Patent Macracanthorhynchus ingens Infection in a 17-Month-Old Child, Ohio

Abstract

Limited data exist on human Macracanthorhynchus infections. We report an asymptomatic 17-month-old who passed eggs and an adult Macracanthorhynchus ingens worm, indicating parasite maturation and reproduction. Macracanthorhynchus ingens may have a greater capacity to mature in humans versus Macracanthorhynchus hirudinaceus.

Acanthocephala are a unique and uncommonly encountered subdivision of parasitic helminths in human medicine, distinct from the other helminths that may be more familiar to healthcare providers (nematodes, cestodes, trematodes). The most commonly implicated species infecting humans (Macracanthorhynchus spp and Moniliformis moniliformis), among others, follow a multistage life cycle in which the vertebrate definitive host, harboring adult Acanthocephalans in its intestinal tract, sheds eggs containing larval acanthors in feces. Arthropod intermediate hosts ingest these eggs, and the acanthor ultimately develops into an acanthella and then a cystacanth. The definitive host is infected upon consumption of the arthropod containing an infectious cystacanth, which develop into adult male and female Acanthocephalans. Infections are often asymptomatic, although abdominal pain and other complications including intestinal perforation can arise from the insertion of the helminth’s spiny proboscis into the intestinal wall [1]. Diagnosis may also be challenging, because eggs may not be produced in the aberrant human host or may be mistaken for other helminths or artifacts [2]. Among the Acanthocephalans that infect humans, M moniliformis, a rodent parasite, and Macracanthorhynchus hirudinaceus, a swine parasite, are the most frequently reported [1]. However, Macracanthorhynchus ingens of raccoons (occasionally other carnivores) is morphologically similar to M hirudinaceus and has been reported in 3 prior human cases [3–5]. In this study, we describe a fourth case of M ingens infection, in a child.

CASE REPORT

A 17-month-old girl from Ohio presented to her local primary care physician (PCP) after her mother noticed worm-like objects in her stool and attempted to treat the child at home with an unknown dose of over-the-counter enterobiasis medication (pyrantel pamoate). The PCP submitted a stool specimen to a reference laboratory for ova and parasite examination; eggs were detected and were reported as M hirudinaceus. A second stool specimen collected 1 week later during a consultation with a pediatric infectious disease physician at a referral children’s hospital again showed such eggs. The patient was not experiencing any obvious gastrointestinal symptoms; she had no diarrhea, vomiting, abdominal pain, hematochezia, or changes in bowel habits. She was experiencing normal growth and development for a child of her age. The patient lived in rural northeastern Ohio and no travel outside of this region was reported. Animal exposure was limited to indoor cats. The patient’s residence was near pig and dairy farms.

Brown, textured, embryonated eggs measuring an average of 91.1 × 50.1 µm (range 87.4–95.1 × 44.5–54.0 µm, of 10 eggs measured) were identified in a stool specimen provided to the Centers for Disease Control and Prevention (CDC) (Figure 1A and B). A subsequent stool specimen containing the worm was preserved in TOTAL- FIX and also sent to the CDC for identification. Acanthors liberated from eggs in the submitted stool specimen under coverslip pressure measured 75 µm (Figure 1C). Morphological analysis of the adult worm allowed specific identification of M ingens based on comparisons to published descriptions [3, 6, 7]; measurements were obtained as described by Richardson [7]. The adult female worm was 12.5 cm in total length, off-white, and pseudoannulated (wrinkled) (Figure 1D). The invaginated proboscis was dissected out with a scalpel for further examination. The proboscis was mostly spherical, measuring 583-µm wide, and was ringed in hooks of varying lengths and shapes corresponding to Type I, II, and III hooks described by Moore [6]. The total number of hooks was not determined due to the slightly damaged state of the proboscis. Intact hooks measured 71–167 µm, with the largest located towards the anterior. Ultimately, hook and proboscis width measurements allowed the distinction of M ingens versus other similar Acanthocephala such as M hirudinaceus (larger hooks, proboscis) and Oligacanthorhynchus microcephalus (= tortuosa) (smaller hooks, proboscis) [7].

Figure 1.

(A–C) Macracanthorhynchus ingens eggs from patient’s stool specimen; showing 1 egg in 2 focal planes to illustrate the surface texture (A and B) and liberated acanthor (C) (bar = 50 µm). (D) The adult female worm with an invaginated proboscis (bar = 1 cm).

For further confirmation, deoxyribonucleic acid was extracted from a piece of the adult worm and subject to polymerase chain reaction (PCR) and sequencing. Species-specific primers targeting the cytochrome c oxidase subunit I (COX-I) mitochondrial gene (MI-COXI-F, AGC TAG GGA GTG TTG GGG C and MI-COXI-R, CTG ATA TAT GAG GGC CCT TCC) were designed to amplify a fragment of ~580 base pairs. The amplicon sequence showed high homology (99%) with M ingens mitochondrial COX-I gene (GenBank accession no. AF416997).

After confirmatory diagnosis of M ingens infection, the patient received additional treatment with 2 doses of pyrantel pamoate 11 mg/kg base 2 weeks apart. Stool specimens collected approximately 4 weeks after completing the treatment course were negative for eggs on ova and parasite evaluation.

Patient Consent Statement

The patient’s written consent was obtained, and the design of the work has been approved by local ethical committees.

DISCUSSION

The recovery of the intact worm and the preservation of the specimen in a PCR-compatible fixative (ie, ethanol-based) allowed definitive morphological and molecular confirmation as M ingens. Although formalin is sufficient for preservation of eggs and worm morphology, it may greatly hinder molecular identification. This patient was asymptomatic, consistent with other reported cases of M ingens infections (Table 1). However, other cases of acanthocephaliasis have involved acute abdominal pain and intestinal perforation due to the penetration of the proboscis into the gastrointestinal wall [8, 9]. Many cases of M hirudinaceus infections involve abdominal perforation requiring emergency surgery, during which an immature worm is typically identified [1, 9]. In experimentally infected animals, M hirudinaceus was noted to cause a greater degree of pathology than M ingens [10]. Therefore, it seems M ingens could be less likely than M hirudinaceus to cause intestinal perforation, giving it more of an opportunity to mature and produce eggs.

Table 1.

Summary of Reported Cases of Macracanthorhynchus Ingens in Humans

Case	Age/Sex	Location	Clinical Features	Worms Recovered	Eggs in Stool?	Possible Exposure History	Treatment/ Management
Dingley and Beaver [3]	10 months/female	Texas	Asymptomatic	Three 5- to 7-cm adult male worms; six 9- to 20-cm adult female worms	Yes	Known to eat insects; many racoons around home	Niclosamide followed by mebendazole
Brien et al [4]	15 months/male	Texas	Asymptomatic	13-cm adult female worm; “several smaller worms”	Yes	Rural area with many racoons	Mebendazole (100 mg bid, 3 days)
Mathison et al [5]	18 months/female	Florida	Asymptomatic	14-cm adult female worm	No	Millipedes in home	Pyrantel pamoate (11 mg/kg base, 3 doses)
Present case	17 months/female	Ohio	Asymptomatic	12.5-cm adult female worm	Yes	Reported arthropods in mouth	Pyrantel pamoate (11 mg/kg base 2 weeks apart)

Although it is generally assumed that Macracanthorhynchus spp do not or seldom reach sexual maturity in the aberrant human host, 3 of 4 confirmed M ingens cases, including this one, have involved detection of eggs in stool [3–5]. Although only 1 worm was recovered successfully, other worms (including an adult male) may have been passed previously and missed. Ultimately, as Mathison et al [5] suggest, following up the passage of these eggs in stool via repeat testing or recovery of adult worms is important for ruling out spurious passage (ie, consuming eggs from environmental sources that are then subsequently passed in stool) and confirming authentic infection.

The first documented case of M ingens infection in humans was reported in 1985 [3]. Nine Acanthocephala were found in the stools of a 10-month-old child in Texas over the course of 2 months. Raccoon infections with M ingens were noted to be prevalent in the area at that time. The second case was reported in 2012: a 15-month-old child with M ingens infection was successfully treated using 3 days of mebendazole [4]. The third documented case was reported in 2016 in an 18-month-old girl from Florida who had no travel history [5]. She passed worms in her stool over the course of 5 months, but stool examinations were negative for eggs, and she was successfully treated with pyrantel pamoate. The authors of that report indicated they had identified 2 other cases of M ingens infection that were not published.

Macracanthorhynchus ingens is abundant in raccoons in the Eastern United States and Canada, whereas M hirudinaceus is apparently scarce in swine in these locations [11–14]. The reported geographic distribution for M ingens includes southern, eastern, and some central states of the United States, and also Ontario, Canada [13, 14]. In these areas, M ingens should be considered as the most likely etiology when Macracanthorhynchus spp eggs or adult worms are recovered from patients. For example, although no morphologically or molecularly confirmed human infections with M hirudinaceus have been reported in the United States [3], 1 case was reported in a 17-month-old boy in Louisiana who passed a female Acanthocephalan worm (reported as M hirudinaceus) in his stool [15]. However, without the availability of proboscis or hook measurements or PCR results, it is not possible to distinguish M ingens from M hirudinaceus. Given the rarity of M hirudinaceus in the United States, and particularly considering the high prevalence of M ingens in the southeast [14], it is possible that this case may have represented M ingens instead.

Macracanthorhynchus infections in children have been successfully treated with pyrantel pamoate 11 mg/kg per dose and mebendazole (100 mg/dose for 3 days) [4, 5], both of which are considered safe medications in the pediatric population. Infection with Macracanthorhynchus spp is prevented by avoiding ingestion of insect intermediate hosts such as beetles, cockroaches, or millipedes.

CONCLUSIONS

This report adds to the evidence for Macracanthorhynchus spp developing to patent infection in a human host. North American physicians should be aware of the possibility of transmission to young children who may ingest invertebrates harboring infective cystacanths. Although most infections are asymptomatic or mild, M ingens infection should be considered for children with acute abdominal pain who may have recently ingested insects or who may be passing eggs or worm pieces in the stool. Given inherent challenges with identifying esoteric zoonotic parasites, expert consultation is recommended in these cases.