Creeping eruption caused by a larva of the suborder Spirurina type X

ARTICLE

Creeping disease, or cutaneous larva migrans, is characterized by a linear eruption on the skin. It is caused by the parasitism of organisms such as larvae of Gastrophilus equi linnaeus or Hypoderma bovis, Gnathostoma spp., Spirometra erinacei, or larvae of the suborder Spirurina [1]. Because a considerable number of people are fond of eating raw or nearly-raw fish and shellfish in Japan, opportunities for developing creeping eruption caused by parasites present in raw fish and shellfish are relatively high. Creeping eruption caused by Gnathostoma spp. is most frequently observed in Japan [2]. Recently, the incidence of the creeping eruption caused by Spirurina ingested by eating contaminated raw small squids (Watasenia scintillans) has been increasing [3]. We present a case of creeping eruption caused by larvae of the suborder Spirurina type X ingested in this manner. Histologically, the transverse section of a larval worm was identified in the upper to middle layer of the dermis, and patient’s serum reacted with larvae of the suborder Spirurina type X by ELISA.

Case report

A 46 year-old Japanese male, residing in Tokyo, presented with a serpiginous eruption accompanied by itching and pain in the abdomen. He was the manager of a tennis club and he had no history of going abroad. Eight days before his first visit to the hospital, a small erythematous patch appeared on the upper right side of the abdomen, then it gradually extended to upper left side forming a linear pattern. No whole-body symptom such as fever, vomiting or abdominal pain was observed. He ate raw small squids (Watasenia scintillans) at a pub five days before the appearance of the symptoms. On examination, he had a serpiginous erythematous eruption with some vesicles, which started from the right side of the abdomen and spread slightly upward to the upper left side of the abdomen, then lower part of the abdomen (Fig. 1 a, b). At the end of the lesion, edematous erythema was observed. We diagnosed him as having creeping eruption, based on the fact that he ate raw Watasenia scintillans and on the appearance of a serpiginous eruption. Since the linear edematous erythema was observed to extend further to the upper left side of the abdomen on the day of first visit, we considered this to be the direction of movement of the larval worm. We removed the affected spindle-shaped area of skin, which was 3.5 cm at its largest diameter and 2.5 cm at its smallest diameter, including the topmost part of the eruption. In the unfixed skin tissues, we attempted to visually detect the larval worm by cutting three lines along the long axis from the dermal side, but we were unsucessful. Histological findings revealed the transverse section of the larval worm in the upper to middle layer of the dermis only in the second section from the margin of the exanthema on ten serial sections of HE-stained specimens (Fig. 2 a). No significant changes were observed in the epidermis. A fissure formed around the larval worm, and moderate infiltration of cells composed mainly of neutrophils was observed around the fissure (Fig. 2 b). There were no lateral alae or spines on the cuticle of the larva, and the fibrous subcuticular layer was present below the cuticle; lateral chords protruded from both sides of the body cavity and were in contact with the intestine. There was a muscle layer of the polymyarian coelomyrian type below the cuticle of the larva, but we could not count the number of muscle cells due to the degeneration of the tissue. The blood tests revealed no abnormal results except for slight increases in the serum GPT and LDH levels. The eosinophil count was within the normal range, and the plasma IgE level was normal. Serum antibody titers against various parasites were measured by ELISA. The
patient serum was positive only for the antibody against larvae of the suborder Spirurina type X, and was negative for all other anti-parasite antibodies. Based on the above findings, we diagnosed him as having the creeping eruption caused by larvae of the suborder Spirurina type X. There was no recurrence five months after a skin biopsy.

Discussion

We described above a case of creeping eruption caused by larvae of the suborder Spirurina type X. The larvae of the suborder Spirurina type X were identified to be nematode which belongs to the suborder Spirurina [4]. However, since their adult larval worm has not yet been identified, their species has not yet been determined; thus they have no scientific name. Hasegawa classified the larvae of the suborder Spirurina into types I to XIII^c. Among them, the one observed in humans is only type X. A type X larva has a body length of 5.43-9.80 mm and width of 74-110 mum, with two lateral pseudolabia at the head and two large tubercles at the tail [4]. It is considered that their intermediate hosts are small squid (Watasenia scintillans) [hotaruika], dried squid (Ommastrephes sloanipacificus) [surumeika], sandfish (Arctoscopus japonicus) [hatahata], and cod (Theragra chalcogramma) [sketoudara], and their final hosts are sea mammals and birds, but their life history has not yet been clarified in detail. Ando et al. reported that larvae of the suborder Spirurina type X were found in the internal organs of 44 out of 77 Theragra chalcogramma examined, and of 4 out of 162 Watasenia scintillans [3]. Recently, the incidence of infections through eating raw Watasenia scintillans has been increasing, and infections are often observed from March to July when Watasenia scintillans are caught.

To diagnose creeping eruption, it is necessary to prove the presence of parasitism. There are three methods obtaining proof: (1) extraction of the larval worm from the tissue, (2) preparation of tissue specimens and identification of the type of worm based on the structure of the cross section of the larval worm, (3) measurement of the titer of serum antibodies against various parasites. As methods of extracting the larval worm, extraction of the parasite from live tissue specimens can be performed, or the larval worm can be extracted by degrading it using digesting solution [5]. The rate of detection of the cross section of the larval worm on a tissue specimen is not high even when serial sections of specimens are prepared. Recently, the measurement of the titers to anti-parasite antibody has been widely used. The intracutaneous method, Ouchterloy method and ELISA are frequently performed. Depending on the type of method, sensitivity and specificity differ, and cross-reactions are also observed [6]. Detection of anti-parasite antibody is effective as an auxiliary method, together with the detection of the larval worm.

The creeping eruption caused by larvae of the suborder Spirurina type X and by Gnathostoma spp. can be clinically differentiated to some extent. While the exanthema caused by type X larvae is often a serpiginous narrow erythema accompanied by vesicles, that caused by Gnathostoma spp. often has migrating erythema only [7, 8]. This difference is considered to be caused by a difference in the depth of the skin layer at which the larval worm moves in a serpiginous manner. Histologically, type X larvae are often detected in a shallow layer of the dermis and Gnathostoma spp. are detected in the middle to deep layer of the dermis. The transverse section of the larval worm can be identified by its characteristics such as small size, presence of cuticle, types of subcuticlar polymyarian muscle layers, and number of muscle cells. Anatomical characteristics of type X larvae observed in their cross section are the absence of spines or lateral alae in the cuticle, a large number of muscle cells in one quadrant, and a small number of digestive-tract cells in comparison to Gnathostoma spp [1, 9].

Type X larvae can also cause abdominal manifestation due to visceral larva migrans [10-13]. Characteristic clinical features were abdominal pain, nausea, vomiting, diarrhea and ileus with ascites. These symptoms occur several hours to 2 days after the patients ate Watasenia scintillans. Most cases recovered in several days by only drip infusion. However, some reported cases were diagnosed ileus or peritonitis and operated with partial ileectomy [11, 13]

For treatment, extraction of the larval worm by removing the affected skin is the most effective method. However, determination of the amount of skin to remove is a difficult problem, because the speed of movement differs from worm to worm. Marking the skin and a day’s observation of the moving worm is recommended. However, when biopsy should be performed immediately, considering the possibility that the worm may not move at all or that it may move in the opposite direction, removal of the skin of 3-4 cm in length from a position slightly away from the margin of the exanthema is recommended. Recurrence can occur after the excision [6]. Usually the eruption resolves within two months. It is speculated that type X larvae survive for only a short time in humans and dies out because they may be inappropriate hosts for their growth [7, 14]. Another choice of treatment is anthelminthic drugs such as thiabendazole or ivermectin. But the effect of anthelminthics in creeping eruption remains unclear [7].

We would like to express our gratitude to Professor K. Sugane, Department of Parasitolofy, Shinshuu University, for his assistance in conducting ELISA of the serum samples.

REFERENCES

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8
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11
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12
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14
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