Oh mercy mercy me
Oh things ain't what they used to be.
Oil wasted on the oceans and upon our seas
Fish full of mercury.
Marvin Gaye, “Mercy Mercy Me (the Ecology),” 1971
Recent studies have suggested that prenatal exposure to mercury among populations with high fish consumption may cause offspring developmental delays.1,2 In response, the US Congress mandated that the National Academy of Sciences review data regarding the toxicologic effects of mercury.3 Subsequently, in January 2001 the US Food and Drug Administration issued an advisory counseling pregnant women to avoid consuming specified long-lived predatory fish, which may contain high levels of organic mercury, and to limit ingestion of all other fish.4,5
Many women likely learned of these guidelines from the popular press6–8 or from their obstetricians.9 However, limited data are available on fish consumption practices among pregnant women in the United States10 and regarding whether women have changed their habits in response to the advisory. This is an important issue because consumption of the polyunsaturated fatty acids in fish oils may confer benefits to the fetus such as reduced risk of preterm delivery and enhanced infant cognition11–14 as well as improve cardiovascular health among nonpregnant adults.15 It is possible that these benefits could outweigh the harm from mercury exposure. Here we describe fish consumption reported by women enrolled in a pregnancy cohort during a 2.5-year period spanning publication of the mercury advisory.
MATERIALS AND METHODS
We used an interrupted time series design16,17 to estimate the impact of the advisory on total fish intake as well as consumption of dark meat fish, canned tuna, shellfish, and white meat fish individually. We divided the study time into three periods. The preadvisory period ran from April 1999 through December 2000. The advisory was published in January 2001. We allowed a 3-month “wash-in” period, January–March 2001, because dietary questionnaires asked about consumption up to 3 months before the survey date. The postadvisory period ran from April 2001 through February 2002.
Study subjects were participants in Project Viva, a prospective cohort study of gestational diet, pregnancy outcomes, and offspring health. We recruited women attending their initial prenatal visit at eight urban and suburban obstetric offices of a multispecialty group practice in eastern Massachusetts. Eligibility criteria included fluency in English, gestational age less than 22 weeks at the initial prenatal clinical appointment, and singleton pregnancy. We enrolled 2609 women (63% of those eligible) between April 23, 1999, and March 1, 2002, of whom subsequently 145 women became ineligible because of multiple gestation (n = 6), transfer of obstetric care to a nonstudy site (n = 49), or they were no longer pregnant (n = 80). This analysis is limited to 2235 of the 2464 remaining subjects (91%) who completed at least one of the three dietary questionnaires during the pre- or postadvisory periods.
After obtaining informed consent, we collected demographic and health history information by interview and self-administered questionnaire. We used a combination of incentives, mail and phone follow-up, and outreach within the clinical offices to promote questionnaire completion. Institutional review boards of participating institutions approved the study. All procedures were in accordance with the ethical standards for human experimentation established by the Declaration of Helsinki.18
Participants completed semiquantitative food frequency questionnaires after each trimester of pregnancy. The semiquantitative food frequency questionnaire was modified for use in pregnancy from an extensively validated instrument.19 We previously calibrated the first-trimester questionnaire against maternal blood nutrient levels.20 For every gram of intake per day, red blood cell concentrations of long-chain omega-3 fatty acids were higher by 1.72% among 72 black women (P = .09) and by 4.79% among 132 white women (P < .001). In the study population, seafood comprised 85–90% of the dietary source for these omega-3 fatty acids.
The first-trimester semiquantitative food frequency questionnaire, administered at study enrollment, asked about average consumption “during this pregnancy” (ie, since the last menstrual period), and the second semiquantitative food frequency questionnaire, administered at 26–28 weeks' gestation, asked about consumption “during the past 3 months.” A limited third-trimester semiquantitative food frequency questionnaire focused on fish intake in the month before delivery. Questions regarding fish queried intake of “canned tuna fish (3–4 oz.),” “shrimp, lobster, scallops, clams (1 serving),” “dark meat fish, e.g. mackerel, salmon, sardines, blue-fish, swordfish (3–5 oz.),” and “other fish, e.g. cod, haddock, halibut (3–5 oz.).” Response options ranged from “never/less than 1 per month” to “1 or more servings per day.” We generated a count of monthly servings as the average within each category; for example, we coded “1–3 servings per month” as two servings per month.
Because trimester-specific analyses yielded similar results, we combined data from all three trimesters. Within each period, we determined subject characteristics (excluding the 170 subjects who completed questionnaires in both periods). We compared means using t tests and proportions using χ2 tests. In addition, we calculated mean consumption of total fish and of each of the four fish types and determined the percentage of women who consumed more than 13 total fish servings per month (more than three servings per week). We compared consumption in the pre- and postadvisory periods using Poisson regression,21 with period as the predictor. We assumed that all missing data were missing at random.22
Next, we evaluated the effect of the advisory using an interrupted time series analysis. We performed Poisson regression with servings of fish per month as the dependent variable and period, month, and enrollment site as predictors. We accounted for repeated observations within individuals using generalized estimating equations.23 We assessed change over time (slope) in mean fish consumption within the preadvisory period and in the post- versus preadvisory period. We also determined change in level at the beginning of the postadvisory period compared with the end of the preadvisory period. Inclusion of subject race/ethnicity, age, and education did not change estimates, so we did not include these characteristics in the final models.
Table 1 presents characteristics of the 2235 participants who completed dietary questionnaires before and after the fish consumption advisory. There were 1300 subjects who completed all three dietary surveys, 365 who completed two, and 570 who completed one only. Subjects returned a total of 5200 semiquantitative food frequency questionnaires—approximately 88% completion for the first-trimester questionnaire, 72% for the second, and 90% for the third—of which 555 were completed during the wash-in period and 4645 were completed during the pre- or postadvisory periods and thus included in this analysis.
Average fish consumption was lower in women surveyed after the mercury advisory than in those surveyed before the advisory (Table 2). The proportion of subjects consuming fish in excess of the recommendation declined in parallel with the decrease in mean fish consumption. Fewer subjects surveyed in the postadvisory period consumed more than three total fish servings per week, compared with women surveyed before the advisory (15% versus 11%, Table 2).
Time series analysis revealed that intake of total fish and intake of canned tuna, dark meat fish, and white meat fish decreased after the mercury advisory (Table 3). In the postadvisory period, consumption of total fish, canned tuna, and dark meat fish continued to show significant declines over time, with a nonsignificant decrease in white meat fish. Shellfish consumption did not change.
Figure 1 displays mean servings of total fish, canned tuna, and dark meat fish consumed per month by the study population before and after the mercury advisory. Postadvisory declines in canned tuna, dark meat fish, and total fish are evident. For clarity of presentation we did not include white meat fish, which also declined, or shellfish, which did not decline.
The January 2001 federal advisory recommended that pregnant women avoid consuming predatory fish likely to contain high levels of mercury, including dark meat fish such as mackerel and swordfish.5 It also advised limiting consumption of shellfish, canned tuna, and smaller ocean fish to two to three servings per week.5
Pregnant women in this cohort consumed diminishing amounts of total fish after media attention to the adverse health effects of mercury exposure. Intake of canned tuna, dark meat fish, and white meat fish each lessened, whereas there was no observed change in shellfish consumption. The decline in total fish consumption included a decrease in the proportion of women who consumed more than three fish servings per week.
It is unlikely that our findings resulted from trends in enrollment characteristics, as subjects were drawn from the same obstetric practices over the 2.5 years of study. Additionally, adjustment for age, race or ethnicity, and education did not materially change results. All subjects resided in eastern Massachusetts; women living elsewhere may not have responded similarly. As with all studies based on questionnaires, it is possible that subjects reported eating more or less fish than they actually consumed. If subjects surveyed before the advisory over-reported intake or those surveyed after the advisory underreported intake, the true behavior change would be less than we observed. Although seasonal changes in fish consumption may occur, it is unlikely that seasonal variation accounted for the observed trends, as both pre-and postadvisory periods began in April and ended in the winter.
Many health advisories do not change behavior. Previous studies have demonstrated that changes in health-related behaviors do occur when advisories contain a simple message regarding a potentially serious condition and are well publicized through media coverage that reaches both health care providers and the general public.24 The 2001 US Food and Drug Administration consumer advisory regarding the risk of mercury exposure from dietary fish intake meets many of these criteria. Numerous media sources reported on mercury contamination of fish after the advisory was published.6–8 Additional well-publicized calls for more stringent restrictions on fish intake by state and nongovernmental agencies25–28 may also have influenced study subjects. Women may be particularly responsive to behavior change messages during pregnancy.
The results of this time series analysis suggest that pregnant women in this cohort acted in accordance with the federal guidelines to reduce fish consumption. Further research specifically asking pregnant women about their awareness of and responses to this advisory would be needed to confirm that the decrease in consumption resulted from the warnings, as opposed to other factors. Recently, however, nutritional considerations have led to recommendations for increased seafood consumption. The American Heart Association has suggested that adults should consume fish at least twice weekly to promote cardiovascular health.29 Nutrition experts have advised that pregnant women consume elongated fatty acids equivalent to approximately three to four oil-rich fish meals per week.30 The extent to which these more recent, apparently conflicting messages will affect future fish consumption among pregnant women is not known.
In conclusion, these results suggest that a broadly disseminated health advisory may substantially change dietary behavior among pregnant women. However, further research is needed into the relative risks and benefits of fish intake during pregnancy. The same fish that concentrate mercury contain long-chain polyunsaturated fatty acids that may benefit both the pregnant woman and her infant.11,13,15,31 It is not yet clear whether the risks of mercury outweigh the health benefits of a seafood diet for adults32,33 or children.1,2,34 Longitudinal studies that include gestational diet, mercury biomarkers, and child follow-up will help determine the balance of the dangerous toxins and beneficial nutrients in fish. The ultimate goal is to reduce environmental mercury pollution, allowing everyone to derive the health benefits of a marine diet free from contaminants.
1. Grandjean P, Weihe P, White RF, Debes F, Araki S, Yokoyama K, et al. Cognitive deficit in 7-year-old children with prenatal exposure to methylmercury. Neurotoxicol Teratol 1997;19:417–28.
2. Davidson PW, Myers GJ, Cox C, Axtell C, Shamlaye C, Sloane-Reeves J, et al. Effects of prenatal and postnatal methylmercury exposure from fish consumption on neurodevelopment: Outcomes at 66 months of age in the Seychelles Child Development Study. JAMA 1998;280:701–7.
3. National Research Council. Toxicological effects of methylmercury. Washington: National Academy Press, 2000.
4. Environmental Protection Agency. National advice on mercury in fish caught by family and friends: For women who are pregnant or may become pregnant, nursing mothers, and young children. Washington: Environmental Protection Agency, 2001. Available at: http://www.epa.gov/ost/fishadvice/factsheet.html
. Accessed 2002 Aug 1.
5. Food and Drug Administration. Consumer advisory: An important message for pregnant women and women of childbearing age who may become pregnant about the risks of mercury in fish. Washington: FDA, 2001. Available at: http://www.cfsan.fda.gov/∼lrd/tphgfish.html
. Accessed 2002 Aug 1.
6. Associated Press. F.D.A. warns women not to eat some fish. New York Times 2001 Jan 14:20.
7. Braile R. Warning sounded on safety of seafood. Boston Globe 2001 Mar 11:1.
8. Reuters. Pregnant women warned not to eat shark, swordfish, mackerel. Washington Post 2001 Jan 12:A12.
9. Do your pregnant patients know about the dangers of eating fish? ACOG Today 2001;45(9):5.
10. Stern AH, Gochfeld M, Weisel C, Burger J. Mercury and methylmercury exposure in the New Jersey pregnant population. Arch Environ Health 2001;56:4–10.
11. Olsen SF, Secher NJ. Low consumption of seafood in early pregnancy as a risk factor for preterm delivery: Prospective cohort study. BMJ 2002;324(7335):447.
12. Olsen SF, Grandjean P, Weihe P, Videro T. Frequency of seafood intake in pregnancy as a determinant of birth weight: Evidence for a dose dependent relationship. J Epidemiol Community Health 1993;47:436–40.
13. Lauritzen L, Hansen HS, Jorgensen MH, Michaelsen KF. The essentiality of long chain n-3 fatty acids in relation to development and function of the brain and retina. Prog Lipid Res 2001;40:1–94.
14. Neuringer M, Reisbick S, Janowsky J. The role of n-3 fatty acids in visual and cognitive development: Current evidence and methods of assessment. J Pediatr 1994;125(5 Pt 2):S39–47.
15. Hu FB, Bronner L, Willett WC, Stampfer MJ, Rexrode KM, Albert CM, et al. Fish and omega-3 fatty acid intake and risk of coronary heart disease in women. JAMA 2002;287:1815–21.
16. Soumerai SB, Avorn J, Gortmaker S, Hawley S. Effect of government and commercial warnings on reducing prescription misuse: The case of propoxyphene. Am J Public Health 1987;77:1518–23.
17. Cook T, Campbell D. Quasi-experimentation: Design and analysis issues for field settings. Boston: Houghton Mifflin, 1979.
18. World Medical Association. World Medical Association Declaration of Helsinki. Recommendations guiding physicians in biomedical research involving human subjects. JAMA 1997;277:925–6.
19. Willett WC, Sampson L, Stampfer MJ, Rosner B, Bain C, Witschi J, et al. Reproducibility and validity of a semiquantitative food frequency questionnaire. Am J Epidemiol 1985;122:51–65.
20. Rifas-Shiman SL, Fawzi W, Rich-Edwards JW, Willett WC, Gillman MW. Validity of a semi-quantitative food frequency questionnaire (SFFQ) during early pregnancy. Paediatr Perinat Epidemiol 2000;14(4):A25–6.
21. Dobson AJ. An introduction to generalized linear models. 2nd ed. New York: Chapman & Hall/CRC, 2002.
22. Little RJA, Rubin DB. Statistical analysis with missing data. 2nd ed. Hoboken, New Jersey: John Wiley & Sons, 2002.
23. Zeger SL, Liang KY. Longitudinal data analysis for discrete and continuous outcomes. Biometrics 1986;42:121–30.
24. Soumerai SB, Ross-Degnan D, Kahn JS. Effects of professional and media warnings about the association between aspirin use in children and Reye's syndrome. Milbank Q 1992;70:155–82.
25. Environmental Working Group. Brain food: What women should know about mercury contamination of fish. Washington: Environmental Working Group, 2001. Available at: http://www.ewg.org/reports/BrainFood/foreword.html
. Accessed 2002 Aug 1.
26. Blood and hair mercury levels in young children and women of childbearing age—United States 1999. MMWR Morb Mortal Wkly Rep 2001;50(8):140–3.
27. MDPH issues new consumer advisories on fish consumption and mercury contamination. Boston: Massachusetts Department of Public Health, 2001. Available at: http://www.state.ma.us/dph/media/pr0724.htm
. Accessed 2002 Aug 1.
28. Daniel M. Mercury levels in fish bring warning. Boston Globe 2001 Jul 25:A1.
29. Kris-Etherton PM, Harris WS, Appel LJ. Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation 2002;106:2747–57.
30. Simopoulos AP, Leaf A, Salem N. Workship on the essentiality of and recommended dietary intakes for omega-6 and omega-3 fatty acids. Tiverton, United Kingdom: International Society for the Study of Fatty Acids and Lipids, 1999. Available at: http://www.issfal.org.uk/adequateintakes.htm
. Accessed 2002 Aug 1.
31. SanGiovanni JP, Parra-Cabrera S, Colditz GA, Berkey CS, Dwyer JT. Meta-analysis of dietary essential fatty acids and long-chain polyunsaturated fatty acids as they relate to visual resolution acuity in healthy preterm infants. Pediatrics 2000;105:1292–8.
32. Guallar E, Sanz-Gallardo MI, van't Veer P, Bode P, Aro A, Gomez-Aracena J, et al. Mercury, fish oils, and the risk of myocardial infarction. N Engl J Med 2002;347:1747–54.
33. Yoshizawa K, Rimm EB, Morris JS, Spate VL, Hsieh CC, Spiegelman D, et al. Mercury and the risk of coronary heart disease in men. N Engl J Med 2002;347:1755–60.
34. Goldman LR, Shannon MW. Mercury in the environment: Implications for pediatricians. Pediatrics 2001;108:197–205.