Hostname: page-component-5c6d5d7d68-vt8vv Total loading time: 0.001 Render date: 2024-08-09T15:49:32.408Z Has data issue: false hasContentIssue false
  • English
  • Français

The functional significance of leucocytes in human reproduction

Published online by Cambridge University Press:  02 March 2009

CLR Barratt ,
E Kessopoulou ,
LA Thompson ,
MJ Tomlinson  and
ID Cooke
CLR Barratt*
Affiliation:
Jessop Hospital for Women, Sheffield, UK
E Kessopoulou
Affiliation:
Jessop Hospital for Women, Sheffield, UK
LA Thompson
Affiliation:
Jessop Hospital for Women, Sheffield, UK
MJ Tomlinson
Affiliation:
Jessop Hospital for Women, Sheffield, UK
ID Cooke
Affiliation:
Jessop Hospital for Women, Sheffield, UK
*
CLR Barratt, Research Scientist, University Department of Obstetrics and Gynaecology, Jessop Hospital for Women, Sheffield S3 7RE, UK.
Get access Rights & Permissions [Opens in a new window]

Extract

There is now considerable evidence that leucocytes and their products have significant effects on the functional capacity of spermatozoa both in the male and female reproductive tract. Recent advances in the accurate detection of these leucocytes and their products using monoclonal antibodies and a parallel increase in the application of sophisticated sperm function tests has now made it possible to further determine the influence of the leucocytes on sperm function. It is therefore likely that this field of reproductive biology will be an area of considerable activity in the near future.

Type
Articles
Information
Reproductive Medicine Review , Volume 1 , Issue 2 , July 1992 , pp. 115 - 129
Copyright
Copyright © Cambridge University Press 1992

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

1 Barratt, CLR, Bolton, AE, Cooke, ID. Functional significance of white blood cells in the male and female reproductive tract. Hum Reprod 1990; 5: 639–48.CrossRefGoogle Scholar
2 Auroux, M. Nonspermatozoal cells in human semen: a study of 1243 subfertile and 253 fertile men. Arch Androl 1984; 12: 197–201.Google Scholar
3 Maruyama, DK, Hale, RW, Rogers, J. Efects of white blood cells on the in vitro penetration of zona-free hamster eggs by human spermatozoa. J Androl 1985; 6: 127–35.Google Scholar
4 Cohen, J, Edwards, R, Fehilly, C et al. In vitro fertilisation: a treatment for male infertility. Fertil Steril 1985; 43: 422.CrossRefGoogle Scholar
5 Wolff, H, Anderson, DJ. Immunohistologic characterization and quantitation of leucocyte subpopulations in human semen. Fertil Steril 1988; 9: 497–504.Google Scholar
6 Wolff, H, Politch, JA, Martinez, A, Haimovici, F, Hill, JA, Anderson, DJ. Leucocytospermia is associated with poor semen quality. Fertil Steril 1990; 53: 528–36.Google Scholar
7 Wolff, H, Anderson, DJ. Evaluation of granulocyte elastase as a seminal plasma marker for leucocytospermia. Fertil Steril 1988; 50: 129–32.Google Scholar
8 Wang, AW, Anderson, D. Prevalence of leucocytospermia in male infertility patients in Beijing, China. J Androl 1991; 51 (suppl): 129.Google Scholar
9 Tomlinson, MJ, Barratt, CLR, Bolton, AE, Cooke, ID. Seminal leucocytes and semen quality. J Reprod Fertil 1990; Abstract series 6: 60.Google Scholar
10 Hughes, L, Ryder, TA, McKenzie, ML, Pryse-Davies, J, Stedronska, J, Hendry, WF. The use of transmission electron microscopy to study non spermatozoa cells in semen. In: Frajese, G, Hafez, EFE, Conti, C, Fabbrini, A eds.Oligozoospermia: recent progress in andrology. New York: Raven Press, 1981: 65–75.Google Scholar
11 Tomlinson, MJ, White, A, Barratt, CLR, Bolton, AE, Cooke, ID. The removal of morphologically abnormal sperm forms by phagocytes: a positive role for seminal leucocytes. Hum Reprod 1992; 7: 517–22.Google Scholar
12 Cohen, J. Immunological aspects of sperm selection and transport. In: Crighton, DB ed.Immunological aspects of reproduction in mammals. London: Butterworths, 1984: 77–89.Google Scholar
13 Amann, RP, Almquist, J. Reproductive capacity of dairy bulls. VI. Effects of unilateral vasectomy and ejaculation frequency on sperm reserves: aspects of epididymal physiology. J Reprod Fertil 1962; 3: 260–68.CrossRefGoogle Scholar
14 Orgebin-Crist, MC. Gonadal and epididymal sperm reserves in the rabbit: estimation of sperm production. Reprod Fertil 1968; 15: 15–25.Google Scholar
15 Gerbauer, MR, Pickett, BW, Swierstra, EE. Reproductive physiology of the stallion II – daily production and output of sperm. J Anim Sci 1974; 39: 732–36.Google Scholar
16 Amann, RP. A critical review of methods for evaluation of spermatogenesis from seminal characteristics. J Androl 1981; 2: 31–58.Google Scholar
17 Olar, TT, Amann, RP. Pickett BW. Relationships amongst testicular size, daily production and output of spermatozoa, and extra gonadal spermatozoal reserves of the dog. Biol Reprod 1983; 29: 1114–20.Google Scholar
18 Johnson, L, Petty, CS, Neaves, WB. Further quantification of human spermatogenesis: germ cell loss during post prophase of meiosis and its relationship to daily sperm production. Biol Reprod 1983; 29: 207–15.Google Scholar
19 Barratt, CLR, Cohen, J. Fate of superfluous sperm products after vasectomy and in the normal male tract of the mouse. J Reprod Fertil 1986; 71: 221–26.Google Scholar
20 Barrait, CLR, Cohen, J. Quantitation of sperm disposal and phagocytic cells in the Iracl of short and long lerm vasectomized mice. J Reprod Fertil 1987; 81: 377–84.CrossRefGoogle Scholar
21 Barratt, CLR, Cohen, J. Quantitative effects of short-and long-term vasectomy on mouse spermalogenesis and sperm transport. Contraception 1988; 27: 415–24.Google Scholar
22 Riva, A, Cossu, M, Usae, E, Tesla-Riva, F. Spermatophagy by epithelial cells of Ihe seminal vesicle and of the ampulla ductus deferenlis in man: a scanning and transmission EM sludy. In: Frajese, G, Hafez, EFE, Conti, C, Fabbrini, A eds.Oligozoospermia: recent progress in andrology. New York: Raven Press, 1981: 45–53.Google Scholar
23 Murakami, M, Nishida, S, Iwanaga, S, Shiromoto, M. Scanning and transmission electron microscopic evidence of epithelial phagocytosis in the terminal region of the vas deferens of the cat. Experienta 1988; 40: 958–60.Google Scholar
24 Phadke, AM. Fate of spermatozoa in cases of obstructive azoospermia and after ligation of the vas deferens in man. J Reprod Fert 1964; 7: 1–12.Google Scholar
25 Mitchinson, MJ, Sherman, KP, Stainef Smith, AM. Brown palches in the epididymis. J Pathol 1975; 115: 57–62.Google Scholar
26 Alexander, NJ, Anderson, DJ. Immunology of semen. Fertil Steril 1987; 47: 192–205.Google Scholar
27 Barratt, CLR, Cooke, ID. Sperm loss in the urine of sexually rested men. Int J Androl 1988; 11: 201–207.Google Scholar
28 Olsen, GP, Shields, JW. Seminal lymphocytes, plasma and AIDS. Nature 1984; 309: 116–17.Google Scholar
29 Schaeffer, AJ, Wendel, EF, Dunn, JK, Grayhack, JT. Prevalence and significance of prostatic inflammation. J Urol 1981; 125: 215–19.Google Scholar
30 Hunt, JS. Cytokine networks in the utero-placental unit: macrophages as pivotal regulatory cells. J Reprod Immunol 1987; 16: 1–17.Google Scholar
31 Hill, JA, Haimovici, F, Politch, JA, Anderson, DJ. Effects of soluble products of activated lymphocytes and macrophages on human sperm motion parameters. Fertil Steril 1987; 47: 460–65.Google Scholar
32 Eiserman, J, Register, KB, Strickler, RG, Collins, JL. The effect of tumour necrosis factor on human sperm motility in vitro. J Androl 1989; 10: 270–74.Google Scholar
33 Hill, JA, Cohen, J, Anderson, DJ. The effects of lymphokines and monokines on human sperm fertilizing ability in the zona-free hamster egg penetration test. Am J Obstet Gynecol 1989; 160: 1154–59.Google Scholar
34 Cavender, D, Haskard, DO, Joseph, B, Ziff, M. Interleukin-1 increases the binding of human B and T lymphocytes to endothelial cell monolayers. J Immunol 1986; 136: 203–207.Google Scholar
35 Cavender, D, Saegusa, Y, Ziff, M. Simulation of endothelial cell binding of lymphocytes by tumor necrosis factor. J Immunol 1987; 139: 1855–60.Google Scholar
36 Ding, AH, Nathan, CF, Stuehr, DV. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages: comparison of activation cytokines and evidence for independent production. J Immunol 1988; 141: 2407–12.Google Scholar
37 Hibbs, JB, Taintor, RR, Varrin, Z, Rachlin, EM. Nitric oxide: a cytotoxic activated macrophage effector molecule. Biochem Biophys Res Commun 1988; 157: 1.Google Scholar
38 Skoskiewicz, MJ, Colvin, RB, Schneeberger, EE, Russell, PS. Widespread and selective induction of major histocompatibility complex-determined antigens in vivo by inlerferon. J Exp Med 1985; 162: 1645–64.Google Scholar
39 Anderson, DJ, Hill, JA. Cell mediated immunity in infertility. Am J Reprod Immunol Microbiol 1988; 17: 22–30.Google Scholar
40 Bendzten, K, Srenson, M, Jonsson, V, Hippe, E. Autoantibodies to cytokines – friends or foes? Immunol Today 1990; 11: 167–69.Google Scholar
41 Hill, JA, Anderson, DJ. Lymphocyte activity in the presence of peritoneal fluid from fertile women and infertile women with and without endometriosis. Am J Obstet Gynecol 1989; 161: 861–64.Google Scholar
42 Steinleitner, A, Lambert, H, Roy, S. Immunomodulation with pentoxifylline abrogates macrophage-mediated infertility capacity of spermatozoa. Eur J Obstet Gynacol Reprod Biol 1991; 24: 49–52.Google Scholar
43 Strieter, DJ, Remick, DG, Ward, PA et al. Cellular and molecular regulation of tumour necrosis factor-alpha production by pentoxifylline. Biochem Biophys Res Commun 1988; 155: 1230–34.Google Scholar
44 Bessler, H, Gilgal, R, Djaldetti, M, Zahavi, I. Effect of pentoxifylline on the phagocytic activity, cAMP levels, and Superoxide anion production by monocyles and polymorphonuclear cells. J Leukocyte Biol 1986; 40: 747–54.Google Scholar
45 Yovich, JM, Edirishinghe, WR, Cummins, JM, Yovich, JL. Influence of pentoxifylline in severe male factor infertility. Fertil Steril 1990; 53: 715.Google Scholar
46 Kessopoulou, E, Barrait, CLR, Cooke, ID. Reactive oxygen species and seminal leucocytes. J Reprod Fertil 1990; Abstract series 6:2.Google Scholar
47 De Lamirande, E, Gagnon, C. ATP depletion plays an important role in the inhibition of sperm motility observed after treatment with reactive oxygen species. The Male Germ Cell-Spermatogonium to Fertilization, 11th North American Testis Workshop, 1991: Abstract no. 141.Google Scholar
48 Stuehr, DJ, Gross, SS, Sakuma, I, Levi, R, Nathan, CF. Activated murine macrophages secrete a metabolite of arginine with the bioactivity of endothelium derived relaxing factor (EDRF) and the chemical reactivity of nitric oxide. J Exp Med 1989; 169: 1011–20.Google Scholar
49 Craven, PA, DeRubertis, FR. Requirement for heme in the activation of purified guanylate cyclase by nitric oxide. Biochem Biophys Acta 1983; 745: 310–21.Google Scholar
50 Ignarro, IJ. Haem-dependent activation of guanylate cyclase and cyclic GMP formation by endogenous nitric oxide: a unique transduction mechanism for transcellular signalling. Pharmacol Toxicol 1990; 67: 1–7.Google Scholar
51 Stuehr, DJ, Nathan, CF. A macrophage product responsible for cytostasis and respiratory inhibition in tumour target cells. J Exp Med 1959; 169: 1543–55.Google Scholar
52 Tomlinson, MJ, East, SJ, Barratt, CLR, Bolton, AE, Cooke, ID. Possible role of reactive nitrogen intermediates in leucocyte-mediated sperm dysfunction. Am J Reprod Immunol 1992; 27: 89–92.Google Scholar
53 Marletta, MA, Yoon, PS, Iyengar, R, Leaf, CD, Wishnow, JS. Macrophage oxidation of l-arginine to nitrite and nitrate: nitric oxide is an intermediate. Biochemistry 1988; 27: 8706–11.Google Scholar
54 Estensen, RD, Hill, HR, Quie, PG, Hogan, N, Goldberg, ND. Cyclic CGP and cell movement. Nature 1973; 245: 458–60.Google Scholar
55 Shapiro, BM, Cook, S, Quest, AFG, Obedorf, J, Wother, D. Molecular mechanisms of sea-urchin sperm activation before fertilization. J Reprod Fertil [Suppl] 1990; 42: 3–8.Google Scholar
56 Fraser, LR, Monks, NJ. Cyclic nucleotides and mammalian sperm capacitation. J Reprod Fertil [Suppl] 1990; 42: 9–21.Google Scholar
57 Harrison, RAP, Vickers, SE. Use of fluorescent probes to assess membrane integrity in mammalian spermatozoa. J Reprod Fertil 1990; 88: 343.Google Scholar
58 Ford, WCL. The role of oxygen free radicals in the pathology of human spermatozoa: implications for IVF. In: Matson, PL, Lieberman, BA eds.Clinical IVF Forum. Manchester: Manchester University Press, 1990: 123–39.Google Scholar
59 Lunec, J. Free radicals: their involvement in disease processes. Ann Clin Biochem 1990; 27: 173–82.Google Scholar
60 Del Maestro, RF. An approach to free radicals in medicine and biology. Acta Physiol Scand [Suppl] 1980; 492: 153–68.Google Scholar
61 Jones, R, Mann, T. Lipid peroxidation in spermatozoa. Proc R Soc Lond [Biol] 1973; 108: 103–107.Google Scholar
62 Jones, R, Mann, T. Damage to ram spermatozoa by peroxidation of endogenous phospholipids. J Reprod Fertil 1977; 50: 261–68.Google Scholar
63 Jones, R, Mann, T, Sherins, R. Peroxidative breakdown of phospholipids in human spermatozoa, spermicidal properties of fatty acid peroxides, and protective action of seminal plasma. Fertil Steril 1979; 31: 531–37.Google Scholar
64 Alvarez, JG, Touchstone, JC, Blasco, L, Storey, BT. Spontaneous lipid peroxidation and production of hydrogen peroxide and Superoxide in human spermatozoa. J Androl 1987; 8: 338–48.Google Scholar
65 Alvarez, JG, Storey, BT. Role of glutathione peroxidase in protecting mammalian spermatozoa from loss of motility caused by spontaneous lipid peroxidalion. Gamete Res 1989; 23: 77–90.Google Scholar
66 Aitken, RJ, Clarkson, JS, Hargreave, TB, Irvine, DS, Wu, FC. Analysis of the relationship between defective sperm function and the generation of reactive oxygen species in cases of oligozoospermia. J Androl 1989; 10: 214–20.Google Scholar
67 Aitken, RJ, Irvine, DS, Wu, FC. Prospective analysis of sperm-oocyle fusion and reactive oxygen species generation as criteria for the diagnosis of infertility. Am J Obstet Gynecol 1991; 164: 542–52.Google Scholar
68 Barratt, CLR, Harrison, PE, Robinson, AE, Kessopoulou, E, Cooke, ID. Seminal while blood cells in men with urethral tract infection. A monoclonal antibody study. Br J Urol 1991; 68: 531–36.Google Scholar
69 Barratt, CLR, Kessopoulou, E, Tomlinson, MJ, Zhu, JJ, Cooke, ID. Determination of the origin of the oxygen species in semen and association with quantitative semen analysis. J Androl 1991; 53 (suppl): 116.Google Scholar
70 Kessopoulou, E, Tomlinson, MJ, Barratt, CLR, Bolton, AE, Cooke, ID. Origin of reactive oxygen species in human semen: spermatozoa or leucocytes. J Reprod Fertil 1991; 94: 463–70.CrossRefGoogle Scholar
71 Aitken, RJ, Clarkson, JS. Significance of reactive oxygen species and antioxidants in defining the efficacy of sperm preparation techniques. J Androl 1988; 9: 367–76.Google Scholar
72 Barratt, CLR, Li, TC, Monteiro, EF. Diagnosis and detection of male accessory gland infection. In: Barratt, CLR, Cooke, ID eds.Advances in clinical andrology. Lancaster: MTP Press, 1988: 91–97.Google Scholar
73 Schlegel, PN, Chang, TSK, Marshall, FF. Antibiotics: potential hazards to male fertility. Fertil Steril 1991; 55: 235–45.Google Scholar
74 Slater, K, Wiseman, MS, Shale, DJ, Fletcher, J. The effeel of pentoxifylline on neutrophil function in vitro and ex vivo in human volunteers. In: Mandell, GJ, Novick, WJ eds. Pentoxifylline and leucocyte function. New Jersey: Hoechst-Roussel Pharmaceuticals Inc, 1988: 115–24.Google Scholar
75 Drevon, CA. Absorption, transport and metabolism of vitamin E. Free Radic Res Commun 1991; 14: 229–46.Google Scholar
76 Monteiro, EF, Spencer, RC, Kinghorn, GRY, Barratt, CLR, Cooke, S, Cooke, ID. Sexually transmitted disease in potential semen donors. Br Med J 1987; 295: 415.Google Scholar
77 Barratt, CLR, Monteiro, E, Chauhan, M, Cooke, S, Cooke, ID. Screening potential semen donors for sexually transmitted diseases in donor insemination centres in the UK. Br J Obstet Gynaecol 1989; 96: 461–66.Google Scholar
78 Barratt, CLR, Robinson, A, Spencer, RC et al. Seminal peroxidase positive cells are not an adequate indicator of asymptomatic urethral genital infection. Int J Androl 1990; 13: 361–68.Google Scholar
79 Wolff, H, Neubert, U, Zebhauser, et al. Chlamydia trachomatis induces an inflammatory response in the male genital tract and is associated with altered semen quality. Fertil Steril 1991; 55: 1017–19.Google Scholar
80 Alexander, NJ. Sexual transmission of human immunodeficiency virus: virus entry into the male and female genital tract. Fertil Steril 1990; 54: 1–18.Google Scholar
81 Anderson, DJ, Wolff, H, Pudney, J, Wenhao, Z, Martinez, A, Mayer, K. Presence of HIV in semen. In: Alexander, NJ, Gabelnick, HL, Spieler, JM eds. Heterosexual transmission of AIDS. New York: Alan R Liss, 1990: 167–180.Google Scholar
82 Pudney, J, Anderson, D. HIV-1 in the reproductive tract of a man with epididymal obstruction: a case report. J Androl 1991; 36 (suppl): 47.Google Scholar
83 Edwards, JNT, Morris, HB. Langerhan cells and lymphocyte subsets in the female reproductive tract. Br J Obstet Gynecol 1985; 92: 947–82.Google Scholar
84 Roitt, IM. Essential immunology, sixth edition. Oxford: Blackwell Scientific Publications, 1988.Google Scholar
85 Austin, CR. Fate of spermatozoa in the female genital tract. J Reprod Fertil 1960; 1: 151–56.Google Scholar
86 Mattner, PE. Phagocytosis of spermatozoa by leucocytes in bovine cervical mucus in vitro. J Reprod Fertil 1969; 20: 133–34.Google Scholar
87 Phillips, DM, Mahler, S. Leucocyte emigration and migration in the vagina following mating in the rabbit. Anat Rec 1911; 189: 45–60.Google Scholar
88 Tyler, KR. Histological changes in the cervix of the rabbit after coitus. J Reprod Fertil 1977; 46: 345–431.Google Scholar
89 Taylor, NJ. Investigation of sperm-induced cervical leucocytosis by a double mating study in rabbits. J Reprod Fertil 1982; 66: 157–60.Google Scholar
90 Moyer, DL, Rimdust, S, Mishel, DR. Sperm distribution and degredation in the human female reproductive tract. J Obstet Gynecol 1970; 35: 831–40.Google Scholar
91 Pandya, IJ, Cohen, J. The leucocytic reaction of the human uterine cervix to spermatozoa. Fertil Steril 1985; 70: 71–77.Google Scholar
92 Thompson, LA, Barratt, CLR, Bolton, AE, Cooke, ID. The effect of ovulation induction drugs on spermatozoa transport. J Reprod Fertil 1990; Abstract series 6: 37.Google Scholar
93 Thompson, LA, Tomlinson, MJ, Barratt, CLR, Bolton, AE, Cooke, ID. Positive immunoselection – a method of isolating leucocytes from leucocytic reacted cervical mucus samples. Am J Reprod Immunol 1991; 26: 58–61.Google Scholar
94 Thompson, LA, Barratt, CLR, Bolton, AE, Cooke, ID. The leucocytic reaction of the human uterine cervix. J Reprod Fertil 1990; Abstract series 5:11.Google Scholar
95 Marcus, SL. Influence on ovarian hormones on the leucocytic response to spermatozoa in the uterus of the golden hamster. Fertil Steril 1966; 17: 212–20.Google Scholar
96 Howe, GR. Leucocytic response to spermatozoa in ligated segments of the rabbit vagina, uterus and oviduct. J Reprod Fertil 1967; 13: 563–66.Google Scholar
97 Brinsfield, M, Clark, CF, Gerich, V, Hawk, H. Disappearance and phagocytosis of sperm in sheep uteri. J Anim Sci 1970; 31: 218–22.Google Scholar
98 Soupart, P. Leucocytes and sperm capacitation in the rabbit uterus. Fertil Steril 1970; 21: 724–56.Google Scholar
99 Hunter, RHF. Pre-ovulatory arrest and periovulatory redistribution of competent spermatozoa in the isthmus of the pig oviduct. J Reprod Fertil 1984; 72: 203–211.Google Scholar
100 Witkin, SS. Production of interferon gamma by lymphocytes exposed to antibody coated spermatozoa – a mechanism for sperm antibody production in females. Fertil Steril 1988; 50: 498–502.Google Scholar
101 Pockley, AG, Barratt, CLR, Bolton, AE. Placental protein 14 (PP14) content and immunosuppressive activities of human cervical mucus. Soc Exp Biol 1990; 7: 317–23.Google Scholar
102 Sinosich, MJ, Saunders, DM. Potential role of pregnancy associated plasma protein in human reproduction. J Reprod Immunol 1987; 10: 724.Google Scholar
103 Ahlgren, M. Sperm transport to and survival in the human fallopian tube. Gynecologic Investigation 1975; 6: 206–14.Google Scholar
104 Mortimer, D, Templeton, AA. Sperm transport in human female reproduction in relation to semen analysis characteristics and time of ovulation. J Reprod Fertil 1982; 64: 401–408.Google Scholar
105 Gallagher, GR, Senger, PL. Concentrations of spermatozoa in the vagina of heifers after deposition of semen in the uterine horns, uterine body or cervix. J Reprod Fertil 1989; 86: 19–25.Google Scholar
106 Smith, TT, Yanagimachi, R. Attachment and release of spermatozoa from the caudal isthmus of the hamster oviduct. J Reprod Fertil 1991; 91: 567–73.Google Scholar
107 Vogelpoel, FR, Verhoef, J. Activation of polymorphonuclear leucocytes by spermatozoa. Arch Androl 1985; 14: 123–31.Google Scholar
108 Barratt, CLR, Cooke, ID. Review – sperm transport in the human female reproductive tract – a dynamic interaction. Int J Androl 1991; 14: 394–411.Google Scholar
109 Kopf, GS, Gerton, GL. The mammalian sperm acrosome and the acrosome reaction. In: Wasserman, P ed.Elements of mammalian fertilization. New York: CRC Press, 1990: 153–203.Google Scholar
110 Cohen, J, Werrett, DJ. Antibodies and sperm survival in the female tract of the mouse and rabbit. J Reprod Fertil 1975; 39: 297–310.Google Scholar
111 Castilla, JA, Molina, R, Lopez-Novof, MA, Vergera, F, Garrido, F, Herruzo, AJ. Immunosuppressive properties of human follicular fluid. Fertil Steril 1990; 53: 271–75.Google Scholar
112 Bodel, P, Dillard, GM, Kaplan, SS, Maolwista, SE. Anti-inflammatory effects of estradiol on human blood leucocytes. J Lab Clin Med 1972; 80: 373–84.Google Scholar
113 Broome, AW, Winter, AJ, McNutt, SH, Casida, LE. Variations in uterine response to experimental infection due to hormonal state of ovaries. II. The mobilization of leucocytes and their importance in uterine bacterial activity. J Vet Res 1960; 47: 675–82.Google Scholar
114 Ho, PC, Tang, GWK, Fu, KH, Fan, MC, Lawton, JWN. Immunologie studies in patients with premature ovarian failure. Obstet Gynecol 1988; 71: 622–26.Google Scholar