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Cestode Infections of Mammary Glands and Female Reproductive Organs: Potential for Vertical Transmission?

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Cestode Infections of Mammary Glands and Female Reproductive Organs: Potential for Vertical Transmission? J. Helminthol. Soc. Wash. 61(2), 1994, pp. 162-168 Cestode Infections of Mammary Glands and Female Reproductive Organs: Potential for Vertical Transmission? DAVID BRUCE CONN Department of Biology, The University of the South, Sewanee, Tennessee 37383-1000 ABSTRACT: A widely studied aberrant strain of tetrathyridia of Mesocestoides vogei infecting laboratory mice is the only cestode for which vertical transmission has been verified experimentally. Vertical transmission has been reported for Taenia saginata in cattle and Echinococcus sp. in humans, but the validity of these cases has proved difficult to verify. However, metacestode stages of Taenia solium, Echinococcus granulosus, Echinococcus multilocularis, Multiceps sp., Diphyllobothrium mansoni, Spirometra erinacei, and Proteocephalus ambloplitis have been reported from the mammary glands, uterus, placenta, and/or ovary of several naturally infected hosts. Such infection foci, particularly the mammary glands, suggest a potential for vertical transmission in these species. Such possibilities warrant further study in these and other cestodes. Field surveys of hosts should be conducted to elucidate the prevalence of cestode localization in female organs in which there is potential for transmission. KEY WORDS: Cestoda, Echinococcus, mammary glands, maternal transmission, Mesocestoides, placenta, pre- natal, sparganosis, Taenia, uterus. In recent years, interest in vertical transmis- Living parent condition sion of parasitic organisms has grown substan- By including only living parents, transmission tially. This has resulted in the elucidation of sev- by cannibalism as proposed by Mead and Olsen eral fascinating examples of transniammary and (1971) for Ophiotaenia filaroides plerocercoids intrauterine transmission of parasites as re- and by Kroeze and Freeman (1982) for Taenia viewed by Shoop (1991). Increased research ac- crassiceps cysticerci can be eliminated. As these tivity over the past 2 decades has revealed that authors suggested, cannibalism may have im- vertical transmission is common among many portant epizootiological implications. However, nematodes and trematodes. Conversely, the lim- cannibalism may occur among siblings and fre- ited data available seem to suggest that vertical quently involves a parent eating its young rather transmission is not common among cestodes. than vice versa. Thus, it is more accurate to re- However, efforts to identify cases of vertical gard this as a type of paratenesis that happens transmission among cestodes have been fewer to involve intra- rather than interspecific ex- than those involving nematodes and trematodes. change. Many cestodes have been reported to localize in female organs, which suggests the potential for vertical transmission. The present review sum- Reproduction in offspring condition marizes the published cases of vertical trans- The inclusion in the preceding definition of mission and invasion of female organs by ces- only parasites having the potential to reproduce todes and suggests directions for future research within the filial host ensures that the only cases in this area. recognized are those in which transmission re- sults in the establishment of a new source of parasite dissemination. This epizootiologically The Concept of Vertical Transmission relevant condition excludes those cases in which In this review, vertical transmission is denned microfilariae are transmitted transplacentally to as the transmission of parasites directly (i.e., unborn young as has been described for several without any intervening period either outside a species of filarial nematodes (Eberhard et al., host or in a host of another species) from a living 1993). Transplacental transmission of microfi- parent (usually a mother) to its viable offspring lariae obviously involves a specific parental/filial in which parasite reproduction can occur. This relationship but does not actually result in per- may occur in parasites having either monoxe- manent establishment of parasites in the young. nous or heteroxenous life cycles and restricts the The only epizootiological significance of this concept of vertical transmission to those situa- would be the chance that the total number of tions involving specific parental/filial relation- reservoirs available to insect vectors would be ships. increased temporarily. However, even this may 162 Copyright © 2011, The Helminthological Society of Washington CONN - CESTODE VERTICAL TRANSMISSION? 16 3 be unimportant inasmuch as the intensity of con- erally undergo more extensive histozoic migra- genital microfilaremia in most cases is probably tion than do the larvae and juveniles of cestodes. so low that the potential for transmission to in- The only histozoic migratory stages of cestodes sect intermediate hosts is negligible (Mantovani are the oncospheres and, in some species, the and Jackson, 1966). metacestodes. In most cestode taxa, these stages Vertical transmission of helminths has been are restricted to oviparous arthropod interme- demonstrated conclusively only among placental diate hosts where, as discussed above, vertical mammals. In the case of prenatal transmission transmission is unlikely. Notable exceptions to this is not surprising given the lack of transmis- this include the pseudophyllideans, the proteo- sion routes available in oviparous hosts. Among cephalideans, and the cyclophyllidean families insect hosts, Fay (1961) stated that some evi- Taeniidae and Mesocestoididae. Each of these dence existed for occasional passage of Leidy- groups has oncospheres and/or metacestodes that nema appendiculata eggs within the oothecae of migrate through the tissues of vertebrate inter- cockroaches, though she presented no data. mediate hosts, so it is not surprising that some Among avian hosts, trematodes of the genus species of each group have been reported to infect Prosthogonimus inhabit the oviducts and occa- mammary glands or female reproductive organs sionally the shelled eggs (Schell, 1985) but have (Table 1). not been reported to invade the developing chicks. Taeniids have received more attention than All known cases of postnatal vertical transmis- other cestodes, probably because of their veter- sion of helminths involve transmammary pas- inary and medical importance. Vertical trans- sage of the helminth into the nursing young. mission of taeniids would be possible only at the However, postnatal vertical transmission of pro- oncosphere or metacestode stages. If it occurred, tozoan symbionts is known to occur among ter- transmission of oncospheres could result in cys- mites during trophallaxis and proctodeal feeding ticercosis, coenurosis, or hydatidosis (depending (Cleveland, 1928). There may be some potential on the taeniid species) in the young of infected for postnatal vertical transmission among esoph- mothers. Taenia solium might present an inter- ageal nematodes of birds that feed their young esting case because humans can serve as both by regurgitation from the crop. Potential can- intermediate and definitive host, thereby result- didates for further study of this possibility might ing in either cysticercosis or adult taeniasis in the include parasites such as species of Capillaria young of infected mothers. that are capable of autoinfection of their avian Shillinger and Cram (1923) cited several au- hosts. In such cases, both paternal and maternal thors whose early reports of congenital E. gran- relationships might be involved. ulosus hydatidosis in humans were thought to have been misdiagnoses of nonparasite fetal anomalies. Shillinger and Cram's (1923) opinion Vertical Transmission of Cestodes was cited in a more recent review by Loke (1983), All helminths that are known to undergo ver- who neither agreed nor disagreed with their in- tical transmission are characterized by a histo- terpretation. Similarly, Gluhovschi et al. (1970) zoic migratory stage in the life cycle. Such a mi- reported the occurrence of 6 large but "sterile" gratory habit possibly provided an essential hydatid cysts of Echinococcus granulosus in the preadaptation for those species that penetrate the viscera of an unborn calf whose mother had an placenta, uterine wall, or mammary glands. Con- abnormal placenta. The authors regarded this as sidering this, it is not surprising that most ver- a rare instance of prenatal hydatidosis in which tically transmitted helminths are nematodes, transmission of oncospheres had been facilitated particularly strongylates and ascaridoids (Miller, by placental pathology. However, although the 1981; Lyons, 1994) or strigeoid trematodes cysts looked like hydatids upon gross examina- (Snoop, 1991, 1994). tion, the fact that they were "incompletely de- Vertical transmission appears to be rare among veloped" and "sterile" made absolute identifi- cestodes in comparison with nematodes and cation impossible. trematodes. This may be related to the fact that Several authors have reported evidence for virtually all adult tapeworms inhabit the intes- prenatal transmission of Taenia saginata (=Cys- tinal lumen of their vertebrate hosts. This is also ticercus bovis) among cattle. McManus (1960) true of adult strigeoids, strongylates, and asca- reported a 3.07% prevalence of cysticercosis bo- rids, but the juveniles of these nematodes gen- vis among 14,855 Kenyan calves, some of which Copyright © 2011, The Helminthological Society of Washington 164 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, 61 (2), JULY 1994 Table 1. Cestode infections reported from female organs. All are
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