Natural killer cells and pregnancy outcomes in women with recurrent miscarriage and infertility: A systematic review

Human Reproduction

Volumn 26, Issue 8, 2011, Pages 1971-1980

  Tang, A W ^a   Alfirevic, Z ^a   Quenby, S ^b  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

infertility; natural killer cells; pregnancy outcomes; recurrent miscarriage; systematic review

Indexed keywords

ASSISTED REPRODUCTIVE TECHNOLOGY; CELL COUNT; CELL DENSITY; FEMALE INFERTILITY; HUMAN; IDIOPATHIC DISEASE; IMPLANTATION; LIVE BIRTH; NATURAL KILLER CELL; PERIPHERAL NATURAL KILLER CELL; PREGNANCY OUTCOME; PUBLICATION; RECURRENT DISEASE; REPRODUCTIVE PROCEDURES; REVIEW; SPONTANEOUS ABORTION; SYSTEMATIC REVIEW; UTERINE NATURAL KILLER CELL;

EID: 79960530853     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/der164     Document Type: Review

References (54)

1. Aoki K, Kajiura S, Matsumoto Y, Ogasawara M, Okada S, Yagami Y, Gleicher N. Preconceptional natural-killer-cell activity as a predictor of miscarriage. Lancet 1995;345:1340-1342.
2. Baczkowski T, Kurzawa R. Immunophenotypic profiles of peripheral blood lymphocytes on the day of embryo transfer in women undergoing in vitro fertilization. Folia Histochem Cytobiol 2007;45 Suppl 1:S73-S77.
3. Beer AE, Kwak JY, Ruiz JE. Immunophenotypic profiles of peripheral blood lymphocytes in women with recurrent pregnancy losses and in infertile women with multiple failed in vitro fertilization cycles. Am J Reprod Immunol 1996;35:376-382. (Pubitemid 26131083)
4. Benschop R, Geenen R, Mills P, Naliboff B, Kiecolt-Glaser J, Herbert T, Van Der Pompe G, Miller G, Matthews K, Godaert G et al. Cardiovascular and immune responses to acute psychological stress in young and old women: a meta-analysis. Psychosom Med 1998; 60:290-296. (Pubitemid 28279973)
5. Bulmer JN, Lash GE. Human uterine natural killer cells: a reappraisal. [Review] [101 refs]. Mol Immunol 2005;42:511-521. (Pubitemid 39655962)
6. Bulmer JN, Morrison L, Longfellow M, Ritson A, Pace D. Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Hum Reprod 1991;6:791-798.
7. Clifford K, Flanagan AM, Regan L. Endometrial CD56+ natural killer cells in women with recurrent miscarriage: a histomorphometric study. Hum Reprod 1999;14:2727-2730. (Pubitemid 29520681)
8. Coulam CB, Goodman C, Roussev RG, Thomason EJ, Beaman KD. Systemic CD56+ cells can predict pregnancy outcome. Am J Reprod Immunol 1995;33:40-46.
9. Dosiou C, Giudice LC. Natural killer cells in pregnancy and recurrent pregnancy loss: endocrine and immunologic perspectives. Endocr Rev 2005;26:44-62. (Pubitemid 40209386)
10. Emmer PM, Veerhoek M, Nelen WL, Steegers EA, Joosten I. Natural killer cell reactivity and HLA-G in recurrent spontaneous abortion. Transplant Proc 1999;31:1838-1840. (Pubitemid 29275477)
11. Emmer PM, Nelen WL, Steegers EA, Hendriks JC, Veerhoek M, Joosten I. Peripheral natural killer cytotoxicity and CD56(pos)CD16(pos) cells increase during early pregnancy in women with a history of recurrent spontaneous abortion. Hum Reprod 2000;15:1163-1169. (Pubitemid 30251319)
12. Farquharson RG, Jauniaux E, Exalto N. Updated and revised nomenclature for description of early pregnancy events. Hum Reprod 2005; 20:3008-3011. (Pubitemid 41662648)
13. Fukui A, Fujii S, Yamaguchi E, Kimura H, Sato S, Saito Y. Natural killer cell subpopulations and cytotoxicity for infertile patients undergoing in vitro fertilization. Am J Reprod Immunol 1999;41:413-422. (Pubitemid 29373985)
14. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, Prus D, Cohen-Daniel L, Arnon TI, Manaster I et al. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 2006;12:1065-1074. (Pubitemid 44353388)
15. Hiby SE, Apps R, Sharkey AM, Farrell LE, Gardner L, Mulder A, Claas FH, Walker JJ, Redman CW, Morgan L et al. Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2. J Clin Invest 2010;120:4102-4110.
16. Kalkunte SS, Mselle TF, Norris WE, Wira CR, Sentman CL, Sharma S. Vascular endothelial growth factor C facilitates immune tolerance and endovascular activity of human uterine NK cells at the maternal-fetal interface. J Immunol 2009;182:4085-4092.
17. King A, Balendran N, Wooding P, Carter NP, Loke YW. CD32 leukocytes present in the human uterus during early placentation: phenotypic and morphologic characterization of the CD56++ population. Dev Immunol1991;1:169- 190.
18. Kitaya K, Yamaguchi T, Yasuo T, Okubo T, Honjo H. Post-ovulatory rise of endometrial CD16(2) natural killer cells: in situ proliferation of residual cells or selective recruitment from circulating peripheral blood? J Reprod Immunol 2007;76:45-53. (Pubitemid 350100877)
19. Kwak JY, Beaman KD, Gilman-Sachs A, Ruiz JE, Schewitz D, Beer AE. Up-regulated expression of CD56+, CD56+/CD16+, and CD19+ cells in peripheral blood lymphocytes in pregnant women with recurrent pregnancy losses. Am J Reprod Immunol 1995;34:93-99.
20. Lachapelle MH, Miron P, Hemmings R, Roy DC. Endometrial T, B, and NK cells in patients with recurrent spontaneous abortion. Altered profile and pregnancy outcome. J Immunol 1996;156:4027-4034. (Pubitemid 26137691)
21. Ledee-Bataille N, Dubanchet S, Kadoch J, Castelo-Branco A, Frydman R, Chaouat G. Controlled natural in vitro fertilization may be an alternative for patients with repeated unexplained implantation failure and a high uterine natural killer cell count. Fertil Steril 2004;82:234-236. (Pubitemid 38976493)
22. Ledee-Bataille N, Bonnet-Chea K, Hosny G, Dubanchet S, Frydman R, Chaouat G. Role of the endometrial tripod interleukin-18, -15, and -12 in inadequate uterine receptivity in patients with a history of repeated in vitro fertilization-embryo transfer failure. Fertil Steril 2005; 83:598-605. (Pubitemid 40348570)
23. Matsubayashi H, Hosaka T, Sugiyama Y, Suzuki T, Arai T, Kondo A, Sugi T, Izumi S, Makino T. Increased natural killer-cell activity is associated with infertile women. Am J Reprod Immunol 2001;46:318-322. (Pubitemid 33034814)
24. Matsubayashi H, Shida M, Kondo A, Suzuki T, Sugi T, Izumi S, Hosaka T, Makino T. Preconception peripheral natural killer cell activity as a predictor of pregnancy outcome in patients with unexplained infertility. Am J Reprod Immunol 2005;53:126-131. (Pubitemid 40352721)
25. Matteo MG, Greco P, Rosenberg P, Mestice A, Baldini D, Falagario T, Martino V, Santodirocco M, Massenzio F, Castellana L et al. Normal percentage of CD56bright natural killer cells in young patients with a history of repeated unexplained implantation failure after in vitro fertilization cycles. Fertil Steril 2007;88:990-993. (Pubitemid 47505239)
26. Michimata T, Ogasawara MS, Tsuda H, Suzumori K, Aoki K, Sakai M, Fujimura M, Nagata K, Nakamura M, Saito S. Distributions of endometrial NK cells, B cells, T cells, and Th2/Tc2 cells fail to predict pregnancy outcome following recurrent abortion. Am J Reprod Immunol 2002;47:196-202. (Pubitemid 34436209)
27. Michou VI, Kanavaros P, Athanassiou V, Chronis GB, Stabamas S, Tsilivakos V. Fraction of the peripheral blood concentration of CD56+/CD162/CD32 cells in total natural killer cells as an indication of fertility and infertility. Fertil Steril 2003;80:691-697. (Pubitemid 37152381)
28. Moffett-King A. Natural killer cells and pregnancy. Nat Rev Immunol 2002; 2:656-663. (Pubitemid 37328723)
29. Morikawa M, Yamada H, Kato EH, Shimada S, Ebina Y, Yamada T, Sagawa T, Kobashi G, Fujimoto S. NK cell activity and subsets in women with a history of spontaneous abortion. Cause, number of abortions, and subsequent pregnancy outcome. Gynecol Obstet Invest 2001a;52:163-167. (Pubitemid 34701706)
30. Morikawa M, Yamada H, Kato EH, Shimada S, Kishi T, Yamada T, Kobashi G, Fujimoto S. Massive intravenous immunoglobulin treatment in women with four or more recurrent spontaneous abortions of unexplained etiology: down-regulation of NK cell activity and subsets. Am J Reprod Immunol 2001b;46:399-404. (Pubitemid 33138339)
31. Nagler A, Lanier LL, Cwirla S, Phillips JH. Comparative studies of human FcRIII-positive and negative natural killer cells. J Immunol 1989; 143:3183-3191. (Pubitemid 20010143)
32. Ntrivalas EI, Kwak-Kim JY, Gilman-Sachs A, Chung-Bang H, Ng SC, Beaman KD, Mantouvalos HP, Beer AE. Status of peripheral blood natural killer cells in women with recurrent spontaneous abortions and infertility of unknown aetiology. Hum Reprod 2001;16:855-861. (Pubitemid 32451817)
33. Pantazi A, Tzonis P, Perros G, Graphou O, Keramitsoglou T, Koussoulakos S, Margaritis L, Varla-Leftherioti M. Comparative analysis of peripheral natural killer cells in the two phases of the ovarian cycle. Am J Reprod Immunol 2010;63:46-53.
34. Porter TF, Lacoursiere Y, Scott JR. Immunotherapy for recurrent miscarriage. Cochrane Database Syst Rev 2006;CD000112.
35. Putowski L, Darmochwal-Kolarz D, Rolinski J, Oleszczuk J, Jakowicki J. The immunological profile of infertile women after repeated IVF failure (preliminary study). Eur J Obstet Gynecol Reprod Biol 2004;112:192-196. (Pubitemid 38117339)
36. Quack KC, Vassiliadou N, Pudney J, Anderson DJ, Hill JA. Leukocyte activation in the decidua of chromosomally normal and abnormal fetuses from women with recurrent abortion. Hum Reprod 2001; 16:949-955. (Pubitemid 32451832)
37. Quenby S, Bates M, Doig T, Brewster J, Lewis-Jones DI, Johnson PM, Vince G. Pre-implantation endometrial leukocytes in women with recurrent miscarriage. Hum Reprod 1999;14:2386-2391. (Pubitemid 29425436)
38. Quenby S, Kalumbi C, Bates M, Farquharson R, Vince G. Prednisolone reduces preconceptual endometrial natural killer cells in women with recurrent miscarriage. Fertil Steril 2005;84:980-984. (Pubitemid 41417735)
39. Quenby S, Nik H, Innes B, Lash G, Turner M, Drury J, Bulmer J. Uterine natural killer cells and angiogenesis in recurrent reproductive failure. Hum Reprod 2009;24:45-54.
40. Shakhar K, Ben-Eliyahu S, Loewenthal R, Rosenne E, Carp H. Differences in number and activity of peripheral natural killer cells in primary versus secondary recurrent miscarriage. Fertil Steril 2003;80:368-375. (Pubitemid 36959796)
41. Shakhar K, Rosenne E, Loewenthal R, Shakhar G, Carp H, Shamgar B.-E. High NK cell activity in recurrent miscarriage: what are we really measuring? Hum Reprod 2006;21:2421-2425. (Pubitemid 44530622)
42. Shimada S, Kato EH, Morikawa M, Iwabuchi K, Nishida R, Kishi R, Onoe K, Minakami H, Yamada H. No difference in natural killer or natural killer T-cell population, but aberrant T-helper cell population in the endometrium of women with repeated miscarriage. Hum Reprod 2004;19:1018-1024. (Pubitemid 38456073)
43. Souza SS, Ferriani RA, Santos CM, Voltarelli JC. Immunological evaluation of patients with recurrent abortion. J Reprod Immunol 2002;56:111-121. (Pubitemid 34754359)
44. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. J Am Med Assoc 2000;283:2008-2012. (Pubitemid 30214957)
45. Thum MY, Bhaskaran S, Abdalla HI, Ford B, Sumar N, Shehata H, Bansal AS. An increase in the absolute count of CD56dimCD16+CD69+ NK cells in the peripheral blood is associated with a poorer IVF treatment and pregnancy outcome. Hum Reprod 2004;19:2395-2400. (Pubitemid 39406706)
46. Thum MY, Bhaskaran S, Bansal AS, Shehata H, Ford B, Sumar N, Abdalla HI. Simple enumerations of peripheral blood natural killer (CD56+ NK) cells, B cells and T cells have no predictive value in IVF treatment outcome. Hum Reprod 2005;20:1272-1276. (Pubitemid 40790252)
47. Thum MY, Abdalla HI, Bhaskaran S, Harden EL, Ford B, Sumar N, Shehata H, Bansal A. The relationship of systemic TNF-alpha and IFN-gamma with IVF treatment outcome and peripheral blood NK cells. Am J Reprod Immunol 2007;57:210-217. (Pubitemid 46231938)
48. Thum MY, Bhaskaran S, Abdalla HI, Ford B, Sumar N, Bansal A. Prednisolone suppresses NK cell cytotoxicity in vitro in women with a history of infertility and elevated NK cell cytotoxicity. Am J Reprod Immunol 2008;59:259-265. (Pubitemid 351250426)
49. Timmons BW, Cieslak T. Human natural killer cell subsets and acute exercise: a brief review. Exerc Immunol Rev 2008;14:8-23.
50. Tuckerman E, Laird SM, Prakash A, Li TC. Prognostic value of the measurement of uterine natural killer cells in the endometrium of women with recurrent miscarriage. Hum Reprod 2007; 22:2208-2213. (Pubitemid 47241868)
51. Vujisic S, Lepej SZ, Aksamija A, Jerkovic L, Sokolic B, Kupesic S, Vince A. B- and T-cells in the follicular fluid and peripheral blood of patients undergoing IVF/ET procedures. Am J Reprod Immunol 2004; 52:379-385. (Pubitemid 40068858)
52. Wang Q, Li TC, Wu YP, Cocksedge KA, Fu YS, Kong QY, Yao SZ. Reappraisal of peripheral NK cells in women with recurrent miscarriage. Reprod Biomed Online 2008;17:814-819.
53. Yamada H, Kato EH, Kobashi G, Ebina Y, Shimada S, Morikawa M, Sakuragi N, Fujimoto S. High NK cell activity in early pregnancy correlates with subsequent abortion with normal chromosomes in women with recurrent abortion. Am J Reprod Immunol 2001; 46:132-136. (Pubitemid 32691195)
54. Yamada H, Morikawa M, Kato EH, Shimada S, Kobashi G, Minakami H. Pre-conceptional natural killer cell activity and percentage as predictors of biochemical pregnancy and spontaneous abortion with normal chromosome karyotype. Am J Reprod Immunol 2003; 50:351-354. (Pubitemid 37203580)