|Year : 2012 | Volume
| Issue : 3 | Page : 332-337
US Udgaonkar1, R Dharamsi2, SA Kulkarni1, SR Shah1, SS Patil1, AL Bhosale1, SA Gadgil1, RS Mohite1
1 Department of Microbiology, Bharati Vidyapeeth Deemed University Medical College and Hospital, Sangli, Maharashtra, India
2 Dharamsi Hospital, Super-speciality centre for digestive diseases, India
|Date of Submission||17-Apr-2012|
|Date of Acceptance||16-Jul-2012|
|Date of Web Publication||8-Aug-2012|
U S Udgaonkar
Department of Microbiology, Bharati Vidyapeeth Deemed University Medical College and Hospital, Sangli, Maharashtra
Source of Support: None, Conflict of Interest: None
Purpose: Intestinal myiasis is a condition when the fly larvae inhabit the gastrointestinal tract and are passed out in faeces. This type of infestation results when eggs or larvae of the fly, deposited on food are inadvertently taken by man. They survive the unfavourable conditions within the gastrointestinal tract and produce disturbances, which may vary from mild to severe. The condition is not uncommon and is often misdiagnosed as pinworm infestation. Correct diagnosis by the clinical microbiologist is important to avoid unnecessary treatment. Materials and Methods: We had 7 cases of intestinal myiasis. In 2 cases the larvae were reared to adult fly in modified meat and sand medium (developed by Udgaonkar). This medium is simple and can be easily prepared in the laboratory. Results: Of the 7 larvae, 5 were Sarcophaga haemorrhoidalis, 1 Megaselia species and 1 was identified as Muscina stabulans. Conclusions: S. haemorrhoidalis was the commonest maggot involved. A high index of suspicion is required for clinical diagnosis when the patient complains of passing wriggling worms in faeces for a long period without any response to antihelminthics. The reason for long duration of illness and recurrence of infestation is baffling. The nearest to cure was colonic wash. We feel prevention is of utmost importance, which is to avoid eating food articles with easy access to flies.
Keywords: Enteric myiasis, intestinal myiasis, Megaselia, Muscina stabulans, Sarcophaga haemorrhoidalis
|How to cite this article:|
Udgaonkar U S, Dharamsi R, Kulkarni S A, Shah S R, Patil S S, Bhosale A L, Gadgil S A, Mohite R S. Intestinal myiasis. Indian J Med Microbiol 2012;30:332-7
|How to cite this URL:|
Udgaonkar U S, Dharamsi R, Kulkarni S A, Shah S R, Patil S S, Bhosale A L, Gadgil S A, Mohite R S. Intestinal myiasis. Indian J Med Microbiol [serial online] 2012 [cited 2019 Jul 24];30:332-7. Available from: http://www.ijmm.org/text.asp?2012/30/3/332/99496
| ~ Introduction|| |
The term 'myiasis' now in general use was coined by Reverend F. W. Hope in 1880 to refer to a disease resulting from invasion of living tissue of man or animals by dipterous fly larvae resulting in disturbances. This was different from those caused by other insect larvae, termed "Scholechiasis."  Myiasis covers a variety of association between dipterous larvae and mammals. The most comprehensive definition is: "the infestation of live human and vertebrate animals with dipterous larvae, which at least for certain period, feed on the host's dead or living tissue, liquid body substances or ingested food." Intestinal myiasis is diagnosed from the presence of larvae in faeces or vomitus. Obligatory gut parasite of animals will not develop in humans and therefore species that cause intestinal myiasis are facultative or accidental parasites.
Myiasis is classified clinically into cutaneous myiasis involving wounds, body cavity myiasis involving nasopharynx, eyes, auditory canal and myiasis involving internal organs principally gut lumen and urogenital system. From medical standpoint, the clinical classification is more important because it aids in diagnosis and identification of species responsible. The parasitological classification is the obligate, facultative and accidental myiasis based on host-parasite relationship. It assists in understanding the biological background and hence the possible methods of prevention and control. Obligate myiasis producing larvae feed on living tissue. Facultative myiasis larvae feed on carrion usually but may invade the body when there is prior infestation, e.g., myiasis of wounds. In accidental myiasis, eggs or the larvae are ingested accidentally with food, not killed in the GI tract and passed out in faeces.  Intestinal myiasis is often mistaken for pinworm infestation and treated. However, the condition does not respond to antihelminthics. For correct laboratory diagnosis, careful macroscopic examination of fresh stool specimen, without contamination, is important.
| ~ Materials and Methods|| |
We had 7 patients who gave history of passing maggots for a period varying from few months to several years. Their average age was around 25-38 years. There were 6 male patients and 1 female patient.
The excretion of maggots was intermittent, so patients were asked to come when they were passing worms. They were instructed to collect stool specimen in a wide-mouthed clean stool container in the laboratory toilet instead of bringing it fromth home. This was not easy but was insisted upon.
The macroscopic as well as microscopic examination of stool did not show any abnormal finding. But when the container was left open for some time and the stool specimen raked a bit, the wriggling maggots emerged on the surface. Most of the times there were 4 to 5 maggots present. They were pearly white in colour, about 3 mm × 1 mm in size and segmented. Twelve segments could be counted under the scanner of a light microscope. Each segment was lined with fine hair-like structure. The anterior end had a pair of black-coloured hooks [Figure 1]. The segmented forward movement was very characteristic. The maggots were killed using hot water  and preserved in 10% formalin.
|Figure 1: Microphotograph of the anterior end of Muscina stabulans showing the cephalo-pharyngeal skeleton with 2 hooks. [×100 Olympus binocular microscope]|
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The posterior end was manipulated, mounted on a slide and examined under microscope with ×10 and ×40 objectives. For the fifth case, we left 2 of the larvae in the stool container for about 2 days to develop to third instar stage of development. During this period, the larvae increased in size from 3 mm × 1 mm to 15 mm × 4 mm. After killing the larvae, the posterior end was dissected transversely with a sharp new scalpel and mounted on a slide to observe the posterior spiracles situated at posterior end of the larva. They are useful diagnostic characters. It has a sclerosed outer ring, the peritreme. Within the peritreme the spiracular slits are placed. The slits are organs of respiration and their numbers indicate the stage of larva. They are 1 or 2 in the first instar, 2 in the second instar and 3 in the third instar larva. The morphology and arrangement of the spiracular slits whether slender, straight, curved, parallel or divergent etc. are important distinguishing features. The other feature is the presence or absence of "button," whether the peritreme encloses the button or not. Button is the prominence present within the peritreme and has taxonomic value in species identification  [Figure 2], [Figure 3]. On the basis of these results, a presumptive identification of larvae was done in our laboratory. In the fifth and sixth case the larvae were also reared to adult fly. The larvae and fly were both sent for identification.
|Figure 2: Two larvae of Sarcophaga haemorrhoidalis. The posterior end of the 1 on the left is cut to examine the posterior spiracle|
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|Figure 3: Third instar larva of S. haemorrhoidalis showing 3 slits in the posterior spiracle. Arrow shows 1 slit. (×100 Olympus binocular microscope)|
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Rearing of larvae was done in modified meat and sand medium, which we had developed in our laboratory. The medium had meat pieces of Robertson cooked meat medium on top of about 3 inches heighted moist sand, in a used empty blood culture bottle. The mouth of the bottle was covered with cotton wrapped in gauze and sterilized in a laboratory autoclave. The larvae were picked very carefully with a thin wooden stick and dropped into the medium. It was then left at room temperature. After about a week the medium was observed daily for the emergence of flies. The larvae sank into the meat, fed on them, later buried in sand to pupate till the fly hatched out [Figure 4]. It took around 12 to 14 days for the larvae to develop to adult. Once the fly was reared, the top of the bottle was covered with a polythene bag. The cotton top was slid open to release the fly carefully into the polythene bag and caught [Figure 5]. The fly got killed in a day when left in the closed polythene bag itself. The larvae and 2 adult flies were sent out for final identification and confirmation of species. The larvae were transported in formalin and the adults in a small plastic container.
|Figure 5: The medium with plastic cover. The top plug is slid open to catch the fly|
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| ~ Results and Details of Clinical Cases|| |
Our first patient was a 25-year-old engineer who was presented with a history of passing worms for 5 years. He complained of flatulence, generalised pain in abdomen, mild tenderness all over the abdomen, gastrointestinal disturbances and diarrhoea. He was treated by many physicians for suspected pinworm infestation. The colonoscopy showed mildly congested colon and superficial ulcers. Worms were seen sticking to colonic mucosa and within the lumen. He was relieved of his symptoms after colonic wash.
The second case was a 35-year-old bank employee, who was passing worms in stool for more than 3 years. He complained of indigestion, flatulence and an uncomfortable feeling over abdomen. He became epileptic later and was also operated for appendicitis. After colonic wash, his GI symptoms and myiasis were abated. He was put on antiepileptic treatment and was lost to further follow-up.
The third case was a 28-year-old robust police constable who came with vague abdominal symptoms, indigestion, flatulence and burning sensation all over body. He was passing "worms" in his faeces for a month. No specific treatment was given. However, we lost him to follow-up.
The fourth patient was a 30-year-old farmer with a history of passing "worms" for 3 months. He complained of general weakness and was found to be anaemic with haemoglobin of 7 g%. He had a history of abdominal pain, gastrointestinal disturbances and flatulence. He used to defecate in open fields.
The fifth case was a teacher aged 38 years. He had recently changed his occupation and started working in his farm. He was passing "worms" for the past 6 months and complained of abdominal pain, GI disturbances and flatulence. His routine investigations did not show any abnormality. The abdominal sonography report was portal hypertension and gastropathy. The gastric biopsy showed areas of congestion and ulcers . The fresh stool examination showed 4 wriggling worms. Two of the larvae were reared to adult in our laboratory in the modified meat and sand medium.
All larvae were identified and confirmed as those of S. haemorrhoidalis except the fourth case in which the report was Sarcophaga species.
The sixth case was a 27-year-old housewife having 3 children who had been passing "worms" for the last 6 years. She had undergone hysterectomy for chronic cervicitis and came with vague pain all over abdomen, especially in the right upper abdomen with loss of appetite and indigestion. The larvae recovered were reared to adult stage and identified as that of Megaselia spp.
The seventh patient was a farmer, aged 35, who was thin built, and was symptom-free except for some vague abdominal discomfort. He was very apprehensive and worried about his condition. His haemoglobin was 11 g%. The stool examination revealed 5 larvae, identified as second instar of Muscina stabulans [Figure 6]. The repeat stool examination after 4 days also showed larvae with same type of posterior spiracle.
The identifications were done by using standard keys by Soulsby in 1982. 
All patients were treated with colonic wash, using oral polyethylene glycol (PEG), 137.15 g dissolved in 2 L of water. The patients were asked to drink it within a period of 2 hours. This produced 4 to 5 bowel movements over the next few hours. To prevent further attack, the patients were counselled against eating out, especially uncovered food articles accessible to flies. With all said and done our gastroenterologist, one of the authors, is of the opinion that after some time period, few of these patients come back with recurrence.
| ~ Discussion|| |
When the intestinal tract is invaded by fly maggots, the condition is called intestinal myiasis. The condition is known as gastric myiasis when the stomach is involved. The invasion of the digestive tract in general is called enteric myiasis, a term that can be used to include both gastric and intestinal myiasis. 
Around 50 species of fly larvae have been reported either positively or questionably, from cases of enteric myiasis. These species are principally members of the families Muscidae, Calliphoridae and Sarcophagidae, which commonly deposit their eggs or larvae on cold meat, cheese and other food of man and are thus ingested, may be swallowed with contaminated food, pass through intestine unaffected and excreted in faeces. 
The posterior spiracle is important for the species identification. , While trying to manipulate the posterior end to visualise the spiracles, the fragile larvae used to be damaged at times. Hence in our fifth patient, we left the 2 larvae in the stool container itself for 2 days. The larvae developed in size from 3 mm to 15 mm. We could thereafter dissect the posterior end easily to examine the spiracles.[Figure 2], [Figure 3]
The identification is also facilitated by rearing the larva to adult stage. The method described in the textbook used raw meat.  The sterility of raw meat obtained from market was questionable, so we modified the medium and replaced raw meat with meat pieces of Robertson cooked meat medium. The medium worked well for us.
S. haemorrhoidalis was the commonest fly maggot in our cases and has been reported by others in India. ,,[ 9] Reports of intestinal myiasis from Japan caused by Sarcophaga peregrina, Hermetia illucens and Sarcophaga crassipalpis are available in literature. The latter was also thought to be a carrier of Salmonella More Details enteritidis in patients. 
The larvae of M. stabulans found in 1 of our patients have been reported from India , and abroad. ,, The female of M. stabulans is capable of passing 140-200 eggs on food. 
Megaselia larva from 1 of our patients was reared to adult and identified. Though not a common cause of intestinal myiasis, it is reported in literature. ,
The other species involved commonly are the little house fly (Fannia canicularis), the latrine fly (Fannia scalaris), the cheese skipper fly (Piophila casei), the black soldier fly (H. illucens), Tubifera tenax, Musca domestica and Eristalis tenax, all of which have been reported as causative agents of human intestinal myiasis. ,,,, The age of our patients ranged from 25 to 38 years but there is no age bar for intestinal myiasis. Intestinal myiasis in a 1-year-old child by M. stabulans was reported from CDC, Atlanta. The child's dietary history revealed that she was fed overripe banana, kept hanging in a wire basket. Flies were often seen around the fruits. Here, no treatment was prescribed. The parents were advised to cover the fruits and wash them before consumption. 
Another case of infantile intestinal myiasis in an 8-month-old girl was reported from Japan. The child had become irritable and was passing blood mucus in stool along with worms. The worms were larvae of S. peregrina. 
The infestation can be very obstinate. A case of intestinal myiasis was described by Herms and Gilbert early in 1930, in a lady with recurrent attacks of nausea, vomiting, nervousness and blood in stools. She was hospitalized, observed, and was given Santonin by mouth and colonic irrigation with Thymol. Tetrachloroethylene capsule given orally caused gastric distress, so it was given through a tube manipulated beyond the stomach. Many larvae were recovered from the faeces. There was improvement for few weeks but the attacks recurred. Three lots of fly larvae were studied. Adults of 3 genera Calliphora, Phaenicia (Lucilia) and Sarcophaga were reared from these larvae. She improved apparently for few weeks but symptoms recurred violently with evacuation of larvae through vomitus and stools. Recurrence was attributed to repeated infestation, the patient's poor health condition and apparent sensitivity to infestation.  The author's suggestion of paedogenesis (larvae reproducing larvae) was, however, not substantiated.  Both Santonin and tetrachloroethylene are outdated drugs with toxic side effects, they are no more used.
Flies have been reported to even deposit eggs near anus particularly where old fashioned privies are used. The larvae on hatching may make their way to intestine. Parasitism of this type appears to last long. Several authentic cases caused by Eristalis, which commonly lives in sewages have been reported.  It occurs in humans, usually in small children or helpless and bedridden adults, living under filthy conditions. No such situation was there in our patients.
The reality of enteric myiasis as a pathological condition in man has been questioned by many workers. Zumpt does not consider enteric infestation in human as true myiasis, as the ingested larvae do not normally feed while they complete their development in human digestive tract. He puts it as the ability of the fly maggots to resist extremely unfavourable environment, rather than an adaptation to facultative form of parasitism. 
The subject has been discussed in considerable detail by Riley,  James  who came to the conclusion that genuine enteric myiasis does occur from time to time when conditions in the alimentary canal are such as to favour the survival of the parasite.
The larvae can cause severe clinical syndrome in human beings, depending on the larval species, their number and location within the digestive tract. In many instances, they are passed out in faeces without causing much disturbance as in most of our cases. But severe infestations have said to cause depression and malaise in patients. They may cause vomiting, bloody diarrhoea, and pain in abdomen due to injury to intestinal mucosa. , Our first case also had ulcers in colonic mucosa. Haemorrhagic vomiting  and rectal bleeding  have also been reported.
Intermittent passage of worms, GI disturbances, flatulence and vague abdominal pain were the common findings in our cases. The other important feature was anxiety.
We never found any case of gastric myiasis. Here, the case of a 5-year-old boy has been described. The boy, for some time, vomited everything he ate. His breath was "worse than a rotten egg." He was emaciated, nervous and anaemic. After some propriety worm remedy, the boy discharged an object wriggling vigorously in faeces in 2 days. After the passage of larva, the boy improved and his vomiting and nervous symptoms disappeared. The worm was identified as rat-tailed larva of Eristalis. The sources of infection were pointed out to be eating of over-ripe decaying peaches, drinking of "ditch" water polluted with kitchen refuse and exposure to stable manure in the yard where he played. The child according to the mother was extremely intolerant to milk and vomited it out. The reason given was that the milk always taken in quantity would threaten the survival of larvae by drowning, evoking vigorous activity in them leading to vomiting. 
Four cases of gastric myiasis are reported from Egypt in 2011. The patients were a 10-year-old boy and 3 adults. They had offensive haematemesis. Gastric endoscopy showed live maggots, identified as Sarcophaga species and Oestrus species. Gastric endoscopy showed hyperaemic gastric mucosa and hyperaemic regular active pylorus. Antral gastritis was marked. Two patients had minute-moving worms sticking to mucosa. One of the patients, a 40-year-old male had a history of accidentally swallowing an adult fly 6 months back. 
The association of intestinal myiasis and epilepsy, which our second patient developed cannot be explained. However nervousness, depression, vertigo,  twitching of eyelids and convulsive movements have been documented in literature. 
"Pseudomyiasis" is an entity that refers to the accidental ingestion of dead or living fly larvae passed out in faeces with no associated pathological changes or symptoms.  Pseudomyiasis can also occur when the female fly oviposits on uncovered faecal specimen. These can be wrongly diagnosed and treated with antihelminthics. ,
The source of infection in our patients may be due to eating food from vendors that had been exposed to flies. Possibility of anal route of infestation also cannot be ruled out as defecation on road side and in the open field is a practice in some parts of the country. S. haemorrhoidalis found in majority of our cases is an excrement feeder. The larvae can penetrate the rectum immediately after deposition. It has been described as rectal myiasis.  E. tenax, the rat-tailed larva also is said to be an agent of rectal myiasis. They are attracted to faeces, lay eggs or larvae near or within the anal canal, and can penetrate the rectum. 
| ~ Conclusion|| |
Intestinal myiasis has not found a rightful place in the textbooks of medicine and parasitology. The treatment is not outlined properly. It is important for public health officials and physicians to know the significance of prevention and precautions, and advising the public and patients against eating uncovered food that has access to flies. Defecation in the open must be strongly discouraged. In terms of treatment, Ivermectin is said to be worth a trial  but we have not found it to be effective. The nearest to a cure, presently, is colonic irrigation using PEG. It helped our patients to flush out the larvae. Purgatives also will have the same effect. 
The long duration of symptoms in intestinal myiasis and recurrences in these patients is baffling. It poses a challenge not only to the treating doctors but also to the medical entomologists and epidemiologists. A high index of suspicion will diagnose intestinal myiasis especially when the patient complains of passing small wriggling "worms" in faeces for long without any response to antihelminthics. We strongly feel that the condition is more common than reported. Possible source of infection in the patient should be traced and eliminated.
| ~ Acknowledgments|| |
We are thankful to Professor P. Rajendran, Professor, Department of Microbiology, Dr. ALM Postgraduate Institute of Basic Medical Sciences, Chennai and Dr. A. Joseph, Retired Professor of Madras Veterinary College for getting the identification of the larvae of S. haemorrhoidalis and the adult of Megaselia. We are also thankful to Dr. Abhay Choudhary, Director at Haffkine Institute, Mumbai, Dr. Mira Ramaiya, HOD, Zoonosis, Haffkine Institute and Dr. T. V. Sathe, Professor and Head, Department of Zoology, Shivaji University, Kolhapur for identifying the larva and adult of S. haemorrhoidalis.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]
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