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Published in: Reproductive Biology and Endocrinology 1/2017

Open Access 01-12-2017 | Research

Serum periostin levels in early in pregnancy are significantly altered in women with miscarriage

Authors: A. Freis, J. Schlegel, R. J. Kuon, A. Doster, J. Jauckus, T. Strowitzki, A. Germeyer

Published in: Reproductive Biology and Endocrinology | Issue 1/2017

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Abstract

Background

Miscarriage is a common complication in pregnancy and there is still a lack of biomarkers usable in asymptomatic patients before the event occurs. Periostin (PER), whose levels rise particularly during injury or inflammation, has been shown to play an important local role in implantation and early embryonic development. As PER has been described as a biomarker in various medical conditions we intended to evaluate if changes in PER serum levels may help to identify women at risk for spontaneous abortion in the first trimester.

Methods

Women between 18 and 42 years without confounding comorbidities who conceived by IVF/ICSI and ovarian hyperstimulation were analysed in the study after informed consent. Maternal serum samples from 41 patients were assessed at the time of pregnancy testing (PT) and the following first ultrasound checkup (US). Patients were subsequently divided in two groups: (1) patients with subsequent miscarriage in the first trimester (n = 18) and (2) patients with ongoing pregnancy (n = 23), allowing for statistical analysis and investigating the change of PER levels per individual. PER levels were measured using enzyme-linked immunosorbent assay. Statistical analysis was performed using the Fisher exact and Student’s t test. p ≤ 0.05 was considered to be significant.

Results

There was no significant difference concerning possible confounders between the two groups. We did not find any significant difference in PER levels at the time point of PT or US. By investigating the interindividual changes of PER between the two time points however, we observed that patients with a following miscarriage showed increasing levels of PER at the time point of PT compared to US in contrast to patients with an ongoing pregnancy who demonstrated a decrease in PER levels. These alterations were significant in the absolute as well as in the relative comparison.

Conclusion

The relative expression of PER between PT and US is significantly altered in asymptomatic women with subsequent miscarriage compared to women with ongoing pregnancy. Therefore systemic PER levels might represent a potential promising biomarker for the assessment of pregnancy outcome.

Trial registration

Not applicable.
Literature
2.
go back to reference Regan L, Rai R. Epidemiology and the medical causes of miscarriage. Baillieres Best Pract Res Clin Obstet Gynaecol. 2000;14(5):839-54. Regan L, Rai R. Epidemiology and the medical causes of miscarriage. Baillieres Best Pract Res Clin Obstet Gynaecol. 2000;14(5):839-54.
3.
go back to reference van den Berg MMJ, van Maarle MC, van Wely M, Goddijn M. Genetics of early miscarriage. BBA. Elsevier B.V. 2012;1822:1951–9.PubMed van den Berg MMJ, van Maarle MC, van Wely M, Goddijn M. Genetics of early miscarriage. BBA. Elsevier B.V. 2012;1822:1951–9.PubMed
4.
go back to reference Andersen AN, Wolfarth J, Christens P, Olsen J, Medbye M. Maternal age and fetal loss: population based register linkage study. BMJ. 2000:1708–12. Andersen AN, Wolfarth J, Christens P, Olsen J, Medbye M. Maternal age and fetal loss: population based register linkage study. BMJ. 2000:1708–12.
6.
go back to reference Balsells M, García-Patterson A, Corcoy R. Systematic review and meta-analysis on the association of prepregnancy underweight and miscarriage. Eur J Obstet Gynecol. Elsevier Ireland Ltd. 2016;207:73–9.CrossRef Balsells M, García-Patterson A, Corcoy R. Systematic review and meta-analysis on the association of prepregnancy underweight and miscarriage. Eur J Obstet Gynecol. Elsevier Ireland Ltd. 2016;207:73–9.CrossRef
7.
go back to reference Ness RB, Grisso JA, Hirschinger N, Markovic N, Shaw LM, Day NL, et al. Cocaine and tobacco use and the risk of spontaneous abortion. N Engl J Med. 2000;340:333–9.CrossRef Ness RB, Grisso JA, Hirschinger N, Markovic N, Shaw LM, Day NL, et al. Cocaine and tobacco use and the risk of spontaneous abortion. N Engl J Med. 2000;340:333–9.CrossRef
8.
go back to reference Idolazzi L, Ridolo E, Fassio A, Gatti D, Montagni M, Caminati M, et al. Periostin: the bone and beyond. Eur J Intern Med. European Federation of Internal Medicine. 2017;38:12–6.CrossRefPubMed Idolazzi L, Ridolo E, Fassio A, Gatti D, Montagni M, Caminati M, et al. Periostin: the bone and beyond. Eur J Intern Med. European Federation of Internal Medicine. 2017;38:12–6.CrossRefPubMed
9.
go back to reference Izuhara K, Arima K, Ohta S, Suzuki S, Yamamoto K-I, Inamitsu M. Periostin in allergic inflammation. Allergol Int. Elsevier Masson SAS. 2014;63:143–51.CrossRef Izuhara K, Arima K, Ohta S, Suzuki S, Yamamoto K-I, Inamitsu M. Periostin in allergic inflammation. Allergol Int. Elsevier Masson SAS. 2014;63:143–51.CrossRef
10.
11.
go back to reference Germeyer A, Savaris RF, Jauckus J, Lessey B. Endometrial beta3 integrin profile reflects endometrial receptivity defects in women with unexplained recurrent pregnancy loss. Reprod Biol Endocrinol. 2014;12:53. doi:10.1186/1477-7827-12–53. Germeyer A, Savaris RF, Jauckus J, Lessey B. Endometrial beta3 integrin profile reflects endometrial receptivity defects in women with unexplained recurrent pregnancy loss. Reprod Biol Endocrinol. 2014;12:53. doi:10.​1186/​1477-7827-12–53.
12.
go back to reference Kanno A, Satoh K, Masamune A, Hirota M, Kimura K, Umino J, et al. Periostin, secreted from stromal cells, has biphasic effect on cell migration and correlates with the epithelial to mesenchymal transition of human pancreatic cancer cells. Int J Cancer. 2008;122:2707–18.CrossRefPubMed Kanno A, Satoh K, Masamune A, Hirota M, Kimura K, Umino J, et al. Periostin, secreted from stromal cells, has biphasic effect on cell migration and correlates with the epithelial to mesenchymal transition of human pancreatic cancer cells. Int J Cancer. 2008;122:2707–18.CrossRefPubMed
14.
go back to reference Izuhara K, Matsumoto H, Ohta S, Ono J, Arima K, Ogawa M. Recent developments regarding periostin in bronchial asthma. Allergol Int. Elsevier B.V. 2015;64:S3–S10.CrossRefPubMed Izuhara K, Matsumoto H, Ohta S, Ono J, Arima K, Ogawa M. Recent developments regarding periostin in bronchial asthma. Allergol Int. Elsevier B.V. 2015;64:S3–S10.CrossRefPubMed
15.
go back to reference Izuhara K, Conway SJ, Moore BB, Matsumoto H, Holweg CTJ, Matthews JG, et al. Roles of Periostin in respiratory disorders. Am J Respir Crit Care Med. 2016;193:949–56.CrossRefPubMedPubMedCentral Izuhara K, Conway SJ, Moore BB, Matsumoto H, Holweg CTJ, Matthews JG, et al. Roles of Periostin in respiratory disorders. Am J Respir Crit Care Med. 2016;193:949–56.CrossRefPubMedPubMedCentral
16.
go back to reference Tepekoy F, Akkoyunlu G, Demir R. The role of Wnt signaling members in the uterus and embryo during pre-implantation and implantation. J Assist Reprod Genet. 2014;32:337–46.CrossRefPubMedPubMedCentral Tepekoy F, Akkoyunlu G, Demir R. The role of Wnt signaling members in the uterus and embryo during pre-implantation and implantation. J Assist Reprod Genet. 2014;32:337–46.CrossRefPubMedPubMedCentral
17.
go back to reference Ng YH, Zhu H, Leung PCK. Twist modulates human Trophoblastic cell invasion via regulation of N-Cadherin. Endocrinology. 2012;153:925–36.CrossRefPubMed Ng YH, Zhu H, Leung PCK. Twist modulates human Trophoblastic cell invasion via regulation of N-Cadherin. Endocrinology. 2012;153:925–36.CrossRefPubMed
18.
go back to reference Morelli M, Misaggi R, Di Cello A, Zuccalà V, Costanzo F, Zullo F, et al. Tissue expression and serum levels of periostin during pregnancy: a new biomarker of embryo–endometrial cross talk at implantation. Eur J Obstet Gynecol. Elsevier Ireland Ltd; 2014;175:140–144. Morelli M, Misaggi R, Di Cello A, Zuccalà V, Costanzo F, Zullo F, et al. Tissue expression and serum levels of periostin during pregnancy: a new biomarker of embryo–endometrial cross talk at implantation. Eur J Obstet Gynecol. Elsevier Ireland Ltd; 2014;175:140–144.
19.
go back to reference Malanchi I, Santamaria-Martínez A, Susanto E, Peng H, Lehr H-A, Delaloye J-F, et al. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature. Nature Publishing Group. 2011;481:85–9.CrossRefPubMed Malanchi I, Santamaria-Martínez A, Susanto E, Peng H, Lehr H-A, Delaloye J-F, et al. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature. Nature Publishing Group. 2011;481:85–9.CrossRefPubMed
20.
go back to reference Wang Z, Xiong S, Mao Y, Chen M, Ma X, Zhou X, et al. Periostin promotes immunosuppressive premetastatic niche formation to facilitate breast tumour metastasis. J Pathol. 2016;239:484–95.CrossRefPubMed Wang Z, Xiong S, Mao Y, Chen M, Ma X, Zhou X, et al. Periostin promotes immunosuppressive premetastatic niche formation to facilitate breast tumour metastasis. J Pathol. 2016;239:484–95.CrossRefPubMed
21.
go back to reference Ahn HW, Farmer JL, Bazer FW, Spencer TE. Progesterone and interferon tau-regulated genes in the ovine uterine endometrium: identification of periostin as a potential mediator of conceptus elongation. Reproduction. 2009;138:813–25.CrossRefPubMed Ahn HW, Farmer JL, Bazer FW, Spencer TE. Progesterone and interferon tau-regulated genes in the ovine uterine endometrium: identification of periostin as a potential mediator of conceptus elongation. Reproduction. 2009;138:813–25.CrossRefPubMed
22.
go back to reference Hiroi H, Momoeda M, Nakazawa F, Koizumi M, Tsutsumi R, Hosokawa Y, et al. Expression and regulation of Periostin/OSF-2 gene in rat uterus and human Endometrium. Endocr J. 2008;55:183–9.CrossRefPubMed Hiroi H, Momoeda M, Nakazawa F, Koizumi M, Tsutsumi R, Hosokawa Y, et al. Expression and regulation of Periostin/OSF-2 gene in rat uterus and human Endometrium. Endocr J. 2008;55:183–9.CrossRefPubMed
23.
go back to reference Zhu S, Barbe MF, Amin N, Rani S, Popoff SN, Safadi FF, et al. Immunolocalization of Periostin-like factor and Periostin during embryogenesis. J Histochem Cytochem. 2008;56:329–45.CrossRefPubMedPubMedCentral Zhu S, Barbe MF, Amin N, Rani S, Popoff SN, Safadi FF, et al. Immunolocalization of Periostin-like factor and Periostin during embryogenesis. J Histochem Cytochem. 2008;56:329–45.CrossRefPubMedPubMedCentral
24.
go back to reference Dobreva MP, Lhoest L, Pereira PNG, Umans L, Chuva de Sousa Lopes SM, Zwijsen A. Periostin as a biomarker of the amniotic membrane. Stem Cells Int. 2012;2012:1–10.CrossRef Dobreva MP, Lhoest L, Pereira PNG, Umans L, Chuva de Sousa Lopes SM, Zwijsen A. Periostin as a biomarker of the amniotic membrane. Stem Cells Int. 2012;2012:1–10.CrossRef
25.
go back to reference Song H-J, Zhang P, Guo X-J, Liao L-M, Zhou Z-M, Sha J-H, et al. The proteomic analysis of human neonatal umbilical cord serum by mass spectrometry. Acta Pharmacol Sin. Nature Publishing Group. 2009:1550–8. Song H-J, Zhang P, Guo X-J, Liao L-M, Zhou Z-M, Sha J-H, et al. The proteomic analysis of human neonatal umbilical cord serum by mass spectrometry. Acta Pharmacol Sin. Nature Publishing Group. 2009:1550–8.
26.
go back to reference Alfieri CM, Cheek J, Chakraborty S, Yutzey KE. Wnt signaling in heart valve development and osteogenic gene induction. Dev Biol. 2010;338:127–35.CrossRefPubMed Alfieri CM, Cheek J, Chakraborty S, Yutzey KE. Wnt signaling in heart valve development and osteogenic gene induction. Dev Biol. 2010;338:127–35.CrossRefPubMed
28.
go back to reference Quaresima B, Crugliano T, Gaspari M, Faniello MC, Cosimo P, Valanzano R, et al. A proteomics approach to identify changes in protein profiles in serum of familial Adenomatous polyposis patients. Cancer Lett. Elsevier Ireland Ltd. 2008;272:40–52.CrossRefPubMed Quaresima B, Crugliano T, Gaspari M, Faniello MC, Cosimo P, Valanzano R, et al. A proteomics approach to identify changes in protein profiles in serum of familial Adenomatous polyposis patients. Cancer Lett. Elsevier Ireland Ltd. 2008;272:40–52.CrossRefPubMed
29.
go back to reference Alpha Scientists in Reproductive Medicine and ESHRE Special Interest Group of Embryology. The Istanbul consensus workshop on embryo assessment: proceedings of an expert meeting. Hum Reprod. 2011;26(6):1270–83. Alpha Scientists in Reproductive Medicine and ESHRE Special Interest Group of Embryology. The Istanbul consensus workshop on embryo assessment: proceedings of an expert meeting. Hum Reprod. 2011;26(6):1270–83.
30.
go back to reference Duan L, Yan D, Zeng W, Yang X, Wei Q. Predictive power progesterone combined with beta human chorionic gonadotropin measurements in the outcome of threatened miscarriage. Arch Gynecol Obstet. 2010;283:431–5.CrossRefPubMed Duan L, Yan D, Zeng W, Yang X, Wei Q. Predictive power progesterone combined with beta human chorionic gonadotropin measurements in the outcome of threatened miscarriage. Arch Gynecol Obstet. 2010;283:431–5.CrossRefPubMed
31.
go back to reference Pillai RN1, Konje JC2, Tincello DG1, Potdar N3. Role of serum biomarkers in the prediction of outcome in women with threatened miscarriage: a systematic review and diagnostic accuracy meta-analysis. Hum Reprod Update. 2016;22(2):228–39. Pillai RN1, Konje JC2, Tincello DG1, Potdar N3. Role of serum biomarkers in the prediction of outcome in women with threatened miscarriage: a systematic review and diagnostic accuracy meta-analysis. Hum Reprod Update. 2016;22(2):228–39.
32.
go back to reference Jayasena CN, Abbara A, Izzi-Engbeaya C, Comninos AN, Harvey RA, Gonzalez Maffe J, et al. Reduced levels of plasma Kisspeptin during the antenatal booking visit are associated with increased risk of miscarriage. J Clin Endocrinol Metabol. 2014;99:E2652–60.CrossRef Jayasena CN, Abbara A, Izzi-Engbeaya C, Comninos AN, Harvey RA, Gonzalez Maffe J, et al. Reduced levels of plasma Kisspeptin during the antenatal booking visit are associated with increased risk of miscarriage. J Clin Endocrinol Metabol. 2014;99:E2652–60.CrossRef
33.
go back to reference Warrick J, Gronowski A, Moffett C, Zhao Q, Bishop E, Woodworth A. Serum activin a does not predict ectopic pregnancy as a single measurement test, alone or as part of a multi-marker panel including progesterone and hCG. Clin Chim Acta. Elsevier B.V. 2012;413:707–11.CrossRefPubMed Warrick J, Gronowski A, Moffett C, Zhao Q, Bishop E, Woodworth A. Serum activin a does not predict ectopic pregnancy as a single measurement test, alone or as part of a multi-marker panel including progesterone and hCG. Clin Chim Acta. Elsevier B.V. 2012;413:707–11.CrossRefPubMed
34.
go back to reference Dhiman P, Senthilkumar GP, Rajendiran S, Sivaraman K, Soundararaghavan S, Kulandhasamy M. Serum activin B concentration as predictive biomarker for ectopic pregnancy. Clin Biochem. Elsevier B.V. 2016;49:609–12.CrossRefPubMed Dhiman P, Senthilkumar GP, Rajendiran S, Sivaraman K, Soundararaghavan S, Kulandhasamy M. Serum activin B concentration as predictive biomarker for ectopic pregnancy. Clin Biochem. Elsevier B.V. 2016;49:609–12.CrossRefPubMed
35.
go back to reference Daponte A, Deligeoroglou E, Garas A, Pournaras S, Hadjichristodoulou C, Messinis IE. Activin a and Follistatin as biomarkers for ectopic pregnancy and missed abortion. Dis Markers. 2013;35:497–503.CrossRefPubMedPubMedCentral Daponte A, Deligeoroglou E, Garas A, Pournaras S, Hadjichristodoulou C, Messinis IE. Activin a and Follistatin as biomarkers for ectopic pregnancy and missed abortion. Dis Markers. 2013;35:497–503.CrossRefPubMedPubMedCentral
36.
go back to reference Al Mohamady M, Fattah GA, Elkattan E, Bayoumy R, Hamed D. Correlation of serum CA-125 and progesterone levels with ultrasound markers in the prediction of pregnancy outcome in threatened miscarriage. Int J Fertil Steril. 2016;9:506–11.PubMed Al Mohamady M, Fattah GA, Elkattan E, Bayoumy R, Hamed D. Correlation of serum CA-125 and progesterone levels with ultrasound markers in the prediction of pregnancy outcome in threatened miscarriage. Int J Fertil Steril. 2016;9:506–11.PubMed
37.
go back to reference Hanita O, Roslina O, Nor Azlin M. ORIGINAL ARTICLEMaternal level of pregnancy-associated plasma protein a as a predictor of pregnancy failure in threatened abortion. Malaysian J Pathol. 2012;34:145–51. Hanita O, Roslina O, Nor Azlin M. ORIGINAL ARTICLEMaternal level of pregnancy-associated plasma protein a as a predictor of pregnancy failure in threatened abortion. Malaysian J Pathol. 2012;34:145–51.
38.
go back to reference Tong S, Ngian G-L, Onwude JL, Permezel M, Saglam B, Hay S, et al. Diagnostic accuracy of maternal serum macrophage inhibitory Cytokine-1 and pregnancy-associated plasma protein-a at 6–10 weeks of gestation to predict miscarriage. Obstet Gynecol. 2012;119:1000–8.CrossRefPubMed Tong S, Ngian G-L, Onwude JL, Permezel M, Saglam B, Hay S, et al. Diagnostic accuracy of maternal serum macrophage inhibitory Cytokine-1 and pregnancy-associated plasma protein-a at 6–10 weeks of gestation to predict miscarriage. Obstet Gynecol. 2012;119:1000–8.CrossRefPubMed
39.
go back to reference Hannan NJ, Bambang K, Kaitu’u-Lino TJ, Konje JC, Tong S. A Bioplex analysis of cytokines and chemokines in first trimester maternal plasma to screen for predictors of miscarriage. Proost P, editor. PLoS One. 2014;9:e93320–7.CrossRefPubMedPubMedCentral Hannan NJ, Bambang K, Kaitu’u-Lino TJ, Konje JC, Tong S. A Bioplex analysis of cytokines and chemokines in first trimester maternal plasma to screen for predictors of miscarriage. Proost P, editor. PLoS One. 2014;9:e93320–7.CrossRefPubMedPubMedCentral
40.
go back to reference Barnhart KT, Guo W, Cary MS, Morse CB, Chung K, Takacs P, et al. Differences in serum human chorionic Gonadotropin rise in early pregnancy by race and value at presentation. Obstet Gynecol. 2016;128:504–11.CrossRefPubMedPubMedCentral Barnhart KT, Guo W, Cary MS, Morse CB, Chung K, Takacs P, et al. Differences in serum human chorionic Gonadotropin rise in early pregnancy by race and value at presentation. Obstet Gynecol. 2016;128:504–11.CrossRefPubMedPubMedCentral
Metadata
Title
Serum periostin levels in early in pregnancy are significantly altered in women with miscarriage
Authors
A. Freis
J. Schlegel
R. J. Kuon
A. Doster
J. Jauckus
T. Strowitzki
A. Germeyer
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2017
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-017-0307-9

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