Decline in Fish Consumption Among Pregnant
Women After a National Mercury Advisory
Emily Oken, MD, Ken P. Kleinman, ScD, Wendy E. Berland, MPH, Steven R. Simon, MD, MPH,
Janet W. Rich-Edwards, ScD, and Matthew W. Gillman, MD, SM
OBJECTIVE: A well-publicized January 2001 federal advisory recommended that pregnant women limit consumption of certain fish because of concerns about mercury
contamination. We endeavored to estimate the extent to
which pregnant women changed fish consumption habits
after dissemination of this national advisory.
METHODS: We performed interrupted time series analysis
of data from a cohort of pregnant women (2235 who
completed at least one dietary questionnaire) visiting obstetric offices in a multispecialty group practice in eastern
Massachusetts, surveyed before the advisory from April
1999 through December 2000 and after the advisory from
April 2001 through February 2002. Main outcome measures were consumption of total fish and of four fish types:
canned tuna, dark meat fish, shellfish, and white meat fish.
Subjects reported fish consumption on semiquantitative
food frequency questionnaires administered at each trimester of pregnancy.
RESULTS: We observed diminished consumption of dark
meat fish, canned tuna, and white meat fish after the
national mercury advisory. These decreases resulted in a
reduction in total fish consumption of approximately 1.4
servings per month (95% confidence interval 0.7, 2.0) from
December 2000 to April 2001, with ongoing declines
through the end of the study period. There was no change
in shellfish intake.
CONCLUSION: After dissemination of federal recommendations, pregnant women in this cohort reported reduced consumption of fish, including tuna, dark meat fish, and white
meat fish. Because these fish may confer nutritional benefits
to mother and infant, public health implications of these
changes remain unclear. (Obstet Gynecol 2003;102:346 –51.
From the Department of Ambulatory Care and Prevention, Harvard Medical
School and Harvard Pilgrim Health Care; Division of Women’s Health, Brigham
and Women’s Hospital; and Departments of Maternal and Child Health and
Nutrition, Harvard School of Public Health, Boston, Massachusetts.
Supported by research grants from the National Institutes of Health (HD 34568,
HL 64925, HL 68041) and by Harvard Medical School and the Harvard
Pilgrim Health Care Foundation.
The authors thank Stephen Soumerai, ScD, who provided guidance in performing
time series analysis, experience regarding investigations of behavior change following
health advisories, and helpful comments on the manuscript.
346
© 2003 by The American College of Obstetricians and
Gynecologists.)
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
VOL. 102, NO. 2, AUGUST 2003
© 2003 by The American College of Obstetricians and Gynecologists. Published by Elsevier.
0029-7844/03/$30.00
doi:10.1016/S0029-7844(03)00484-8
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 firsttrimester 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
VOL. 102, NO. 2, AUGUST 2003
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, bluefish, 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 ␹2 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.
RESULTS
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.
Oken et al
Decline in Fish Consumption
347
Table 1. Subject Characteristics Before and After the January 2001 Mercury Advisory, Reported by Pregnant Women
Enrolled in Project Viva From April 1999 Through February 2002
Subject characteristics
Age at enrollment (y) [mean (SD)]
Race/ethnicity (%)
White
Black
Hispanic
Asian
More than one race
Education (%)
High school
Some college
College graduate
Graduate school
Before advisory,
April 1999–December 2000
(n ⫽ 1161)
After advisory,
April 2001–February 2002
(n ⫽ 904)
P
31.8 (5.2)
32.1 (5.2)
.20
66
16
6
7
4
67
15
8
5
3
.46
.48
.01
.25
.32
10
23
35
28
9
22
36
30
.24
.55
.72
.11
SD ⫽ standard deviation.
This table excludes the 170 subjects who completed dietary questionnaires both before and after advisories. Percentages may not add up to 100%
because of missing data.
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.
DISCUSSION
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 in-
Table 2. Mean Fish Consumption Before and After the January 2001 Mercury Advisory, Reported on 4645 Dietary
Questionnaires Completed by 2235 Pregnant Women Enrolled in Project Viva
Type of fish [mean (SD) servings per mo]
Canned tuna
Dark meat fish
Shellfish
White meat fish
4 types combined
⬎3 fish meals per mo (%)
Before advisory
(n ⫽ 2744),
April 1999–December 2000
After advisory
(n ⫽ 1902),
April 2001–February 2002
P
2.9 (3.8)
1.3 (2.4)
1.7 (2.5)
1.7 (2.5)
7.7 (7.0)
15
2.1 (3.2)
1.1 (2.1)
1.7 (2.4)
1.5 (2.0)
6.4 (5.7)
11
⬍.001
.06
.23
⬍.001
⬍.001
⬍.001
SD ⫽ standard deviation.
Fish consumption was assessed by semiquantitative food frequency questionnaires administered after each trimester of pregnancy.
348
Oken et al
Decline in Fish Consumption
OBSTETRICS & GYNECOLOGY
Table 3. Estimated Change Over Time (Slope) in Fish Consumption Before the January 2001 Mercury Advisory, Change in
Slope (Preadvisory Subtracted From Postadvisory), and Change in Mean Servings per Month Consumed (End of
the Preadvisory Period Subtracted From the Beginning of the Postadvisory Period)
Type of fish
Slope preadvisory
[% change per
month (95% CI)]
Change in slope
[% change
(95% CI)]
Change in consumption
[servings per month
(95% CI)]
Canned tuna
Dark meat fish
Shellfish
White meat fish
4 types combined
⫺0.4 (⫺1.5, 0.6)
3.6 (2.1, 5.0)
1.0 (⫺0.2, 2.2)
1.0 (⫺0.2, 2.2)
0.8 (0.1, 1.6)
ⴚ2.1 (ⴚ3.6, ⴚ0.6)
ⴚ5.5 (ⴚ8.0, ⴚ2.9)
0.8 (⫺3.1, 1.6)
⫺1.9 (⫺4.3, 0.6)
ⴚ2.1 (ⴚ3.6, ⴚ0.6)
ⴚ0.6 (ⴚ0.9, ⴚ0.2)
ⴚ0.3 (ⴚ0.5, ⴚ0.1)
⫺0.2 (⫺0.4, 0.004)
ⴚ0.3 (ⴚ0.5, ⴚ0.04)
ⴚ1.4 (ⴚ2.0, ⴚ0.7)
CI ⫽ confidence interval.
Results from Poisson regression analysis of 4645 questionnaires from 2235 women enrolled in Project Viva, adjusting for repeated observations
within individuals and controlling for clustering by recruitment site. Bold type indicates that CIs do not include zero.
cluded 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 overreported 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 preand postadvisory periods began in April and ended in
the winter.
Many health advisories do not change behavior. Previous studies have demonstrated that changes in healthrelated 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. Fur-
Figure 1. Mean consumption of
canned tuna, dark meat fish, and
total fish reported by 2235
Project Viva participants surveyed
before and after the January 2001
mercury advisory. The shaded region indicates a 3-month wash-in
period. Lines represent estimates
for each category of fish from interrupted time series analysis using Poisson regression, controlling
for recruitment site and adjusting
for repeated observations within
individuals.
Oken. Decline in Fish Consumption. Obstet
Gynecol 2003.
VOL. 102, NO. 2, AUGUST 2003
Oken et al
Decline in Fish Consumption
349
ther 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.
REFERENCES
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
350
Oken et al
Decline in Fish Consumption
6.
7.
8.
9.
the risks of mercury in fish. Washington: FDA, 2001.
Available at: http://www.cfsan.fda.gov/⬃lrd/tphgfish.html.
Accessed 2002 Aug 1.
Associated Press. F.D.A. warns women not to eat some
fish. New York Times 2001 Jan 14:20.
Braile R. Warning sounded on safety of seafood. Boston
Globe 2001 Mar 11:1.
Reuters. Pregnant women warned not to eat shark, swordfish, mackerel. Washington Post 2001 Jan 12:A12.
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.
OBSTETRICS & GYNECOLOGY
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.
VOL. 102, NO. 2, AUGUST 2003
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.
Address reprint requests to: Emily Oken, MD, Department of Ambulatory Care and Prevention, 133 Brookline
Avenue, 6th Floor, Boston, MA 02215; E-mail: emily_oken@
harvardpilgrim.org.
Received January 3, 2003. Received in revised form March 11, 2003.
Accepted March 20, 2003.
Oken et al
Decline in Fish Consumption
351