Morphological Adaptations of Intestinal Helminths

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868 THE JOURNAL OF PARASITOLOGY, VOL. 77, NO. 6, DECEMBER 1991thought to be surface amplification, as the efficientabsorption of nutrients by the tegument wasessential for helminths that had no gut. Microtricheswere also implicated in protection fromthe host (Morseth, 1966; McVicar, 1972), anchoring(Rothman, 1963; Mount, 1970; Hayungaand Mackiewicz, 1975), and locomotion(Rothman, 1963; Berger and Mettrick, 1971).Other suggestions have included the possibilitythat the microtriches might anchor the parasiteby interdigitating with the intestinal microvilli(Rothman, 1963) or that the spines might actlike cilia to facilitate absorption by agitating themicrohabitat and thus recirculating the intestinalcontents (Rietschel, 1935). There is strong evidencethat "membrane digestion" (adsorption ofdigestive enzymes by the surface membrane) occursin cestodes (Smyth, 1972) and that contactstimulus between the mucosa and the scolex maytrigger strobilization and development (Smyth,1969a); however, the role of the microtriches inthese processes is not clearly defined.Some very revealing clues about microthrixfunction were obtained from observations madeby Braten (1968) who carefully compared thesurfaces of larval and adult specimens of Diphyllobothriumlatum. As a result of detailedmeasurements from electron micrographs, heobserved that both the number and size of thetegumental microtriches of D. latum adults weresignificantly greater than those of the plerocercoidstage. This represented a significant surfacearea amplification that could be correlated withthe increased metabolic demands of transitionfrom the intermediate to the definite host. However,his measurements further revealed that mostof the growth in the microtriches occurred in theproximal shaft whereas the size of the distal spineremained relatively constant. From this he concludedthat the shaft of the microthrix was involvedin nutrient absorption but that the spinemust have some other function, perhaps protectionor anchoring. An anchoring function for themicrothrix spine was given further support bythe work of Mount (1970) who showed that therostellar hooks of Taenia crassiceps appear todevelop directly from microtriches with unusuallylarge spines.The greatest amount of variation in attachmentorgans is seen in cestodes, particularly thoseof fishes. The rosette of the monozoic cestodariansappears to be a delicate holdfast organwhereas the larger, strobilated eucestodes requirethe stronger attachment afforded by a scolex. Thecestodes of elasmobranchs display an impressivevariety of holdfast modifications, with elaboratebothridia and a fingerlike projection of the scolex,the myzorhynchus, that penetrates the mucosato afford an even firmer anchoring. As illustratedby Williams et al. (1970), the scolexoften appears tailored for an exact fit with themucosal villi of its host. "Williams dispelled thesuggestion that the scolex subsequently grows tofit in with the host's mucosa after the establishmentof infection by stressing that the main featuresof scolex morphology are present at an earlydevelopmental stage. In a young specimen ofEcheneibothrium sp. the scolex is almost identicalin size and form with that of an adult specimen"(Crompton, 1973).In his examination of the parasite-host interfaceof 3 tetraphyllidean species, McVicar (1972)observed that the tegument of the bothridial rimof Acanthobothrium quadripartitum was attachedso firmly that parts of the host mucosalcells appear to be pulled apart, leaving noticeableintracellular spaces. Examination of the sites ofbothridial attachment for the other species revealeda breakdown of the host intestinal microvilliand the accumulation of membrane-boundosmophilic material in the host cells. In Echeneibothrium,species of which possess a myzorhynchus,the intestine showed signs of severedamage at the site of penetration. Both the presenceof tegumental microtriches with well developedproximal shafts and the high level ofalkaline phosphatase activity in the tegument ofthe myzorhynchus, together with the obviousdegradation of host tissue, lend credence toSmyth's (1969b) suggestion of a "placental role"for the attachment organs of at least some cestodespecies.HOST RESPONSE TO THE PARASITEFor the most part the host response to intestinalhelminths involves a typical inflammatoryreaction (see review by Befus and Bienenstock,1982). Histological changes in the mucosa followinginfection may include goblet cell hyperplasia(Ackert et al., 1939), hyperplasia of thepaneth cells (Roberts-Thomson et al., 1976),villus atrophy and crypt hyperplasia (Symons,1965; Manson-Smith et al., 1979), and the typicalhistopathological changes associated with anintestinal granulomatous response (Jones andRubin, 1974).McVicar (1972) had concluded that "variationin the degree of damage inflicted by the bothridia
HAYUNGA-MORPHOLOGICAL ADAPTATIONS OF INTESTINAL HELMINTHS 869FIGURE 1. Section through a nodule of Hunterellanodulosa, showing loss of epithelium at the opening ofthe nodule and hyperplasia of the submucosal tissue.Note how the posterior part of the worm extends intothe lumen of the gut (plastic section, toluidine blue).(From Hayunga and Mackiewicz [1975], courtesy ofPergamon Press.)of the tapeworms of R. naevus seems to dependpartly on the cestode's size, mode of attachmentand ability to move." The results of his examinationof the parasite-host interface of tetraphyllideanssuggested a strong relationship betweenscolex structure and intestinal damage.Around the same time as that study, Mackiewicz(1972) was independently asking similar questionsabout caryophyllidean cestodes. Caryophyllideansdisplay considerable variation inscolex structure, ranging from the totally undifferentiatedanterior surface of Hunterella nodulosato species whose attachment organs includebothria, loculi, and terminal discs, each in variousdegrees of development. Furthermore, theirrestriction to cyprinid fishes should allow for directcomparisons of intestinal damage.Mackiewicz et al. (1972) reported that thegreatest degree of intestinal damage was observedfor those caryophyllidean species withpoorly developed attachment organs. Monobothriumingens, H. nodulosa, Monobothrium ulmeri,and Biacetabulum biloculoides were eachassociated with pronounced granulomatous reactions,resulting in the formation of conspicuousnodular lesions that in some cases containednecrotic material. The presence of an eosinophilic,perhaps mucoid, layer at the parasite-hostinterface, best seen in M. ulmeri, "varies fromspecies to species. It is generally absent wherethere is no tissue reaction and is most pronouncedin the nodules and other lesions." It isprobably a secretory product of the parasite; suchmaterial was suggested by Liu and Edward (1971)to function as an adhesive. In contrast, thosespecies with well developed, specialized holdfastorgans elicit little or no response; intestinal damageappears limited to compression of the villiand minor distortion of the shape of the crypts.This topic was pursued further by Hayunga(1977) who examined scolex structure of the mostundifferentiated species, H. nodulosa, at both thelight and electron microscopic levels. As shownin Figure 1, H. nodulosa is found in the anteriorgut, clustered within a nodular lesion characterizedby a loss of epithelium and extensive hyperplasiaof the submucosal tissue. Althoughlacking holdfast organs, worms are anchoredfirmly in the nodule and must be removed forciblyfor examination. When relaxed, the posteriorportion of the parasite extends into the lumenof gut.Electron microscopic examination of the tegumentof H. nodulosa revealed typical cestodemicrotriches covering the surface of the anteriorportion of the worm (Fig. 2). However, microtricheson the posterior surface were noteworthyin that they lacked the terminal spine (Fig. 3) andmore closely resembled the surface microvilli ofthe cestodarian Gyrocotyle urna as described byLyons (1969). These findings support earlier conclusionsthat the proximal shaft of the microthrixis primarily involved in the absorption of nutrients,whereas the spine assists in anchoring theparasite. However, as the crypt of the nodule isdevoid of host epithelium, any anchoring functionof the microtriches must be achieved bymeans other than interdigitation with intestinalmicrovilli (Hayunga and Mackiewicz, 1975). Lackof phosphatase activity on the scolex surfacewould be consistent with the notion that the absorptionof nutrients is restricted to the posteriorpart of the worm, and it suggests there may beregional differences in tegumental function (Hayunga,1979a). The idea of localized tegumentalactivity in flatworms was given further supportby experimental work on Schistosoma mansonireproductive behavior (Popiel and Basch, 1984).Light microscopic examination of the lesionassociated with H. nodulosa infection shows anarea of chronic inflammation and extensive infiltrationof lymphocytes. A prominent eosinophilicmatrix is found between the parasite andhost tissue. Tegumental microtriches are so firmlyattached to this matrix that often portions ofthe tegument are left behind when worms areforcibly removed from the nodule (Hayunga,1977, 1979b). Electron microscopic examination
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Morphological Adaptations of Intestinal Helminths

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