Portuguese Version

Year:  2001  Vol. 67   Ed. 6 - (1º)

Artigo Original

Pages: 755 to 761

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Treatment of human cavitary myiasis with oral ivermectin

Author(s): Fernando A. Q. Ribeiro1,
Celina S. B. Pereira2,
Adriana Alves3,
Manuel A. Marcon4

Keywords: myiasis, treatment, ivermectin

Abstract:
Introduction: Human myiasis is relatively common. It is unpleasant not only for the patients affected by this parasitical disease, but also for the doctors that must treat them. It is more common in undeveloped and tropical countries, although there have been reports of myiasis all over the Planet. It usually affects the elderly, the ill and the mentally disabled, but there have also been reports in healthy patients. The larvae usually lay their eggs in necrotic or infected tissues, however they may also lay eggs in areas of the body that are apparently healthy. Treatment of this parasitic infection is basically through removal of the larvae, a painful and cumbersome task, sometimes made impossible in smaller cavities. There have also been reports of drugs used topically to facilitate the removal, but with frustrating results. Study design: Prospective randomized. Methods: This study used oral ivermectin (until 300 µg/Kg). This drug has already been reported for the treatment of other diseases. The patients were submitted to hepatic and renal function tests before and after treatment, and followed as out patients. Results: The larvae were eliminated in all patients and there were no abnormalities in the blood tests.

Introduction

Myiasis

Definition: Affection caused by the presence of fly larvae in humans or other vertebrate animal organs and tissues, where they are nourished and progress as parasites21. Infestation of live vertebrates by diptera larvae that are fed from living or dead tissues of the host, liquid body substances or the food ingested by the host11.

Classification: Based on site of affection, they may be cutaneous, subcutaneous or cavitary (nose, paranasal sinuses, ear, mouth, anus, vagina, etc).

Based on biological characteristics of the fly:

a) Mandatory (primary or biontophagous) caused by diptera larvae that naturally develop on and inside vertebrates, feeding from living tissues.
- Oestridae - develops in nasopharyngeal cavities of various mammals;
- Calliphoridae (genus Cochliomyia and Chrysomya);
- Cuterebridae;
- Muscidae (genus Philornis).

These three families of flies develop in cutaneous and subcutaneous tissues of mammal and avian.
- Gasterophilidae - develops in digestive tract of horses and other mammals.

b) Optional (secondary or necrobiontophagous), caused by diptera larvae that normally develop in organic decomposition matter, but they may also occasionally develop in living host necrotic tissue.
- Calliphoridae (genus Cochliomyia, Chrysomya and Phaenicia);
- Sarcophagidae;
- Muscidae (Fannia).

c) Pseudomyiasis (accidental). Caused by diptera larvae ingested through food, which may lead to more or less severe episodes.
- Stratyomidae (Hermetia illuscens);
- Syrphidae;
- Muscidae;
- Tephritidae.

Myiasis affections are frequently found in rural areas among farm animals, such as cattle, goat, sheep, swine, etc. and also in domestic animals, such as cats and dogs, causing damage to the herds and economic losses. It may also affect human beings, normally elderly, sick or debilitated people. Myiasis are more common in developing countries, such as in Latin America, Africa, Middle East and Asia, but it may also happen in developed countries or affect tourists travelling in tropical countries23, 6. They may be manifested differently. The primary form, caused by biontophagous larvae (that feed from living tissues), are common in cattle (affection in the umbilical cord of calves), but rare in human beings. If present, they are normally severe and caused by larvae of Cochliomyia homivorax (fleshfly) that lay 20 to 400 eggs on the edges of scratches and wounds. Larvae that come to life within 24 hours are voracious and destroy healthy tissues, leading to severe hemorrhages if proliferating in a cavity.

Sometimes they may cross intact tissues causing furunculous myiasis (as we will see ahead). In Europe, North America, Australia, Asia and Africa, human beings may be contaminated on the ocular conjunctiva and nasal mucosa by larvae of Oestrus ovis, which normally develop in the frontal sinuses of sheep18, 13. A peculiar type of primary myiasis (furunculous or botfly) is more common, affecting healthy people, especially in rural areas. The fly that transmits botfly is normally Dermatobia hominnis, family Cuterebridae, which has a quite curious life cycle. The fecundated adult fly lays its eggs, while flying, on the abdomen of another fly, normally hematophagous. When the fly stings a person, one larva is detached and goes into the healthy tissue or through small lesions on the skin of the host, where a furunculous develops, up to the moment it is detached and fall on the floor, continuing its biological cycle7, 9.

The most common is to find myiasis in patients who have cavitary necrotic lesions, such as middle ear cholesteatoma, nasal ulcer-granulomatous diseases or tumors of the nose (leischmaniosis, Hansen's disease, etc.), oral, anal, vaginal and ophthalmic tumors, and skin lesions7, 9, 20, 19, 15, 10. These secondary myiasis affections are caused by necrobiontophagous fly larvae (they feed from dead tissue), and the most common in our population is Cochliomya macellaria and Phaenicia cuprina (Lucilia). The larvae of some Sarcophagidae and species from genus Chrysomyia, Fannia, Musca and Muscina may also cause secondary myiasis.

Pseudomyiasis, or accidental myiasis, after massive injection of fly larvae, are frequently seen in other animals, but they are not common in human beings1. Other types of fly may cause myiasis in human beings, but since it is rare, the identification is based on anatomical details of the fly. The diptera species vary around the world and some that cause myiasis are Wohlfahrtia magnifica, in Europe, Russia, Africa and Middle East, and Chrysomya bezziana, in the Far East and tropical Africa. Cordylobia arthropophaga, also in Africa, causes furunculous myiasis (botfly). Controlled myiasis (Lucilia) have been used a number of times as a cleaning treatment of necrotic tissues in infected wounds (gangrene, etc.), and the stage of necrobiontophagous larvae in corpses help the coroner teams date the time of death.

Ivermectin
Ivermectin belongs to the chemical group of avermectins, a semi-synthetic macrolide antibiotic isolated from Streptomyces avermitilis. It is widely used in large sized animals, such as cattle, horses, goat, sheep and camels, for treatment and control of parasitosis caused by gastrointestinal and pulmonary nematoid, in infections by botfly (myiasis), lice and adjuvant in the treatment of scabies and tick.

It is effective against:

Gastrointestinal roundworms: Haemonchus ssp, Ostertagia ssp, Trichostrongylus axei, Cooperia ssp, Bunostomum phlebotomum, Oessophagostomum radiatum, Strongyloides pappilosus and Nematodirus ssp.
Pulmonary worms: Dictyocaulus viviparus.

Botfly and myiasis: larvae of Dermatobia hominis. (and larvae of other flies).
Lice: Linognathus vituli, Haematopinus eurysternus.

Scabies: Psoroptes communis var. bovis, Sarcoptes scabiei and Chorioptes bovis.
Ticks: Boophilus microplus.

Maggot-infestation (myiasis by biontophagous larvae) of the umbilical cord of calves: as prevention, used in the first week after birth, preferably within 24 hours.

It may also be used as a prevention of maggot-infested conditions in castration wounds, right after the surgical procedure.

Dosage:
It should be administered subcutaneously, at 200mg of ivermectin per kg of body mass, equivalent to 1ml of the product to each 50kg body mass.

Action:
It interferes in the transmission of nervous impulses, on the nervous endings, by stimulation to the release of gamma amino butyric acid (GABA). In roundworms (nematoid), ivermectin stimulates the release of GABA in nervous endings, favoring its fixation at the level of receptors, interrupting nervous impulses and determining extermination of parasites. In ectoparasites, such as mite, lice and arthropods, its effect is similar to the one on nematoid; however, the nervous impulse is interrupted between the nervous transmission and the muscle, producing paralysis and death.

Acetylcholine, the main peripheral neurotransmitter in mammals, is not affected by ivermectin.
Ivermectin does not penetrate easily the central nervous system barrier of mammals, in which GABA acts as a neurotransmitter, keeping a wide safety margin with the use of the recommended dose.

Use in humans:
Ivermectin has been used as a prophylactic agent in the treatment of filariasis caused by Onchocerca volvulus, Wuchereria bancrofti, Brugia malayi and Brugia timori (oncocercosis, loiasis, loa-loa, elephantiasis), proven to be a safe method at the recommended dose of 200mg/Kg. Even at doses of 300-400mg/Kg, patients submitted to treatment did not present significant clinical side effects, except for mild pruritus. Authors have also conducted hematological tests, liver and renal function tests and results were within normal ranges, except for mild eosinophilia. The treatment has been recommended because it is less toxic than the previous one with DEC (diethylcarbamazine), which presented frequent cases of encephalitis16. It has also been used as prophylactic treatment with repetitive doses every three months, during two years, at 200mg/Kg in populations of endemic areas, where more than 600 people underwent treatment and no significant side effects were reported, showing that it is an excellent method to eradicate filariasis 5.

Ivermectin has lately been used to treat scabies, with a single oral dose of 100-200mg/Kg with better results than the ones obtained with topical benzyl benzoate. These conditions are normally benign and caused by Sarcoptes scabiei; however, especially in immunodepressed patients, such as AIDS patients, scabies may progress to a severe form called Norwegian scabies. In both cases, results of treatment with ivermectin are surprisingly good and do not present side effects.

Other studies have also shown the excellent results obtained from the treatment of strongyloidiasis with ivermectin, which has lower toxicity than thiabenzadole. The drug has been approved by US FDA for this kind of treatment.

Treatment for human myiasis:
The condition of myiasis in human beings demonstrated poor hygiene and insufficient care of our patients. It normally affects patients with necrotizing diseases such as ulcer-granulomatous (leischmaniosis, Hansen's disease, etc.) or tumor affections. If not properly taken care of, these people may be exposed to fly's eggs and develop myiasis, which is a degrading condition, to say the least. It is frequently seen in elderly and mentally-handicapped patients, those forgotten in nursing homes or asylums, or even in total abandoned conditions. Healthy people may also be affected if myiasis is caused by a biontophagous larva (that feeds from living tissue) and present severe conditions that may be fatal, caused by hemorrhages or central nervous system affection. In healthy patients, we can also detect furunculous myiasis (botfly), quite common in the rural area.

Treatment is mechanical, that is, larvae have to be removed one by one, a painful, disturbing and embarrassing procedure both for the patients and the physicians. These patients, owing to their peculiar characteristics, are not always very collaborative, hindering the cure process. A number of attempts have been made to force the larvae out by applying a series of asphyxiating topical drugs, including powder chloroform, still in use nowadays. In some situations of cavitary myiasis, such as of middle ear or nasal and sinusal cavities, the identification of all larvae is impossible and the use of these drugs may contribute to their agitation and migration into inaccessible regions. Systemic drugs, such as camphor oil, mercury oxide cyanide, mercury sulfuride, among others, were tested but did not succeed in sending away the larvae. In furunculous myiasis (botfly), it is a habit, especially in the countryside, to force the expulsion of larvae by asphyxia, with a piece of bacon or even adhesive tape. It is a long and unsuccessful procedure, sometimes requiring small surgical interventions under anesthesia.

Many methods have been described for the clinical treatment of human myiasis, but none of them proved to be 100% effective2, 4, 12, 17.

Historically, we found the description of the use of various antiseptics, asphyxiating and mercury agents. The substances used to be applied by nasal lavage, inhalations, and external ear instillation; sometimes also as systemic drugs.

To illustrate, we listed various substances reported in the literature and widely used in Brazil:

Topical use:
· sodium hydrochloride
· chlorinated water
· chloroform water
· infusion of belladonna leaves
· 96% alcohol
· acridine
· creosote
· creolin
· 1:4000 potassium permanganate
· 4% borate water
· benzene
· chloroform
· ether
· phenol
· chloroethyl
· carbolated oil
· olive oil
· calomel (powder)
· iodineform (powder)

Systemic use:

a. Intravenous drugs

Mercury oxide cyanide (by Prado Moreira, described in 1933, was the first IV medication used to treat human myiasis). The method advocated daily use of IV 1 to 2cc, up to total cure. For years, it was used with enthusiasm by many authors; however, later, its efficacy started to be questioned because it was always associated to topical medication, which could have been responsible for the cure.

b. Intra-muscular (IM) medication:

Thiozol (mercury sulfuride)

c. Subcutaneous medications:
25% camphor oil, 2cc, subcutaneous, BID. The method was described by Mazza, in 196517.

Some new studies referred to experimental use of ivermectin for the treatment of cutaneous human myiasis, either topically24 or PO3, 14, 8. One of the studies reported that the patient also had cavitary myiasis (nasal)14. Another study22 treated oral myiasis with subcutaneous ivermectin.

The purpose of the present study was to investigate the possibility of treating cavitary human myiasis with oral ivermectin, a well known drug for the treatment of animal myiasis, which presents excellent result in larvae eradication, with no side effects resultant from the treatment of other human beings' diseases16.

Material and Method

Seven consecutive patients who had come to the Ambulatory of Otorhinolaryngology at Santa Casa de São Paulo, with clinical picture of cavitary myiasis were treated with two pills of ivermectin (12 mg), after approval by the Medical Research Ethics Committee of Santa Casa de São Paulo. Twenty-four hours later, they were reevaluated to check the presence and status of larvae on the lesion. Patients had blood collected for analysis and renal and liver function, before and one week after treatment with the pills.

Tests performed:
Complete blood count: hemoglobulin, hematocrit, neutrophil, lymphocyte, monocyte, eosinophil, platelet.
Renal tests: urea, creatinine.
Liver tests: total bilirubin, direct and indirect bilirubin, TGO and TGP, coagulation time, prothrombin time, bleeding time, prothromboplastin time, and activated partial thromboplastin time.
RESULTS
Patient 1:
Identification: FCS, 25-year-old male patient. Had larvae in the oral cavity for one day, after a three-day bus trip (patient came from the Northeast of Brazil to São Paulo).
Oral examination: Oral cavity had 2 larvae on the right tonsil, absence of necrosis or any other alteration. Good general health status.
Initial lab tests: Normal.

Used two pills (12mg) of oral ivermectin; 24-hour reevaluation: absence of larvae. Patient reported that one "dead" larva had been expelled approximately 12 hours after the medication, while brushing his teeth (sic). Physical examination did not show alterations or larvae. Patient was discharged that same day.

Patient 2
Identification: DRS, 65-year-old female patient.
Patient with history of tumor exeresis (meningioma) partial resection of left hemiface (left frontal craniotomy + partial lobotomy + orbit exeresis + anterior and superior walls of the left maxillary sinus), reconstructed with skin graft + fat. She reported purulent bilateral rhinorrhea, especially from the left nasal fossa for 7 days, progressing for three days with discharge of a large number of larvae (about 200 - sic), bilaterally, through the nasal fossae. She had been taking amoxicillin for 24 hours.

ENT examination: Partial deformity of left hemiface, with extensive vertical scar since the forehead up to the lateral margin of the lateral nasal pyramid, absence of left ocular globe and the region was recovered with skin graft. Centered nasal pyramid, reduction of left nasal vestibule diameter. Left nasal fossa with absence of nasal lateral wall, formation of a large cavity filled with purulent secretion and living larvae. Right nasal fossa with preserved structures, but it also contained some amount of purulent secretion and living larvae. Fetid odor from the nasal fossae.
Initial lab tests: Normal.

Dose used: Two pills (12mg) PO of ivermectin. 24-hour reevaluation: patient still had discharge of living larvae. We used another pill of 6mg ivermectin and amoxicillin was maintained. Patient was instructed to wash the nose with saline solution. 48-hour evaluation: no discharge of larvae and no detection of larvae in the nasal cavity, patient referred facial edema, pruritus and petechiae, and decided to interrupt amoxicillin, with regression of the condition in the following days.
Lab tests 7 days later: Normal.

Reevaluation 7 days later: absence of larvae and presence of a small amount of purulent secretion. Patient was instructed to wash the nose frequently. We ordered paranasal sinuses CT scan and after the result, we referred the patient back in order to carry on with the initial treatment.

Patient 3:
Identification: JCS, 37-year-old male patient. Patient referred that he felt as if there were "things" moving inside his right ear for three days. He reported history of chronic otorrhea for 30 years.
ENT Examination: Right ear: large amount of living larvae in the internal third of the external acoustic canal. Tympanic membrane was not visualized.
Initial lab test: Normal.
Two pills (12mg) of ivermectin were used.
24-hour reevaluation: presence of some living and some dead larvae (recorded in video for documentation purpose), all in the external third of the external acoustic canal. Lavage was performed and we decided to administer one more pill of oral ivermectin. 48-hour reevaluation: external acoustic canal was slightly hyperemic. Tympanic membrane with central perforation and granulation tissue. No further larvae were visualized. Otological lavage and no detection of larvae.
Patient did not come back to perform the 7-day lab test, as instructed.

Patient 4:
Identification: CV, 36-year-old male patient. Patient with mental retardation and absence of communication, had been extremely agitated for the past 24 hours, associated to serum-sanguinolent discharge from the left ear.
ENT examination: External acoustic canal with serum-sanguinolent discharge and evidence of a large amount of living larvae. Very agitated patient, difficult to control.
We used two pills of oral ivermectin (12mg).
Initial lab test: Normal.
24-hour assessment: removal of a large amount of dead larvae; 48-hour assessment: tympanic membrane with central perforation, no evidence of larvae.
Lab test 7 days later: Normal.

Patient 5:
Identification: ERL, 30-year-old female patient, no previous history of otologic disease, reported introduction of a fly into the left ear 12 hours before. It remained inside for 15 minutes and then left spontaneously. She had no complaints for 12 hours, when she started with tinnitus and otalgia on the left.
ENT examination: external acoustic canal filled with a large amount of small-sized larvae (5mm). Lavage with saline solution and removal of about 100 larvae. After the procedure, we noticed that the membrane was intact, but with bruises. We also found the orifice through which the larvae passed, the probable site for egg inoculation, but it was not possible to remove them all because they "hid" behind the integral portion of the canal, up to the tympanic ring. One was partially seen by transparency inside the tympanic cavity.
We used two pills of oral ivermectin (12mg).
Initial lab tests: Normal.
Twenty-four hours later the patient still presented innumerous living larvae at the otoscopy, most of them exiting through the orifice on the external acoustic canal, as described above. We performed a new lavage and removed approximately 50 larvae that were twice as big as the ones removed on the day before, but with reduced mobility. On the third day, the patient had no larvae and no complaint of otalgia or tinnitus. Normal otoscopy.
Lab tests after 7 days: Normal.

Patient 6:
Identification: MLCP, female 60-year-old patient.
Earache and discharge for 4 days. Patient referred otalgia with otorrhea on the left ear for four days, worsened in the last 48 hours, when she noticed the discharge of "living" larvae. She reported history of otorrhea two years before, which had been treated and controlled.
ENT examination: Left ear external acoustic canal with hyperemia, mucous-purulent secretion and living larvae inside it. Tympanic membrane could not be visualized.
Initial lab tests: Normal.
Evolution: Obese patient (130Kg), she was medicated with 3 pills of ivermectin (18 mg). 12 hours later she still presented living larvae in the external acoustic canal and local pain.
We prescribed two more pills. She returned 36 hours later and maintained severe otalgia and some living larvae inside the external auditory canal. 48 hours later, she referred improvement of otalgia, and the three remaining living larvae were removed from her ear. At otoscopy, we observed tympanic membrane perforation and remains of the fly's body, which were removed. We did not find any further larvae.
Lab tests 7 days later: Normal.

Patient 7:
Identification: IMS, 17-year-old male patient. Patient referred otalgia on the left for two days, which progressed to sensation of living foreign body and otorrhea. The patient referred otologic surgery in that ear four years before.
Physical examination: Radical cavity with large amount of serum-sanguinolent secretion and many movable and living larvae.
Therapy: two pills of oral ivermectin (12mg).
Initial lab tests: Normal.
24-hour reevaluation: Patient reported otalgia. We visualized ample radical cavity recovered by serum-sanguinolent secretion with approximately 6 living larvae inside it, but with little mobility. All larvae were easily removed, including two that were in the auditory tube.
Seven-day reevaluation: No further complaints. Upon examination, the cavity had good aspect, normal epithelium, with some remains of cream and no larvae.
Lab tests 7 days later: Normal.

Discussion

Seven patients with cavitary myiasis were treated in the Ambulatory of ENT at Santa Casa de São Paulo, with oral ivermectin at the initial dose of 2 pills or 12mg (approximately 200 mg/Kg). The location of myiasis varied, similarly to the literature19, 15, 9:

One in the oral cavity - tonsil had no apparent lesion;
One in the nasal cavity - after exeresis of a tumor;
Four in the middle ear - chronic otitis media, and
One in the external acoustic canal - no apparent lesion.

Three of the patients had complete eradication of the larvae after the initial dosage and two had to take one more 6mg pill after 24 hours. Patient 5 was obese (130Kg) and her initial dose was insufficient (18mg, that is, less than 26mg, that is the recommended initial dose) and the larvae were eradicated only 3 days later. All larvae were completely eradicated after treatment, some of them after simple lavage with saline solution and others spontaneously (possibly swallowed or discharged in the environment). Patients 1 and 5 had no previous lesion, making us believe that they had been contaminated by Cochliomyia homivorax (fleshfly), and case 5 was very typical because of local aggressiveness (they were patients from a higher social-economic background). The other 4 cases had damaged tissue affections, with suppuration and necrosis, and they were possibly caused by the so-called secondary species. Four of the patients (2, 4, 5 and 6) were submitted to all lab tests (complete blood count, renal and liver function tests) pre and post-treatment, all of them within normal ranges. Two of them did not come back for the lab tests 7 days later. We used one week as a reference because that would be enough time to detect abnormalities in the lab tests if the drug was toxic. Laboratory tests with the same drug, at the same concentration, for other diseases (filariasis, Norwegian scabies, strongyloidiasis) did not demonstrate harmful effects either5. We noticed that the use of oral ivermectin up to a dose of 300mg/Kg, did not cause complications in the patients and eliminated all the larvae from cavitary myiasis. Even though it is a difficult site to access, larvae were eliminated spontaneously or through lavages, which did not compromise the subjects either locally or systemically. Since the initial dosage of about 200mg/Kg did not eradicate the larvae, requiring complementation, we suggest to start treatment with the dose of 300mg/Kg. In other words, patients who are 40 to 60 Kg would take 2 pills (12mg), whereas those between 60 and 90Kg would take 3 pills (18 mg).

Conclusion

Ivermectin at 300mg/Kg eradicates cavitary myiasis larvae with no toxicity to the patient. Larvae die and are eliminated spontaneously or through lavage, dispensing the unpleasant individual collection.

References

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1 Joint Professor, Medical School, Santa Casa de São Paulo.
2 Doctorate studies under course, Medical School, Santa Casa de São Paulo.
3 Master studies under course, Medical School, Santa Casa de São Paulo.
4 Resident Physician, Medical School, Santa Casa de São Paulo.

Study conducted at the Medical School, Santa Casa de São Paulo.
Address correspondence to: Rua Itapeva Nº. 500, 01332000 São Paulo /SP Tel-fax 2885414 - E-mail quinta@dialdata.com.br

Study presented at II Congresso Triológico de ORL, in Goiânia /GO, in August 2001.

Article submitted on April 17, 2001. Article accepted on June 4, 2001.

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