Transactions of the Royal Society of Tropical Medicine and Hygiene (2005) 99, 914—918
Unusual cases of human myiasis due to Old World screwworm fly acquired indoors in Hong Kong J.C.M. Chan a, J.S.W. Lee b,∗, D.L.K. Dai c, J. Woo d a
Department of Medicine, Alice Ho Miu Ling Nethersole Hospital, Tai Po, New Territories, Hong Kong SAR, China b Department of Medicine and Geriatrics, Tai Po Hospital, Tai Po, New Territories, Hong Kong SAR, China c Department of Medicine and Therapeutics, Prince of Wales Hospital, Shatin, New Territories, Hong Kong SAR, China d Department of Medicine and Therapeutics, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong SAR, China Received 25 February 2005 ; received in revised form 20 June 2005; accepted 23 June 2005 Available online 8 September 2005 KEYWORDS Myiasis; Chrysomya bezziana; Nosocomial infestation; Oral hygiene; Hong Kong
Summary Myiasis is the infestation of tissue by the larvae of flies. We report eight cases of human myiasis in Hong Kong. All patients were nursing home residents with an average age of 81.8 years. Seven patients were bedridden with advanced dementia. Four patients had pre-existing wounds. Five had poor oral hygiene and four of those were on tube feeding. All of the five patients with poor oral hygiene suffered from oral myiasis. Two patients had vaginal infestations and one had wound myiasis in his diabetic foot ulcer. Seven cases were infested by Chrysomya bezziana, an obligatory parasite that requires living mammalian tissue for its larval development. Larvae of the Calliphoridae family were responsible for the remaining case. Patients were managed with manual removal of larvae and irrigation of the site of infestation with saline. All infestations were nosocomial, being acquired in nursing homes. Carers of the old and debilitated should be made aware of the need for better oral care, especially for those on tube feeding. The use of window screens in nursing homes should be encouraged to reduce the chance of flies entering the vicinity of these patients. Electrocuters could also be mounted indoors to kill flies that do enter. © 2005 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved.
1. Introduction ∗
Corresponding author. Tel.: +852 2607 6111; fax: +852 2468 5800. E-mail address: jleesw
[email protected] (J.S.W. Lee).
Myiasis is caused when fly larvae invade living tissue or when they are harboured in the nasopharyngeal, gastric or urogenital tracts (White, 2003). Larvae
0035-9203/$ — see front matter © 2005 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.trstmh.2005.06.020
Unusual cases of human myiasis
can generally be divided into benign (eating only dead tissue) or malignant (eating healthy tissue), but in some cases a benign infestation can become malignant, for example if all dead tissue is consumed. Symptoms range from mild itch at the site of larvae penetration to painful ulcers and furuncles. The commonest sites of infestation are wounds and body orifices.
1.1. Types of myiasis Myiasis can be classified according to the site of infestation, for example cutaneous tissues and body cavities including the gut lumen. It can also be classified into three different groups emphasising different host relationships: obligatory myiasis, facultative myiasis and accidental myiasis. Obligatory myiasis requires a living host (humans, domestic or wild vertebrates) for the development of the larval stages (e.g. human botflies Dermatobia hominis, Old World screwworm flies Chrysomya bezziana, and some species of sarcophagid flies, for example Wohlfahrtia magnifica). Facultative myiasis is caused by flies that normally lay eggs in decaying animal tissues (e.g. blow flies Calliphora), but occasionally lay eggs on open wounds or orifices, especially when these are necrotic and malodorous. This had led to their use in maggot debridement therapy (Sherman et al., 2000). Accidental myiasis implies the accidental ingestion of eggs or larvae, which may survive for a period in the gastrointestinal tract (e.g. house fly Musca domestica).
1.2. Myiasis in Hong Kong Chrysomya bezziana, also called the Old World screwworm fly, merits special discussion because it is endemic in the southern Asia Pacific region. It feeds on and invades healthy mammalian tissue, occasionally leading to death of the host. Hundreds of eggs can be laid by a single female. The larva leaves the host after 5—7 days and falls to the ground where it pupates. The whole life cycle lasts for approximately 24 days. Human infestation is uncommon, but may occur with outbreaks in dogs, pigs and cattle in rural areas (Goddard, 2000). Human infestation is rare in urban indoor circumstances. In Hong Kong, myiasis caused by C. bezziana has been reported both in stray and pet dogs in recent years (Chemonges-Nielsen, 2003). The first case of human infestation in Hong Kong was reported in 2003 (Ng et al., 2003). As of January 2005, a total of 21 sporadic human cases of myiasis due to C. bezziana had been reported to the Department of Health in Hong Kong. The age ranged from 49 years to 90 years, with a median of
915
79 years. Among these, 62% were bedridden older nursing home residents, and 48% were on nasogastric tube feeding. Seven of the eight cases reported here belong to this series.
2. Methods Cases of human myiasis reported to the local hospital authority between April 2002 and November 2003 were included. Demographic characteristics, co-morbidities, sites involved, species of maggots identified, management and clinical outcomes were recorded. Apart from the first case, which was diagnosed prior to the set up arrangement with the government laboratory, all larvae were sent to the microbiology laboratories of the corresponding hospitals and also to the laboratory of the Pest Control Advisory Section of the Hong Kong Food and Environmental Hygiene Department for identification. Larvae of C. bezziana were identified by anatomical features: open peritreme of the posterior spiracle and four to five lobes on the anterior spiracles. Some of the larvae were allowed to form pupae and later hatched into mature flies that were identified as C. bezziana. No adult fly identification was done for the first case.
3. Results Eight cases of human myiasis were identified in Hong Kong between April 2002 and November 2003. All patients were nursing home residents. The mean age was 81.8 years (range 69—96 years). Except for one patient who had diabetes, all were bedridden with advanced dementia. None of our patients had peripheral vascular diseases. Patient characteristics, presentation and management are presented in Table 1. None of the patients were reported to have any close contact with animals. As they were all nursing home residents, the exposure was defined as nosocomial. The oral cavity was the commonest site of infestation in our series (five of eight cases). Two patients had vaginal myiasis. Another patient had larvae identified in his gangrenous diabetic foot ulcer. Seven of the eight patients were infested by the larvae of C. bezziana. For the first patient, the larvae were identified to be of the Calliphoridae family, of which C. bezziana is a member. All patients received local treatment for the ulcers or wounds, including careful manual removal of maggots and wound irrigation with normal saline. Antibiotics were given for concomitant infections.
916
Table 1
Cases of human myiasis in Hong Kong between April 2002 and November 2003
Age (years)/ sex
Time of presentation
Co-morbidities
Functional status
Pre-existing wounds
82/F
April 2002
Dementia, suspected Ca uterus
Bedridden
Perineal ulcer
89/F (Ng et al., 2003)
September 2002 Old stroke, dementia, poor oral hygiene October 2002 Old stroke, dementia, poor oral hygiene October 2002 Dementia, poor oral hygiene
Bedridden, tube fed
77/F
November 2002
Bedridden, tube fed
79/F
71/M
September 2003 Hypertension, fractured femur, dementia October 2003 Diabetes, blind
Ambulatory
96/M
November 2003
Bedridden
69/F
88/M
Dementia, poor oral hygiene
Ca prostate, dementia, poor oral hygiene
Bedridden, tube fed
Bedridden, tube fed
Post-menopausal bleeding, larvae infested ulcerated growth anterior to anus, pus discharging from vagina, fever None Larvae found in mouth during routine oral care in hospital Oral ulcer Gum bleeding with multiple palate and oral ulcers None Larvae found during mouth care, large hard palate ulcer (CT showed extensive tissue damage and erosion to bone and teeth) None Larvae emerged from small opening in skin of supraclavicular fossa and bleeding gum Sacral bed sore Incidental finding of larvae on diaper and perineum Foot ulcer Gangrenous toe with foul-smelling discharge and fever, larvae found in toe web space
None
Site maggots found
Species of maggots
Management
Outcome
Perineal ulcer
Calliphoridae family
Saline irrigation of wound, manual removal of larvae, course of ampicillin
Discharged
Palate, jaw
Chrysomya bezziana Debridement by dental surgeon, manual removal of larvae Chrysomya bezziana Debridement by dental surgeon
Died of pneumonia subsequently
Palate, jaw
Chrysomya bezziana Debridement by dental surgeon, 90 larvae removed
Discharged
Palate, subclavian sinus
Chrysomya bezziana Wound irrigation with saline
Died of pneumonia
Perineum, labia majora
Chrysomya bezziana Manual removal of larvae, irrigation with saline Chrysomya bezziana Intravenous ampicillin and cloxacillin, surgical debridement and toe amputation, more larvae removed intraoperatively within wound Chrysomya bezziana Manual removal of larvae, intravenous broad-spectrum antibiotics
Discharged
Palate, jaw
Foot
Hard palate, Fever with ulcerated hard palate (CT showed maxillary sinuses air locules around maxilla and mandibles), blood culture grew Group G streptococci
Discharged
Discharged
Died of pneumonia 5 days after admission
J.C.M. Chan et al.
F: female; M: male; Ca: carcinoma.
Bedridden, tube fed
Presenting symptoms
Unusual cases of human myiasis
Four patients received surgical management of their wounds: surgical debridement of the palate and oropharynx in three patients and toe amputation for the patient with diabetic foot gangrene. Three of the eight patients died of pneumonia shortly after admission. The remaining five patients survived and were discharged.
4. Discussion All of our cases were nursing home residents, with advanced age and debilitated conditions. Seven of our eight cases were bedridden with dementia. They were not dissimilar to children with myiasis in developing areas who were also dependent on others to maintain their own hygiene (Jiang, 2002). In the United States, homelessness and alcoholism were the commonest patient characteristics and most patients were middle-aged (Sherman et al., 2000). In Hong Kong, institutionalised older persons who cannot take care of their own hygiene, especially their oral care, are at risk of suffering from myiasis due to C. bezziana, as evidenced by the high prevalence of debilitated nursing home residents among reported cases in Hong Kong. Myiasis has not yet been reported among younger adults, perhaps due to the general awareness of personal hygiene. Infants in Hong Kong, although also unable to care for their own hygiene, usually receive good care from their parents, thus reducing their risk of myiasis. Co-morbid conditions such as diabetes and peripheral vascular disease were highly prevalent in two American and Australian series (Lukin, 1989; Sherman et al., 2000). However, only one of eight patients in our series had diabetes. Psychiatric illness and cognitive impairment were associated factors in our series as well as in a Sri Lankan series (Kumarasinghe et al., 2000). Myiasis has been reported both in urban and rural areas around the world, but mostly in rural outdoor circumstances (Jiang, 2002; Lukin, 1989; Sherman et al., 2000). Myiasis occurring in an urban indoor situation is unusual. The proportion of nosocomial infestations, defined as infestations acquired inside an institution, ranges from 5% to 43% (Lukin, 1989; Sherman et al., 2000). Hong Kong has a warm climate and windows are often left open in the warmer months in many institutions for the elderly. It is probable that adult, gravid female flies gained access to open wounds or orifices of the patients in this study via open windows. Chrysomya bezziana is an obligatory parasite and requires living animal tissue for larval development. Dogs in the city have
917
been reported to suffer from C. bezziana myiasis and it is possible that they, or other stray animals, can serve as urban reservoir hosts for this zoonosis (Chemonges-Nielsen, 2003). The most common sites of involvement in human myiasis are the skin, wounds, eyes and ears (Jiang, 2002; Lukin, 1989; Sherman et al., 2000). Oral myiasis was rare in previous studies. It has been associated with poor dental hygiene, mental handicap and inability to close the mouth (Al-Ismaily and Scully, 1995; Bhatt and Jayakrishnan, 2000; Gursel et al., 2002). Among the 21 cases reported so far in Hong Kong, 11 (52.4%) have involved the oral cavity. The high prevalence of oral myiasis in our series, together with poor oral hygiene and the use of nasogastric feeding tubes, highlights the need for better dental care for debilitated older persons. Education regarding the importance of oral care in the institutionalised, even if they are on non-oral feeding, should be promoted among nursing staff. Vaginal myiasis in our series was likely to be secondary to nearby wounds (sacral sore in one and pus discharging from carcinoma of the corpus in another). Calliphora was responsible for the majority of cases in a North American and an Australian series of human myiasis (Lukin, 1989; Sherman et al., 2000). Our series involved mostly C. bezziana, the Old World screwworm fly, which is endemic in the Afrotropical and Asia Pacific regions, including southern China but excluding Australia (Goddard, 2000). It is the only animal myiasis reported in the epidemiology report of the Agriculture, Fisheries and Conservation Department in Hong Kong and has been reported to have caused aggressive myiasis among pet dogs in the city in the recent years (Chemonges-Nielsen, 2003). Human myiasis is usually most common during the warmer months of the year, late spring to autumn, when adult flies are most active. All our cases presented during the warmer months, between April and November.
5. Conclusions and recommendations Human myiasis is largely a rural disease. Occurrence, as reported here, in an urban indoor situation among institutionalised older persons calls for the need to improve wound and dental care for debilitated persons, especially those on longterm tube feeding and those who may not be able to close their mouth completely. Window and door screens should be promoted in nursing homes, and insect electrocuting devices could also be used to kill flies indoors. Stray dogs should be reported to
918
the authorities for control, and pet dogs should be examined regularly by their owners for signs of myiasis, which should be treated by veterinary surgeons. Conflicts of interest statement The authors have no conflicts of interest concerning the work reported in this paper.
Acknowledgements We would like to thank Dr Daisy Dai, Hospital Authority Head Office, for providing information on the four patients with myiasis in 2002, and to Drs Mamie Hui and Edmond Lam of the Prince of Wales Hospital in Hong Kong for providing information on the first two cases in our series.
References Al-Ismaily, M., Scully, C., 1995. Oral myiasis: report of two cases. Int. J. Paediatr. Dent. 5, 177—179.
J.C.M. Chan et al.
Bhatt, A.P., Jayakrishnan, A., 2000. Oral myiasis: a case report. Int. J. Paediatr. Dent. 10, 67—70. Chemonges-Nielsen, S., 2003. Chrysomya bezziana in pet dogs in Hong Kong: a potential threat to Australia. Aust. Vet. J. 81, 202—205. Goddard, J., 2000. Physician’s Guide to Arthropods of Medical Importance, third ed. CRC Press, Boca Raton, FL. Gursel, M., Aldemir, O.S., Ozgur, Z., Ataoglu, T., 2002. A rare case of gingival myiasis caused by diptera (Calliphoridae). J. Clin. Periodontol. 29, 777—780. Jiang, C., 2002. A collective analysis on 54 cases of human myiasis in China from 1995—2001. Chin. Med. J. 115, 1445—1447. Kumarasinghe, S.P., Karunaweera, N.D., Ihalamulla, R.L., 2000. A study of cutaneous myiasis in Sri Lanka. Int. J. Dermatol. 39, 689—694. Lukin, L.G., 1989. Human cutaneous myiasis in Brisbane: a prospective study. Med. J. Aust. 150, 237—240. Ng, K.H.L., Yip, K.T., Choi, C.H., Yeung, K.H., Auyeung, T.W., Tsang, A.C.C., Chow, L., Que, T.L., 2003. A case of oral myiasis due to Chrysomya bezziana. Hong Kong Med. J. 9, 454—456. Sherman, R.A., Hall, M.J., Thomas, S., 2000. Medicinal maggots: an ancient remedy for some contemporary afflictions. Annu. Rev. Entomol. 45, 55—81. White, B.G., 2003. Ectoparasites: leeches and leech infestation, myiasis, jigger fleas, scabies, louse infestation, in: Cook, G.C., Zumla, A. (Eds), Manson’s Tropical Diseases, 21st ed. Saunders, London, pp. 1599—1610.