely seen in humans but frequent in cattle (called bicheiras), primary myiasis results from the invasion of living tissue-feeding (biophagous) fly larvae. Comparatively, secondary myasis develop when necrobiophagous fly larvae in- vade and feed on dead tissues, commonly seen in humans in which the patients suffer necrotic cavity lesion (Shinohara et al. 2004). The life cycle of the sheep bot fly begins from the fertilization of eggs in the female which later hatch into 1mm larvae in the fe- male’s body. Subsequently, a few larvae are directly released in a tiny drop of mucus into the nostrils of the animal host, after which the larvae migrate through the mucosa of the nostrils into the nasal sinuses. The matura- tion of the larvae continues at this stage fol- lowing their growth and molting into the se- cond larval stage, reaching a full length of 20mm with characteristic dark-striped seg- ments. Upon full maturation, the larva pre- pares itself for pupation in the ground after it emerges and falls from the nostrils. Temper- ature plays a crucial role in the determination of the period of larval growth. In warmer weather conditions, larval maturation may be completed within 25–35d, while this may take a much longer time in colder climates up to 10 months. The temperature-depend- ent, pupal development stage is completed within 3–9 weeks, followed by the emer- gence of winged adults from the soil and sub- sequent mating. During the first few weeks (normally 2–4 weeks) after nuptial flight, the adults do not feed but may take up water (Capelle and Kenneth 2012). Human infestation of the disease has been recognized extensively over the years (Pam- piglione et al. 2012). The disease is readily associated with shepherds having close con- tact with sheep, although a few more cases have been recorded in non-native individuals who harbor the disease and import them into their localities (Masoodi and Hosseini 2004). The disease is medically curable, or corrected with some medication (Gregory et al. 2004). Hospital-acquired nosocomial myiasis in patients is unusually observed, and oral my- iasis occurs at any place, though not very common in developed countries (Reuler et al. 1985). The underlying symptoms of oral my- iasis condition entail traumatized face, mouth bleeding, distinctive lesions and debilitation of the palate (Bhatt and Jayakrishnan 2000). Globally, nosocomial myiasis are evident in intensive care units, however, only a few cases are documented due to underreporting of the disease (Joo and Kim 2001). A study by Najjari et al. and Yaghoobi et al indicated the presence of several cases of myiasis in ICU patients in Iran (Najjari et al. 2014), (Yaghoobi et al. 2005). There have been a recent report projecting the rate of nosocom- ial myiasis infections as 4%, and a mortality rate of 1.3% (Alizadeh et al. 2014). This novel case report highlights a case of pharyngeal myiasis caused by the larva of O. ovis for the first time in Emam Reza Hospi- tal, Tabriz, Eastern Azerbaijan, Iran. J Arthropod-Borne Dis, March 2017, 11(1): 166–170 T Hazratian et al.: Pharyngeal Myiasis Caused … 168 http://jad.tums.ac.ir Published Online: March 14, 2017 Case report A 55yr old addicted Iranian man residing in the Shahindeje villages of West Azerbai- jan Province, northern Iran and referred to the Emam Reza Hospital of Tabriz with clin- ical history of Chronic Obstructive Pulmo- nary Disease (COPD) for 4yr was hospital- ized due to respiratory distress, 20 days ago. Urgent treatment was given, including naso- gastric intubation with a mechanical ventila- tor (MV) due to his respiratory distress con- dition. Pulmonary nodules were observed in his lungs following diagnosis, and a CT scan revealed cavities in his lungs. During the na- sogastric intubation procedure, a larva was seen emerging from the patient’s mouth by an ICU staff of the hospital, 30 days after hospitalization. This patient having a clinical history of COPD finally died a few moments later. Laboratory diagnosis was performed in the Entomology Department of the School of Medicine, Tabriz University of Medical Sci- ences. Interestingly, larvae of O. ovis were identified and confirmed following the la- boratory proceedings. Precisely, the larva of O. ovis was identified as follows; the first segment (head) carried a highly sclerotized tissue surrounding the opening of the respir- atory canal followed by 5 rides and two cau- dal swellings. Myiasis of this type has not been previ- ously reported from Tabriz. This case report is the premier report of human pharyngeal myiasis caused by O. ovis. The majority of myiasis cases reported in the literature from Iran were nasal myiasis originating from var- ious areas. The agents of these cases were Chrysomyia bezziana, Lucilia sericata and Er- ystalis tenax (Diptera: Syrphidae), (Youssefi et al. 2012). Lucilia sericata (Diptera: Calli- phoridae) and Ch. bezziana (Diptera: Calli- phoridae) have been identified as causative agents of wound myiasis in Iran (Alizadeh et al. 2014). Ophthalmomyiasis is an infestation of human eyes and orbital tissues with fly larvae belonging to the botfly species of O. ovis, and auricular myiasis is caused by Ch. bezziana and Lu. sericata (Akbarzadeh 2012). However, oral myiasis arises from the infes- tation of obligatory parasitic fly larvae of O. ovis (Diptera: Oestridae) and Wohlfahrtia mag- nifica (Diptera: Sarcophagidae) (Alizadaeh et al. 2014). Ingestion of whole flies leads to intestinal myiasis or accidental myiasis in hu- man. In Iran, two fly species of Sarcophaga haemorrhoidalis and Er. tenax are the main causative agents of intestinal myiasis (Kha- lili et al. 2007, Mandell et al. 2010). Another type of myiasis, the urogenital myiasis, rare- ly occurs in Iran, and two cases of this type have been reported so far in the country in which the larvae of Ch. bezzizna and Wo. Magnifica were detected (Salimi et al. 2010). All nosocomial myiasis infections recorded in Iran are of the nasal type caused by fac- ultative myiasis agents, Lu. sericata (Dip- tera: Sarcophagidae) (Mowlavi et al. 2011). This current study illustrates several in- teresting facts. First, the dwelling of the pa- tient in poor hygienic conditions of a rural setting was a predisposition factor for larval infestation. Second, lack of awareness also contributed to this condition in the patient. Fig. 1. The pair of sharply curved mouth hooks and stout spines of the larva of Oestrus ovis according to the laboratory diagnosis J Arthropod-Borne Dis, March 2017, 11(1): 166–170 T Hazratian et al.: Pharyngeal Myiasis Caused … 169 http://jad.tums.ac.ir Published Online: March 14, 2017 Fig. 2. Posterior spiracles in larvae of Oestrus ovis without 3 distinct slits and not divided into several plates Conclusion This is by our knowledge the first report of an imported case of pharyngeal myiasis caused by O. ovis in northwestern Iran. Myiasis of this type has not been previously reported from Tabriz, and this case of human pharyn- geal myiasis caused by O. ovis is primarily reported for the first time in Iran. The larva belonged to the species of O. ovis according to the morphological characters of larva in which the first segment was characterized by a strongly sclerotized tissue surrounding the outlet of the respiratory canal, completely followed by 5 rides and two caudal swelling. Acknowledgements We would like to thank the staff of Emam Reza Hospital Med laboratory for the provi- sion of the specimen, and we appreciate the contributive effort of Mrs Afsaneh Dowlat- khah in the Department of Parasitology, School of medicine, Tabriz university of Medical Sci- ences. 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