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Association between heavy metal exposures and the prevalence of pelvic inflammatory disease: a cross-sectional study from the National Health and Nutrition Examination Survey 2013–2018

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Abstract

Pelvic inflammatory disease (PID) is a common medical condition in women. However, the correlation between exposure to heavy metals, including cadmium (Cd), lead (Pb), manganese (Mn), mercury (Hg), and selenium (Se), and PID, is unclear. Using a large sample size from the National Health and Nutrition Examination Survey, these relationships were studied and verified. PID diagnosis was acquired through a self-reported questionnaire (2013–2018). Heavy metal exposure (Cd, Pb, Mn, Hg, and Se) was measured using mass spectrometry of blood samples. Covariate data were obtained through questionnaires and physical tests. Individuals with complete covariate data were included in the study. The relationship between heavy metal exposure (Cd, Pb, Mn, Hg, and Se) and PID was demonstrated using logistic regression analysis, weighted quantile sum (WQS) regression analysis, and restricted cubic splines (RCS). Overall, 2743 participants were included. Of these, 183 were diagnosed with PID. Through weighted univariate and multivariate regression analyses, the heavy metals of Cd and Pb were positively correlated with the prevalence of PID. However, no significant relationship was observed in the heavy metals of Mn, Hg, and Se. The joint effect of heavy metals further confirmed the important role of Cd and Pb in WQS analysis. After visualizing the RCS, significant curved and linear relationships were observed for Cd and Pb, respectively. Most subgroup analyses confirmed these results. In conclusion, exposure to Cd was nonlinearly correlated with the risk of PID, whereas exposure to Pb showed a linear relationship. Our findings increase the awareness of the environmental effects of exposure to heavy metals in PID. However, further studies are needed to elucidate the causality and underlying mechanisms between heavy metal exposure and the prevalence of PID.

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Data availability

Data used in this study are publicly available (https://www.cdc.gov/nchs/nhanes).

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Acknowledgements

The authors thank all NHANES participants, staff, and investigators. We thank Zhang Jing (Shanghai Tongren Hospital) for “nhanesR” assistance with the NHANES database. We thank Editage for linguistic editing and proofreading the manuscript.

Funding

This study was supported by Shanghai Committee of Science and Technology (23S21900400) National Nature Science Foundation of China (NO. 82305284), and the Siming Research Project in Shuguang Hospital Affiliated to ShangHai University of Traditional Chinese Medicine (SGKY-)202306.

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Author notes

  1. Panwei Hu, Hui Hu, and Xiaomei Jiang contributed equally.

Authors and Affiliations

  1. Department of Obstetrics and Gynecology, Shuguang Hospital Affiliated to Shanghai University of Traditional Chinese Medicine, Shanghai, 201210, China

    Panwei Hu, Hui Hu, Cong Qi, Peizhi He & Qinhua Zhang

  2. Department of Obstetrics and Gynecology, Seventh People’s Hospital of Shanghai University of Traditional Chinese Medicine, Shanghai, 200137, China

    Xiaomei Jiang

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  1. Panwei Hu
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Contributions

Panwei Hu and Xiaomei Jiang: manuscript drafting, study design, data analysis, and interpretation. Xiaomei Jiang: study design. Hui Hu: study concept. Cong Qi, Peizhi He, and Qinhua Zhang: revision and supervision of the article. All authors provided final approval for the version to be published.

Corresponding author

Correspondence to Qinhua Zhang.

Ethics declarations

Ethics approval and consent to participate

The National Center for Health Statistics Ethics Review Board approved the project (https://www.cdc.gov/nchs/nhanes/irba98.htm). Written informed consent was obtained in advance from all participants, and no external ethical approval was required as the National Center for Health Statistics Ethics Review Board approved all research.

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The authors declare no competing interests.

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Responsible Editor: Lotfi Aleya

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Highlights

• To date, the association between heavy metal exposures and pelvic inflammatory disease (PID) is uncertain.

• There were significant associations between exposure to metals (cadmium and lead) and the risk of PID, while no significant relationship was observed in the heavy metals of manganese, mercury, and selenium.

• Significant curved and linear relationships were observed for cadmium and lead, respectively.

• This study raises public health concerns associated with the environmental effects of exposure to heavy metals in the prevalence of PID.

Supplementary information

ESM 1

(DOCX 26 kb)

Supplementary Fig.1

The WQS analysis between heavy metals and the risk for PID (n = 3384 after imputation). The analysis was adjusted for all covariates (age, BMI, diabetes mellitus, education attainment, hypertension, marital status, poverty, pregnant history, race, regular period) is shown. WQS weighted quantile sum, PID pelvic inflammatory disease, BMI body mass index, OR Odds ratios, 95% CI 95% confidence intervals (PNG 112 kb)

High resolution image (TIF 585 kb)

Supplementary Fig.2

RCS between heavy metals (cadmium and lead) and the risk for PID (n = 3384 after imputation). A. The association between cadmium and PID risk is shown. B. The association between lead and PID risk is shown. This model was adjusted for all covariates (age, BMI, diabetes mellitus, education attainment, hypertension, marital status, poverty, pregnant history, race, regular period). PID pelvic inflammatory disease, BMI body mass index, OR Odds ratios, 95% CI 95% confidence intervals (PNG 136 kb)

High resolution image (TIF 499 kb)

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Hu, ., Hu, H., Jiang, X. et al. Association between heavy metal exposures and the prevalence of pelvic inflammatory disease: a cross-sectional study from the National Health and Nutrition Examination Survey 2013–2018. Environ Sci Pollut Res 30, 112433–112444 (2023). https://doi.org/10.1007/s11356-023-30176-6

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