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Ectoparasitic infestations in homeless children
Ectoparasitic Infestations in Homeless Children Benjamin Estrada, MD Most human ectoparasites live on the surface of their host and depend on that host to complete their life cycle. The most common ectoparasitic infestations of medical importance in humans include pediculosis, scabies, myiasis, and tungiasis. Different host factors are related, with increased risk of acquiring ectoparasitic infestation occurring among the homeless. Although these ectoparasitic infections can be found worldwide, their prevalence is affected significantly by environmental conditions in different geographical areas. This review focuses on the epidemiology, clinical presentation, diagnosis, and treatment of common ectoparasitic infestations among homeless children and their families. The most frequent bacterial infections associated with these infestations also are discussed. © 2003 Elsevier Inc. All rights reserved.
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ignificant risk factors for acquiring ectoparasitic infestations exist among homeless children compared with the general population. Those factors include poverty associated with lack of hygiene and crowding, which frequently is observed in shelters, day drop-in centers, and refugee camps. The lack of financial resources frequently is reflected in poor sanitary conditions in many of these facilities. Environmental factors such as geographical location, humidity, and temperature also play roles in the development of ectoparasitosis among this population. Whereas some infestations such as Pediculosis corporis are more prevalent in areas of cold weather, others such as those caused by fly larvae and fleas are observed more frequently in areas with warm climates. Additionally, situations such as war and natural catastrophes commonly related to homelessness and displacement frequently are related to outbreaks of ectoparasitic infestations among children and their families.1,2
Body Lice Infestations Lice infestations have been prevalent among humans for thousands of years. The oldest eggs of Pediculus spp. have been found in the Judean desert and date from between 6900 to 6300 BC.3 Although more than three thousand species of lice exist, the only three that affect humans are Pediculus humanus capitis (head lice), Pediculus humanus
From the Division of Pediatric Infectious Diseases, University of South Alabama, Mobile, AL. Address reprint requests to Benjamin Estrada, Associate Professor of Pediatrics, Division of Pediatric Infectious Diseases, University of South Alabama, 1504 Springhill Avenue, #5222, Mobile, AL 36695; e-mail: [email protected] © 2003 Elsevier Inc. All rights reserved. 1045-1870/03/1401-0004$30.00/0 doi:10.1053/spid.2003.127213
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humanus (body lice), and Phthirus pubis. P. humanus capitis is known to affect all levels of society, P. pubis is transmitted sexually, and P. humanus humanus has been associated more frequently with conditions of lack of hygiene and extreme poverty.3,4 Consequently, infestation with P. humanus humanus, also known as “vagabond’s disease,” is an issue of concern among homeless children and their families, including those living in refugee camps.5 Particular environmental factors involved in the life cycle of this ectoparasite can play significant roles in the predisposition for infestation among homeless individuals. Close body-to-body contact is associated strongly with transmission of lice. For that reason, infestation occurs more frequently in crowded environments such as homeless shelters, refugee camps, and jails, especially when hygienic standards are lacking. Although the distribution of P. humanus humanus is universal, infestation with this parasite is more prevalent among homeless individuals who live in environments in which cold weather predominates and who need several layers of clothing to protect themselves from low temperatures, especially during the winter months. Lack of frequent changes of clothing among this population is a factor that favors the development of environmental conditions needed for the completion of the P. humanus humanus life cycle.1-6 Typically, lice lay their eggs in the folds of clothing, especially in areas that are particularly close to higher body temperature regions such as the genitals, axilla, and abdomen. If these eggs are held at constant temperatures, they usually hatch within 6 to 9 days. After hatching, the louse moves to the skin, where it feeds on human blood and returns to the clothing promptly after feeding. Other lice may be attracted to the area of infestation by the ammonium present in the parasite feces, which frequently are deposited in the garments. The optimal level of humidity for lice to survive is between 70 and 90 percent.3,4
Seminars in Pediatric Infectious Diseases, Vol 14, No 1 ( January), 2003: pp 20-24
Ectoparasitic Infestations in Homeless Children Individuals infested with body lice may harbor several hundred parasites. Although no skin lesions may be apparent initially, several weeks after infestation humans develop an allergic response to the biologically active proteins produce by lice, which may trigger intense pruritus with subsequent development of skin lesions. Consequently, these lesions may become superinfected by bacterial organisms such as Staphylococcus aureus and Streptococcus spp. The skin lesions caused by P. humanus typically present as red macules or papules more frequently localized around the abdomen and neck. Persons affected by this parasite occasionally may develop fever and adenopathy. In addition to these clinical findings, the presence of nits in clothing seams should be considered confirmatory evidence of infestation.4-6 The body lice is an efficient vector for bacteria that can cause systemic disease such as Bartonella quintana, Rickettsia prowasekii, and Borrellia recurrentis. Acinetobacter spp. and Serratia marcescens also have been isolated from body lice, but whether they can be transmitted by this ectoparasite is not known.4,6 Infection with B. quintana is the bacterial disease most frequently associated wth infestation of body lice. This organism is known to be the causative agent of Trench fever epidemics during World War I and II. During the last decade, different reports about the development of infection with this organism among homeless patients have linked it to infestation with body lice. Studies performed among homeless patients in the United States and France have demonstrated that the seroprevalence of antibodies against B. quintana in these populations is significantly high (25% and 30%, respectively).7-11 In a study performed in Russia, lice infestation occurred in 11 percent of patients included in the study population and B. quintana was detected by polymerase chain reaction (PCR) among 12.3 percent of louse samples collected from these patients.12 The spectrum of symptoms caused by infection with B. quintana includes an acute febrile illness associated with malaise, headache, a macular rash, bacillary angiomatosis, and chronic bacteremia. Patients may remain bacteremic with this organism for as long as one year, and episodes of endocarditis also have been reported. The recommended treatment for patients infected with B. quintana includes doxycycline and gentamicin, although other antibiotics such as erythromycin, rifampin, azithromycin, clarithromycin, and amoxicillin also have been reported to be effective.8 R. prowasekii, which causes epidemic typhus, is a louseborne disease that has been reported in situations such as war or famine, especially when lack of sanitation and crowding are likely to occur. Significant outbreaks of epidemic typhus occurred during the first half of the twentieth century, followed by a significant decrease on their occurrence.4 However, a resurgence of typhus after 1995 has been observed in countries such as Russia, Burundi, and Peru. Several recent outbreaks of epidemic typhus have been reported in refugee camps in Africa as well. Treatment with tetracycline and chloramphenicol is effective against R. prowasekii; however, a single dose of doxycycline for chil-
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dren older than 8 years probably is the most effective therapy.13-17 B. recurrentis is another organism that can be transmitted efficiently by body lice. This bacterium is the etiologic agent of outbreaks of relapsing fever, which have been reported recently among displaced individuals in African refugee camps. The antibiotics recommended in the treatment of relapsing fever include penicillin, chloramphenicol, tetracycline, and erythromycin.4,18 The development of bacterial infections associated with P. humanus can be prevented by implementing strategies aimed to reduce infestation of body lice. Because the body louse resides in the individual’s clothing and not on the human body, the most effective therapeutic modality for its eradication is frequent changing and cleaning of bedding and clothing, including underwear. In homeless shelters, bedding should be washed with hot water and treated with insecticides daily. The clothes should be washed with hot water, and some investigations recommend the application to this garment of insecticides such as DDT, 1 percent Malathion, or 1 percent permethrin.1,5 Although successful treatment with ivermectin given in two doses 200 mg/kg/dose 10 days apart has been reported effective in the treatment of individuals with head lice, systemic treatment for those infested with body lice is not recommended. For older children and adolescents with heavy infestations of lice, application of gamma benzene hexachloride (lindane) lotion has been used. However, this product can be absorbed through the skin, and it has been associated with neurological adverse effects, such as epileptiform convulsions and muscle spasms. For that reason, its application in young children is not recommended. An additional disadvantage of the use of lindane lotion is that this formulation must remain on the skin for approximately 12 hours after its application. Because of this requirement, it usually is not a practical therapeutic approach because homeless individuals often visit shelters for shorter periods of time. A more practical option for treatment of lice among the homeless adult population seems to be the application of lindane shampoo, which must remain in contact with the skin for only five minutes. The effectiveness of this approach may increase if it is coupled with delousing of bedding and clothing as previously described.1,4
Scabies Scabies is an ectoparasitic disease caused by Sarcoptes scabiei var hominis. This ectoparasitosis has been known to infect humans for thousands of years. The main route of transmission is skin-to-skin contact, but indirect infestation with fomites also can occur. Lack of hygiene, poverty, and crowded environments have been identified as significant risk factors that favor the transmission of this parasite.3 Scabies has been reported to be a significant problem in homeless shelters and refugee camps, as well as among the general population in developing countries. Observations reveal that the prevalence of scabies among children younger than 5 years of age living in displacement camps
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may be as high as 77 percent and increases to 86 percent among those who are 5 to 9 years old.19 Typically, the mites of S. scabiei develop tunnels into the epidermis mainly through the stratum corneum. They deposit feces, and females lay their eggs between the stratum corneum and the stratum granulosum. The incubation period of S. scabiei is 3 weeks. The most significant clinical finding is generalized nocturnal pruritus. The lesions observed in patients with scabies include burrows and nodules with associated significant excoriation. In children, the lesions generally involve wrists, elbows, axilla, neck, and interdigital spaces. Scabies in children may present as vesicles and pustules involving the hands and feet, including palms and soles. Occasionally, the lesions present in a generalized distribution, which may include the scalp among young infants and immunocompromised patients. In many cases, the original lesions may become superinfected with Streptococcus or Staphylococcus spp.3 Helpful tools in the diagnosis of scabies include skin scrapings or skin biopsies in which mites may be identified. If possible, laboratory diagnosis of scabies should be performed among homeless children because other skin diseases in this particular population, such as acropustulosis, postscabeitic nonspecific reactions, atopic dermatitis, and contact dermatitis, have similar clinical characteristics.3 Several medications, including permethrin, lindane, benzyl benzoate, crotamiton, and ivermectin, are used to treat scabies. Application of benzyl benzoate 10 percent and 25 percent lotion is utilized widely in the treatment of scabies. This product should be washed thoroughly from the skin 12 to 24 hours after application and generally is safe for use in children. Permethrin 5 percent cream is considered by many physicians to be the first-line therapy among children older than 2 months. Permethrin is well tolerated and should be rinsed well 8 to 12 hours after its application. Additionally, it has been associated with fewer side effects than have other scabicides such as lindane, particularly in children. Although the antiscabeitic efficacy of lindane compounds is very similar to that of permethrin, it should not be used in young children because of the potential for causing side effects previously discussed in this review. In older children, this alternative should be used only if other regimens have failed.3,20 Topical scabicides should be applied after a bath to the entire skin, including groin, fingernails, toenails, and retroauricular areas, avoiding mucous membranes. All infested individuals and their household contacts should be treated. In addition, clothes and bed linen should be washed carefully.3,5 Treatment with a single dose of oral ivermectin 100 g/kg to 200 g/kg has been reported to be effective among adults with scabies, including patients infected with human immunodeficiency virus (HIV). The mechanism of action of this drug is that it interrupts S. scabiei neurotransmission. The topical application of a 1 percent solution of ivermectin recently was reported to be effective in the treatment of scabies in children. Although this therapeutic approach
seems to be practical, no data support its safety or efficacy in children at the present time.21
Myiasis Myiasis is the infestation caused by dipterous larvae also known as “maggots.” Although myiasis occurs more commonly in tropical countries, it does occur worldwide.22-25 Homeless children are at increased risk of exposure to flies for different reasons. First, they live in poorly protected environments with lack of hygiene. Soiled clothing on these children attracts flies, especially among those who are not yet toilet trained. Additionally, abandoned children, especially those in developing countries and those living in extreme poverty, frequently live close to areas in which sanitation is not existent. These areas include garbage deposits or city slums where the prevalence of flies generally is high. In the United States, one-third of cases of myiasis occur among homeless persons.26 The most common species of flies that can cause myiasis include Phaenicia sericata (green blowfly), Megaselia spp., and Cuterebra spp. in the United States, whereas Dermatobia hominis is more prevalent in Central and South America. Other species such as those members of the genus Cordylobia, Wohlfahrtia, and Sarcophaga are found more frequently in Europe, Asia, and Africa. In the United States, myiasis is reported more frequently in the southeastern and southwestern regions and more commonly from late spring to early fall.26-28 The life cycle of flies that cause myiasis varies depending on the species involved. The adult P. sericata deposits its eggs directly into the infected tissues. These eggs eventually develop into the larva and pupa. The life cycle is closed when pupas become adult flies. Other species such as D. hominis can capture other insects such as mosquitoes during their flight. Once having captured the mosquitoes, the fly attaches to the eggs and soon releases them. These mosquitoes then deposit the larvae into the target tissue. Some species of flies, such as members of the family Calliphoridae, have predilection for livestock but also can infest humans.22,26,27 The anatomical sites in which larvae are deposited in human hosts vary. Some species of flies have predilection for wounds, whereas others can affect normal tissues.28 Direct wound infestation may be clinically evident, whereas deposits of larvae into the subcutaneous tissue, such as occurs in furuncular myiasis, may offer a diagnostic challenge.29,30 Typically, a significant inflammatory reaction develops in the involved site and frequently is associated with ulceration and superinfection with bacterial pathogens. Myiasis involves more commonly exposed areas of the body such as ears and eyes.31-33 A study aimed to evaluate the epidemiology of myiasis among children in India reported that 86.16 percent of cases were aural, 11.7 percent were nasal, and 2.12 percent were ocular.34 Other anatomical areas such as the genitourinary and gastrointestinal tracts also may be involved. Umbilical myiasis caused by P. sericata has been reported in the neonatal period.35 Additionally,
Ectoparasitic Infestations in Homeless Children persons with leprosy who have decreased skin sensation are at increased risk of being infested with fly larvae.36,37 Practitioners need to be aware of the possibility that furuncular myiasis may be mistakenly diagnosed as bacterial furunculosis. In furuncular myiasis, the larva penetrates into the affected tissues, leaving small pores through which it can breath. If a bacterial infection has been suspected as the possible etiology of furunculosis and no improvement is observed with administration of standard antibiotic therapy, myiasis should be suspected.29,30 Different methods that have been advocated for the treatment of myiasis include application of terfinadine or chlorophorm to facilitate the removal of the larvae. Mechanical expulsion of the larva by applying pressure to the affected area frequently is considered as a therapeutic alternative. Although surgical extraction of the parasite is the preferred option, less traditional modalities such as application of mineral oil, petroleum jelly, or bacon to the site of infestation aimed to decrease oxygenation to the larvae also have been used. Snake venom extractors have been used successfully in the removal of larva in furuncular myiasis, and laser photocoagulation has been used in cases of ophthalmomyiasis. Although the number of studies is not sufficient to support the safety and efficacy of pharmacological therapy of myiasis, topical application of a solution containing 1 percent ivermectin in propylene glycol has been effective in the treatment of 4 patients infested with Cochliomyia hominivorax.34,38-41 The organisms most commonly associated with bacterial superinfection in patients with myiasis include S. aureus, Streptotoccus pyogenes, and Clostridium tetani. When bacterial infection is suspected, appropriate antibiotic therapy should be administered, and immunization against C. tetani should be considered.29,37,42
Tungiasis Tungiasis is an ectoparasitic infestation caused by the flea, Tunga penetrans, also known as chigo, nigua, or jigger flea. T. penetrans is a free-living arthropod, but it can penetrate the skin of the host, which may include humans and other mammal species such as dogs, cats, pigs, cattle, sheep, goats, horses, rats, and mice. After penetrating the stratum corneum, the gravid flea usually locates in the epidermis. Once inside the epidermis, it may remain in the host for several weeks. During this period, each flea may release approximately 200 eggs. After the gravid flea has released all its eggs, it dies, and the parasite is expelled.43-45 Although infestation with this arthropod has been reported in several areas within the United States, its prevalence is higher in areas such as the Caribbean, Latin America, Africa, and the Indian subcontinent. Dry soil is known to provide the appropriate environment for the development of T. penetrans. In tropical climates, tungiasis occurs more frequently during the dry season. This infestation is observed more commonly among children than in adults in developing countries, where its prevalence peaks in the 5- to 10-year-old group. Researchers have suggested
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that tungiasis occurs less frequently in adults because the increased keratinization of the skin may act as a barrier against penetration by the fleas through the epidermis. Homeless children and those living in extreme poverty who walk barefooted on unpaved streets are at high risk of acquiring infestation with this ectoparasite. Individuals infested with this parasite become symptomatic between 1 and 3 days after the flea has penetrated the epidermis.45-49 Typically, patients present with painful nodular skin lesions of the lower extremities, most commonly the feet, that appear progressively after walking barefoot in an endemic area. These lesions are approximately 6 mm in diameter, have a black center, and are located commonly in the subungal folds, interdigital spaces, and soles. Small children also are susceptible to infestations by fleas in other areas such as hands, neck, and genitals. Lesions secondary to infestation with T. penetrans can be differentiated histologically from those caused by scabies and myasis by the presence of exoskeleton, typical egg morphology, and distribution of the striated muscle of the parasite that are found in biopsy specimens of the affected patients.43,50 Tungiasis is not a systemic disease, but bacterial superinfection of the lesions is a relatively common occurrence. S. aureus and members of the family enterobacteriacea are the most common organisms associated with this infestation. However, superinfection with other organisms such as Bacillus spp., Enterococcus faecalis, Streptococcus pyogenes, Clostridium, Peptostreptococcus, or Pseudomonas spp. has been reported.51 The treatment of choice is removal of the fleas with a needle or through a small incision performed under sterile conditions. Successful treatment with antiparasitic drugs such as ivermectin and thiabendazole has been reported in several cases, including generalized tungiasis. Treatment with niridazole given orally also has been reported to be effective in the treatment of tungiasis in children. However, at the present time, no significant data support the safety and efficacy of these therapeutic modalities. The application of topical antibiotics to the site where the flea has been removed usually is indicated, and systemic antibiotic therapy may be necessary when bacterial superinfection occurs, especially when multiple lesions are involved. Researchers have recommended that patients diagnosed with tungiasis be immunized against Clostridium tetani because of the risk of developing superinfection with this organism. This disease can be prevented by wearing appropriate footwear and by performing frequent inspections of the potentially affected areas. Unfortunately, many homeless children and their families in the developing world where this parasite is most prevalent are not able to afford shoes.44,45
Conclusion In summary, homeless children and those living in extreme poverty are at increased risk of acquiring ectoparasitic infestations. The prevalence of different ectoparasitic diseases largely depends on environmental factors. Practitioners who care for these populations should become familiar
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with their clinical presentation, as well as with the diagnostic and therapeutic challenges with which they can be associated.
References 1. Zlotnick C: Pediculosis corporis and the homeless. J Community Health Nurs 4:43-48, 1987 2. Morrone A, Cavalloti C, Latini O, et al: Skin diseases in a population of homeless people. J Eur Acad Dermatol Venerol 15:593, 2000 3. Chosidow O: Scabies and pediculosis. Lancet 355:819-826, 2000 4. Raoult D, Roux V: The body louse as a vector of reemerging human diseases. Clin Infect Dis 29:888-911, 1999 5. Angel TA, Nigro J, Levy ML: Infestations in the pediatric patient. Pediatr Clin North Am 47:921-935, 2000 6. Raoult D, Foucault C, Brouqui P: Infections in the homeless. Lancet Infect Dis 1:77-84, 2001 7. La Scola B, Fournier PE, Brouqui P, et al: Detection and culture of Bartonella quintana, Serratia marcescens, and Acinetobacter spp from decontaminated human body lice. J Clin Microbiol 39:1707-1709, 2001 8. Spach DH, Kanter AS, Dougherty MJ, et al: Bartonella (Rochalimaea) quintana bacteremia in inner-city patients with chronic alcoholism. NEJM 332:424-428, 1995 9. Jackson LA, Spach DH: Emergence of Bartonella quintana among homeless persons. Emerg Infect Dis 2:141-144, 1996 10. Rooux V, Didier R: Body lice as tools for diagnosis and surveillance of reemerging diseases. J Clin Microbiol 37:596-599, 1999 11. Guibal F, de La Salmoniere P, Rybojad M, et al: High seroprevalence to Bartonella quintana in homeless patients with cutaneous parasitic infestation in downtown Paris. J Am Acad Dermatol 44:219-223, 2000 12. Brouqui P, Lascola B, Roux V, et al: Chronic Bartonella quintana bacteremia in homeless patients. NEJM 340:184-189, 1999 13. Rydkina EB, Roux V, Gagua EM, et al: Bartonella quintana in body lice collected from homeless persons in Russia. Emerg Infect Dis 5:176-178, 1999 14. Raoult D, Ndihokubwayo JB, Tissot-Dupont H, et al: Outbreak of epidemic typhus associated with trench fever in Burundi. Lancet 352:353-358, 1998 15. Rioult D, Roux V, Ndihokubwayo JB, et al: Jail fever (epidemic typhus) outbreak in Burundi. Emerg Infect Dis 3:357-360, 1997 16. World Health Organization: Epidemic typhus risk in Rwandan refugee camps. Wkly Epidemiol Rec 69: 259, 1994 17. Ndihokubwayo JB, Raoult D: Epidemic typhus in Africa. Med Trop 59:181-192, 1999 18. Brown V, Larouze B, Desve G, et al: Clinical presentation of louse-borne relapsing fever among Ethiopian refugees in northern Somalia. Ann Trop Med Parasitol 82:499-502, 1988 19. Terry BC, Kanjah F, Sahr F, et al: Sarcoptes scabiei infestation among children in a displacement camp in Sierra Leone. Public Health 115:208-211, 2001 20. Walker GJA, Johnstone PW: A systematic review of the treatment of scabies. Arch Dermatol 136:387-388, 2000 21. Victoria J, Trujillo R: Topical ivermectin: A new successful treatment for scabies. Pediatr Dermatol 18:63-65, 2001 22. Rao R, Nosanchuk JS, Mackenzie R: Cutaneous myiasis acquired in New York State. Pediatrics 99:601-602, 1997 23. Sucharit S, Tumrasvin W, Vutikes S: A survey of houseflies in Bangkok and neighboring provinces. Southeast Asian J Trop Med Public Health Mar(1):85-90, 1976 24. Ryan ME: Cutaneous myiasis in Pennsylvania. Pediatr Infect Dis 3:135-137, 1984
25. Noutsis C, Millikan LE: Myiasis. Dermatol Clin 12:729-736, 1994. 26. Sherman RA: Wound myiasis in urban and suburban United States. Arch Intern Med 160:2004-2014, 2000 27. Bapat SS: Neonatal myiasis. Pediatrics 106:E6, 2000 28. Martin AM, Montes I, Dominguez de Luis F: Otitis externa por larvas de mosca. Enferm Infec Microbiol Clin 19:403-405, 2001 29. Zywocinski KN: “Flies in the flesh”: A case report and review of cutaneous myiasis. Cutis 55:47-48, 1995 30. Boggild AK, Keystone JS, Kain KC: Furuncular myiasis: A simple and rapid method for extraction of intact Dermatobia hominis larvae. Clin Infect Dis 35:336-338, 2002 31. Gewirtzman A, Rabinovitz H: Botfly infestation (myiasis) masquerading as furunculosis. Cutis 63:71-72, 1999 32. Emborsky ME, Faden H: Ophthalmomyiasis in a child. Pediatr Infect Dis J 21:82-83, 2002 33. Engelbrecht NE, Yeatts RP: Palpebral myiasis causing preseptal cellulitis. Arch Ophtalmol 116:684, 1998 34. Goodman RL, Montalvo MA, Reed BJ, et al: Anterior orbital myiasis caused by human botfly (Dermatobia hominis). Arch Ophthalmol 118:1002-1003, 2000 35. Singh I, Gathwala G, Yadav SP, et al: Myiasis in children: The Indian perspective. Int J Pediatr Otorhinolaryngol 25:127-131, 1993 36. Szekely R, Herreros C, Rojo M: Human umbilical myiasis by Phanecia sericata in a newborn child. Bol Chil Parasitol 30:25-26, 1975 37. Husain S, Malaviya GN, Girdhar A, et al: Nasal myiasis in leprosy. Lepr Rev 62:389-394, 1991 38. Husain A, Malaviya GN, Husain S, et al: Characterization of microbial flora of leprous ulcers infested with maggots. Acta Leprol 8:143-147, 1993 39. Brewer TF, Wilson ME, Gonzales E, et al: Bacon therapy and furuncular myiasis. JAMA 270:2087-2088, 1993 40. Forman AR, Cruess AF, Benson WE: Ophthalmomyiasis treated by argon-laser photocoagulation. Retina 4:163-165, 1984 41. Victoria J, Trujillo R, Barreto M: Tropical medicine rounds. Int J Dermatol 38:142-144, 1999 42. Chin RL: Cellulitis due to botfly larvae. NEJM 337:429-430, 1997 43. Grunwald MH, Shai A, Mosovich B, et al: Tungiasis. Australas J Dermatol 41:46-47, 2000. 44. Gelmetti C, Carrera C, Veraldi S: Tungiasis in a 3-year-old child. Pediatr Dermatol 17:293-295, 2000 45. Heukelbach J, de Oliveira FAS, Hesse G, et al: Tungiasis: A neglected health problem of poor communities. Trop Med Int Health 6:267-272, 2001 46. Fein H, Naseem S, Witte DP, et al: Tungiasis in North America: A report of 2 cases in internationally adopted children. J Pediatr 139:744-746, 2001 47. Sansusi ID, Brown EB, Shepard TG, et al: Tungiasis: Report of one case and review of the 14 reported cases in the United States. J Am Acad Dermatol 20:941-944, 1989 48. Bell A, Neely CL, Peeples J: Tungiasis in Tennessee. South Med J 72:141-143, 1979 49. Brothers WS, Heckmann RA: Tungiasis in North America. Cutis 25:636-638, 1980 50. Smith MD, Procop GW: Typical histologic features of Tunga penetrans in skin biopsies. Arch Pathol Lab Med 126:714-716, 2002 51. Feldmeier H, Heukelbach J, Eisele M, et al: Bacterial superinfection in human tungiasis. Trop Med Int Health 7:559-564, 2002
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ignificant risk factors for acquiring ectoparasitic infestations exist among homeless children compared with the general population. Those factors include poverty associated with lack of hygiene and crowding, which frequently is observed in shelters, day drop-in centers, and refugee camps. The lack of financial resources frequently is reflected in poor sanitary conditions in many of these facilities. Environmental factors such as geographical location, humidity, and temperature also play roles in the development of ectoparasitosis among this population. Whereas some infestations such as Pediculosis corporis are more prevalent in areas of cold weather, others such as those caused by fly larvae and fleas are observed more frequently in areas with warm climates. Additionally, situations such as war and natural catastrophes commonly related to homelessness and displacement frequently are related to outbreaks of ectoparasitic infestations among children and their families.1,2
Body Lice Infestations Lice infestations have been prevalent among humans for thousands of years. The oldest eggs of Pediculus spp. have been found in the Judean desert and date from between 6900 to 6300 BC.3 Although more than three thousand species of lice exist, the only three that affect humans are Pediculus humanus capitis (head lice), Pediculus humanus
From the Division of Pediatric Infectious Diseases, University of South Alabama, Mobile, AL. Address reprint requests to Benjamin Estrada, Associate Professor of Pediatrics, Division of Pediatric Infectious Diseases, University of South Alabama, 1504 Springhill Avenue, #5222, Mobile, AL 36695; e-mail: [email protected] © 2003 Elsevier Inc. All rights reserved. 1045-1870/03/1401-0004$30.00/0 doi:10.1053/spid.2003.127213
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humanus (body lice), and Phthirus pubis. P. humanus capitis is known to affect all levels of society, P. pubis is transmitted sexually, and P. humanus humanus has been associated more frequently with conditions of lack of hygiene and extreme poverty.3,4 Consequently, infestation with P. humanus humanus, also known as “vagabond’s disease,” is an issue of concern among homeless children and their families, including those living in refugee camps.5 Particular environmental factors involved in the life cycle of this ectoparasite can play significant roles in the predisposition for infestation among homeless individuals. Close body-to-body contact is associated strongly with transmission of lice. For that reason, infestation occurs more frequently in crowded environments such as homeless shelters, refugee camps, and jails, especially when hygienic standards are lacking. Although the distribution of P. humanus humanus is universal, infestation with this parasite is more prevalent among homeless individuals who live in environments in which cold weather predominates and who need several layers of clothing to protect themselves from low temperatures, especially during the winter months. Lack of frequent changes of clothing among this population is a factor that favors the development of environmental conditions needed for the completion of the P. humanus humanus life cycle.1-6 Typically, lice lay their eggs in the folds of clothing, especially in areas that are particularly close to higher body temperature regions such as the genitals, axilla, and abdomen. If these eggs are held at constant temperatures, they usually hatch within 6 to 9 days. After hatching, the louse moves to the skin, where it feeds on human blood and returns to the clothing promptly after feeding. Other lice may be attracted to the area of infestation by the ammonium present in the parasite feces, which frequently are deposited in the garments. The optimal level of humidity for lice to survive is between 70 and 90 percent.3,4
Seminars in Pediatric Infectious Diseases, Vol 14, No 1 ( January), 2003: pp 20-24
Ectoparasitic Infestations in Homeless Children Individuals infested with body lice may harbor several hundred parasites. Although no skin lesions may be apparent initially, several weeks after infestation humans develop an allergic response to the biologically active proteins produce by lice, which may trigger intense pruritus with subsequent development of skin lesions. Consequently, these lesions may become superinfected by bacterial organisms such as Staphylococcus aureus and Streptococcus spp. The skin lesions caused by P. humanus typically present as red macules or papules more frequently localized around the abdomen and neck. Persons affected by this parasite occasionally may develop fever and adenopathy. In addition to these clinical findings, the presence of nits in clothing seams should be considered confirmatory evidence of infestation.4-6 The body lice is an efficient vector for bacteria that can cause systemic disease such as Bartonella quintana, Rickettsia prowasekii, and Borrellia recurrentis. Acinetobacter spp. and Serratia marcescens also have been isolated from body lice, but whether they can be transmitted by this ectoparasite is not known.4,6 Infection with B. quintana is the bacterial disease most frequently associated wth infestation of body lice. This organism is known to be the causative agent of Trench fever epidemics during World War I and II. During the last decade, different reports about the development of infection with this organism among homeless patients have linked it to infestation with body lice. Studies performed among homeless patients in the United States and France have demonstrated that the seroprevalence of antibodies against B. quintana in these populations is significantly high (25% and 30%, respectively).7-11 In a study performed in Russia, lice infestation occurred in 11 percent of patients included in the study population and B. quintana was detected by polymerase chain reaction (PCR) among 12.3 percent of louse samples collected from these patients.12 The spectrum of symptoms caused by infection with B. quintana includes an acute febrile illness associated with malaise, headache, a macular rash, bacillary angiomatosis, and chronic bacteremia. Patients may remain bacteremic with this organism for as long as one year, and episodes of endocarditis also have been reported. The recommended treatment for patients infected with B. quintana includes doxycycline and gentamicin, although other antibiotics such as erythromycin, rifampin, azithromycin, clarithromycin, and amoxicillin also have been reported to be effective.8 R. prowasekii, which causes epidemic typhus, is a louseborne disease that has been reported in situations such as war or famine, especially when lack of sanitation and crowding are likely to occur. Significant outbreaks of epidemic typhus occurred during the first half of the twentieth century, followed by a significant decrease on their occurrence.4 However, a resurgence of typhus after 1995 has been observed in countries such as Russia, Burundi, and Peru. Several recent outbreaks of epidemic typhus have been reported in refugee camps in Africa as well. Treatment with tetracycline and chloramphenicol is effective against R. prowasekii; however, a single dose of doxycycline for chil-
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dren older than 8 years probably is the most effective therapy.13-17 B. recurrentis is another organism that can be transmitted efficiently by body lice. This bacterium is the etiologic agent of outbreaks of relapsing fever, which have been reported recently among displaced individuals in African refugee camps. The antibiotics recommended in the treatment of relapsing fever include penicillin, chloramphenicol, tetracycline, and erythromycin.4,18 The development of bacterial infections associated with P. humanus can be prevented by implementing strategies aimed to reduce infestation of body lice. Because the body louse resides in the individual’s clothing and not on the human body, the most effective therapeutic modality for its eradication is frequent changing and cleaning of bedding and clothing, including underwear. In homeless shelters, bedding should be washed with hot water and treated with insecticides daily. The clothes should be washed with hot water, and some investigations recommend the application to this garment of insecticides such as DDT, 1 percent Malathion, or 1 percent permethrin.1,5 Although successful treatment with ivermectin given in two doses 200 mg/kg/dose 10 days apart has been reported effective in the treatment of individuals with head lice, systemic treatment for those infested with body lice is not recommended. For older children and adolescents with heavy infestations of lice, application of gamma benzene hexachloride (lindane) lotion has been used. However, this product can be absorbed through the skin, and it has been associated with neurological adverse effects, such as epileptiform convulsions and muscle spasms. For that reason, its application in young children is not recommended. An additional disadvantage of the use of lindane lotion is that this formulation must remain on the skin for approximately 12 hours after its application. Because of this requirement, it usually is not a practical therapeutic approach because homeless individuals often visit shelters for shorter periods of time. A more practical option for treatment of lice among the homeless adult population seems to be the application of lindane shampoo, which must remain in contact with the skin for only five minutes. The effectiveness of this approach may increase if it is coupled with delousing of bedding and clothing as previously described.1,4
Scabies Scabies is an ectoparasitic disease caused by Sarcoptes scabiei var hominis. This ectoparasitosis has been known to infect humans for thousands of years. The main route of transmission is skin-to-skin contact, but indirect infestation with fomites also can occur. Lack of hygiene, poverty, and crowded environments have been identified as significant risk factors that favor the transmission of this parasite.3 Scabies has been reported to be a significant problem in homeless shelters and refugee camps, as well as among the general population in developing countries. Observations reveal that the prevalence of scabies among children younger than 5 years of age living in displacement camps
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may be as high as 77 percent and increases to 86 percent among those who are 5 to 9 years old.19 Typically, the mites of S. scabiei develop tunnels into the epidermis mainly through the stratum corneum. They deposit feces, and females lay their eggs between the stratum corneum and the stratum granulosum. The incubation period of S. scabiei is 3 weeks. The most significant clinical finding is generalized nocturnal pruritus. The lesions observed in patients with scabies include burrows and nodules with associated significant excoriation. In children, the lesions generally involve wrists, elbows, axilla, neck, and interdigital spaces. Scabies in children may present as vesicles and pustules involving the hands and feet, including palms and soles. Occasionally, the lesions present in a generalized distribution, which may include the scalp among young infants and immunocompromised patients. In many cases, the original lesions may become superinfected with Streptococcus or Staphylococcus spp.3 Helpful tools in the diagnosis of scabies include skin scrapings or skin biopsies in which mites may be identified. If possible, laboratory diagnosis of scabies should be performed among homeless children because other skin diseases in this particular population, such as acropustulosis, postscabeitic nonspecific reactions, atopic dermatitis, and contact dermatitis, have similar clinical characteristics.3 Several medications, including permethrin, lindane, benzyl benzoate, crotamiton, and ivermectin, are used to treat scabies. Application of benzyl benzoate 10 percent and 25 percent lotion is utilized widely in the treatment of scabies. This product should be washed thoroughly from the skin 12 to 24 hours after application and generally is safe for use in children. Permethrin 5 percent cream is considered by many physicians to be the first-line therapy among children older than 2 months. Permethrin is well tolerated and should be rinsed well 8 to 12 hours after its application. Additionally, it has been associated with fewer side effects than have other scabicides such as lindane, particularly in children. Although the antiscabeitic efficacy of lindane compounds is very similar to that of permethrin, it should not be used in young children because of the potential for causing side effects previously discussed in this review. In older children, this alternative should be used only if other regimens have failed.3,20 Topical scabicides should be applied after a bath to the entire skin, including groin, fingernails, toenails, and retroauricular areas, avoiding mucous membranes. All infested individuals and their household contacts should be treated. In addition, clothes and bed linen should be washed carefully.3,5 Treatment with a single dose of oral ivermectin 100 g/kg to 200 g/kg has been reported to be effective among adults with scabies, including patients infected with human immunodeficiency virus (HIV). The mechanism of action of this drug is that it interrupts S. scabiei neurotransmission. The topical application of a 1 percent solution of ivermectin recently was reported to be effective in the treatment of scabies in children. Although this therapeutic approach
seems to be practical, no data support its safety or efficacy in children at the present time.21
Myiasis Myiasis is the infestation caused by dipterous larvae also known as “maggots.” Although myiasis occurs more commonly in tropical countries, it does occur worldwide.22-25 Homeless children are at increased risk of exposure to flies for different reasons. First, they live in poorly protected environments with lack of hygiene. Soiled clothing on these children attracts flies, especially among those who are not yet toilet trained. Additionally, abandoned children, especially those in developing countries and those living in extreme poverty, frequently live close to areas in which sanitation is not existent. These areas include garbage deposits or city slums where the prevalence of flies generally is high. In the United States, one-third of cases of myiasis occur among homeless persons.26 The most common species of flies that can cause myiasis include Phaenicia sericata (green blowfly), Megaselia spp., and Cuterebra spp. in the United States, whereas Dermatobia hominis is more prevalent in Central and South America. Other species such as those members of the genus Cordylobia, Wohlfahrtia, and Sarcophaga are found more frequently in Europe, Asia, and Africa. In the United States, myiasis is reported more frequently in the southeastern and southwestern regions and more commonly from late spring to early fall.26-28 The life cycle of flies that cause myiasis varies depending on the species involved. The adult P. sericata deposits its eggs directly into the infected tissues. These eggs eventually develop into the larva and pupa. The life cycle is closed when pupas become adult flies. Other species such as D. hominis can capture other insects such as mosquitoes during their flight. Once having captured the mosquitoes, the fly attaches to the eggs and soon releases them. These mosquitoes then deposit the larvae into the target tissue. Some species of flies, such as members of the family Calliphoridae, have predilection for livestock but also can infest humans.22,26,27 The anatomical sites in which larvae are deposited in human hosts vary. Some species of flies have predilection for wounds, whereas others can affect normal tissues.28 Direct wound infestation may be clinically evident, whereas deposits of larvae into the subcutaneous tissue, such as occurs in furuncular myiasis, may offer a diagnostic challenge.29,30 Typically, a significant inflammatory reaction develops in the involved site and frequently is associated with ulceration and superinfection with bacterial pathogens. Myiasis involves more commonly exposed areas of the body such as ears and eyes.31-33 A study aimed to evaluate the epidemiology of myiasis among children in India reported that 86.16 percent of cases were aural, 11.7 percent were nasal, and 2.12 percent were ocular.34 Other anatomical areas such as the genitourinary and gastrointestinal tracts also may be involved. Umbilical myiasis caused by P. sericata has been reported in the neonatal period.35 Additionally,
Ectoparasitic Infestations in Homeless Children persons with leprosy who have decreased skin sensation are at increased risk of being infested with fly larvae.36,37 Practitioners need to be aware of the possibility that furuncular myiasis may be mistakenly diagnosed as bacterial furunculosis. In furuncular myiasis, the larva penetrates into the affected tissues, leaving small pores through which it can breath. If a bacterial infection has been suspected as the possible etiology of furunculosis and no improvement is observed with administration of standard antibiotic therapy, myiasis should be suspected.29,30 Different methods that have been advocated for the treatment of myiasis include application of terfinadine or chlorophorm to facilitate the removal of the larvae. Mechanical expulsion of the larva by applying pressure to the affected area frequently is considered as a therapeutic alternative. Although surgical extraction of the parasite is the preferred option, less traditional modalities such as application of mineral oil, petroleum jelly, or bacon to the site of infestation aimed to decrease oxygenation to the larvae also have been used. Snake venom extractors have been used successfully in the removal of larva in furuncular myiasis, and laser photocoagulation has been used in cases of ophthalmomyiasis. Although the number of studies is not sufficient to support the safety and efficacy of pharmacological therapy of myiasis, topical application of a solution containing 1 percent ivermectin in propylene glycol has been effective in the treatment of 4 patients infested with Cochliomyia hominivorax.34,38-41 The organisms most commonly associated with bacterial superinfection in patients with myiasis include S. aureus, Streptotoccus pyogenes, and Clostridium tetani. When bacterial infection is suspected, appropriate antibiotic therapy should be administered, and immunization against C. tetani should be considered.29,37,42
Tungiasis Tungiasis is an ectoparasitic infestation caused by the flea, Tunga penetrans, also known as chigo, nigua, or jigger flea. T. penetrans is a free-living arthropod, but it can penetrate the skin of the host, which may include humans and other mammal species such as dogs, cats, pigs, cattle, sheep, goats, horses, rats, and mice. After penetrating the stratum corneum, the gravid flea usually locates in the epidermis. Once inside the epidermis, it may remain in the host for several weeks. During this period, each flea may release approximately 200 eggs. After the gravid flea has released all its eggs, it dies, and the parasite is expelled.43-45 Although infestation with this arthropod has been reported in several areas within the United States, its prevalence is higher in areas such as the Caribbean, Latin America, Africa, and the Indian subcontinent. Dry soil is known to provide the appropriate environment for the development of T. penetrans. In tropical climates, tungiasis occurs more frequently during the dry season. This infestation is observed more commonly among children than in adults in developing countries, where its prevalence peaks in the 5- to 10-year-old group. Researchers have suggested
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that tungiasis occurs less frequently in adults because the increased keratinization of the skin may act as a barrier against penetration by the fleas through the epidermis. Homeless children and those living in extreme poverty who walk barefooted on unpaved streets are at high risk of acquiring infestation with this ectoparasite. Individuals infested with this parasite become symptomatic between 1 and 3 days after the flea has penetrated the epidermis.45-49 Typically, patients present with painful nodular skin lesions of the lower extremities, most commonly the feet, that appear progressively after walking barefoot in an endemic area. These lesions are approximately 6 mm in diameter, have a black center, and are located commonly in the subungal folds, interdigital spaces, and soles. Small children also are susceptible to infestations by fleas in other areas such as hands, neck, and genitals. Lesions secondary to infestation with T. penetrans can be differentiated histologically from those caused by scabies and myasis by the presence of exoskeleton, typical egg morphology, and distribution of the striated muscle of the parasite that are found in biopsy specimens of the affected patients.43,50 Tungiasis is not a systemic disease, but bacterial superinfection of the lesions is a relatively common occurrence. S. aureus and members of the family enterobacteriacea are the most common organisms associated with this infestation. However, superinfection with other organisms such as Bacillus spp., Enterococcus faecalis, Streptococcus pyogenes, Clostridium, Peptostreptococcus, or Pseudomonas spp. has been reported.51 The treatment of choice is removal of the fleas with a needle or through a small incision performed under sterile conditions. Successful treatment with antiparasitic drugs such as ivermectin and thiabendazole has been reported in several cases, including generalized tungiasis. Treatment with niridazole given orally also has been reported to be effective in the treatment of tungiasis in children. However, at the present time, no significant data support the safety and efficacy of these therapeutic modalities. The application of topical antibiotics to the site where the flea has been removed usually is indicated, and systemic antibiotic therapy may be necessary when bacterial superinfection occurs, especially when multiple lesions are involved. Researchers have recommended that patients diagnosed with tungiasis be immunized against Clostridium tetani because of the risk of developing superinfection with this organism. This disease can be prevented by wearing appropriate footwear and by performing frequent inspections of the potentially affected areas. Unfortunately, many homeless children and their families in the developing world where this parasite is most prevalent are not able to afford shoes.44,45
Conclusion In summary, homeless children and those living in extreme poverty are at increased risk of acquiring ectoparasitic infestations. The prevalence of different ectoparasitic diseases largely depends on environmental factors. Practitioners who care for these populations should become familiar
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with their clinical presentation, as well as with the diagnostic and therapeutic challenges with which they can be associated.
References 1. Zlotnick C: Pediculosis corporis and the homeless. J Community Health Nurs 4:43-48, 1987 2. Morrone A, Cavalloti C, Latini O, et al: Skin diseases in a population of homeless people. J Eur Acad Dermatol Venerol 15:593, 2000 3. Chosidow O: Scabies and pediculosis. Lancet 355:819-826, 2000 4. Raoult D, Roux V: The body louse as a vector of reemerging human diseases. Clin Infect Dis 29:888-911, 1999 5. Angel TA, Nigro J, Levy ML: Infestations in the pediatric patient. Pediatr Clin North Am 47:921-935, 2000 6. Raoult D, Foucault C, Brouqui P: Infections in the homeless. Lancet Infect Dis 1:77-84, 2001 7. La Scola B, Fournier PE, Brouqui P, et al: Detection and culture of Bartonella quintana, Serratia marcescens, and Acinetobacter spp from decontaminated human body lice. J Clin Microbiol 39:1707-1709, 2001 8. Spach DH, Kanter AS, Dougherty MJ, et al: Bartonella (Rochalimaea) quintana bacteremia in inner-city patients with chronic alcoholism. NEJM 332:424-428, 1995 9. Jackson LA, Spach DH: Emergence of Bartonella quintana among homeless persons. Emerg Infect Dis 2:141-144, 1996 10. Rooux V, Didier R: Body lice as tools for diagnosis and surveillance of reemerging diseases. J Clin Microbiol 37:596-599, 1999 11. Guibal F, de La Salmoniere P, Rybojad M, et al: High seroprevalence to Bartonella quintana in homeless patients with cutaneous parasitic infestation in downtown Paris. J Am Acad Dermatol 44:219-223, 2000 12. Brouqui P, Lascola B, Roux V, et al: Chronic Bartonella quintana bacteremia in homeless patients. NEJM 340:184-189, 1999 13. Rydkina EB, Roux V, Gagua EM, et al: Bartonella quintana in body lice collected from homeless persons in Russia. Emerg Infect Dis 5:176-178, 1999 14. Raoult D, Ndihokubwayo JB, Tissot-Dupont H, et al: Outbreak of epidemic typhus associated with trench fever in Burundi. Lancet 352:353-358, 1998 15. Rioult D, Roux V, Ndihokubwayo JB, et al: Jail fever (epidemic typhus) outbreak in Burundi. Emerg Infect Dis 3:357-360, 1997 16. World Health Organization: Epidemic typhus risk in Rwandan refugee camps. Wkly Epidemiol Rec 69: 259, 1994 17. Ndihokubwayo JB, Raoult D: Epidemic typhus in Africa. Med Trop 59:181-192, 1999 18. Brown V, Larouze B, Desve G, et al: Clinical presentation of louse-borne relapsing fever among Ethiopian refugees in northern Somalia. Ann Trop Med Parasitol 82:499-502, 1988 19. Terry BC, Kanjah F, Sahr F, et al: Sarcoptes scabiei infestation among children in a displacement camp in Sierra Leone. Public Health 115:208-211, 2001 20. Walker GJA, Johnstone PW: A systematic review of the treatment of scabies. Arch Dermatol 136:387-388, 2000 21. Victoria J, Trujillo R: Topical ivermectin: A new successful treatment for scabies. Pediatr Dermatol 18:63-65, 2001 22. Rao R, Nosanchuk JS, Mackenzie R: Cutaneous myiasis acquired in New York State. Pediatrics 99:601-602, 1997 23. Sucharit S, Tumrasvin W, Vutikes S: A survey of houseflies in Bangkok and neighboring provinces. Southeast Asian J Trop Med Public Health Mar(1):85-90, 1976 24. Ryan ME: Cutaneous myiasis in Pennsylvania. Pediatr Infect Dis 3:135-137, 1984
25. Noutsis C, Millikan LE: Myiasis. Dermatol Clin 12:729-736, 1994. 26. Sherman RA: Wound myiasis in urban and suburban United States. Arch Intern Med 160:2004-2014, 2000 27. Bapat SS: Neonatal myiasis. Pediatrics 106:E6, 2000 28. Martin AM, Montes I, Dominguez de Luis F: Otitis externa por larvas de mosca. Enferm Infec Microbiol Clin 19:403-405, 2001 29. Zywocinski KN: “Flies in the flesh”: A case report and review of cutaneous myiasis. Cutis 55:47-48, 1995 30. Boggild AK, Keystone JS, Kain KC: Furuncular myiasis: A simple and rapid method for extraction of intact Dermatobia hominis larvae. Clin Infect Dis 35:336-338, 2002 31. Gewirtzman A, Rabinovitz H: Botfly infestation (myiasis) masquerading as furunculosis. Cutis 63:71-72, 1999 32. Emborsky ME, Faden H: Ophthalmomyiasis in a child. Pediatr Infect Dis J 21:82-83, 2002 33. Engelbrecht NE, Yeatts RP: Palpebral myiasis causing preseptal cellulitis. Arch Ophtalmol 116:684, 1998 34. Goodman RL, Montalvo MA, Reed BJ, et al: Anterior orbital myiasis caused by human botfly (Dermatobia hominis). Arch Ophthalmol 118:1002-1003, 2000 35. Singh I, Gathwala G, Yadav SP, et al: Myiasis in children: The Indian perspective. Int J Pediatr Otorhinolaryngol 25:127-131, 1993 36. Szekely R, Herreros C, Rojo M: Human umbilical myiasis by Phanecia sericata in a newborn child. Bol Chil Parasitol 30:25-26, 1975 37. Husain S, Malaviya GN, Girdhar A, et al: Nasal myiasis in leprosy. Lepr Rev 62:389-394, 1991 38. Husain A, Malaviya GN, Husain S, et al: Characterization of microbial flora of leprous ulcers infested with maggots. Acta Leprol 8:143-147, 1993 39. Brewer TF, Wilson ME, Gonzales E, et al: Bacon therapy and furuncular myiasis. JAMA 270:2087-2088, 1993 40. Forman AR, Cruess AF, Benson WE: Ophthalmomyiasis treated by argon-laser photocoagulation. Retina 4:163-165, 1984 41. Victoria J, Trujillo R, Barreto M: Tropical medicine rounds. Int J Dermatol 38:142-144, 1999 42. Chin RL: Cellulitis due to botfly larvae. NEJM 337:429-430, 1997 43. Grunwald MH, Shai A, Mosovich B, et al: Tungiasis. Australas J Dermatol 41:46-47, 2000. 44. Gelmetti C, Carrera C, Veraldi S: Tungiasis in a 3-year-old child. Pediatr Dermatol 17:293-295, 2000 45. Heukelbach J, de Oliveira FAS, Hesse G, et al: Tungiasis: A neglected health problem of poor communities. Trop Med Int Health 6:267-272, 2001 46. Fein H, Naseem S, Witte DP, et al: Tungiasis in North America: A report of 2 cases in internationally adopted children. J Pediatr 139:744-746, 2001 47. Sansusi ID, Brown EB, Shepard TG, et al: Tungiasis: Report of one case and review of the 14 reported cases in the United States. J Am Acad Dermatol 20:941-944, 1989 48. Bell A, Neely CL, Peeples J: Tungiasis in Tennessee. South Med J 72:141-143, 1979 49. Brothers WS, Heckmann RA: Tungiasis in North America. Cutis 25:636-638, 1980 50. Smith MD, Procop GW: Typical histologic features of Tunga penetrans in skin biopsies. Arch Pathol Lab Med 126:714-716, 2002 51. Feldmeier H, Heukelbach J, Eisele M, et al: Bacterial superinfection in human tungiasis. Trop Med Int Health 7:559-564, 2002