Per- and Polyfluoroalkyl Substances and Breastfeeding as a Vulnerable Function: A Systematic Review of Epidemiological Studies
Abstract
:1. Introduction
2. Materials and Methods
3. Results
3.1. Study Characteristics
3.2. Study Risk of Bias Assessment
3.3. Breastfeeding Initiation
3.4. Exclusive Breastfeeding
3.5. Total Breastfeeding
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Facet 1 | PFAS Perfluoroalkyl substances Polyfluoroalkyl substances PFOS PFOA |
Facet 2 | Breastfeeding (Title) Breast Feeding (Mesh/key term) |
Restrictions | English language |
Exclusions | Reviews |
PubMed Search | (“PFAS” OR “Perfluoroalkyl Substances” OR “polyfluoroalkyl substances” OR “PFOS” OR “PFOA”) AND (“Breastfeeding” [Title] OR “Breast Feeding” [Mesh]) NOT (Review [Publication Type]) Filter: “English” |
Embase (Ovid) Search | (1) PFAS.af. (2) Perfluoroalkyl Substances.af. (3) Polyfluoroalkyl substances.af. (4) PFOS.af. (5) PFOA.af. (6) Breastfeeding.m_titl. (7) exp breast feeding/ (8) 1 or 2 or 3 or 4 or 5 (9) 6 or 7 (10) 8 and 9 (11) limit 10 to English language (12) limit 11 to “review” (13) 11 not 12 |
Population | Human: Pregnant women or new mothers |
Exposure | Per- and polyfluoroalkyl substance (PFAS) exposure |
Comparator | Increasing exposure or high versus low exposure |
Outcomes | Total duration of breastfeeding Duration of exclusive breastfeeding Breastfeeding initiation |
First Author (Publication Year) | Country | Study Design | N | PFAS Concentrations (Median, ng/mL) | Breastfeeding Duration (Median, Months) |
---|---|---|---|---|---|
Fei et al. (2010) [40] | Denmark | Prospective cohort study: Danish National Birth Cohort with data collection in years 1996–2002. | 1346 | PFOS: 33.4 PFOA: 5.2 | Total: 7.9 Exclusive: 3.9 |
Romano et al. (2016) [45] | USA | Prospective cohort study: The Health Outcomes and Measures of the Environment study with data collection in years 2003–2006. | 336 | PFOS: 13.9 PFOA: 5.5 PFHxS: 1.5 PFNA: 1.0 | Total: 6 1 Exclusive: 0.07 1 |
Timmerman et al. (2017) [44] | Faroe Islands | Prospective cohort study: Two birth cohorts with data collection in years 1997–2000 and 2007–2009. | 987 | PFOS: 19.5 PFOA: 2.4 PFHxS: 1.5 PFNA: 0.6 PFDA: 0.3 | Total: 9 Exclusive: 5 |
Rosen et al. (2018) [42] | Norway | Prospective cohort study: Norwegian Mother and Child Cohort Study with data collection in years 1999–2008. | 1716 | PFOS: 12.9 PFOA: 2.56 PFHxS: 0.64 PFNA: 0.45 PFDA: 0.09 PFHpS: 0.14 PFUnDA: 0.19 PFDoDA: 0.04 PFTrDA: 0.04 | Total: > 6 2 Exclusive: NA |
Nielsen et al. (2022) [41] | Sweden | Natural experiment (contamination of drinking water): Municipality of Ronneby plus reference group from nearby municipality, children born in years 1999–2009. | 2374 | NA 3 | Total: 6–7 Exclusive: NI |
Timmermann et al. (2022) [43] | Denmark | Prospective cohort study: Odense Child Cohort with data collection in years 2010–2012. | 925 | PFOS: 7.56 PFOA: 1.68 PFHxS: 0.35 PFNA: 0.64 PFDA: 0.29 ∑PFAS: 10.86 | Total: 7.6 Exclusive: 2.5 |
First Author (Publication Year) | Statistical Analysis Model | Effect Estimate |
---|---|---|
Fei et al. (2010) [40] | Cox regression + logistic regression |
|
Romano et al. (2016) [45] | Poisson regression with robust standard errors + Cox regression |
|
Timmerman et al. (2017) [44] | Linear regression |
|
Rosen et al. (2018) [42] | Cox regression with censoring at 3 or 6 months + logistic regression. Excluded women who never initiated breastfeeding. |
|
Nielsen et al. (2022) [41] | Modified Poisson regression with robust error variance + Cox regression with censoring at 6/12 months for exclusive/total breastfeeding |
|
Timmermann et al. (2022) [43] | Cox regression. Women terminating breastfeeding for reasons not related to insufficient lactation or with no reason given were censured. |
|
First Author (Publication Year) | Bias Due to Confounding | Bias Arising from Measurement of the Exposure | Bias in Selection of Participants | Bias Due to Post-Exposure Interventions | Bias Due to Missing Data | Bias Arising from Measurements of the Outcome | Bias in Selection of the Reported Results | Overall Risk of Bias | |
---|---|---|---|---|---|---|---|---|---|
Confounding from Previous Breastfeeding | Other Confounding | ||||||||
Fei et al. (2010) [40] | Low risk. Stratification by parity. | Low risk. Adjusted for parity, maternal age at delivery, pre-pregnancy body mass index, maternal socioeconomic status, alcohol consumption, and smoking during pregnancy, and gestational age at blood drawing. | Low risk. Blood samples, GA 4–14 weeks. | Low risk. Selection was not affected by the exposure or outcome. | Low risk. Participants were unaware of their exposure. | Low risk. Few data were missing and controlled for. | Low risk of bias towards null. Interviews at 6 and 18 months after birth. | Low risk. Multiple analyses were performed, but all estimates were provided. | Low |
Romano et al. (2016) [45] | Low risk. Adjustment for total duration of breastfeeding previous children and stratification by parity. | Low risk. Adjusted for parity, maternal age, race/ethnicity, marital status, household income, maternal serum cotinine during pregnancy, alcohol use during pregnancy, and gestational week at blood draw. | Low risk of bias towards null. Blood samples, GA 16 weeks (85%), 26 weeks (10%), or delivery (5%). | Low risk. Selection was not affected by the exposure or outcome. | Low risk. Participants were unaware of their exposure. | Low risk. The proportion of missing data was most likely similar across groups. | Low risk of bias towards null. Standardized surveys by phone every 3 months until breastfeeding was discontinued or the child’s third birthday. | Low risk. Multiple analyses were performed, but all estimates were provided. | Low |
Timmerman et al. (2017) [44] | Low risk. Tested interaction between PFAS and parity. | Low risk. Adjusted for parity, cohort, maternal age, pre-pregnancy BMI, pregnancy alcohol intake, pregnancy smoking, education, and employment. | Low risk of bias towards null. Blood samples, GA 34–36 weeks (older cohort) or two weeks after their term date (younger cohort). | Low risk. Selection was not affected by the exposure or outcome. | Low risk. Participants were unaware of their exposure. | Low risk. Few data were missing and controlled for. | Low risk of bias towards null. Questionnaire followed by an interview at 18 months (only younger cohort) and 5 years after birth. | Low risk. Multiple analyses were performed, but all estimates were provided. | Low |
Rosen et al. (2018) [42] | Low risk. Adjustment for previous breastfeeding duration and stratification by parity. | Low risk. Adjusted for parity, maternal age at birth, smoking during pregnancy, pre-pregnancy BMI, and prior study status. | Low risk. Blood samples GA 17–20 weeks. | Low risk. Combined data from two prior nested case-control studies. Selection was not affected by the exposure or outcome. | Low risk. Participants were unaware of their exposure. | Low risk. Missing data were imputed using the Markov chain Monte Carlo method. | Low risk of bias towards null. Self-reported questionnaire 6 months after delivery. | Low risk. Multiple analyses were performed, but all estimates were provided. | Low |
Nielsen et al. (2022) [41] | Low risk. Use of residential address (and stratification by parity). | Low risk. Adjusted for parity, maternal age, BMI, education level, country of birth, and tobacco use during pregnancy. | Low risk of bias towards null. Residential addresses of mothers during the 5-year window before delivery. | Low risk. Participants were selected based on residential address. Selection was not related to the outcome. | Low risk. Participants were aware of their exposure risk, but all were advised to breastfeed. | Low risk. Few data were missing. | Moderate risk of bias towards null. Child health care charts. Information on breastfeeding and formula feeding was available monthly during the first year and less frequently thereafter. | Low risk. Multiple analyses were performed, but all estimates were provided. | Low |
Timmermann et al. (2022) [43] | Low risk. Tested interaction between PFAS and parity. | Low risk. Adjusted for education, body mass index, national origin, and expectations of giving formula, parity, smoking, duration of previous breastfeeding, and previous inadequate lactation. | Low risk. Blood samples, median GA 12 weeks (5th–95th percentiles, 10–16 weeks). | Low risk. Selection was not affected by the exposure or outcome. | Low risk. Participants were unaware of their exposure. | Low risk. The proportion of missing data was most likely similar across groups. | Low risk of bias towards null. Self-reported questionnaire 3 and 18months post-partum. Weekly text messages from a subgroup of women. Additional information from health visitor contacts for early weaners. | Low risk. Multiple analyses were performed, but all estimates were provided. | Low |
First Author (Publication Year) | Total Breastfeeding (All) | Total Breastfeeding (Primiparous) | Exclusive Breastfeeding (All) | Exclusive Breastfeeding (Primiparous) | Author Conclusion |
---|---|---|---|---|---|
Fei et al. (2010) [40] | PFOS: HR: 1.40 (1.18; 1.65) OR 3: 1.89 (1.19; 3.01) OR 6: 2.07 (1.46; 2.93) OR 3-ng/mL: 1.17 (1.04; 1.32) OR 6-ng/mL: 1.19 (1.09; 1.31) PFOA: HR: 1.40 (1.17; 1.68) OR 3: 2.68 (1.60; 4.50) OR 6: 2.60 (1.78; 3.81) OR 3-ng/mL: 1.09 (1.02; 1.15) OR 6-ng/mL: 1.10 (1.05; 1.16) | PFOS: HR: 1.17 (0.90; 1.52) OR 3: 1.24 (0.62–2.46) OR 6: 1.52 (0.89; 2.60) OR 3-ng/mL: 1.12 (0.94; 1.34) OR 6-ng/mL: 1.20 (1.04; 1.37) PFOA: HR: 0.98 (0.69; 1.38) OR 3: 1.82 (0.66; 5.07) OR 6: 1.50 (0.74; 3.06) OR 3-ng/mL: 1.02 (0.93; 1.10) OR 6-ng/mL: 1.03 (0.97; 1.10) | PFOS: HR: 1.37 (1.14; 1.64) OR 1: 1.55 (0.89; 2.71) OR 4: 1.86 (1.24; 2.79) OR 1-ng/mL: 1.09 (0.93; 1.27) OR 4-ng/mL: 1.14 (1.02; 1.27) PFOA: HR: 1.37 1.12–1.69 OR 1: 2.19 1.16; 4.14 OR 4: 2.59 1.66; 4.04 OR 1-ng/mL: 1.05 (0.98; 1.13) OR 4-ng/mL: 1.06 (1.00; 1.12) | PFOS: HR: 1.23 (0.93; 1.64) OR 1: 0.78 (0.35; 1.70) OR 4: 1.19 (0.66; 2.15) OR 1-ng/mL: 0.98 (0.78; 1.23) OR 4-ng/mL: 1.04 (0.89; 1.22) PFOA: HR: 1.16 0.81; 1.66 OR 1: 0.55 0.21;1.42 OR 4: 0.91 0.43;1.89 OR 1-ng/mL: (0.93 0.82; 1.06) OR 4-ng/mL: (0.98 (0.91; 1.06) | These findings suggest that PFOA and PFOS may reduce the ability to lactate, but could equally reflect reverse causation since no association was seen in primiparous women. |
Romano et al. (2016) [45] | PFOS: | PFOS: | PFOS: | Maternal serum PFOA concentrations were inversely related to the duration of any breastfeeding. Maternal serum PFAS concentrations were not associated with exclusive breastfeeding. | |
RR 3: 1.32 (0.97; 1.79) | RR 3: 1.21 (0.71; 2.08) 1 | RR 3: 0.98 (0.87; 1.10) | |||
RR 6: 1.25 (0.98; 1.58) | RR 6: 1.07 (0.70; 1.61) 1 | ||||
PFOA: | PFOA: | PFOA: | |||
HR: 1.13 (0.95; 1.35) | RR 3: 2.17 (1.17; 4.01) 1 | RR 3: 1.12 (0.98; 1.28) | |||
RR 3: 1.77 (1.23; 2.54) | RR 6: 1.41 (0.85; 2.32) 1 | ||||
RR 6: 1.41 (1.06; 1.87) | |||||
PFHxS: | PFHxS: | ||||
RR 3: 1.39 (0.99; 1.96) | RR 3: 0.94 (0.84; 1.06) | ||||
RR 6: 1.22 (0.96; 1.55) | |||||
PFNA: | PFNA: | ||||
RR 3: 1.12 (0.81; 1.53) | RR 3: 0.96 (0.85; 1.08) | ||||
RR 6: 1.13 (0.90; 1.43) | |||||
Timmerman et al. (2017) [44] | PFOS months: −1.4 (−2.1; −0.6) PFOA months: −1.3 (−1.9; −0.7) PFHxS months: −0.2 (−0.5; 0.2) PFNA months: −1.3 (−2.0; −0.7) PFDA months: −0.8 (−1.4; −0.3) | PFOS months: −1.3 (−2.3; −0.3) PFOA months: −1.1 (−2.0; −0.1) PFHxS months: −0.1 (−0.5; 0.3) PFNA months: −1.6 (−2.6; −0.6) PFDA months: −1.6 (−2.6; −0.7) | PFOS months: −0.3 (−0.6; −0.1) PFOA months: −0.5 (−0.7; −0.3) PFHxS months: −0.1 (−0.2; 0.1) PFNA months: −0.2 (−0.5; −0.0) PFDA months: −0.2 (−0.4; 0.0) | PFOS months: −0.2 (−0.6; 0.1) PFOA months: −0.4 (−0.8; 0.0) PFHxS months: −0.0 (−0.1; 0.1) PFNA months: −0.3 (−0.8; 0.1) PFDA months: −0.5 (−0.9; −0.1) | Increased maternal serum PFAS concentrations are associated with a decreased duration of breastfeeding. |
Rosen et al. (2018) [42] | PFOS: | PFOS: | Unexpected observation of inverse associations of PFNA, PFDA, and PFUnDA with breastfeeding cessation. A positive association of PFOS with breastfeeding was observed when accounting for other exposures. No association between PFOA and breastfeeding was observed. | ||
HR 3: 1.01 (0.84; 1.21) | HR 3: 0.94 (0.77; 1.16) | ||||
HR 6: 0.99 (0.87; 1.14) | HR 6: 0.94 (0.81; 1.09) | ||||
OR 3: 0.99 (0.80; 1.21) | |||||
OR 6: 0.98 (0.83; 1.14) | |||||
PFOA: | PFOA: | ||||
HR 3: 0.85 (0.68; 1.06) | HR 3: 0.84 (0.67; 1.04) | ||||
HR 6: 0.94 (0.80; 1.11) | HR 6: 0.91 (0.78; 1.06) | ||||
OR 3: 0.84 (0.66; 1.08) | |||||
OR 6: 0.95 (0.79; 1.15) | |||||
PFHxS: | PFHxS: | ||||
HR 3: 0.88 (0.75; 1.03) | HR 3: 0.93 (0.78; 1.11) | ||||
HR 6: 0.92 (0.82; 1.03) | HR 6: 0.96 (0.84; 1.09) | ||||
OR 3: 0.86 (0.72; 1.03) | |||||
OR 6: 0.91 (0.80; 1.05) | |||||
PFNA: | PFNA: | ||||
HR 3: 0.77 (0.63; 0.93) | HR 3: 0.72 (0.58; 0.88) | ||||
HR 6: 0.84 (0.73; 0.97) | HR 6: 0.81 (0.69; 0.95) | ||||
OR 3: 0.73 (0.59; 0.91) | |||||
OR 6: 0.83 (0.70; 0.98) | |||||
PFDA: | PFDA: | ||||
HR 3: 0.73 (0.62; 0.86) | HR 3: 0.69 (0.58; 0.82) | ||||
HR 6: 0.82 (0.72; 0.92) | HR 6: 0.78 (0.68; 0.89) | ||||
OR 3: 0.70 (0.58; 0.84) | |||||
OR 6: 0.80 (0.69; 0.93) | |||||
PFHpS: | PFHpS: | ||||
HR 3: 0.96 (0.81; 1.14) | HR 3: 0.95 (0.77; 1.16) | ||||
HR 6: 0.96 (0.85; 1.08) | HR 6: 0.96 (0.83; 1.11) | ||||
OR 3: 0.96 (0.79; 1.15) | |||||
OR 6: 0.96 (0.83; 1.11) | |||||
PFUnDA: | PFUnDA: | ||||
HR 3: 0.73 (0.62; 0.86) | HR 3: 0.68 (0.57; 0.81) | ||||
HR 6: 0.81 (0.72; 0.93) | HR 6: 0.78 (0.68; 0.90) | ||||
OR 3: 0.70 (0.58; 0.84) | |||||
OR 6: 0.79 (0.68; 0.91) | |||||
PFDoDA: | PFDoDA: | ||||
HR 3: 0.97 (0.68; 1.41) | HR 3: 0.97 (0.64; 1.46) | ||||
HR 6: 0.90 (0.69; 1.17) | HR 6: 0.88 (0.65; 1.19) | ||||
OR 3: 0.97 (0.65; 1.45) | |||||
OR 6: 0.88 (0.65; 1.19) | |||||
PFTrDA: | PFTrDA: | ||||
HR 3: 0.99 (0.69; 1.40) | HR 3: 0.87 (0.58; 1.30) | ||||
HR 6: 0.98 (0.76; 1.26) | HR 6: 0.98 (0.74; 1.29) | ||||
OR 3: 0.97 (0.66; 1.43) | |||||
OR 6: 0.97 (0.72; 1.29) | |||||
Nielsen et al. (2022) [41] | ∑PFAS: RR initiation: 2.37 (0.84; 6.69) RR 6: 1.17 (0.07–1.40) HR 0: 1.58 (1.12; 2.22) HR 3: 1.32 (1.06; 1.63) HR 6: 1.09 (0.93; 1.29) HR 10: 0.86 (0.65; 1.14) | ∑PFAS: RR initiation: 2.92 (0.34; 23.01) RR 6: 1.56 (1.16; 2.11) HR 0: 2.49 (1.50; 4.14) HR 3: 1.82 (1.32; 2.51) HR 6: 1.33 (1.05; 1.69) HR 10: 0.88 (0.59; 1.30) | ∑PFAS: RR 3: 1.12 (0.92; 1.37) HR: 1.14 (0.92; 1.40) | ∑PFAS: RR 3: 1.21 (0.92; 1.61) HR: 1.30 (0.96; 1.76) | Exposure to high levels of PFAS seemed to be associated with increased risks of not initiating breastfeeding and shorter breastfeeding duration in primiparous women. The findings imply that the ability of first-time mothers to establish breastfeeding is a sensitive outcome after high exposure to PFAS. |
Timmermann et al. (2022) [43] | PFOS HR: 1.18 (1.05; 1.33) PFOA HR: 1.17 (1.05; 1.31) PFHxS HR: 1.05 (0.96; 1.14) PFNA HR: 1.17 (1.04; 1.31) PFDA HR: 1.02 (0.93; 1.12) ∑PFAS HR: 1.23 (1.08; 1.40) | PFOS HR: 1.15 (1.00; 1.33) PFOA HR: 1.19 (1.04; 1.37) PFHxS HR: 1.04 (0.93; 1.16) PFNA HR: 1.18 (1.02; 1.36) PFDA HR: 1.03 (0.91; 1.16) ∑PFAS HR: 1.21 (1.03; 1.43) | PFOS HR: 0.94 (0.85; 1.04) PFOA HR: 1.02 (0.93; 1.12) PFHxS HR: 0.92 (0.86; 0.98) PFNA HR: 0.91 (0.82; 1.01) PFDA HR: 0.97 (0.89; 1.06) ∑PFAS HR: 0.94 (0.84; 1.05) | PFOS HR: 0.95 (0.84; 1.08) PFOA HR: 0.98 (0.87; 1.12) PFHxS HR: 0.94 (0.85; 1.03) PFNA HR: 0.89 (0.78; 1.02) PFDA HR: 0.97 (0.86; 1.09) ∑PFAS HR: 0.94 (0.81; 1.09) | Higher serum PFAS concentrations were associated with a shorter duration of breastfeeding. |
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Timmermann, A.; Avenbuan, O.N.; Romano, M.E.; Braun, J.M.; Tolstrup, J.S.; Vandenberg, L.N.; Fenton, S.E. Per- and Polyfluoroalkyl Substances and Breastfeeding as a Vulnerable Function: A Systematic Review of Epidemiological Studies. Toxics 2023, 11, 325. https://doi.org/10.3390/toxics11040325
Timmermann A, Avenbuan ON, Romano ME, Braun JM, Tolstrup JS, Vandenberg LN, Fenton SE. Per- and Polyfluoroalkyl Substances and Breastfeeding as a Vulnerable Function: A Systematic Review of Epidemiological Studies. Toxics. 2023; 11(4):325. https://doi.org/10.3390/toxics11040325
Chicago/Turabian StyleTimmermann, Amalie, Oyemwenosa N. Avenbuan, Megan E. Romano, Joseph M. Braun, Janne S. Tolstrup, Laura N. Vandenberg, and Suzanne E. Fenton. 2023. "Per- and Polyfluoroalkyl Substances and Breastfeeding as a Vulnerable Function: A Systematic Review of Epidemiological Studies" Toxics 11, no. 4: 325. https://doi.org/10.3390/toxics11040325