Human Exposure to Equine Halicephalobus gingivalis in an Occupational Context

Simple Summary

Halicephalobus gingivalis can cause deadly infections in the brains and other organs of horses. In very rare cases, humans can also be exposed to this parasite when working closely with infected animals. This report describes a case where a veterinarian was exposed to the parasite while performing a routine procedure on a sick horse. The horse had severe symptoms, including eye and kidney problems, and died despite treatment. The veterinarian, after receiving preventive medication, remained healthy and showed no signs of infection. This case highlights the need for safer practices, such as avoiding oral contact with equipment used on animals, to protect veterinarians and other animal healthcare workers from potential infections. Raising awareness of these rare but serious risks is important to improve safety in veterinary practice.

Abstract

Halicephalobus gingivalis (H. gingivalis) is a very rare opportunistic cause of fatal meningoencephalomyelitis in equids but may also cause parasitic infections in exposed humans via zoonotic transmission (from animals to humans). We herein report a 39-year-old veterinarian who was exposed to aspirated gastric contents while inserting a nasogastric tube into a horse with signs of uveitis. This procedure requires application of oral suction to the end of the tube to ensure correct placement. Histopathology of the horse’s enucleated eye later revealed H. gingivalis infection, and the horse developed acute kidney injury, ataxia, and other signs of neurological disease. The horse later progressed to death despite supportive care and administration of the broad-spectrum antiparasitic, ivermectin. Two months later, the veterinarian received prophylactic ivermectin consisting of two 200-mcg/kg doses. The patient reported feeling well and was without any systemic or focal signs or symptoms prior to this prophylactic treatment and continued feeling well when followed up at 4 months post exposure. Blood work was unremarkable, with no eosinophilia (eosinophils 0.1 × 10⁹/L, normal <0.4 × 10⁹/L). Meticulous hand hygiene and alternatives to unprotected oral suction should be considered in veterinary medicine as the potentially increasing risk of occupational exposure to zoonotic helminthiases makes this a public health concern.

1. Introduction

Halicephalobus gingivalis (H. gingivalis) is a free-living nematode with wide geographic distribution and, though rare, may be of increasing concern in veterinary care settings [1]. Due to advances in veterinary medicine and greater expenditures on veterinary care given the widespread availability of pet insurance, its increasing risk of occupational exposure makes it a public health concern. H. gingivalis is commonly found in soil, decaying vegetation, and manure, with a life cycle that includes both free-living and parasitic stages. The parasite reproduces parthenogenetically, allowing females to produce offspring without mating, and infects hosts by penetrating tissues through skin wounds or mucous membranes, followed by hematogenous spread to other organs. In animals, particularly horses, the parasite typically invades neural, ocular, and renal tissues, leading to systemic infection [1]. Clinical manifestations associated with H. gingivalis infection in humans primarily involve severe neurological conditions such as meningoencephalitis, often accompanied by additional neurologic signs including brainstem manifestations, ophthalmoplegia, ring-enhancing lesions, encephalopathy, and visual impairment [1]. The widespread practice of unprotected oral suction during nasogastric intubation in equine veterinary settings significantly increases the risk of occupational exposure to H. gingivalis. Given the poor prognosis, and subsequent high fatality rate, associated with human infection by this parasite, prophylactic measures may be considered. As a result, this case report aims to understand the clinical manifestations of human H. gingivalis infection and highlight the importance of recognizing and mitigating the zoonotic potential of helminthiases to humans in the provision of veterinary medicine.

2. Case Presentation

A previously well 25-year-old horse presented for veterinary care with a 2-week history of a painful right eye unresponsive to topical hydrocortisone. Uveitis was diagnosed and both topical and oral therapies initiated; however, without improvement by later 2 weeks, enucleation was elected. Three days prior to enucleation, colic was noted, which prompted insertion of a nasogastric tube (NGT). Once located in the stomach, oral suction to the end of the tube is often carried out to evaluate reflux as horses are unable to vomit. Not uncommonly, such a procedure results in oral exposure of the veterinarian to aspirated gastric contents of the horse, and such was the case with this patient [2,3].

Histopathology of the enucleated eye revealed extensive granulomatous cyclitis, chorioretinitis, and optic neuritis with numerous H. gingivalis organisms throughout the tissue. Treatment with ivermectin at 1200 mcg/kg was administered orally, on the basis of previously published works [4]. However, 7 days following treatment, the horse began to develop progressive ataxia and depression, consistent with a systemic H. gingivalis infection, which worsened over the next 6 days. Euthanasia was elected on day 13 following treatment. Though no postmortem was conducted, the neurological and renal symptoms likely resulted from systemic dissemination of H. gingivalis from the initial infection site.

Given the oral exposure to aspirated gastric contents of a horse with active H. gingivalis meningoencephalitis and dissemination, the veterinarian was referred to our Tropical Disease Unit. At the initial visit approximately 2 months post exposure (a delay reflective of standard turnaround time for initial histopathological confirmation followed by evaluation and referral to our specialized unit by primary care), the previously well 39-year-old veterinarian reported feeling clinically well without systemic or focal signs or symptoms. Specifically, neurologic, head and neck, and gastrointestinal review of systems were negative. Further, the patient reported no fever, weight loss, or night sweats. She continued to work and attend to her activities of daily living routinely. In light of the potential exposure to H. gingivalis and after discussion of risks versus benefits, the veterinarian elected to take a standard prophylactic course of ivermectin consisting of two 200-mcg/kg oral doses two weeks apart. Basic blood work was requested.

At follow-up 4 months post exposure, the patient continued to feel well and reported excellent tolerance of the ivermectin. Blood work was unremarkable; specifically, there was no eosinophilia (eosinophils 0.1 × 10⁹/L, normal <0.4 × 10⁹/L). The patient agreed to notify our unit immediately should she develop any symptoms, particularly those suspicious for H. gingivalis infection, including fever, nausea, vomiting, or neurologic symptoms.

3. Discussion

Halicephalobus gingivalis is a rare opportunistic parasite that causes fatal meningoencephalomyelitis predominantly in equids (e.g., horses, donkeys, zebras), but can also affect ruminants such as cattle, and, more rarely, humans [5,6]. The worm is particularly neurotropic, but, like Strongyloides spp., its larvae (Figure 1) can be found in a range of human and horse tissues, including kidney, lung, optic nerves, and heart [1,7]. In horses, central nervous system (CNS) disease is the most common clinical presentation, with >80% of the 30 reported equine cases in the past 50 years presenting with encephalitis. Over the same time period, seven human cases have been reported, none of whom were treated with anti-helminthic therapies, and all of whom succumbed to meningoencephalitis (

Table 1. Published human cases of Halicephalobus gingivalis infection, diagnosed post mortem. Reproduced with permission from Onyiche et al. [1], Parasite Epidemiology and Control; published on behalf of the World Federation of Parasitologists, 2018.

Location	Year	Patient	Exposure Route	Clinical Presentation	Publication
Canada	1975	5-year-old male	Wound contamination (manure)	Meningoencephalitis, mandibular injuries	Hoogstraten and Young (1975) [8]
United States	1979	47-year-old male	Unknown	Meningoencephalitis, brainstem signs	Shadduck et al. (1979) [9]
United States	1981	54-year-old male	Wound (ulcer) contamination	Bilateral internuclear ophthalmoplegia.	Gardiner et al. (1981) [10]
United States	2010	39-year-old female	Wound contamination (koi pond)	Meningoencephalitis, bilateral ring enhancing lesions	Ondrejka et al. (2010) [11]
United States	2013	65-year-old female	Unknown	Encephalopathy, blurring of vision	Papadi et al. (2013) [12]
Australia	2014	74-year-old female	Unknown	Meningoencephalitis, frontoparietal meningitis	Lim et al. (2015) [7]
Germany	2015	49-year-old (sex not reported)	Workplace exposure (paper mill)	Meningoencephalitis	Monoranu et al. (2015) [13]

) [1]. Ownership of and/or direct exposure to horses was confirmed in two of the seven fatal cases, while soil exposure, mill work, heavy alcohol use, and immunosuppressive therapy were contributory in the others. In six of the seven fatal human cases with a reported cerebrospinal fluid profile, four had a lymphocytic pleocytosis, while only one had an eosinophilic pleocytosis.

Treatment of horses with H. gingivalis infection involves ivermectin either with or without albendazole, though high-quality intervention trials supporting clinical recommendations are lacking; if there is CNS involvement, prognosis is guarded [4]. Given the high tolerability and safety of ivermectin along with the potentially severe consequences of H. gingivalis infection, post-exposure prophylactic doses of ivermectin (as one would treat strongyloidiasis) seem prudent [14], albeit without evidence underpinning this intervention. Given the uncertain aspects of the parasite’s life cycle, notably the prepatent period and migration route in humans, the optimal timing of post-exposure prophylaxis of an asymptomatic person with oral ivermectin is unknown. As such, a specific protocol is neither evidence-based nor likely generalizable. However, given the incubation period of other human Rhabditida nematodes—such as Strongyloides stercoralis—post-exposure prophylaxis within 1–3-months of potential exposure seems wise.

In addition to post-exposure ivermectin, the efficacy of which remains uncertain, steps to prevent zoonotic transmission can be undertaken. Specifically, when evaluating reflux following nasogastric intubation, alternatives to unprotected oral suction include mechanical or hydraulic aspiration to prevent direct oral contact with gastric contents. Such alternatives should be considered, particularly if there is any infectious disease concern. Potential occupational exposure to zoonotic helminthiases can also be reduced by wearing respirators and double gloves and engaging in meticulous hand hygiene after animal contact, particularly after handling highly infectious animal effluents such as fecal matter [14].

4. Conclusions

This case report highlights the potential occupational risks associated with H. gingivalis infections in equine veterinary settings, particularly in relation to unprotected oral suction during nasogastric intubation. The fatal outcomes associated with infections caused by H. gingivalis in both humans and equines suggest that prophylactic treatment, though based on limited evidence, may be justified given the severe consequences of such infection. Similarly, adopting alternative methods, such as mechanical or hydraulic aspiration, and practicing thorough hand hygiene to mitigate zoonotic transmission risks and enhance the safety of veterinary professionals is strongly recommended. Ultimately, this case contributed to the limited body of knowledge on potential human exposure to H. gingivalis, emphasizing the need for heightened awareness and early intervention and the importance of recognizing and mitigating the zoonotic potential of helminthiases in veterinary practice.