Association of pre-pregnancy maternal overweight/obesity and dietary intake during pregnancy with the levels of persistent organic pollutants in the human milk of Brazilian women

doi:10.21203/rs.3.rs-2128648/v1

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Association of pre-pregnancy maternal overweight/obesity and dietary intake during pregnancy with the levels of persistent organic pollutants in the human milk of Brazilian women

https://doi.org/10.21203/rs.3.rs-2128648/v1

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published 26 Jan, 2023

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Persistent organic pollutants (POPs) are toxic chemical compounds that can bioaccumulate, adhere to lipid matrices, and affect human health. This study aimed to investigate the association between maternal pre-pregnancy overweight/obesity or dietary intake during pregnancy and POPs concentrations in the human milk of Brazilian women. A total of 77 women were followed from the third trimester of pregnancy until 119 days postpartum. Pregnancy dietary intake, which was estimated using a semi-quantitative food frequency questionnaire, and pre-pregnancy body mass index were collected at baseline. Human milk samples were collected between 2 and 119 days postpartum, and POPs concentrations were analysed using gas chromatography-triple quadrupole mass spectrometry. Multivariate logistic regression and linear regression models were used to investigate the association between pre-pregnancy overweight/obesity, dietary intake during pregnancy, and POPs concentrations in human milk. The analysis was adjusted for the maternal age and schooling, total cholesterol serum levels, and time postpartum and corrected for multiple comparisons using the Benjamini–Hochberg test. Significant associations were observed in the adjusted models between pre-pregnancy overweight/obesity and dichlorodiphenyldichloroethane (ppDDE), polychlorinated biphenyl (PCB)74, PCB138, PCB153, PCB170, PCB180, total PCBs, total 4PCBs, total 2 organochlorine pesticides (OCPs), and total POPs concentrations; and higher daily lipid intake during pregnancy increased human milk hexachlorobenzene (HCB). Collectively, this study showed that pre-pregnancy overweight/obesity and total lipid intake during pregnancy were associated with POPs concentrations in the milk of Brazilian women. To promote adequate nutritional status since preconception and surveillance and control of POP in the environment could be essential to ensure binomial mother-infant health.

Persistent organic pollutants

human milk

dichlorodiphenyltrichloroethane

polychlorinated biphenyls

obesity

pregnancy

Persistent organic pollutants (POPs) are toxic chemical compounds produced by environmental pollutants. They accumulate in living organisms and have long half-lives, can remain in the environment for long periods, bioaccumulate in soil and water, and can be transported with dust by air (UNEP 2017). POPs also exhibit a wide spatial distribution. Therefore, they can be found in places that have never been produced or used (Harrad 2009).

POPs can negatively affect human and animal health by acting as endocrine disruptors and altering hormonally regulated metabolic processes (WHO 2007; Heindel et al. 2017). POPs adherence and maintenance in lipidic body fluids occur because of their lipophilic characteristics. Human lipidic matrices, such as serum and fat tissue, can accumulate these compounds and are considered important for evaluating POPs concentrations in the human body. Interestingly, human milk can be regarded as the main matrix to detect contamination because the POPs levels found in milk can predict maternal risk due to prenatal exposure, which can affect the health of women and infants (UNEP 2017; Müller et al. 2019). Notably, predisposition to the development of obesity is one of the main health risks in infants. The mechanism can be explained by the increased number of adipocytes as well as fat storage in existing adipocytes, changes in the basal metabolic rate, energy balance shift to favour calorie storage, and alteration of hormonal control of appetite and satiety (Grun et al. 2009; Heindel et al. 2015).

Maternal adiposity and dietary intake are critical factors associated with increased POPs concentrations or their presence in lipidic matrices. Maternal adiposity appears to be positively related to POPs concentrations in human milk, although the findings are controversial (Mostafalou et al. 2016; Ellsworth et al. 2020; Gautam et al. 2020). Moreover, dietary intake can also act as an important carrier of POPS if food chain contamination is common. Ultra-processed poultry, fish and seafood, red meat, milk, and eggs are potential food sources for POPs contamination owing to their high fat content (WHO 2007; Aerts et al. 2019; Hu et al. 2021). Additionally, POPs have toxic properties, and because of the possibility of overtaking international boundaries, biomagnification could be considered a public health issue (UNEP 2021).

Owing to these environmental issues mentioned above, global sustainability agendas have been proposed. In 2000, the Millennium Development Goals were published to ensure environmental sustainability (United Nations 2015), and in 2015, the Sustainable Development Goals were published to prevent environmental degradation and promote sustainability, aiming to curb climate change and reduce air, water, and soil pollution and contamination by 2030 (United Nations 2015a). In 2001, the Stockholm Convention was established to eliminate or reduce the emissions of 12 priority POPs in the environment, including polybrominated diphenyl ethers (PBDEs), organochlorine pesticides (OCPs) (such as dichlorodiphenyltrichloroethane [DDT]), and polychlorinated biphenyls (PCBs), mainly in developing countries (UNEP 2019).

Historically, Latin American countries have been more susceptible to environmental impact because of their history of weak environmental policies and economic models based on agriculture with considerable use of defensives and pesticides and activities, such as livestock and mining, which result in the production and release of synthetic organic chemicals (Ryan and Ibarra 2016; UNEP 2019; FAO 2022). Only after the 2000s, the environmental policies began to be strengthened based on a growing body of evidence about the role of environmental pollution in human health (García-Guadilla and Blauert 1992; Ryan and Ibarra 2016).

Considering the historical risk to human health posed by exposure to POPs, investigating the magnitude of POPs contamination in human body fluids in Latin American countries is paramount. To the best of our knowledge, studies investigating the relation between overweight/obesity and dietary intake and multiple POPs in human milk and the main associated factors are scarce in Latin Americans, especially in Brazilian women (Fång et al. 2015; Iribarne-Durán et al. 2022). Therefore, the current study aimed to investigate the association between maternal pre-pregnancy overweight/obesity, dietary intake during pregnancy, and POPs concentrations in the human milk of Brazilian women.

Study design

This study was part of a prospective cohort study that recruited pregnant women between January 2017 and April 2019. The study protocol has been previously described by Ferreira et al. (2020) and Batalha et al. (2021). The study was conducted in a public health care centre in Rio de Janeiro, Brazil. It followed a non-probabilistic sample of 147 women and their infants from the third trimester of pregnancy to 12 months postpartum. This study included women between 18 and 40 years old, in the 28th − 35th gestational weeks, without infectious or chronic diseases (except obesity), with a singleton pregnancy, and who lived in the programmatic area (neighbourhood) and intended to remain living within the catchment area after the child's birth.

A total of 72 women were excluded from the 147 participants: 59 due to a lack of milk samples and 13 due to different factors, including a positive test for syphilis, delivering a stillborn or preterm infant, and chronic disease development (diabetes and hypertension). Women who reported implausible daily energy intake (< 600 or ≥ 6,500 kcal/day) were also excluded (n = 4) (Yonezawa et al. 2020; Panbehkar-Jouybari et al. 2021). The final sample of the present study comprised 77 women who provided one human milk sample between 2 and 119 days postpartum (Fig. 1). The complete dataset was used to obtain the largest possible sample size for women with at least one milk sample in one of three periods; first, samples at 28–50 days postpartum (n = 59) were kept for those women who had samples in two or more different periods; afterwards, women with samples only at 2–18 days postpartum were included, and finally, women with samples only in 88–119 days postpartum were included. This decision was made based on preliminary analyses before exploring the relationship between pre-pregnancy overweight/obesity or maternal dietary intake and POPs concentration.

The study was approved by the Research Ethics Committee of the Maternity School of Rio de Janeiro Federal University (protocol number: 49218115.0.0000.5275) and the Municipal Secretariat of Health and Civil Defense of the State of Rio de Janeiro (protocol number: 49218115.0.0000.5275). The project was carried out following the rules of the Declaration of Helsinki of 1975, and written consent was obtained from all participants freely and spontaneously during the research period.

Pre-pregnancy overweight/obesity and dietary intake during pregnancy

Maternal pre-pregnancy body mass index (BMI) was calculated using self-reported pre-pregnancy weight (kg)/height (m)² measured at 28–50 days postpartum (WHO 1995). Height was measured in duplicate using a stadiometer (Altura Exata, Belo Horizonte, Brazil). A third measurement was performed when a difference higher than 0.5 cm between the first two measurements was observed. In these cases, the mean of two similar measurements was used. The pre-pregnancy overweight/obesity variable was constructed based on the pre-pregnancy BMI categories (i.e., overweight/obesity BMI > 25 kg/m² and normal weight BMI < 25 kg/m²). Two women had BMI < 18.5 kg/m² (18.2 and 18.3 kg/m²), and considering the proximity to the cut-off (18.5 kg/m²), both were arbitrarily grouped in the normal weight category.

A semi-quantitative food frequency questionnaire validated for Brazilian pregnant women was used at baseline to evaluate the usual dietary intake during the pregnancy (Barbieri et al. 2015). Estimates of dietary intake of total lipid, cholesterol, and saturated, monounsaturated, and polyunsaturated fat were considered. All dietary estimates were adjusted for total energy using the residual method (Willett 1997). The dietary intake estimates of ultra-processed food (UPF) were also considered. The UPF group was defined according to the NOVA food classification and included food with the addition of preservatives, synthetic vitamins or minerals, and additives aimed at increasing durability, such as ready-to-eat food (Monteiro et al. 2010). Women who presented an intake with the proportion of energy contribution in the UPF group in the third tertile were regarded as having a high UPF intake. Additionally, food groups with an increased potential for POPs contamination, such as poultry, fish, seafood, red meat, milk, and eggs, were included in the analyses as a sum of daily intake in grams (Aerts et al. 2019; Hu et al. 2021).

Human milk collection and POPs concentration analyses

The participants manually collected 12 mL of milk samples from the same breast at 2–18, 28–50, and 88–119-day visits. The sample collection was performed according to the Brazilian Network of Human Milk Banks protocol and occurred in the morning, ideally before 10 am and after breakfast. A hygiene protocol was followed before collection, including hand sanitisation, face masks, and hair covering. A trained interviewer was available when participants needed help during collection; the interviewer used nitrile gloves and followed the protocol mentioned.

After collection, the aliquoted samples were immediately stored at -20 ºC, transferred to the Federal University of Rio de Janeiro in a temperature-controlled box ( < − 5°C), and stored at -80 ºC. The samples were shipped by aeroplane in a box with dry ice at a temperature below − 80°C, with a temperature monitor to the Finnish Institute for Health and Welfare (THL, Finland), where analyses took place.

The concentrations of POPs were analysed in 200 µL of human milk samples by gas chromatography-triple quadrupole mass spectrometry (GC-MS/MS) with an Agilent 7010 GC-MS/MS system (Wilmington, DE, USA). The POPs analyses included nine OCPs and their metabolites: dichlorodiphenyltrichloroethane (ppDDT), dichlorodiphenyldichloroethene (ppDDE), a-hexachlorocyclohexane (a-HCH), b-HCH, c-HCH, pentachlorobenzene (PeCB), hexachlorobenzene (HCB), transnonachlor and oxychlordane, 11 non-dioxin-like PCB (congeners 28, 52, 74, 99, 101, 138, 153, 170, 180, 183, and 187), two dioxin-like PCBs (congeners 118 and 156), and three polybrominated diphenyl ethers (PBDEs 47, 99, and 153).

POPs detected below the limit of quantification (LOQ) were arbitrarily changed to half the LOQ, where < LOQ refers to the POPs concentrations below the quantification capacity of the method used and not exactly absent (Aerts et al. 2019). Exposure to multiple POPs concentrations was also investigated. The group analyses included 1) the sum of all PCBs, 2) sum of the four most prevalent individual PCB congeners (118, 138, 153, and 180), 3) sum of OCP quantified in ≥ 90% of the samples, and 4) sum of 10 POPs quantified in ≥ 90% of the samples.

Covariables

Self-reported sociodemographic and lifestyle data were collected at the study baseline using a structured questionnaire and comprised maternal age (tertiles: 18–23, 24–29, and 30–40 years), schooling (categorized in 1–9 years [elementary school]; 10–12 years [high school] and 13–18 years [undergraduate education], based on the Brazilian education system )), living with a partner (yes/no), parity (primiparous/multiparous), alcohol intake during pregnancy (yes/no), and physical activity during pregnancy (yes/no). Gestational weight gain was calculated as the difference between the last weight measured during pregnancy collected from the pregnancy passbook and self-reported pre-pregnancy weight. Blood samples were collected by a nursing technician while the women were fasting. Plasma and serum were aliquoted and stored at -80°C until analysis. Serum lipid parameters included total cholesterol, triglycerides, high-density lipoprotein cholesterol, and low-density lipoprotein cholesterol. The enzymatic method was used for the total cholesterol analyses, the enzymatic colourimetric method for triglycerides and high-density lipoprotein cholesterol analyses, and the Martin formula for low-density lipoprotein cholesterol and very-low-density lipoprotein cholesterol analyses.

Statistical analysis

The distribution of variables was analysed using histograms and the Shapiro–Wilk test. Preliminary analyses were performed to investigate the differences between the three periods (2–18, 28–50, and 88–119 days postpartum) in women's profiles (sociodemographic data, reproductive data, biomarkers, and dietary intake) and human milk POPs concentrations. The Kruskal–Wallis test, followed by Dunn's test for multiple comparisons, was used for time comparisons. Differences in POP concentrations are presented as boxplots. The frequency of POPs detection in human milk samples considering the LOQ is shown using a bar plot chart.

A theoretical model was built to determine the main model adjustments according to the literature to investigate the association between maternal pre-pregnancy overweight/obesity and dietary intake during pregnancy and POPs concentration in human milk (Fig. 2). POPs quantified in ≥ 90% samples (LOQ ≥ 90%) were considered continuous variables. Exploratory analyses between dietary intake variables and POPs concentrations were performed using Spearman rank correlation. The Mann–Whitney test was used to evaluate differences in POPs concentrations according to pre-pregnancy BMI categories. Subsequently, multivariate linear regression analysis models were performed with pre-pregnancy BMI categories and pregnancy dietary intake as exposures and POPs concentration as outcomes.

The POPs quantified between 20–90% of the samples were considered categorical variables. The categories were defined as follows: 1) concentrations > LOQ, indicating the presence of POPs in human milk, and 2) concentrations ≤ LOQ, indicating the absence of POPs (Aerts et al. 2019; Porta et al. 2022). Multivariate logistic regression models were used in this categorical POPs. In both linear and logistic regression models, p-values were adjusted for multiple comparisons using the Benjamini-Hochberg test to control the false discovery rate (Benjamini and Hochberg, 1995).

The analyses were adjusted for the following variables: the categorical maternal age (tertiles), as the major age tertiles may indicate higher exposure periods due to bioaccumulation, a characteristic of the POPs (Aerts et al. 2019); the categorical schooling, grouped in educational levels (1–9, 10–12, and 13–18 years) (Grešner et al. 2021; Hassan et al. 2022); the total cholesterol serum level during the third trimester of pregnancy; and the days postpartum when the human milk samples were collected, which were considered confounders because of biological plausibility. All plots and statistical analyses were performed using R, version 4.1.2 (R Core Team 2021). An alpha of 0.05 was adopted for all analyses.

Overall, no differences were observed when comparing maternal demographic, anthropometric, and dietary intake profiles and biochemical parameters of women who attended each visit (Table 1). Additionally, POPs concentrations in human milk, also did not differ among the three visits, except for HCB concentration, which presented higher levels at 28–50 days postpartum compared to 2–18 and 88–119 days postpartum (Supplementary Fig. 3, Supplementary Table 1).

Table 1

Demographic, anthropometric, and dietary intake profiles and biochemical parameters of women at the baseline (3rd trimester of pregnancy; n = 77).
Variables	2-18dpp (n = 19)	28-50dpp (n = 59)	88-119dpp (n = 33)	All women (n = 77)
Maternal age (years)		n (%)
18–23	5 (26.3)	21 (35.6)	5 (15.2)	26 (34.0)
24–29	7 (36.8)	21 (35.6)	16 (48.5)	26 (34.0)
30–40	7 (36.8)	17 (28.8)	12 (36.4)	25 (32.0)
Schooling (years)
1–9 (Elementary School)	8 (42.1)	17 (28.8)	12 (36.4)	23 (29.9)
10–12 (High School)	9 (47.4)	35 (59.3)	18 (54.5)	46 (59.7)
13–18 (Higher Education)	2 (10.5)	7 (11.9)	3 (9.1)	8 (10.4)
Lives with a partner
No	2 (10.5)	10 (16.9)	4 (12.1)	11 (14.3)
Yes	17 (89.5)	48 (81.4)	28 (84.8)	65 (84.4)
Parity
Multiparous	9 (47.4)	32 (54.2)	13 (39.4)	39 (50.6)
Primiparous	10 (52.6)	27 (45.8)	20 (60.6)	38 (49.4)
Alcohol intake during pregnancy
No	7 (36.8)	31 (52.5)	21 (63.6)	40 (51.9)
Yes	12 (63.2)	27 (45.8)	11 (33.3)	36 (46.8)
Physical activity during pregnancy
No	13 (68.4)	42 (71.2)	18 (54.5)	51 (66.2)
Yes	5 (26.3)	16 (27.1)	14 (42.4)	24 (31.2)
Anthropometric measurements	Median [IQR]
Pre-pregnancy BMI (kg/m²)	27 [23–29]	24 [21–28]	24 [22–29]	25 [21–29]
Total gestational weight gain (kg)	10 [8–15]	12 [9–16]	12 [9–16]	12 [9–16]
Lipids serum parameters (mg/dL)
Total cholesterol	212 [182–225]	222 [196–258]	224 [204–250]	221 [193–256]
Triglycerides	217 [131–278]	188 [141–259]	178 [145–211]	192 [143–245]
High-density lipoprotein cholesterol	59 [56–69]	62 [58–71]	69 [59–76]	64 [57–74]
Low-density lipoprotein cholesterol	118 [97.5–126]	123 [111–158]	118 [109–139]	120 [106–150]
Dietary intake^a
Total energy (kcal)	2610 [1790–2900]	2740 [1900–3800]	2610 [1910–3020]	2740 [1940–3790]
Carbohydrates (g)	437 [399–449]	441 [405–474]	442 [412–487]	439 [402–468]
Lipids (g)	90 [87–97]	89 [76–99]	90 [80–96]	89 [81–99]
Proteins (g)	123 [109–133]	117 [103–133]	118 [107–130]	118 [105–133]
Cholesterol (mg)	391 [333–517]	359 [268–460]	371 [329–485]	359 [278–497]
Saturated fat (g)	37 [33–41]	35 [29–41]	35 [29–39]	35 [31–41]
Monounsaturated fat (g)	30 [29–32]	30 [26–33]	30 [27–32]	30 [27–32]
Polyunsaturated fat (g)	20 [19–25]	20 [17–24]	20 [18–23]	20 [17–24]
Note: IQR: interquartile range interval; BMI: body mass index; dpp: days postpartum a Nutrients were adjusted for total daily energy intake using the residual method (Willet, 1997). No differences were observed between samples from three visits, according to Fisher's exact test, chi-square test (categorical variables), and Kruskal Wallis (continuous variables).

Some POPs were quantified in less than 13% of the human milk samples, such as PeCB (1%), α-HCH (1%), BDE-99 (4%), γ-HCH (5%), BDE-47 (6%), BDE-153 (9%), PCB 28 (10%), and oxychlordane (13%). In contrast, ppDDE was quantified in 99% of the samples, and PCB 153 and PCB 138 in all samples (Fig. 3). A similar phenomenon was observed in POPs according to the lactation period (Supplementary Fig. 1). In addition, among various POPs, ppDDE, PCB 153, and PCB 138 had the highest medians, i.e., 742 pg/mL, 73.3 pg/mL and 105 pg/mL, respectively. The OCPs (ppDDE and HCB) and the entire PCB group had the highest median levels (Fig. 4 and Table 2).

Table 2

Concentrations of POPs in human milk 2–119 days postpartum (n = 77).
POPs (pg/mL)	Median	IQR	LOQ (pg/ml)
POPs quantified in ≥ 90% of the samples
HCB	46.3	[31.4–64.6]	10
ppDDE	742.0	[327.0–2340.0]	40
PCB74	16.8	[8.6–33.2]	5
PCB99	22.9	[14.0–44.9]	5
PCB118	36.2	[20.9–73.2]	5
PCB138	73.3	[48.1–160.0]	5
PCB153	105.0	[66.7–227.0]	5
PCB170	27.5	[16.3–59.6]	5
PCB180	49.1	[28.4–103.0]	5
PCB187	22.7	[12.1–49.7]	5
POPs quantified in < 90% of the samples
PeCB	<LOQ	[< LOQ -<LOQ]	10
α -HCH	<LOQ	[< LOQ -<LOQ]	20
β -HCH	42.8	[18.5–69.0]	15
γ -HCH	<LOQ	[< LOQ - <LOQ]	20
Oxychlordane	<LOQ	[< LOQ - <LOQ]	25
Transnonachlor	6.29	[< LOQ − 9.92]	5
ppDDT	16.8	[< LOQ − 35.9]	15
PCB28	<LOQ	[< LOQ - <LOQ]	40
PCB52	<LOQ	[< LOQ - <LOQ]	5
PCB101	<LOQ	[< LOQ − 8.85]	5
PCB156	9.02	[6.36–25.0]	5
PCB183	8.12	[< LOQ − 15.7]	5
BDE47	<LOQ	[< LOQ - <LOQ]	15
BDE99	<LOQ	[< LOQ - <LOQ]	15
BDE153	<LOQ	[< LOQ - <LOQ	15
Note: POPs: persistent organic pollutants; IQR: interquartile range; LOQ: Limit of quantification; HCB: hexachlorobenzene; ppDDE: dichlorodiphenyldichloroethane; PCBs: polychlorinated biphenyls; PeCB: pentachlorobenzene; HCH: hexachlorocyclohexane; ppDDT: dichlorodiphenyltrichloroethane; PBDE: polybrominated diphenyl ethers.

The dietary intakes of total lipid, saturated fat, and monounsaturated fat during pregnancy were positively correlated with POPs (except for ppDDE, total OCP, and total POP) in human milk. A few negative correlations were observed between the food groups and some POPs, including between the poultry group and PCB congeners 74, 138, and 153; the total of all PCBs and the four most prevalent PCB congeners; and between the milk group and ppDDE and the sum of OCPs (Fig. 5). Mothers with pre-pregnancy overweight/obesity had a higher concentration of all POPs in human milk than those with normal weight, except for HCB, where no differences were found (Fig. 6).

No significant associations were observed in logistic regression models between pre-pregnancy BMI categories and dietary intake during pregnancy, and the presence or absence of POPs in human milk after Benjamini–Hochberg correction for multiple testing (Supplementary Fig. 4). Interestingly, significant associations were observed in the adjusted linear regressions between pre-pregnancy overweight/obesity and POPs concentrations (≥ LOQ in 90% of the samples). Compared with mothers with normal weight, those with pre-pregnancy overweight/obesity had increased levels of ppDDE by 4471.45 pg/mL (95% CI: 470.24, 8472.65), PCB74 by 16.8 pg/mL (95% CI: 4.89, 28.72), PCB138 by 81.16 pg/mL (95% CI: 9.65, 152.68), PCB153 by 113.75 pg/mL (95% CI: 17.08, 210.43), PCB170 by 28.5 pg/mL (95% CI: 4.44, 52.56), PCB180 by 46.89 pg/mL (95% CI: 4.97, 88.81), total PCBs by 410.38 pg/mL (95% CI: 49.31, 771.44), total 4PCBs by 283.35 pg/mL (95% CI: 37.63, 529.07), total 2OCPs by 4478.67 pg/mL (95% CI: 473.39, 8483.96), and total all POPs by 4815.93 pg/mL (95% CI: 745.15, 8886.71) in human milk between 2 and 119 days postpartum. A higher daily lipid intake during pregnancy increased human milk HCB to 0.54 pg/mL (95% CI: 0.19, 0.9) (Fig. 7).

This study presented several interesting findings. In summary, PeCB, α-HCH, γ-HCH, PCB 28, oxychlordane, and all BDEs showed lower frequency (< 13%), whereas ppDDE, PCB 153, and PCB 138 were quantified in most samples (> 99%). Adjusted models revealed that pre-pregnancy overweight/obesity, compared with normal weight, resulted in higher concentrations of ppDDE, PCB74, PCB138, PCB153, PCB170, PCB180, total PCBs, total 4PCBs, total 2OCPs, and total POPs in human milk at 2–119 days postpartum. In addition, dietary lipid intake during pregnancy was directly associated with the HCB concentration in human milk.

Our founds revealed high concentrations of some OCPs and PCBs in the human milk of Brazilian women, in line with other studies. Fång et al. (2015) showed lower levels of pesticides, such as DDT and its metabolites, in human milk samples in European countries but high concentrations of these pesticides in human milk samples in Brazil, Mexico, and countries of Central America, Africa, and Asia, which may indicate recent use of defensives. Similar to DDT, PCBs are usually found at higher levels in Latin America than in Europe (Martinez et al. 2022). The history of an economy based on the exploitation of natural resources, combined with a history of colonisation, is common in Latin American and African countries. As demonstrated by Murrey (2020), the colonialism, defined as the territorial, political, social, and cultural domination imposed by European countries on American and African societies, resulted in a historical inheritance of non-sustainable extraction of natural resources and expansion of monoculture, which might significantly contribute to environmental degradation, reduced biodiversity, and deforestation. Moreover, this history also contributed strongly to late and weak environmental policies and regulations, thereby resulting in the recent widespread use of pesticides in Latin American countries (Melgarejo et al. 2020).

In Brazil, although DDT was banned from commercialisation in 1985, its use continued until 1998 for public health actions for malaria control (BRASIL 1985; BRASIL 2001). In 2009, the Brazilian government prohibited its import and storage (BRASIL 2009). Notably, Brazilian studies conducted in the 2000s observed a higher concentration of DDT in human milk samples (Paumgartten et al. 2000; Azeredo et al. 2008). Consistently, our study identified DDT in > 50% of human milk samples more than 10 years after the initial prohibition date. In addition, DDE, a product of DDT degradation, was found in the milk of most participants. Although European countries also found a presence of DDT in human milk, like a Spanish cohort study with milk collection between 1 and 9 months postpartum, inequities could be observed, with low-income mothers presenting higher DDT and DDE concentrations in milk (Rovira et al. 2022).

Overall, the presence of POPs in the food chain is a common method of contaminating human matrices and tissues. In countries where a weak environmental policy is observed, the entire food system and food security can be compromised (Melgarejo et al. 2020). PBDEs are a group of POPs widely used as flame retardants and are present in many materials, such as plastics. Therefore, diet may be a common source of PBDEs contamination (Souza et al. 2021). Indeed, a Brazilian study found that animal milk was the food source with the highest levels of PBDE, which is worrisome in the long run. However, to date, there is no control or specifications for PBDEs use in Brazil (Souza et al. 2021).

Our findings revealed that PBDEs 47, 99, and 153 were detected in 6%, 4%, and 9% of the samples, respectively. In contrast, Souza et al. (2022) found the presence of the PBDEs 47, 99, and 153 in 100%, 31–55%, and 8–16% of Brazilian women's human milk samples, respectively. Despite the similarity in the detection of PBDE 153 in our and Souza et al. (2022) studies, the results of PBDE 47 and 99 were inconsistent. These conflicting results could be attributed to the different methods used to quantify the PBDEs. Souza et al. (2022) performed their analysis by gas chromatography GC-MS single quadrupole and used the limit of detection (LOD), while our study used GC-MS triple quadrupole and LOQ. Although LOD can detect low concentrations (near 0), it is more imprecise. However, LOQ can identify the analytes with a higher confidence degree (Armbruster et al. 1994; Homer et al. 2017), and the combination of GC-MS triple quadrupole and LOQ guarantees better accuracy and reliability.

A direct association between dietary lipid intake during pregnancy and HCB in human milk was observed in the present study. Overall, our findings suggest that dietary intake strongly influences the presence of OPCs, such as HCB, in human milk. HCB, a fungicide with high volatility and lipophilic characteristics, easily adheres to soil and has a higher half-life in water. As a result, it has a high possibility of contaminating the food chain. Indeed, it is commonly found in foods with high lipid content, such as milk, eggs, red meat, and fish (Qi et al. 2022). Our findings concerning the high presence of OCPs in human milk and its association with dietary intake support the notion that regulation and surveillance of continuous environmental contamination of OCPs are essential for ensuring food security, sustainable food systems, and health.

In the present study, congeners 138, 153, 180, and 118 were the most prevalent PCBs; similarly, Avila et al. (2022) also described these congeners as the predominant components in the human milk of Colombian women. PCBs have wide industrial applications, such as hydraulic and heat exchange fluids, electrical transformers, and large capacitors (UNEP 2017). Fortunately, the three most prevalent PCBs are non-dioxin-like, and only the fourth PCB, PCB 118, is dioxin-like, considering the more toxic congener category (Avila et al. 2022). Moreover, our findings also revealed that pre-pregnancy overweight or obesity was associated with higher concentrations of many PCBs congeners and ppDDE in human milk. Similarly, Rovira et al. (2022) and Ellsworth et al. (2020) also found a relation between DDE and PCB in human milk and obesity. Rovira et al. (2022) found a positive correlation between BMI and DDE in the milk of Spanish women, while Ellsworth et al. (2020) showed that the milk of overweight or obese American women had significantly higher PCB levels. It is known that long PCBs half-lives (commonly more than ten years) can explain the slow reduction levels in human milk (Hu et al. 2020). Considering the PCBs and metabolites of DDT in the environment and the global advancement of obesity, this result is very worrisome.

DDT, its degradation products, and PCBs can be considered endocrine-disrupting chemicals (Gupta et al. 2020) and can alter hormonally regulated metabolic processes (Heindel et al. 2017). The presence of these endocrine-disrupting chemicals in human milk can be related to infant obesity development, as observed in a study with Japanese children, which found a direct association between ppDDE levels of infant girls aged 0–24 months, which were estimated from human milk, and the BMI z-score of infants aged 42 months (Plouffe et al. 2020). Notably, Endocrine-disrupting chemicals can alter an infant's hormonal control by disrupting hormonal signalling systems, increasing the number of adipocytes, and controlling appetite and satiety (Grun et al. 2009; Heindel et al. 2015). Additionally, POPs, which act as endocrine disruptors, can contribute to the development of chronic non-communicable diseases. In a cohort study, Berg et al. (2019) followed Japanese-American employees with occupational pesticide exposure; they found that the group with high exposure to pesticides presented a 42% higher risk of developing cardiovascular diseases, such as cerebrovascular accidents and coronary heart disease, than that with low and moderate exposure. This phenomenon is probably because DDT and its metabolite DDE could harm cardiomyocytes, resulting in cardiotoxicity (Truong et al. 2020). However, it is necessary to investigate whether exposure to smaller doses of these pesticides in the long term can result in similar effects.

The global epidemiological scenario of nutritional transition is directly influenced by socioeconomic, political, environmental, and agricultural issues, which directly impact the nutritional and health status of populations (Jaime et al. 2018). Therefore, the effects of POPs on human life and, specifically, their association with obesity and non-communicable diseases are considered a public health problem (Kezios et al. 2013). In Brazil, the economic impact of obesity on chronic non-communicable diseases is high, and it is estimated that US$ 654 million in health care costs related to non-communicable diseases are attributable to overweight and obesity (Ferrari et al. 2022). Because overweight and obesity can be associated with an increased risk of POPs contamination in human milk, preventing and fighting the obesity syndemic and reducing environmental impacts is urgently needed.

This study has some limitations. First, the loss of follow-up in our cohort limited our findings regarding POPs variation in human milk over time because there was a small sample size at some time points. To overcome this problem, the total sample size was analysed independently of the time point, as no differences were found among the periods evaluated. Second, human milk was extracted manually, and it was unable to ensure that the breast was empty. Considering that human milk posterior is more concentrated in lipids, the POPs concentration could be underestimated. This study’s strength lies in that the method used to evaluate the POPs concentrations has a high measurement precision. Additionally, the analysis of twenty-five POPs can also be considered an asset. Moreover, the best-fit model was used in statistical analyses, and the control for the false discovery ratio was performed to avoid bias.

In conclusion, OCPs (ppDDE and HCB) and PCBs were quantified in most milk samples from Brazilian women, and ppDDE, PCB 138, and PCB 153 were present in almost all samples. Pre-pregnancy overweight/obesity was associated with higher concentrations of OCPs and PCBs in human milk collected at 2–119 days postpartum, and the dietary intake of total lipids was directly related to the concentration of HCB in human milk. It is essential to note that human milk is the most recommended food for children, and its benefits outweigh the risks. Our findings further support that adequate pre-pregnancy nutritional status, surveillance, and control of POP contamination in human milk are essential to ensure binomial mother-infant health. However, further epidemiologic studies considering longitudinal POPs concentrations in human milk in larger samples are necessary to better investigate the causal effects.

Acknowledgments

We thank all cohort participants and their children and the Rio de Janeiro Public Health Center, where the data was collected. We also thank the Rio de Janeiro State Research Support Foundation – FAPERJ, the National Council for Scientific and Technological Development – CNPq and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES), for funding this study. We would like to thank Editage (www.editage.com) for English language editing.

Authors’ contributions

Ana Lorena Ferreira and Gilberto Kac: study conception and design; Ana Lorena Ferreira, Nathalia Freitas-Costa, Amanda Figueredo and Nadya Alves-Santos: conducted the research data collection; Ana Lorena Ferreira: analyzed the data and performed the statistical analysis and written the first draft of the manuscript; Ana Lorena Ferreira, Nathalia Freitas-Costa, Samary Freire, Amanda Figueredo, Marina Padilha, Nadya Alves-Santos and Gilberto Kac contributed to review, editing, provided a critical evaluation and approved the final manuscript.

Funding

This study was supported by Carlos Chagas Filho Foundation for Research Support of Rio de Janeiro State (FAPERJ) by grant #E-26/200.429/2020 and supports #E-26/210.190/2014 (200585) and #E-26/010.002429/2019 (211560).

Data availability

All datasets used and/or generated in the manuscript, codebook, and analytic code will be made available upon reasonable request pending application and approval.

Ethics approval

The study was approved by two Research Ethics Committees and was carried out following the rules of the Declaration of Helsinki, conforms to the requirements of the journal

Consent to participate

Written consent from all participants was obtained freely and spontaneously during the research.

Consent for publication

All authors have approved the names and order of authors and the manuscript before submission.

Competing Interests

The authors have no relevant financial or non-financial interests to disclose.

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SupplementaryTable1.docx
SupplementaryFig.1.tiff
Supplementary Fig. 1 Frequency of POPs detection in human milk samples above the limit of quantification (LOQ) at 2–18 (n=19), 28–50 (n=59), and 88–119 (n=33) days postpartum. Note: PeCB: pentachlorobenzene; HCH: hexachlorocyclohexane; BDEs: brominated diphenyl ethers; PCBs: polychlorinated biphenyls; ppDDT: dichlorodiphenyltrichloroethane; HCB: hexachlorobenzene; ppDDE: dichlorodiphenyldichloroethane. Dashed lines indicate the relative frequency of the limits of quantification for continuous (≥90%) and categorical (≥20% and ≤90%) POPs.
SupplementaryFig.2.tiff
Supplementary Fig. 2 Median POPs concentrations detected in human milk samples at 2–18 (n=19), 28–50 (n=59), and 88–119 (n=33) days postpartum. Note: Concentrations below the limit of quantification (LOQ) were considered half of the LOQ values. OCPs: Organochlorine pesticides; PBDEs: polybrominated diphenyl ethers; PCBs: polychlorinated biphenyls; PeCB: pentachlorobenzene; ppDDE: dichlorodiphenyldichloroethane; HCB: hexachlorobenzene; HCH: hexachlorocyclohexane; ppDDT: dichlorodiphenyltrichloroethane; BDE: brominated diphenyl ethers.
SupplementaryFig.3.tiff
Supplementary Fig. 3 Boxplot with POPs concentrations in human milk according to variation at 2–18 (n=19), 28–50 (n=59), and 88–119 (n=33) days postpartum. Note: P-values were calculated according to Kruskal–Wallis test with Dunn’s post-hoc test for multiple comparisons. POPs with a frequency limit of quantification above 80% in all three periods were considered for time variation analysis. POPs: persistent organic pollutants; LOQ: Limit of quantification; IQR: interquartile range interval; ppDDE: dichlorodiphenyltrichloroethane; HCB: hexachlorobenzene; PCBs: polychlorinated biphenyls.
SupplementaryFig.4.tiff
Supplementary Fig. 4 Adjusted logistic regressions for associations between maternal pre-pregnancy overweight/obesity or dietary intake during pregnancy and the presence of POPs quantified between 20 and 90% of samples at 2-119 days postpartum (n=77). Note: UP: Ultraprocessed; PP: pre-pregnancy; ppDDT: dichlorodiphenyltrichloroethane; HCH: hexachlorocyclohexane; PCBs: polychlorinated biphenyls.

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Association of pre-pregnancy maternal overweight/obesity and dietary intake during pregnancy with the levels of persistent organic pollutants in the human milk of Brazilian women

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Pre-pregnancy overweight/obesity and dietary intake during pregnancy

Human milk collection and POPs concentration analyses

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