Journal of Assisted Reproduction and Genetics

, Volume 28, Issue 3, pp 191–197 | Cite as

Considerations of viscosity in the preliminaries to mammalian fertilisation

Gamete Biology

Abstract

Migration of spermatozoa in the female genital tract will be strongly influenced by the viscosity of the fluids encountered, yet little systematic analysis has been given to such a consideration. This essay reviews the series of milieux confronting a fertilising sperm during its progression to the oviduct ampulla. Two groups are discussed, first those in which ejaculation is into the vagina, second those in which semen enters the uterus during a protracted mating. Viscous glycoprotein secretions that accumulate in the oviduct isthmus of both groups before ovulation are highlighted, as is the environment generated in the ampulla by the post-ovulatory suspension of oocyte(s), cumulus cells and spermatozoa; follicular and peritoneal fluids may also be present. The viscosity of all female tract fluids responds to cyclical variations in temperature, and these exist within the oviduct near the time of ovulation. Gradations in viscosity influence the pattern and strength of sperm flagellar activity and the rate of forward movement. Measurements of sperm motility are currently made in a physiological medium of constant viscosity and temperature, thereby overlooking changes in the female genital tract. A more sophisticated approach might reveal an adequate fertilising potential in a proportion of putatively poor semen samples.

Keywords

Semen Sperm motility Cervix Uterus Oviduct Ovarian steroid hormones Temperature gradients 

Notes

Acknowledgements

This essay was written during tenure of a Gerhard Mercator Professorship in Veterinary Physiology awarded by the Deutsche Forschungsgemeinschaft (German Research Council), for which grateful acknowledgement is made. We are also grateful to Mrs Frances Anderson who prepared the typescript in the Highlands of Scotland.

References

  1. 1.
    Verstegen J, Iguer-Ouada M, Onclin K. Computer assisted semen analyzers in andrology research and veterinary practice. Theriogenology. 2002;57:146–79.CrossRefGoogle Scholar
  2. 2.
    Holt WV, O’Brien J, Abaigar T. Applications and interpretation of computer-assisted sperm analyses and sperm sorting methods in assisted breeding and comparative research. Reprod Fertil Dev. 2007;19:709–18.PubMedCrossRefGoogle Scholar
  3. 3.
    Kathiravan P, Kalatharan J, Karthikeya G, Rengarajan K, Kadirvel G. Objective sperm motion analysis to assess dairy bull fertility using computer-aided system—a review. Reprod Domest Anim 2010;Apr 7. (Epub ahead of print).Google Scholar
  4. 4.
    Parkes AS. Marshall’s physiology of reproduction. 3rd ed. London: Longmans, Green & Co; 1965.Google Scholar
  5. 5.
    Greep RO, Astwood B. Handbook of physiology, Section 7, Endocrinology II. Female reproductive system, Part 2. Washington, DC: American Physiological Society; 1973.Google Scholar
  6. 6.
    Knobil E, Neill J. The physiology of reproduction. 2nd ed. New York: Raven Press; 1994.Google Scholar
  7. 7.
    Knobil E, Neill J. Encyclopaedia of reproduction. San Diego: Academic; 1998.Google Scholar
  8. 8.
    Rikmenspoel R. Movements and active moments of bull sperm flagella as a function of temperature and viscosity. J Exp Biol. 1984;108:205–30.PubMedGoogle Scholar
  9. 9.
    Hirai M, Cerbito WA, Wijayagunawardane MP, Braun J, Leidl W, Ohosaki K, et al. The effect of viscosity of semen diluents on motility of bull spermatozoa. Theriogenology. 1997;47:1463–78.PubMedCrossRefGoogle Scholar
  10. 10.
    Rizvi AA, Quraishi MI, Sarkar V, DuBois C, Biro S, Mulhall J. The effect of pH and viscosity on bovine spermatozoa motility under controlled conditions. Int Urol Nephrol. 2009;41:523–30.PubMedCrossRefGoogle Scholar
  11. 11.
    Hunter RHF. Temperature gradients in female reproductive tissues and their potential significance. Anim Reprod. 2009;6:7–15.Google Scholar
  12. 12.
    Mann T, Lutwak-Mann C. Male reproductive function and semen. Berlin: Springer-Verlag; 1981.Google Scholar
  13. 13.
    Blandau RJ. Gamete transport—comparative aspects. In: Hafez ESE, Blandau RJ, editors. The mammalian oviduct. Chicago: University of Chicago Press; 1969. p. 129–62.Google Scholar
  14. 14.
    Hafez ESE, Hafez B. Reproduction in farm animals. 7th ed. Baltimore: Lippincott, Williams & Wilkins; 2000.Google Scholar
  15. 15.
    Moghissi KS. Cervical mucus. In: American handbook of physiology, Section 7, Endocrinology II. Female reproductive system. Washington, DC: American Physiological Society, 1973; Part 2:29.Google Scholar
  16. 16.
    Hunter RHF, Barwise L, King R. Sperm transport, storage and release in the sheep oviduct in relation to the time of ovulation. Br Vet J. 1982;138:225–32.PubMedGoogle Scholar
  17. 17.
    Hunter RHF. The Fallopian tubes: their role in fertility and infertility. Berlin: Springer-Verlag; 1988.Google Scholar
  18. 18.
    Bedford JM. The saga of mammalian sperm from ejaculation to syngamy. In: Gibian H, Plotz EJ, editors. Proc. 21st Mosbach Symposium. Berlin: Springer Verlag; 1970. p. 124–82.Google Scholar
  19. 19.
    Mullins KJ, Saacke RG. Study of the functional anatomy of bovine cervical mucosa with special reference to mucus secretion and sperm transport. Anat Rec. 1989;225:106–17.PubMedCrossRefGoogle Scholar
  20. 20.
    Hunter RHF. Physiology and technology of reproduction in female domestic animals. New York: Academic; 1980.Google Scholar
  21. 21.
    Harper MJK. Gamete and zygote transport. In: Knobil E, Neill JD, editors. The physiology of reproduction. 2nd ed. New York: Raven; 1994.Google Scholar
  22. 22.
    Hunter RHF. Interrelationships between spermatozoa, the female reproductive tract, and the egg investments. In: Proceedings University of Nottingham, 34th Easter School. London: Butterworths; 1982. p. 49–63.Google Scholar
  23. 23.
    Claus R. Oestrogens of the boar: effects on male and female reproductive functions. In: Holstein AF, Voigt KD, Grässlin D, editors. Reproductive biology and medicine. Berlin: Diesbach Verlag; 1989. p. 136–47.Google Scholar
  24. 24.
    Wu ASH, Carlson SD, First NL. Scanning electron microscopic study of the porcine oviduct and uterus. J Anim Sci. 1976;42:804–9.PubMedGoogle Scholar
  25. 25.
    Fléchon JE, Hunter RHF. Distribution of spermatozoa in the utero-tubal junction and isthmus of pigs, and their relationship with the luminal epithelium after mating. Tissue Cell. 1981;13:127–39.PubMedCrossRefGoogle Scholar
  26. 26.
    Hunter RHF, Fléchon B, Fléchon JE. Pre- and peri-ovulatory distribution of viable spermatozoa in the pig oviduct: scanning electron microscope study. Tissue Cell. 1987;19:423–36.PubMedCrossRefGoogle Scholar
  27. 27.
    Rodriguez-Martinez H, Saravia F, Wallgren M, Martinez E, Sanz L, Roca J, et al. Spermadhesin PSP-1/PSP-II heterodimer induces migration of polymorphonuclear neutrophils into the uterine cavity of the sow. J Reprod Immunol. 2010;84:57–65.PubMedCrossRefGoogle Scholar
  28. 28.
    McKenzie FF, Miller JC, Bauguess LC. The reproductive organs and semen of the boar. Res Bull Missouri Exp Statn. 1938;279.Google Scholar
  29. 29.
    Burger JF. Sex physiology of pigs. Onderstepoort J Vet Res Suppl 1952; No 2.Google Scholar
  30. 30.
    Du Mesnil du Buisson F, Dauzier L. Distribution et résorption du sperme dans le tractus genital de la truie: survie des spermatozoides. Ann Endocrinol. 1955;16:413–22.Google Scholar
  31. 31.
    Andersen DH. Lymphatics of the Fallopian tube of the sow. Contrib Embryol Carneg Inst (Wash). 1927;19:135–48.Google Scholar
  32. 32.
    Andersen DH. Comparative anatomy of the tubo-uterine junction. Histology and physiology in the sow. Am J Anat. 1928;42:255–305.CrossRefGoogle Scholar
  33. 33.
    Hunter RHF. Histophysiology of the Fallopian tubes in relation to sperm binding, release and completion of capacitation. Ital J Anat Embryol. 2001;106 Suppl 2:279–89.PubMedGoogle Scholar
  34. 34.
    Hunter RHF. Vital aspects of Fallopian tube physiology in pigs. Reprod Domest Anim. 2002;37:186–90.PubMedCrossRefGoogle Scholar
  35. 35.
    Hunter RHF. Ovarian endocrine control of sperm progression in the Fallopian tubes. Oxf Rev Reprod Biol. 1995;17:85–125.Google Scholar
  36. 36.
    Suarez SS. Gamete and zygote transport. In: Neill JD, editor. The physiology of reproduction. 3rd ed. Amsterdam: Elsevier; 2006.Google Scholar
  37. 37.
    Jansen RPS. Cyclic changes in the human Fallopian tube isthmus and their functional importance. Am J Obstet Gynecol. 1980;136:292–308.PubMedGoogle Scholar
  38. 38.
    Hunter RHF, Nichol R. Transport of spermatozoa in the sheep oviduct: pre-ovulatory sequestering of cells in the caudal isthmus. J Exp Zool. 1983;228:121–8.PubMedCrossRefGoogle Scholar
  39. 39.
    Motta PM, Nottola SA, Familiari G. Cumulus corona cells at fertilisation and segmentation. A paracrine organ. In: Motta PM, editor. Microscopy of reproduction and development: a dynamic approach. Rome: Antonio Delfino Editor; 1997. p. 177–86.Google Scholar
  40. 40.
    Hunter RHF. Physiology of the Graafian follicle and ovulation. Cambridge: Cambridge University Press; 2003.Google Scholar
  41. 41.
    Hunter RHF, Einer-Jensen N. Potential amplification of early pregnancy signals by ovarian follicular cells in suspension within the Fallopian tube. Zygote. 2003;11:237–43.PubMedCrossRefGoogle Scholar
  42. 42.
    Hunter RHF, Einer-Jensen N, Greve T. Somatic cell amplification of early pregnancy factors in the Fallopian tube. Ital J Anat Embryol. 2005;110:195–203.PubMedGoogle Scholar
  43. 43.
    Georgiou AS, Snijders AP, Sostaric E, Aflatoonian R, Vazquez JL, Vazquez JM, et al. Modulation of the oviductal environment by gametes. J Proteome Res. 2007;6:4656–66.PubMedCrossRefGoogle Scholar
  44. 44.
    Liu YX. Plasminogen activator/plasminogen activator inhibitors in ovarian physiology. Front Biosci: A Journal and Virtual Library. 2004;9:3356–73.CrossRefGoogle Scholar
  45. 45.
    Yaniz JL, Lopez-Gatius F, Santolaria P, Mullins KJ. Study of the functional anatomy of bovine oviductal mucosa. Anat Rec. 2000;260:268–78.PubMedCrossRefGoogle Scholar
  46. 46.
    Papi M, Brunelli R, Sylla L, Parasassi T, Monaci M, Maulucci G, et al. Mechanical properties of zona pellucida hardening. Eur Biophys J. 2010;39:987–92.PubMedCrossRefGoogle Scholar
  47. 47.
    Coy P, Cánovas S, Mondéjar I, Saavedra M, Romar R, Grullón L, et al. Oviduct-specific glycoprotein and heparin modulate sperm-zona pellucida interaction during fertilization and contribute to the control of polyspermy. Proc Natl Acad Sci USA. 2008;105:15809–14.PubMedCrossRefGoogle Scholar
  48. 48.
    David A, Vilensky A, Nathan H. Temperature changes in the different parts of the rabbit’s oviduct. Int J Gynecol Obstet. 1972;10:52–6.Google Scholar
  49. 49.
    Hunter RHF, Nichol R. A preovulatory temperature gradient between the isthmus and ampulla of pig oviducts during the phase of sperm storage. J Reprod Fertil. 1986;77:599–606.PubMedCrossRefGoogle Scholar
  50. 50.
    Bahat A, Eisenbach M. Sperm thermotaxis. Mol Cell Endocrinol. 2006;252:115–9.PubMedCrossRefGoogle Scholar
  51. 51.
    Tjioe DY, Oentoeng S. The viscosity of human semen and the percentage of motile spermatozoa. Fertil Steril. 1968;19:562–5.PubMedGoogle Scholar
  52. 52.
    Esfandiari N, Burjaq H, Gotlieb L, Casper RF. Seminal hyperviscosity is associated with poor outcome of in vitro fertilization and embryo transfer: a prospective study. Fertil Steril. 2008;90:1739–43.PubMedCrossRefGoogle Scholar
  53. 53.
    Elzanaty S, Malm J, Giwercman A. Visco-elasticity of seminal fluid in relation to the epididymal and accessory sex gland function and its impact on sperm motility. Int J Androl. 2004;27:94–100.PubMedCrossRefGoogle Scholar
  54. 54.
    Elia J, Delfino M, Imbrogno N, Capogreco F, Lucarelli M, Rossi T, et al. Human semen hyperviscosity: prevalence, pathogenesis and therapeutic aspects. Asian J Androl. 2009;11:609–15.PubMedCrossRefGoogle Scholar
  55. 55.
    Smith DJ, Gaffney EA, Gadêlha H, Kapur N, Kirkman-Brown JC. Bend propagation in the flagella of migrating human sperm, and its modulation by viscosity. Cell Motil Cytoskeleton. 2009;66:220–36.PubMedCrossRefGoogle Scholar
  56. 56.
    Giuliano S, Carretero M, Gambarotta M, Neild D, Trasorras V, Pinto M, et al. Improvement of llama (Lama glama) seminal characteristics using collagenase. Anim Reprod Sci. 2010;118:98–102.PubMedCrossRefGoogle Scholar
  57. 57.
    Micó V, Zalevsky Z, Ferreira C, Garcia J. Superresolution digital holographic microscopy for three-dimensional samples. Opt Express. 2008;16:19260–70.PubMedCrossRefGoogle Scholar
  58. 58.
    Foo JYA. Modelling of energy expended by free swimming spermatozoa in temperature-dependent viscous semen. J Med Eng Technol. 2010;34:78–84.PubMedCrossRefGoogle Scholar
  59. 59.
    Coy P, Gadea J, Rath D, Hunter RHF. Differing sperm ability to penetrate the oocyte in vivo and in vitro as revealed using colloidal preparations. Theriogenology. 2009;72:1171–9.PubMedCrossRefGoogle Scholar
  60. 60.
    Suarez SS, Dai X. Hyperactivation enhances mouse sperm capacity for penetrating viscoelastic media. Biol Reprod. 1992;46:686–91.PubMedCrossRefGoogle Scholar
  61. 61.
    Hunter RHF, Greve T. Are lower fertility bulls necessarily less fertile? Proposals concerning insemination procedures. Anim Reprod Sci. 1997;48:113–21.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Ronald H. F. Hunter
    • 1
    • 4
  • P. Coy
    • 2
  • J. Gadea
    • 2
  • D. Rath
    • 3
  1. 1.Institute of Reproductive MedicineHannover Veterinary UniversityHannoverGermany
  2. 2.Department of Physiology, Faculty of Veterinary MedicineUniversity of MurciaMurciaSpain
  3. 3.Institute for Animal BreedingMarienseeGermany
  4. 4.LadfieldJedburghScotland

Personalised recommendations