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Published in: Reproductive Biology and Endocrinology 1/2013

Open Access 01-12-2013 | Research

Successful implantation after reducing matrix metalloproteinase activity in the uterine cavity

Authors: Noriko Yoshii, Toshio Hamatani, Noboru Inagaki, Takeshi Hosaka, Osamu Inoue, Mitsutoshi Yamada, Rei Machiya, Yasunori Yoshimura, Yasushi Odawara

Published in: Reproductive Biology and Endocrinology | Issue 1/2013

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Abstract

Background

Recently, the concept of recurrent implantation failure (RIF) in assisted reproductive technology has been enlarged. Chronic uterine inflammation is a known cause of implantation failure and is associated with high matrix metalloproteinase (MMP) activity in uterine cavity flushing. MMP activity of women with RIF has been reported to be higher than that of fertile women. In the present retrospective study we evaluated the efficacy of treatment for high MMP activity in the uterine cavity of patients with RIF.

Methods

Of the 597 patients recruited to the study, 360 patients underwent MMP measurements and 237 patients did not (control group). All patients had failed to become pregnant, despite at least two transfers of good-quality embryos. Gelatinase MMP-2 and MMP-9 activity in uterine flushing fluid was detected by enzymology (MMP test). All samples were classified into two groups (positive or negative) based on the intensity of the bands on the enzyme zymogram, which represents the degree of MMP activity. Patients who tested positive on the initial test were treated for 2 weeks with a quinolone antibiotic and a corticosteroid, and subsequently underwent a second MMP test. Negative results on the second MMP tests after treatment and subsequent rates of pregnancy and miscarriage were used to evaluate the efficacy of treatment. Data were analyzed by the Mann–Whitney U-test and the chi-square test.

Results

Of the patients who underwent the MMP test, 15.6% had positive results (high MMP activity). After treatment, 89.3% of patients had negative results on the second MMP test. These patients had a significantly better pregnancy rate (42.0%) than the control group (26.6%), as well as a lower miscarriage rate (28.5% vs 36.5%, respectively).

Conclusions

A 2-week course of antibiotics and corticosteroids effectively improves the uterine environment underlying RIF by reducing MMP activity.
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Literature
1.
go back to reference Lee TH, Chen CD, Tsai YY, Chang LJ, Ho HN, Yang YS: Embryo quality is more important for younger women whereas age is more important for older women with regard to in vitro fertilization outcome and multiple pregnancy. Fertil Steril. 2006, 86: 64-69.CrossRefPubMed Lee TH, Chen CD, Tsai YY, Chang LJ, Ho HN, Yang YS: Embryo quality is more important for younger women whereas age is more important for older women with regard to in vitro fertilization outcome and multiple pregnancy. Fertil Steril. 2006, 86: 64-69.CrossRefPubMed
2.
go back to reference Navot D, Bergh PA, Williams MA, Garrisi GJ, Guzman I, Sandler B, Grunfeld L: Poor oocyte quality rather than implantation failure as a cause of age-related decline in female fertility. Lancet. 1991, 337: 1375-1377.CrossRefPubMed Navot D, Bergh PA, Williams MA, Garrisi GJ, Guzman I, Sandler B, Grunfeld L: Poor oocyte quality rather than implantation failure as a cause of age-related decline in female fertility. Lancet. 1991, 337: 1375-1377.CrossRefPubMed
3.
go back to reference Déchaud H, Maudelonde T, Daurès JP, Rossi JF, Hédon B: Evaluation of endometrial inflammation by quantification of macrophages, T lymphocytes, and interleukin-1 and −6 in human endometrium. J Assist Reprod Genet. 1998, 15: 612-618.PubMedCentralCrossRefPubMed Déchaud H, Maudelonde T, Daurès JP, Rossi JF, Hédon B: Evaluation of endometrial inflammation by quantification of macrophages, T lymphocytes, and interleukin-1 and −6 in human endometrium. J Assist Reprod Genet. 1998, 15: 612-618.PubMedCentralCrossRefPubMed
4.
go back to reference Mukherjee T, Copperman AB, McCaffrey C, Cook CA, Bustillo M, Obasaju MF: Hydrosalpinx fluid has embryotoxic effects on murine embryogenesis: a case for prophylactic salpingectomy. Fertil Steril. 1996, 66: 851-853.PubMed Mukherjee T, Copperman AB, McCaffrey C, Cook CA, Bustillo M, Obasaju MF: Hydrosalpinx fluid has embryotoxic effects on murine embryogenesis: a case for prophylactic salpingectomy. Fertil Steril. 1996, 66: 851-853.PubMed
5.
go back to reference Strandell A, Waldenström U, Nilsson L, Hamberger L: Hydrosalpinx reduces in-vitro fertilization/embryo transfer pregnancy rates. Hum Reprod. 1994, 9: 861-863.PubMed Strandell A, Waldenström U, Nilsson L, Hamberger L: Hydrosalpinx reduces in-vitro fertilization/embryo transfer pregnancy rates. Hum Reprod. 1994, 9: 861-863.PubMed
6.
go back to reference Vandromme J, Chasse E, Lejeune B, Van Rysselberge M, Delvigne A, Leroy F: Hydrosalpinges in in-vitro fertilization: an unfavourable prognostic feature. Hum Reprod. 1995, 10: 576-579.PubMed Vandromme J, Chasse E, Lejeune B, Van Rysselberge M, Delvigne A, Leroy F: Hydrosalpinges in in-vitro fertilization: an unfavourable prognostic feature. Hum Reprod. 1995, 10: 576-579.PubMed
7.
go back to reference Woessner JF: Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J. 1991, 5: 2145-2154.PubMed Woessner JF: Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J. 1991, 5: 2145-2154.PubMed
8.
go back to reference Salamonsen LA, Woolley DE: Matrix metalloproteinases in normal menstruation. Hum Reprod. 1996, Suppl 2: 124-133.CrossRef Salamonsen LA, Woolley DE: Matrix metalloproteinases in normal menstruation. Hum Reprod. 1996, Suppl 2: 124-133.CrossRef
9.
go back to reference Shah BH, Catt KJ: Matrix metalloproteinases in reproductive endocrinology. Trends Endocrinol Metab. 2004, 15: 47-49.CrossRefPubMed Shah BH, Catt KJ: Matrix metalloproteinases in reproductive endocrinology. Trends Endocrinol Metab. 2004, 15: 47-49.CrossRefPubMed
10.
go back to reference Zhang J, Nie G, Jian W, Woolley DE, Salamonsen LA: Mast cell regulation of human endometrial matrix metalloproteinases: a mechanism underlying menstruation. Biol Reprod. 1998, 59: 693-703.CrossRefPubMed Zhang J, Nie G, Jian W, Woolley DE, Salamonsen LA: Mast cell regulation of human endometrial matrix metalloproteinases: a mechanism underlying menstruation. Biol Reprod. 1998, 59: 693-703.CrossRefPubMed
11.
go back to reference Huang HY, Wen Y, Irwin JC, Kruessel JS, Soong YK, Polan ML: Cytokine-mediated regulation of 92-kilodalton type IV collagenase, tissue inhibitor or metalloproteinase-1 (TIMP-1), and TIMP-3 messenger ribonucleic acid expression in human endometrial stromal cells. J Clin Endocrinol Metab. 1998, 83: 1721-1729.PubMed Huang HY, Wen Y, Irwin JC, Kruessel JS, Soong YK, Polan ML: Cytokine-mediated regulation of 92-kilodalton type IV collagenase, tissue inhibitor or metalloproteinase-1 (TIMP-1), and TIMP-3 messenger ribonucleic acid expression in human endometrial stromal cells. J Clin Endocrinol Metab. 1998, 83: 1721-1729.PubMed
12.
go back to reference Salamonsen LA, Butt AR, Hammond FR, Garcia S, Zhang J: Production of endometrial matrix metalloproteinases, but not their tissue inhibitors, is modulated by progesterone withdrawal in an in vitro model for menstruation. J Clin Endocrinol Metab. 1997, 82: 1409-1415.PubMed Salamonsen LA, Butt AR, Hammond FR, Garcia S, Zhang J: Production of endometrial matrix metalloproteinases, but not their tissue inhibitors, is modulated by progesterone withdrawal in an in vitro model for menstruation. J Clin Endocrinol Metab. 1997, 82: 1409-1415.PubMed
13.
go back to reference Liu G, Zhang X, Lin H, Wang H, Li Q, Ni J, Zhu C: Effects of E-cadherin on mouse embryo implantation and expression of matrix metalloproteinase-2 and -9. Biochem Biophys Res Commun. 2006, 343: 832-838.CrossRefPubMed Liu G, Zhang X, Lin H, Wang H, Li Q, Ni J, Zhu C: Effects of E-cadherin on mouse embryo implantation and expression of matrix metalloproteinase-2 and -9. Biochem Biophys Res Commun. 2006, 343: 832-838.CrossRefPubMed
14.
go back to reference Mulayim N, Savlu A, Guzeloglu-Kayisli O, Kayisli UA, Arici A: Regulation of endometrial stromal cell matrix metalloproteinase activity and invasiveness by interleukin-8. Fertil Steril. 2004, 81 (Suppl 1): 904-911.CrossRefPubMed Mulayim N, Savlu A, Guzeloglu-Kayisli O, Kayisli UA, Arici A: Regulation of endometrial stromal cell matrix metalloproteinase activity and invasiveness by interleukin-8. Fertil Steril. 2004, 81 (Suppl 1): 904-911.CrossRefPubMed
15.
go back to reference Inagaki N, Stern C, McBain J, Lopata A, Kornman L, Wilkinson D: Analysis of intra-uterine cytokine concentration and matrix-metalloproteinase activity in women with recurrent failed embryo transfer. Hum Reprod. 2003, 18: 608-615.CrossRefPubMed Inagaki N, Stern C, McBain J, Lopata A, Kornman L, Wilkinson D: Analysis of intra-uterine cytokine concentration and matrix-metalloproteinase activity in women with recurrent failed embryo transfer. Hum Reprod. 2003, 18: 608-615.CrossRefPubMed
17.
go back to reference Thornhill AR, deDie-Smulders CE, Geraedts JP, Harper JC, Harton GL, Lavery SA, Moutou C, Robinson MD, Schmutzler AG, Scriven PN, Sermon KD, Wilton L: ESHRE PGD consortium 'Best practice guidelines for clinical preimplantation genetic diagnosis (PGD) and preimplantation genetic screening (PGS)'. Hum Reprod. 2005, 20: 35-48.CrossRefPubMed Thornhill AR, deDie-Smulders CE, Geraedts JP, Harper JC, Harton GL, Lavery SA, Moutou C, Robinson MD, Schmutzler AG, Scriven PN, Sermon KD, Wilton L: ESHRE PGD consortium 'Best practice guidelines for clinical preimplantation genetic diagnosis (PGD) and preimplantation genetic screening (PGS)'. Hum Reprod. 2005, 20: 35-48.CrossRefPubMed
18.
go back to reference Gardner DK, Lane M, Stevens J, Schlenker T, Schoolcraft WB: Blastocyst score affects implantation and pregnancy outcome: towards a single blastocyst transfer. Fertil Steril. 2000, 73: 1155-1158.CrossRefPubMed Gardner DK, Lane M, Stevens J, Schlenker T, Schoolcraft WB: Blastocyst score affects implantation and pregnancy outcome: towards a single blastocyst transfer. Fertil Steril. 2000, 73: 1155-1158.CrossRefPubMed
19.
go back to reference Veeck L: Preembryo grading and degree of cytoplasmic fragmentation. An atlas of human gametes and conceptuses: an illustrated reference for assisted reproductive technology. Edited by: Veeck L. 1999, New York, USA: Parthenon, 46-51.CrossRef Veeck L: Preembryo grading and degree of cytoplasmic fragmentation. An atlas of human gametes and conceptuses: an illustrated reference for assisted reproductive technology. Edited by: Veeck L. 1999, New York, USA: Parthenon, 46-51.CrossRef
20.
go back to reference Inagaki N, Ung L, Otani T, Wilkinson D, Lopata A: Uterine cavity matrix metalloproteinases and cytokines in patients with leiomyoma, adenomyosis or endometrial polyp. Eur J Obstet Gynecol Reprod Biol. 2003, 111: 197-203.CrossRefPubMed Inagaki N, Ung L, Otani T, Wilkinson D, Lopata A: Uterine cavity matrix metalloproteinases and cytokines in patients with leiomyoma, adenomyosis or endometrial polyp. Eur J Obstet Gynecol Reprod Biol. 2003, 111: 197-203.CrossRefPubMed
21.
go back to reference Kleiner DE, Stetler-Stevenson WG: Quantitative zymography: detection of picogram quantities of gelatinases. Anal Biochem. 1994, 218: 325-329.CrossRefPubMed Kleiner DE, Stetler-Stevenson WG: Quantitative zymography: detection of picogram quantities of gelatinases. Anal Biochem. 1994, 218: 325-329.CrossRefPubMed
22.
go back to reference Mikolajczyk M, Wirstlein P, Skrzypczak J: Leukaemia inhibitory factor and interleukin 11 levels in uterine flushings of infertile patients with endometriosis. Hum Reprod. 2006, 21: 3054-3058.CrossRefPubMed Mikolajczyk M, Wirstlein P, Skrzypczak J: Leukaemia inhibitory factor and interleukin 11 levels in uterine flushings of infertile patients with endometriosis. Hum Reprod. 2006, 21: 3054-3058.CrossRefPubMed
23.
go back to reference Fridman R, Fuerst TR, Bird RE, Hoyhtya M, Oelkuct M, Kraus S, Komarek D, Liotta LA, Berman ML, Stetler-Stevenson WG: Domain structure of human 72-kDa gelatinase/type IV collagenase. Characterization of proteolytic activity and identification of the tissue inhibitor of metalloproteinase-2 (TIMP-2) binding regions. J Biol Chem. 1992, 267: 15398-15405.PubMed Fridman R, Fuerst TR, Bird RE, Hoyhtya M, Oelkuct M, Kraus S, Komarek D, Liotta LA, Berman ML, Stetler-Stevenson WG: Domain structure of human 72-kDa gelatinase/type IV collagenase. Characterization of proteolytic activity and identification of the tissue inhibitor of metalloproteinase-2 (TIMP-2) binding regions. J Biol Chem. 1992, 267: 15398-15405.PubMed
24.
go back to reference Lopata A, Agresta F, Quinn MA, Smith C, Ostor AG, Salamonsen LA: Detection of endometirial cancer by determination of matrix metalloproteinases in the uterine cavity. Gynecol Oncol. 2003, 90: 318-324.CrossRefPubMed Lopata A, Agresta F, Quinn MA, Smith C, Ostor AG, Salamonsen LA: Detection of endometirial cancer by determination of matrix metalloproteinases in the uterine cavity. Gynecol Oncol. 2003, 90: 318-324.CrossRefPubMed
25.
go back to reference Inoue T, Kanzaki H, Iwai M, Imai K, Narukawa S, Higuchi T, Katsuragawa H, Mori T: Tumour necrosis factor alpha inhibits in-vitro decidualization of human endometrial stromal cells. Hum Reprod. 1994, 9: 2411-2417.PubMed Inoue T, Kanzaki H, Iwai M, Imai K, Narukawa S, Higuchi T, Katsuragawa H, Mori T: Tumour necrosis factor alpha inhibits in-vitro decidualization of human endometrial stromal cells. Hum Reprod. 1994, 9: 2411-2417.PubMed
26.
go back to reference Kariya M, Kanzaki H, Takakura K, Imai K, Okamoto N, Emi N, Kariya Y, Mori T: Interleukin-1 inhibits in vitro decidualization of human endometrial stromal cells. J Clin Endocrinol Metab. 1991, 73: 1170-1174.CrossRefPubMed Kariya M, Kanzaki H, Takakura K, Imai K, Okamoto N, Emi N, Kariya Y, Mori T: Interleukin-1 inhibits in vitro decidualization of human endometrial stromal cells. J Clin Endocrinol Metab. 1991, 73: 1170-1174.CrossRefPubMed
27.
go back to reference Kojima K, Kanzaki H, Iwai M, Hatayama H, Fujimoto M, Inoue T, Horie K, Nakayama H, Fujita J, Mori T: Expression of leukemia inhibitory factor in human endometrium and placenta. Biol Reprod. 1994, 50: 882-887.CrossRefPubMed Kojima K, Kanzaki H, Iwai M, Hatayama H, Fujimoto M, Inoue T, Horie K, Nakayama H, Fujita J, Mori T: Expression of leukemia inhibitory factor in human endometrium and placenta. Biol Reprod. 1994, 50: 882-887.CrossRefPubMed
28.
go back to reference Lessey BA, Castelbaum AJ, Sawin SW, Sun J: Integrins as markers of uterine receptivity in women with primary unexplained infertility. Fertil Steril. 1995, 63: 535-542.PubMed Lessey BA, Castelbaum AJ, Sawin SW, Sun J: Integrins as markers of uterine receptivity in women with primary unexplained infertility. Fertil Steril. 1995, 63: 535-542.PubMed
29.
go back to reference Song H, Lim H, Paria BC, Matsumoto H, Swift LL, Morrow J, Bonventre JV, Dey SK: Cytosolic phospholipase A2alpha is crucial [correction of A2alpha deficiency is crucial] for 'on-time' embryo implantation that directs subsequent development. Development. 2002, 129: 2879-2889.PubMed Song H, Lim H, Paria BC, Matsumoto H, Swift LL, Morrow J, Bonventre JV, Dey SK: Cytosolic phospholipase A2alpha is crucial [correction of A2alpha deficiency is crucial] for 'on-time' embryo implantation that directs subsequent development. Development. 2002, 129: 2879-2889.PubMed
30.
go back to reference Licht P, Lösch A, Dittrich R, Neuwinger J, Siebzehnrübl E, Wildt L: Novel insights into human endometrial paracrinology and embryo-maternal communication by intrauterine microdialysis. Hum Reprod Update. 1998, 4: 532-538.CrossRefPubMed Licht P, Lösch A, Dittrich R, Neuwinger J, Siebzehnrübl E, Wildt L: Novel insights into human endometrial paracrinology and embryo-maternal communication by intrauterine microdialysis. Hum Reprod Update. 1998, 4: 532-538.CrossRefPubMed
31.
go back to reference Mikołajczyk M, Skrzypczak J, Szymanowski K, Wirstlein P: The assessment of LIF in uterine flushing–a possible new diagnostic tool in states of impaired fertility. Reprod Biol. 2003, 3: 259-270.PubMed Mikołajczyk M, Skrzypczak J, Szymanowski K, Wirstlein P: The assessment of LIF in uterine flushing–a possible new diagnostic tool in states of impaired fertility. Reprod Biol. 2003, 3: 259-270.PubMed
32.
go back to reference Nastri CO, Gibreel A, Raine-Fenning N, Maheshwari A, Ferriani RA, Bhattacharya S, Martins WP: Endometrial injury in women undergoing assisted reproductive techniques. Cochrane Database Syst Rev. 2012, 7: CD009517(1-43)- Nastri CO, Gibreel A, Raine-Fenning N, Maheshwari A, Ferriani RA, Bhattacharya S, Martins WP: Endometrial injury in women undergoing assisted reproductive techniques. Cochrane Database Syst Rev. 2012, 7: CD009517(1-43)-
33.
go back to reference Shohayeb A, El-Khayat W: Does a single endometrial biopsy regimen (S-EBR) improve ICSI outcome in patients with repeated implantation failure? a randomised controlled trial. Eur J Obstet Gynecol Reprod Biol. 2012, 164: 176-179.CrossRefPubMed Shohayeb A, El-Khayat W: Does a single endometrial biopsy regimen (S-EBR) improve ICSI outcome in patients with repeated implantation failure? a randomised controlled trial. Eur J Obstet Gynecol Reprod Biol. 2012, 164: 176-179.CrossRefPubMed
34.
go back to reference Goto S, Kadowaki T, Hashimoto H, Kokeguchi S, Shiotani M: Stimulation of endometrium embryo transfer can improve implantation and pregnancy rates for patients undergoing assisted reproductive technology for the first time with a high-grade blastocyst. Fertil Steril. 2009, 92: 1264-1268.CrossRefPubMed Goto S, Kadowaki T, Hashimoto H, Kokeguchi S, Shiotani M: Stimulation of endometrium embryo transfer can improve implantation and pregnancy rates for patients undergoing assisted reproductive technology for the first time with a high-grade blastocyst. Fertil Steril. 2009, 92: 1264-1268.CrossRefPubMed
35.
go back to reference Olivennes F, Lédée-Bataille N, Samama M, Kadoch J, Taupin JL, Dubanchet S, Chaouat G, Frydman R: Assessment of leukemia inhibitory factor levels by uterine flushing at the time of egg retrieval does not adversely affect pregnancy rates with in vitro fertilization. Fertil Steril. 2003, 79: 900-904.CrossRefPubMed Olivennes F, Lédée-Bataille N, Samama M, Kadoch J, Taupin JL, Dubanchet S, Chaouat G, Frydman R: Assessment of leukemia inhibitory factor levels by uterine flushing at the time of egg retrieval does not adversely affect pregnancy rates with in vitro fertilization. Fertil Steril. 2003, 79: 900-904.CrossRefPubMed
36.
go back to reference Berkkanoglu M, Isikoglu M, Seleker M, Ozgur K: Flushing the endometrium prior to the embryo transfer does not affect the pregnancy rate. Reprod Biomed Online. 2006, 3: 268-271.CrossRef Berkkanoglu M, Isikoglu M, Seleker M, Ozgur K: Flushing the endometrium prior to the embryo transfer does not affect the pregnancy rate. Reprod Biomed Online. 2006, 3: 268-271.CrossRef
37.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
38.
go back to reference Quenby S, Nik H, Innes B, Lash G, Turner1 M, Drury J, Bulmer J: Uterine natural killer cells and angiogenesis in recurrent reproductive failure. Hum Reprod. 2009, 24: 45-54.CrossRefPubMed Quenby S, Nik H, Innes B, Lash G, Turner1 M, Drury J, Bulmer J: Uterine natural killer cells and angiogenesis in recurrent reproductive failure. Hum Reprod. 2009, 24: 45-54.CrossRefPubMed
39.
go back to reference Check JH, Choe JK, Lee G, Dietterich C: The effect on IVF outcome of small intramural fibroids not compressing the uterine cavity as determined by a prospective matched control study. Hum Reprod. 2002, 17: 1244-1248.CrossRefPubMed Check JH, Choe JK, Lee G, Dietterich C: The effect on IVF outcome of small intramural fibroids not compressing the uterine cavity as determined by a prospective matched control study. Hum Reprod. 2002, 17: 1244-1248.CrossRefPubMed
40.
go back to reference Hart R, Khalaf Y, Yeong CT, Seed P, Taylor A, Braude P: A prospective controlled study of the effect of intramural uterine fibroids on the outcome of assisted conception. Hum Reprod. 2001, 16: 2411-2417.PubMed Hart R, Khalaf Y, Yeong CT, Seed P, Taylor A, Braude P: A prospective controlled study of the effect of intramural uterine fibroids on the outcome of assisted conception. Hum Reprod. 2001, 16: 2411-2417.PubMed
42.
go back to reference Tremellen KP, Russell P: The distribution of immune cells and macrophages in the endometrium of women with recurrent reproductive failure. II: adenomyosis and macrophages. J Reprod Immunol. 2012, 93: 58-63.CrossRefPubMed Tremellen KP, Russell P: The distribution of immune cells and macrophages in the endometrium of women with recurrent reproductive failure. II: adenomyosis and macrophages. J Reprod Immunol. 2012, 93: 58-63.CrossRefPubMed
43.
go back to reference Kitaya K: Prevalence of chronic endometritis in recurrent miscarriages. Fertil Steril. 2011, 95: 1156-1158.CrossRefPubMed Kitaya K: Prevalence of chronic endometritis in recurrent miscarriages. Fertil Steril. 2011, 95: 1156-1158.CrossRefPubMed
44.
go back to reference Romero R, Espinoza J, Mazor M: Can endometrial infection/inflammation explain implantation failure, spontaneous abortion, and preterm birth after in vitro fertilization?. Fertil Steril. 2004, 82: 799-804.CrossRefPubMed Romero R, Espinoza J, Mazor M: Can endometrial infection/inflammation explain implantation failure, spontaneous abortion, and preterm birth after in vitro fertilization?. Fertil Steril. 2004, 82: 799-804.CrossRefPubMed
45.
go back to reference Farooki MA: Epidemiology and pathology of chronic endometritis. Int Surg. 1967, 48: 566-573.PubMed Farooki MA: Epidemiology and pathology of chronic endometritis. Int Surg. 1967, 48: 566-573.PubMed
46.
go back to reference Kasius JC, Fatemi HM, Bourgain C, Sie-Go DM, Eijkemans RJ, Fauser BC, Devroey P, Broekmans FJ: The impact of chronic endometritis on reproductive outcome. Fertil Steril. 2011, 96: 1451-1456.CrossRefPubMed Kasius JC, Fatemi HM, Bourgain C, Sie-Go DM, Eijkemans RJ, Fauser BC, Devroey P, Broekmans FJ: The impact of chronic endometritis on reproductive outcome. Fertil Steril. 2011, 96: 1451-1456.CrossRefPubMed
47.
go back to reference Johnston-MacAnanny EB, Hartnett J, Engmann LL, Nulsen JC, Sanders MM, Benadiva CA: Chronic endometritis is a frequent finding in women with recurrent implantation failure after in vitro fertilization. Fertil Steril. 2010, 93: 437-441.CrossRefPubMed Johnston-MacAnanny EB, Hartnett J, Engmann LL, Nulsen JC, Sanders MM, Benadiva CA: Chronic endometritis is a frequent finding in women with recurrent implantation failure after in vitro fertilization. Fertil Steril. 2010, 93: 437-441.CrossRefPubMed
48.
go back to reference Kitaya K, Tada Y, Taguchi S, Funabiki M, Hayashi T, Nakamura Y: Local mononuclear cell infiltrates in infertile patients with endometrial macropolyps versus micropolyps. Hum Reprod. 2012, Epub ahead of print Kitaya K, Tada Y, Taguchi S, Funabiki M, Hayashi T, Nakamura Y: Local mononuclear cell infiltrates in infertile patients with endometrial macropolyps versus micropolyps. Hum Reprod. 2012, Epub ahead of print
49.
go back to reference Polisseni F, Bambirra EA, Camargos AF: Detection of chronic endometritis by diagnostic hysteroscopy in asymptomatic infertile patients. Gynecol Obstet Invest. 2003, 55: 205-210.CrossRefPubMed Polisseni F, Bambirra EA, Camargos AF: Detection of chronic endometritis by diagnostic hysteroscopy in asymptomatic infertile patients. Gynecol Obstet Invest. 2003, 55: 205-210.CrossRefPubMed
50.
go back to reference Fragouli E, Katz-Jaffe M, Alfarawati S, Stevens J, Colls P, Goodall NN, Tormasi S, Gutierrez-Mateo C, Prates R, Schoolcraft WB, Munne S, Wells D: Comprehensive chromosome screening of polar bodies and blastocysts from couples experiencing repeated implantation failure. Fertil Steril. 2010, 94: 875-887.CrossRefPubMed Fragouli E, Katz-Jaffe M, Alfarawati S, Stevens J, Colls P, Goodall NN, Tormasi S, Gutierrez-Mateo C, Prates R, Schoolcraft WB, Munne S, Wells D: Comprehensive chromosome screening of polar bodies and blastocysts from couples experiencing repeated implantation failure. Fertil Steril. 2010, 94: 875-887.CrossRefPubMed
Metadata
Title
Successful implantation after reducing matrix metalloproteinase activity in the uterine cavity
Authors
Noriko Yoshii
Toshio Hamatani
Noboru Inagaki
Takeshi Hosaka
Osamu Inoue
Mitsutoshi Yamada
Rei Machiya
Yasunori Yoshimura
Yasushi Odawara
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2013
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-11-37

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