Strongyloides stercoralis infection in marmosets: replication of complicated and uncomplicated human disease and parasite biology

Abstract

BackgroundStrongyloides stercoralis can undergo an alternative autoinfective life cycle in the host, which, in some individuals can lead to a lethal infection. However, due to a number of factors, such as, the majority of those infected are from low-income backgrounds and the limitation in experimental models for studying human S. stercoralis, strongyloidiasis remains neglected. Improved knowledge of animal models that are susceptible to this parasite is needed in order to investigate the immunological mechanisms involved during infection and in particular to further understand the natural history of the autoinfective cycle.MethodsCallithrix penicillata were inoculated subcutaneously with 100 (n = 2), 300 (n = 4) or 500 (n = 9) third-stage infective larvae (L3i) of S. stercoralis of human origin. Three marmosets received smaller inocula (i.e., one received 100 and two received 300 L3i) to ensure a greater capacity to withstand the infection after immunosuppression, which was triggered by administration of dexamethasone during early patency. Qualitative faecal analyses began at 7 days post-infection (DPI), and semi-quantitative tests were also performed for the dexamethasone-treated primates and the three matched controls. During the necropsies, specimens of S. stercoralis were recovered and tissue fragments were processed for histopathology.ResultsThe mean prepatency and patency periods were 16.1 ± 3.0 and 161.1 ± 72.2 DPI, respectively. The marmosets typically tolerated the infection well, but immunosuppressed individuals exhibited higher numbers of larvae in the faeces and progressive clinical deterioration with late disseminated infection. In these cases, the number of females recovered was significantly higher than the number of inoculated L3i. Large quantities of larvae were observed migrating through the host tissues, and histopathology revealed pulmonary and intestinal injuries consistent with those observed in human strongyloidiasis.ConclusionsBoth complicated and uncomplicated strongyloidiasis occur in C. penicillata that is described as a susceptible small non-human primate model for S. stercoralis. This host permits the maintenance of a human strain of the parasite in the laboratory and can be useful for experimental investigations of strongyloidiasis. In parallel, we discuss data related to the autoinfective cycle that provides new insights into the biology of S. stercoralis.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-014-0579-2) contains supplementary material, which is available to authorized users.

Strongyloides stercoralis infection in marmosets: replication of complicated and uncomplicated human disease and parasite biology

“…Eggs, rhabditiform and filariform larvae observed in the bronchioles and other segments of the airway, oesophagus and stomach were considered to be products of adult worms located in the lung parenchyma or in the terminal segments of the tracheobronchial tree. The idea that at least one generation of S. stercoralis can occur in the host lungs was corroborated by the observation of adult parasites [84,85,104,105] and eggs, which are sometimes embryonated, in the lungs and in the airways of human patients [4,97,98,106]. Furthermore, the observation of 4 apparently fertile parasitic females of S. stercoralis together with 21 rhabditiform larvae/ g of kidney tissue from an immunosuppressed dog infected with human nematodes [47] also indicates that the nematode may produce offspring in organs other than those of the digestive system.…”

Infección natural por Strongyloides stercoralis en Pithecia monachus (Primates, Pitheciidae). Primer reporte en el Perú

“…Penner (1981) reportó tres casos de autoinfección fatal con S. stercoralis en Gorilla gorilla y Pan troglodytes ocurridos en el Zoológico de San Diego (EEUU). En Sudamérica no hay investigaciones confirmadas de infección natural de primates con S. stercoralis, porque los reportes solo se refieren a resultados de estudios coprológicos; sin embargo, al estudiar el comportamiento de Callithrix penicillata como animal modelo para investigar aspectos clínicos y patológicos de la infección por S. stercoralis, se concluyó que este primate es susceptible a la infección (Mati et al, 2014).…”

The severely under‐recognized public health risk of strongyloidiasis in North American cities—A One Health approach

“…Individuals exposed to contaminated soil due to inadequate sanitation may also be risk; this might include any individual contacting soil where humans (or dogs) have recently engaged in open air defecation or near or with shallow latrines, including individuals living in homeless encampments, which are not uncommon in US cities (Herring, 2014). Additionally, given the potential infection of non-human primates with S. stercoralis (Mati, Raso, & Melo, 2014), zoo workers could potentially be at risk. Finally, many commercial dog-breeding breeding facilities (e.g.…”