A review of guidance on fish consumption in pregnancy: Is it fit for purpose?

Abstract

Introduction

When women become pregnant, they are likely to receive a great deal of information on foods to avoid or limit. Inevitably, this advice will vary from country to country, but several countries provide detailed information specifically on types of fish to limit and those to avoid completely. This advice relates mainly to the mercury content of fish with the aim of reducing the exposure of the pregnant woman and avoiding adverse effects on the neurodevelopment of the fetus.

Mercury is a widespread environmental toxin. It is present in the environment through natural processes such as volcanic activity and the weathering of rocks, but also through anthropogenic activities such as mining, smelting, power generation and manufacturing.(1; 2) Exposure can also occur through dental amalgams(3), cosmetics(4) and some food items(5), primarily fish in which it accumulates from contaminated aquatic environments.(6) Acute toxicity in humans is associated with severe neurological symptoms and ultimately death(7; 8). However, there is not thought to be any lower limit for adverse effects. Since mercury passes through the placenta(9; 10), the fetus is assumed to be vulnerable to its toxic effects, which are amplified by the sensitivity of the rapidly developing nervous system. It is therefore recommended that pregnant women minimise exposure to mercury.

Because mercury levels in aquatic environments and local fish species vary, many countries have produced their own guidance. However, little is known about fish consumption in the adult female populations of many of these countries, and less still about the impact of the advice on consumption of fish during pregnancy. The aims of this review are: (1) to identify, summarise and compare national and international guidelines on fish consumption during pregnancy, as well as for women planning pregnancy or breastfeeding; (2) to appraise the evidence base for the guidelines; (3) to comment on the data available on fish consumption in women of child-bearing age and during pregnancy; (4) to provide some ideas for research and other activities that would inform improvements in guidance and dissemination to ensure maximum benefit to the developing fetus.

Current national and international guidelines

Evidence for beneficial effects of fish on child health and development

The guidance in the UK was developed from the recommendations of the Scientific Advisory Committee on Nutrition (SACN) published in 2004. These were based on calculation of the mercury content of fish that would result in exposure at a provisional tolerable weekly intake (PTWI) of 1.6 µg/kg bodyweight for pregnant women as being sufficient to protect against adverse effects on neurodevelopment in the fetus (3.3 µg/kg for breastfeeding women).(36) Similar approaches have been adopted by other countries, but they fail to take into account the potential risk-payoff from fish consumption(37; 38; 39): fish is a rich source of protein, as well as other nutrients required for fetal neurodevelopment including iodine, selenium, choline, vitamin D and long-chain n-3 fatty acids. Iodine levels in particular have been shown to be low in pregnant women in the UK,(40) and this has been associated with adverse effects on offspring IQ.(41) Indeed, studies from a UK birth cohort have shown evidence of a positively beneficial effect of eating fish in pregnancy on a range of developmental outcomes in the child(42; 43; 44). Evidence for risk is also sometimes based on studies from the Faroe Islands, where mercury exposure is derived from consumption of pilot whales rather than fish(45). The evidence for beneficial effects of fish consumption on many aspects of maternal health and child development has increased in recent years. In the UK, the Avon Longitudinal Study of Parents and Children (ALSPAC; observational birth cohort) includes data on prenatal measures of mercury exposure, together with maternal fish consumption and a range of childhood outcome indicators. In this cohort, consumption of two to three portions of fish per week is associated with beneficial effects on child development, suggesting that limiting fish intake might actually be detrimental.(37) Fish consumption made only a small contribution to the variation in blood levels of mercury during pregnancy.(46) There was no effect on the likelihood of the baby being born with a low birthweight or preterm; indeed, birthweight was lower in the babies of mothers who did not eat fish during pregnancy, suggesting that fish consumption has a beneficial effect on birthweight.(47) Other measures of child development, such as child behaviour, social, motor and communication skills, and IQ similarly showed no association with prenatal mercury exposure.(42; 43; 44; 48) These findings have been substantiated by similar evidence from outside the UK, for example from the Seychelles Development Study, where there is daily fish consumption and mercury exposure levels are about ten times higher than typical exposures in the USA: a variety of neurodevelopmental tests have been applied at ten age points in 24 years of follow up without any evidence of associations with prenatal exposure to mercury(49; 50; 51). Similarly, no associations of prenatal fish intake or mercury exposure with cognitive outcomes in children aged about 7 years in Project Viva in the USA, despite adjustment for long-chain n-3 fatty acids (DPA + EPA) and selenium.(52) In the Norwegian Mother and Child Cohort Study seafood intake was positively associated with birth weight, whereas mercury exposure was negatively associated, suggesting that the balance of the risks and benefits of seafood might need further quantification.(53) However, unlike the other studies described, prenatal mercury exposure was calculated from dietary intakes (food frequency questionnaires) and may not represent mercury exposure in the same way. Other studies have shown similar positive associations of child neurodevelopment with prenatal fish intake.(54)

How much fish do pregnant women eat?

It would therefore seem to be disadvantageous if the guidelines had the unintended consequence of reducing fish consumption in pregnant women. To understand the impact of these guidelines on fish consumption it is necessary first to have accurate nationally representative data specifically from pregnant women. Fish consumption in women of child-bearing age and pregnant women has consistently been shown to be below recommended levels. In a compilation of data on pregnant women from 19 European birth cohort studies with recruitment from 1996 to the date of publication (2014)(55), the median fish intake ranged from 0.4 times/week in the Netherlands (the Generation R study) to 4.5 times/week in Spain (INMA-Childhood and Environment Project). The median oily fish intakes in Italy (Genetic and Environment: Prospective Study on Infancy in Italy (GASPII), Portugal (Generation XXI), Spain (INMA) and Poland (Polish Mother and Child Cohort Study, REPRO-PL) were more than twice the overall median intake of 0.5 times/week. Portion sizes of different fish types varied from 100 g to 150 g across cohorts that included this information. Thus in 14 of the 19 studies, the median intake was less than 2–3 times per week, and no study reported an intake of oily fish of more than once/week (six studies had no data on oily fish intake). A more recent (2017) compilation of 17 cohorts in 11 European countries plus 1 cohort in the USA, which included some of same studies as the previous compilation, found an overall consumption of 1.5 times/week (oily fish 0.6 times/week): women in all but three of the cohorts (Spain, INMA; Portugal, Generation XXI; Italy, NINFEA) ate fish less than twice/week, and none of the cohorts reported an oily fish intake more than once/week.(56)

More specifically, in the UK (where the recommended intake is for at least 2 portions fish/week with at least 1 portion of oily fish/week; Table 2), women aged 19–64 years old participating in the National Diet and Nutrition Survey (NDNS) from 2008 to 2012 ate a mean of 22 g fish/day (about 1 portion/week) including just 8 g oily fish/day (about 0.3 portion/week)(57); mean consumption in pregnant women enrolled in the Avon Longitudinal Study of Parents and Children (ALSPAC) was 235 g/week (about 1.5 portion/week) but 12% ate no fish at all(37); in the Southampton Women’s Study, total fish consumption was 1.8 times/week and oily fish consumption was about 0.5 times/week.(55; 58) Findings in the USA are similar: women of child-bearing age in the National Health and Nutrition Surveys ate a median of 81 g/week (about 0.5 portion/week) and 23% reported not eating any fish(59; 60); mean fish intake in pregnant women was 1.5 portions/week and 14% never ate any fish. In Australia, mean intakes are a little higher about 28 g/day,(61) but still fall far short of national recommended intakes (Table 2).

The methodology used in the surveys conducted is critical to the interpretation of studies on fish consumption: dietary recalls or dietary records are not ideal to capture an item that might be infrequently consumed and have the potential to underestimate fish/seafood intake. For example, in data compiled by EFSA, all country-level surveys were conducted with 24-hour dietary recalls or dietary records and this was noted as being likely to ‘have the potential for overestimating the high ends of the distribution of fish/seafood consumption’.(16) EFSA also noted that conversion of values from daily to weekly to enable comparisons can magnify inaccuracies, as well as there being considerable between-country variation in mean portion size. Methods based on food-frequency questionnaires are likely to be more accurate for this type of low frequency food, but still present difficulties over the length and depth of detail in the questionnaire.(62)

What evidence is there for the effect of guidelines?

Despite evidence of fish consumption below recommended levels in pregnancy, there has been very little research on the impact of the guidelines on consumption levels, or consideration of how consumption levels could be optimised. Most public messages usually struggle to have impact, but there is some evidence that messages that are more ‘alarming’ achieve greater change. As an illustration of this effect, the US FDA issued an advisory notice on avoidance of predatory fish and limitation of consumption of all other fish in 2001 (before this time there was no specific guidance for pregnant women as mercury from commercial fish was not thought to pose any significant health threats). The result of the advisory, which was widely promoted, was a reduction in total fish consumption in pregnancy by about 0.4 portions/week during the year following the notice, with diminished consumption of dark meat fish, canned tuna and white meat fish.(63) Shimshack et al.(38) provided estimates of the observed effects of this advisory on mercury and omega-3 fatty acid intakes and found that mercury intakes across the US population did fall by 17%, but omega-3 intakes also fell by 21%, providing evidence of an unintended consequence. They attributed the fall in omega-3 intake to ‘coarse information and broad behavioural guidance’ with lack of a detailed explanation of the recommendation that consumers select ‘a variety of other kinds of fish’.(38) The 2001 advisory was replaced in 2004 and again in 2017 (Table 3). For the 2004 guidance(64), there is some evidence that in face of confusing and complex guidelines, and lack of readily available advice, many women gave up eating fish: analysis of focus groups for 22 pregnant women who ate <2 portions of fish/week in the USA in 2009/10 showed that many of them had received advice to limit their fish intake and knew that fish could contain mercury. Because of this advice, and a lack of knowledge about which types of fish were safer to eat, many of the women reported that they would rather avoid fish altogether than risk harm to themselves or their baby. They felt that advice from a doctor on eating fish and readily available information on which fish are safe to eat would have encouraged them to eat more fish.(65) There is direct evidence of lower intakes in pregnant women compared with non-pregnant women in Australia, where mean intakes were 28 g/day in pregnant women but significantly greater at 33 g/day in women who were not pregnant, trying to conceive or <1 year postpartum.(61)

There is some evidence, however, that targeted education during pregnancy can result in increases in fish consumption. Fifty-five pregnant women in the USA who were low fish eaters (≤2 servings/month) were randomised to receive control messages, advice to eat low-mercury fish, or advice to eat low-mercury fish plus coupons to buy fish: fish consumption increased in both intervention groups without an increase in blood mercury levels compared with baseline values.(66) Although this was a pilot study with small numbers of women, it does indicate that women are receptive and willing to increase their fish intake and can achieve this without increasing mercury exposure when given appropriate targeted advice.

Summary and Conclusion

There is great variation in the content, complexity and presentation style of guidance for pregnant women on fish consumption between countries. This partly reflects local environmental conditions, species availability and consumption preferences, and to some extent local preferences for delivery of public health messages. The guidelines have largely been based on the mercury content of fish with far less consideration being given to the positive beneficial effects nutrients provided by fish. There is evidence for a low levels of several nutrients provided by fish – notably iodine – in pregnant women and it is essential that pregnant women are given balanced advice in order to make informed choices.

There is some evidence that pregnant women find the advice confusing and prefer to give up eating fish altogether rather than take the risk of harm. There is general agreement that pregnant women should eat at least two portions of fish per week, but this message is not always clear and prominent. Fish consumption falls below this level in many countries and this may have adverse effects on offspring health and development. Guidance needs to be clear, simple and memorable, and appropriately disseminated, to achieve impact.(67) Guidance could include visual rather than narrative content. Use of technology, for example, the development of apps, could enable women to record their fish consumption in real time and give feedback on compliance with guidance over a week or other time period.

Acknowledgments

Footnotes

References