Phthalate exposure in association with the use of personal care products among general population from Shanghai

Abstract

Phthalates are used in a wide variety of personal care products (PCPs) as solubilizer, denaturant or color fixative. However, there are few studies referring the correlation between phthalate exposure and PCPs use among general population in China. In this study, ten metabolites of phthalates in spot urine samples (N = 500) were quantified using ultra-performance liquid chromatography tandem mass spectrometry. The frequency and duration of 12 types of PCPs were collected by questionnaire survey. The associations of phthalate metabolites and PCPs use were assessed by multivariable liner regression models. Median concentration of mono-benzylphthalate (MBzP) was significantly higher among frequent users of almost all PCPs. Low molecular weight phthalates (monomethyl phthalate (MMP), mono-n-butylphthalate (MnBP) and monoisobutylphthalate (MiBP)) were significantly lower among frequent user of some rinse-off PCPs (e.g., shampoo, facial cleanser, and body wash). Meanwhile, monoethylphthalate (MEP) was positive correlated with frequently use of facial moisturizer. Mono-2-ethylhexylphthalate (MEHP) and MBzP showed a significant positive association with frequently use of body lotion. Univariate linear analyses indicated a significant decreasing trend between urinary concentrations of MMP, MnBP, and the number of rinse-off PCPs being frequently used, and a significant increasing trend between urinary MBzP and the number of leave-on products being frequently used. These findings indicated that the use of some PCPs, especially leave-on PCPs, could be a potential source of exposure to some phthalates.

Introduction

Phthalates are ubiquitous endocrine disrupting chemicals that may partially from the use of cosmetics and personal care products (PCPs) (Guo et al. 2014). For example, high molecular weight phthalates (HMWP, molecular weight > 250D, e.g., DBP and DEHP) are mainly used to enhance the flexibility of PCPs, and low molecular weight phthalates (LMWP, molecular weight < 250D, e.g., DMP, DEP, and DnBP) are mainly used to improve solubility, adhesion, fragrance holding and soft feeling of lotion, nail polish, cosmetic, and other PCPs (Net et al. 2015; Dong et al. 2017; Harley et al. 2020).

Previous studies have suggested that PCPs use is possible sources to phthalates. For example, a Norwegian biomonitoring study reported that phthalate exposure was associated with the use of shower gel, hand cream, toothpaste, anti-wrinkle cream and shaving products (Husoy et al. 2019). A Korea biomonitoring study found the exposure of phthalates related to PCPs use in various age groups (Lim 2020). A number of biomonitoring studies found that the Chinese population is widely exposed to phthalates (Guo et al. 2011). However, the contribution of PCPs to phthalate exposure in China is still unclear. One study analyzed 9 phthalates in 52 PCPs collected from Tianjin, China, and the author found hand and body lotions were the major contributors to the phthalates exposure (Guo et al. 2014). However, the investigation regarding the contribution of PCPs to the body burden of phthalates in China is limited.

Previous human studies on the association between the use of PCPs and the body burden of phthalates (assessed by urinary metabolites) were largely limited to pregnant women and children (Lang et al. 2016; Berger et al. 2018; Machtinger et al. 2018). In pregnant women, increased concentrations of phthalate metabolites in urine were found to be associated with the use of leave-on PCPs including makeup or cosmetics, hair spray or hair products, lotion or sunscreen, deodorant, nail polish, and perfume (Just et al. 2010; Machtinger et al. 2018; Fisher et al. 2019; Hsieh et al. 2019). In infants, increased concentrations of urinary metabolites of several phthalates were found to be associated with the use of infant lotion and powder as well as baby shampoo (Sathyanarayana et al. 2008). Few studies have investigated such association in general population.

Here, we provide some data on general population, and highlighted the importance of leave-on PCPs for their contribution to phthalate exposure.

Methods and materials

Study population and sample collection

The studied population was from Shanghai Food Consumption Survey (SHFCS), a multiple cross-sectional study performed by Fudan University from 2012 to 2014. The SHFCS has been described in detail in previous studies (Dong et al. 2018). The SHFCS contained 3322 participants from 25 communities in its first interview of 4-times dietary survey (fall 2012, spring and winter 2013, and summer 2014). Questionnaire on the use of PCPs were conducted in 726 participants of 6 communities in fall 2012. After the excluded samples of lacking anthropometric measurements (34 participants), not measuring urinary metabolites of phthalates (108), having unreasonable creatinine concentration (6 participants, < 20 μmol/L or > 30,000 μmol/L), and being aged ≤ 18 years (78), 500 participants were included in this study. The Ethics Committee of the School of Public Health at Fudan University approved this study. All participants gave informed consent at enrollment.

The use of personal care products

Exposure information on the use of 12 PCPs was collected, which included frequency and the duration of these PCPs. Considering the relative long using interval of hair dye and nail polish, and the short half-life period of most phthalates, hair dye and nail polish were excluded when we conducted the analysis. We categorized the 10 PCPs as two categories according to the purpose of use, resident time on skin, and the surfactant-based formulation for further analysis: 1) rinse-off products, including shampoo, hair conditioner, facial cleanser and body wash; 2) leave-on products, including facial moisturizer, body lotion, eye cream, sunscreen, cosmetic and perfume. The studied population was also divided into two categories according to the frequency of PCPs use: (1) frequent users, with frequency of “≥ 3~4 times per week”; (2) occasional users, with frequency of “≤ 1~2 times per week.”

Determination of phthalate metabolites in urine

We measured 10 phthalate metabolites, including monomethyl phthalate (MMP), monoethylphthalate (MEP), mono-n-butylphthalate (MnBP), monoisobutylphthalate (MiBP), mono-benzylphthalate (MBzP), mono-2-ethylhexylphthalate (MEHP), mono-2-ethyl-5-oxohexyphthalate (MEOHP), mono-2-ethyl-5-hydroxyhexylphthalate (MEHHP), mono-2-ethyl-5-carboxypentylphthalate (MECPP), and mono-2-carboxymethyl-hexyl phthalate (MCMHP) by liquid chromatography tandem mass spectrometry (API 4000, LC-MS/MS, Shimadzu, Japan) according to the methods reported elsewhere (Tranfo et al. 2013). Briefly, unfroze urine sample from − 80 °C and incubated with β-glucuronidase at 37 °C for 2 h, then mixed with six isotopically labeled internal standards including 13C4-MnBP, 13C4-MEHP, 13C4-MEOHP, 13C4-MEHHP, 13C4-MECPP, and 13C4-MCMHP(Cambridge Isotope Laboratories, USA), and then extracted by PLS solid phase extraction column(DIKMA, China). Eluent was filtered with 0.2-μm filter and analyzed by LC-MS/MS. For the quality control of laboratory procedures, we processed one procedural blanks in each batch of 20 samples.

The limits of detection (LOD) for MMP, MEP, MnBP, MiBP, MBzP, MEHP, MEOHP, MECPP, MEHHP, and MCMHP were 0.02, 0.20, 0.04, 0.04, 0.20, 0.60, 0.10, 0.20, 0.03 and 0.50 μg/L, respectively. Summary measurements of ΣLMWP (< 250 Da) and ΣHMWP (> 250 Da) referred to method as described previously. Briefly, molar concentrations of 10 metabolites were calculated separately. And then, each category (ΣLMWP or ΣHMWP) were calculated according to the following formulas. The merged metabolite concentrations were expressed in micrograms per liter.

$$ \mathrm{LMWP}\left(\upmu \mathrm{g}/\mathrm{L}\right)=\frac{\left[\mathrm{MMP}+\mathrm{MEP}+\mathrm{MnBP}+\mathrm{MiBP}\ \right]\left(\upmu \mathrm{mol}/\mathrm{L}\right)}{\left[{\mathrm{MW}}_{\mathrm{MMP}}+{\mathrm{MW}}_{\mathrm{MEP}}+{\mathrm{MW}}_{\mathrm{MnBP}}+{\mathrm{MW}}_{\mathrm{MiBP}}\right]\left(\mathrm{g}/\mathrm{mol}\right)/4} $$
$$ \mathrm{HMWP}\left(\upmu \mathrm{g}/\mathrm{L}\right)=\frac{\left[\mathrm{MEHP}+\mathrm{MEOHP}+\mathrm{MEHHP}+\mathrm{MECPP}+\mathrm{MCMHP}+\mathrm{MBzP}\ \right]\left(\upmu \mathrm{mol}/\mathrm{L}\right)}{\left[{\mathrm{MW}}_{\mathrm{MEHP}}+{\mathrm{MW}}_{\mathrm{MEOHP}}+{\mathrm{MW}}_{\mathrm{MEHHP}}+{\mathrm{MW}}_{\mathrm{MECPP}}+{\mathrm{MW}}_{\mathrm{MCMHP}}+{\mathrm{MW}}_{\mathrm{MBzP}}\right]\left(\mathrm{g}/\mathrm{mol}\right)/6} $$

Statistical analysis

Analyses were conducted in SPSS version 22.0. Urinary sample concentrations below the LOD were assumed to be LOD/2 for calculation (Dewalque et al. 2014). The creatinine-corrected concentrations were natural log-transformed to facilitate further analysis. P values presented are two-tailed with a significance level of 0.05. Continuous variables were summarized as median (interquartile range) and categorical variables as percentages (%). The PCPs use was applied in the statistical model as dichotomized formats. The frequencies of PCPs use were grouped into two categories (occasional users were defined as 0 and frequent users were defined as 1). The differences in urinary phthalate metabolites between and occasional users of PCPs were analyzed using Mann-Whitney U test.

Multivariable linear regression models were used to analyze the relationship between PCPs use and each metabolite of phthalates. Of note, as the distribution of phthalate metabolite concentrations was non-normal, we used log-transformation to enable the data’s normality in statistical analyses. We display the results by percent change in urinary metabolites or summary measure concentrations by exponentiating the beta coefficients from these models. According to the number of PCPs being frequently used, we divided the users of rinse-off and leave-on products into three groups (one, two, three or more products in frequently use), respectively. Adjusted trend tests by univariate linear analyses were conducted for the association between the number of PCPs being used and certain metabolite of phthalates. Confounders for the aforementioned analyses included age, gender, educational status (primary school or below, middle school or technical secondary school, and university and the above), marital status (married or others), smoking status (never smoked or current/past smoker), body mass index, average monthly intake (< 2000, 2000 to 3000, 3000 to 5000, and > 5000, CNY), total, and various types of food intake in 24 h.

Results

Demographic characteristics

Demographic characteristics of study participants are presented in Table 1. The participants were mostly nonsmokers (80%) and married (79.6%). The participants had a median age of 56 and median BMI of 23.4 kg/m2 at the time of enrollment. The usage pattern of PCPs for study participants are shown in Table 2. Shampoos were the most frequently used PCPs (45.6%), followed by body wash (39.2%) and facial moisturizer (38.6%).

Table 1 Demographic characteristics of study population (N = 500)
Table 2 The frequency of 12 personal care products use (N = 500)

Urinary concentrations of phthalate metabolites

Table 3 presents the detection rate, distribution, and geometric mean of each phthalate metabolite with creatinine adjustment. The median value of creatinine-corrected concentration in MMP, MEP, MnBP, MiBP, MEHP, MEOHP, MECPP, MEHHP, MCMHP, and MBzP were 8.23, 21.40, 38.94, 22.49, 10.02, 6.55, 18.16, 16.34, 19.43, and 2.26 μg/g creatinine, respectively.

Table 3 The distribution of urinary phthalate metabolite concentration (μg/g creatinine, N = 500)

Personal care products use and phthalate metabolite concentrations

The differences in urinary phthalate metabolites between frequent and occasional users of PCPs are presented in Table 4. Urinary MBzP concentration was higher in frequent users of almost all products except shampoo. The urinary concentrations of MMP, MiBP, ΣLMWP, and MEOHP were significantly lower in frequent users of rinse-off PCPs, while MEP, MBzP, and ΣHMWP were significantly higher in frequent user of leave-on PCPs. Specifically, the frequent users of shampoo had significantly lower levels of MnBP (32.97 vs 43.44 μg/g creatinine, P = 0.002), MiBP (20.13 vs 24.08 μg/g creatinine, P = 0.048), and MEOHP (5.92 vs 6.91 μg/g creatinine, P = 0.005) than those in occasional users of shampoo. The frequent users of facial cleanser had lower MiBP (17.04 vs 24.06 μg/g creatinine, P = 0.007) and ΣLMWP (52.97 vs 68.93 μg/L, P = 0.003) than those in occasional users of facial cleanser. The frequent users of body wash had lower MnBP (36.08 vs 40.43 μg/g creatinine, P = 0.011) concentration than that in occasional users of body wash.

Table 4 The differences in urinary phthalate metabolites between frequent and occasional users of PCPs (μg/g creatinine)

Regression results

The adjusted percent change in urinary phthalate metabolite concentrations with PCPs use was calculated (Fig. 1). Lower MMP (28.3%) and ΣLMWP (20.6%) were associated with using facial cleanser frequently. For rinse-off PCPs, frequent users of body wash had 63.7% lower MnBP. Frequent users of body lotion had 58.3% higher MEHP and 54.9% higher MBzP. Frequent users of facial moisturizer had 34.6% higher MEP.

Fig. 1
figure1

Heatmap for % change of urinary phthalate metabolite concentration in participants reporting frequently use of PCPs compared to occasional users. Multivariate linear regression models were adjusted for creatinine, different categories food intake by 24-h recall data, age, gender, education, smoking, marriage, and BMI. *P value < 0.05. **P value < 0.01

Univariate linear analyses

Figure 2 shows the adjusted associations between the number of rinse-off and leave-on PCPs used and the phthalate metabolite concentrations. There were negative trends between the number of rinse-off PCPs used and MMP, MnBP and ΣLMWP concentrations. The P for trend of MMP, MnBP and ΣLMWP were 0.021, 0.002 and 0.026, respectively. For rinse-off PCPs, there was a positive trend between the number of rinse-off PCPs used and MBzP concentration (P for trend < 0.001).

Fig. 2
figure2

Univariate linear analyses of simultaneously use rinse-off or leave-on products in a high frequency in association with select phthalate metabolite concentration. Data were adjusted for creatinine, different categories food intake by 24-h recall data, age, gender, education, smoking, marriage, and BMI. Each point in the horizontal axis represents calculated GM of selected phthalate metabolite concentration. aThe unit of LMWP is μg/L, which take right Y axis as a reference

Discussion

This study found that several phthalate metabolites negatively correlated with frequent use of rinse-off PCPs, while some phthalate metabolites positively correlated with the frequent use of leave-on PCPs. Our results suggested that the use of some leave-on PCPs may be the source of phthalates exposure. To our best knowledge, this is the first study to evaluate the associations between detailed usage patterns of PCPs among general population in China.

Compared to the total study population in SHFCS, the concentrations of LMWP in this selected population were obviously higher, and HMWP were similar, which may reflect a selection bias (Dong et al. 2018). Compared to the general population from NHANES 2011–2012, the concentration of MEP and MBzP and secondary metabolites of DEHP were lower, while MnBP, MiBP, and MEHP were higher (Shiue 2015). Compared to the general population from Korean National Environmental Health Survey (KoNEHS), MnBP, MBzP and metabolites of DEHP were much lower (Park et al. 2019). The different phthalates exposure levels observed in our study compared to other regions, suggest that there are population differences, which may be due to variations of exposure pathways or physiology.

PCPs use has been reported as an important source to phthalate exposure. For example, PCPs were reported as the major contributors to DEP exposure in many countries (Wormuth et al. 2006; Koniecki et al. 2011; Guo and Kannan 2013; Koch et al. 2013). However, this study only found a higher MEP concentration in frequent users of facial moisturizer. Previous research proved that DEP was used in fragranced products as a denaturant to make a long-lasting scent; therefore, the urinary MEP concentrations may associate with the use of perfumes (Parlett et al. 2013). This study did not find a significant association between MEP concentration and the use of perfume, which consistent with a research in Taiwan (Hsieh et al. 2019). This inconsistency may attribute to the different life habits between western countries and China. We could not get the verification in this study because of the low usage rate of perfumes (< 5%).

BBzP was only detected in 12% of the rinse-off and in of the leave-on PCPs in the USA (Guo and Kannan 2013). The use of body lotion (Duty et al. 2005) and skin make-up (Larsson et al. 2014) has been reported to negatively associate with concentration of MBzP. On the contrary, our result showed that urinary MBzP had a stable higher concentration in frequent users of most personal care products. Furthermore, our results indicated that the use of body lotion was positively associated with the concentration of MBzP, which consistent with a research in Taiwan (Hsieh et al. 2019). In China, BzBP was rarely found in the PCPs samples (Guo et al. 2014). Our results indicated the potential body burden of China’s population from BBzP-containing PCPs still exist, even in low detection frequency.

In this study, we only found significant and positive association between MEHP, the primary metabolite of DEHP and body lotion use (26.2%, P = 0.05). A Taiwan study also found only a minor association between hair spray use and the concentrations of ∑DEHP metabolite (26.2%, P = 0.05) (Hsieh et al. 2019). There are several possible explanations for the weak association we found between DEHP and PCPs use. Firstly, DEHP had low detection frequencies in PCPs. For example, one study has shown DEHP was only detected in 3% PCPs in China and DEHP was the most abundant phthalate in food (Guo et al. 2014). Due to a similarity of life style and diet habit, food may be a major exposure source of exposure to DEHP for the Shanghai general population. Secondly, on the basis of results reported in many countries, it is clear that the main source of DEHP exposure is diet (Koch et al. 2013; Serrano et al. 2014).

Our results support the previous findings that the rinse-off PCPs use was negatively associated with urinary concentrations of phthalate metabolite (Hsieh et al. 2019). This study found 3 individual (MMP, MnBP, and MiBP) and summary measures of urinary LMWP were lower in participants who reported using rinse-off PCPs in a high frequency (≥ 3~4 times per week). A Taiwan study found a negative association between urinary MMP and face wash (Hsieh et al. 2019). DMP and DiBP were found in rinse-off PCPs via a survey in the USA with 10% and 27% detection frequencies, but the highest level of these compounds were only 0.32 and 0.39 μg/g, which were far below DEP (3530 μg/g) (Guo and Kannan 2013). These results indicated these phthalates may only present in rinse-off PCPs with a tiny amount, and the surfactant in rinse-off PCPs may avoid an extra dermal absorption of these phthalates from another source, which result in the negative correlation between frequently use of rinse-off PCPs and urinary concentration of phthalates. Another possible explanation could be the washing behavior. Washing hands with soap and water could effectively remove the phthalates (Gong et al. 2014; Lin et al. 2017).

Discrepancies between our findings and other researches might be due to the different questionnaire design in PCPs use (e.g., using frequency in long-term versus 24 or 48-h recalls). This study has several limitations. The half-time of most phthalates were very shot (about 12~48 h) and the metabolism developed within hours after exposure. Phthalates do not accumulate in the body. Nevertheless, the use of PCPs is relatively consistent; a single spot urine sample might not reflect a chronic or long-term exposure of phthalates. Furthermore, we did not collect the detail information of PCPs used such as brand, amount and water temperature during usage. The participants in this study have a median age of 56 years [IQR (41, 64)]. This subgroup rarely used colored and fragrance cosmetic such as hair dye, nail polish and perfume. For this reason, this study may underestimated the dermal exposure of phthalates from certain PCPs among youth population. Moreover, we did not get diet and other lifestyle information. Phthalate exposure may be impacted by these factors. Another weakness of this study is that the possibility of chance findings cannot be excluded, due to limited sample size. Thus, longitudinal studies are needed to confirm these findings.

Conclusion

The results showed that the frequent users of shampoo, facial cleanser, or body wash had a significant lower urinary concentration of the LMWP, including MMP, MnBP, and MiBP. MEP was positive correlated with frequently use of facial moisturizer. MEHP and MBzP showed a significant positive association with frequently use of body lotion. These results indicated the use of some leave-on PCPs could be a potential source of phthalate exposure.

Data availability

Extra data is available by emailing to chenb@fudan.edu.cn on reasonable request.

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Acknowledgments

We thank all participants for their participation and kind assistance. BC contributed to the conception and study design; JQ, RD, and MW contributed to the acquisition of data; JQ, RD, and QY performed data analysis; JQ, RD, and JC contributed to the interpretation of data; JQ, RD, and BC contributed to manuscript writing, and critically revised the manuscript. All authors read and approved the final manuscript. The guarantor is BC.

Funding

This work was supported by the National Natural Science Foundation of China (grant number 82003412), China Postdoctoral Science Foundation Grant (grant numbers 2019M651380), and the China Postdoctoral Science Foundation Grant (grant numbers 2019T120306).

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Correspondence to Bo Chen.

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The Ethics Committee of the School of Public Health at Fudan University approved this study. All participants gave informed consent at enrollment.

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Qin, J., Dong, R., Wu, M. et al. Phthalate exposure in association with the use of personal care products among general population from Shanghai. Environ Sci Pollut Res (2021). https://doi.org/10.1007/s11356-021-12375-1

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Keywords

  • Phthalates
  • Leave-on personal care products
  • Rinse-off personal care products
  • General population
  • Multivariable liner regression
  • Univariate linear analyses