Association of maternal prenatal copper concentration with gestational duration and preterm birth: a multicountry meta-analysis

Nagendra K. Monangi; Huan Xu; Yue-Mei Fan; Rasheeda Khanam; Waqasuddin Khan; Saikat Deb; Jesmin Pervin; Joan T. Price; Lovejeet Kaur; Abdullah Al Mahmud; Le Quang Thanh; Angharad Care; Julio A. Landero; Gerald F. Combs; Elizabeth Belling; Joanne Chappell; Jing Chen; Fansheng Kong; Craig Lacher; Salahuddin Ahmed; Nabidul Haque Chowdhury; Sayedur Rahman; Furqan Kabir; Imran Nisar; Aneeta Hotwani; Usma Mehmood; Ambreen Nizar; Javairia Khalid; Usha Dhingra; Arup Dutta; Said Mohamed Ali; Fahad Aftab; Mohammed Hamad Juma; Monjur Rahman; Tahmeed Ahmed; M Munirul Islam; Bellington Vwalika; Patrick Musonda; Ulla Ashorn; Kenneth Maleta; Mikko Hallman; Laura Goodfellow; Juhi K. Gupta; Ana Alfirevic; Susan K. Murphy; Larry Rand; Kelli K. Ryckman; Jeffrey C. Murray; Rajiv Bahl; James A. Litch; Courtney Baruch-Gravett; Shailaja Sopory; Uma Chandra Mouli Natchu; Pavitra V. Kumar; Neha Kumari; Ramachandran Thiruvengadam; Atul Kumar Singh; Pankaj Kumar; Zarko Alfirevic; Abdullah H. Baqui; Shinjini Bhatnagar; Jane E. Hirst; Cathrine Hoyo; Fyezah Jehan; Laura Jelliffe-Pawlowski; Anisur Rahman; Daniel E. Roth; Sunil Sazawal; Jeffrey S.A. Stringer; Per Ashorn; Ge Zhang; Louis J. Muglia; Jose Villar; Rose McGready; Fernando C. Barros; Cesar G. Victora; Shama Munim; Aris T. Papageorgh; Roseline Ochieng; Rachel Craik; Hellen Barsosio; James A. Berkley; Maria Carvalho; Leila Cheikh Ismail; Ann Lambert; Shane A. Norris; Chrystelle OO. Tshivuila-Matela; Francois Nosten; Ricardo Uauy; Zulfiqar A. Bhutta; Stephen Kennedy

doi:10.1016/j.ajcnut.2023.10.011

Association of maternal prenatal copper concentration with gestational duration and preterm birth: a multicountry meta-analysis

Nagendra K. Monangi, Huan Xu, Yue-Mei Fan, Rasheeda Khanam, Waqasuddin Khan, Saikat Deb, Jesmin Pervin, Joan T. Price, Lovejeet Kaur, Abdullah Al Mahmud, Le Quang Thanh, Angharad Care, Julio A. Landero, Gerald F. Combs, Elizabeth Belling, Joanne Chappell, Jing Chen, Fansheng Kong, Craig Lacher, Salahuddin AhmedNabidul Haque Chowdhury, Sayedur Rahman, Furqan Kabir, Imran Nisar, Aneeta Hotwani, Usma Mehmood, Ambreen Nizar, Javairia Khalid, Usha Dhingra, Arup Dutta, Said Mohamed Ali, Fahad Aftab, Mohammed Hamad Juma, Monjur Rahman, Tahmeed Ahmed, M Munirul Islam, Bellington Vwalika, Patrick Musonda, Ulla Ashorn, Kenneth Maleta, Mikko Hallman, Laura Goodfellow, Juhi K. Gupta, Ana Alfirevic, Susan K. Murphy, Larry Rand, Kelli K. Ryckman, Jeffrey C. Murray, Rajiv Bahl, James A. Litch, Courtney Baruch-Gravett, Shailaja Sopory, Uma Chandra Mouli Natchu, Pavitra V. Kumar, Neha Kumari, Ramachandran Thiruvengadam, Atul Kumar Singh, Pankaj Kumar, Zarko Alfirevic, Abdullah H. Baqui, Shinjini Bhatnagar, Jane E. Hirst, Cathrine Hoyo, Fyezah Jehan, Laura Jelliffe-Pawlowski, Anisur Rahman, Daniel E. Roth, Sunil Sazawal, Jeffrey S.A. Stringer, Per Ashorn, Ge Zhang, Louis J. Muglia, Jose Villar, Rose McGready, Fernando C. Barros, Cesar G. Victora, Shama Munim, Aris T. Papageorgh, Roseline Ochieng, Rachel Craik, Hellen Barsosio, James A. Berkley, Maria Carvalho, Leila Cheikh Ismail, Ann Lambert, Shane A. Norris, Chrystelle OO. Tshivuila-Matela, Francois Nosten, Ricardo Uauy, Zulfiqar A. Bhutta, Stephen Kennedy

Research output: Contribution to journal › Article › peer-review

3 Citations (Scopus)

Abstract

Background

Copper (Cu), an essential trace mineral regulating multiple actions of inflammation and oxidative stress, has been implicated in risk for preterm birth (PTB).

Objectives

This study aimed to determine the association of maternal Cu concentration during pregnancy with PTB risk and gestational duration in a large multicohort study including diverse populations.

Methods

Maternal plasma or serum samples of 10,449 singleton live births were obtained from 18 geographically diverse study cohorts. Maternal Cu concentrations were determined using inductively coupled plasma mass spectrometry. The associations of maternal Cu with PTB and gestational duration were analyzed using logistic and linear regressions for each cohort. The estimates were then combined using meta-analysis. Associations between maternal Cu and acute-phase reactants (APRs) and infection status were analyzed in 1239 samples from the Malawi cohort.

Results

The maternal prenatal Cu concentration in our study samples followed normal distribution with mean of 1.92 μg/mL and standard deviation of 0.43 μg/mL, and Cu concentrations increased with gestational age up to 20 wk. The random-effect meta-analysis across 18 cohorts revealed that 1 μg/mL increase in maternal Cu concentration was associated with higher risk of PTB with odds ratio of 1.30 (95% confidence interval [CI]: 1.08, 1.57) and shorter gestational duration of 1.64 d (95% CI: 0.56, 2.73). In the Malawi cohort, higher maternal Cu concentration, concentrations of multiple APRs, and infections (malaria and HIV) were correlated and associated with greater risk of PTB and shorter gestational duration.

Conclusions

Our study supports robust negative association between maternal Cu and gestational duration and positive association with risk for PTB. Cu concentration was strongly correlated with APRs and infection status suggesting its potential role in inflammation, a pathway implicated in the mechanisms of PTB. Therefore, maternal Cu could be used as potential marker of integrated inflammatory pathways during pregnancy and risk for PTB.

Original language	English
Pages (from-to)	221-231
Number of pages	11
Journal	American Journal of Clinical Nutrition
Volume	119
Issue number	1
Early online date	27 Oct 2023
DOIs	https://doi.org/10.1016/j.ajcnut.2023.10.011
Publication status	Published - 2 Jan 2024

Keywords

acute-phase reactants
copper
gestational duration
inflammation
low- and middle-income countries
nutrition
pregnancy
preterm birth

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1016/j.ajcnut.2023.10.011Licence: CC BY

1-s2Final published version, 1.92 MBLicence: CC BY

Cite this

Monangi, N. K., Xu, H., Fan, Y.-M., Khanam, R., Khan, W., Deb, S., Pervin, J., Price, J. T., Kaur, L., Al Mahmud, A., Thanh, L. Q., Care, A., Landero, J. A., Combs, G. F., Belling, E., Chappell, J., Chen, J., Kong, F., Lacher, C., ... Kennedy, S. (2024). Association of maternal prenatal copper concentration with gestational duration and preterm birth: a multicountry meta-analysis. American Journal of Clinical Nutrition, 119(1), 221-231. https://doi.org/10.1016/j.ajcnut.2023.10.011

@article{22c6f3f8a8484b1489463e77699b22b4,

title = "Association of maternal prenatal copper concentration with gestational duration and preterm birth: a multicountry meta-analysis",

abstract = "BackgroundCopper (Cu), an essential trace mineral regulating multiple actions of inflammation and oxidative stress, has been implicated in risk for preterm birth (PTB).ObjectivesThis study aimed to determine the association of maternal Cu concentration during pregnancy with PTB risk and gestational duration in a large multicohort study including diverse populations.MethodsMaternal plasma or serum samples of 10,449 singleton live births were obtained from 18 geographically diverse study cohorts. Maternal Cu concentrations were determined using inductively coupled plasma mass spectrometry. The associations of maternal Cu with PTB and gestational duration were analyzed using logistic and linear regressions for each cohort. The estimates were then combined using meta-analysis. Associations between maternal Cu and acute-phase reactants (APRs) and infection status were analyzed in 1239 samples from the Malawi cohort.ResultsThe maternal prenatal Cu concentration in our study samples followed normal distribution with mean of 1.92 μg/mL and standard deviation of 0.43 μg/mL, and Cu concentrations increased with gestational age up to 20 wk. The random-effect meta-analysis across 18 cohorts revealed that 1 μg/mL increase in maternal Cu concentration was associated with higher risk of PTB with odds ratio of 1.30 (95\% confidence interval [CI]: 1.08, 1.57) and shorter gestational duration of 1.64 d (95\% CI: 0.56, 2.73). In the Malawi cohort, higher maternal Cu concentration, concentrations of multiple APRs, and infections (malaria and HIV) were correlated and associated with greater risk of PTB and shorter gestational duration.ConclusionsOur study supports robust negative association between maternal Cu and gestational duration and positive association with risk for PTB. Cu concentration was strongly correlated with APRs and infection status suggesting its potential role in inflammation, a pathway implicated in the mechanisms of PTB. Therefore, maternal Cu could be used as potential marker of integrated inflammatory pathways during pregnancy and risk for PTB.",

keywords = "acute-phase reactants, copper, gestational duration, inflammation, low- and middle-income countries, nutrition, pregnancy, preterm birth",

author = "Monangi, \{Nagendra K.\} and Huan Xu and Yue-Mei Fan and Rasheeda Khanam and Waqasuddin Khan and Saikat Deb and Jesmin Pervin and Price, \{Joan T.\} and Lovejeet Kaur and \{Al Mahmud\}, Abdullah and Thanh, \{Le Quang\} and Angharad Care and Landero, \{Julio A.\} and Combs, \{Gerald F.\} and Elizabeth Belling and Joanne Chappell and Jing Chen and Fansheng Kong and Craig Lacher and Salahuddin Ahmed and Chowdhury, \{Nabidul Haque\} and Sayedur Rahman and Furqan Kabir and Imran Nisar and Aneeta Hotwani and Usma Mehmood and Ambreen Nizar and Javairia Khalid and Usha Dhingra and Arup Dutta and Ali, \{Said Mohamed\} and Fahad Aftab and Juma, \{Mohammed Hamad\} and Monjur Rahman and Tahmeed Ahmed and Islam, \{M Munirul\} and Bellington Vwalika and Patrick Musonda and Ulla Ashorn and Kenneth Maleta and Mikko Hallman and Laura Goodfellow and Gupta, \{Juhi K.\} and Ana Alfirevic and Murphy, \{Susan K.\} and Larry Rand and Ryckman, \{Kelli K.\} and Murray, \{Jeffrey C.\} and Rajiv Bahl and Litch, \{James A.\} and Courtney Baruch-Gravett and Shailaja Sopory and \{Chandra Mouli Natchu\}, Uma and Kumar, \{Pavitra V.\} and Neha Kumari and Ramachandran Thiruvengadam and Singh, \{Atul Kumar\} and Pankaj Kumar and Zarko Alfirevic and Baqui, \{Abdullah H.\} and Shinjini Bhatnagar and Hirst, \{Jane E.\} and Cathrine Hoyo and Fyezah Jehan and Laura Jelliffe-Pawlowski and Anisur Rahman and Roth, \{Daniel E.\} and Sunil Sazawal and Stringer, \{Jeffrey S.A.\} and Per Ashorn and Ge Zhang and Muglia, \{Louis J.\} and Jose Villar and Rose McGready and Barros, \{Fernando C.\} and Victora, \{Cesar G.\} and Shama Munim and Papageorgh, \{Aris T.\} and Roseline Ochieng and Rachel Craik and Hellen Barsosio and Berkley, \{James A.\} and Maria Carvalho and Ismail, \{Leila Cheikh\} and Ann Lambert and Norris, \{Shane A.\} and Tshivuila-Matela, \{Chrystelle OO.\} and Francois Nosten and Ricardo Uauy and Bhutta, \{Zulfiqar A.\} and Stephen Kennedy",

year = "2024",

month = jan,

day = "2",

doi = "10.1016/j.ajcnut.2023.10.011",

language = "English",

volume = "119",

pages = "221--231",

journal = "American Journal of Clinical Nutrition",

issn = "0002-9165",

publisher = "Elsevier B.V.",

number = "1",

}

Monangi, NK, Xu, H, Fan, Y-M, Khanam, R, Khan, W, Deb, S, Pervin, J, Price, JT, Kaur, L, Al Mahmud, A, Thanh, LQ, Care, A, Landero, JA, Combs, GF, Belling, E, Chappell, J, Chen, J, Kong, F, Lacher, C, Ahmed, S, Chowdhury, NH, Rahman, S, Kabir, F, Nisar, I, Hotwani, A, Mehmood, U, Nizar, A, Khalid, J, Dhingra, U, Dutta, A, Ali, SM, Aftab, F, Juma, MH, Rahman, M, Ahmed, T, Islam, MM, Vwalika, B, Musonda, P, Ashorn, U, Maleta, K, Hallman, M, Goodfellow, L, Gupta, JK, Alfirevic, A, Murphy, SK, Rand, L, Ryckman, KK, Murray, JC, Bahl, R, Litch, JA, Baruch-Gravett, C, Sopory, S, Chandra Mouli Natchu, U, Kumar, PV, Kumari, N, Thiruvengadam, R, Singh, AK, Kumar, P, Alfirevic, Z, Baqui, AH, Bhatnagar, S, Hirst, JE, Hoyo, C, Jehan, F, Jelliffe-Pawlowski, L, Rahman, A, Roth, DE, Sazawal, S, Stringer, JSA, Ashorn, P, Zhang, G, Muglia, LJ, Villar, J, McGready, R, Barros, FC, Victora, CG, Munim, S, Papageorgh, AT, Ochieng, R, Craik, R, Barsosio, H, Berkley, JA, Carvalho, M, Ismail, LC, Lambert, A, Norris, SA, Tshivuila-Matela, COO, Nosten, F, Uauy, R, Bhutta, ZA & Kennedy, S 2024, 'Association of maternal prenatal copper concentration with gestational duration and preterm birth: a multicountry meta-analysis', American Journal of Clinical Nutrition, vol. 119, no. 1, pp. 221-231. https://doi.org/10.1016/j.ajcnut.2023.10.011

TY - JOUR

T1 - Association of maternal prenatal copper concentration with gestational duration and preterm birth: a multicountry meta-analysis

AU - Monangi, Nagendra K.

AU - Xu, Huan

AU - Fan, Yue-Mei

AU - Khanam, Rasheeda

AU - Khan, Waqasuddin

AU - Deb, Saikat

AU - Pervin, Jesmin

AU - Price, Joan T.

AU - Kaur, Lovejeet

AU - Al Mahmud, Abdullah

AU - Thanh, Le Quang

AU - Care, Angharad

AU - Landero, Julio A.

AU - Combs, Gerald F.

AU - Belling, Elizabeth

AU - Chappell, Joanne

AU - Chen, Jing

AU - Kong, Fansheng

AU - Lacher, Craig

AU - Ahmed, Salahuddin

AU - Chowdhury, Nabidul Haque

AU - Rahman, Sayedur

AU - Kabir, Furqan

AU - Nisar, Imran

AU - Hotwani, Aneeta

AU - Mehmood, Usma

AU - Nizar, Ambreen

AU - Khalid, Javairia

AU - Dhingra, Usha

AU - Dutta, Arup

AU - Ali, Said Mohamed

AU - Aftab, Fahad

AU - Juma, Mohammed Hamad

AU - Rahman, Monjur

AU - Ahmed, Tahmeed

AU - Islam, M Munirul

AU - Vwalika, Bellington

AU - Musonda, Patrick

AU - Ashorn, Ulla

AU - Maleta, Kenneth

AU - Hallman, Mikko

AU - Goodfellow, Laura

AU - Gupta, Juhi K.

AU - Alfirevic, Ana

AU - Murphy, Susan K.

AU - Rand, Larry

AU - Ryckman, Kelli K.

AU - Murray, Jeffrey C.

AU - Bahl, Rajiv

AU - Litch, James A.

AU - Baruch-Gravett, Courtney

AU - Sopory, Shailaja

AU - Chandra Mouli Natchu, Uma

AU - Kumar, Pavitra V.

AU - Kumari, Neha

AU - Thiruvengadam, Ramachandran

AU - Singh, Atul Kumar

AU - Kumar, Pankaj

AU - Alfirevic, Zarko

AU - Baqui, Abdullah H.

AU - Bhatnagar, Shinjini

AU - Hirst, Jane E.

AU - Hoyo, Cathrine

AU - Jehan, Fyezah

AU - Jelliffe-Pawlowski, Laura

AU - Rahman, Anisur

AU - Roth, Daniel E.

AU - Sazawal, Sunil

AU - Stringer, Jeffrey S.A.

AU - Ashorn, Per

AU - Zhang, Ge

AU - Muglia, Louis J.

AU - Villar, Jose

AU - McGready, Rose

AU - Barros, Fernando C.

AU - Victora, Cesar G.

AU - Munim, Shama

AU - Papageorgh, Aris T.

AU - Ochieng, Roseline

AU - Craik, Rachel

AU - Barsosio, Hellen

AU - Berkley, James A.

AU - Carvalho, Maria

AU - Ismail, Leila Cheikh

AU - Lambert, Ann

AU - Norris, Shane A.

AU - Tshivuila-Matela, Chrystelle OO.

AU - Nosten, Francois

AU - Uauy, Ricardo

AU - Bhutta, Zulfiqar A.

AU - Kennedy, Stephen

PY - 2024/1/2

Y1 - 2024/1/2

N2 - BackgroundCopper (Cu), an essential trace mineral regulating multiple actions of inflammation and oxidative stress, has been implicated in risk for preterm birth (PTB).ObjectivesThis study aimed to determine the association of maternal Cu concentration during pregnancy with PTB risk and gestational duration in a large multicohort study including diverse populations.MethodsMaternal plasma or serum samples of 10,449 singleton live births were obtained from 18 geographically diverse study cohorts. Maternal Cu concentrations were determined using inductively coupled plasma mass spectrometry. The associations of maternal Cu with PTB and gestational duration were analyzed using logistic and linear regressions for each cohort. The estimates were then combined using meta-analysis. Associations between maternal Cu and acute-phase reactants (APRs) and infection status were analyzed in 1239 samples from the Malawi cohort.ResultsThe maternal prenatal Cu concentration in our study samples followed normal distribution with mean of 1.92 μg/mL and standard deviation of 0.43 μg/mL, and Cu concentrations increased with gestational age up to 20 wk. The random-effect meta-analysis across 18 cohorts revealed that 1 μg/mL increase in maternal Cu concentration was associated with higher risk of PTB with odds ratio of 1.30 (95% confidence interval [CI]: 1.08, 1.57) and shorter gestational duration of 1.64 d (95% CI: 0.56, 2.73). In the Malawi cohort, higher maternal Cu concentration, concentrations of multiple APRs, and infections (malaria and HIV) were correlated and associated with greater risk of PTB and shorter gestational duration.ConclusionsOur study supports robust negative association between maternal Cu and gestational duration and positive association with risk for PTB. Cu concentration was strongly correlated with APRs and infection status suggesting its potential role in inflammation, a pathway implicated in the mechanisms of PTB. Therefore, maternal Cu could be used as potential marker of integrated inflammatory pathways during pregnancy and risk for PTB.

AB - BackgroundCopper (Cu), an essential trace mineral regulating multiple actions of inflammation and oxidative stress, has been implicated in risk for preterm birth (PTB).ObjectivesThis study aimed to determine the association of maternal Cu concentration during pregnancy with PTB risk and gestational duration in a large multicohort study including diverse populations.MethodsMaternal plasma or serum samples of 10,449 singleton live births were obtained from 18 geographically diverse study cohorts. Maternal Cu concentrations were determined using inductively coupled plasma mass spectrometry. The associations of maternal Cu with PTB and gestational duration were analyzed using logistic and linear regressions for each cohort. The estimates were then combined using meta-analysis. Associations between maternal Cu and acute-phase reactants (APRs) and infection status were analyzed in 1239 samples from the Malawi cohort.ResultsThe maternal prenatal Cu concentration in our study samples followed normal distribution with mean of 1.92 μg/mL and standard deviation of 0.43 μg/mL, and Cu concentrations increased with gestational age up to 20 wk. The random-effect meta-analysis across 18 cohorts revealed that 1 μg/mL increase in maternal Cu concentration was associated with higher risk of PTB with odds ratio of 1.30 (95% confidence interval [CI]: 1.08, 1.57) and shorter gestational duration of 1.64 d (95% CI: 0.56, 2.73). In the Malawi cohort, higher maternal Cu concentration, concentrations of multiple APRs, and infections (malaria and HIV) were correlated and associated with greater risk of PTB and shorter gestational duration.ConclusionsOur study supports robust negative association between maternal Cu and gestational duration and positive association with risk for PTB. Cu concentration was strongly correlated with APRs and infection status suggesting its potential role in inflammation, a pathway implicated in the mechanisms of PTB. Therefore, maternal Cu could be used as potential marker of integrated inflammatory pathways during pregnancy and risk for PTB.

KW - acute-phase reactants

KW - copper

KW - gestational duration

KW - inflammation

KW - low- and middle-income countries

KW - nutrition

KW - pregnancy

KW - preterm birth

U2 - 10.1016/j.ajcnut.2023.10.011

DO - 10.1016/j.ajcnut.2023.10.011

M3 - Article

SN - 0002-9165

VL - 119

SP - 221

EP - 231

JO - American Journal of Clinical Nutrition

JF - American Journal of Clinical Nutrition

IS - 1

ER -

Association of maternal prenatal copper concentration with gestational duration and preterm birth: a multicountry meta-analysis

Abstract

Keywords

UN SDGs

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