Skip to main content

Advertisement

Log in

Tubal transport of gametes and embryos: a review of physiology and pathophysiology

  • Review Article
  • Published:
Journal of Assisted Reproduction and Genetics Aims and scope Submit manuscript

Abstract

With the advent of assisted reproductive technology in the past three decades, the clinical importance of fallopian tubes has been relatively overlooked. However, successful spontaneous conception requires normal function of the tube to provide not only a conduit for the gametes to convene and embryo to reach the uterine cavity, but also a physiologically optimized environment for fertilization and early embryonic development. In this review, after a brief description of normal human tubal anatomy and histology, we will discuss tubal transport and its principal effectors, including ciliary motion, muscular contractility and tubal fluid. Furthermore, we will discuss the ciliary ultrastructure and regulation of ciliary beat frequency by ovarian steroids, follicular fluid, angiotensin system, autonomic nervous system and other factors such as adrenomedullin and prostaglandins. In the last section, we describe the adverse impact of various pathological conditions, such as endometriosis, infection and smoking on tubal function and ciliary motility.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. El-Mowafi DM, Diamond MP. Fallopian tube. In: Knobil E, Neill JD, editors. Encyclopedia of reproduction. San Diego: Academic; 1998. p. 149–58.

    Google Scholar 

  2. DeLancey JOL. Surgical anatomy of the female pelvis. In: Rock JA, Jones HW, Te Linde RW, editors. Te Linde’s operative gynecology. 10th ed. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2008. p. 82–112.

    Google Scholar 

  3. Lyons RA, Saridogan E, Djahanbakhch O. The reproductive significance of human Fallopian tube cilia. Hum Reprod Update. 2006;12(4):363–72. doi:10.1093/humupd/dml012.

    PubMed  CAS  Google Scholar 

  4. Woodruff JD, Pauerstein CJ. The fallopian tube; structure, function, pathology, and management. Baltimore: Williams & Wilkins; 1969.

    Google Scholar 

  5. Amso NN, Crow J, Lewin J, Shaw RW. A comparative morphological and ultrastructural study of endometrial gland and fallopian tube epithelia at different stages of the menstrual cycle and the menopause. Hum Reprod. 1994;9(12):2234–41.

    PubMed  CAS  Google Scholar 

  6. Crow J, Amso NN, Lewin J, Shaw RW. Morphology and ultrastructure of fallopian tube epithelium at different stages of the menstrual cycle and menopause. Hum Reprod. 1994;9(12):2224–33.

    PubMed  CAS  Google Scholar 

  7. Ferenczy A, Richart RM, Agate Jr FJ, Purkerson ML, Dempsey EW. Scanning electron microscopy of the human fallopian tube. Science. 1972;175(4023):783–4.

    PubMed  CAS  Google Scholar 

  8. Patek E. The epithelium of the human fallopian tube. A surface ultrastructural and cytochemical study. Acta Obstetricia et Gynecologica Scandinavica Suppl. 1974;31:1–28.

    CAS  Google Scholar 

  9. Satir P. Mechanisms of ciliary movement: contributions from electron microscopy. Scanning Microsc. 1992;6(2):573–9.

    PubMed  CAS  Google Scholar 

  10. Jarboe EA. Fallopian tube. In: Mutter GL, Prat J, editors. Pathology of the female reproductive tract. 3rd ed. Edinburgh: Churchill Livingstone; 2014. p. 459–86.

    Google Scholar 

  11. Pauerstein CJ, Woodruff JD. The role of the “indifferent” cell of the tubal epithelium. Am J Obstet Gynecol. 1967;98(1):121–5.

    PubMed  CAS  Google Scholar 

  12. Ovalle WK, Nahirney PC. Female reproductive system. In: Ovalle WK, Nahirney PC, editors. Netter’s essential histology. 2nd ed. Philadelphia: Elsevier Saunders; 2013. p. 403–29.

    Google Scholar 

  13. Cunningham FG, Leveno K, Bloom S, Hauth J, Rouse D, Spong C. Williams obstetrics. 23rd ed. New York: McGraw-Hill Medical; 2010.

    Google Scholar 

  14. Jansen RP. Endocrine response in the fallopian tube. Endocr Rev. 1984;5(4):525–51. doi:10.1210/edrv-5-4-525.

    PubMed  CAS  Google Scholar 

  15. Eddy CA, Pauerstein CJ. Anatomy and physiology of the fallopian tube. Clin Obstet Gynecol. 1980;23(4):1177–93.

    PubMed  CAS  Google Scholar 

  16. Pauerstein CJ, Woodruff JD, Zachary AS. Factors influencing physiologic activities in the fallopian tube; the anatomy, physiology, and pharmacology of tubal transport. Obstet Gynecol Surv. 1968;23(3):215–43.

    PubMed  CAS  Google Scholar 

  17. Djahanbahkch O, Ezzati M, Saridogan E. Physiology and pathophysiology of tubal transport: ciliary beat and muscular contractility, relevance to tubal infertility, recent research, and future directions. In: Ledger WL, Tan SL, Bahathiq A, editors. The fallopian tube in infertility and IVF practice. Cambridge: Cambridge University Press; 2010. p. 18–29.

    Google Scholar 

  18. Satir P. The role of axonemal components in ciliary motility. Comp Biochem Physiol A Comp Physiol. 1989;94(2):351–7.

    PubMed  CAS  Google Scholar 

  19. Satir P. Structural basis of ciliary movement. Environ Health Perspect. 1980;35:77–82.

    PubMed  CAS  PubMed Central  Google Scholar 

  20. Satir P, Matsuoka T. Splitting the ciliary axoneme: implications for a “switch-point” model of dynein arm activity in ciliary motion. Cell Motil Cytoskeleton. 1989;14(3):345–58. doi:10.1002/cm.970140305.

    PubMed  CAS  Google Scholar 

  21. Sale WS, Satir P. Direction of active sliding of microtubules in Tetrahymena cilia. Proc Natl Acad Sci U S A. 1977;74(5):2045–9.

    PubMed  CAS  PubMed Central  Google Scholar 

  22. Verdugo P. Ca2 + −dependent hormonal stimulation of ciliary activity. Nature. 1980;283(5749):764–5.

    PubMed  CAS  Google Scholar 

  23. Hoops HJ, Witman GB. Outer doublet heterogeneity reveals structural polarity related to beat direction in Chlamydomonas flagella. J Cell Biol. 1983;97(3):902–8.

    PubMed  CAS  Google Scholar 

  24. Hagiwara H, Ohwada N, Aoki T, Takata K. Ciliogenesis and ciliary abnormalities. Med Electron Microsc Off J Clin Electron Microsc Soc Jpn. 2000;33(3):109–14. doi:10.1007/s007950000009.

    CAS  Google Scholar 

  25. Hagiwara H, Ohwada N, Aoki T, Suzuki T, Takata K. The primary cilia of secretory cells in the human oviduct mucosa. Med Mol Morphol. 2008;41(4):193–8. doi:10.1007/s00795-008-0421-z.

    PubMed  Google Scholar 

  26. Hoyer-Fender S. Centriole maturation and transformation to basal body. Semin Cell Dev Biol. 2010;21(2):142–7. doi:10.1016/j.semcdb.2009.07.002.

    PubMed  Google Scholar 

  27. Seeley ES, Nachury MV. The perennial organelle: assembly and disassembly of the primary cilium. J Cell Sci. 2010;123(Pt 4):511–8. doi:10.1242/jcs.061093.

    PubMed  CAS  PubMed Central  Google Scholar 

  28. Sanderson MJ. High-speed digital microscopy. Methods (San Diego, Calif). 2000;21(4):325–34. doi:10.1006/meth.2000.1022.

    CAS  Google Scholar 

  29. Nasr G, Schoevaert D, Marano F, Venant A, Legrand JJ. Progress in the measurement of ciliary beat frequency by automated image analysis: application to mammalian tracheal epithelium. Anal Cell Pathol J Eur Soc Anal Cell Pathol. 1995;9(3):165–77.

    CAS  Google Scholar 

  30. Verdugo P, Johnson NT, Tam PY. beta-Adrenergic stimulation of respiratory ciliary activity. J Appl Physiol Respir Environ Exerc Physiol. 1980;48(5):868–71.

    PubMed  CAS  Google Scholar 

  31. Allen-Gipson DS, Romberger DJ, Forget MA, May KL, Sisson JH, Wyatt TA. IL-8 inhibits isoproterenol-stimulated ciliary beat frequency in bovine bronchial epithelial cells. J Aerosol Med Off J Int Soc Aerosols Med. 2004;17(2):107–15. doi:10.1089/0894268041457138.

    CAS  Google Scholar 

  32. Noreikat K, Wolff M, Kummer W, Kolle S. Ciliary activity in the oviduct of cycling, pregnant, and muscarinic receptor knockout mice. Biol Reprod. 2012;86(4):120. doi:10.1095/biolreprod.111.096339.

    PubMed  Google Scholar 

  33. Klein MK, Haberberger RV, Hartmann P, Faulhammer P, Lips KS, Krain B, et al. Muscarinic receptor subtypes in cilia-driven transport and airway epithelial development. Eur Respir J. 2009;33(5):1113–21. doi:10.1183/09031936.00015108.

    PubMed  CAS  PubMed Central  Google Scholar 

  34. Jankovic SM, Protic BA, Jankovic SV. Contractile effect of acetylcholine on isolated isthmic segment of fallopian tubes. Methods Find Exp Clin Pharmacol. 2004;26(2):87–91.

    PubMed  CAS  Google Scholar 

  35. Wolff M, Noreikat K, Ibanez-Tallon I, Lips KS, Kolle S, Kummer W. Cholinergic receptors in the murine oviduct: inventory and coupling to intracellular calcium concentration. Life Sci. 2012;91(21–22):1003–8. doi:10.1016/j.lfs.2012.03.016.

    PubMed  CAS  Google Scholar 

  36. Saridogan E, Djahanbakhch O, Puddefoot JR, Demetroulis C, Collingwood K, Mehta JG, et al. Angiotensin II receptors and angiotensin II stimulation of ciliary activity in human fallopian tube. J Clin Endocrinol Metab. 1996;81(7):2719–25. doi:10.1210/jcem.81.7.8675601.

    PubMed  CAS  Google Scholar 

  37. Leung PS, Sernia C. The renin-angiotensin system and male reproduction: new functions for old hormones. J Mol Endocrinol. 2003;30(3):263–70.

    PubMed  CAS  Google Scholar 

  38. O”Mahony OA, Djahanbahkch O, Mahmood T, Puddefoot JR, Vinson GP. Angiotensin II in human seminal fluid. Hum Reprod. 2000;15(6):1345–9.

    Google Scholar 

  39. Verdugo P, Rumery RE, Tam PY. Hormonal control of oviductal ciliary activity: effect of prostaglandins. Fertil Steril. 1980;33(2):193–6.

    PubMed  CAS  Google Scholar 

  40. Hermoso M, Barrera N, Morales B, Perez S, Villalon M. Platelet activating factor increases ciliary activity in the hamster oviduct through epithelial production of prostaglandin E2. Pflugers Arch - Eur J Physiol. 2001;442(3):336–45.

    CAS  Google Scholar 

  41. Andrade YN, Fernandes J, Vazquez E, Fernandez-Fernandez JM, Arniges M, Sanchez TM, et al. TRPV4 channel is involved in the coupling of fluid viscosity changes to epithelial ciliary activity. J Cell Biol. 2005;168(6):869–74. doi:10.1083/jcb.200409070.

    PubMed  CAS  PubMed Central  Google Scholar 

  42. Lyons RA, Djahanbakhch O, Mahmood T, Saridogan E, Sattar S, Sheaff MT, et al. Fallopian tube ciliary beat frequency in relation to the stage of menstrual cycle and anatomical site. Hum Reprod. 2002;17(3):584–8.

    PubMed  CAS  Google Scholar 

  43. Bendz A, Hansson HA, Svendsen P, Wiqvist N. On the extensive contact between veins and arteries in the human ovarian pedicle. Acta Physiol Scand. 1982;115(2):179–82. doi:10.1111/j.1748-1716.1982.tb07063.x.

    PubMed  CAS  Google Scholar 

  44. Mahmood T, Saridogan E, Smutna S, Habib AM, Djahanbakhch O. The effect of ovarian steroids on epithelial ciliary beat frequency in the human Fallopian tube. Hum Reprod. 1998;13(11):2991–4.

    PubMed  CAS  Google Scholar 

  45. Nishimura A, Sakuma K, Shimamoto C, Ito S, Nakano T, Daikoku E, et al. Ciliary beat frequency controlled by oestradiol and progesterone during ovarian cycle in guinea-pig Fallopian tube. Exp Physiol. 2010;95(7):819–28. doi:10.1113/expphysiol.2010.052555.

    PubMed  CAS  Google Scholar 

  46. Critoph FN, Dennis KJ. Ciliary activity in the human oviduct. Br J Obstet Gynaecol. 1977;84(3):216–8.

    PubMed  CAS  Google Scholar 

  47. Paltieli Y, Eibschitz I, Ziskind G, Ohel G, Silbermann M, Weichselbaum A. High progesterone levels and ciliary dysfunction–a possible cause of ectopic pregnancy. J Assist Reprod Genet. 2000;17(2):103–6.

    PubMed  CAS  PubMed Central  Google Scholar 

  48. Nakahari T, Nishimura A, Shimamoto C, Sakai A, Kuwabara H, Nakano T, et al. The regulation of ciliary beat frequency by ovarian steroids in the guinea pig Fallopian tube: interactions between oestradiol and progesterone. Biomed Res. 2011;32(5):321–8.

    PubMed  CAS  Google Scholar 

  49. Bylander A, Nutu M, Wellander R, Goksor M, Billig H, Larsson DG. Rapid effects of progesterone on ciliary beat frequency in the mouse fallopian tube. Reprod Bioland Endocrinol RB&E. 2010;8:48. doi:10.1186/1477-7827-8-48.

    Google Scholar 

  50. Bylander A, Lind K, Goksor M, Billig H, Larsson DJ. The classical progesterone receptor mediates the rapid reduction of fallopian tube ciliary beat frequency by progesterone. Reprod Bioland Endocrinol RB&E. 2013;11(1):33. doi:10.1186/1477-7827-11-33.

    CAS  Google Scholar 

  51. Nutu M, Weijdegard B, Thomas P, Thurin-Kjellberg A, Billig H, Larsson DG. Distribution and hormonal regulation of membrane progesterone receptors beta and gamma in ciliated epithelial cells of mouse and human fallopian tubes. Reprod Bioland Endocrinol RB&E. 2009;7:89. doi:10.1186/1477-7827-7-89.

    Google Scholar 

  52. Li HW, Liao SB, Chiu PC, Tam WW, Ho JC, Ng EH, et al. Expression of adrenomedullin in human oviduct, its regulation by the hormonal cycle and contact with spermatozoa, and its effect on ciliary beat frequency of the oviductal epithelium. J Clin Endocrinol Metab. 2010;95(9):E18–25. doi:10.1210/jc.2010-0273.

    PubMed  Google Scholar 

  53. Liao SB, Ho JC, Tang F, O WS. Adrenomedullin increases ciliary beat frequency and decreases muscular contraction in the rat oviduct. Reproduction. 2011;141(3):367–72. doi:10.1530/REP-10-0230.

    PubMed  CAS  Google Scholar 

  54. Liao SB, Li HW, Ho JC, Yeung WS, Ng EH, Cheung AN, et al. Possible role of adrenomedullin in the pathogenesis of tubal ectopic pregnancy. J Clin Endocrinol Metab. 2012;97(6):2105–12. doi:10.1210/jc.2011-3290.

    PubMed  CAS  Google Scholar 

  55. Halbert SA, Tam PY, Adams RJ, Blandau RJ. An analysis of the mechanisms of egg transport in the ampulla of the rabbit oviduct. Gynecol Investig. 1976;7(5):306–20.

    CAS  Google Scholar 

  56. Afzelius BA, Camner P, Eliasson R, Mossberg B. Kartagener’s syndrome does exist. Lancet. 1978;2(8096):950.

    PubMed  CAS  Google Scholar 

  57. Pedersen H. Absence of dynein arms in endometrial cilia: cause of infertility? Acta Obstet Gynecol Scand. 1983;62(6):625–7.

    PubMed  CAS  Google Scholar 

  58. McComb P. The determinants of successful surgery for proximal tubal disease. Fertil Steril. 1986;46(6):1002–4.

    PubMed  CAS  Google Scholar 

  59. Halbert SA, Patton DL, Zarutskie PW, Soules MR. Function and structure of cilia in the fallopian tube of an infertile woman with Kartagener’s syndrome. Hum Reprod. 1997;12(1):55–8.

    PubMed  CAS  Google Scholar 

  60. Ezzati M. The role of dynein and its mutations in the ciliary activity of human fallopian tubes. In: Allahbadia G, Saridogan E, Djahanbakhch O, editors. The fallopian tube. Tunbridge Wells: Anshan; 2009. p. 30–4.

    Google Scholar 

  61. Talo A, Brundin J. Muscular activity in the rabbit oviduct: a combination of electric and mechanic recordings. Biol Reprod. 1971;5(1):67–77.

    PubMed  CAS  Google Scholar 

  62. Daniel EE, Lucien P, Posey VA, Paton DM. A functional analysis of the myogenic control systems of the human fallopian tube. Am J Obstet Gynecol. 1975;121(8):1046–53.

    PubMed  CAS  Google Scholar 

  63. Brundin J. Pharmacology of the oviduct. In: Hafez ESE, Blandau RJ editors. The mammalian oviduct: comparative biology and methodology. Chicago: University of Chicago Press; 1969. p. 261–9.

  64. Jansen RP. Fallopian tube isthmic mucus and ovum transport. Science. 1978;201(4353):349–51.

    PubMed  CAS  Google Scholar 

  65. Day BN, Polge C. Effects of progesterone on fertilization and egg transport in the pig. J Reprod Fertil. 1968;17(1):227–30.

    PubMed  CAS  Google Scholar 

  66. Hunter RH. Polyspermic fertilization in pigs after tubal deposition of excessive numbers of spermatozoa. J Exp Zool. 1973;183(1):57–63. doi:10.1002/jez.1401830107.

    PubMed  CAS  Google Scholar 

  67. Hunter RH, Leglise PC. Polyspermic fertilization following tubal surgery in pigs, with particular reference to the role of the isthmus. J Reprod Fertil. 1971;24(2):233–46.

    PubMed  CAS  Google Scholar 

  68. Hodgson BJ, Talo A, Pauerstein CJ. Oviductal ovum surrogate movement: interrelation with muscular activity. Biol Reprod. 1977;16(3):394–6.

    PubMed  CAS  Google Scholar 

  69. Okamura H, Morikawa H, Oshima M, Man-i M, Nishimura T. A morphologic study of mesotubarium ovarica in the human. Obstet Gynecol. 1977;49(2):197–201.

    PubMed  CAS  Google Scholar 

  70. Leese HJ, Tay JI, Reischl J, Downing SJ. Formation of Fallopian tubal fluid: role of a neglected epithelium. Reproduction. 2001;121(3):339–46.

    PubMed  CAS  Google Scholar 

  71. Tay JI, Rutherford AJ, Killick SR, Maguiness SD, Partridge RJ, Leese HJ. Human tubal fluid: production, nutrient composition and response to adrenergic agents. Hum Reprod. 1997;12(11):2451–6.

    PubMed  CAS  Google Scholar 

  72. Gardner DK, Lane M, Calderon I, Leeton J. Environment of the preimplantation human embryo in vivo: metabolite analysis of oviduct and uterine fluids and metabolism of cumulus cells. Fertil Steril. 1996;65(2):349–53.

    PubMed  CAS  Google Scholar 

  73. Sterin-Speziale N, Gimeno MF, Zapata C, Bagnati PE, Gimeno AL. The effect of neurotransmitters, bradikynin, prostaglandins, and follicular fluid on spontaneous contractile characteristics of human fimbriae and tubo-ovarian ligaments isolated during different stages of the sexual cycle. Int J Fertil. 1978;23(1):1–11.

    PubMed  CAS  Google Scholar 

  74. Morikawa H, Okamura H, Takenaka A, Morimoto K, Nishimura T. Physiological study of the human mesotubarium ovarica. Obstet Gynecol. 1980;55(4):493–6.

    PubMed  CAS  Google Scholar 

  75. Maguiness SD, Shrimanker K, Djahanbakhch O, Deeks JJ, Teisner B, Grudzinskas JG. In-vitro synthesis of total protein and placental protein PP14 by the fallopian tube mucosa: variation in relation to anatomical site, the ovarian cycle and the menopause. Hum Reprod. 1993;8(5):678–83.

    PubMed  CAS  Google Scholar 

  76. Maguiness SD, Shrimanker K, Djahanbakhch O, Teisner B, Grudzinskas JG. Evidence for the in-vitro de-novo synthesis of immunoglobulin and a previously undescribed 17 kDa protein (TEP-2) by the mucosa of the fallopian tube. Hum Reprod. 1993;8(8):1199–202.

    PubMed  CAS  Google Scholar 

  77. Abe H, Satoh T, Hoshi H. Primary modulation by oestradiol of the production of an oviduct-specific glycoprotein by the epithelial cells in the oviduct of newborn golden hamsters. J Reprod Fertil. 1998;112(1):157–63.

    PubMed  CAS  Google Scholar 

  78. Bedaiwy MA, Falcone T. Peritoneal fluid environment in endometriosis. Clinicopathological Implications Minerva Ginecol. 2003;55(4):333–45.

    CAS  Google Scholar 

  79. Halme J, Becker S, Hammond MG, Raj MH, Raj S. Increased activation of pelvic macrophages in infertile women with mild endometriosis. Am J Obstet Gynecol. 1983;145(3):333–7.

    PubMed  CAS  Google Scholar 

  80. Halme J, Becker S, Haskill S. Altered maturation and function of peritoneal macrophages: possible role in pathogenesis of endometriosis. Am J Obstet Gynecol. 1987;156(4):783–9.

    PubMed  CAS  Google Scholar 

  81. Zeller JM, Henig I, Radwanska E, Dmowski WP. Enhancement of human monocyte and peritoneal macrophage chemiluminescence activities in women with endometriosis. Am J Reprod Immunol Microbiol AJRIM. 1987;13(3):78–82.

    CAS  Google Scholar 

  82. Lyons RA, Djahanbakhch O, Saridogan E, Naftalin AA, Mahmood T, Weekes A, et al. Peritoneal fluid, endometriosis, and ciliary beat frequency in the human fallopian tube. Lancet. 2002;360(9341):1221–2. doi:10.1016/S0140-6736(02)11247-5.

    PubMed  Google Scholar 

  83. Papathanasiou A, Djahanbakhch O, Saridogan E, Lyons RA. The effect of interleukin-6 on ciliary beat frequency in the human fallopian tube. Fertil Steril. 2008;90(2):391–4. doi:10.1016/j.fertnstert.2007.07.1379.

    PubMed  CAS  Google Scholar 

  84. Reeve L, Lashen H, Pacey AA. Endometriosis affects sperm-endosalpingeal interactions. Hum Reprod. 2005;20(2):448–51. doi:10.1093/humrep/deh606.

    PubMed  CAS  Google Scholar 

  85. Fortier KJ, Haney AF. The pathologic spectrum of uterotubal junction obstruction. Obstet Gynecol. 1985;65(1):93–8.

    PubMed  CAS  Google Scholar 

  86. Almeida Jr OD. Microlaparoscopy and a GnRH agonist: a combined minimally invasive approach for the diagnosis and treatment of occlusive salpingitis isthmica nodosa associated with endometriosis. JSLS J Soc Laparoendosc Surg Soc Laparoendoscopic Surg. 2005;9(4):431–3.

    Google Scholar 

  87. Jenkins CS, Williams SR, Schmidt GE. Salpingitis isthmica nodosa: a review of the literature, discussion of clinical significance, and consideration of patient management. Fertil Steril. 1993;60(4):599–607.

    PubMed  CAS  Google Scholar 

  88. Ding GL, Chen XJ, Luo Q, Dong MY, Wang N, Huang HF. Attenuated oocyte fertilization and embryo development associated with altered growth factor/signal transduction induced by endometriotic peritoneal fluid. Fertil Steril. 2010;93(8):2538–44. doi:10.1016/j.fertnstert.2009.11.011.

    PubMed  Google Scholar 

  89. Gupta S, Goldberg JM, Aziz N, Goldberg E, Krajcir N, Agarwal A. Pathogenic mechanisms in endometriosis-associated infertility. Fertil Steril. 2008;90(2):247–57. doi:10.1016/j.fertnstert.2008.02.093.

    PubMed  CAS  Google Scholar 

  90. Simon C, Gutierrez A, Vidal A, de los Santos MJ, Tarin JJ, Remohi J, et al. Outcome of patients with endometriosis in assisted reproduction: results from in-vitro fertilization and oocyte donation. Hum Reprod. 1994;9(4):725–9.

    PubMed  CAS  Google Scholar 

  91. Marcoux S, Maheux R, Berube S. Laparoscopic surgery in infertile women with minimal or mild endometriosis. Canadian Collaborative Group on Endometriosis. New Engl J Med. 1997;337(4):217–22. doi:10.1056/NEJM199707243370401.

    PubMed  CAS  Google Scholar 

  92. Parazzini F. Ablation of lesions or no treatment in minimal-mild endometriosis in infertile women: a randomized trial. Gruppo Italiano per lo Studio dell’Endometriosi. Hum Reprod. 1999;14(5):1332–4.

    PubMed  CAS  Google Scholar 

  93. Practice Committee of the American Society for Reproductive M. Endometriosis and infertility: a committee opinion. Fertil Steril. 2012;98(3):591–8. doi:10.1016/j.fertnstert.2012.05.031.

    Google Scholar 

  94. Barnhart KT. Clinical practice. Ectopic pregnancy. New Engl J Med. 2009;361(4):379–87. doi:10.1056/NEJMcp0810384.

    PubMed  CAS  Google Scholar 

  95. Tuomivaara L, Kauppila A. Ectopic pregnancy: a case–control study of aetiological risk factors. Arch Gynecol Obstet. 1988;243(1):5–11.

    PubMed  CAS  Google Scholar 

  96. Coste J, Bouyer J, Job-Spira N. Construction of composite scales for risk assessment in epidemiology: an application to ectopic pregnancy. Am J Epidemiol. 1997;145(3):278–89.

    PubMed  CAS  Google Scholar 

  97. Hunter RH. Tubal ectopic pregnancy: a patho-physiological explanation involving endometriosis. Hum Reprod. 2002;17(7):1688–91.

    PubMed  CAS  Google Scholar 

  98. Clayton HB, Schieve LA, Peterson HB, Jamieson DJ, Reynolds MA, Wright VC. Ectopic pregnancy risk with assisted reproductive technology procedures. Obstet Gynecol. 2006;107(3):595–604. doi:10.1097/01.AOG.0000196503.78126.62.

    PubMed  Google Scholar 

  99. Bouyer J, Coste J, Shojaei T, Pouly JL, Fernandez H, Gerbaud L, et al. Risk factors for ectopic pregnancy: a comprehensive analysis based on a large case–control, population-based study in France. Am J Epidemiol. 2003;157(3):185–94.

    PubMed  Google Scholar 

  100. Bouyer J. Epidemiology of ectopic pregnancy: incidence, risk factors and outcomes. J Gynecol Obstet Biol Reprod. 2003;32(7 Suppl):S8–17.

    CAS  Google Scholar 

  101. Neri A, Marcus SL. Effect of nicotine on the motility of the oviducts in the rhesus monkey: a preliminary report. J Reprod Fertil. 1972;31(1):91–7.

    PubMed  CAS  Google Scholar 

  102. Mitchell JA, Hammer RE. Effects of nicotine on oviducal blood flow and embryo development in the rat. J Reprod Fertil. 1985;74(1):71–6.

    PubMed  CAS  Google Scholar 

  103. Knoll M, Shaoulian R, Magers T, Talbot P. Ciliary beat frequency of hamster oviducts is decreased in vitro by exposure to solutions of mainstream and sidestream cigarette smoke. Biol Reprod. 1995;53(1):29–37.

    PubMed  CAS  Google Scholar 

  104. Knoll M, Talbot P. Cigarette smoke inhibits oocyte cumulus complex pick-up by the oviduct in vitro independent of ciliary beat frequency. Reprod Toxicol (Elmsford, NY). 1998;12(1):57–68.

    CAS  Google Scholar 

  105. Pier B, Kazanjian A, Gillette L, Strenge K, Burney RO. Effect of cigarette smoking on human oviductal ciliation and ciliogenesis. Fertil Steril. 2013;99(1):199–205. doi:10.1016/j.fertnstert.2012.08.041.

    PubMed  CAS  Google Scholar 

  106. Shao R, Zou S, Wang X, Feng Y, Brannstrom M, Stener-Victorin E, et al. Revealing the hidden mechanisms of smoke-induced fallopian tubal implantation. Biol Reprod. 2012;86(4):131. doi:10.1095/biolreprod.112.098822.

    PubMed  Google Scholar 

  107. Haggerty CL, Gottlieb SL, Taylor BD, Low N, Xu F, Ness RB. Risk of sequelae after Chlamydia trachomatis genital infection in women. J Infect Dis. 2010;201 Suppl 2:S134–55. doi:10.1086/652395.

    PubMed  Google Scholar 

  108. Paavonen J, Eggert-Kruse W. Chlamydia trachomatis: impact on human reproduction. Hum Reprod Update. 1999;5(5):433–47.

    PubMed  CAS  Google Scholar 

  109. McGee ZA, Jensen RL, Clemens CM, Taylor-Robinson D, Johnson AP, Gregg CR. Gonococcal infection of human fallopian tube mucosa in organ culture: relationship of mucosal tissue TNF-alpha concentration to sloughing of ciliated cells. Sex Transm Dis. 1999;26(3):160–5.

    PubMed  CAS  Google Scholar 

  110. McGee ZA, Johnson AP, Taylor-Robinson D. Pathogenic mechanisms of Neisseria gonorrhoeae: observations on damage to human fallopian tubes in organ culture by gonococci of colony type 1 or type 4. J Infect Dis. 1981;143(3):413–22.

    PubMed  CAS  Google Scholar 

  111. McGee ZA, Clemens CM, Jensen RL, Klein JJ, Barley LR, Gorby GL. Local induction of tumor necrosis factor as a molecular mechanism of mucosal damage by gonococci. Microb Pathog. 1992;12(5):333–41.

    PubMed  CAS  Google Scholar 

  112. Stephens DS, McGee ZA, Cooper MD. Cytopathic effects of the pathogenic Neisseria. Studies using human fallopian tube organ cultures and human nasopharyngeal organ cultures. Antonie van Leeuwenhoek. 1987;53(6):575–84.

    PubMed  CAS  Google Scholar 

  113. Woods 2nd ML, McGee ZA. Molecular mechanisms of pathogenicity of gonococcal salpingitis. Drugs. 1986;31 Suppl 2:1–6.

    PubMed  Google Scholar 

  114. Cooper MD, Rapp J, Jeffery-Wiseman C, Barnes RC, Stephens DS. Chlamydia trachomatis infection of human fallopian tube organ cultures. J Gen Microbiol. 1990;136(6):1109–15.

    PubMed  CAS  Google Scholar 

  115. Dixon RE, Hwang SJ, Hennig GW, Ramsey KH, Schripsema JH, Sanders KM, et al. Chlamydia infection causes loss of pacemaker cells and inhibits oocyte transport in the mouse oviduct. Biol Reprod. 2009;80(4):665–73. doi:10.1095/biolreprod.108.073833.

    PubMed  CAS  PubMed Central  Google Scholar 

  116. Brunham RC, Peeling RW. Chlamydia trachomatis antigens: role in immunity and pathogenesis. Infect Agents Dis. 1994;3(5):218–33.

    PubMed  CAS  Google Scholar 

  117. Eckert LO, Hawes SE, Wolner-Hanssen P, Money DM, Peeling RW, Brunham RC, et al. Prevalence and correlates of antibody to chlamydial heat shock protein in women attending sexually transmitted disease clinics and women with confirmed pelvic inflammatory disease. The Journal of infectious diseases. 1997;175(6):1453–8.

    PubMed  CAS  Google Scholar 

  118. Toye B, Laferriere C, Claman P, Jessamine P, Peeling R. Association between antibody to the chlamydial heat-shock protein and tubal infertility. J Infect Dis. 1993;168(5):1236–40.

    PubMed  CAS  Google Scholar 

  119. LaVerda D, Kalayoglu MV, Byrne GI. Chlamydial heat shock proteins and disease pathology: new paradigms for old problems? Infect Dis Obstet Gynecol. 1999;7(1–2):64–71. doi:10.1155/s1064744999000137.

    PubMed  CAS  PubMed Central  Google Scholar 

  120. Toth M, Jeremias J, Ledger WJ, Witkin SS. In vivo tumor necrosis factor production in women with salpingitis. Surgery, gynecology & obstetrics. 1992;174(5):359–62.

    CAS  Google Scholar 

  121. Ojcius DM, Souque P, Perfettini JL, Dautry-Varsat A. Apoptosis of epithelial cells and macrophages due to infection with the obligate intracellular pathogen Chlamydia psittaci. J Immunol (Baltimore, Md : 1950). 1998;161(8):4220–6.

    CAS  Google Scholar 

  122. Kinnunen A, Surcel HM, Halttunen M, Tiitinen A, Morrison RP, Morrison SG, et al. Chlamydia trachomatis heat shock protein-60 induced interferon-gamma and interleukin-10 production in infertile women. Clin Exp Immunol. 2003;131(2):299–303.

    PubMed  CAS  PubMed Central  Google Scholar 

  123. Ault KA, Kelly KA, Ruther PE, Izzo AA, Izzo LS, Sigar IM, et al. Chlamydia trachomatis enhances the expression of matrix metalloproteinases in an in vitro model of the human fallopian tube infection. Am J Obstet Gynecol. 2002;187(5):1377–83.

    PubMed  CAS  Google Scholar 

  124. Leng Z, Moore DE, Mueller BA, Critchlow CW, Patton DL, Halbert SA, et al. Characterization of ciliary activity in distal Fallopian tube biopsies of women with obstructive tubal infertility. Hum Reprod. 1998;13(11):3121–7.

    PubMed  CAS  Google Scholar 

  125. Laufer N, Simon A, Schenker JG, Sekeles E, Cohen R. Fallopian tubal mucosal damage induced experimentally by Escherichia coli in the rabbit. A scanning electron microscopic study. Pathol Res Pract. 1984;178(6):605–10. doi:10.1016/s0344-0338(84)80094-1.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mohammad Ezzati.

Additional information

Capsule Tubal transport of gametes and embryo requires coordinated actions of ciliary movement, tubal peristalsis and tubal fluid. Ciliary movement is controlled by many different signals and can be adversely affected by a variety of conditions such as endometriosis, infection and smoking.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ezzati, M., Djahanbakhch, O., Arian, S. et al. Tubal transport of gametes and embryos: a review of physiology and pathophysiology. J Assist Reprod Genet 31, 1337–1347 (2014). https://doi.org/10.1007/s10815-014-0309-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10815-014-0309-x

Keywords

Navigation