Intestinal Myiasis in a Malaysian Patient Caused by Larvae Of

Home , Clogmia, Tachinidae

Journal of Medical Entomology, 53(4), 2016, 957–960 doi: 10.1093/jme/tjw014 Advance Access Publication Date: 25 April 2016 Short Communication Short Communication

Intestinal Myiasis in a Malaysian Patient Caused by Larvae of Clogmia albipunctatus (Diptera: Psychodidae) Downloaded from https://academic.oup.com/jme/article/53/4/957/2222215 by Murdoch University Library user on 15 December 2020 Aida Syafinaz Mokhtar,1 Kamil Ali Obeid Braima,1 How Peng Chin,2 John Jeffery,1 Siti Nursheena Mohd Zain,3 Mahmud Rohela,1 Yee Ling Lau,1 Ibrahim Jamaiah,1 John-James Wilson,4,5 and Noraishah Mydin Abdul-Aziz1,6

1Department of Parasitology, Faculty of Medicine, University of Malaya, 50603 Kuala Lumpur, Malaysia (aidasyaﬁnaz87@gmail. com; [email protected]; [email protected]; [email protected]; [email protected]; [email protected]; [email protected]), 2Klinik Hope, 29-1, Jalan 4/1, Taman Bukit Serdang, 43300 Seri Kembangan, Selangor, Malaysia (how- [email protected]), 3Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603 Kuala Lumpur, Malaysia ([email protected]), 4Museum of Zoology, Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603 Kuala Lumpur, Malaysia ([email protected]), 5Ecology and Biodiversity Program, Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603 Kuala Lumpur, Malaysia, and 6Corresponding author, e-mail: [email protected]

Received 17 November 2015; Accepted 9 February 2016

Abstract We report a case of human intestinal myiasis in a 41-yr-old female patient presented at a clinic in Seri Kembangan, Selangor, Malaysia. Larvae passed out in the patient’s feces were sent to the Department of Parasitology, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia. DNA barcoding conﬁrmed the second case of intestinal myiasis in Malaysia involving the larvae of Clogmia albipunctatus (Duckhouse) (Diptera: Psychodidae). We review reported cases of myiasis and discuss the present case of intestinal myiasis in an urban patient.

Key words: DNA barcoding, intestinal myiasis, Clogmia albipunctatus, Malaysia

Clogmia albipunctatus (Duckhouse) is a cosmopolitan fly belonging after she cleaned up, postdefecation. She was prescribed albendazole to the family Psychodidae and is one of the medically important in- (oral tablets) for three consecutive days as a treatment for helminth- sects associated with urban environments (Smith and Thomas iasis. Physical and systemic examinations were unremarkable, and 1979). Psychodid larvae can cause myiasis in humans through infest- she was well following the treatment. However, the patient travels ation of healthy or traumatized tissues (Hall and Smith 1993). frequently. The following relevant information was volunteered: the Human myiasis can be presented in various forms with cutaneous case occurred following a field excursion during which the patient myiasis the most common form (Tu et al. 2007). Other infestation consumed a meal in an area infested by flies. Following this, she sites include nasal, aural, pulmonary, ophthalmic cavities, body cav- experienced a brief, severe, abdominal colic associated with cold ities, and the gastrointestinal and urogenital systems (Tu et al. 2007, sweats on 4th February. The symptoms were transient and resolved El-Badry et al. 2014). Intestinal myiasis may result from accidental spontaneously. On 26th March 2015, the patient presented again at ingestion of larvae. Subsequently, this form of myiasis presents the clinic with a similar complaint: a “worm” was found on the toi- symptoms such as nausea, vomiting, abdominal pain and distention, let floor after cleaning herself. This time, she brought the “worm” loss of appetite, weight loss, and episodic diarrhea (Ramana 2012). to the clinic. However, a stool specimen was not provided for exam- This is the second reported case of human intestinal myiasis in ination. She was treated again with albendazole. The patient re- Malaysia caused by larvae of C. albipunctatus. Microscopic examin- covered without further complications. The collected “worm” was ation revealed the structure of the larvae and DNA barcoding estab- sent to the Department of Parasitology, Faculty of Medicine, lished the species identity. University of Malaya, Kuala Lumpur, Malaysia, for identification.

Case Report Materials and Methods A 41-yr-old female from an urban area was first seen at the general The University of Malaya Medical Center Ethics Committee (MEC practitioner’s clinic on 18th February 2015 with a complaint of Ref. No. 201312-0608) approved our research protocols involving passing out “worms”. The “worms” were noticed on the toilet floor human subjects. The patient provided written consent for this study.

VC The Authors 2016. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For Permissions, please email: [email protected] 957 958 Journal of Medical Entomology, 2016, Vol. 53, No. 4 Downloaded from https://academic.oup.com/jme/article/53/4/957/2222215 by Murdoch University Library user on 15 December 2020

Fig. 1. Larva of C. albipunctatus from the patient’s feces. (A) Dorsal view of the brown and slender larva. (B) Magnification of dorsal view of the head. (C) Magnification of lateral view of segments. (D) Magnification of the tail showing sclerotized breathing tube (Online figure in color).

The larval specimen was examined under a stereomicroscope (Thomas et al. 1980, Baharuddin et al. 1995, Ahmad et al. 2009), T. (Fig. 1) and identified as a psychodid larva. As identification of flies albipunctatus (¼Clogmia albipunctatus)(Smith and Thomas 1979), at larval stages is considered inconclusive using morphological char- Eristalis spp. (Lee 1989), Hermetia illucens (L.) (Lee et al. 1995), acteristics, DNA barcoding (Ratnasingham and Hebert 2013) was and Lucilia cuprina (Weidemann) (Nazni et al. 2011) flies were used to establish the species identity of the specimen. DNA was ex- among the causative species. tracted from the whole specimen using a NucleoSpin Tissue kit Reid (1953) documented the first case of human myiasis (cutane- (Macherey-Nagel, Germany) and a fragment of cytochrome c oxi- ous myiasis) in Malaysia caused by the Old-World screw-worm fly, dase subunit 1 mitochondrial DNA was amplified using the “Lep” C. bezziana. In 1984, Oothuman and Jeffery (1984) reviewed all primer combinations via polymerase chain reaction (PCR; Wilson known cases of human myiasis and classified the infestations as uro- 2012). Cycle sequencing was performed bidirectionally using the genital, cutaneous, and intestinal myiasis according to Zumpt’s PCR primers. The resulting DNA barcode was uploaded to the (1965) nomenclature. Since then, more cases of human myiasis have Barcode of Life Datasystems (BOLD; Ratnasingham and Hebert been reported, which include oral myiasis (Lee and Cheong 1985, 2013) and is available in the public dataset (BOLD:AAF9305). Roszalina and Rosalan 2002), urogenital myiasis (Lee 1989), aural myiasis (Lee and Yong 1991, Johari and Khanijow 1993, Rohela Results and Discussion et al. 2006, Ahmad et al. 2009), intestinal myiasis (Cheong et al. 1973, Baharuddin et al. 1995, Lee et al. 1995), nasopharyngeal The DNA barcode from the specimen (designated as WO1) demon- myiasis (Lee et al. 2005, Nazni et al. 2011), ophthalmomyiasis strated 98% similarity to a DNA barcode from Tamil Nadu, India (Alhady et al. 2008), and cutaneous myiasis (Rahoma and Latif (named Telmatoscopus (¼Clogmia) albipunctatus) and was nested 2010). within a cluster of DNA barcodes named C. albipunctatus (assigned The life cycle of C. albipunctatus is completed in one to three BOLD BIN Number - BOLD: AAF9305) on a BOLD identification tree (Fig. 2). Using a strict tree-based assignment model (Wilson weeks (Rocha et al. 2011). Larvae of C. albipunctatus can cause et al. 2011), we concluded that the specimen was the larval stage of myiasis (Costa et al. 1998, Tu et al. 2007), or trigger bronchial C. albipunctatus. asthma in people who accidentally inhale fragments of their disinte- Most reported myiasis cases in Malaysia have been attributed to grated body parts (Robinson 1996). The first documented case of infestations of Chrysomya bezziana (Villeneuve) (Reid 1953, human intestinal myiasis due to infestation of T. (¼Clogmia) albi- Ramalingam et al. 1980, Ramalingam 1982, Abu-Bakar et al. 1984, punctatus larvae was by Tokunaga (1953) in Japan. In Malaysia, Lee and Cheong 1985, Johari and Khanijow 1993, Lee et al. 2005, the first case of intestinal myiasis caused by this fly was reported Rohela et al. 2006). In addition, Chrysomya megacephala (F.) was reported by Smith and Thomas (1979) with another report (Abu-Bakar et al. 1984, Lee and Yong 1991), Sarcophaga spp. from several years later Taiwan (Tu et al. 2007). Journal of Medical Entomology, 2016, Vol. 53, No. 4 959

Fig. 2. BOLD identification tree. This tree is produced by a full database sequence identification request in the Barcode of Life Datasystems for the specimen coded W1. The sequence groups closely with those from Tamil Nadu, India, and the species is nested within a cluster of T. (¼Clogmia) albipunctatus (Online figure in color). 960 Journal of Medical Entomology, 2016, Vol. 53, No. 4

We report the fourth documented case of intestinal myiasis in Lee, H. L. 1989. A case of human urogenital myiasis caused by the drone ﬂy Malaysia and the second caused by C. albipunctatus. In the present Eristalis species (Diptera: Syrphidae) in Malaysia. Trop. Biomed. 6: 49–51. case, based on careful history taking by the patient, we postulate the Lee, H. L., and W. H. Cheong. 1985. A case of human oral myiasis caused by patient developed intestinal myiasis due to ingestion of eggs ovi- Chrysomya bezziana Villeneuve, 1914 (Diptera: Calliphoridae) in Malaysia. posited by female flies contaminating her meal during fieldwork. J. Malays. Soc. Health 5: 65–66. Lee, H. L., and Y. K. Yong. 1991. Human aural myiasis. Southeast Asian J. The time interval between the day of ingestion (4th February) and Trop. Med. Public Health 22: 274–275. the day of first larval discharge (18th February) was 14 d. We can Lee, H. L., P. Chandrawathani, W. Y. Wong, S. Tharam, and W. Y. Lim. speculate that the larvae passed in the patient’s feces developed in 1995. A case of human enteric myiasis due to larvae of Hermetia illucens the intestine after ingestion given that larval period of this species

(Family: Stratiomyiadae): First report in Malaysia. Malays. J. Pathol. 17: Downloaded from https://academic.oup.com/jme/article/53/4/957/2222215 by Murdoch University Library user on 15 December 2020 ranges from 12 to 15 d (Williams 1943). However, the patient may 109–111. have had repeated exposure to the eggs or early-stage larvae from Lee, H. L., M. Krishnasamy, and J. Jeffery. 2005. A case of human nasopha- contaminated food that resulted in persistent infestation. It also is ryngeal myiasis caused by Chrysomya bezziana Villeneuve, 1914 (Diptera: noteworthy that the patient is from an urban area, whereas myiasis Calliphoridae) in Malaysia. Trop. Biomed. 22: 87–88. is usually associated with patients from rural areas with poor hy- Nazni, W. A., J. Jeffery, H. L. Lee, A. M. Lailatul, W. K. Chew, C. C. Heo, I. giene and low economic status (Fernandes et al. 2009). Sadiyah, A. M. Khairul, S. K. Heah, and H. H. Mohd. 2011. Nosocomial The present case may serve as a note to physicians to include in- nasal myiasis in an intensive care unit. Malays. J. Pathol. 33: 53–56. testinal myiasis as a possible cause of gastrointestinal disorders. At Oothuman, P., and J. Jeffery. 1984. Human myiasis in Malaysia-a review. J. Malays. Soc. Health 4: 53–56. present, there is no specific treatment for intestinal myiasis; how- Rahoma, A. H., and B. Latif. 2010. Human foot myiasis in Malaysia with a re- ever, purgatives, albendazole, mebendazole, and levamizole were review of the literature. J. Trop. Med. Parasitol. 33: 41–43. ported to cure some patients (Francesconi and Lupi 2012), as seen in Ramalingam, S. 1982. Primary and secondary cutaneous myiasis in Malaysia this case. Preventive measures such as high levels of personal hy- [abstract]. Eighteenth Annual Scientific Seminar–Malaysian Soc. Par. Trop. giene, careful storage of food, and other vector control measures are Med. needed to prevent possible re-exposure. Ramalingam, S., A. Nurulhuda, and L. H. Bee. 1980. Urogenital myiasis caused by Chrysomya bezziana (Diptera: Calliphoridae) in Peninsular Malaysia. Southeast Asian J. Trop. Med. Public Health 11: 405. Acknowledgments Ramana, K. V. 2012. Human Myiasis. J. Med. Microbiol. Diagnosis 1: e105. This study was supported by research grants PG042-2013A, RP003D-13SUS, Ratnasingham, S., and P.D.N. Hebert. 2013. A DNA-based registry for all ani- and UMRG RG509-13HTM from University of Malaya, Kuala Lumpur, mal Species: The Barcode Index Number (BIN) System. PLoS ONE 8: Malaysia, and UM.C/HIR/MOHE/MED/16 from the Ministry of Higher e66213. Education, Malaysia. Reid, J. A. 1953. Notes on house flies and blow flies in Malaya, Kuala Lumpur: Malaya. Bull. Inst. Med. Res. 7: 26. Robinson, W. H. 1996. Fly pests in indoor and household environments, pp. References Cited 293–295. In W. H. Robinson (eds.), Urban entomology: Insect and mite pests in the human environment. Chapman and Hall, London, United Abu-Bakar, E., K. N. Subramaniam, J. Jeffery, and P. Oothuman. 1984. Kingdom. Cutaneous myiasis in a burn case caused by Chrysomya bezziana Rocha, T., J. David, A. de Oliveira, and F. H. Caetano. 2011. Villeneuve, 1914 and Chrysomya megacephala (Fabricius, 1791) (Diptera: Ultramorphological features of the egg of Telmatoscopus albipunctatus Calliphoridae). J. Malays. Soc. Health 4: 18–20. (Williston) (Diptera, Psychodidae). Rev. Bras. Entomol. 55: 179–182. Ahmad, N. W., A. Ismail, J. Jeffery, S. Ibrahim, A. Abdul-Hadi, M. N. Rohela, M., I. Jamaiah, L. Amir, and V. Nissapatorn. 2006. A case of auricular Ibrahim, H. C. Chin, and L. H. Lim. 2009. Aural myiasis in a neonate in myiasis in Malaysia. Southeast Asian J. Trop. Med. Public Health. 37: peninsular Malaysia. Parasit. Vectors 2: 63. 91–94. Alhady, M., K. Zabri, and C. N. Chua. 2008. Ophthalmomyiasis from Roszalina, R., and R. Rosalan. 2002. Oral myiasis: case report. Malaysian J. Chrysomyia bezziana (Screwworm Fly). Med. J. Malaysia 63: 269–270. Med. Sci. 9: 47–50. Baharuddin, O., S. H. Ting, and I. Zulkifli. 1995. A case of intestinal myiasis in Smith, K. G., and V. Thomas. 1979. Intestinal myiasis in man caused by larvae a baby caused by flesh fly (Diptera: Sarcophagidae). Trop. Biomed. 12: 95. Cheong, W. H., S. Mahadevan, and K. J. Lie. 1973. A case of intestinal myiasis of Colgmia (¼Telmatoscopus) albipunctatus Williston (Psychodidae, in Malaysia. Southeast Asian J. Trop. Med. Public Health 4: 281. Diptera). Trans. R. Soc. Trop. Med. Hyg. 73: 349–350. Costa, J.M.L., L. S. Melo, I. Figueiredo, R. Cipriano, S. L. Sousa, F. Thomas, V., K. G. Smith, and J. P. Dear. 1980. Dermal myiasis in man caused Fernandes, and M. L. Rodrigues. 1998. Leishmaniose cutanea^ difusa (Lcd) by Sarcophaga krameri (Boettcher) (Diptera: Sarcophagidae) in Malaysia. no estado do Maranhao,~ Brasil: relato de dois casos novos. Rev. Soc. Bras. Southeast Asian J. Trop. Med. Public Health 11: 140. Med. Trop. 31: 114–220. Tokunaga, M. 1953. Moth-flies that cause myiasis in man in Japan. Jpn. J. El-Badry, A. A., H. K. Salem, and Y. A. El-Aziz Edmardash. 2014. Human Sani. Zool. 4: 101–107. urinary myiasis due to larvae of Clogmia (Telmatoscopus) albipunctata Tu, W. C., H. C. Chen, K. M. Chen, L. C. Tang, and S. C. Lai. 2007. Intestinal Williston (Diptera: Psychodidae) first report in Egypt. J. Vector Borne Dis. myiasis caused by larvae of Telmatoscopus albipunctatus in a Taiwanese 51: 247–249. man. J. Clin. Gastroenterol. 41: 400–402. Fernandes, L. F., F. C. Pimenta, and F. F. Fernandes. 2009. First report of human Williams, F. X. 1943. Biological studies in Hawaiian water-loving insects-Part myiasis in Goias state, Brazil: frequency of different types of myiasis, their vari- III Diptera or Flies-C, Tipulidae and Psychodidae. Proc. Hawaiian Entomol. ous etiological agents, and associated factors. J. Parasitol. 95: 32–38. Soc. 11: 313–338. Francesconi, F., and O. Lupi. 2012. Myiasis. Clin. Microbiol. Rev. 25: Wilson, J. J. 2012. DNA barcodes for insects. Method Mol. Biol. 858: 17–46. 79–105. Wilson, J. J., R. Rougerie, J. Shonfeld, D. H. Janzen, W. Hallwachs, M. Hall, M.J.R., and K. G. Smith. 1993. Diptera causing myiasis in man, pp. Hajibabaei, I. J. Kitching, J. Haxaire, and P.D.N. Hebert. 2011. When spe- 429–469. In R. P. Lane and R. W. Crosskey (eds.), Medical Insects and cies matches are unavailable are DNA barcodes correctly assigned to higher Arachnids. Chapman and Hall, London, United Kingdom. taxa? An assessment using sphingid moths. BMC Ecol. 11. Johari, S., and V. K. Khanijow. 1993. A case of aural myiasis caused by Zumpt, F. 1965. Myiasis in man and animals in the Old World: A textbook Chrysomya bezziana Villeneuve, 1914 (Diptera: Calliphoridae), the old for physicians, veterinarians and zoologists. Butterworths and Co. Ltd, world screw worm. Trop. Biomed. 10: 149–152. London, United Kingdom.