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American Journal of Epidemiology Copyright © 1998 by The Johns Hopkins University School of Hygiene and Public Health All rights reserved Vol. 148, No. 2 Printed in U.S.A. Fish Consumption and Breast Milk PCB Concentrations among Mohawk Women at Akwesasne Edward F. Fitzgerald, 1 Syni-An Hwang, 1 Brian Bush, 2 Katsi Cook, 3 and Priscilla Worswick 3 A study was conducted to determine the relation between the consumption of contaminated local fish and concentrations of total polychlorinated biphenyls (PCBs) and 68 PCB congeners in the milk of nursing Mohawk women residing near three hazardous waste sites. From 1986 to 1992, 97 Mohawk women were interviewed and donated at least 50 ml of breast milk. The comparison population consisted of 154 Caucasians. After adjustment for potential confounders, Mohawk mothers who gave birth in 1986-1989 had a geometric mean milk total PCB concentration of 0.602 ppm (fat basis) compared with 0.375 ppm for the control group (p = 0.009). These Mohawk women also had significantly higher geometric mean concentrations of nine congeners. Beginning in 1990, however, there were no significant differences between the Mohawk women and the comparison group. Estimated cumulative lifetime exposure from local fish consumption was significantly related to milk total PCB and to three congeners only among those Mohawks who gave birth from 1986 to 1989. The reduction in breast milk PCB concentrations parallels a corresponding decrease in local fish consumption and may be the result of the advisories that have been issued over the past decade recom- mending against the consumption of local fish by pregnant and nursing Mohawk women. Am J Epidemiol 1998:148:164-72. hazardous waste; Indians, North American; milk, human; organochlorine; polychorinated biphenyls Polychlorinated biphenyls (PCBs) are very persis- tent, lipophilic compounds that bioaccumulate and biomagnify in the food chain (1). Ingestion, including the consumption of contaminated sportfish (2), is con- sequently a major route of human exposure. Native American communities, particularly those around the Great Lakes and the Pacific Northwest, are believed to be at particularly high risk of such exposure, since they typically are more dependent on local fish and game as a food source than are other populations. However, very few studies have directly assessed PCB body burdens and fish consumption among Native American people, especially those who live on reser- vations and reside outside of Alaska (3). The purpose of this paper is to present data regarding the associa- tion between the consumption of local fish contami- nated with PCBs from hazardous waste and the milk Received for publication July 17, 1997, and accepted for publi- cation December 30, 1997. Abbreviation: PCBs, polychlorinated biphenyls. 1 Bureau of Environmental and Occupational Epidemiology, New York State Department of Health, Albany, NY. 2 Laboratory of Organic Analytical Chemistry, Wadsworth Center, New York State Department of Health, Albany, NY. 3 Akwesasne Task Force on the Environment, Mohawk Nation at Akwesasne. Reprint requests to Dr. Edward F. Fitzgerald, Bureau of Environ- mental and Occupational Epidemiology, New York State Depart- ment of Health, 2 University Place, Room 105, Albany, NY 12203. PCB concentrations of nursing Mohawk women at Akwesasne. Akwesasne is a Native American community of more than 10,000 persons located along the St. Law- rence River in New York, Ontario, and Quebec (figure 1). Less than 100 feet (30.7 m) to the west of Akwe- sasne is the General Motors/Central Foundry Division Superfund hazardous waste site. This facility used Aroclor 1248 (Monsanto Industrial Chemical Co., St. Louis, Missouri), a commercial mixture of various PCB congeners, as a hydraulic fluid in its die-casting machines from 1959 to 1974 (4). When these ma- chines leaked, the fluids were collected in the waste- water system and disposed of on the property. Con- centrations of PCBs range up to 40,000 ppm in on-site soils and sludges and up to 5,700 ppm offshore in St. Lawrence River sediment (5). Reynolds Metals, Inc. and the Aluminum Company of America operate aluminum-processing facilities in the area and have used Aroclor 1248 in their heat-transfer equipment. These facilities also have released PCBs into the St. Lawrence River and its tributaries (6). The PCBs have entered the local food chain, with some species of fish, reptiles, amphibians, birds, and mammals having lev- els that exceed the US Food and Drug Administra- tion's tolerance limits for human consumption of 2 ppm (wet weight) for fish and 3 ppm (lipid weight) for 164

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American Journal of EpidemiologyCopyright © 1998 by The Johns Hopkins University School of Hygiene and Public HealthAll rights reserved

Vol. 148, No. 2Printed in U.S.A.

Fish Consumption and Breast Milk PCB Concentrations amongMohawk Women at Akwesasne

Edward F. Fitzgerald,1 Syni-An Hwang,1 Brian Bush,2 Katsi Cook,3 and Priscilla Worswick3

A study was conducted to determine the relation between the consumption of contaminated local fish andconcentrations of total polychlorinated biphenyls (PCBs) and 68 PCB congeners in the milk of nursing Mohawkwomen residing near three hazardous waste sites. From 1986 to 1992, 97 Mohawk women were interviewedand donated at least 50 ml of breast milk. The comparison population consisted of 154 Caucasians. Afteradjustment for potential confounders, Mohawk mothers who gave birth in 1986-1989 had a geometric meanmilk total PCB concentration of 0.602 ppm (fat basis) compared with 0.375 ppm for the control group (p =0.009). These Mohawk women also had significantly higher geometric mean concentrations of nine congeners.Beginning in 1990, however, there were no significant differences between the Mohawk women and thecomparison group. Estimated cumulative lifetime exposure from local fish consumption was significantlyrelated to milk total PCB and to three congeners only among those Mohawks who gave birth from 1986 to1989. The reduction in breast milk PCB concentrations parallels a corresponding decrease in local fishconsumption and may be the result of the advisories that have been issued over the past decade recom-mending against the consumption of local fish by pregnant and nursing Mohawk women. Am J Epidemiol1998:148:164-72.

hazardous waste; Indians, North American; milk, human; organochlorine; polychorinated biphenyls

Polychlorinated biphenyls (PCBs) are very persis-tent, lipophilic compounds that bioaccumulate andbiomagnify in the food chain (1). Ingestion, includingthe consumption of contaminated sportfish (2), is con-sequently a major route of human exposure. NativeAmerican communities, particularly those around theGreat Lakes and the Pacific Northwest, are believed tobe at particularly high risk of such exposure, sincethey typically are more dependent on local fish andgame as a food source than are other populations.However, very few studies have directly assessed PCBbody burdens and fish consumption among NativeAmerican people, especially those who live on reser-vations and reside outside of Alaska (3). The purposeof this paper is to present data regarding the associa-tion between the consumption of local fish contami-nated with PCBs from hazardous waste and the milk

Received for publication July 17, 1997, and accepted for publi-cation December 30, 1997.

Abbreviation: PCBs, polychlorinated biphenyls.1 Bureau of Environmental and Occupational Epidemiology, New

York State Department of Health, Albany, NY.2 Laboratory of Organic Analytical Chemistry, Wadsworth Center,

New York State Department of Health, Albany, NY.3 Akwesasne Task Force on the Environment, Mohawk Nation at

Akwesasne.Reprint requests to Dr. Edward F. Fitzgerald, Bureau of Environ-

mental and Occupational Epidemiology, New York State Depart-ment of Health, 2 University Place, Room 105, Albany, NY 12203.

PCB concentrations of nursing Mohawk women atAkwesasne.

Akwesasne is a Native American community ofmore than 10,000 persons located along the St. Law-rence River in New York, Ontario, and Quebec (figure1). Less than 100 feet (30.7 m) to the west of Akwe-sasne is the General Motors/Central Foundry DivisionSuperfund hazardous waste site. This facility usedAroclor 1248 (Monsanto Industrial Chemical Co., St.Louis, Missouri), a commercial mixture of variousPCB congeners, as a hydraulic fluid in its die-castingmachines from 1959 to 1974 (4). When these ma-chines leaked, the fluids were collected in the waste-water system and disposed of on the property. Con-centrations of PCBs range up to 40,000 ppm in on-sitesoils and sludges and up to 5,700 ppm offshore in St.Lawrence River sediment (5). Reynolds Metals, Inc.and the Aluminum Company of America operatealuminum-processing facilities in the area and haveused Aroclor 1248 in their heat-transfer equipment.These facilities also have released PCBs into the St.Lawrence River and its tributaries (6). The PCBs haveentered the local food chain, with some species of fish,reptiles, amphibians, birds, and mammals having lev-els that exceed the US Food and Drug Administra-tion's tolerance limits for human consumption of 2ppm (wet weight) for fish and 3 ppm (lipid weight) for

164

Fish Consumption and Breast Milk PCB Concentrations 165

Key:» • - Akwesasne Boundary

Intemational/ProvincalBoundary

| J Industrial Plant

9 4 Fish Sampling Station

Scale:

« i i

Kilometers

0 I

Miles

2

J

N

s

C*

Cornwall City, Ontario

Figure 1. Map of the Mohawk Nation at Akwesane.

poultry (7, 8). An interim clay cap and liner wasplaced on the General Motors/Central Foundry Divi-sion landfill in 1988, but removal of contaminatedsoils and sediments has only recently started at allthree facilities.

The pollution is a major concern of the Mohawkpeople, since their tradition and culture emphasize theinterdependence of man and the environment and be-cause many residents formerly depended on local fish,waterfowl, and mammals for food. An earlier articleby Fitzgerald et al. (9) described fish PCB concentra-tions, consumption rates, species preference, fish prep-aration methods, and sociodemographic factors asso-ciated with fish consumption among 97 nursingMohawk women from 1986 through 1992 and a ruralcomparison group of nursing Caucasians. That reportnoted a significantly greater average rate of local fishconsumption among the Mohawks relative to the con-trols before pregnancy (respective annual means of

23.5 and 14.1 local fish meals for the period more than1 year before pregnancy). However, 60 percent of allMohawk women who had previously eaten local fishceased consumption once they were pregnant com-pared with only 38 percent of the comparison women.These changes may be related to the advisories thathave been issued over the past decade by Mohawk,state, and provincial authorities against the consump-tion of fish from that area of the St. Lawrence River bypregnant and nursing women, infants, and children.

The objective of this paper is to relate local fishconsumption to breast milk concentrations of totalPCB and 68 PCB congeners in the Mohawk and com-parison women. Breast milk was chosen as the sam-pling fluid since monitoring the levels of chemicalcontaminants in human milk is a useful indicator ofmaternal exposure and because it is a major source ofexposure to environmental pollutants among breast-fed infants (10). The project is a collaborative effort

Am J Epidemiol Vol. 148, No. 2, 1998

166 Fitzgerald et al.

among the New York State Department of Health, theSt. Regis Mohawk Tribe, the Mohawk Council ofAkwesasne, the Akwesasne Task Force on the Envi-ronment, and the State University of New York atAlbany.

MATERIALS AND METHODS

Interview

Detailed descriptions of ascertainment, interview,and dietary assessment are published elsewhere (9).Briefly, all nursing Mohawk women who lived atAkwesasne and who gave birth between March 1,1988, and March 31, 1992, were eligible for inclusion.A total of 93 (78.2 percent) participated. As part of apilot project, four other Mohawk mothers were inter-viewed from 1986 to 1987. They were added to thestudy to increase the number of participants who gavebirth prior to 1990, resulting in total sample size of 97Mohawk participants. The dietary assessment con-sisted of the participant's report of her consumption ofvarious foodstuffs, emphasizing local species of fishand game. The specific method combined a food fre-quency with a limited dietary history to estimate usualintake (11). It focused upon consumption at threepoints in time: 1) during the index pregnancy; 2) in theyear before the pregnancy; and 3) more than 1 yearbefore the pregnancy.

Comparative data were obtained from nursing moth-ers who lived in Warren or Schoharie County and gavebirth during the same period. Like Akwesasne, thesecounties are primarily rural in character. However, areview of records maintained by the New York StateDepartment of Health indicated that both countieswere relatively free of PCB contamination, and ac-cording to studies performed by the New York StateDepartment of Environmental Conservation, fish inboth regions show only background contamination(12). The mothers were recruited through the localWomen and Infant Care clinics and were not selectedon the basis of their fish consumption habits. A total of154 women (52.4 percent) participated. All were Cau-casian. Detailed comparisons with the Mohawk moth-ers regarding other sociodemographic factors, physicalcharacteristics, reproductive histories, and lifestylevariables are published elsewhere (9).

Breast milk analysis

After the interview was completed, project person-nel instructed the mothers in the use of a breast pump/infant nurser. Mothers were asked to provide at least50 ml of breast milk 1 month postpartum. The chem-ical analysis was performed by one of the coauthors(B. B.), using methods (including quality assurance

and control, accuracy, and precision) published else-where (13). Briefly, the milk samples were extractedby using ethanol and hexane and then transferred to aFlorisil clean-up column (US Silica Co., BerkeleySprings, West Virginia) containing 10 g 4 percentdeactivated Florisil topped with 1 cm anhydrous so-dium sulfate. The eluate was analyzed with a Hewlett-Packard 5890 gas chromatograph (Hewlett-ParkardCo., Avondale, Pennsylvania) using a phenylmethyl-octadecyl, silyl-bonded, fused-silica capillary columnand an electron-capture detector. A computerizeddata management system reported each of 68 PCB-containing zones or peaks and summed the congenerconcentrations to report total PCB. In some cases, thecapillary column was unable to resolve two congeners,so the result was reported as their sum.

The method detection limit for total PCB was 4.5ppb (whole milk) or 180 ppb (fat basis, assuming a fatcontent of 2.5 percent and a volume of 50 ml). Themedian method detection limit for the 68 individualPCB congeners was 0.2 ppb (whole milk) or 8 ppb (fatbasis). However, the instrument is capable of detectingsignals in milk extracts as low as 0.001 ppb (wholemilk) for each PCB congener. Concentrations betweenthis instrument detection limit of 0.001 ppb andmethod detection limits were reported by the labora-tory and included as such in the statistical analysisbecause many chemists and statisticians believe that areported result, even if it is below the "criterion fordetection," remains the best available estimate of thetrue value and is preferable to assigning a zero or anarbitrary constant such as one-half the method detec-tion limit (14). However, to prevent misconceptionsregarding the level of certainty attached to the results,aggregate data are presented only if the geometricmean for all study participants equaled or exceeded themethod detection limit for a given congener.

Dietary exposure assessment

The exposure of each Mohawk woman to total PCBthrough the consumption of local fish was estimatedby multiplying the total number of local fish meals thatshe reported eating during each time period (during, 1year before, and > 1 year before the index pregnancy)for a particular species by the PCB concentration ofthat species and the duration of consumption. If amother recalled from which of seven specific locationsthe fish was obtained, the data for that location wereused. Otherwise, PCB concentrations for that specieswere averaged across all seven locations. The resultwas summed over all species, multiplied by an averageof 200 g of fish per meal (the weight of a typicalportion), and expressed as milligrams. The values foreach time period were then combined to estimate each

Am J Epidemiol Vol. 148, No. 2, 1998

Fish Consumption and Breast Milk PCB Concentrations 167

woman's cumulative lifetime exposure. However, be-cause maternal recall of diet is likely to be impreciseand because the mean PCB level of a composite sam-ple may not be typical of the individual fish that awoman consumed, cumulative lifetime exposure wascategorized into three ordinal levels for most statisticalanalyses: "none" for those Mohawks who reportednever eating local fish, and "low" or "high" for allothers, dividing along the median value.

In addition to total PCB, cumulative lifetime dietaryexposures were estimated for the three leading conge-ners found in fish taken near General Motors/CentralFoundry Division: 1) 2,4,4'-trichlorobiphenyl (IUPACno. 28); 2) 2,5,2',5'-tetrachlorobiphenyl (IUPAC no.52); and 3) 2,4,3',4'-tetrachlorobiphenyl (IUPAC no.66). However, the exposure estimates for each of thesethree individual congeners were highly correlated withthe estimates for total PCB (r = 0.99). The estimatefor total PCB therefore was used as a proxy for awoman's dietary exposure to individual congeners.

Statistical analysis

Multiple linear regression was used to test for theeffect of fish consumption after evaluating the effectof 11 background variables, including maternal age,education, previous breastfeeding, body mass index,and occupation, that could potentially confound anyassociation between exposure and breast milk PCBlevel (15). Models were first constructed for total PCBby using backward elimination to delete nonsignificant{p > 0.10) background variables one at a time. Thencumulative lifetime exposure from local fish consump-tion was added to estimate its effect after adjustmentfor all remaining background variables. The GeneralLinear Model procedure of Statistical Analysis System(16) was used to calculate least-square means forevery category of fish consumption after centeringeach covariate around its grand mean.

To determine whether there were changes in breastmilk PCB concentrations during the course of thestudy period, the year of the index child's birth was

also entered as a variable in the regression models. Tomaximize cell frequencies, it was categorized a prioriinto three levels: 1986-1989, 1990, and 1991-1992.Interactions between time period and risk factors, suchas cumulative lifetime exposure from local fish con-sumption, were also assessed by testing their cross-products.

The milk PCB concentrations were first fat adjustedby dividing the whole-milk level by the percent fat fora given sample. The result was micrograms of chem-ical per gram of milk fat (ppm). This adjustment wasnecessary because the concentration of these lipophiliccompounds in whole milk is very dependent on the fatcontent of the milk (17). These fat-adjusted valueswere then transformed by using natural logarithmsbecause their distributions were log-normal in shape.The results are presented as geometric means by tak-ing the anti-log of the means of the log-transformedvalues after adjustment for potential confounders.

RESULTS

Breast milk total PCB

The breast milk total PCB data for the Mohawk andcomparison women were similar when averagedacross the entire study period. For example, the geo-metric mean concentration on a fat basis for the 97Mohawk participants was 0.336 ppm (standard er-ror = 0.026 ppm), while the geometric mean for the154 controls was 0.372 ppm (standard error = 0.022ppm). Approximately 19.6 percent of the Mohawkshad a value of less than the method detection limit of0.180 ppm; a milk level of less than the methoddetection limit was observed among 14.9 percent ofthe controls. The maximum levels were 2.39 ppm(Mohawks) and 2.34 ppm (controls).

Differences between the Mohawks and the controlswere evident, however, when milk total PCB concen-trations were evaluated by year of the index child'sbirth. The results are displayed in table 1, after adjust-ment for previous breastfeeding, maternal age, alcohol

TABLE 1. Adjustedf geometric mean breast milk total PCB$ concentration (ppm, fat basis) by Mohawkor control and time period, Mohawk Nation at Akwesasne, 1986-1992

Mohawkor

control

MohawksControls

No.

1952

1986-1989

X

0.602*0.375

No.

3857

Time period

1990

X

0.3520.404

No.

4045

1991-1992

X

0.2540.318

• p < 0.01 for Mohawk versus control in 1986-1989, F, -,, = 0.18, p = 0.674 for Mohawk or control; F4J41 =9.75, p< 0.001 for time period; F^-, = 4.94, p = 0.008 for'M or Cx time period.

t Adjusted for maternal age, antibiotic use before pregnancy, previous breastfeeding, and alcohol consumptionbefore pregnancy.

i PCB, polychlorinated biphenyl.

Am J Epidemiol Vol. 148, No. 2, 1998

168 Fitzgerald et al.

consumption before pregnancy, and antibiotic use be-fore pregnancy. The latter variables were the onlybackground factors found to be significantly related tomilk total PCB in the multiple regression analyses.The coefficients were -0.0031 (p < 0.001) for pre-vious breastfeeding (weeks), 0.0370 (p < 0.001) formaternal age (years), 0.0202 (p = 0.050) for alcoholconsumption before pregnancy (drink-years), and0.5935 (p < 0.001) for antibiotic use before preg-nancy (yes vs. no).

The adjusted geometric-mean breast milk total PCBconcentration of the Mohawk mothers who gave birthin 1986-1989 was 0.602 ppm, compared with 0.375for the controls who participated during the sameperiod (p = 0.009 for pairwise contrast). No signifi-cant difference was noted between mothers who par-ticipated later in the study. This time-dependent asso-ciation was represented statistically in the analysis ofvariance as a significant interaction between whetherthe mother was a Mohawk or a control and the timeperiod (p = 0.008). The Mohawks showed a signifi-cant and monotonic decline in their adjusted geometricmeans according to when they participated (p < 0.001for test of linear trend). In contrast, no significantdifference in adjusted geometric mean breast milkPCB level over time was evident for the controls.

As noted previously, cumulative lifetime PCB ex-posure from local fish consumption among the Mo-hawks was categorized as 1) none, 2) low, or 3) high,with the 80 women in the latter two groups dividedaccording to their median exposure of 8 mg. Table 2shows the adjusted geometric mean milk total PCBconcentrations for these three categories by the year ofthe index child's birth and with the inclusion of thecontrols.

The analysis of variance indicated that the interac-tion between cumulative lifetime dietary exposure and

the year when the woman gave birth was significant,i.e., the effect offish consumption varied according totime period. An examination of the cell means re-vealed that milk total PCB levels increased with cu-mulative lifetime PCB exposure from local fish con-sumption between 1986 and 1989 (p = 0.009 for testof linear trend including the controls). In comparison,among women who participated in 1990 or 1991—1992, no significant associations were observed. Re-garding pairwise contrasts, the adjusted geometricmean for the high exposure category was significantlygreater than that for the controls in 1986-1989 (p =0.011). No other pairwise contrast was statisticallysignificant. Similar results were observed when localfish consumption during or in the year before preg-nancy was examined (data not shown).

Breast milk congener-specific PCB

Of the 17 congeners with geometric means thatexceeded their method detection limits, nine were sig-nificantly greater among the Mohawk women whogave birth in 1986-1989 relative to control mothersafter adjustment for previous breastfeeding, maternalage, alcohol consumption before pregnancy, and anti-biotic use before pregnancy (table 3). The congenersfound to be elevated ranged in degree of chlorinationfrom tetra- to octachlorobiphenyls. Consistent with theresults for total PCB, the Mohawk women who gavebirth in 1990 or 1991-1992 had geometric mean milkconcentrations for most congeners that equaled orwere less than those of the controls (data not shown).

After adjustment for maternal age, antibiotic usebefore pregnancy, previous breastfeeding, and alcoholconsumption before pregnancy, six congeners showeda significant monotonic trend in 1986-1989, with cu-mulative lifetime exposure to total PCB from local fish

TABLE 2. Adjustedt geometric mean breast milk total PCBfc concentration (ppm, fat basis) byestimated lifetime exposure from local fish consumption among Mohawks and time period, withcontrols, Mohawk Nation at Akwesasne, 1986-1992

Time periodFish

consumption

ControlsMohawks

NoneLow exposureHigh exposure

No.

52

379

1986-1989

X

0.372*

0.3970.6030.691

No.

57

61220

1990

X

0.406

0.5020.2990.349

No.

45

82111

1991-1992

X

0.319

0.1740.2650.309

* p = 0.009 for test of linear trend in 1986-1989 with controls. F^^ss = 0.64, p = 0.590 for fish consumption;F4235 = 9.38, p < 0.001 for time period; F^ 2^ = 2.64, p = 0.017 for fish consumption x time period.

t Adjusted for previous breastfeeding, maternal age, antibiotic use before pregnancy, and alcohol consumptionbefore pregnancy.

t PCB, polychlorinated biphenyl.

Am J Epidemiol Vol. 148, No. 2, 1998

Fish Consumption and Breast Milk PCB Concentrations 169

TABLE 3. Adjustedf geometric mean breast milkconcentrations (ppb, fat basis) by PCB+. congener for Mohawkand control women, Mohawk Nation at Akwesasne, 1986-1989

Structure IUPAC+.no.

Mohawk Control(n=19) (n=52)

2,3,4,4' + 3,4,2',3'2,4,5,2',4'2,4,5,3',4'2,4,5,2',4',5'2,3,4,6,2',3',6' + 2,3,5,6,3',4'2,3,4,2',4',5'2,3,4,6,2',3',4' + 2,3,4,5,3',4'2,3,4,5,2',4',5'2,3,4,5,2',3',5',6'

60 +99

118153176 +138171 +180199

55

163

156

4.0***32.9***37.5***49.8**13.5*53.5**8.3*

18.4**4.3**

1.514.817.932.8

7.729.9

5.84.22.6

• p < 0.05; ** p < 0.01; *•• p < 0.001.t Adjusted for previous breastfeeding, maternal age, antibiotic

use before pregnancy, and alcohol consumption before pregnancy.+. PCB, polychlorinated biphenyl; IUPAC, International Union of

Pure and Applied Chemistry.

consumption. Three of these six had geometric meansthat equaled or exceeded their method detection limit(table 4).

DISCUSSION

Caution must be exercised when comparing re-ported PCB levels across studies, given differences inanalytic methods, time periods, and populations. Ingeneral, however, the milk total PCB concentrations ofboth the Mohawk and control mothers are within the0.5-1.5 ppm range for average levels in breast milkfrom other studies in the United States (18). Muchhigher concentrations have been observed among Inuitwomen of Hudson Bay, Quebec, Canada (19). Atmo-spheric transport of organochlorines and movement inocean currents have contaminated the Arctic foodchain, including the fish, seal, walrus, beluga, caribou,and narwhal that the Inuit people are heavily depen-dent upon as food sources (20).

Women who reported nursing their previous chil-dren had lower milk total PCB levels. Previous lacta-tions are likely to deplete the adipose stores, resulting

in lower levels in the milk fat (17). Breast milk totalPCB concentrations also increased with maternal ageand alcohol consumption prepregnancy, probably re-flecting the greater cumulative lifetime exposure ofolder women to PCBs and the adverse effect of alcoholon the liver's ability to metabolize PCBs. These find-ings are similar to the results of other studies (21). Inaddition, breast milk total PCB increased with antibi-otic use before the index pregnancy. An inspection ofthe responses of the 16 women who reported antibioticuse revealed that they were primarily short-term userswho took a broad range of antibiotics shortly beforepregnancy. One other study has reported such a rela-tion (22). Although such an association may reflectchance, it may also indicate that either antibiotics orthe underlying infections for which they were pre-scribed affect distribution, biotransformation, or ex-cretion.

When the data were examined according to the yearin which the index child was born, Mohawk motherswho delivered in 1986-1989 had a significantly ele-vated geometric mean milk total PCB concentrationrelative to the comparison women. This differencebetween study groups in 1986-1989 was directly as-sociated with estimated cumulative lifetime exposureto PCBs from the consumption of local fish. In fact,the adjusted mean for those Mohawk women whonever ate local fish was not significantly different fromthat for the control mothers.

Mohawk mothers who gave birth in 1986-1989 hadsignificantly higher geometric means for nine PCBcongeners relative to the controls. One was a coelutingpeak that is a major constituent of Aroclor 1248, i.e.,2,3,4,4'- and 3,4,2',3'-tetrachlorobiphenyl (IUPACno. 60 and no. 55). Two others, (IUPAC no. 99 and no.118), are also found in Aroclor 1248. The remainderare exclusively Aroclor 1254/1260 congeners (23).They probably do not reflect exposure to PCBs fromthe local industrial facilities, but are consistent withmore general Lake Ontario and St. Lawrence Riverexposures (24). IUPAC no. 99 and no. 118 were also

TABLE 4. Adjusted* geometric mean breast milk concentration (ppb, fat basis) for selected PCBfcongeners by estimated cumulative lifetime exposure to total PCB from local fish consumption amongMohawks, with controls, Mohawk Nation at Akwesasne, 1986-1989

Congener(IUPAC

no.)

99118146

Controls(n = 52)

14.817.94.8

Mohawks' fish consumption

None

24.531.4

1.0

Lowexposure

(n = 7)

29.737.2

5.8

Highexposure(1 = 9)

39.539.9

7.9

Ftest

0.0160.0540.008

p value

Trend

0.0090.0410.006

* Adjusted for previous breastfeeding, maternal age, antibiotic use before pregnancy, and alcoholconsumption before pregnancy,

t PCB, polychlorinated biphenyl.

Am J Epidemiol Vol. 148, No. 2, 1998

170 Fitzgerald et al.

significantly elevated among Mohawk fish eaters from1986 to 1989. Each congener accounted for 2 to 3percent of the total PCB residue in yellow perchcaught offshore from General Motors/Central FoundryDivision. The third congener associated with local fishconsumption, IUPAC no. 146, was not detected in anyappreciable level in fish caught near the General Mo-tors/Central Foundry Division. It is more typical ofAroclors 1254 and 1260 than of 1248 and may againreflect more general Lake Ontario and St. LawrenceRiver contamination. Other congeners prevalent inlocal fish, e.g., IUPAC nos. 28, 52, and 66, were alsoelevated among Mohawk participants relative to thecontrols but are not reported in tables 3 or 4 becausethe method detection limits for these congeners weregreater than the concentrations observed in half ormore of the milk samples.

The decline in milk PCB levels among the Mohawkmothers according to when they gave birth parallels asecular trend in local fish consumption, i.e., Mohawkwomen who participated after 1989 were less likely toeat local fish, especially during pregnancy, than weremothers who gave birth earlier (9). No such trend wasapparent among the controls. It is unlikely thatchanges in fish PCB levels contributed to the reductionin milk PCB concentrations, since, in contrast to thefish consumption rates, the levels of PCBs in the fishremained relatively constant over time.

The Mohawk mothers who participated in 1986—1989 were also less likely to remove the skin or trimthe fat from any fish they did eat before they cookedit (33 percent compared with 95 percent for motherswho gave birth in 1990 or later). These methods ofpreparation help reduce the contaminant levels ofmany species of fish before they are consumed (25).Such changes in fish consumption patterns are proba-bly in response to the local health advisories. As aresult, even those Mohawk women who ate local fishin recent years may have reduced their exposures tolevels that are insufficient to cause a detectable in-crease in body burden when compared with the gen-eral population. The finding that most of the controlsalso had detectable levels of PCBs in their breast milkprobably reflects the facts that PCBs are ubiquitouspollutants and that even commercially available meatsand other foodstuffs are contaminated (26).

The lack of an association between local fish con-sumption and breast milk PCB concentrations after1989 has implications for research that relies on fishconsumption as a surrogate measure of PCB internaldose or body burden (27, 28). The data suggest thatvalidation studies are necessary, especially when fishconsumption rates are relatively low or when the fish

are commonly prepared in ways that reduce their con-taminant burden.

It is unlikely that the declines in fish consumptionrates and breast milk PCB levels among the Mohawksby year of the index child's birth reflect a selectionbias, since the same procedures and staff were used torecruit participants throughout the study period andbecause the staff were unaware of the participant'sexposure status and PCB body burden at the time ofrecruitment. Some differences were observed in ageand education among the Mohawk participants overtime, but controlling for them did not alter the results.The Mohawk women were more likely than the com-parison mothers to participate in the study, perhapsbecause they were more aware of and concerned aboutfish contamination. These differences in awarenessand concern may result, in turn, in differences in recalland reporting between the Mohawk and comparisongroups. The findings that the fish consumption ratesand the breast milk PCB levels of the Mohawk moth-ers declined over time while both variables remainedconstant among the controls, however, help to validatethe dietary histories.

Declines in the PCB milk levels over time are con-sistent with the results of other cross-sectional studies.For example, the PCB levels detected in this study areapproximately 50 percent lower than those previouslyreported by Bush et al. (24) in their 1977 investigationof 40 women recruited as walk-in cases from mater-nity facilities in Albany, Rochester, and Oswego, NewYork. Similar declines in milk PCB concentrationsover the past 10-20 years have been reported in Can-ada (29), Sweden (30), and Norway (31). This de-crease in human body burden parallels declines inenvironmental compartments and may be attributed tothe ban on PCB production in most industrializedcountries and the imposition of stricter regulationsconcerning their use and disposal (32).

The health risks to the infant of pre- or postnatalexposure to PCBs at the level observed in this studyare controversial (33). For instance, some studies havereported a negative association between maternal ex-posure to PCBs and birth weight (34, 35), whereasothers have not (36, 37). No differences in mean birthweight were observed between the Mohawks and con-trols in our study, but our power to detect a differenceof 200 g (the magnitude of the effect cited by Fein etal. (34)) was only 0.133, given the small sample size.

Caution must be exercised regarding health impli-cations, and the possibility of subtle, long-term effectssuch as disruption of the endocrine system (38) cannotbe ruled out. However, since the period of exposure isrelatively short, nursing is estimated by the WorldHealth Organization to account for less than 5 percent

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Fish Consumption and Breast Milk PCB Concentrations 171

of the total lifetime intake of these chemicals (39). Asthe natural foodstuff for newborn and small infants,breast milk also has well-recognized immunologic,psychologic, nutritional, and economic benefits (40).The World Health Organization, the American Acad-emy of Pediatrics, and other responsible bodies haveconcluded that these benefits outweigh the risks fromchemical contaminants at the low levels found in thisand most other studies (41).

ACKNOWLEDGMENTS

Funding for this project was provided in part by theAgency for Toxic Substances and Disease Registry (grantH75/ATH290026) and the National Institute of Environ-mental Health Sciences (grant P42 ES04913).

The authors express their appreciation to the followingpersons for their past and present help: Ann Casey, SusanDzurica, Patricia Roundpoint, Kenneth Jock, Trudy Lauzon,F. Henry Lickers, Judith Quinn, and Bao-zhu Yang.

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