Sparganosis: an under-recognised zoonosis in Australia?

Abstract

Sparganosis is a rare zoonotic parasitosis that is sporadically reported worldwide. In Australia, the causative tapeworms are considered endemic in wildlife animals, however, there have been only five reported human infections. We present three additional cases of sparganosis, involving two Australian born gentlemen who have never travelled overseas and a woman who emigrated from Ethiopia. The first man presented with two unusual subcutaneous lumps that migrated along the anterior abdominal wall connected by a tunnel. The second man presented with two separate lumps, one on the thigh and the other on the left upper abdomen over a 4-week interval. The woman presented with 6 weeks of intermittent fevers, night sweats, abdominal pain and passing intestinal worms. This series of patients suggests that sparganosis is under-recognised in Australia and serves as a reminder for clinicians to the varied presentations that can be characteristic of this lesser known zoonosis.

Background

Sparganosis or spirometrosis is a parasitic infection by the plerocercoid larval stage (also termed as sparganum) of several species of cestodes within the genus Spirometra.¹ Etymologically, the term sparganum is derived from the Greek word sparganon, which translates as a swathing band and aptly describes the macroscopic features of the flat, white, sticky, ribbon-like larva. The first case of human infection was discovered by Patrick Manson in China in 1882. The genus Spirometra has a worldwide distribution but they are most common in East Asian countries such as Japan, Korea and China. Clinical presentation can be variable depending on the organs involved but cutaneous manifestation is common.

Case presentation

An 84-year-old Australian man from Queensland presented to a district hospital with two unusual masses in the abdominal wall in the left iliac fossa where one moved superiorly to the anterior abdomen over a 3-week period (figure 1). Initially, these masses were about 5 cm in diameter, duly tender without cutaneous discolouration. The upper lesion then became erythematous and failed therapy with oral antibiotics.

Figure 1.

Postoperative wounds demonstrating previous locations of the two adjacent spargana in the anterolateral abdominal wall—a common location for subcutaneous sparganosis.

The patient was a well beef cattle farmer without any major comorbidities and has never travelled overseas. He had intermittent exposure to pigs and drank fresh tank water but denied consuming wildlife in which these parasites were considered endemic.

The second patient was a 45-year-old Australian man who found a lump on the left upper quadrant of his abdomen. It was approximately 3 cm in diameter with no overlying skin changes but caused a dull ache and was mobile on palpation. He had a similar lump removed from his left medial thigh 3 weeks earlier. The histology of this first lump was non-specific and the differential diagnoses were either an abscess or foreign body granulation tissue.

He was a property developer who also has never travelled overseas. He had a negative exploratory laparotomy at 21 years of age after a motor vehicle accident but otherwise was fit and healthy. He had temporarily relocated to the rural areas for about 18 months for construction projects and had his medical needs addressed at remote hospitals. Apart from frequently visiting construction sites, he denied unusual practices where he would be at risk of acquiring a zoonotic infestation.

The third patient was a 34-year-old Ethiopian woman who had immigrated to Australia 6 months prior. She presented to a tertiary hospital emergency department with 6 weeks of intermittent fever, night sweats, abdominal pain and passing intestinal worms in her bowel motions which she had collected a jar-full for inspection. She had no cutaneous masses.

She worked in a fish market and consumed unfiltered water in her native country. She was treated for intestinal worms 12 months previously and was tested again by International Medical Organisation before taking refuge in Australia.

Investigations

In the 84-year-old man, the ultrasound (US) of the masses appeared as focal subcutaneous cellulitis; however, the patient’s routine panel of haematological, biochemical tests as well as cysticercosis serology were normal. A fine needle aspiration was suggestive of an abscess.

For the 45-year-old man, an US was obtained for the proximal thigh lump, which was also non-diagnostic, but no investigation was performed for his abdominal wall lump as the clinician thought it was a simple cyst.

The 34-year-old female patient had full blood count, urea and electrolytes, liver function tests, ova, cysts and parasites examination of the larva collected. These were flat and white measuring up to 17 mm in length and 6 mm in diameter. They were identified as spargana with the likely species being Spirometra mansonoides.

Treatment

Intraoperatively, the lesions on the abdominal wall of the beef cattle farmer were of a creamy yellow consistency and had a long communicating tunnel between the two masses. They were excised completely; histological examination demonstrated a sparganum in each lesion surrounded by necrotising granulomatous infiltration in the lower dermis and subcutis.

The anterior abdominal wall lesion in the 45-year-old man was excised and histology demonstrated sparganosis.

The 34-year-old woman was treated with 3 days of mebendazole and provided contraception advice.

Outcome and follow-up

For the excised masses, the wounds healed well, and subsequently no new lumps arose. The female patient’s fever and abdominal pain resolved. No evidence of recurrence was noted at 12 months.

Discussion

The species of sparganosis include S. mansoni, S ranarum, S. mansonoides, S. erinaceieuropaei and S. proliferum.¹ The two primary causative agents are S. mansoni, common in North and South America, and S. erinaceieuropaei, a common tapeworm in Asia and Australia with a wide distribution in South East Queensland and New South Wales infesting cats, dogs and foxes.^1–3 The sparganum parasitises a range of hosts, these include lizards, snakes, frogs and wild pigs.² Their complex life cycle is demonstrated in the diagram below (figure 2).

Figure 2.

Life cycle of sparganum. The adult tapeworms live in the intestine of cats, dogs, pigs and foxes (7). Eggs (1) are shed in faeces and embryonate (2) in the environment and hatches in water to release coracidia (3). These oncospheres (coracidia) are ingested by crustaceans (4—first intermediate hosts) and develop into procercoid larvae. Infected crustaceans are then eaten by secondary intermediate hosts such as fish, reptiles and amphibians (5). The procercoid larva then crosses the small intestinal wall and migrates to diverse locations in the body where it develops into the plerocercoid larva (second-stage larva), also termed sparganum 1. The cycle is completed when the intermediate hosts are ingested by a definitive host (7) and allows maturation of the larvae into adult worms. Humans (8) cannot be definitive hosts but rather paratenic or accidental hosts where the parasites remain in larval form (adapted from Centers for Disease Control and Prevention [CDC], 2011 [http://www.dpd.cdc.gov/DPDx/HTML/Sparganosis.htm]; reproduced with permission of CDC).

The cycle is completed when a secondary intermediate host, such as fish, infected with the sparganum is eaten by a carnivorous definitive host such as a dog. The sparganum matures into the adult tapeworm in two to 3 weeks, which then can survive up to 30 years.^{4 5} There are a number of paratenic hosts where the sparganum encysts in tissues, and perhaps increase in size, but does not mature into the adult worm. A wide range of animals including pigs, mice and birds may ingest the infected intermediate hosts and then serve as reservoirs where the sparganum survives.¹

Humans are accidental and paratenic hosts, contracting the infection by drinking water contaminated by infected Cyclops crustaceans, or by ingesting undercooked flesh of frogs, snakes and pigs. Transmission can also occur when open wounds are treated with application of traditional frog or snake poultices.

Human sparganal infection commonly presents as subcutaneous nodules or abscesses but cases of pulmonary, ocular, cerebral sparganosis have been reported and clinical symptoms depend on the location of the lesions. In Australia, there have been four case reports of subcutaneous sparganosis in local Australians dating back as early as 1905.^{2 6–8} A single case of cerebral sparganosis was reported in an East Timorese refugee.⁹ Human sparganal infestations in Australia are collated in table 1.

Table 1.

Human sparganosis in Australia

	Year reported
	1905	1915	1953	1983	1994	2017	2017	2018
Age (years)	*	42	38	28	23	34	45	84
Gender	Male	Male	Female	Male	Male	Female	Male	Male
Migration status	*	Local resident	Local resident	Local resident	East Timorese refugee	Ethiopian refugee	Local resident	Local resident
Comorbidities	*	Nil	Nil	*	Nil	Intestinal worms treated 12 months prior	Laparotomy at 21 years old for motor vehicle accident	Hypertension
Risk factors	*	Frequent camper	*	Hunter and consumed wild pigs, rabbits, snakes	Soldier in East Timor jungle	Fishmonger, drank unfiltered water	Frequent visits to rural construction sites as property developer	Farmer, drank fresh tank water
Predominant presenting symptoms	Subcutaneous mass—right subcostal margin	Inflamed mass on leg	Several lumps on thigh	Migratory subcutaneous lump in lumbar region	Seizures and subcutaneous cervical nodules	Fever, abdominal pain and passing intestinal worms	Left upper quadrant subcutaneous mass	Left iliac fossa migratory subcutaneous mass
Treatment	Excision	Excision	Excision	Excision	Surgical excision of brain lesion and praziquantel	Mebendazole	Excision	Excision
Outcome	Cure	Cure	Cure	Cure	Cure	Cure	Cure	Cure

*Information not provided.

Worldwide, human sparganosis case reports are sporadically documented, particularly in East Asia. Liu et al recently reviewed the global burden of this disease (over 1600 cases) and identified improvement in healthcare system in endemic regions as one of the factors for increased reporting of this neglected zoonosis.¹⁰ Globally, cerebrospinal sparganosis has a poor prognosis with the highest prevalence of over 440 identified cases, mainly in China and Korea.¹⁰ Subcutaneous infestation has occurred over 220 cases according to Liu et al followed by ocular (74 cases) and pulmonary infections (40 cases).^{10 11} Visceral and proliferative sparganosis are even more rarely reported.¹⁰

Diagnosis of sparganosis is usually made by histological identification of the sparganum in excised tissue (figure 3). Spargana are white flat worms typically 1–2 mm wide and range from 2 to 115 mm in length. Characteristic features of the larva form include an absence of hooklets and bladder wall as well as lacking internal organs appearing as a solid non-cavitated body. Serological testing is not available in Australia and often it is only complementary to diagnosis due to potential cross-reactivity with other cestodes common in spargana-endemic regions.¹²

Figure 3.

Photomicrograph with periodic acid–Schiff stain (magnification x2) which highlights tegument encompassing a solid, non-cavitated parenchyma without alimentary tract, which are typical features of a sparganum.

Medical treatment of sparganosis is reportedly ineffective where the immature forms of the parasite can be resistant to praziquantel and mebendazole.¹ However, Munckhof et al reported to have successfully treated a case of suspected disseminated sparganosis with praziquantel over 2 weeks. In our patient with intestinal sparganosis, antihelminthics appeared to be effective with resolution of symptoms, however this patient was already treated with a course of mebendazole 12 months prior. It would be difficult to ascertain whether recurrence was due to new transmission or partial response to initial treatment. In addition, mebendazole is poorly absorbed into the blood stream; its utility for treatment of cutaneous manifestation cannot be commented base on the above cases.

Excision of the parasite is still the treatment of choice, which is often curative and therefore highlights the importance of surgeons being aware of this rare zoonotic disease. One of the reported patients had a lump from his thigh removed 3 weeks earlier without a clear histological diagnosis and hence there were conjectures of whether this was unrecognised sparganosis.

Although the first patient has never travelled overseas, his lifestyle would have exposed him to Spirometra species from drinking tank water, fishing and raising pigs. For the second man, transmission can only be speculated to be during his visits to damp, unhygienic construction sites in the rural environment. Contact history for the Ethiopian patient can probably be attributed to fish handling and drinking unsanitised water in a poverty-stricken country. However, she had been living in cleaner Australian conditions over 6 months before manifesting symptoms suggesting that incubation period for sparganosis can be lengthy and varied, supporting previous literature reports. In addition, all the native Australian infections occurred in rural settings and therefore rural practitioners should be more cognisant of this disease.

Given the ease with which spargana can be transmitted between species and their endemic nature within Australia’s wildlife, it is surprising to see that very few cases have been reported. We would like to draw the attention of clinicians to consider this rare parasitic disease as a differential, especially in unusual presentations where it could be a diagnostic challenge.

Learning points.

• Human sparganosis is a very rare parasitic infection in native Australians.

• The treatment of choice for subcutaneous sparganosis is excision and can be curative.

• This lesser known zoonotic disease is endemic in Australia’s wildlife, the sparganum parasitises a wide range of hosts and is likely under-recognised in the Australian population.