Cutaneous Manifestations of a Zoonotic Onchocerca Species in an Adult Male acquired in Nova Scotia: Report of a Case and Review of the Literature
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1 JCM Accepts, published online ahead of print on 5 February 2014 J. Clin. Microbiol. doi: /jcm Copyright 2014, American Society for Microbiology. All Rights Reserved Cutaneous Manifestations of a Zoonotic Onchocerca Species in an Adult Male acquired in Nova Scotia: Report of a Case and Review of the Literature Jonathan H. Lai MD, FRCP(C) 1 ; Noreen M.G. Walsh MD, FRCP(C), FRCPath (UK) 1 ; Bobbi S. Pritt MD, MSc., (D)TMH 2 ; Lynne Sloan MT (ASCP) 2 ; Lawrence E. Gibson, MD 3, 4 ; Leon Desormeau MD, FRCP(C) 5 ; David J.M. Haldane MB, FRCP(C) 6 1 Division of Anatomical Pathology, Department of Pathology and Laboratory Medicine, Capital District Health Authority and Dalhousie University, Halifax, NS, Canada 2 Division of Infectious Diseases and Clinical Microbiology, Department of Pathology and Laboratory Medicine, Mayo Clinic, Rochester, MN, United States of America 3 Division of Anatomical Pathology, Department of Pathology and Laboratory Medicine, Mayo Clinic, Rochester, MN, United States of America 4 Department of Dermatology, Mayo Clinic, Rochester, MN, United States of America 5 Department of Pathology and Laboratory Medicine, St. Martha s Regional Hospital, Antigonish, NS, Canada 6 Division of Microbiology, Department of Pathology and Laboratory Medicine, Capital District Health Authority and Dalhousie University, Halifax, NS, Canada Contact Information: David J. M. Haldane MB, ChB, FRCP(C) Director Provincial Public Health Laboratory Network Director of Special Pathogens (CDHA) Division of Microbiology, Department of Pathology and Laboratory Medicine. Rm 326, Mackenzie Building, VG Site Queen Elizabeth II Health Sciences Centre 5788 University Ave, Halifax, Nova Scotia, Canada. B3H 2Y9 David.Haldane@cdha.nshealth.ca Tel: ; FAX:
2 30 Abstract A 65 year old male with known hypertension and hypercholesterolemia sought medical attention because of a three month history of skin swelling on his upper back. Histopathology and molecular techniques were employed and identified an organism in the Onchocerca genus. This represents a very uncommon example of cutaneous infection by a zoonotic Onchocerca species. Key Words: filariasis, zoonotic filariasis, cutaneous infection, nematode, Onchocerca Introduction Filariasis is a parasitic infection caused by nematodes (roundworms) belonging to the family Filarioidea. When filariae that normally infect animals infect humans, the condition is termed zoonotic filariasis. These are often transmitted by bloodsucking arthropod vectors such as black flies and mosquitoes. Zoonotic filariasis has been reported worldwide with variable clinical presentations ranging from an asymptomatic state to a serious illness with widespread dissemination of the organism. Zoonotic filariasis of the skin is most commonly caused by filariae of the Dirofilaria, Onchocerca, or Brugia genera. We describe an inflammatory skin lesion caused by a zoonotic Onchocerca species in an adult male acquired in Nova Scotia, Canada. Case Report A 65 year old Caucasian man from rural Nova Scotia sought medical attention because of sudden onset of localized swelling of the skin in the inferior left scapular area. He had noted a small, mildly tender pruritic papule one morning measuring less than 1 cm which he regarded as a possible insect bite. Over the course of one day, the lesion enlarged to form a nodule measuring approximately 4 cm in diameter. Medical attention was sought. The patient was given a ten day course of antibiotics
3 51 52 which caused the swelling to decrease in size, but the nodule did not resolve completely. Elective surgical excision was undertaken Within the last 5 years, the patient had traveled to Florida in April, 2009 and had been working in Ontario until May 31, While in Ontario, he had been in charge of maintaining a high-rise apartment block in Windsor for 12 years. Prior to this, he had worked in the automotive industry. There was no history of foreign travel. During the past three years, the patient had resided in rural Nova Scotia where he had a pet dog with a free range in an open hayfield where contact with wild animals was minimal. During this period, the dog showed no symptoms of infection and remains healthy to this day. The patient s medications included hydrochlorothiazide 12.5 mg OD and simvastatin 20 mg OD for hypertension and hypercholesterolemia respectively. He was otherwise healthy. There was no history of immunosuppression. On examination, an erythematous nodule was evident on the left upper back just inferior to the scapula. This area had been covered by clothing and the patient could not recall any history of an arthropod bite. No other skin lesions were detected. Preliminary blood work was not performed. Following excision, the specimen was submitted to the laboratory for processing. Clinically interpreted as a cyst, the submitted sample consisted of an ellipse of skin and subcutaneous adipose tissue measuring 1.4 x 0.3 x 1.3 cm. It was serially sectioned and submitted in total. Histopathologic examination revealed a dense, nodular, superficial and deep, perivascular lymphocytic infiltrate with abundant eosinophils in the dermis and superficial panniculus. Small foci of interstitial granulomatous inflammation were noted (Fig. 1a, b). Close to the edge of the biopsy, in association with the inflammatory infiltrate, cross sections of a nematode were noted (Fig. 1c, d) A microbiological consultation confirmed the presence of a nematode measuring 60 x 68 micrometers. There were no lateral alae, and the cuticle was smooth with a 3 micrometer diameter
4 thickness. The lateral cords had 2 cells with prominent nuclei, but the dorsal and ventral lines were not prominent. A muscular layer was present internal to the cuticle. An esophagus and possibly a reproductive system were present, although a double uterus was not observed. No ova or larvae were seen within the organism. Based on the microbiologist s evaluation, certain organisms were excluded, including: Strongyloides stercoralis, hookworm, Toxocara canis or T. cati, Gnathostoma spp., and Baylisascaris procyonis. Candidate organisms included Brugia spp., Mansonella spp., and Acanthocheilonema delicata. A trichrome stain was not performed and unstained slides were not available for examination. Because the nematode could not be further identified by conventional microscopic examination, the specimen was referred in consultation to the Mayo Clinic in Rochester, MN. There, a molecular approach to identification of the organisms was undertaken. The polymerase chain reaction (PCR) using primers for the mitochondrial NADH dehydrogenase subunit 5 gene of Onchocerca species was employed (1). Sequence analysis of the amplified product (174 bp) in conjunction with a query in the public NCBI (National Center for Biotechnology Information) Nucleotide database enabled identification of the nematode as an Onchocerca species, with closest (96%) homology to O. volvulus, O. dukei, and O. linealis. The localized clinical lesion was considered to be a result of accidental inoculation by a zoonotic species, without further implications for the patient s health. Excision was regarded as curative and the patient remains well ten months after excision of the lesion. Discussion Zoonotic filaria are occasionally identified in biopsy specimens or removed intact from superficial sites such as the orbit or conjunctiva (2). The site of human infection is often analogous to the site of infection in the native mammalian host (2). In humans, zoonotic nematodes have typically
5 been found in the subcutaneous tissue, heart, lungs, eyes, lymphatic system, brain, and spinal cord (2). Zoonotic filariae that have been isolated in humans include Dirofilaria, Brugia, Onchocerca, Dipetalonema, Loaina, and Meningonema (2). While many filariae species can cause infections in birds, reptiles, and amphibians, only filariae with natural mammalian hosts cause zoonotic filariasis in man (2) Human infection occurs by way of an arthropod vector, which had previously ingested a blood meal from an animal with an active filarial infection. During their development, filarial larvae elicit a minimal host response with the exception of colonization of sensitive areas such as conjunctiva (2). However, due to the incompatibility of the host, the larvae inevitably die and generate an intense hostinflammatory response to the organism (2). Why humans mount a host response only when the larvae die is unclear. It is known that larvae live for an extended period of time within their natural hosts without generating a host response (2). Rarely, filariaemia is seen in zoonotic filariasis (2). Removal of the parasite is therapeutic. Onchocerca are natural parasites of animals, often cows and horses (2). Many species of Onchocerca can be found within connective tissues of wild and domestic animals worldwide (3). In tropical areas where Onchocerca volvulus is endemic, human infection is quite common. Human onchocerciasis, also known as river blindness, manifests as intense pruritis, skin depigmentation and ocular scarring due to migration of the microfilariae (3). The adult filariae are stationary in the human host and are found within a subcutaneous nodule. In our case, it is unclear what the vector might have been. Certainly, the pet dog could be suspected although this is unlikely given that the dog showed no symptoms of infection and remains healthy to this day. Previous reports suggest that Simulium spp. (blackflies) are often implicated as vectors in zoonotic Onchocerciasis (4, 5) To date, 16 cases of zoonotic filaria by animal Onchocerca spp. have been reported outside endemic areas (Table 1). All cases, but one, were infected by a single female worm. The remaining
6 patient with systemic lupus erythematosus on immunosuppressive therapy had multiple lesions and multiple worms on the face and neck (1). The adult form of Onchocerca has a marked predilection for connective tissues and often assumes a coiled nodular appearance; a characteristic seen also in their natural hosts (2). Histomorphologic assessment of the parasite may allow accurate identification to the genus level. Features of relevance include cuticle thickness, musculature development, hypodermis development, lateral chords, and a vestigial digestive system. Speciation of zoonotic Onchocerca spp., however, is often difficult and requires molecular ancillary techniques, namely DNA sequencing. In our case, histomorphology was inconclusive and PCR and sequence analysis was required for identification. By utilizing primers for the mitochondrial NADH dehydrogenase subunit 5 gene, we were able to determine that this organism was of the Onchocerca genus. However, an attempt at speciation utilizing primers for the 18S gene provided by the Centers for Disease Control and Prevention was unsuccessful. We surmise that this may have been due to the fragmented nature of DNA in formalin-fixed paraffinembedded tissue. Conclusion Although rare, pathologists and dermatopathologists should be aware of zoonotic filariasis. Usually, a thorough clinical history with a focus on recent exposure to animals and/or arthropod bites is helpful in establishing the correct diagnosis. Immunosuppression may lead to more severe infections, although this needs to be further investigated. Consultation with a microbiologist is particularly valuable in this type of setting. Specific identification to the genus and species level may require ancillary molecular techniques.
7 Reference Age/Gender Anatomical Site Geographic Location Species Azarova et al. (1965) (6) 15/Female Tendon of oculomotor muscle Russia O. spp. Siegenthaler et al. (1965) (7) 25/Male Knee Switzerland O. spp. Beaver et al. (1974) (8) 48/Female Wrist Illinois, U.S.A. O. spp. Most likely O. cervicalis Ali-Khan. (1977) (9) 43/Female Wrist Ontario, Canada O. spp. Beaver et al. (1989) (10) 2/Female Left foot (Plantar aspect) Oita, Japan O. spp. Takaoka et al. (1996) (11) 57/Female Wrist Oita, Japan O. spp. most likely O. gutturosa Burr et al. (1998) (12) 52/Female Right cornea Colorado, U.S.A. O. spp. most likely O. cervicalis Pampiglione et al. (2001) (13) 16/Male Subconjunctival area Albania O. spp. Wright et al. (2002) (14) 50/Female Left subdeltoid mass Minnesota, U.S.A. O. gutturosa Takaoka et al. (2005) (15) 69/Female Right infraclavicular region Oita, Japan O. dewittei japonica Sallo et al. (2005) (16) 65/Male Anterior vitreous cavity Hungary O. spp. Koehsler et al. (2007) (1) 59/Female Multiple nodules on face and neck U.S.A. O. jakutensis Hira et al. (2008) (17) 12/Female Suprapubic skin nodule Kuwait O. spp. Uni et al. (2010) (18) 70/Male Subcutaneous nodule left knee Hiroshima, Japan O. dewittei japonica Otranto et al. (2011) (5) 18/Female Left subconjunctival area Edirne, Turkey O. lupi Eberhard et al. (2012) (19) 56/Male Left anterior chamber Oregon, U.S.A. O. spp. Table 1. Previously reported zoonotic filariasis by Onchocerca spp. outside endemic areas.
8 References 1. Koehsler M, Soleiman A, Aspock H, Auer H, Walochnik J. Onchocerca jakutensis filariasis in humans. Emerg Infect Dis2007 Nov;13(11): Orihel TC, Eberhard ML. Zoonotic filariasis. Clin Microbiol Rev1998 Apr;11(2): Gutierrez Y. Diagnostic features of zoonotic filariae in tissue sections. Hum Pathol1984 Jun;15(6): Takaoka H, Fukuda M, Otsuka Y, Aoki C, Uni S, Bain O. Blackfly vectors of zoonotic onchocerciasis in Japan. Med Vet Entomol2012 Dec;26(4): Otranto D, Sakru N, Testini G, Gurlu VP, Yakar K, Lia RP, Dantas-Torres F, Bain O. Case report: First evidence of human zoonotic infection by Onchocerca lupi (Spirurida, Onchocercidae). Am J Trop Med Hyg2011 Jan;84(1): Azarova NS, Miretskii O, Sonin MD. [1st case of human infection by the nematode Onchocerca Diesing, 1841 in the USSR]. Med Parazitol (Mosk)1965 Mar-Apr;34(2): Siegenthaler R, Gubler R. [Para-articular nematode granuloma (Indigenous Onchocerca)]. Schweiz Med Wochenschr1965 Aug 14;95(33): Beaver PC, Horner GS, Bilos JZ. Zoonotic onchocercosis in a resident of Illinois and observations on the identification of Onchocerca species. Am J Trop Med Hyg1974 Jul;23(4): Ali-Khan Z. Tissue pathology and comparative microanatomy of Onchocerca from a resident of Ontario and other enzootic Onchocerca species from Canada and the U.S.A. Ann Trop Med Parasitol1977 Dec;71(4): Beaver PC, Yoshimura H, Takayasu S, Hashimoto H, Little MD. Zoonotic Onchocerca in a Japanese child. Am J Trop Med Hyg1989 Mar;40(3): Takaoka H, Bain O, Tajimi S, Kashima K, Nakayama I, Korenaga M, Aoki C, Otsuka Y. Second case of zoonotic Onchocerca infection in a resident of Oita in Japan. Parasite1996 Jun;3(2): Burr WE, Jr., Brown MF, Eberhard ML. Zoonotic Onchocerca (Nematoda:Filarioidea) in the cornea of a Colorado resident. Ophthalmology1998 Aug;105(8): Pampiglione S, Vakalis N, Lyssimachou A, Kouppari G, Orihel TC. Subconjunctival zoonotic Onchocerca in an Albanian man. Ann Trop Med Parasitol2001 Dec;95(8): Wright RW, Neafie RC, McLean M, Markman AW. Zoonotic onchocerciasis of the shoulder. A case report. J Bone Joint Surg Am2002 Apr;84-A(4): Takaoka H, Yanagi T, Daa T, Anzai S, Aoki C, Fukuda M, Uni S, Bain O. An Onchocerca species of wild boar found in the subcutaneous nodule of a resident of Oita, Japan. Parasitol Int2005 Mar;54(1): Sallo F, Eberhard ML, Fok E, Baska F, Hatvani I. Zoonotic intravitreal Onchocerca in Hungary. Ophthalmology2005 Mar;112(3): Hira PR, Al-Buloushi A, Khalid N, Iqbal J, Bain O, Eberhard ML. Zoonotic filariasis in the Arabian Peninsula: autochthonous onchocerciasis and dirofilariasis. Am J Trop Med Hyg2008 Nov;79(5): Uni S, Boda T, Daisaku K, Ikura Y, Maruyama H, Hasegawa H, Fukuda M, Takaoka H, Bain O. Zoonotic filariasis caused by Onchocerca dewittei japonica in a resident of Hiroshima Prefecture, Honshu, Japan. Parasitol Int2010 Sep;59(3): Eberhard ML, Sims AC, Bishop HS, Mathison BA, Hoffman RS. Ocular zoonotic onchocerca infection in a resident of Oregon. Am J Trop Med Hyg2012 Dec;87(6):
9 Figure Legend Figure 1. a) Elliptical excision of skin and panniculus, at scanning magnification, shows a superficial and deep perivascular inflammatory infiltrate extending to the panniculus. There are no epidermal changes. (H&E, 5x) b) Higher power view of the infiltrate reveals a predominantly lymphohistiocytic population with numerous eosinophils, along with a focal interstitial histiocytic component. (H&E, 72x) c) Adjacent to the interstitial histiocytic inflammatory infiltrate, a cross section of Onchocerca adult nematode is seen. (H&E, 98x) d) Higher power view of the Onchocerca adult nematode in cross section. (H&E, 200x) Abbreviation: H&E Hematoxylin and Eosin Downloaded from on August 16, 2018 by guest
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