Seminal fluid and reproduction: Much more than previously thought

Journal of Assisted Reproduction and Genetics

Volumn 31, Issue 6, 2014, Pages 627-636

  Bromfield, John J ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

Fertility; Inflammation; Programming; Seminal fluid

Indexed keywords

ADULT DISEASE; ARTIFICIAL INSEMINATION; FIRST TRIMESTER PREGNANCY; INFLAMMATION; LYMPHOCYTE ACTIVATION; NONHUMAN; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROGENY; REPRODUCTION; REVIEW; SEMINAL PLASMA; SPERM; TRANSPORT MEDIUM; ANIMAL; EMBRYO DEVELOPMENT; ENDOMETRIUM; FEMALE; FERTILITY; HUMAN; IMMUNOLOGY; MALE; MOUSE; NIDATION; PATHOLOGY; PREGNANCY; SPERMATOZOON;

MUS;

ANIMALS; EMBRYO IMPLANTATION; EMBRYONIC DEVELOPMENT; ENDOMETRIUM; FEMALE; FERTILITY; HUMANS; INFLAMMATION; MALE; MICE; PREGNANCY; REPRODUCTION; SEMEN; SPERMATOZOA;

EID: 84904121644     PISSN: 10580468     EISSN: 15737330     Source Type: Journal    
DOI: 10.1007/s10815-014-0243-y     Document Type: Review

References (118)

1. Queen K, Dhabuwala CB, Pierrepoint CG. The effect of the removal of the various accessory sex glands on the fertility of male rats. J Reprod Fertil. 1981;62(2):423-6. (Pubitemid 11034889)
2. Black CA, Rohan LC, Cost M, Watkins SC, Draviam R, Alber S, et al. Vaginal mucosa serves as an inductive site for tolerance. J Immunol. 2000;165(9):5077-83.
3. Cukierski MA, Sina JL, Prahalada S, Robertson RT. Effects of seminal vesicle and coagulating gland ablation on fertility in rats. Reprod Toxicol. 1991;5(4):347-52.
4. Chan OC, Chow PH, O WS. Total ablation of paternal accessory sex glands curtails developmental potential in preimplantation embryos in the golden hamster. Anat Embryol (Berl). 2001;204 (2):117-22. (Pubitemid 32761701)
5. Tremellen KP, Valbuena D, Landeras J, Ballesteros A, Martinez J, Mendoza S, et al. The effect of intercourse on pregnancy rates during assisted human reproduction. Hum Reprod. 2000;15(12):2653-8. (Pubitemid 32004634)
6. Maxwell WM, Evans G, Mortimer ST, Gillan L, Gellatly ES, McPhie CA. Normal fertility in ewes after cervical insemination with frozen-thawed spermatozoa supplemented with seminal plasma. Reprod Fertil Dev. 1999;11(2):123-6.
7. Tremellen KP, Seamark RF, Robertson SA. Seminal transforming growth factor beta1 stimulates granulocyte-macrophage colonystimulating factor production and inflammatory cell recruitment in the murine uterus. Biol Reprod. 1998;58(5):1217-25. (Pubitemid 28217246)
8. Robertson SA, Mau VJ, Tremellen KP, Seamark RF. Role of high molecular weight seminal vesicle proteins in eliciting the uterine inflammatory response to semen in mice. J Reprod Fertil. 1996;107(2):265-77.
9. Robertson SA, Mau VJ, Hudson SN, Tremellen KP. Cytokineleukocyte networks and the establishment of pregnancy. Am J Reprod Immunol. 1997;37(6):438-42.
10. Robertson SA, Prins JR, Sharkey DJ, Moldenhauer LM. Seminal fluid and the generation of regulatory T cells for embryo implantation. Am J Reprod Immunol. 2013;69(4):315-30. doi:10.1111/aji.12107.
11. Sharkey DJ, Macpherson AM, Tremellen KP, Mottershead DG, Gilchrist RB, Robertson SA. TGF-beta mediates proinflammatory seminal fluid signaling in human cervical epithelial cells. J Immunol. 2012;189(2):1024-35. doi:10.4049/ jimmunol.1200005.
12. Sharkey DJ, Tremellen KP, Jasper MJ, Gemzell-Danielsson K, Robertson SA. Seminal fluid induces leukocyte recruitment and cytokine and chemokine mRNA expression in the human cervix after coitus. J Immunol. 2012;188(5):2445-54. doi:10.4049/jimmunol.1102736.
13. Bromfield JJ, Schjenken JE, Chin PY, Care AS, Jasper MJ, Robertson SA. Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring. Proc Natl Acad Sci U S A. 2014;111(6):2200-5. doi:10.1073/pnas.1305609111.
14. Tremellen KP. Seminal priming for successful mammalian pregnancy. In: Gupta S, editor. Reproductive Immunology. New Delhi: Narosa Publishing House; 1999. p. 88-96.
15. Barker DJ, Osmond C, Golding J, Kuh D, Wadsworth ME. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. Bmj. 1989;298(6673):564-7. (Pubitemid 19072097)
16. Barker DJ. Mothers, Babies and Health in Later Life. Edinburgh, NY: Churchill Livingstone; 1998.
17. Roseboom TJ, van der Meulen JH, Ravelli AC, Osmond C, Barker DJ, Bleker OP. Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview. Mol Cell Endocrinol. 2001;185(1-2):93-8. (Pubitemid 33103957)
18. Kind KL, Roberts CT, Sohlstrom AI. Katsman A. Robinson JS et al. Chronic maternal feed restriction impairs growth but increases adiposity of the fetal guinea pig. Am J Physiol Regul Integr Comp Physiol: Clifton PM; 2004.
19. Desai M, Gayle D, Babu J, Ross MG. Programmed Obesity in Intrauterine Growth Restricted Newborns: Modulation by Newborn Nutrition. Am J Physiol Regul Integr Comp Physiol. 2005;288(1):R91-6. (Pubitemid 40023917)
20. Robinson JS, Falconer J, Owens JA. Intrauterine growth retardation: clinical and experimental. Acta Paediatr Scand Suppl. 1985;319:135-42. (Pubitemid 16118032)
21. Elias SG, Peeters PH, Grobbee DE, van Noord PA. Breast cancer risk after caloric restriction during the 1944-1945 Dutch famine. J Natl Cancer Inst. 2004;96(7):539-46. (Pubitemid 38559578)
22. Elias SG, Peeters PH, Grobbee DE, van Noord PA. The 1944-1945 Dutch famine and subsequent overall cancer incidence. Cancer Epidemiol Biomarkers Prev. 2005;14(8):1981-5. (Pubitemid 41161211)
23. Elias SG, van Noord PA, Peeters PH, den Tonkelaar I, Grobbee DE. Childhood exposure to the 1944-1945 Dutch famine and subsequent female reproductive function. Hum Reprod. 2005;20(9):2483-8. (Pubitemid 41222495)
24. Kind KL, Clifton PM, Katsman AI, Tsiounis M, Robinson JS, Owens JA. Restricted fetal growth and the response to dietary cholesterol in the guinea pig. Am J Physiol. 1999;277(6 Pt 2):R1675-82. (Pubitemid 30043774)
25. Belobrajdic D, McIntosh G, Owens J. The effects of dietary protein on rat growth, body composition and insulin sensitivity. Asia Pac J Clin Nutr. 2003;12 Suppl:S42.
26. Kwong WY, Wild AE, Roberts P, Willis AC, Fleming TP. Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development. 2000;127(19):4195-202.
27. Wu G, Bazer FW, Cudd TA, Meininger CJ, Spencer TE. Maternal nutrition and fetal development. J Nutr. 2004;134(9):2169-72. (Pubitemid 39201580)
28. McConnell JM, Petrie L. Mitochondrial DNA turnover occurs during preimplantation development and can be modulated by environmental factors. Reprod Biomed Online. 2004;9(4):418-24. (Pubitemid 39335265)
29. Taylor PD, McConnell J, Khan IY, Holemans K, Lawrence KM, Asare-Anane H, et al. Impaired glucose homeostasis and mitochondrial abnormalities in offspring of rats fed a fat-rich diet in pregnancy. Am J Physiol Regul Integr Comp Physiol. 2005;288(1):R134-9. (Pubitemid 40023923)
30. Sayer AA, Cooper C. Fetal programming of body composition and musculoskeletal development. Early Hum Dev. 2005;81(9):735-44. (Pubitemid 41253518)
31. Fowden AL, Forhead AJ. Endocrine mechanisms of intrauterine programming. Reproduction. 2004;127(5):515-26. (Pubitemid 38745069)
32. Fowden AL, Giussani DA, Forhead AJ. Endocrine and metabolic programming during intrauterine development. Early Hum Dev. 2005;81(9):723-34. (Pubitemid 41253517)
33. Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ. Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature. 2010;467(7318):963-6. doi:10.1038/nature09491.
34. Gardner DK, Lane M. Ex vivo early embryo development and effects on gene expression and imprinting. Reprod Fertil Dev. 2005;17(3):361-70. (Pubitemid 40425690)
35. Lane M, Gardner DK. Ammonium induces aberrant blastocyst differentiation, metabolism, pH regulation, gene expression and subsequently alters fetal development in the mouse. Biol Reprod. 2003;69(4):1109-17. (Pubitemid 37173840)
36. Lane M, Gardner DK. Understanding cellular disruptions during early embryo development that perturb viability and fetal development. Reprod Fertil Dev. 2005;17(3):371-8. (Pubitemid 40425691)
37. Robertson SA, Mayrhofer G, Seamark RF. Ovarian steroid hormones regulate granulocyte-macrophage colony-stimulating factor synthesis by uterine epithelial cells in the mouse. Biol Reprod. 1996;54(1):183-96. (Pubitemid 126506814)
38. Robertson SA. Granulocyte-Macrophage Colony Stimulating Factor (GM-CSF): A Paracrine Regulator in the Pre-Implantation Mouse Uterus. Adelaide: University of Adelaide; 1993.
39. Sjoblom C, Wikland M, Robertson SA. Granulocyte-macrophage colony-stimulating factor (GM-CSF) acts independently of the beta common subunit of the GM-CSF receptor to prevent inner cell mass apoptosis in human embryos. Biol Reprod. 2002;67(6):1817-23. (Pubitemid 35388012)
40. Robertson SA, Sjoblom C, Jasper MJ, Norman RJ, Seamark RF. Granulocyte-macrophage colony-stimulating factor promotes glucose transport and blastomere viability in murine preimplantation embryos. Biol Reprod. 2001;64(4):1206-15. (Pubitemid 32239193)
41. Lavranos TC, Rathjen PD, Seamark RF. Trophic effects of myeloid leukaemia inhibitory factor (LIF) on mouse embryos. J Reprod Fertil. 1995;105(2):331-8. (Pubitemid 26008027)
42. Hardy K, Spanos S. Growth factor expression and function in the human and mouse preimplantation embryo. J Endocrinol. 2002;172(2):221-36. (Pubitemid 34183071)
43. Schultz GA, Heyner S. Growth factors in preimplantation mammalian embryos. Oxf Rev Reprod Biol. 1993;15:43-81.
44. Harvey MB, Kaye PL. Mediation of the actions of insulin and insulin-like growth factor-1 on preimplantation mouse embryos in vitro. Mol Reprod Dev. 1992;33(3):270-5.
45. Brice EC, Wu JX, Muraro R, Adamson ED, Wiley LM. Modulation of mouse preimplantation development by epidermal growth factor receptor antibodies, antisense RNA, and deoxyoligonucleotides. Dev Genet. 1993;14(3):174-84. (Pubitemid 23219916)
46. Tamada H, Higashiyama C, Takano H, Kawate N, Inaba T, Sawada T. The effects of heparin-binding epidermal growth factor-like growth factor on preimplantation-embryo development and implantation in the rat. Life Sci. 1999;64(22):1967-73. (Pubitemid 29236580)
47. Sjoblom C, Roberts CT, Wikland M, Robertson SA. Granulocytemacrophage colony-stimulating factor alleviates adverse consequences of embryo culture on fetal growth trajectory and placental morphogenesis. Endocrinology. 2005;146(5):2142-53. (Pubitemid 40577498)
48. Aitken RJ, Baker MA, Sawyer D. Oxidative stress in the male germ line and its role in the aetiology of male infertility and genetic disease. Reprod Biomed Online. 2003;7(1):65-70. (Pubitemid 36874408)
49. Sanocka D, Miesel R, Jedrzejczak P, Chelmonska-Soyta AC, Kurpisz M. Effect of reactive oxygen species and the activity of antioxidant systems on human semen; association with male infertility. Int J Androl. 1997;20(5):255-64. (Pubitemid 28025217)
50. Garrido N, Meseguer M, Simon C, Pellicer A, Remohi J. Prooxidative and anti-oxidative imbalance in human semen and its relation with male fertility. Asian J Androl. 2004;6(1):59-65. (Pubitemid 38418340)
51. Wolters-Everhardt E, Dony JM, Lemmens WA, Doesburg WH, De Pont JJ. Buffering capacity of human semen. Fertil Steril. 1986;46(1):114-9. (Pubitemid 16100841)
52. Wolters-Everhardt E, Dony JM, Peters WH, De Pont JJ. Buffering substances of human semen. Fertil Steril. 1987;48(1):159-61. (Pubitemid 17093272)
53. Kelly RW. Prostaglandins in primate semen: biasing the immune system to benefit spermatozoa and virus? Prostaglandins Leukot Essent Fatty Acids. 1997;57(2):113-8. (Pubitemid 27303864)
54. Peitz B, Olds-Clarke P. Effects of seminal vesicle removal on fertility and uterine sperm motility in the house mouse. Biol Reprod. 1986;35(3):608-17.
55. Ying Y, Chow PH. Cheung MP. O WS Effects ofmale accessory sex glands on sperm decondensation and oocyte activation during in vivo fertilization in golden hamsters Int J Androl. 1999;22:68-76. (Pubitemid 29136949)
56. Pang SF, Chow PH, Wong TM. The role of the seminal vesicles, coagulating glands and prostate glands on the fertility and fecundity of mice. J Reprod Fertil. 1979;56(1):129-32.
57. WS O, Chen HQ, Chow PH. Effects of male accessory sex gland secretions on early embryonic development in the golden hamster. J Reprod Fertil. 1988;84(1):341-4.
58. Jiang HY, O WS, Lee KH, Tang PL, Chow PH. Ablation of paternal accessory sex glands is detrimental to embryo development during implantation. Anat Embryol (Berl). 2001;203 (4):255-63. (Pubitemid 32396415)
59. De M. Determination of the number and distribution of macrophages, lymphocytes and granulocytes in the mouse uterus from mating through implantation. J Leukoc Biol. 1991;50:252-62.
60. Thompson LA, Barratt CL, Bolton AE, Cooke ID. The leukocytic reaction of the human uterine cervix. Am J Reprod Immunol. 1992;28(2):85-9. (Pubitemid 23017927)
61. Phillips DM, Mahler S. Leukocyte emigration and migration in the vagina following mating in the rabbit. Anat Rec. 1977;189(1):45-59. (Pubitemid 8196451)
62. O'Leary S, Jasper MJ, Warnes GM, Armstrong DT, Robertson SA. Seminal plasma regulates endometrial cytokine expression, leukocyte recruitment and embryo development in the pig. Reproduction. 2004;128(2):237-47. (Pubitemid 39162695)
63. Pandya IJ, Cohen J. The leukocytic reaction of the human uterine cervix to spermatozoa. Fertil Steril. 1985;43(3):417-21. (Pubitemid 15111130)
64. Troedsson MH, Loset K, Alghamdi AM, Dahms B, Crabo BG. Interaction between equine semen and the endometrium: the inflammatory response to semen. Anim Reprod Sci. 2001;68(3-4):273-8. (Pubitemid 34029597)
65. Anderson DJ, Tarter TH. Immunosuppressive effects of mouse seminal plasma components in vivo and in vitro. J Immunol. 1982;128(2):535-9. (Pubitemid 12168396)
66. Fahmi HA, Hunter AG, Markham RJ, Seguin BE. Immunosuppressive activity of bovine seminal plasma on bovine lymphocytes in vitro. J Dairy Sci. 1985;68(9):2315-21.
67. Saxena S, Jha P, Farooq A. Immunosuppression by human seminal plasma. Immunol Invest. 1985;14(3):255-69. (Pubitemid 16256817)
68. James K. Immunosuppression by seminal plasma and its possible clinical significance. Immunol Today. 1984;5(12):357-63.
69. Anderson DJ, Tarter TH. Immunosuppressive effects of mouse seminal plasma components in vivo and in vitro. J Immunol. 1982;128(2):535-9. (Pubitemid 12168396)
70. Kelly RW, Carr GG, Critchley HO. A cytokine switch induced by human seminal plasma: an immune modulation with implications for sexually transmitted disease. Hum Reprod. 1997;12(4):677-81. (Pubitemid 27223028)
71. Robertson S, Sharkey D. The role of semen in induction of maternal immune tolerance to pregnancy. Semin Immunol. 2001;13(4):243-54. (Pubitemid 32666204)
72. Thaler CJ. Immunological role for seminal plasma in insemination and pregnancy. Am J Reprod Immunol. 1989;21(3-4):147-50. (Pubitemid 20173974)
73. Quayle AJ, Xu C, Mayer KH, Anderson DJ. T lymphocytes and macrophages, but not motile spermatozoa, are a significant source of human immunodeficiency virus in semen. J Infect Dis. 1997;176(4):960-8. (Pubitemid 27411038)
74. Uyenoyama MK. Coevolution of the major histocompatibility complex and the t-complex in the mouse. I Generation and maintenance of high complementarity associations Genetics. 1989;121(1):139-51. (Pubitemid 19026327)
75. Iyer SV, Nandedkar TD, Hegde UC. Production of H-Yantibody in the ascites fluid ofmouse and localization of the antigen on cells and tissues. Gamete Res. 1989;22(1):37-49. (Pubitemid 19202187)
76. Anderson DJ, Bach DL, Yunis EJ, DeWolf WC. Major histocompatibility antigens are not expressed on human epididymal sperm. J Immunol. 1982;129(2):452-4. (Pubitemid 12039359)
77. Hutter H, Dohr G. HLA expression on immature and mature human germ cells. J Reprod Immunol. 1998;38(2):101-22. (Pubitemid 28342648)
78. Yao GD, Shu YM, Shi SL, Peng ZF, Song WY, Jin HX, et al. Expression and Potential Roles of HLA-G in Human Spermatogenesis and Early Embryonic Development. PloS one. 2014;9(3):e92889. doi:10.1371/journal.pone.0092889.
79. Beer AE, Billingham RE. Host responses to intra-uterine tissue, cellular and fetal allografts. J Reprod Fertil, Suppl. 1974;21:59-88.
80. Watson JG, Chaykin S, Carroll J. Repoduction in mice: The fate of sprematozoa not involved in fertilisation. Gamete Res. 1983;7:75-84. (Pubitemid 13114546)
81. Parr MB, Parr EL. Antigen recognition in the female reproductive tract: I. Uptake of intraluminal protein tracers in the mouse vagina J Reprod Immunol. 1990;17(2):101-14. (Pubitemid 20101933)
82. Parr EL, Parr MB, Zheng LM, Young JD.Mouse granulated metrial gland cells originate by local activation of uterine natural killer lymphocytes. Biol Reprod. 1991;44(5):834-41.
83. Johansson M, Bromfield JJ, Jasper MJ, Robertson SA. Semen activates the female immune response during early pregnancy in mice. Immunology. 2004;112(2):290-300. (Pubitemid 38703575)
84. Piazzon I, Matusevich M, Deroche A, Nepomnaschy I, Pasqualini CD. Early increase in graft-versus-host reactivity during pregnancy in the mouse. J Reprod Immunol. 1985;8(2-3):129-37. (Pubitemid 16174693)
85. O'Hearn M, Hilgard HR. Pregnancy-induced alterations in graft-versus-host responsiveness of uterine-draining and peripheral lymph node cells toward fetal alloantigens. Transplantation. 1981;32(5):389-91. (Pubitemid 12244276)
86. Kapovic M, Rukavina D. Kinetics of lymphoproliferative responses of lymphocytes harvested from the uterine draining lymph nodes during pregnancy in rats. J Reprod Immunol. 1991;20:93-101.
87. Clark D. Contoversies in reproductive immunology. Crit Rev Immunol. 1991;11 (3,4):215-47.
88. Beer AE, Scott JR, Billingham RE. Histoincompatibility and maternal immunological status as determinants of fetoplacental weight and litter size in rodents. J Exp Med. 1975;142(1):180-96.
89. Aluvihare VR, Kallikourdis M, Betz AG. Regulatory T cells mediate maternal tolerance to the fetus.Nat Immunol. 2004;5(3):266-71. (Pubitemid 38332123)
90. Guerin LR, Moldenhauer LM, Prins JR, Bromfield JJ, Hayball JD, Robertson SA. Seminal fluid regulates accumulation of FOXP3+ regulatory T cells in the preimplantation mouse uterus through expanding the FOXP3+ cell pool and CCL19-mediated recruitment. Biol Reprod. 2011;85(2):397-408. doi:10.1095/biolreprod.110.088591.
91. Vacchio MS, Jiang SP. The fetus and the maternal immune system: pregnancy as a model to study peripheral T-cell tolerance. Crit Rev Immunol. 1999;19(5-6):461-80. (Pubitemid 30053174)
92. Billingham R. Transplantation immunity and the maternal-fetal relation. N Engl J Med. 1964;270(13):667-71.
93. Daimon E, Wada Y. Role of neutrophils in matrix metalloproteinase activity in the preimplantation mouse uterus. Biol Reprod. 2005;73(1):163-71. (Pubitemid 40863611)
94. Chow PH, Jiang HY, Poon HK, Lee KH, O WS. Embryos sired by males without accessory sex glands induce failure of uterine support: a study of VEGF, MMP and TGF expression in the golden hamster. Anat Embryol (Berl). 2003;206 (3):203-13. (Pubitemid 36313000)
95. van der Heijden OW, Essers YP, Spaanderman ME, De Mey JG, van Eys GJ, Peeters LL. Uterine Artery Remodeling in Pseudopregnancy Is Comparable to that in Early Pregnancy. Biol Reprod. 2005;73(6):1289-93. (Pubitemid 41698621)
96. Kosaka K, Fujiwara H, Tatsumi K, Yoshioka S, Higuchi T, Sato Y, et al. Human peripheral blood mononuclear cells enhance cell-cell interaction between human endometrial epithelial cells and BeWocell spheroids. Hum Reprod. 2003;18(1):19-25. (Pubitemid 36138846)
97. Hill JA. T-helper 1-type immunity to trophoblast: evidence for a new immunological mechanism for recurrent abortion in women. Hum Reprod. 1995;10 Suppl 2:114-20. (Pubitemid 26023496)
98. Raghupathy R. Th1-type immunity is incompatible with successful pregnancy. Immunol Today. 1997;18(10):478-82. (Pubitemid 27441590)
99. Kanbour A, Ho HN, Misra DN, MacPherson TA, Kunz HW, Gill TJ. Differential expression of MHC class I antigens on the placenta of the rat. A mechanism for the survival of the fetal allograft J Exp Med. 1987;166(6):1861-82. (Pubitemid 18000361)
100. Kiger N, Chaouat G, Kolb JP, Wegmann TG, Guenet JL. Immunogenetic studies of spontaneous abortion in mice. Preimmunization of females with allogeneic cells J Immunol. 1985;134(5):2966-70. (Pubitemid 15249806)
101. Klonoff-Cohen HS, Savitz DA, Celafo RC, McCann MF. An epidemiologic study of contraception and preeclampsia. Journal of the American Medical association. 1989;262:3143-7. (Pubitemid 20002632)
102. Robillard PY, Hulsey TC, Perianin J, Janky E, Miri EH, Papiernik E. Association of pregnancy-induced hypertension with duration of sexual cohabitation before conception. The Lancet. 1995;344:973-5. (Pubitemid 24306548)
103. Dekker GA, Robillard PY, Hulsey TC. Immune maladaptation in the etiology of preeclampsia: a review of corroborative epidemiologic studies. ObstetGynecolSurv. 1998;53(6):377-82. (Pubitemid 28267940)
104. Robertson SA, Bromfield JJ, Tremellen KP. Seminal 'priming' for protection from pre-eclampsia-a unifying hypothesis. J Reprod Immunol. 2003;59(2):253-65. (Pubitemid 36957855)
105. Lambert RD. Safety issues in assisted reproductive technology: aetiology of health problems in singleton ART babies. Hum Reprod. 2003;18(10):1987-91. (Pubitemid 37265056)
106. Perri T, Chen R, Yoeli R, Merlob P, Orvieto R, Shalev Y, et al. Are singleton assisted reproductive technology pregnancies at risk of prematurity? J Assist Reprod Genet. 2001;18(5):245-9. (Pubitemid 32613765)
107. Wang JX, Norman RJ, Kristiansson P. The effect of various infertility treatments on the risk of preterm birth. Hum Reprod. 2002;17(4):945-9. (Pubitemid 34411127)
108. Schieve LA, Meikle SF, Ferre C, Peterson HB, Jeng G, Wilcox LS. Low and very low birth weight in infants conceived with use of assisted reproductive technology. N Engl J Med. 2002;346(10):731-7. (Pubitemid 34983993)
109. Ochsenkuhn R, Strowitzki T, Gurtner M, Strauss A, Schulze A, Hepp H, et al. Pregnancy complications, obstetric risks, and neonatal outcome in singleton and twin pregnancies after GIFT and IVF. Arch Gynecol Obstet. 2003;268(4):256-61. (Pubitemid 37210324)
110. Hansen M, Kurinczuk JJ, Bower C, Webb S. The risk of major birth defects after intracytoplasmic sperm injection and in vitro fertilization. N Engl J Med. 2002;346(10):725-30. (Pubitemid 34983992)
111. Marchand E, Poncelet C, Carbillon L, Pharisien I, Tigaizin A, Chanelles O. Is there more complications with pregnancies from the assisted reproductive technology than spontaneous pregnancies? A retrospective study over 6 years. Journal de gynecologie, obstetrique et biologie de la reproduction. 2011;40(6):522-8. doi:10.1016/j.jgyn.2011.06.010.
112. Berry KA, Baron IS, Weiss BA, Baker R, Ahronovich MD, Litman FR. In vitro fertilization and late preterm preschoolers' neuropsychological outcomes: the PETIT study. Am J Obstet Gynecol. 2013;209 (4):356 e1-6. doi:10.1016/j.ajog. 2013.06.041.
113. Thompson JG, Kind KL, Roberts CT, Robertson SA, Robinson JS. Epigenetic risks related to assisted reproductive technologies: short- and long-term consequences for the health of children conceived through assisted reproduction technology: more reason for caution? Hum Reprod. 2002;17(11):2783-6. (Pubitemid 35350891)
114. Carp HJ, Serr DM, Mashiach S, Nebel L. Influence of insemination on the implantation of transferred rat blastocysts. Gynecol Obstet Invest. 1984;18(4):194-8. (Pubitemid 14008853)
115. Coulam CB, Stern JJ. Effect of seminal plasma on implantation rates. Early Pregnancy. 1995;1(1):33-6.
116. Marconi G, Auge L, Oses R, Quintana R, Raffo F, Young E. Does sexual intercourse improve pregnancy rates in gamete intrafallopian transfer? Fertil Steril. 1989;51(2):357-9. (Pubitemid 19050544)
117. Bellinge BS, Copeland CM, Thomas TD, Mazzucchelli RE, O Neil G, Cohen MJ. The influence of patient insemination on the implantation rate in an in vitro fertilization and embryo transfer program. Fertil Steril. 1986;46(2):252-6. (Pubitemid 16041814)
118. Fishel S, Webster J, Jackson P, Faratian B. Evaluation of high vaginal insemination at oocyte recovery in patients undergoing in vitro fertilization. Fertil Steril. 1989;51(1):135-8. (Pubitemid 19033733)