Invasion of the vertebrate skin by cercariae of Trichobilharzia ocellata  : penetration processes and stimulating host signals

Abstract

The penetration of Trichobilharzia ocellata cercariae into the skin of their duck hosts was described using electron microscopy and histology. The behavior patterns of the cercariae on their exposure to human skin differed only little from those known for Schistosoma mansoni cercariae. After their attachment to living human skin the cercariae crept to wrinkles within a mean of 8 s, and full penetration was achieved within a mean of 4.0 min (83 s to 13.3 min). Tail shedding occurred as early as within a mean of 6.5 s of the first penetration attempts. It was supported by a muscular sphincter at the cercarial hindbody. The skin-surface stimuli for cercarial penetration were contained in the lipid fraction of the duck and human skin surface; hydrophilic components were effective only in some T. ocellata isolates. The penetration-stimulating components of duck-skin lipids were exclusively free fatty acids with the same chemical characteristics known to stimulate penetration of Schistosoma species. Skin-surface lipids of the abnormal human host, with their higher fatty acid contents, stimulated higher cercarial penetration rates than did skin lipids of the natural duck host. Fatty acids as penetration stimuli may offer advantages for T. ocellata cercariae by increasing the specificity for an invasion of terrestrial vertebrates, which is additionally determined by cholesterol and ceramides as signals for attachment and enduring contact behavior.

Avian Schistosomes and Outbreaks of Cercarial Dermatitis

“…Full penetration of living human skin was achieved within a mean of 4 min (83 s to 13.3 min), which was significantly faster than the case for the human parasite S. mansoni (6.58 min, on average) (177). Faster penetration of avian schistosome cercariae might be a consequence of these parasites' adaptation to lower concentrations of fatty acids in duck skin; therefore, reaction to higher concentrations in human skin may induce faster invasion (177,178). Another explanation may be that different histolytic enzymes are used for penetration (see below).…”

“…Surprisingly, there were few differences between the avian T. szidati and human S. mansoni organisms in their pattern of invasive behavior toward living human skin; most cercariae did not penetrate the skin immediately after attachment but performed a leech-like creeping which lasted 0 to 80 s for T. szidati and 15 s to 5.58 min for S. mansoni (177). Such behavior guided the cercariae to skin wrinkles or hair follicles, where most penetration sites were located (178) (Fig. 3).…”

“…3). Penetration behavior and production of secretions stimulate neighboring cercariae to use the same entry site on the skin (177,178). Invasion of the skin is facilitated by secretions of cercarial penetration glands released from openings at the apex of the muscular head organ by spasmodic contractions of cercarial body musculature (179).…”

“…Invasion of the skin is facilitated by secretions of cercarial penetration glands released from openings at the apex of the muscular head organ by spasmodic contractions of cercarial body musculature (179). The head organ performs concurrent thrust movements against the skin surface while the cercaria is firmly attached by the ventral sucker (176,178,180). Signals for skin invasion seem to be universal for schistosomes-fatty acids, especially polyunsaturated fatty acids containing 18 carbons and two or three cis double bonds (linoleic and linolenic acids), which are bound in cell membranes and occur as free molecules on the surface of human and bird skin (176).…”

Penetration ofTrichobilharziacercariae into mammals: dangerous or negligible event?

“…Nevertheless, these penetration stimuli are not strictly host-specific, because cercariae of bird schistosomes readily penetrate also the skin of nonpermissive hosts-mammals (humans). This phenomenon can probably be explained by a high content of penetration signals (fatty acids) in the mammalian skin (Haas & van de Roemer, 1998). Skin disruption is facilitated by products of cercarial penetration glands.…”