Strongyloides fuelleborni kellyi in New Guinea: neglected, ignored and unexplored

The Western Pacific region has among the highest burden of strongyloidiasis in the world¹. While Strongyloides stercoralis is endemic in Papua New Guinea (PNG), the island also harbours a second human-infecting Strongyloides species, Strongyloides fuelleborni kellyi.

The presence of a previously undescribed Strongyloides was first identified by Allan Kelly of the PNG Institute of Medical Research in 1971². Due to close morphological resemblance to S. fuelleborni fuelleborni, a parasite of humans and non-human primates in Africa and Asia, the species was originally described as a Strongyloidesfuelleborni-like helminth, later changed to S. f. kellyi. Sequencing of the 18S ribosomal RNA gene revealed clustering at this target within a distinct clade including S. cebus, S. papillosus and S. venezuelensis but separate from S. f. fuelleborni³.

Infection is primarily found in infants and young children, with egg loads peaking at 20 months of age^4–8. High-intensity infection in infants <2 years of age can cause a rapidly fatal disease known as swollen belly syndrome (SBS), characterised by gross abdominal distension and respiratory distress⁸. SBS is most commonly seen in infants around 2 months of age⁸. The characteristic swollen belly observed in this condition is due to ascites following a protein-losing enteropathy. The signs and symptoms of SBS include a very low serum protein, ascites, peripheral oedema, mild diarrhoea with very high numbers of S. f. kellyi eggs in faeces, occasional vomiting, a high-pitched cry, fever (in some cases) and respiratory distress⁸. Haemoglobin levels remain normal⁸. Heavy infections in older children may be associated with failure to thrive, but many older children appear asymptomatic⁸.

Strongyloides fuelleborni kellyi has been found in multiple provinces of PNG⁷ and has also been reported from Irian Jaya in Indonesian Western New Guinea⁵. No work has been performed on the distribution or prevalence of this parasite since 1997⁹. Historical surveys conducted between 1981 and 1997 reported prevalence in children from endemic areas ranging between 20% and 93%, with most studies finding a prevalence of over 60% in children aged <10 years^4,6–13. Prevalence peaked between 20 and 36 months of age^4,6. Prevalence in children from high-intensity infection communities may reach 100%^4,8 and it was not unusual in such communities for children to pass more than 100 000 eggs per mL of faeces⁸. Prevalence rose steeply from 1 month to 4 months of age⁶, but by 10 years of age prevalence fell and the intensity of infection rarely exceeded 500 eggs per mL of faeces⁸. Prevalence in adults from affected communities was only 5–10%. The parasite was found infecting people in both rural and remote communities, and larger towns and cities⁶, although with a much lower prevalence in urban areas^4,12. Environmental factors such as altitude, slope of ground, landform, rainfall and population densities do not influence distribution of the parasite, although it is uncommon in areas with limestone and polygonal karst⁷. It is not known if an animal reservoir of infection exists⁸. Pigs were investigated extensively as a potential zoonotic source but no S. f. kellyi infections were found¹⁴.

In high prevalence communities, patent infection may occur in infants only 14–18 days old. The exposure of infants to filariform (infective) larvae in soiled bedding used to line string bags in which they were carried might have led to rapid external autoinfection, causing the very high-intensity infections seen in this age group⁸. Internal autoinfection, which is seen in S. stercoralis infections, is thought not to occur. This is because S. f. kellyi are passed as eggs in faeces, unlike S. stercoralis, which are passed as larvae^8,15. Also, prevalence and egg counts are observed to decline with age^{4,6,7,9,11,13}, indicating that maintenance of infection via an autoinfective process is likely not occurring.

S. f. kellyi eggs average 51.4 (47–55.8) µm in length by 32.1 (31.1–33.1) µm in width¹⁵ and contain well developed larvae⁸ that hatch within hours of passage⁸. In asymptomatic adults, these are normally single eggs free in the faeces (JM Shield, personal communication). However, in children with heavy infections, strings of eggs encased within a fine membrane (Figure 1)^8,15 or masses of eggs (Figure 2) may be seen⁸. The hatched larvae are morphologically indistinguishable from those of S. stercoralis¹⁵.

Figure 1.  Strongyloides fuelleborni kellyi eggs (~51 × 32 µm) within a mucous membrane string, saline wet mount (image by Dr Paul Crouch-Chivers, courtesy of Dr Jennifer Shield, La Trobe University).

Figure 2.  Strongyloides fuelleborni kellyi egg mass in a child with high-intensity infection, saline wet mount (image by Dr Paul Crouch-Chivers, courtesy of Dr Jennifer Shield, La Trobe University).

Diagnosis of infection in very young infants may often be missed or delayed as it is generally assumed by clinicians that children of this age cannot yet have acquired intestinal helminths⁸. Misdiagnosis as hookworm is common due to the similar morphology of eggs⁸. Diagnosis from faeces is reliant on the presence of proficient microscopists who are aware of the existence and morphology of S. f. kellyi eggs, which are smaller and more developed upon passage than those of hookworm.

The parthenogenic adult parasitic female of S. f. kellyi appears to be morphologically indistinguishable from S. f. fuelleborni¹⁵. It may be differentiated from S. stercoralis by the presence of spiral rather than straight ovaries¹⁵. Due to the difficulty in obtaining adult parasitic females this approach is not viable for routine diagnosis. S. f. kellyi may be differentiated from S. f. fuelleborni and S. stercoralis in its cultured free-living adult stage. Like S. f. fuelleborni, the free-living female of S. f. kellyi has a prominent post-vulval constriction, which is not seen in S. stercoralis¹⁵. There is also slight variation in the morphology of a portion of the peri-vulval cuticle of the S. f. kellyi free-living female when compared to that seen in S. f. fuelleborni¹⁴. Differences in the morphology of free-living males involve a more anterior position of the phasmidal pore relative to the sub-ventral, sub-dorsal post-cloacal papillae¹⁴. Detection and differentiation of these very subtle morphologic differences requires a very advanced level of parasitological expertise.

A treatment intervention study using thiabendazole (25 mg/kg twice daily for 3 days) was conducted between 1983 and 1984. This study found that thiabendazole eliminated egg passage in 86 of 88 infected children, with a very significant reduction in egg passage in the remaining two participants¹⁶. Reinfection after treatment was common⁶. Fifty-eight percent of treated children were found to be reinfected 18 months after treatment⁶. The modal time for reinfection was 9 months⁶. The standard treatment in PNG for Strongyloides in adults in PNG is albendazole 400 mg daily for 3 days¹⁷. Standard treatment for children with anaemia and oedema is albendazole 200 mg for those 5–9.9 kg and 400 mg for those ≥10kg daily for 3 days. Oedema in this context may include SBS due to S. f. kellyi¹⁷. The efficacy of ivermectin, moxidectin or combination anthelmintic therapies against S. f. kellyi has not been explored.

Very little work has been performed on S. f. kellyi in the past 30 years. Important questions, such as what is the current prevalence and distribution, and if it might be a zoonosis with an animal reservoir, have not been answered. This human helminth remains neglected, ignored, and unexplored, despite being present and likely widespread in Australia’s nearest neighbour.

The author declares no conflicts of interest.

This research did not receive any specific funding.