Urinary metal profiles in mother-offspring pairs and their association with early dysglycemia in the International Hyperglycemia and Adverse Pregnancy Outcome Follow Up Study (HAPO-FUS)

Malek El Muayed; Janice C. Wang; Winifred P. Wong; Boyd E. Metzger; Katelyn B. Zumpf; Miranda G. Gurra; Rebecca A. Sponenburg; M. Geoffrey Hayes; Denise M. Scholtens; Lynn P. Lowe; William L. Lowe

doi:10.1038/s41370-022-00511-z

Urinary metal profiles in mother-offspring pairs and their association with early dysglycemia in the International Hyperglycemia and Adverse Pregnancy Outcome Follow Up Study (HAPO-FUS)

Malek El Muayed^*, Janice C. Wang, Winifred P. Wong, Boyd E. Metzger, Katelyn B. Zumpf, Miranda G. Gurra, Rebecca A. Sponenburg, M. Geoffrey Hayes, Denise M. Scholtens, Lynn P. Lowe, William L. Lowe

^*Corresponding author for this work

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

1 Scopus citations

Abstract

Background: Variations in dietary intake and environmental exposure patterns of essential and non-essential trace metals influence many aspects of human health throughout the life span. Objective: To examine the relationship between urine profiles of essential and non-essential metals in mother-offspring pairs and their association with early dysglycemia. Methods: Herein, we report findings from an ancillary study to the international Hyperglycemia and Adverse Pregnancy Outcome Follow-Up Study (HAPO-FUS) that examined urinary essential and non-essential metal profiles from mothers and offspring ages 10–14 years (1012 mothers, 1013 offspring, 968 matched pairs) from 10 international sites. Results: Our analysis demonstrated a diverse exposure pattern across participating sites. In multiple regression modelling, a positive association between markers of early dysglycemia and urinary zinc was found in both mothers and offspring after adjustment for common risk factors for diabetes. The analysis showed weaker, positive, and negative associations of the 2-h glucose value with urinary selenium and arsenic respectively. A positive association between 2-h glucose values and cadmium was found only in mothers in the fully adjusted model when participants with established diabetes were excluded. There was a high degree of concordance between mother and offspring urinary metal profiles. Mother-to-offspring urinary metal ratios were unique for each metal, providing insights into changes in their homeostasis across the lifespan. Significance: Urinary levels of essential and non-essential metals are closely correlated between mothers and their offspring in an international cohort. Urinary levels of zinc, selenium, arsenic, and cadmium showed varying degrees of association with early dysglycemia in a comparatively healthy cohort with a low rate of preexisting diabetes. Impact statement: Our data provides novel evidence for a strong correlation between mother and offspring urinary metal patterns with a unique mother-to-offspring ratio for each metal. The study also provides new evidence for a strong positive association between early dysglycemia and urinary zinc, both in mothers and offspring. Weaker positive associations with urinary selenium and cadmium and negative associations with arsenic were also found. The low rate of preexisting diabetes in this population provides the unique advantage of minimizing the confounding effect of preexisting, diabetes related renal changes that would alter the relationship between dysglycemia and renal metal excretion.

Original language	English (US)
Pages (from-to)	855-864
Number of pages	10
Journal	Journal of Exposure Science and Environmental Epidemiology
Volume	33
Issue number	6
DOIs	https://doi.org/10.1038/s41370-022-00511-z
State	Published - Nov 2023

Funding

ICP-MS metal analysis was performed at Quantitative Bio-elemental Imaging Center, Northwestern University that is supported by NASA Ames Research Center (NNA04CC36G). Data and urine samples used in this ancillary study originated from the Hyperglycemia and Adverse Pregnancy Outcome Follow Up Study (HAPO-FUS). Group Information: The collaborator members of the HAPO Follow-up Study Cooperative Research Group by field center are: Bangkok, Thailand: C. Deerochanawong, T. Tanaphonpoonsuk (Rajavithi Hospital) and S. Binratkaew, U. Chotigeat, W. Manyam (Queen Sirikit National Institute of Child Health); Barbados: M. Forde, A. Greenidge, K. Neblett, P. M. Lashley, D. Walcott (Queen Elizabeth Hospital, School of Clinical Medicine and Research, University of the West Indies); Belfast, Ireland: K. Corry, L. Francis, J. Irwin, A. Langan, D. R. McCance, M. Mousavi (Belfast Health and Social Care Trust) and I. S. Young (Queen’s University); Bellflower, California: J. Gutierrez, J. Jimenez, J. M. Lawrence, D. A. Sacks, H. S. Takhar, E. Tanton (Kaiser Permanente of Southern California); Chicago, Illiniois: W. J. Brickman, J. Howard, J. L. Josefson, L. Miller (Ann and Robert H. Lurie Children’s Hospital and Northwestern University Feinberg School of Medicine); Cleveland, Ohio: J. Bjaloncik, P. M. Catalano, A. Davis, K. Koontz, L. Presley, S. Smith, A. Tyhulski (MetroHealth Medical Center and Case Western Reserve University); Hong Kong, China: A. Li, R. C. Ma, R. Ozaki, W. H. Tam, M. Wong, C. Yuen (Chinese University of Hong Kong and Prince of Wales Hospital); Manchester, England: P. E. Clayton, A. Khan, A. Vyas (Royal Manchester Children’s Hospital, Manchester University Hospitals NHS Foundation Trust, Manchester Academic Healthy Sciences Centre and School of Medical Sciences, Faculty of Biology, Medicine, and Health, University of Manchester) and M. Maresh (St Mary’s Hospital, Manchester University Hospitals NHS Foundation Trust, Manchester Academic Health Sciences Centre); Petah-Tikva, Israel: H. Benzaquen, N. Glickman, A. Hamou, O. Hermon, O. Horesh, Y. Keren, S. Shalitin (Schneider Children’s Medical Center of Israel) and Y. Lebenthal (Jesse Z. and Sara Lea Shafer Institute for Endocrinology and Diabetes, National Center for Childhood Diabetes, Schneider Children’s Medical Center of Israel, Sackler Faculty of Medicine, Tel Aviv University); and Toronto, Ontario, Canada: K. Cordeiro, J. Hamilton, H. Y. Nguyen, S. Steele (Hospital for Sick Children, University of Toronto). Coordinating Center: Northwestern University Feinberg School of Medicine (F. Chen, A. R. Dyer, W. Huang, A. Kuang, M. Jimenez, L. P. Lowe, W. L. Lowe Jr, B. E. Metzger, M. Nodzenski, A. Reisetter, D. Scholtens, O. Talbot, P. Yim). Consultants: D. Dunger, A. Thomas. National Institute of Diabetes and Digestive and Kidney Diseases: M. Horlick, B. Linder, A. Unalp-Arida. Eunice Kennedy Shriver National Institute of Child Health and Human Development: G. Grave. ICP-MS metal analysis was performed at Quantitative Bio-elemental Imaging Center, Northwestern University that is supported by NASA Ames Research Center (NNA04CC36G). Data and urine samples used in this ancillary study originated from the Hyperglycemia and Adverse Pregnancy Outcome Follow Up Study (HAPO-FUS). Group Information: The collaborator members of the HAPO Follow-up Study Cooperative Research Group by field center are: Bangkok, Thailand: C. Deerochanawong, T. Tanaphonpoonsuk (Rajavithi Hospital) and S. Binratkaew, U. Chotigeat, W. Manyam (Queen Sirikit National Institute of Child Health); Barbados: M. Forde, A. Greenidge, K. Neblett, P. M. Lashley, D. Walcott (Queen Elizabeth Hospital, School of Clinical Medicine and Research, University of the West Indies); Belfast, Ireland: K. Corry, L. Francis, J. Irwin, A. Langan, D. R. McCance, M. Mousavi (Belfast Health and Social Care Trust) and I. S. Young (Queen’s University); Bellflower, California: J. Gutierrez, J. Jimenez, J. M. Lawrence, D. A. Sacks, H. S. Takhar, E. Tanton (Kaiser Permanente of Southern California); Chicago, Illiniois: W. J. Brickman, J. Howard, J. L. Josefson, L. Miller (Ann and Robert H. Lurie Children’s Hospital and Northwestern University Feinberg School of Medicine); Cleveland, Ohio: J. Bjaloncik, P. M. Catalano, A. Davis, K. Koontz, L. Presley, S. Smith, A. Tyhulski (MetroHealth Medical Center and Case Western Reserve University); Hong Kong, China: A. Li, R. C. Ma, R. Ozaki, W. H. Tam, M. Wong, C. Yuen (Chinese University of Hong Kong and Prince of Wales Hospital); Manchester, England: P. E. Clayton, A. Khan, A. Vyas (Royal Manchester Children’s Hospital, Manchester University Hospitals NHS Foundation Trust, Manchester Academic Healthy Sciences Centre and School of Medical Sciences, Faculty of Biology, Medicine, and Health, University of Manchester) and M. Maresh (St Mary’s Hospital, Manchester University Hospitals NHS Foundation Trust, Manchester Academic Health Sciences Centre); Petah-Tikva, Israel: H. Benzaquen, N. Glickman, A. Hamou, O. Hermon, O. Horesh, Y. Keren, S. Shalitin (Schneider Children’s Medical Center of Israel) and Y. Lebenthal (Jesse Z. and Sara Lea Shafer Institute for Endocrinology and Diabetes, National Center for Childhood Diabetes, Schneider Children’s Medical Center of Israel, Sackler Faculty of Medicine, Tel Aviv University); and Toronto, Ontario, Canada: K. Cordeiro, J. Hamilton, H. Y. Nguyen, S. Steele (Hospital for Sick Children, University of Toronto). Coordinating Center: Northwestern University Feinberg School of Medicine (F. Chen, A. R. Dyer, W. Huang, A. Kuang, M. Jimenez, L. P. Lowe, W. L. Lowe Jr, B. E. Metzger, M. Nodzenski, A. Reisetter, D. Scholtens, O. Talbot, P. Yim). Consultants: D. Dunger, A. Thomas. National Institute of Diabetes and Digestive and Kidney Diseases: M. Horlick, B. Linder, A. Unalp-Arida. Eunice Kennedy Shriver National Institute of Child Health and Human Development: G. Grave. The HAPO Follow-up Study was funded by grant 1U01DK094830 from the National Institute of Diabetes and Digestive and Kidney Diseases and the Eunice Kennedy Shriver National Institute of Child Health and Human Development. The HAPO Follow-up Study data were collected and managed using REDCap electronic data capture tools hosted at Northwestern University Feinberg School of Medicine. REDCap is supported at Feinberg School of Medicine by the Northwestern University Clinical and Translational Science Institute. The research reported in this article was supported, in part by grant UL1TR001422 from the National Center for Advancing Translational Sciences, National Institutes of Health. This ancillary study was also partially supported by grants from the National Institutes of Health/National Institute of Environmental Health Sciences (5R01ES027011) awarded to MEM.

Keywords

Child exposure/ Health
Dietary exposure
Disease
Environmental monitoring
Health studies
Metals

ASJC Scopus subject areas

Epidemiology
Toxicology
Pollution
Public Health, Environmental and Occupational Health

UN SDGs

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

Access to Document

10.1038/s41370-022-00511-z

Cite this

El Muayed, M., Wang, J. C., Wong, W. P., Metzger, B. E., Zumpf, K. B., Gurra, M. G., Sponenburg, R. A., Hayes, M. G., Scholtens, D. M., Lowe, L. P., & Lowe, W. L. (2023). Urinary metal profiles in mother-offspring pairs and their association with early dysglycemia in the International Hyperglycemia and Adverse Pregnancy Outcome Follow Up Study (HAPO-FUS). Journal of Exposure Science and Environmental Epidemiology, 33(6), 855-864. https://doi.org/10.1038/s41370-022-00511-z

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abstract = "Background: Variations in dietary intake and environmental exposure patterns of essential and non-essential trace metals influence many aspects of human health throughout the life span. Objective: To examine the relationship between urine profiles of essential and non-essential metals in mother-offspring pairs and their association with early dysglycemia. Methods: Herein, we report findings from an ancillary study to the international Hyperglycemia and Adverse Pregnancy Outcome Follow-Up Study (HAPO-FUS) that examined urinary essential and non-essential metal profiles from mothers and offspring ages 10–14 years (1012 mothers, 1013 offspring, 968 matched pairs) from 10 international sites. Results: Our analysis demonstrated a diverse exposure pattern across participating sites. In multiple regression modelling, a positive association between markers of early dysglycemia and urinary zinc was found in both mothers and offspring after adjustment for common risk factors for diabetes. The analysis showed weaker, positive, and negative associations of the 2-h glucose value with urinary selenium and arsenic respectively. A positive association between 2-h glucose values and cadmium was found only in mothers in the fully adjusted model when participants with established diabetes were excluded. There was a high degree of concordance between mother and offspring urinary metal profiles. Mother-to-offspring urinary metal ratios were unique for each metal, providing insights into changes in their homeostasis across the lifespan. Significance: Urinary levels of essential and non-essential metals are closely correlated between mothers and their offspring in an international cohort. Urinary levels of zinc, selenium, arsenic, and cadmium showed varying degrees of association with early dysglycemia in a comparatively healthy cohort with a low rate of preexisting diabetes. Impact statement: Our data provides novel evidence for a strong correlation between mother and offspring urinary metal patterns with a unique mother-to-offspring ratio for each metal. The study also provides new evidence for a strong positive association between early dysglycemia and urinary zinc, both in mothers and offspring. Weaker positive associations with urinary selenium and cadmium and negative associations with arsenic were also found. The low rate of preexisting diabetes in this population provides the unique advantage of minimizing the confounding effect of preexisting, diabetes related renal changes that would alter the relationship between dysglycemia and renal metal excretion.",

keywords = "Child exposure/ Health, Dietary exposure, Disease, Environmental monitoring, Health studies, Metals",

author = "{El Muayed}, Malek and Wang, {Janice C.} and Wong, {Winifred P.} and Metzger, {Boyd E.} and Zumpf, {Katelyn B.} and Gurra, {Miranda G.} and Sponenburg, {Rebecca A.} and Hayes, {M. Geoffrey} and Scholtens, {Denise M.} and Lowe, {Lynn P.} and Lowe, {William L.}",

note = "Publisher Copyright: {\textcopyright} 2022, The Author(s), under exclusive licence to Springer Nature America, Inc.",

year = "2023",

month = nov,

doi = "10.1038/s41370-022-00511-z",

language = "English (US)",

volume = "33",

pages = "855--864",

journal = "Journal of Exposure Science and Environmental Epidemiology",

issn = "1559-0631",

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El Muayed, M, Wang, JC, Wong, WP, Metzger, BE, Zumpf, KB, Gurra, MG, Sponenburg, RA, Hayes, MG , Scholtens, DM, Lowe, LP & Lowe, WL 2023, 'Urinary metal profiles in mother-offspring pairs and their association with early dysglycemia in the International Hyperglycemia and Adverse Pregnancy Outcome Follow Up Study (HAPO-FUS)', Journal of Exposure Science and Environmental Epidemiology, vol. 33, no. 6, pp. 855-864. https://doi.org/10.1038/s41370-022-00511-z

Urinary metal profiles in mother-offspring pairs and their association with early dysglycemia in the International Hyperglycemia and Adverse Pregnancy Outcome Follow Up Study (HAPO-FUS). / El Muayed, Malek; Wang, Janice C.; Wong, Winifred P. et al.
In: Journal of Exposure Science and Environmental Epidemiology, Vol. 33, No. 6, 11.2023, p. 855-864.

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

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T1 - Urinary metal profiles in mother-offspring pairs and their association with early dysglycemia in the International Hyperglycemia and Adverse Pregnancy Outcome Follow Up Study (HAPO-FUS)

AU - El Muayed, Malek

AU - Wang, Janice C.

AU - Wong, Winifred P.

AU - Metzger, Boyd E.

AU - Zumpf, Katelyn B.

AU - Gurra, Miranda G.

AU - Sponenburg, Rebecca A.

AU - Hayes, M. Geoffrey

AU - Scholtens, Denise M.

AU - Lowe, Lynn P.

AU - Lowe, William L.

PY - 2023/11

Y1 - 2023/11

N2 - Background: Variations in dietary intake and environmental exposure patterns of essential and non-essential trace metals influence many aspects of human health throughout the life span. Objective: To examine the relationship between urine profiles of essential and non-essential metals in mother-offspring pairs and their association with early dysglycemia. Methods: Herein, we report findings from an ancillary study to the international Hyperglycemia and Adverse Pregnancy Outcome Follow-Up Study (HAPO-FUS) that examined urinary essential and non-essential metal profiles from mothers and offspring ages 10–14 years (1012 mothers, 1013 offspring, 968 matched pairs) from 10 international sites. Results: Our analysis demonstrated a diverse exposure pattern across participating sites. In multiple regression modelling, a positive association between markers of early dysglycemia and urinary zinc was found in both mothers and offspring after adjustment for common risk factors for diabetes. The analysis showed weaker, positive, and negative associations of the 2-h glucose value with urinary selenium and arsenic respectively. A positive association between 2-h glucose values and cadmium was found only in mothers in the fully adjusted model when participants with established diabetes were excluded. There was a high degree of concordance between mother and offspring urinary metal profiles. Mother-to-offspring urinary metal ratios were unique for each metal, providing insights into changes in their homeostasis across the lifespan. Significance: Urinary levels of essential and non-essential metals are closely correlated between mothers and their offspring in an international cohort. Urinary levels of zinc, selenium, arsenic, and cadmium showed varying degrees of association with early dysglycemia in a comparatively healthy cohort with a low rate of preexisting diabetes. Impact statement: Our data provides novel evidence for a strong correlation between mother and offspring urinary metal patterns with a unique mother-to-offspring ratio for each metal. The study also provides new evidence for a strong positive association between early dysglycemia and urinary zinc, both in mothers and offspring. Weaker positive associations with urinary selenium and cadmium and negative associations with arsenic were also found. The low rate of preexisting diabetes in this population provides the unique advantage of minimizing the confounding effect of preexisting, diabetes related renal changes that would alter the relationship between dysglycemia and renal metal excretion.

AB - Background: Variations in dietary intake and environmental exposure patterns of essential and non-essential trace metals influence many aspects of human health throughout the life span. Objective: To examine the relationship between urine profiles of essential and non-essential metals in mother-offspring pairs and their association with early dysglycemia. Methods: Herein, we report findings from an ancillary study to the international Hyperglycemia and Adverse Pregnancy Outcome Follow-Up Study (HAPO-FUS) that examined urinary essential and non-essential metal profiles from mothers and offspring ages 10–14 years (1012 mothers, 1013 offspring, 968 matched pairs) from 10 international sites. Results: Our analysis demonstrated a diverse exposure pattern across participating sites. In multiple regression modelling, a positive association between markers of early dysglycemia and urinary zinc was found in both mothers and offspring after adjustment for common risk factors for diabetes. The analysis showed weaker, positive, and negative associations of the 2-h glucose value with urinary selenium and arsenic respectively. A positive association between 2-h glucose values and cadmium was found only in mothers in the fully adjusted model when participants with established diabetes were excluded. There was a high degree of concordance between mother and offspring urinary metal profiles. Mother-to-offspring urinary metal ratios were unique for each metal, providing insights into changes in their homeostasis across the lifespan. Significance: Urinary levels of essential and non-essential metals are closely correlated between mothers and their offspring in an international cohort. Urinary levels of zinc, selenium, arsenic, and cadmium showed varying degrees of association with early dysglycemia in a comparatively healthy cohort with a low rate of preexisting diabetes. Impact statement: Our data provides novel evidence for a strong correlation between mother and offspring urinary metal patterns with a unique mother-to-offspring ratio for each metal. The study also provides new evidence for a strong positive association between early dysglycemia and urinary zinc, both in mothers and offspring. Weaker positive associations with urinary selenium and cadmium and negative associations with arsenic were also found. The low rate of preexisting diabetes in this population provides the unique advantage of minimizing the confounding effect of preexisting, diabetes related renal changes that would alter the relationship between dysglycemia and renal metal excretion.

KW - Child exposure/ Health

KW - Dietary exposure

KW - Disease

KW - Environmental monitoring

KW - Health studies

KW - Metals

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El Muayed M, Wang JC, Wong WP, Metzger BE, Zumpf KB, Gurra MG et al. Urinary metal profiles in mother-offspring pairs and their association with early dysglycemia in the International Hyperglycemia and Adverse Pregnancy Outcome Follow Up Study (HAPO-FUS). Journal of Exposure Science and Environmental Epidemiology. 2023 Nov;33(6):855-864. doi: 10.1038/s41370-022-00511-z

Urinary metal profiles in mother-offspring pairs and their association with early dysglycemia in the International Hyperglycemia and Adverse Pregnancy Outcome Follow Up Study (HAPO-FUS)

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UN SDGs

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