Infestation of a diabetic foot by Wohlfahrtia magnifica

Myiasis is the infestation of animals or humans by larvae from some species of dipteran flies. Depending on the tissues invaded, the maggots of these insects can produce different diseases of the skin, or mucoses (ocular, genitourinary, and oropharyngeal). Wohlfahrtia magnifica is one of the species causing myiasis; although it is a real veterinary problem, it rarely infests humans and extraordinarily in the context we describe. We herein present the case of a diabetic patient diagnosed with class IV peripheral vascular disease (Fontaine classification) who suffered infestation by W. magnifica and the management given to this pathologic process. The patient consented to the publication of this report. Myiasis is the infestation of animals or humans by larvae from some species of dipteran flies. Depending on the tissues invaded, the maggots of these insects can produce different diseases of the skin, or mucoses (ocular, genitourinary, and oropharyngeal). Wohlfahrtia magnifica is one of the species causing myiasis; although it is a real veterinary problem, it rarely infests humans and extraordinarily in the context we describe. We herein present the case of a diabetic patient diagnosed with class IV peripheral vascular disease (Fontaine classification) who suffered infestation by W. magnifica and the management given to this pathologic process. The patient consented to the publication of this report. A 62-year-old man attended the emergency department with an ulcer in the base of the right foot toes. Visual inspection revealed involvement of the second and third toes and their interdigital and digitoplantar folds, exhibiting necrotic tissue and several insect larvae that were sent to the microbiology laboratory (Figs 1 and 2). The parasites were not confined to the areas of tissue necrosis but rather seemed to feed also on adjacent healthy tissue. Femoral and popliteal arterial pulses were positive and posterior tibial and dorsalis pedis pulses were negative bilaterally. The ankle-brachial pressure indices were 0.55 and 0.68 in the right and left limbs, respectively, with compressible vessels and a capillary refill time longer than 2 seconds. Measurement of toe pressures in the affected foot was deemed unadvisable because of the necrotic, contaminated, and fragile condition of the tissues in the diseased forefoot.Fig 2Macroscopic appearance and specific features of larvae of Wohlfahrtia magnifica. A, The length reaches 13 mm. B, In the frontal view of the cephalic segment, instar III larvae exhibit a system of mouth hooks formed by only one pair of thick and long curved hooks. C, Posterior portieres of instar III. The posterior spiracle displays a button area slightly chitinized and two incomplete rings (peritremes). The peritremes have three variably shaped peritremal slits: the inner one is curved, the median one is straight and long, and the outer one is curved and long.View Large Image Figure ViewerDownload (PPT) The patient had a history of insulin-dependent diabetes mellitus with poor glycemic control, poor personal hygiene, moderate alcohol intake, and tobacco smoking (20 cigarettes/day). He underwent percutaneous transluminal coronary angioplasty and stenting of the left anterior descending, circumflex, and right coronary arteries 9 years before. The values of blood tests at admission were as follows: 17,000 leukocytes/μL with 6% band neutrophils; glycemia, 379 mg/dL; C-reactive protein, 32 mg/L; lactate, 9.9 mg/dL; and procalcitonin, 0.61 ng/mL. The initial management included thorough scrubbing of the extremity and a 4-hour immersion of the affected foot in povidone-iodine solution to eradicate any residual maggots. Initial treatment included intravenous daptomycin, aztreonam, and metronidazole as an empirical broad-spectrum protocol. It was changed to intravenous piperacillin-tazobactam 24 hours after admission, which was maintained until the fourth day after revascularization, when it was de-escalated to oral treatment with ciprofloxacin and clindamycin for 2 weeks. No parasite-specific pharmacologic treatment was used because no recurrence of the myiasis was detected after the initial management. Arteriography of the lower limbs (Fig 3) disclosed a nonsignificant stenosis of the right femoropopliteal junction with a well-developed artery and a severe ostial stenosis of the right peroneal artery with good caliber in all its segments. The anterior tibial artery was occluded in its proximal segment and refilled in its diseased distal third through collateral circulation. The posterior tibial artery was filiform and tapered in its middle segment (Fig 3). The patient underwent revascularization with a Y bypass from right distal popliteal to anterior tibial and peroneal arteries using inverted saphenous vein. The infected forefoot was debrided, and the first three toes were amputated. The amputation stump was left open, and a vacuum-assisted closure system was installed to enhance the granulation process. The larvae obtained from the patient (n = 6) were identified as third instar larvae of Wohlfahrtia magnifica, commonly named spotted flesh fly (Fig 2). After 20 days of vacuum-assisted closure therapy, the wound was closed with a free full-thickness skin graft covering the debrided area from the first metatarsal head to the lateral edge of the forefoot stump. Healing of the graft boundaries was slow and required administration of platelet-rich plasma gel to enhance tissue growth. The healing was complete within 25 weeks after the revascularization surgery. The patient was discharged from the hospital and observed in the diabetic foot clinic (Fig 3). In the case herein reported, the affected territory belonged almost entirely to the angiosome corresponding to the anterior tibialis, and therefore this was our main target according to the principle of angiosome-guided revascularization.1Attinger C. Cooper P. Blume P. Bulan E. The safest surgical incisions and amputations applying the angiosome principles and using the Doppler to assess the arterial-arterial connections of the foot and ankle.Foot Ankle Clin. 2001; 6: 745-799Abstract Full Text Full Text PDF PubMed Scopus (79) Google Scholar, 2Terashi H. Iwayama T. Iida O. Kitano I. Tsuji Y. Dynamic skin perfusion pressure: a new measure of assessment for wound healing capacity and alternative angiosome in critical limb ischemia.Plast Reconstr Surg. 2010; 126: 215e-218eCrossref PubMed Scopus (10) Google Scholar However, because the peroneal was the least atheromatous and the larger vessel, whereas the distal segment of the occluded anterior tibialis was patent but smaller and diseased, we constructed a Y graft to increase the odds of graft patency and eventually to improve foot perfusion. Three species of flies cause most cutaneous myiases in humans: Cochliomyia hominivorax, Chrysomyia bezziana, and W. magnifica.3Francesconi F. Lupi O. Myiasis.Clin Microbiol Rev. 2012; 25: 79-105Crossref PubMed Scopus (294) Google Scholar, 4Salimi M. Goodarzi D. Karimfar M. Edalat H. Human urogenital myiasis caused by Lucilia sericata (Diptera: Calliphoridae) and Wohlfahrtia magnifica (Diptera: Sarcophagidae) in Markazi Province of Iran.Iran J Arthropod Borne Dis. 2010; 4: 72-76PubMed Google Scholar, 5McGraw T. Turiansky G. Cutaneous myiasis.J Am Acad Dermatol. 2008; 58: 907-926Abstract Full Text Full Text PDF PubMed Scopus (137) Google Scholar, 6Robbins K. Kachemoune A. Cutaneous myiasis: a review of the common types of myiasis.Int J Dermatol. 2010; 49: 1092-1098Crossref PubMed Scopus (127) Google Scholar Although W. magnifica can infest individuals without any recognizable predisposing characteristics,3Francesconi F. Lupi O. Myiasis.Clin Microbiol Rev. 2012; 25: 79-105Crossref PubMed Scopus (294) Google Scholar patients who suffer myiasis frequently accumulate risk factors including poor personal hygiene and socioeconomic status, advanced age, psychiatric disease, alcohol abuse, peripheral vascular disease, diabetes mellitus, skin ulcers, and open wounds. A poor health care environment, as in armed conflicts and natural disasters, and limited visual acuity that hampers the correct evaluation by the patient of the extent of wounds and the presence of flies or maggots also facilitate the infestation.3Francesconi F. Lupi O. Myiasis.Clin Microbiol Rev. 2012; 25: 79-105Crossref PubMed Scopus (294) Google Scholar The disease is far more common in cattle or other warm-blooded domestic or wild animals than in humans. The parasitic phase is obligatory for W. magnifica to complete its vital cycle. Adult females are larviparous; they lay 120 to 170 eggs that hatch in the uterus and are delivered as larvae that penetrate the skin of a debilitated human and advance through the subcutaneous tissue to feed, producing painful wounds.7Ruíz Martínez I. Soler Cruz M.D. Benítez Rodríguez R. Pérez Jiménez J.M. Díaz López M. Postembryonic development of Wohlfahrtia magnifica.J Parasitol. 1989; 75: 531-539Crossref PubMed Scopus (28) Google Scholar The maggots undergo maturation for 5 to 7 days within the tissue, and meanwhile the host develops a cyst surrounding a group of parasites that drains its content outward, allowing the fall of the larvae to the ground to pupate.3Francesconi F. Lupi O. Myiasis.Clin Microbiol Rev. 2012; 25: 79-105Crossref PubMed Scopus (294) Google Scholar, 8Sotiraki S. Farkas S. Hall M.J. Fleshflies in the flesh: epidemiology, population genetics and control of outbreaks of traumatic myiasis in the Mediterranean Basin.Vet Parasitol. 2010; 174: 12-18Crossref PubMed Scopus (29) Google Scholar The adult female flies feed always on living warm-blooded animals and not on dead tissue. These insects are thermophilic so that their development rate slows when temperatures get colder. The differential diagnosis between infesting larvae is usually based on the clinical picture, exploration findings, and entomologic analysis on the stage of the larvae. Often, however, the maggots must be raised on culture media or meat until pupation, at which time the adult fly morphology allows an easier diagnosis. Medicinal maggots feed almost exclusively on necrotic tissue and respect living tissue, which is a key feature for their use as active debriders of wounds. In addition, their risk of inducing iatrogenic myiasis is negligible. Lucilia (or Phaenicia) sericata is the species generally considered most appropriate for maggot therapy.1Attinger C. Cooper P. Blume P. Bulan E. The safest surgical incisions and amputations applying the angiosome principles and using the Doppler to assess the arterial-arterial connections of the foot and ankle.Foot Ankle Clin. 2001; 6: 745-799Abstract Full Text Full Text PDF PubMed Scopus (79) Google Scholar The association of peripheral vascular disease and diabetes mellitus with wound myiases is well known.9Sherman R.A. Wound myiasis in urban and suburban United States.Arch Intern Med. 2000; 160: 2004-2014Crossref PubMed Scopus (119) Google Scholar, 10Szakacs T.A. MacPherson P. Sinclair B.J. Gill B.D. McCarthy A.E. Nosocomial myiasis in a Canadian intensive care unit.CMAJ. 2007; 177: 719-720Crossref PubMed Scopus (11) Google Scholar Neuropathic ulcers have also been identified as a favorable substrate for the development of wound myiasis.3Francesconi F. Lupi O. Myiasis.Clin Microbiol Rev. 2012; 25: 79-105Crossref PubMed Scopus (294) Google Scholar Olea et al reported infestation by C. hominivorax in a diabetic patient with a painless neurotrophic ulcer of the heel.11Olea M.S. Centeno N. Aybar C.A. Ortega E.S. Galante G.B. Olea L. et al.First report of myiasis caused by Cochliomyia hominivorax (Diptera: Calliphoridae) in a diabetic foot ulcer patient in Argentina.Korean J Parasitol. 2014; 52: 89-92Crossref PubMed Scopus (16) Google Scholar Diabetic patients are prone to development of ulcers related to a peripheral neuropathy (affecting motor, sensory, and autonomic components), macrovascular and microvascular angiopathy, and often dysfunction of the immune system.12Clayton W. Elasy T.A. A review of the pathophysiology, classification, and treatment of foot ulcers in diabetic patients.Clin Diabetes. 2009; 27: 52-58Crossref Scopus (113) Google Scholar As commonly seen in human myiasis, the infestation in our patient occurred in summer, a favorable season for the biologic activity of the flies.3Francesconi F. Lupi O. Myiasis.Clin Microbiol Rev. 2012; 25: 79-105Crossref PubMed Scopus (294) Google Scholar, 11Olea M.S. Centeno N. Aybar C.A. Ortega E.S. Galante G.B. Olea L. et al.First report of myiasis caused by Cochliomyia hominivorax (Diptera: Calliphoridae) in a diabetic foot ulcer patient in Argentina.Korean J Parasitol. 2014; 52: 89-92Crossref PubMed Scopus (16) Google Scholar Treatment of the myiasis was simple and efficacious in the case reported, but this does not imply that differential diagnosis of the disease is unimportant. If we focus on wound myiasis, there are species whose larvae remain within the necrotic tissue, whereas others continue to feed on adjacent living tissue and may be the cause of subcutaneous nodules.13Noutsis C. Millikan L.E. Myiasis.Dermatol Clin. 1994; 12: 729-736PubMed Google Scholar Hence, an appropriate differential diagnosis is important because it has prognostic implications. Furthermore, the global climate change and the human migration flows are modifying the geographic distribution of many species, including arthropods, at a worrying pace, and therefore the precise entomologic diagnosis of the agents causing rare human parasitic entities like the one reported is also warranted for epidemiologic and public health purposes. The treatment of myiasis requires debridement of the necrotic tissue and removal of the larvae in the wound. A multidisciplinary approach with entomologic diagnosis, adequate medical and surgical treatments, and excellent revascularization and reconstructive procedures allows a favorable outcome.

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