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7-2015 Vaginal douching and racial/ethnic disparities in phthalates exposures among reproductive-aged women: National Health and Nutrition Examination Survey 2001–2004 Francesca Branch
Tracey J. Woodruff
Susanna D. Mitro George Washington University
Ami R. Zota George Washington University
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Recommended Citation Branch, F.B., Woodruff, T.J., Mitro, S.D., Zota, A.R. (2015). Vaginal douching and racial/ethnic disparities in phthalates exposures among reproductive-aged women: National Health and Nutrition Examination Survey 2001–2004. Environmental Health, 14:57.
This Journal Article is brought to you for free and open access by the Environmental and Occupational Health at Health Sciences Research Commons. It has been accepted for inclusion in Environmental and Occupational Health Faculty Publications by an authorized administrator of Health Sciences Research Commons. For more information, please contact [email protected]. Branch et al. Environmental Health (2015)14:57 DOI 10.1186/s12940-015-0043-6
RESEARCH Open Access Vaginal douching and racial/ethnic disparities in phthalates exposures among reproductive-aged women: National Health and Nutrition Examination Survey 2001–2004 Francesca Branch1, Tracey J. Woodruff2, Susanna D. Mitro1 and Ami R. Zota1*
Abstract Background: Diethyl phthalate (DEP) and di-n-butyl phthalate (DnBP) are industrial chemicals found in consumer products that may increase risk of adverse health effects. Although use of personal care/beauty products is known to contribute to phthalate exposure, no prior study has examined feminine hygiene products as a potential phthalate source. In this study, we evaluate whether vaginal douching and other feminine hygiene products increase exposure to phthalates among US reproductive-aged women. Methods: We conducted a cross-sectional study on 739 women (aged 20–49) from the National Health and Nutrition Examination Survey 2001–2004 to examine the association between self-reported use of feminine hygiene products (tampons, sanitary napkins, vaginal douches, feminine spray, feminine powder, and feminine wipes/towelettes) with urinary concentrations of monoethyl phthalate (MEP) and mono-n-butyl phthalate (MnBP), metabolites of DEP and DnBP, respectively. Results: A greater proportion of black women than white and Mexican American women reported use of vaginal douches, feminine spray, feminine powder, and wipes/towelettes in the past month whereas white women were more likely than other racial/ethnic groups to report use of tampons (p < 0.05). Douching in the past month was associated with higher concentrations of MEP but not MnBP. No other feminine hygiene product was significantly associated with either MEP or MnBP. We observed a dose–response relationship between douching frequency and MEP concentrations (ptrend < 0.0001); frequent users (≥2 times/month) had 152.2 % (95 % confidence intervals (CI): (68.2 %, 278.3 %)) higher MEP concentrations than non-users. We also examined whether vaginal douching mediates the relationship between race/ethnicity and phthalates exposures. Black women had 48.4 % (95 % CI: 16.8 %, 88.6 %; p = 0.0002) higher MEP levels than white women. Adjustment for douching attenuated this difference to 26.4 % (95 % CI:−0.9 %, 61.2 %; p = 0.06). Mediation effects of douching were statistically significant for black-white differences (z = 3.71, p < 0.001) but not for differences between Mexican Americans and whites (z = 1.80, p = 0.07). Conclusions: Vaginal douching may increase exposure to DEP and contribute to racial/ethnic disparities in DEP exposure. The presence of environmental chemicals in vaginal douches warrants further examination. Keywords: Biomonitoring, Diethyl phthalate, Endocrine disruptors, Environmental justice, Feminine hygiene, Fragrance, Health disparities, NHANES, Personal care products, Phthalates
* Correspondence: [email protected] 1Department of Environmental and Occupational Health, Milken Institute School of Public Health, George Washington University, 950 New Hampshire Avenue NW, Suite 414, Washington DC 20052, USA Full list of author information is available at the end of the article
© 2015 Branch et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http:// creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Branch et al. Environmental Health (2015)14:57 Page 2 of 8
Background phthalates exposure may contribute to disparities in health Phthalate acid esters, also known as phthalates, are a class outcomes [23]. of multifunctional industrial chemicals that warrant public Given the concern over phthalate toxicity, it is import- health concern due to their ubiquitous presence in the en- ant to identify modifiable sources of phthalates exposure vironment and their potential effects on human health. that may be targeted for exposure reduction strategies, Low molecular weight phthalates such as diethyl phthalate particularly for vulnerable populations. Personal care (DEP) and di-n-butyl phthalate (DnBP) are used in fra- product use is considered an important exposure pathway granced personal care products such as cologne/perfume, for DEP and DnBP [24], particularly among reproductive- hair products, deodorant, lotion, body wash, and nail aged women who use multiple products daily [25]. polish to retain scents [1, 2]. Because phthalates are not Numerous studies [10, 19, 25-27] report an association chemically bound to products, product use can lead to between use of colognes/perfumes and other fragranced phthalates exposure through dermal absorption, inhal- products and higher urinary concentrations of mono-ethyl ation, and ingestion. Once in the body, phthalates are phthalate (MEP), a metabolite of DEP, with MEP concen- quickly metabolized and excreted in urine, with elimin- trations in fragrance users approximately 3 times that of ation half-lives less than 24 h [3, 4]. Urinary metabolites of non-users [25]. Associations between personal care prod- DEP and DnBP are detected in 99 % of US women of ucts and MnBP, the primary metabolite of DnBP, are less reproductive age [5]. consistent. Among the studies that examined these rela- Exposure to DnBP and DEP is associated with adverse tionships, five found a positive association between some effects on reproductive, endocrine, and developmental type of personal care product use and urinary MnBP [10, systems. Experimental animal studies find that DnBP, 25, 27-29], three reported no association [25, 26, 28], and but not DEP, has well-documented anti-androgenic ef- one found an inverse association [19]. fects on the reproductive systems of male offspring Feminine care products that are used vaginally, such exposed in utero [6]. The female reproductive system is as douches, tampons, and deodorants, may be an unre thought to be less sensitive to phthalate-induced disrup- cognized exposure source of phthalates. In particular, va- tion than the male reproductive system. However a recent ginal douching, the practice of intravaginal cleansing study that examined the effects of a phthalate mixture with a liquid solution, warrants consideration since most (which included DnBP but not DEP) on female rat off- commercial douches contain fragrance [30] and synthetic spring exposed in utero reported reproductive malforma- fragrances are a mixture of compounds that often contain tions consistent with the Mayer–Rokitansky–Kuster– phthalates [1, 31, 32]. The practice of vaginal douching Hauser syndrome [7]. Moreover, a recent study of DEP may also play a role in shaping chemical exposure dispar- toxicity found evidence of estrogenicity in both in vitro ities, since black women report douching more frequently and in vivo, in adult female rats, suggesting that DEP may than white and Mexican American women [18, 19]. induce reproductive abnormalities in female reproductive Although socio-cultural differences in personal care system by both genomic and non-genomic mode of ac- product use have been hypothesized as a possible driver of tions [8]. The evidence of health effects in humans is still disparities in phthalates exposure [21], to our knowledge, evolving; however, epidemiologic studies suggest that no study to date has characterized this relationship. We prenatal DnBP and DEP exposure is associated with sex conducted a cross-sectional study to examine the associ- steroid hormone concentrations during pregnancy [9] and ation between self-reported use of vaginal douches and may increase the risk of adverse health outcomes during other feminine hygiene products with DEP and DnBP me- early childhood [10-12]. In adult women, DnBP exposure tabolites, MEP and MnBP respectively, among a nationally is associated with increased risks of diabetes [13] and representative sample of U.S. reproductive aged women. endometriosis [14] while DEP exposure is associated with We also examined whether differences in douching would increased biomarkers of oxidative stress [15], elevated partially explain racial/ethnic differences in phthalate mammographic breast density and increased breast cancer metabolites levels. risk [16]. Phthalates exposure varies by race/ethnicity and socio- Methods economic status (SES). Black females and males have Study population higher levels of DEP metabolites than their white counter- We pooled data from the 2001–2002 and 2003–2004 parts [17-20] and lower SES is associated with elevated cycles of the National Health and Nutrition Examination levels of DnBP [17, 21, 22] though reasons underlying Survey (NHANES), a nationally representative survey and social disparities in phthalates exposures remain poorly physical examination of the civilian, non-institutionalized understood. Mounting evidence points to environmental U.S. population conducted by the US Centers for Disease factors in shaping racial/ethnic and socioeconomic dis- Control and Prevention (CDC). These cycles were the parities in reproductive health, so these disparities in only ones in which data were collected on use of feminine Branch et al. Environmental Health (2015)14:57 Page 3 of 8
hygiene products. The sample was restricted to female year sample weights provided in the NHANES laboratory participants aged 20–49 who had self-reported data on files. All analyses were adjusted for the non-random feminine hygiene product use (n = 2432). Of these, 805 sampling design and the sample population weights. A participants had urinary measurements of MEP and (two-sided) P-value <0.05 was considered statistically MnBP. We excluded participants who did not self-identify significant. as non-Hispanic white, non-Hispanic black, or Mexican We tested our primary hypothesis using multivariate American (n = 66) resulting in a final sample size of 739 linear regression models where the outcome was individ- study participants. ual phthalate metabolites and the main exposure variable was use of individual feminine hygiene products. We nat- Phthalate metabolite measurements ural log-transformed phthalate metabolite and creatinine Phthalate metabolites were measured in approximately data prior to regression analysis to account for their non- one-third of NHANES participants. Concentration data for normal distributions. From these regression models, we MEP and MnBP were downloaded from the NHANES estimated the percent changes in phthalate metabolite β website in September 2013. Spot urine samples were col- concentrations by product use as (e( ) −1) * 100 with 95 % β lected in the Mobile Examination Center and stored at confidence intervals (CIs) estimated as (e( ± 1.99 * SE) −1) −20 °C until shipped to CDC’s National Center for Envi- where β and SE are the estimated regression coefficient ronmental Health for analysis. Analytical methods have and standard error, respectively. been described in detail elsewhere [33, 34]. Briefly, concen- We first examined multivariate associations between trations of phthalate metabolites were quantified using solid phthalate metabolite concentrations and feminine hygiene phase extraction-high performance liquid chromatography- product use adjusted only for urinary creatinine concen- isotope dilution-tandem mass spectrometry and expressed trations (to account for urinary dilution) [35]. We then as wet weights (ng/mL). Approximately 99 % of the urinary assessed associations accounting for the following covari- phthalate metabolite data was above the limit of detection ates and potential confounders: age (continuous); body (LOD); values below the LOD were substituted with LOD/ mass index (BMI; continuous); race/ethnicity (non-His- by the CDC [33, 34]. panic white, non-Hispanic black, and Mexican American); Feminine hygiene product use data. As part of the 2001– and educational attainment (less than high school diploma; 2004 NHANES survey, reproductive-aged females were high school diploma or equivalent; or more than high asked the following question during a private face-to-face school diploma). We also conducted a sensitivity analysis interview, “During the past month, have you used any of by further adjusting for household poverty-income ratio the following products for feminine hygiene: tampons, (PIR; the ratio of household income to poverty threshold sanitary napkins, vaginal douches, feminine spray, feminine adjusted to family size and inflation) among the 698 partic- powder, feminine wipes/towelettes, or other feminine ipants with available data. hygiene products?” If the participant responded “yes”,she Lastly, we evaluated whether douche use partially medi- was then asked about the use of each specific product. ated the association between race/ethnicity and phthalate From these questions, we created binary variables (yes/no) exposure in two ways. We first qualitatively examined for each type of product used (e.g. tampons, vaginal whether the effect estimate of race/ethnicity on phthalate douches, etc.) metabolite concentrations changed by greater than ten Data on frequency of use was available for vaginal percent after controlling for douching frequency. We then douche use (but not any other feminine hygiene prod- formally tested for mediation using the Arioan test for ucts). Douching frequency was assessed from the follow- mediation using methodological extensions to accommo- ing survey questions: “During the past 6 months, did you date categorical mediators [36, 37]. douche? By douching we mean putting a substance into your vagina either for routine cleansing or for vaginal irri- Results tation or signs of infection?” If participants responded yes, Phthalate metabolite concentrations, feminine hygiene they were then asked, “During the past 6 months, how product use, and demographic characteristics varied by often did you douche?” We used this data to classify par- race/ethnicity among US reproductive-aged women ticipants into one of three categories indicating intensity (Table 1). Black women were more likely to be obese, and of use: no use, occasional use (douche ≤ once per month), Mexican American women had the lowest educational or frequent use (douche ≥2timespermonth). attainment. Compared to other racial/ethnic groups, white women self-reported significantly higher use of tampons, Statistical analysis whereas black women self-reported significantly higher Analyses were conducted in STATA v13.1. Because we use of the following feminine hygiene products: vaginal combined two survey cycles, we calculated new sample douche, feminine spray, feminine powder, wipes/towel- weights for each participant equal to one half of the two- ettes, and other products (p < 0.05). For example, 37 % of Branch et al. Environmental Health (2015)14:57 Page 4 of 8
Table 1 Demographic characteristics, product use, and concentrations (ng/mL) of MEP and MnBP when com- phthalate metabolite concentrations by race/ethnicity among pared to white or Mexican-American women (p <0.001). US reproductive-aged women, NHANES 2001–2004 (N = 739) Douching was associated with increased urinary MEP White Black Mexican p-valuea concentrations (Table 2) in both unadjusted and adjusted (N = 396) (N = 163) American (N = 180) models. For example, in adjusted models, women that re- Age (years), % ported douching in the past month had 51.6 % (95 % CI: 20-29 29 34 42 0.05 18.8 %, 93.6 %) higher concentrations of MEP than non- 30-39 33 32 32 users. We also observed evidence of a monotonic dose re- 40-49 38 34 26 sponse relationship between douching frequency and MEP concentrations (p-trend <0.001). In adjusted models, BMI (kg/m2), %b <0.001 women who reported occasional douche use in the past <25 44 24 26 6 months had 33.6 % (95 % CI: −0.3 %, 79.2 %) higher 25 – 30 27 25 33 MEP concentrations than non-users, and those who re- ≥30 29 52 41 ported frequent douche use had 152.2 % (95 % CI: 68.2 %, Educational <0.001 278.3 %) higher MEP concentrations than non-users. attainment, % There was evidence of a positive association between < HS graduate 9 25 47 douching and MnBP but it did not reach statistical signifi- HS graduate 22 24 21 cance. There were no other significant associations be- > HS graduate 69 52 31 tween the other feminine hygiene products and either MEP or MnBP although effect estimates were large for Feminine hygiene product use in past monthc,% feminine spray, feminine powder, and other products. As- Tampon 55 31 22 <0.001 sociations did not substantially change when we adjusted Sanitary Napkin 59 66 63 0.13 for household income (data not shown). Vaginal Douche 14 37 10 <0.001 To further understand whether douching partially ex- Feminine Spray 3 16 2 <0.001 plains the relationship between race/ethnicity and phthal- Feminine Powder 2 12 2 <0.001 ate metabolite levels, we modeled two linear regression models for MEP, with and without douching frequency as Wipes/Towelettes 7 16 13 0.004 a covariate (Table 3). In the covariate-adjusted model that Other Products 3 11 5 0.03 did not account for douching, black women had 48.4 % Average douching frequency in past 6 months, % <0.001 higher concentrations of MEP (95 % CI: 16.8 %, 88.6 %), None 83 47 86 and Mexican American women had 58.2 % higher MEP Occasional (≤1/ 11 33 11 concentrations (95 % CI: 24.7 %, 100.8 %) compared to month) white women. After controlling for douching frequency, Frequent (≥2/ 7203 the effect estimate for black women decreased to 26.4 % month) (95 % CI: −0.9 %, 61.2 %), and was no longer statistically Phthalate metabolite concentration (GM (GSE))d significant, while the effect estimate for Mexican Ameri- Mono-ethyl 127 268 247 (26.1) <0.001 can women increased to 70.1 % (95 % CI: 34.1 %, phthalate (MEP; (10.7) (26.5) 115.9 %). Mediation effects of douching were statistically ng/mL) significant for black-white differences (z = 3.71, p < 0.001) Mono-butyl 18.2 (1.0) 32.3 (2.0) 23.7 (2.3) <0.001 but not statistically significant for differences between phthalate (MnBP; ng/mL) Mexican Americans and whites (z = 1.80, p = 0.07). aGroup differences evaluated by ANOVA for natural log transformed phthalate metabolite concentrations and chi square test for categorical variables bData missing for BMI (n =8) Discussion cSome participants used multiple products dGM, Geometric mean; GSE, Geometric standard error In this cross-sectional study of US reproductive aged- women, we found that vaginal douching may be an im- black women reported douching in the previous month portant source of DEP exposure among US reproductive compared to 14 and 10 % of white and Mexican- aged women. In adjusted models, women who reported American women, respectively (Table 1). Similarly, black douching in the past month had 52 % higher urinary women reported douching more frequently than other MEP concentrations than non-users. In addition, there women (p < 0.001). Twenty percent of black women was evidence of a monotonic dose–response relationship reported douching frequently compared to 7 and 3 % in such that women who reported an average douching fre- white and Mexican-American women, respectively. Black quency of two or more times a month had urinary MEP women also had significantly higher geometric mean concentrations that were 152 % higher than nonusers. Branch et al. Environmental Health (2015)14:57 Page 5 of 8
Table 2 Associations of product use and phthalate metabolite concentrations (ng/mL) among US reproductive-aged women, NHANES 2001-2004a MEP MnBP Unadjusted (N = 739) Adjusted (N = 731) Unadjusted (N = 739) Adjusted (N = 731) % change 95 % CI % change 95 % CI % change 95 % CI % change 95 % CI Feminine hygiene product use in past month Tamponb −6.4 (−24.9, 16.6) 6.1 (−16.0, 35.5) 2.4 (−11.8, 18.9) 4.1 (−11.0, 21.9) Sanitary napkinb −7.6 (−21.5, 8.7) −9.0 (−22.8, 7.2) −3.2 (−17.6, 13.6) −4.4 (−18.9, 12.7) Vaginal doucheb 59.5* (22.7, 107.2) 51.6* (18.8, 93.6) 12.2 (−8.3, 37.3) 9.8 (−9.7, 33.6) Feminine sprayb 79.7 (−2.6, 231.4) 63.2 (−12.4, 204.2) 26.4 (−15.0, 88.1) 20.7 (−21.0, 84.3) Feminine powderb 64.9 (−16.4, 225.3) 49.4 (−23.9, 193.2) 23.7 (−25.7, 105.9) 16.6 (−32.1, 100.3) Wipes/ Towelettesb 21.5 (−11.1, 65.9) 14.7 (−16.0, 56.7) −6.5 (−25.8, 17.9) −7.8 (−27.9, 17.9) Other productsb 35.4 (−12.2, 108.7) 26.9 (−19.8, 100.8) 27.8 (−7.5, 76.7) 25.9 (−7.9, 72.1) Average douching frequency in past 6 monthsb Occasional (≤1 month) 40.5* (6.1, 86.1) 33.6 (−0.3,79.2) 7.7 (−5.6, 22.8) 8.2 (−4.5, 22.6) Frequent (≥2 month) 154.4** (68.7, 283.6) 152.2** (68.2, 278.3) 29.0 (−6.2, 77.3) 24.1 (−10.3, 71.8) P-trend <0.001 <0.001 0.094 0.145 aMEP and MnBP concentrations were natural log transformed. All models were adjusted for urinary creatinine; adjusted models additionally controlled for age, race/ethnicity, BMI, and educational attainment bReference group is non-users; *p < 0.05; ** p < 0.001
We found no associations between MEP and the other products could reflect the larger variety of scented and feminine hygiene products. There are many possible rea- unscented products in these different categories relative to sons for the lack of associations found. For example, those available for douching; unfortunately, specific brand scented products used intravaginally may result in greater information and detail about scent was not collected in chemical exposures than scented feminine hygiene prod- NHANES. ucts designed for external use. Alternatively, it is possible We found no association between douching, or any that, despite the large point estimates (see Table 2), the other product use, and urinary MnBP concentrations. wide confidence intervals for the other feminine hygiene This is consistent with most epidemiologic studies that
Table 3 Association between race/ethnicity and MEP (ng/mL) among US reproductive-aged women with and without adjustment for douching frequency, NHANES 2001-2004 Model 1 (N = 731) Model 2 (N = 731) % change 95 % CI % change 95 % CI Race/Ethnicitya Black 48.4* (16.8, 88.6) 26.4 (−0.9, 61.2) Mexican-American 58.2** (24.7, 100.8) 70.1* (34.1, 115.9) Age −0.1 (−1.2, 1.0) −0.4 (−1.5, 0.7) Educational attainmentb < HS graduate 19.0 (−20.2, 77.5) 6.6 (−26.7, 54.9) HS graduate 30.7* (3.4, 65.1) 27.7* (2.3, 59.3) BMI 0.3 (−0.9, 1.5) 0.2 (−1.0, 1.4) Urinary creatinine 129.4** (92.3, 173.8) 124.5** (88.2, 167.9) Douching frequency in past six monthsc Occasional (≤1 month) - - 33.6 (−0.3, 79.2) Frequent (≥2 month) - - 152.2** (68.2, 278.3) R2 0.24 0.27 aReference group is white women bReference group is > HS graduate cReference group is non douche users; *p < 0.05; ** p < 0.001 Branch et al. Environmental Health (2015)14:57 Page 6 of 8
report stronger associations between fragranced personal As our study did not make any direct connection to ad- care products and MEP than MnBP. This may in part be verse health consequences, the human health implications explained by the fact that, on average, higher concentra- of our findings warrant further research. While experi- tions of DEP than DnBP are present in personal care mental animal studies suggest that DEP is not a male products [1, 2]. reproductive toxicant [46], several epidemiologic studies We observed racial/ethnic differences in phthalate expo- have reported associations between maternal concentra- sures as well as feminine hygiene practices consistent with tions of MEP during pregnancy and adverse reproductive prior studies [21, 26]. Compared to white and Mexican and developmental outcomes in their offspring, particu- American women, we found that black women had higher larly males [10, 11, 47]. A recent epidemiologic study of phthalate metabolite levels and were more likely to report adolescent girls found suggestive associations between use of several feminine hygiene products including both in utero and peripubertal MEP concentrations and douches, sprays, and powders. When we controlled for earlier pubertal onset [48]. The disparity between the re- frequency of douching, differences in urinary MEP con- sults in rodent and human studies has not been explained, centrations between black and white women were attenu- but may reflect differences in exposure route (oral admin- ated and no longer statistically significant, suggesting that istration in animals versus dermal or inhalation exposure use of personal care products, such as vaginal douches, in humans), or may be due to other biological differences may contribute to racial/ethnic disparities in phthalates between rodents and humans [25]. Moreover, localized exposures. In contrast, Mexican American women had effects of DEP (or other phthalates) on the vaginal epithe- higher MEP concentrations than white women, but these lium or the vaginal microbiome have not been fully differences were not explained by douching, indicating the considered in prior toxicological or epidemiologic studies. importance of other exposure sources among Mexican Given the high levels of MEP and the widespread expos- Americans. ure in US reproductive-aged women, its effect on vaginal The reasons underlying racial/ethnic differences in health warrant further consideration. douching behavior are complex and likely involve individ- Our current study focused solely on phthalates expos- ual as well as community-level drivers. Among African ure; however, the vaginal route of exposure may also be American and white women, common motivations for important for other chemicals found in these products. douching include: to feel fresh and clean, to remove men- Fragrance is typically a mixture of chemicals [49]. DEP strual blood, to remove vaginal odors, after sexual activity, was a common component of fragrance, but a recent and in response to vaginal discharge or irritation [30, 38]. study suggests that DEP exposure is declining in the US Ferranti hypothesizes that structural forces, such as histor- population [50] and thus manufacturers may be replacing ical odor discrimination against African Americans and it with other chemicals. In addition, preservatives such as targeted advertising of these products to African Ameri- parabens and antimicrobial agents such as triclosan, which cans, have helped to establish the practice of douching as have also been shown to have endocrine-disrupting prop- a beauty norm specifically among the African American erties, may be present in intravaginal products [51]. Fur- community, and that norm is now perpetuated through ther research is needed to understand the effects of cultural and familial traditions [39]. Thus, environmental chemical exposures on reproductive health since little is justice advocates and practitioners may view the dispro- known about the absorption and metabolism of environ- portionate chemical exposures from douching as an “en- mental chemicals that are vaginally administered. A small vironmental injustice of beauty”, a framework that could pharmaceutical study found that serum estradiol concen- also be applied to other beauty practices used predomin- trations were ten times higher when the same dose was ately by women of color such as hair straightening and delivered via vaginal administration compared to oral ad- skin whitening. ministration [52]. The differential uptake observed for Vaginal douching is associated with multiple adverse synthetic hormones may also apply to industrial chemicals health outcomes including increased risks of bacterial since many of them are suspected endocrine disrupters. vaginosis [40], pelvic inflammatory disease [41], and Further work should also examine how variations in vagi- possibly cervical cancer [42], and consequently this prac- nal microbiota may change metabolism and absorption of tice has been discouraged by the American College of environmental chemicals since douching can alter the Obstetrics and Gynecology [43,44]. While these guidance chemical and biological environment of the vagina [53]. documents do not discuss potential chemical hazards and The cross-sectional nature of the study precludes the their consequent health impacts on reproductive health, ability to make any causal inferences about the direction recognition of this and other types of environmental risk of the association between urinary MEP concentration factors is growing among health care providers, and was and douching. Additionally, there may be residual con- recently addressed in an ACOG Committee Opinion enti- founding from unaccounted phthalate sources. Higher tled “Exposure to Toxic Environmental Agents” [45]. MEP levels have been associated with use of multiple Branch et al. Environmental Health (2015)14:57 Page 7 of 8
personal care products such as perfumes/colognes, cos- contemporary populations with more precise data and in- metics, and hair care products [19, 25, 27]. Data on clude assessment of other endocrine-disrupting chemicals these potential sources of exposures were not available that may be used in vaginal douches. Additionally, further in NHANES. It is possible that women who frequently research is needed on the adverse reproductive health douche are also more likely to use other scented consequences of chemical exposures originating from personal care products. Among our study population, feminine hygiene products that are used in and around women who douched reported using more feminine the vaginal area. hygiene products than those who did not douche (data – Abbreviations not shown). However, the observed dose response rela- DEP: Diethyl phthalate; DnBP: Di-n-butyl phthalate; MEP: Monoethyl tionship coupled with the null associations with the phthalate; MnBP: Mono-n-butyl phthalate; SES: Socioeconomic status; other feminine hygiene products supports a plausible re- NHANES: National Health and Nutrition Examination Survey; CDC: US Centers for Disease Control and Prevention; LOD: Limit of detection; CI: Confidence lationship that warrants investigation in future studies. interval; BMI: Body mass index; PIR: Household poverty-income ratio. Another limitation of this study is that we did not have information on the chemical ingredients of the douches Competing interest used by study participants. For example, homemade The authors declare that they have no competing interests. douching solutions comprised of vinegar and water Authors’ contributions would be less likely to have phthalates than commer- ARZ conceived of the research question and directed the study’s cially manufactured products; however, prior studies implementation. FB conducted the statistical programming and data analysis. ARZ and FB led the writing with significant input from SDM and TJW. All suggest that majority of women use commercially manu- authors read and approved the final manuscript. factured douching products [30, 38]. Lastly, there may be exposure misclassification since we only had access Acknowledgements to single, spot urine measurements and phthalates have Funding was provided by Pew Charitable Trusts, Passport Foundation, Forsythia Foundation, the Fred Gellert Family Foundation, and National a short half-life in the human body [3,4]. Previous stud- Institute of Environmental Health Sciences R00ES019881. ies have shown that women’s exposures to MEP and MnBP are relatively stable, with greater variability be- Author details 1Department of Environmental and Occupational Health, Milken Institute tween individuals than within individuals [54]. However, School of Public Health, George Washington University, 950 New Hampshire use of feminine hygiene products is likely episodic, vary- Avenue NW, Suite 414, Washington DC 20052, USA. 2Program on ing across the menstrual cycle. Unfortunately, NHANES Reproductive Health and the Environment, Department of Obstetrics, Gynecology, and Reproductive Sciences, University of California, San only measures whether a product was or was not used Francisco, Oakland, CA, USA. in the last month, so we were not able to determine time since product use (or frequency of use) very precisely. Received: 10 November 2014 Accepted: 7 April 2015 This measurement error is likely nondifferential and would bias our results towards the null. Given the poten- References tial for nondifferential misclassification, the robust finding 1. Koniecki D, Wang R, Moody RP, Zhu J. Phthalates in cosmetic and personal care products: Concentrations and possible dermal exposure. Environ Res. between vaginal douching and MEP levels is quite 2011;111:329–36. remarkable. 2. Hubinger JC, Havery DC. Analysis of consumer cosmetic products for Our study also has several notable strengths. To our phthalate esters. J Cosmet Sci. 2006;57:127–37. 3. Koch HM, Preuss R, Angerer JD. Di (2‐ethylhexyl) phthalate (DEHP): Human knowledge, this study is one of the few, if not only, to metabolism and internal exposure–an update and latest results1. Int J examine the association between self-reported use of fem- Androl. 2006;29:155–65. inine hygiene products and urinary biomarkers of chemical 4. 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