Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-26T16:31:34.295Z Has data issue: false hasContentIssue false
  • English
  • Français

The effect of Trichinella spiralis infection on the mechanical properties of the mammalian diaphragm

Published online by Cambridge University Press:  06 April 2009

C. L. Harwood ,
I. S. Young ,
D. L. Lee  and
J. D. Altringham
C. L. Harwood*
Affiliation:
Department of Biology, The University of Leeds, Leeds LS2 9JT
I. S. Young
Affiliation:
Department of Biology, The University of Leeds, Leeds LS2 9JT
D. L. Lee
Affiliation:
Department of Biology, The University of Leeds, Leeds LS2 9JT
J. D. Altringham
Affiliation:
Department of Biology, The University of Leeds, Leeds LS2 9JT
*
* Corresponding author. Tel: + 44 113 2332851. Fax: + 44 113 2332835. E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Summary

Trichinella spiralis larvae infect and develop within skeletal muscle cells causing major changes to their mechanical properties. The aim of this investigation was to determine the effects of T. spiralis on the power output and fatigue resistance of the mammalian diaphragm under conditions simulating in vivo operation and to relate these to respiratory performance. Infection with T. spiralis leads to major reductions in mechanical stress, work, power output and fatigue resistance. These changes are associated with the number of larvae present in the muscle and the duration of infection. However, the initial decline in mechanical performance occurs during the onset of infection when there are few larvae observed within the muscle cells, indicating that T. spiralis may affect the properties of muscle before encapsulation. This may correspond to the host's inflammatory response and the effects of larval excretory/secretory products. The decline in mechanical performance will have a profound effect on respiration both at rest and during exertion. This must influence the behaviour of the host and increase its chance of capture by predators, which is likely to benefit the parasite by facilitating its transmission.

Keywords

trichinosisTrichinella spiralisforceworkpowerdiaphragm
Type
Research Article
Information
Parasitology , Volume 113 , Issue 6 , December 1996 , pp. 535 - 543
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alkarmi, T., Dar, F. K., Ijaz, M. K. & Fahim, M. (1994). Contractile characteristics of the flexor muscle of mice infected with Trichinella spiralis, T. nativa or T. pseudospiralis. Journal of Parasitology 80, 358–362.CrossRefGoogle ScholarPubMed
Altringham, J. D. & Young, I. S. (1991). Power Output and the frequency of oscillatory work in mammalian diaphragm muscle: the effects of animal size. Journal of Experimental Biology 157, 381–389.Google Scholar
Bagheri, A., Ubelaker, J. E., Stewart, G. L. & Wood, B. (1986). Muscle fibre selectivity of Trichinella spiralis and Trichinella pseudospiralis. Journal of Parasitology 72, 277–282.CrossRefGoogle ScholarPubMed
Bruce, R. G. (1970). The structure and composition of the capsule of Trichinella spiralis in host muscle. Parasitology 60, 223–227.CrossRefGoogle ScholarPubMed
Campbell, W. C. (1983). Epidemiology I: Modes of transmission. In Trichinella and Trichinosis (ed. Campbell, W. C.), pp. 425–444. Plenum Press, New York.CrossRefGoogle Scholar
Casey, M. A. & Harley, J. P. (1978). Trichinella spiralis: Skeletal muscle membrane potentials in infected and uninfected mice. Experimental Parasitology 44, 66–71.CrossRefGoogle ScholarPubMed
Daut, J. & Elzinga, G. (1989). Substrate dependence of energy metabolism in isolated guinea-pig cardiac muscle: a microcalorimetric study. Journal of Physiology 413, 379–397.CrossRefGoogle ScholarPubMed
Davies, A. S. & Gunn, H. M. (1972). Histochemical fibre types in the mammalian diaphragm. Journal of Anatomy 112, 41–60.Google ScholarPubMed
Despommier, D. D. (1975). Adaptive changes in muscle fibers infected with Trichinella spiralis. American Journal of Pathology 78, 477–496.Google ScholarPubMed
Despommier, D. D., Aron, L. & Turgeon, L. (1975). Trichinella spiralis: growth of the intracellular (muscle) larva. Experimental Parasitology 37, 108–116.CrossRefGoogle ScholarPubMed
Despommier, D. D., Gold, A. M., Buck, S. W., Capo, V. & Silberstein, D. (1990). Trichinella spiralis: secreted antigen of the infective L1 larva localizes to the cytoplasm and nucleoplasm of infected host cells. Experimental Parasitology 71, 27–38.CrossRefGoogle Scholar
Despommier, D. D., Symmans, W. F. & Dell, R. (1991). Changes in nurse cell nuclei during synchronous infections with Trichinella spiralis. Journal of Parasitology 77, 290–295.CrossRefGoogle ScholarPubMed
Farris, K. N. & Harley, J. P. (1977). Trichinella spiralis: Alteration of gastrocnemius muscle kinetics in the mouse. Experimental Parasitology 41, 17–30.CrossRefGoogle ScholarPubMed
Gauthier, G. F. & Lowey, S. (1977). Polymorphism of myosin among skeletal muscle fibre types. Journal of Cell Biology 74, 760–779.CrossRefGoogle Scholar
Gauthier, G. F. & Padykula, H. A. (1966). Cytological studies of fiber types in skeletal muscle: a comparative study of the mammalian diaphragm. Journal of Cell Biology 28, 333–354.CrossRefGoogle ScholarPubMed
Hulinska, D., Grimm, M. & MacKinnon, B. M. (1985). Alterations of muscle fibres of mice experimentally infected with Trichinella pseudospiralis, T. spiralis and T. nativa. In Trichinellosis (ed. Kim, C. W.) pp. 152–162. The State University of New York Press, Albany, New York.Google Scholar
Jasmer, D. P. (1990). Trichinella spiralis: altered expression of muscle proteins in trichinosis. Experimental Parasitology 70, 452–465.CrossRefGoogle ScholarPubMed
Jasmer, D. P. (1993). Trichinella spiralis infected skeletal muscles arrest in G2/M and cease muscle gene expression. Journal of Cell Biology 121, 785–793.CrossRefGoogle ScholarPubMed
Jasmer, D. P., Bohnet, S. & Prieur, D. J. (1991). Trichinella spp.: differential expression of acid phosphatase and myofibrillar proteins in infected muscle cells. Experimental Parasitology 72, 321–331.Google Scholar
Josephson, R. K. (1985). Mechanical power output from striated muscle during cyclic contraction. Journal of Experimental Biology 114, 493–512.CrossRefGoogle Scholar
Josephson, R. K. (1993). Contraction dynamics and power output of skeletal muscle. Annual Review of Physiology 55, 527–546.CrossRefGoogle ScholarPubMed
Ko, R. C., Fan, L. & Lee, D. L. (1992). Experimental reorganisation of host muscle cells by excretory/secretory products of infective Trichinella spiralis larvae. Transactions of the Royal Society of Tropical Medicine and Hygiene 86, 77–78.CrossRefGoogle Scholar
Ko, R. C., Fan, L., Lee, D. L. & Compton, H. (1994). Changes in host muscles induced by excretory/secretory products of larval Trichinella spiralis and Trichinella pseudospiralis. Parasitology 108, 195–205.CrossRefGoogle ScholarPubMed
Lee, D. L., Ko, R. C., Yi, X. Y. & Yeung, M. H. F. (1991). Trichinella spiralis: antigenic epitopes from the stichocytes detected in the hypertrophic nuclei and cytoplasm of the parasitised muscle fibre (nurse cell) of the host. Parasitology 102, 117–123.CrossRefGoogle Scholar
Lee, D. L. & Shivers, R. R. (1987). A freeze-fracture study of muscle fibres infected with Trichinella spiralis. Tissue and Cell 19, 665–671.CrossRefGoogle ScholarPubMed
Metzger, J. M., Scheidt, K. B. & Fitts, R. H. (1985). Histochemical and physiological characteristics of the rat diaphragm. Journal of Applied Physiology 59, 1085–1091.Google Scholar
Ochoa, J. & Pallis, C. (1980). Trichinella thrives in both oxidative and glycolytic human muscle fibres. Journal of Neurology, Neurosurgery and Psychiatry 43, 281–282.Google Scholar
Peter, J. B., Barnard, R. J., Edgerton, V. R., Gillespie, C. A. & Stempel, K. E. (1972). Metabolic profiles of three fiber types of skeletal muscle in guinea pigs and rabbits. Biochemistry 11, 2627–2633.CrossRefGoogle Scholar
Pette, D. & Staron, R. S. (1990). Cellular and molecular diversities of mammalian skeletal muscle fibers. Reviews of Physiology, Biochemistry and Pharmacology 116, 1–76.Google Scholar
Philipp, M., Parkhouse, R. M. E. & Ogilvie, B. M. (1981). Molecular basis for stage specificity of primary antibody responses to the surface of Trichinella spiralis. In Trichinellosis. Proceedings of the 5th International Conference on Trichinellosis (ed. Kim, C. W., Ruitenberg, E. J. & Teppema, J. S.), pp. 59–64. Reedbooks, Chertsey, Surrey.Google Scholar
Purkerson, M. & Despommier, D. D. (1974). Fine structure of the muscle phase of Trichinella spiralis in the mouse. In Trichinellosis (ed. Kim, C. W.), pp. 7–23. Intext Educational Publishers, New York.Google Scholar
Rau, M. E. (1983). The open-field behaviour of mice infected with Trichinella spiralis. Parasitology 86, 311–318.CrossRefGoogle ScholarPubMed
Rau, M. E. & Putter, L. (1984). Running responses of Trichinella spiralis-infected CD-1 mice. Parasitology 89, 579–583.CrossRefGoogle ScholarPubMed
Reddington, J. J., Stewart, G. L., Kramar, G. W. & Kramar, M. A. (1981). The effects of host sex and hormones on Trichinella spiralis in the mouse. Journal of Parasitology 67, 548–555.Google Scholar
Ribas-Mujal, D. & Rivera-Pomar, J. M. (1968). Biological significance of the early structural alterations in skeletal muscle fibers infected by Trichinella spiralis. Virchows Archiv-A: Pathology-Pathologische Anatomie 345, 154–168.CrossRefGoogle ScholarPubMed
Stevens, E. D. & Godt, R. E. (1990). The effects of temperature and concomitant changes in pH on muscle. American Journal of Physiology 259, R204–R209.Google ScholarPubMed
Stevens, E. D. & Syme, D. A. (1993). Effect of stimulus duty cycle and cycle frequency on power output during fatigue in rat diaphragm muscle doing oscillatory work. Canadian Journal of Physiology and Pharmacology 71, 910–916.CrossRefGoogle ScholarPubMed
Stewart, G. L. (1983). Pathophysiology of the muscle phase. In Trichinella and Trichinosis (ed. Campbell, W. C.), pp. 241–264. Plenum Press, New York.CrossRefGoogle Scholar
Stewart, G. L. (1989). Biological and immunological characteristics of Trichinella pseudospiralis. Parasitology Today 5, 344–349.Google Scholar
Stewart, G. L. & Charniga, L. M. (1980). Distribution of Trichinella spiralis in the muscles of the mouse. Journal of Parasitology 66, 688–689.CrossRefGoogle ScholarPubMed
Stewart, G. L., Charniga, L. & Boley, R. B. (1982). Myositis in mouse Trichinellosis. Journal of Parasitology 68, 730–732.CrossRefGoogle ScholarPubMed
Stewart, G. L. & Giannini, S. H. (1982). Sarcocystis, Trypanosoma, Toxoplasma, Brugia, Ancylostoma, and Trichinella spp.: a review of the intracellular parasites of striated muscle. Experimental Parasitology 53, 406–447.Google Scholar
Stewart, G. L. & Read, C. P. (1974). Studies on biochemical pathology in trichinosis. I. Changes in myoglobin, free creatine, phosphocreatine, and two protein fractions of mouse diaphragm muscle. Journal of Parasitology 60, 996–1000.CrossRefGoogle ScholarPubMed
Syme, D. A. & Stevens, E. D. (1989). Effect of cycle frequency and excursion amplitude on work done by rat diaphragm muscle. Canadian Journal of Physiology and Pharmacology 67, 1294–1299.CrossRefGoogle ScholarPubMed
Wakelin, D. & Denham, D. A. (1983). The immune response. In Trichinella and Trichinosis (ed. Campbell, W. C.), pp. 265–303. Plenum Press, New York.CrossRefGoogle Scholar
Wakelin, D., Goyal, P. K., Dehlawi, M. S. & HermaneK, J. (1994). Immune responses to Trichinella spiralis and Trichinella pseudospiralis in mice. Immunology 81, 475–479.,Google ScholarPubMed
Wakelin, D. & Grencis, R. K. (1992). T-cell and genetic control of inflammatory cells. In Allergy and Immunity to Helminths: Common Mechanisms or Divergent Pathways, pp. 107–136. Taylor and Francis, London.Google Scholar
Wank, V., Bauer, R., Punkt, K. & Ziegan, J. (1994). Enzyme activity patterns of myosinATPase, alpha-glycerophosphate dehydrogenase and succinate-dehydrogenase within different muscle fibre types. Acta Histochemica 96, 213–218.Google Scholar
Winter, M. D., Ball, M. L., Altringham, J. D. & Lee, D. L. (1994). The effects of Trichinella spiralis and Trichinella pseudospiralis on the mechanical properties of mammalian diaphragm muscle. Parasitology 109, 129–134.Google Scholar
Worthington, J., Young, I. S. & Altringham, J. D. (1991). The relationship between body mass and ventilation rate in mammals. Journal of Experimental Biology 161, 533–536.Google Scholar
Zohar, A. S. & Rau, M. E. (1984). The effect of the intestinal phase of Trichinella spiralis on the open-field behaviour of mice. Journal of Parasitology 70, 927–930.CrossRefGoogle ScholarPubMed
Zohar, A. S. & Rau, M. E. (1986). The role of muscle larvae of Trichinella spiralis in the behavioural alterations of the mouse. Journal of Parasitology 72, 464–466.CrossRefGoogle ScholarPubMed