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Morphologically and Genetically Diagnosed Dermal Dioctophyme Larva in a Chinese Man: Case Report

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Morphologically and Genetically Diagnosed Dermal Dioctophyme Larva in a Chinese Man: Case Report SN Comprehensive Clinical Medicine https://doi.org/10.1007/s42399-020-00256-6 MEDICINE Morphologically and Genetically Diagnosed Dermal Dioctophyme Larva in a Chinese Man: Case Report Takuji Tanaka1 & Toshihiro Tokiwa2 & Hideo Hasegawa3 & Teruki Kadosaka4 & Makoto Itoh4 & Fumiaki Nagaoka4 & Haruhiko Maruyama5 & Yuki Mizuno6 & Hiroyuki Kanoh6 & Naoki Shirai7 Accepted: 11 March 2020 # Springer Nature Switzerland AG 2020 Abstract We present a case of a nematode larva infection found in a cutaneous nodule excised from the left flank of a 48-year-old Chinese male, who was naturalized in Japan and comes and goes frequently to China and Japan. Clinical diagnosis at his first visit to a local hospital was epidermoid cyst. Pathological diagnosis of surgical specimen was cutaneous larva migrans and detailed morphological observation suggested that the worm in the subcutis was a dioctophimatid larva. DNA sequence analysis of the formalin-fixed and paraffin-embedded tissues revealed the larva as the giant kidney worm, Dioctophyme renale (Goeze, 1972). Keywords Dioctophyme renale . Dioctophymiasis . Human . Skin . Histopathology . Genetic diagnosis Introduction remaining 5 were larval infections found in the thigh, abdom- inal wall, and chest wall [3]. Dioctophyme renale (Nematoda: Dioctophymatidae) in We report here a case of skin infection with D. renale larva humans is a large, red-colored nematode parasitic in the kid- developed in a 48-year-old Chinese male. The lesion was neys of various mammals including humans [1]. Because its incidentally found, morphologically diagnosed, and finally female adult attains to 1 m in length, it is usually called as confirmed by DNA sequencing. “giant kidney worm” [2]. Human infection with D. renale is a rare disease with a small number of cases reported in literature [3]. Recent review article by Yang et al. [3]summarizes37 Case Presentation human cases of D. renale infection hitherto known in the world (China, Australia, Greece, India, Indonesia, Iran, A 48-year-old Chinese male, who was naturalized in Japan Japan, Thailand, the USA, and Yugoslavia). Among these and comes and goes frequently to China and Japan, visited cases, the kidneys were involved in 32 cases, while the to the Department of Surgery, the Hayatoku Hospital, Gifu, This article is part of the Topical Collection on Medicine * Takuji Tanaka 4 Parasitology Division, Department of Microbiology and [email protected] Immunology, Aichi Medical University School of Medicine, Nagakute, Aichi 480-1195, Japan 1 Department of Diagnostic Pathology (DDP) & Research Center of 5 Diagnostic Pathology (RC-DiP), Gifu Municipal Hospital, Division of Parasitology, Department of Infectious Diseases, Faculty 7-1 Kashima-cho, Gifu City, Gifu 500-8513, Japan of Medicine, University of Miyazaki, 5200 Kiyotake-cho, Kihara, Miyazaki 889-1692, Japan 2 Laboratory of Veterinary Parasitology, School of Veterinary Medicine, Faculty of Veterinary Science, Nippon Veterinary and Life 6 Science University, 1-7-1 Kyonancho, Musashino, Tokyo 180-8602, Department of Dermatology, Gifu Municipal Hospital, Japan 7-1 Kashima-cho, Gifu City, Gifu 500-8513, Japan 3 Department of Biomedicine and Department of Infectious Disease 7 Control, Faculty of Medicine, Oita University, 1-1 Idaigaoka, Department of Surgery, Hayatoku Hospital, 1-8-1 Usaminami, Gifu Hasama, Yufu 879-5593, Japan City, Gifu 500-8367, Japan SN Compr. Clin. Med. Japan, on 23 January 2018, with complaints of a small skin There were sections through the esophagus and intestine of nodule in the left flank. His past medical history was unre- a nematode as shown in Fig. 1a–d. The diameter of the cross markable. On macroscopic examination of the skin, he had a sections was 180–235 μm. The cuticle was about 5 μmin small skin nodule without itching and abnormal color, 20 mm thickness, and ornamented with fine transverse striations, in diameter, on his left flank (lateral region of the abdomen). which were clearly seen in the obliquely cut sections (Fig. There were no abnormalities on the surface. Also, there was 1b). The pseudocoelomic cavity was filled with substance that no localized tenderness in the nodular area. He did not receive was stained dark (Fig. 1c–e). The somatic musculature was of any clinical and laboratory tests. The lesion was surgically the polymyarian coelomyarian type; somatic muscle cells removed based on the clinical diagnosis of epidermoid cyst. were numerous but exact number could not be counted. The postoperative course was uneventful. Pathological exam- There were eight cords, namely, dorsal, ventral, 2 lateral, 2 ination of the skin nodule removed revealed a worm subdorsal, and 2 subventral ones (Fig. 1c–e). The ventral cord surrounded by thick fibrous capsule in the middle dermis was the most prominent, fan-shaped, containing minute nuclei about 2 mm beneath the epidermis on hematoxylin and eosin arranged in V or U form in cross section. Other cords were (H & E)-stained sections (Fig. 1). There was mild or moderate minute. The alimentary canal was connected with the body infiltration of lymphocytes, eosinophils, plasma cells, and his- wall by two pseudocoelomic membranes, which were hardly tiocytes, in and around the capsule. The epidermis overlaying discernible due to the dark-stained pseudocoelomic substance the lesion did not show any abnormalities. Pathological diag- (Fig. 1c and d). Minute hypodermal nuclei were scattered in nosis was intradermal parasite. Detailed morphological exam- the subcuticular layer (Fig. 1c and d). The esophagus was ination of the worm sections was performed. thick, stained with eosin, containing granular particles, Fig. 1 a Low-magnification view of the pathological section showing a posterior portion of intestine. c–e Dorsal (thin dart), ventral (thick dart), capsule formed around sectioned worms in the middle dermis. b lateral (thick arrows), and subdorsal and subventral (thin arrows) cords. Obliquely cut worm section showing transverse striations of cuticle Bars are magnifications. H & E stain; es, esophagus; hn, hypodermal (arrows). Dart indicating dorsal cord. c Cross section of the esophagus. nuclei; i, intestine; pg, primordial genital organ; and pm, pseudocoelomic d Cross section of anterior portion of the intestine. e Cross section of membrane SN Compr. Clin. Med. scattered nuclei, and a triradiate lumen (Fig. 1c). The intestinal One-year follow-up of the patient revealed a cutaneous wall was composed of one layer of columnar cells each with a nodule again in the left abdomen. However, this was histo- round nucleus in the center and brush border (Fig. 1d and e). pathologically diagnosed as lipoma that did not contain Primordial genital organ was seen in the cross section through worms. the posterior body (Fig. 1e). The morphology of the sectioned worm was identical with those reported previously on larval dioctophymatid infections [4, 5]. Because D. renale infection was strongly suspected on the Discussion morphological findings of the dermal parasite, his serum was examined by multiple-dot enzyme-linked immunosorbent as- We report here a rare case of dermal Dioctophyme larva in a say (dot-ELISA) for various parasitic diseases. However, his Chinese man, which was initially suspected dermal parasite in serum was negative for all 15 parasite antigens examined, the tissue removed for pathological diagnosis. At first, mor- including Trichinella spiralis and Trichuris vulpis. phological diagnosis was made as an infection with a larva To confirm this molecular diagnosis further, DNA extraction belonging to the family Dioctophymatidae. This family in- from the formalin-fixed and paraffin-embedded (FFPE) skin cludes only three genera, namely, Dioctophyme parasitic in tissue containing the worm and sequencing of small subunit the kidney of carnivores, and Eustrongylides and Hystrichis, ribosomal DNA gene, which allowed us to identify the larva both parasitic in the alimentary canals of piscivorous birds. as the giant kidney worm, D. renale (Goeze, 1972), were per- Morphology of L3 larva in cross section resembles each other formed [4]. Semi-nested polymerase chain reaction (PCR) was among the dioctophymatids although Eustrongylides and newly developed based on the initial amplification of about Hystrichis are generally much larger than Dioctophyme [1]. 255 bp with DRSSU1185F/DRSSU1418R primers [4], follow- Hence, strict species identification of the causative agent was ed by a subsequent amplification with DRSSU1185G/ withheld in the previous case reports, only referring to as DR1413R (5′-TCGTTACTCCGTCTCAACAGA-3′)primers. “Dioctophyme-like,”“dioctophymatid,” or Dioctophyme sp. The latter primer was designed based on 18S sequence of [5, 7, 8]. However, in 2014, Tokiwa et al. [4] first applied D. renale (accession no. AB595139) detected from brown rat DNA sequencing for a dioctophymatid larva found in the (Rattus norvegicus)[6]. The PCR solution was prepared fol- tissue sections of a nodule in the dermis and genetically con- lowing a standard procedure using Takara Ex Taq (TaKaRa, firmed it as D. renale. The present case is thus the second case Japan). For the subsequent amplifications, 1 μl of the first in which D. renale infection was genetically proved. PCR product was used as the template. The both reactions The key to understand D. renale infection is its complex consistedofaninitialdenaturationat94°Cfor2min,35cycles life cycle [9]. Definitive hosts are various mammals, usually of 94 °C for 30 s, annealing at 52 °C for 30 s, and extension
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