Association between factor I fibrinogen (rs6050) and factor XI plasma thromboplastin (rs4253417) genetic polymorphisms and recurrent spontaneous miscarriage in Saudi women

Aaishah M. Kaabi; Afrah F. Alkhuriji; Zeneb A. Babay; Ibrahim A. Barakat; Abdullah M. Kaabi; Reem M. Kaabi

doi:10.15537/smj.2025.46.2.20240692

References

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1. Atik RB,
2. Christiansen OB,
3. Elson J,
4. Kolte AM,
5. Lewis S, et al.
ESHRE Guideline Group on RPL, Atik RB, Christiansen OB, Elson J, Kolte AM, Lewis S, et al. ESHRE guideline: recurrent pregnancy loss: an update in 2022. Hum Reprod Open 2023; 1: 2023 hoad002.
2.↵
1. Fainboim L,
2. Belén S,
3. González V,
4. Fernández P
. Evaluation of paternal lymphocyte immunotherapy and potential biomarker mixed lymphocyte reaction‐blocking factor in an Argentinian cohort of women with unexplained recurrent spontaneous abortion and unexplained infertility. Am J Reprod Immunol 2021; 86: e13422.
OpenUrl PubMed
3.↵
1. Chester MR,
2. Tirlapur A,
3. Jayaprakasan K
. Current management of recurrent pregnancy loss. Obstet Gynaecol 2022; 24: 260-271.
OpenUrl
4.↵
1. Quenby S,
2. Gallos ID,
3. Dhillon-Smith RK,
4. Podesek M,
5. Stephenson MD,
6. Fisher J, et al.
Miscarriage matters: the epidemiological, physical, psychological, and economic costs of early pregnancy loss. Lancet 2021; 397: 1658-1667.
OpenUrl CrossRef PubMed
5.↵
1. Guo H,
2. Gao H,
3. Li J,
4. Cong Y,
5. Chen Q,
6. Wang Y, et al.
Impacts of medroxyprogesterone acetate on oocytes and embryos: matched case-control study in women with stage III–IV ovarian endometriosis undergoing controlled ovarian hyperstimulation for in vitro fertilization. Ann Transl Med 2020; 8: 377.
OpenUrl PubMed
6.
1. Zhou WJ,
2. Yang HL,
3. Mei J,
4. Chang KK,
5. Lu H,
6. Lai ZZ, et al.
Fructose-1, 6-bisphosphate prevents pregnancy loss by inducing decidual COX-2+ macrophage differentiation. Sci Adv 2022; 8: eabj2488.
OpenUrl PubMed
7.
1. Dimakou DB,
2. Tamblyn J,
3. Justin C,
4. Coomarasamy A,
5. Richter A
. Diagnosis and management of idiopathic recurrent pregnancy loss (RPL): current immune testing and immunomodulatory treatment practice in the United Kingdom. J Reprod Immunol 2022; 153: 103662.
OpenUrl PubMed
8.↵
1. García-Chávez J,
2. Majluf-Cruz A
. Acquired hemophilia. Gac Med Mex 2020; 156: 67-77.
OpenUrl PubMed
9.↵
1. Sultana S,
2. Nallari P,
3. Ananthapur V
. Recurrent pregnancy loss (RPL): an overview. J Womens Health Dev 2020; 3: 302-315.
OpenUrl
10.↵
1. Voicu DI,
2. Munteanu O,
3. Gherghiceanu F,
4. Arsene LV,
5. Bohiltea RE,
6. Gradinaru DM, et al.
Maternal inherited thrombophilia and pregnancy outcomes. Exp Ther Med 2020; 20: 2411-2414.
OpenUrl PubMed
11.↵
1. Gobjila C,
2. Craina ML,
3. Toader DO,
4. Petre I,
5. Andor CB,
6. Tudor A. et al.
Pro-inflammatoru cytokines (IL6, IL8 and TNF-α) in the evaluation of ivarian endometriosis cyst. Rev Chim 2019; 70: 2944-2847
OpenUrl
12.↵
1. Ashorobi D,
2. Ameer MA,
3. Fernandez R
. Thrombosis. In StatPearls. Treasure Island (FL): StatPearls Publishing; 2019.
13.↵
1. Bauer AT,
2. Gorzelanny C,
3. Gebhardt C,
4. Pantel K,
5. Schneider SW
. Interplay between coagulation and inflammation in cancer: Limitations and therapeutic opportunities. Cancer Treat Rev 2022; 102: 102322.
OpenUrl PubMed
14.↵
1. Branch DW
. What’s new in obstetric antiphospholipid syndrome. Hematology Am Soc Hematol Educ Program 2019; 2019: 421-425.
OpenUrl PubMed
15.↵
1. Liu X,
2. Chen Y,
3. Ye C,
4. Xing D,
5. Wu R,
6. Li F, et al.
Hereditary thrombophilia and recurrent pregnancy loss: a systematic review and meta-analysis. Hum Reprod 2021; 36: 1213-1229.
OpenUrl PubMed
16.↵
1. Litvinov R,
2. Pieters M,
3. de Lange-Loots Z,
4. Weisel J
. Fibrinogen and fibrin. Subcell Biochem 2021; 96: 471-501.
OpenUrl CrossRef PubMed
17.↵
1. Vilar R,
2. Fish RJ,
3. Casini A,
4. Neerman-Arbez M
, Fibrin(ogen) in human disease: both friend and foe. Haematologica 202; 105: 284-296.
18.↵
1. Okumura A,
2. Tanaka H,
3. Tanaka K,
4. Katsuragi S,
5. Kamimoto Y,
6. Ikeda T
. Retrospective study of pregnancies in women with Thr331Ala fibrinogen polymorphisms. J Matern Fetal Neonatal Med 2020; 33: 3894-3899.
OpenUrl PubMed
19.↵
1. Presky KO,
2. Kadir RA
. Women with inherited bleeding disorders–Challenges and strategies for improved care. Thromb Res 2020; 196: 569-578.
OpenUrl PubMed
20.↵
1. Zhang Y,
2. Zuo X,
3. Teng Y
. Women with congenital hypofibrinogenemia/afibrinogenemia: from birth to death. Clin Appl Thromb Hemost 2020; 26: 1076029620912819.
OpenUrl PubMed
21.↵
1. Cimsir MT,
2. Yildiz MS
. Could fibrinogen to albumin ratio be a predictive marker for recurrent pregnancy loss. Int J Clin Pract 2021; 75: e14520.
OpenUrl PubMed
22.↵
1. Fredenburgh JC,
2. Weitz JI
. Factor XI as a target for new anticoagulants. Hamostaseologie 2021; 41: 104-110.
OpenUrl PubMed
23.↵
1. Somers EC
. Pregnancy and autoimmune diseases. Best Pract Res Clin Obstet Gynaecol 2020; 64: 3-10.
OpenUrl
24.↵
1. Rietveld I,
2. Lijfering W,
3. le Cessie S,
4. Bos M,
5. Rosendaal F,
6. Reitsma P, et al.
High levels of coagulation factors and venous thrombosis risk: strongest association for factor VIII and von Willebrand factor. J Thromb Haemost 2019; 17: 99-109.
OpenUrl PubMed
25.↵
1. Sokol J,
2. Biringer K,
3. Skerenova M,
4. Stasko J,
5. Kubisz P
. Activity of coagulation Factor XI in patients with spontaneous miscarriage: the presence of risk alleles. J Obstet Gynaecol 2015; 35: 621-624.
OpenUrl PubMed
26.↵
1. Khorshidi F,
2. Hajizadeh S,
3. Choobineh H,
4. Alizadeh S,
5. Sharifi M,
6. Kavosh Z, et al.
Determining the association of thrombophilic gene polymorphisms with recurrent pregnancy loss in Iranian women. Gynecol Endocrinol 2020; 36: 1082-1085.
OpenUrl PubMed
27.↵
1. Althubyani SA,
2. Alkhuriji AF,
3. Al Omar SY,
4. El-Khadragy MF
. A preliminary study of cytokine gene polymorphism effects on Saudi patients with colorectal cancer. Saudi Med J 2020; 41: 1292-1300.
OpenUrl Abstract/FREE Full Text
28.↵
1. Kavosh Z,
2. Mohammadzadeh Z,
3. Alizadeh S,
4. Sharifi MJ,
5. Hajizadeh S,
6. Choobineh H, et al.
Factor VII R353Q (rs6046), FGA A6534G (rs6050), and FGG C10034T (rs2066865) gene polymorphisms and risk of recurrent pregnancy loss in Iranian women. Indian J Hematol Blood Transfus 2024; 40: 297-302.
OpenUrl PubMed
29.↵
1. Isazadeh A,
2. Hajazimian S,
3. Rahmani SA,
4. Mohammadoo-Khorasani M,
5. Moghtaran N,
6. Fathi Maroufi NF
. The effect of Factor-XI (rs3756008) polymorphism on recurrent pregnancy loss in Iranian Azeri women. Gene Cell Tissue 2016; 4: e13330.
OpenUrl
30.↵
1. Mohamed EI,
2. Merghani MM,
3. Babiker NE
. Estimation of fibrinogen level among Sudanese women with recurrent miscarriage. J Drug Deliv Ther 2021; 11; 140-144.
OpenUrl

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Keywords

[1] 1.↵
Atik RB,
Christiansen OB,
Elson J,
Kolte AM,
Lewis S, et al.
ESHRE Guideline Group on RPL, Atik RB, Christiansen OB, Elson J, Kolte AM, Lewis S, et al. ESHRE guideline: recurrent pregnancy loss: an update in 2022. Hum Reprod Open 2023; 1: 2023 hoad002.

[2] Atik RB,

[3] Christiansen OB,

[4] Elson J,

[5] Kolte AM,

[6] Lewis S, et al.

[7] 2.↵
Fainboim L,
Belén S,
González V,
Fernández P
. Evaluation of paternal lymphocyte immunotherapy and potential biomarker mixed lymphocyte reaction‐blocking factor in an Argentinian cohort of women with unexplained recurrent spontaneous abortion and unexplained infertility. Am J Reprod Immunol 2021; 86: e13422.
OpenUrl PubMed

[8] Fainboim L,

[9] Belén S,

[10] González V,

[11] Fernández P

[12] 3.↵
Chester MR,
Tirlapur A,
Jayaprakasan K
. Current management of recurrent pregnancy loss. Obstet Gynaecol 2022; 24: 260-271.
OpenUrl

[13] Chester MR,

[14] Tirlapur A,

[15] Jayaprakasan K

[16] 4.↵
Quenby S,
Gallos ID,
Dhillon-Smith RK,
Podesek M,
Stephenson MD,
Fisher J, et al.
Miscarriage matters: the epidemiological, physical, psychological, and economic costs of early pregnancy loss. Lancet 2021; 397: 1658-1667.
OpenUrl CrossRef PubMed

[17] Quenby S,

[18] Gallos ID,

[19] Dhillon-Smith RK,

[20] Podesek M,

[21] Stephenson MD,

[22] Fisher J, et al.

[23] 5.↵
Guo H,
Gao H,
Li J,
Cong Y,
Chen Q,
Wang Y, et al.
Impacts of medroxyprogesterone acetate on oocytes and embryos: matched case-control study in women with stage III–IV ovarian endometriosis undergoing controlled ovarian hyperstimulation for in vitro fertilization. Ann Transl Med 2020; 8: 377.
OpenUrl PubMed

[24] Guo H,

[25] Gao H,

[26] Li J,

[27] Cong Y,

[28] Chen Q,

[29] Wang Y, et al.

[30] 6.
Zhou WJ,
Yang HL,
Mei J,
Chang KK,
Lu H,
Lai ZZ, et al.
Fructose-1, 6-bisphosphate prevents pregnancy loss by inducing decidual COX-2+ macrophage differentiation. Sci Adv 2022; 8: eabj2488.
OpenUrl PubMed

[31] Zhou WJ,

[32] Yang HL,

[33] Mei J,

[34] Chang KK,

[35] Lu H,

[36] Lai ZZ, et al.

[37] 7.
Dimakou DB,
Tamblyn J,
Justin C,
Coomarasamy A,
Richter A
. Diagnosis and management of idiopathic recurrent pregnancy loss (RPL): current immune testing and immunomodulatory treatment practice in the United Kingdom. J Reprod Immunol 2022; 153: 103662.
OpenUrl PubMed

[38] Dimakou DB,

[39] Tamblyn J,

[40] Justin C,

[41] Coomarasamy A,

[42] Richter A

[43] 8.↵
García-Chávez J,
Majluf-Cruz A
. Acquired hemophilia. Gac Med Mex 2020; 156: 67-77.
OpenUrl PubMed

[44] García-Chávez J,

[45] Majluf-Cruz A

[46] 9.↵
Sultana S,
Nallari P,
Ananthapur V
. Recurrent pregnancy loss (RPL): an overview. J Womens Health Dev 2020; 3: 302-315.
OpenUrl

[47] Sultana S,

[48] Nallari P,

[49] Ananthapur V

[50] 10.↵
Voicu DI,
Munteanu O,
Gherghiceanu F,
Arsene LV,
Bohiltea RE,
Gradinaru DM, et al.
Maternal inherited thrombophilia and pregnancy outcomes. Exp Ther Med 2020; 20: 2411-2414.
OpenUrl PubMed

[51] Voicu DI,

[52] Munteanu O,

[53] Gherghiceanu F,

[54] Arsene LV,

[55] Bohiltea RE,

[56] Gradinaru DM, et al.

[57] 11.↵
Gobjila C,
Craina ML,
Toader DO,
Petre I,
Andor CB,
Tudor A. et al.
Pro-inflammatoru cytokines (IL6, IL8 and TNF-α) in the evaluation of ivarian endometriosis cyst. Rev Chim 2019; 70: 2944-2847
OpenUrl

[58] Gobjila C,

[59] Craina ML,

[60] Toader DO,

[61] Petre I,

[62] Andor CB,

[63] Tudor A. et al.

[64] 12.↵
Ashorobi D,
Ameer MA,
Fernandez R
. Thrombosis. In StatPearls. Treasure Island (FL): StatPearls Publishing; 2019.

[65] Ashorobi D,

[66] Ameer MA,

[67] Fernandez R

[68] 13.↵
Bauer AT,
Gorzelanny C,
Gebhardt C,
Pantel K,
Schneider SW
. Interplay between coagulation and inflammation in cancer: Limitations and therapeutic opportunities. Cancer Treat Rev 2022; 102: 102322.
OpenUrl PubMed

[69] Bauer AT,

[70] Gorzelanny C,

[71] Gebhardt C,

[72] Pantel K,

[73] Schneider SW

[74] 14.↵
Branch DW
. What’s new in obstetric antiphospholipid syndrome. Hematology Am Soc Hematol Educ Program 2019; 2019: 421-425.
OpenUrl PubMed

[75] Branch DW

[76] 15.↵
Liu X,
Chen Y,
Ye C,
Xing D,
Wu R,
Li F, et al.
Hereditary thrombophilia and recurrent pregnancy loss: a systematic review and meta-analysis. Hum Reprod 2021; 36: 1213-1229.
OpenUrl PubMed

[77] Liu X,

[78] Chen Y,

[79] Ye C,

[80] Xing D,

[81] Wu R,

[82] Li F, et al.

[83] 16.↵
Litvinov R,
Pieters M,
de Lange-Loots Z,
Weisel J
. Fibrinogen and fibrin. Subcell Biochem 2021; 96: 471-501.
OpenUrl CrossRef PubMed

[84] Litvinov R,

[85] Pieters M,

[86] de Lange-Loots Z,

[87] Weisel J

[88] 17.↵
Vilar R,
Fish RJ,
Casini A,
Neerman-Arbez M
, Fibrin(ogen) in human disease: both friend and foe. Haematologica 202; 105: 284-296.

[89] Vilar R,

[90] Fish RJ,

[91] Casini A,

[92] Neerman-Arbez M

[93] 18.↵
Okumura A,
Tanaka H,
Tanaka K,
Katsuragi S,
Kamimoto Y,
Ikeda T
. Retrospective study of pregnancies in women with Thr331Ala fibrinogen polymorphisms. J Matern Fetal Neonatal Med 2020; 33: 3894-3899.
OpenUrl PubMed

[94] Okumura A,

[95] Tanaka H,

[96] Tanaka K,

[97] Katsuragi S,

[98] Kamimoto Y,

[99] Ikeda T

[100] 19.↵
Presky KO,
Kadir RA
. Women with inherited bleeding disorders–Challenges and strategies for improved care. Thromb Res 2020; 196: 569-578.
OpenUrl PubMed

[101] Presky KO,

[102] Kadir RA

[103] 20.↵
Zhang Y,
Zuo X,
Teng Y
. Women with congenital hypofibrinogenemia/afibrinogenemia: from birth to death. Clin Appl Thromb Hemost 2020; 26: 1076029620912819.
OpenUrl PubMed

[104] Zhang Y,

[105] Zuo X,

[106] Teng Y

[107] 21.↵
Cimsir MT,
Yildiz MS
. Could fibrinogen to albumin ratio be a predictive marker for recurrent pregnancy loss. Int J Clin Pract 2021; 75: e14520.
OpenUrl PubMed

[108] Cimsir MT,

[109] Yildiz MS

[110] 22.↵
Fredenburgh JC,
Weitz JI
. Factor XI as a target for new anticoagulants. Hamostaseologie 2021; 41: 104-110.
OpenUrl PubMed

[111] Fredenburgh JC,

[112] Weitz JI

[113] 23.↵
Somers EC
. Pregnancy and autoimmune diseases. Best Pract Res Clin Obstet Gynaecol 2020; 64: 3-10.
OpenUrl

[114] Somers EC

[115] 24.↵
Rietveld I,
Lijfering W,
le Cessie S,
Bos M,
Rosendaal F,
Reitsma P, et al.
High levels of coagulation factors and venous thrombosis risk: strongest association for factor VIII and von Willebrand factor. J Thromb Haemost 2019; 17: 99-109.
OpenUrl PubMed

[116] Rietveld I,

[117] Lijfering W,

[118] le Cessie S,

[119] Bos M,

[120] Rosendaal F,

[121] Reitsma P, et al.

[122] 25.↵
Sokol J,
Biringer K,
Skerenova M,
Stasko J,
Kubisz P
. Activity of coagulation Factor XI in patients with spontaneous miscarriage: the presence of risk alleles. J Obstet Gynaecol 2015; 35: 621-624.
OpenUrl PubMed

[123] Sokol J,

[124] Biringer K,

[125] Skerenova M,

[126] Stasko J,

[127] Kubisz P

[128] 26.↵
Khorshidi F,
Hajizadeh S,
Choobineh H,
Alizadeh S,
Sharifi M,
Kavosh Z, et al.
Determining the association of thrombophilic gene polymorphisms with recurrent pregnancy loss in Iranian women. Gynecol Endocrinol 2020; 36: 1082-1085.
OpenUrl PubMed

[129] Khorshidi F,

[130] Hajizadeh S,

[131] Choobineh H,

[132] Alizadeh S,

[133] Sharifi M,

[134] Kavosh Z, et al.

[135] 27.↵
Althubyani SA,
Alkhuriji AF,
Al Omar SY,
El-Khadragy MF
. A preliminary study of cytokine gene polymorphism effects on Saudi patients with colorectal cancer. Saudi Med J 2020; 41: 1292-1300.
OpenUrl Abstract/FREE Full Text

[136] Althubyani SA,

[137] Alkhuriji AF,

[138] Al Omar SY,

[139] El-Khadragy MF

[140] 28.↵
Kavosh Z,
Mohammadzadeh Z,
Alizadeh S,
Sharifi MJ,
Hajizadeh S,
Choobineh H, et al.
Factor VII R353Q (rs6046), FGA A6534G (rs6050), and FGG C10034T (rs2066865) gene polymorphisms and risk of recurrent pregnancy loss in Iranian women. Indian J Hematol Blood Transfus 2024; 40: 297-302.
OpenUrl PubMed

[141] Kavosh Z,

[142] Mohammadzadeh Z,

[143] Alizadeh S,

[144] Sharifi MJ,

[145] Hajizadeh S,

[146] Choobineh H, et al.

[147] 29.↵
Isazadeh A,
Hajazimian S,
Rahmani SA,
Mohammadoo-Khorasani M,
Moghtaran N,
Fathi Maroufi NF
. The effect of Factor-XI (rs3756008) polymorphism on recurrent pregnancy loss in Iranian Azeri women. Gene Cell Tissue 2016; 4: e13330.
OpenUrl

[148] Isazadeh A,

[149] Hajazimian S,

[150] Rahmani SA,

[151] Mohammadoo-Khorasani M,

[152] Moghtaran N,

[153] Fathi Maroufi NF

[154] 30.↵
Mohamed EI,
Merghani MM,
Babiker NE
. Estimation of fibrinogen level among Sudanese women with recurrent miscarriage. J Drug Deliv Ther 2021; 11; 140-144.
OpenUrl

[155] Mohamed EI,

[156] Merghani MM,

[157] Babiker NE

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Association between factor I fibrinogen (rs6050) and factor XI plasma thromboplastin (rs4253417) genetic polymorphisms and recurrent spontaneous miscarriage in Saudi women

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Association between factor I fibrinogen (rs6050) and factor XI plasma thromboplastin (rs4253417) genetic polymorphisms and recurrent spontaneous miscarriage in Saudi women

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