Attrition of Adult Schistosoma Mansoniin A/J Mice

Table 2. Monthly percent prevalence of gastrointes- Literature Cited tinal nematodes in Cnemidophorus burti stictogrammus, April-September 1966. Babero, B. B., and D. Matthias. 1967. Thubunaea cnemidophorus n. sp., and other helminths from lizards, Cnemidophorus tigris, in Nevada and Ar- Adult izona. Transactions of the American Microscop- Male Female Juvenile ical Society 86:173-177. Benes, E. S. 1985. Helminth parasitism in some cen- Month TV infected N infected N infected tral Arizona lizards. Southwestern Naturalist 30: 467-473. April 0 0 1 0 Eckblad, J. 1984. Key-Stat: An Integrated Series of May 3 0 2 0 0 — Statistical Programs. Oakleaf Systems, Decorah, Iowa. 10 pp. June 12 16.7 5 20.0 0 — July .,8 37.5 5 0 1 0 Goldberg, S. R. 1987a. Larval cestodes (Mesoces- August 10 10.0 4 25.0 0 — toides sp.) in the giant spotted whiptail, Cnemi- September 2 100.0 4 75.0 0 - dophorus burti stictogrammus. Journal of Herpe- tology 21:337. . 1987b. Reproductive cycle of the giant spotted whiptail, Cnemidophorus burti stictogrammus, in Arizona. Southwestern Naturalist 32:510-511. Babero and Matthias (1967) described Thu- Lyon, R. E. 1986. Helminth parasites of six lizard bunaea cnemidophorus in Cnemidophorus tigris species from southern Idaho. Proceedings of the from Clark County, Nevada. They also reported Helminthological Society of Washington 53:291- what they tentatively identified as P. retusa and 293. McAllister, C. T., S. E. Trauth, and J. E. Ubelaker. the cestode Oochoristica bivitellobata from C. ti- 1986. Nematode parasites of the parthenogenetic gris. Pharyngodon cnemidophori was described whiptail lizard, Cnemidophorus laredoensis (Sau- by Read and Amrein (1953) from Cnemidoph- ria: Teiidae) from South Texas. Proceedings of the orus tesselatus tesselatus. Helminthological Society of Washington 53:138- 139. In conclusion, we have presented new host rec- Read, C. P., and Y. U. Amrein. 1953. North Amer- ords and infection prevalences for 5 endopar- ican nematodes of the genus Pharyngodon Diesing asites infecting C. b. stictogrammus in southern (Oxyuridae). Journal of Parasitology 39:365-370. Arizona. Stebbins, R. C. 1985. A Field Guide to Western Rep- We thank Linda Bone and Adrian Sales for tiles and Amphibians. Houghton-Mifflin Com- pany, Boston. 336 pp. assistance in collection of parasites.

Proc. Helminthol. Soc. Wash. 56(1), 1989, pp. 87-90

Research Note

Attrition of Adult Schistosoma mansoni in A/J Mice

MARK D. MALONEY, GERALD C. COLES, AND LLOYD H. SEMPREVIVO Department of Zoology, University of Massachusetts, Amherst, Massachusetts 01003

ABSTRACT: Inbred mice (A/J) were infected by tail Viable eggs were observed within the tissues of one- immersion with Schistosoma mansoni cercariae and half of the dead female worms. the adults isolated from the hepatic portal and mes- KEY WORDS: Schistosoma mansoni, adult worms, enteric veins at 6, 7, 8, and 10 wk postinfection. Dead attrition, A/J mouse, permissive host. adult worms were not observed at 6 and 7 wk postinfection. At 8 and 10 wk, dead worms, predominantly females, were observed among the worm populations. The dead females were irregular in shape, very rigid, In recent years, much attention has been fo- and much smaller than the normal adult females. They cused upon the elimination of larval schisto- lacked pigment and were frequently situated within the somes from permissive vertebrate hosts. In con- gynecophoral canals of apparently healthy male worms. trast, relatively little information is available on

Copyright © 2011, The Helminthological Society of Washington OF WASHINGTON, VOLUME 56, NUMBER 1, JANUARY 1989 89 the elimination of adult schistosomes from these pink—possibly due to undigested hemoglobin, hosts. This reflects the widely held belief that, and they were much smaller than living females while larval stages are vulnerable to immune ef- (Fig. 6), ranging in size from 0.82 to 2.95 mm fectors during infection of permissive hosts, adults while living females were 5.64 to 9.74 mm in are long-lived and remain in the vertebrate host length. Three of the 6 dead females were found for some years. Nevertheless, reports do exist either entirely within, or protruding from, the which describe attrition of adult populations in gynecophoral canal of a living male. Eggs were permissive hosts, thus suggesting that adult found within 3 of the dead females, 1 worm pos- schistosomes also may be vulnerable to acquired sessing 2 eggs (Fig. 7). Only their location within host immune responses. These reports have re- the gynecophoral canals of living males and the lied on the numerical decrease in adult worm presence of laterally-spined eggs clearly identi- populations over time or the discovery of dead fied these worms as female S. mansoni. In 2 cases, parasites in the livers of permissive hosts (for miracidia were observed moving within these review see Damian, 1984). Death of adult worms eggs, indicating their viability. The presence of in the final sites of Schistosoma mansoni infec- viable eggs indicates that the reduction in size of tion, has not, however, been documented. The the dead females was due to size regression rather purpose of the work reported here, therefore, was than the stunting of females in immature stages. to document attrition of adult S. mansoni within Size regression is also supported by the fact that the mesenteric and portal veins of the A/J mouse, no dead worms were observed at 6 or 7 wk post- a permissive host for this parasite. infection even though the majority of worms were A Puerto Rican strain of S. mansoni was main- mature at this time. tained in Biomphalaria glabrata snails and lab- The results presented here directly demon- oratory mice by standard methods. A/J mice were strate that adult S. mansoni located within the infected with 75 cercariae per mouse by tail im- mesenteric and hepatic portal veins are suscep- mersion (Bruce and Radke, 1971). Adult worms tible to elimination in a permissive host. Indeed, were recovered by perfusion (Duvall and DeWitt, observation of dead worms in the perfusate may 1967) at 6, 7, 8, and 10 wk postinfection and underestimate the level of this adult attrition. their viability determined by careful microscopic Dead adult worms in the venous circulation are examination. Infections of longer than 10 wk du- difficult to observe because of their low numbers ration were not investigated due to the high mouse and the fact that dead females, due to their small mortality associated with schistosome egg de- size, may be entirely hidden within the gyne- position and its subsequent pathology. cophoral canals of living male worms. It is also Dead adult schistosomes were never observed quite possible that dead worms which are not in infections of less than 8 wk duration even held within living males are swept away with the though 500 mice were perfused and more than blood and quickly cleared from the circulatory 15,000 viable adults were examined in the sixth system. This could explain the observed dispar- and seventh wk of infection. At 8 wk postinfec- ity in the numbers of dead females versus dead tion, 1 dead female was observed among 1,500 males observed. live worms recovered from 47 mice. Examina- The cause of the adult schistosome attrition is tion of worms at 10 wk postinfection revealed 1 unknown, but it is occurring after worms have dead male and 5 dead female worms among the been mature for only a few weeks, long before 1,800 live worms recovered from 58 mice (Figs. senescence would be a factor. The fact that no 1-7). dead worms were observed at 6 and 7 wk post- The dead female schistosomes only vaguely infection, even though most worms were mature resembled living worms. They were irregularly at this time, suggests that mechanisms discrete shaped and very rigid (Figs. 3, 5), they possessed from those acting against larval forms may be little pigment other than infrequent areas of responsible. This delay in the appearance of dead

Figures 1-7. 1. Dead male schistosome with normal adult male, x 12. 2. Dead female within canal of living adult male, x 25. 3. Dead female schistosome, x 40. 4. Close-up of egg within dead female of Figure 3, x 100. 5. Dead female schistosome, x40. 6. Dead female with live adult female, x!2. 7. Close-up of eggs within dead female of Figure 5, x 200.

Copyright © 2011, The Helminthological Society of Washington 90 worms also suggests that acquired responses may Literature Cited be responsible for adult schistosome attrition in Bruce, J. I., and M. G. Radke. 1971. Culturing Biom- the mouse. phalaria and Oncomelania (Gastropoda) for large In nonpermissive hosts for S. mansoni infec- scale studies of schistosomiasis. I. Cultivation of tion such as the rat, adult worms are eliminated Biomphalaria glabrata and maintenance ofSchis- beginning at 4 wk postinfection (Smithers and tosoma mansoni in the laboratory. Biomedical Re- ports of the 406th Medical Laboratory 19:1-84. Terry, 1965). While there is an immune com- Cioli, D., P. M. Knopf, and A. W. Senft. 1977. A ponent to this "self cure" (Phillips et al., 1975), study of Schistosoma mansoni transferred into host hormones are known to participate in the permissive and nonpermissive hosts. Internation- nonpermissive status of rats by preventing nor- al Journal for Parasitology 7:293-298. Damian, R. T. 1984. Immunity in schistosomiasis: mal maturation and development of the worms a holistic view. Pages 359-420 in John J. Mar- (Knopf and Soliman, 1980). These develop- chalonis, ed. Contemporary Topics in Immuno- mentally stunted worms fail to migrate to the biology. Vol. 12. Plenum Publishing Corporation, mesenteric veins and do not produce viable eggs New York. (Cioli et al., 1977). Therefore, the self-cure phe- Duvail, R. H., and W. B. DeWitt. 1967. An improved perfusion technique for recovering adult schisto- nomenon in nonpermissive hosts is fundamen- somes from laboratory animals. American Journal tally different from the adult attrition observed of Tropical Medicine and Hygiene 16:483-486. in the A/J mouse permissive host model where Knopf, P. M., and M. Soliman. 1980. Effects of host worms complete their maturation, producing vi- endocrine gland removal on the permissive status of laboratory rodents to infection by Schistosoma able eggs, before succumbing to as yet undeter- mansoni. International Journal for Parasitology mined mechanisms of elimination. The eluci- 10:197-204. dation of the mechanisms responsible for adult Phillips, S. M., W. A. Reid, J. I. Bruce, K. Hedlund, schistosome attrition in permissive laboratory R. C. Colvin, R. Campbell, C. L. Diggs, and E. H. hosts could be instrumental in the development Sadun. 1975. The cellular and humoral immune response to Schistosoma mansoni infections in of new strategies for the treatment and preven- inbred rats. I. Mechanisms during initial exposure. tion of human schistosomiasis. If acquired im- Cellular Immunology 19:99-116. mune responses are involved, then the devel- Smithers, S. R., and R. J. Terry. 1965. Acquired opment of an adult schistosome vaccine could resistance to experimental infections of Schisto- soma mansoni in the albino rat. Parasitology 55: complement those vaccines directed against lar- 711-717. val stages which are currently under development. This work was supported in part by NIH Training Grant #5 T32 AI07109.