This study looked to identify determinants of exposure to dioxin in breast milk from breast-feeding women in a hot spot of dioxin exposure in Vietnam. Breast milk was collected from 140 mothers 1 month after delivery. The risk factors investigated included length of residency, drinking of well water and the frequency of animal food consumption. Cluster analysis was performed to identify dietary patterns of fish and meat portions, fish variety and egg variety. Residency, age and parity were clearly associated with increased dioxin levels. Drinking well water and the consumption of marine crab and shrimps were related to higher levels of furans in breast milk. The consumption of quail eggs also appeared to be associated with increased levels of some dioxin isomers in this area. Some mothers who ate no or less meat than fish and mothers who consumed more freshwater fish than marine fish had lower levels of dioxins in their breast milk. However, the type of water and the eating habits of mothers contributed only partly to the increased dioxin levels in their breast milk; the length of residency was the most important risk factor associated with increased dioxin body burdens of mothers.
Several decades after herbicide sprays were used during the Vietnam War, the concentrations of dioxins in the environment and in humans in sprayed areas remain elevated.1, 2, 3 In the “hot spots” of dioxin contamination areas around military airbases that were formerly used for the storage of herbicides, extremely high levels of dioxins were detected in soil samples.4 Our previous study reported that dioxin levels in the breast milk of mothers in the hot spots of dioxin contamination were three to four times higher than those of mothers in unsprayed areas in Vietnam.5 Moreover, the length of residency and the age and the parity of these mothers in hot spot areas were highly related to dioxin levels in breast milk.5 However, other determinants of exposure associated with increased maternal dioxin body burden remain unknown.
In general, more than 90% of human exposure to dioxins comes from the food supply.6 In Japan, seafood is thought to be the food that contributes most to increased dioxin exposure;7 in the Netherlands, the country with the highest levels of dioxin in breast milk in Europe,8 meat was found to be associated with increased maternal dioxin body burden and increased levels of dioxins in breast milk.9 In China, the food most likely associated with increased dioxin levels is freshwater fish.10 Furthermore, previous studies in Norway11 and Japan12 suggested that dietary patterns were important factors related to the levels of dioxin exposure.
In a hot spot of dioxin contamination in Bien Hoa city, Vietnam, high concentrations of dioxins were reported in duck, beef, free-ranging chicken and freshwater fish grown in the local area;13 however, the contribution of food intake and/or dietary patterns to human exposure levels has not been investigated. Therefore, in this study, we investigated the associations between dioxin levels in breast milk and relevant risk factors, including age, length of residency, drinking water and eating habits in mothers living in one of the dioxin hot spots in Da Nang to identify the determinants of exposure associated with increased levels of dioxins in the breast milk of mothers living in a dioxin-contaminated area in Vietnam.
MATERIALS AND METHODS
Study Area and Subjects
Da Nang airbase, which was a storage site for herbicides during the Vietnam War, is located inside Da Nang city, a densely populated area. The Thanh Khe district encloses almost the entire perimeter of this airbase and is situated 3 km away from the airbase. Environmental studies reported high dioxin levels in the soil and sediment of canals and ponds in the Thanh Khe district owing to the passage of water containing soil particles with dioxins from contaminated soil in the airbase.3
In 2008–2009, we conducted an epidemiological follow-up survey targeting 159 mothers who gave birth at Thanh Khe district hospital; we collected breast milk from 147 mothers (92.5%) 1 month postpartum. Face-to-face interviews were conducted with 140 mothers (88.1%) using a questionnaire on background information 4 months postpartum and a food frequency questionnaire (FFQ) 1 year postpartum.
Informed consent was obtained from all mothers. The institutional ethics board of epidemiological studies at Kanazawa Medical University approved the study design, and the Department of Health and Prevention of Diseases of the Da Nang city government in Vietnam reviewed and approved the informed consent process.
Quantification of Dioxin Isomers in Breast Milk
After collection, milk samples were stored in clean polyethylene containers at −4 °C in each local health center and transported to Japan on dry ice. Concentrations of seventeen 2,3,7,8-substituted PCDDs/Fs congeners were analyzed in High Technology Center, Kanazawa Medical University (Uchinada, Japan) using ∼10 ml of breast milk. After fat extraction and a series of purifying operations, quantification was performed using a gas chromatograph (HP-6980; Hewlett-Packard, Palo Alto, CA, USA) equipped with a high-resolution mass spectrometer (HR-GC/MS; Mstation-JMS700, JEOL, Tokyo, Japan) operating in the selected ion-monitoring mode. The established method of analysis has been described in detail in previous studies.5 Concentrations of 17 congeners of PCDDs/Fs were lipid-base calculated. Toxic equivalent factors (TEFs) for each congener were referenced from the WHO 2005-TEF.14 Toxic equivalents (TEQs) of polychlorinated dibenzofurans (PCDDs), PCDFs and PCDDs/Fs were calculated by multiplying each congener concentration by its TEF and adding up the values.
In the present study, the levels of dioxin-like PCBs (dl-PCBs) were not measured in all subjects. However, dl-PCBs congeners were measured in four samples and lower TEQ levels of dl-PCBs were found as compared with those in 12 mothers in northern Vietnam.15 These findings suggest that the contribution of dl-PCBs to total TEQ is not high, and TEQ-PCDDs/Fs can be used as an indicator of dioxin toxicity in this contaminated area.
Structured questionnaires were used to obtain demographic maternal information (age, history of residency, well water use, parity, smoking history of the mother and family members, alcohol consumption, employment and monthly family income); the characteristics of 140 mothers are shown in Table 1.
Because no standardized FFQ was available for Vietnamese in this area, we designed our own questionnaire focused on foods of animal origin that were reported to be sources of contamination in previous studies conducted in a hot spot area in Vietnam13, 16 and in other areas.7, 9, 17 We asked mothers about their weekly intake of 7 main groups of food of animal origin and 28 sub-groups, including fish, meat, eggs and dairy products. For eggs, milk and yogurt, we asked mothers to estimate the quantity ingested per week. The frequencies and amounts of food ingested are shown in Table 1.
Identification of Dietary Clusters
Cluster analysis was performed to identify dietary patterns based on consumption frequency or quantity per week using a k-means cluster algorithm. Before analysis, frequencies and quantities for all food groups were transformed into standardized z-scores, which allowed us to calculate the probability of a score occurring within our normal distribution. Three dietary patterns, including “meat/fish intake pattern,” “fish variety pattern” and “egg variety pattern” were identified from fish and meat intake; intake of marine, freshwater and other type of fish; and intake of chicken, duck and quail eggs, respectively. Food intake frequencies compared across dietary clusters in each dietary pattern are shown in Supplementary Table 1.
The SPSS (ver.11.0) software package for Windows (SPSS; Chicago, IL, USA) was used to perform the statistical analysis. Concentrations of PCDDs/Fs isomers, TEQs of PCDDs, PCDFs and PCDDs/Fs in breast milk were base-10 logarithmically transformed to improve normality. The values of the concentrations of congeners below the detection limits were set to equal half of the detection limits. General linear model (GLM) was used to analyze the associations between dioxins in breast milk and maternal factors, and to test the difference in dioxin levels in breast milk between groups of mothers with different histories of well water use, eating habits and different clusters of dietary patterns after adjusting for maternal age, parity and residency. The GLM procedure in SPSS incorporates normally distributed dependent variables and categorical or continuous independent variables, and computes sums of squares (type III) with effect size to show the magnitude of the effect of independent variables. Partial Eta squared (η2) is calculated for effect sizes in the GLM function of SPSS.
Relationships Between Maternal Factors and Dioxin Levels in Breast Milk
We investigated the association between dioxin levels in breast milk and age, residency and parity (1, primipara; 2, multipara) using GLM analysis. The mean square values with effect sizes of maternal age, length of residency and parity are shown in Table 2. All three TEQs, all seven PCDD isomers and two PCDF isomers were significantly positively correlated with maternal age after adjusting for other factors. In particular, the effect sizes of 1,2,3,7,8-PentaCDD, 1,2,3,4,7,8-HexaCDD and OctaCDD were >0.1, suggesting a higher contribution of age toward the concentrations of these isomers. Parity was also significantly associated with three TEQs, four PCDD isomers and 2,3,4,7,8-PentaCDF, with effect sizes >0.1 for 1,2,3,7,8-PentaCDD, 2,3,4,7,8-PentaCDF and TEQ-PCDDs. Maternal residency in the Thanh Khe area was significantly associated with three TEQs, all PCDD isomers except 1,2,3,4,6,7,8-HeptaCDD and all PCDF isomers except 1,2,3,7,8,9-HexaCDF after adjusting for other factors. The effect sizes of three TEQs, three PCDD isomers (including 2,3,7,8-TetraCDD) and four PCDF isomers were >0.1, suggesting that length of residency contributed more to increased dioxin levels in breast milk than age and parity.
Relationships Between Well Water Use and Dioxin Levels in Breast Milk
The levels of 1,2,3,4,7,8- and 1,2,3,6,7,8-HexaCDDs; 1,2,3,4,6,7,8-HeptaCDD, 1,2,3,4,7,8- and 1,2,3,6,7,8-HexaCDFs; and 1,2,3,4,6,7,8- and 1,2,3,4,7,8,9-HeptaCDFs were found to be significantly higher in mothers who drank well water than in mothers who did not after adjusting for age, residency and parity (Supplementary Table 2). However, the effect sizes associated with these seven isomers were small and there were no significant differences in TEQs in breast milk between mothers in these two groups. These results suggested that well water might contribute to increased levels of dioxin in the breast milk of our subjects but more discussion is needed to make this point clear.
Relationships Between Specific Food Consumption and Dioxin Levels in Breast Milk
The relationships between the consumption of specific food items and dioxin levels in breast milk were investigated after adjusting for age, residency and parity. Dioxin levels in breast milk were compared among four groups characterized by different frequencies of meat consumption: never, sometimes (2–3 times/week), often (4–5 times/week) and daily (≥7 times/week). The adjusted mean levels of dioxins in breast milk and effect sizes are shown in Table 3. Meat-eating categories and dioxin levels in breast milk were significantly associated for TEQs of PCDFs and PCDDs/Fs and 13 dioxin isomers; significant differences were identified between the groups that never consumed meat and the other groups. Breast milk samples in the “never” group had the lowest levels of almost all TEQs and PCDDs/Fs isomers except for 2,3,7,8-TetraCDD, 1,2,3,7,8,9-HexaCDF and OctaCDF isomers, suggesting that meat eating influenced the levels of these isomers. In particular, meat eating explained increased levels of TEQ-PCDFs, 1,2,3,4,7,8- and 1,2,3,6,7,8-HexaCDFs and two HeptaCDFs, as shown by higher effect sizes (≥0.1).
Dioxin levels in breast milk were also compared between groups with different freshwater fish (yes/no) and marine crab and shrimp (yes/no) eating habits (Table 4). Breast milk samples of mothers who ate freshwater fish had significantly lower levels of TEQ-PCDFs and six PCDF isomers than those of mothers who did not consume freshwater fish. In contrast, breast milk samples of mothers who ate marine crab and shrimp had significantly higher levels of TEQ-PCDFs, three PCDD isomers and six PCDF isomers than those of mothers who did not eat these food items. However, the effect sizes for fish-eating habits were small (<0.1), and these eating habits likely contributed slightly to the increased levels of TEQ-PCDFs and nine PCDDs/Fs isomers.
Relationships Between Dietary Patterns and Dioxin Levels in Breast Milk
Dioxin levels in breast milk were also compared among clusters of three dietary patterns, after adjusting for age, length of residency and parity; the results of this analysis are listed in Tables 5, 6, 7.
Table 5 shows the comparisons of dioxin levels in breast milk among mothers of four clusters of fish and meat consumption patterns. The levels of 1,2,3,7,8-PentaCDD and two TEQs of PCDDs and PCDDs/Fs were significantly related to clusters of fish/meat-eating patterns. Milk samples from clusters 2–4 (“high-meat,” “low-meat” and “high-fish and -meat” groups) had significantly higher levels of TEQs-PCDDs, PCDDs/Fs and 1,2,3,7,8-PentaCDD than those from the “high-fish and low-meat” group (cluster 1). However, the effect sizes of fish and meat consumption patterns were generally small, with a maximum value of 0.07 for TEQ-PCDDs.
As shown in Table 6, levels of TEQs of PCDFs and PCDDs/Fs and of five PCDD and seven PCDF congeners in breast milk were found to be significantly related to fish consumption patterns. Breast milk levels of TEQs of PCDFs and PCDDs/Fs and of 12 dioxin isomers in the “low freshwater fish” and “high marine fish” groups (clusters 2 and 3) were significantly higher than those in the “high freshwater fish” group (cluster 1). In addition, the levels of 2,3,7,8-TetraCDF in the “high marine fish” group and of 2,3,4,7,8-PentaCDF in the “low freshwater fish” and “high marine fish” groups were significantly higher than those in the “high freshwater fish” group by tests between groups. However, the effect sizes of fish consumption patterns for all TEQs and isomers were <0.1.
The comparisons of dioxin levels in breast milk among mothers of different egg variety clusters are shown in Table 7. Significant differences in 1,2,3,7,8-PentaCDD, 1,2,3,6,7,8-HexaCDD, OctaCDD and 2,3,4,7,8-PentaCDF levels were identified among the three clusters. The levels of these four isomers in the “quail egg dominant” group were significantly higher than in the “chicken egg dominant.” In particular, 1,2,3,6,7,8-HexaCDD and OctaCDD levels were also higher in the “quail egg dominant” group than in the “low egg intake” group. However, the effect sizes of egg variety patterns were small (≤0.06) for these four isomers.
In this research, the age of mothers was determined to be a strong risk factor for high dioxin concentrations in breast milk. This result confirmed those of previous studies in other countries,18, 19, 20 that mothers’ age and a history of breastfeeding were found to be associated with higher concentrations of dioxins in breast milk. In our present subjects, all mothers breastfed their previous and present child/children, and parity was also found to be significantly associated with high dioxin levels in breast milk even after adjusting for age and residency. This result was in line with a previous report in the USA that breastfeeding can decrease the dioxin concentration in blood and breast milk of women.21 Therefore, parity is strongly related to a decrease in the dioxin body burden of mothers living here. Furthermore, we found that residency around Da Nang airbase was significantly associated with high dioxin levels for all TEQs and almost all isomers. Similar finding was obtained in our previous study that targeted two major hot spots,5 but, in the present study, we showed that effect sizes of length of residency for three TEQs and 2,3,7,8-TetraCDD were large (≥1.2), indicating that long-term residence is a strong risk factor for an increased dioxin body burden in mothers living here. In particular, 2,3,7,8-TetraCDD, which is the most abundant dioxin isomer of Agent Orange, was highly associated with residency. Therefore, decreasing the dioxin levels in the living environment is crucial for decreasing the maternal dioxin body burden.
In a previous study in Canada,22 contamination of persistent organic pollutants in drinking water was suggested to be a potential risk to human health. Although dioxins have low solubility, they are attached to organic carbon in the water (particulate phase) and supplied into water from contaminated sediment.23 In the present study, we found that the levels of some dioxin isomers in breast milk were higher in mothers who still drink/used to drink well water than in mothers who never drank well water after controlling for age, residency and parity. Well water used to be the main source of water for drinking, cooking and daily activities in this area; well water might be one source of exposure to dioxins, as underground water around the airbase may have been contaminated. However, effect sizes of drinking well water for all dioxin isomers were small, thus well water might not be the main route of dioxin exposure here.
Because >90% of human exposure to dioxins in the general environment occurs through foods, diet was thought to have an important role in increasing the body burden of dioxins in contaminated areas. Foods of animal origin, such as meat (which contains a lot of fat), were reported to be high-risk foods for dioxin contamination. Patandin et al.9 indicated that consuming animal products such as meat increased maternal dioxin body burden, leading to increased dioxin levels in breast milk in the Netherlands. In Bien Hoa, a hot spot of dioxin contamination in Vietnam, Schecter et al.13 reported high dioxin levels of 18.8 and 236 ppt TEQ in locally grown chicken and duck meat, respectively, suggesting that chicken and duck meat might be high-risk foods for dioxin exposure in a hot spot in Vietnam. In the present survey, we also measured higher dioxin levels in the breast milk of mothers who ate meat than in mothers who did not eat meat. The effect sizes of meat-eating habits were larger than 0.1 for TEQ-PCDFs, 1,2,3,4,7,8- and 1,2,3,6,7,8-HexaCDFs and 1,2,3,4,6,7,8- and 1,2,3,4,7,8,9-HeptaCDFs, indicating that eating meat might be a determinant of exposure for increased PCDF isomer levels in breast milk. However, no differences in 2,3,7,8-TetraCDD levels in breast milk were identified among groups with different meat-eating frequencies.
The frequency of meat consumption is related to that of fish consumption. Therefore, we also analyzed relationships between dioxin levels in breast milk and meat and fish consumption patterns. Eating habits in the study area were quite similar to those in other coastal cities in Vietnam where marine fish and seafood are eaten daily and freshwater fish are rarely consumed. In previous surveys conducted in Asian countries, fish and seafood have been reported to have high levels of dioxin TEQ. Marine fish had the highest PCDD/F levels of all food samples in Taiwan24 and in Japan;25 this finding was expected, as marine fish typically have high percentages of fat. However, no associations between the intake of marine fish/seafood estimated by FFQs and dioxins in breast milk were detected in previous surveys in Japan20, 25 or in our study. This finding may be explained by the fact that all mothers had similar fish-eating habits and frequently consumed marine fish (8.3 times/week). However, mothers who ate marine crab and shrimp had significantly higher dioxin levels (especially of PCDF isomers) than mothers who did not eat marine crab or shrimp. These results suggest that special marine products might be one of the sources of dioxin in the study area.
Schecter et al.13 reported that freshwater fish was one of the highest dioxin-contaminated foods in Bien Hoa, one of the dioxin hot spots in Vietnam, with high levels of 2,3,7,8-TetraCDD and TEQ-PCDDs/Fs in these animals. In China, Leng et al.10 reported that mothers living in the Tianjin area who consumed high amounts of freshwater fish had higher levels of PCDDs/Fs than mothers in the Yantai area who consumed more marine fish. Similarly, in the present study area, high levels of dioxins in freshwater fish in a lake near the former US airbase and in the breast milk of one mother who frequently consumed freshwater fish from this lake have been reported,3 suggesting that the consumption of freshwater fish is associated with increased levels of dioxins in breast milk. However, in our present survey, we observed lower levels of TEQ-PCDFs and of six PCDF isomers in the breast milk of mothers who ate freshwater fish than in the breast milk of mothers who did not eat freshwater fish. One possible explanation for this unexpected result may be that the frequency of consumption of freshwater fish was low (0.6 times/week), indicating a low association between freshwater fish and increased dioxin exposure in this area. Moreover, freshwater fish consumption is influenced by consumption of marine fish and other seafood. Therefore, we divided the subjects into three clusters in accordance with their fish consumption patterns and analyzed the relationships between dioxin levels in breast milk and fish consumption.
Arisawa et al.12 suggested that the analysis of dietary patterns is useful for identifying the dietary characteristics of people with high dioxin body burden. In the present study, mothers in the “high fish and low meat” group who consumed fish and meat 23.7 and 4.2 times per week, respectively, had lower levels of dioxins in their breast milk than mothers in the three other groups who consumed more meat. This result is consistent with the observation that mothers who did not eat meat had lower levels of dioxin in their breast milk and that no differences in dioxin levels were identified among mothers with different fish-eating habits.
Mothers from the “high freshwater fish” group who consumed freshwater fish 4.2 times a week had lower levels of dioxins (especially HeptaCDD and some PCDF isomers) than mothers from the other two groups who consumed marine fish more frequently, further corroborating the results of the comparison between the groups who did and did not consume freshwater fish. A survey conducted in Japan showed that people who have a dietary pattern of “seafood and alcohol” had significantly increased blood levels of total TEQ- PCDDs/Fs/dl-PCBs, suggesting that increased fish intake is associated with increased dioxin body burden.12 However, the subjects of this study consisted of 1656 residents of both sexes who lived in 60 areas throughout Japan with different dietary habits.12 In a Norwegian study, Kvalem et al.11 studied people who have big differences of dietary habits between them and found that subjects who frequently consumed seafood and game (typical “northern coastal” Norwegian food) had higher blood levels of dioxin-like compounds. Therefore, the lack of a clear relationship between fish consumption and dioxins in breast milk in our survey may be partly due to small differences in lifestyle and dietary habits among our subjects, as all women lived in a single area.
Moreover, 2,3,7,8-TCDD is a typical indicator of dioxin contamination originating from Agent Orange, but frequency and pattern of fish intake and well water use were associated with levels in breast milk of Hexa- and Hepta-CDDs/Fs, particularly furans, in this study. One reason may be that herbicides other than Agent Orange were also used during the Vietnam War. Elevation of dioxin isomers other than 2,3,7,8-TCDD in sediment of lakes and canals was reported in the environmental survey in and around Da Nang airbase.3 The other reason may be chronological changes of the congener compositions when passed through many living organisms in water including underground, river and sea water.5, 23 However, more surveys on levels and dynamics of dioxins in water and aqueous living organisms are needed in this area.
Quail egg intake was thought to be related to increasing levels of certain dioxin isomers in breast milk, although effect sizes were small. However, there are very few studies that have investigated dioxin levels of quail eggs. A study in Taiwan16 reported that a duck egg farmer and family members who consumed duck eggs had higher levels of dioxins in their serum than families who consumed chicken eggs. Kijlstra et al.26 demonstrated a relationship between dioxins in the soil and free-range chicken eggs from laying hens with access to soil in organic farms in the Netherlands. Moreover, in Bien Hoa, a hot spot area of dioxin contamination in Vietnam, high levels of dioxin contamination and particularly high levels of 2,3,7,8-TetraCDD were recently observed in local free-range chicken and duck eggs,15 suggesting that eggs can be associated with increased dioxin body burden in residents of a hot spot. However, quails are not growing around airbase, and contamination of dioxins in quail eggs was not clear in this area.
The results of the analysis of food consumption and dietary patterns suggest that food may contribute only slightly to the increased dioxin levels in the breast milk of women from this area. Three explanations might explain this finding: (1) we could assess only recent foods, (2) many types of food are grown or caught outside of the contaminated area and (3) the rearing of chickens and ducks in this area and the fishing of freshwater fish in the contaminated lake have been prohibited. We cannot readily recommend that mothers living in this area stop eating specific foods associated with dioxin exposure. Furthermore, breastfeeding is still strongly recommended for all infants in a dioxin hot spot, as breast milk is an excellent food for infants because of its ideal levels of nutrients and protective antibodies.
The length of residency was a strong determinant of exposure to dioxins including TCDD for breast-feeding women in a hot spot of dioxin exposure. Drinking well water and the consumption of specific food items, such as marine crab and shrimps, and quail eggs might be related to increased levels of several dioxin isomers other than TCDD. Moreover, these consumptions of mothers contributed only partly to the increased dioxin levels in their breast milk. Therefore, cleaning up the contamination of residential areas are very important measures for preventing continued exposure to dioxins in the next generation.
Mai TA, Doan TV, Tarradellas J, Felippe de Alencastro L, Grandjean D . Dioxin contamination in soils of Southern Vietnam. Chemosphere 2007; 67: 1802–1807.
Schecter A, Hoang TQ, Päpke O, Tung KC, Constable JD . Agent Orange, dioxins, and other chemicals of concern in Vietnam: Update 2006. J Occup Environ Med 2006; 48: 408–413.
Hatfield Consultants and the Office of National Steering Committee 33. Comprehensive Assessment of Dioxin Contamination in Da Nang Airport, Viet Nam: Environmental Levels, Human Exposure and Options for Mitigating Impacts. Final Report 2009. http://www.hatfieldgroup.com/wp-content/uploads/AgentOrangeReports/DANDI-II1450/Da%20Nang%202009%20Report.pdf.
Dwernychunk LW . Dioxin hot spots in Vietnam. Chemosphere 2005; 60: 998–999.
Tai PT, Nishijo M, Kido T, Nakagawa H, Maruzeni S, Anh NTN et al. Dioxin concentrations in breast milk of Vietnamese nursing mothers: A survey four decades after the herbicide spraying. Environ Sci Technol 2011; 45: 6625–6632.
WHO, IARC. Polychlorinated dibenzo-p-dioxins and polychlorinated dibenzo furans, in: IARC Monographs on the evaluation of carcinogenic risks to humans. Vol. 69. IARC: Lyon. 1997.
Sasamoto T, Horii S, Ibe A, Takada N, Shirota K . Concentration changes of PCDDs, PCDFs, and dioxin-like PCBs in human breast milk samples as shown by a follow-up survey. Chemosphere 2006; 64: 642–649.
Baars AJ, Bakker MI, Baumann RA, Boon PE, Freijer JI, Hoogenboom LAP et al. Dioxins, dioxin-like PCBs and nondioxin-like PCBs in foodstuffs: occurrence and dietary intake in the Netherlands. Toxicol Lett 2004; 151: 51–61.
Patandin S, Dagnelie PC, Mulder PG, Op de Coul E, Van der Veen JE, Weisglas-Kuperus N et al. Dietary exposure to polychlorinated biphenyls and dioxins from infancy until adulthood: a comparison between breast-feeding, toddler, and long-term exposure. Environ Health Perspect 1999; 107: 45–51.
Leng JH, Kayama F, Wuang PY, Nakamura M, Nakata T, Wuang Y . Levels of persistent organic pollutants in human milk in two Chinese coastal cities, Tianjin and Yantai: Influence of fish consumption. Chemosphere 2009; 75: 634–639.
Kvalem HE, Knutsen HK, Thomsen C, Haugen M, Stigum H, Brantsaeter AL . Role of dietary patterns for dioxin and PCB exposure. Mol Nutr Food Res 2009; 53: 1438–1451.
Arisawa K, Uemura H, Hiyoshi M, Kitayama A, Takami H, Sawachika F et al. Dietary patterns and blood levels of PCDDs, PCDFs, and dioxin-like PCBs in 1656 Japanese individuals. Chemosphere 2011; 82: 656–662.
Schecter A, Hoang TQ, Pavuk M, Päpke O, Malisch R, Constable JD . Food as a source of dioxin exposure in the residents of Bien Hoa city, Vietnam. J Occup Environ Med 2003; 45: 781–788.
Van den Berg M, Birnbaum LS, Denison M, Vito MD, Farland W, Feeley M et al. The 2005 World Health Organization Revolution of human and mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicol Sci 2006; 93: 223–241.
Nishijo M, Tai PT, Nakagawa H, Maruzeni S, Anh NTN, Luong HV et al. Impact of perinatal dioxin exposure on infant growth: a cross-sectional and longitudinal studies in dioxin-contaminated areas in Vietnam. PLoS One 2012; 7: e4027.
Traag W, Hoang Thi T, Murk T, Hoogenboom L . Dioxins in free range consumption eggs from Vietnam: levels and health risks. Organohalogen Compounds 2012; 74: 1373–1376.
Chen HL, Huang HY, Huang PC, Lee CC . Relationship of PCDD/F concentrations in duck-egg farmers and consumption of ranched duck eggs in central Taiwan. Environ Toxicol Chem 2010; 29: 2402–2408.
Ulaszewska MM, Zuccato E, Capri E, Iovine R, Colombo A, Rotella G et al. The effect of waste combustion on the occurrence of polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzo furans (PCDFs) and polychlorinated biphenyls (PCBs) in breast milk in Italy. Chemosphere 2011; 82: 1–8.
Nakatani T, Okazaki K, Ogaki S, Itano K, Fujita T, Kuroda K et al. Polychlorinated dibenzo-p-dioxins, polychlorinated dibenzofurans, and coplanar polychlorinated biphenyls in human milk in Osaka city, Japan. Arch Environ Contam Toxicol 2005; 49: 131–140.
Guan P, Tajimi M, Uehara R, Watanabe M, Oki I, Ojima T et al. Associations between dietary intake and breast milk dioxin levels in Tokyo, Japan. Pediat Int 2005; 47: 560–566.
Schecter A, Papke O, Lis A, Ball M, Ryan JJ, Olson JR et al. Decrease in milk and blood dioxin levels over two years in a mother nursing twins: estimates of decreased maternal and increased infant dioxin body burden from nursing. Chemosphere 1996; 32: 543–549.
Ritter L, Solomon K, Sibley P, Hall K, Keen P, Mattu G et al. Sources, pathways, and relative risks of contaminants in surface water and groundwater: a perspective prepared for the Walkerton inquiry. J Toxicol Environ Health A 2002; 65: 1–142.
Environmental Agency in Japan Handbook of dynamics model of dioxins. Division of environmental dioxin contamination control, Environmental Agency. Tokyo, Japan 2004. http://www.env.go.jp/chemi/dioxin/hand.
Wang IC, Wu YL, Lin LF, Chang-Chien GP . Human dietary exposure to polychlorinated dibenzo-p-dioxins and polychlorinated dibenzo furans in Taiwan. J Hazard Mater 2009; 164: 621–626.
Nakatani T, Ogaki S, Itano K, Fujita T, Mori Y, Endo G . Toxic equivalent (TEQ) levels and characteristics of PCDD/F and CoPCB concentrations in marine foods in Japan. Bull Environ Contam Toxicol 2006; 77: 237–244.
Kijlstra A, Traag W, Hoogenboom L . Effect of flock size on dioxin levels in eggs from chickens kept outside. Poultry Sci 2007; 86: 2042–2048.
We thank all mothers participating in this study. We are grateful to medical staffs in Health Department of DaNang city, Thanh Khe district hospital, and Commune Health Centers in Thanh Khe district for their collaboration in surveys. This work was supported partly by Project Research from JSPS Asian Core Program, and the Japan Society for the promotion of science (Grant-in-Aid for Scientific Research (B) (25305024) and (25290005)).
The authors declare no conflict of interest.
Supplementary Information accompanies the paper on the Journal of Exposure Science and Environmental Epidemiology website
About this article
Cite this article
Anh, N., Nishijo, M., Tai, P. et al. Maternal risk factors associated with increased dioxin concentrations in breast milk in a hot spot of dioxin contamination in Vietnam. J Expo Sci Environ Epidemiol 24, 489–496 (2014). https://doi.org/10.1038/jes.2013.73
- breast milk
- exposure risk factor
- eating habit