SYSTEMATIC REVIEW

Impact of Regulatory Interventions to Reduce Intake of Artificial Trans–Fatty Acids: A Systematic Review We examined the impact ofregulatoryactiontoreduce levels of artificial trans–fatty acids (TFAs) in food. We searched Medline, Embase, ISI Web of Knowledge, and EconLit (January 1980 to December 2012) for studies related to government regulation of food- or diet-related health behaviors from which we extracted the subsample of legislative initiatives to reduce artificial TFAs in food. We screened 38 162 articles and identified 14 studies that examined artificial TFA controlslimiting permitted levels or mandating labeling. These measures achieved good compliance, with evidence of appropriate reformulation. Regulations grounded on maximum limits and mandated labeling can lead to reductionsinactualandreported TFAs in food and appear to encourage food producers to reformulate their products. (Am J Public Health. 2015; 105:e32–e42. doi:10.2105/AJPH. 2014.302372)

Vivien L. Hendry, PhD, Eva Almíron-Roig, PhD, Pablo Monsivais, PhD, Susan A. Jebb, PhD, Sara E. Benjamin Neelon, PhD, Simon J. Griffin, DM, and David B. Ogilvie, PhD, FFPH

A HIGH INTAKE OF DIETARY trans---fatty acids (TFAs) has been associated with an increased risk of cardiovascular disease.1---4 Artificial TFAs, also known as industrially produced trans fats or hydrogenated fats, are sometimes used in pre-prepared food as a costeffective way to increase shelf life and improve the texture and taste of baked goods.4,5 Although TFAs cannot be completely eliminated from the food supply—they occur naturally at low levels in many food items such as meat and dairy products—levels of artificial or industrially hardened TFAs can be reduced. Guidelines worldwide recommend limiting consumption to less than 1% to 2% of total dietary energy.1---3 On average, consumption in countries such as the United States and the United Kingdom is close to this level, although there can be wide variation within the population.1,6 The National Institute for Health and Clinical Excellence in the United Kingdom estimated that reducing TFAs to 0.7% of total fat energy consumed could save about 571 000 life-years.7 Governments face pressure to intervene to control levels of TFAs in the food supply to protect human health.4,8 Most recently, the US Food and Drug Administration announced that partially hydrogenated oils, an important source of artificial TFAs, would be downgraded from “generally recognized as safe” for use in food by 2015, effectively banning them.9 Options for intervention include mandated maxima for TFAs in

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food (i.e., bans), consumer labeling to guide choices, education to encourage consumers to change dietary habits, and voluntary agreements with food producers to limit the use of artificial TFAs.10,11 Such voluntary agreements have helped reduce levels of artificial TFAs in countries such as the United Kingdom and the Netherlands,12,13 although the impact of such agreements depends on the extent to which industry is willing to agree to and abide by the arrangement.14 Labeling mandates aim to guide consumer choice and put pressure on manufacturers to reduce artificial TFAs in response to consumer demand. Informed individuals can choose to avoid artificial TFAs by not eating the types of food that contain them, so appropriate labeling, along with information and education, may also have an important role. A World Health Organization report that included industry self-regulation found that all types of policy intervention reduced artificial TFAs in food; bans were reported to be the most effective, although the success of labeling and voluntary initiatives varied by type of food.15 Our review independently updates this evidence, with a focus on enforced or enforceable regulatory interventions. Enforced standards such as maximum limits can create a level playing field for food manufacturers, providing a clear, robust framework for action. Furthermore, they can lead to reduced consumption that does not depend on changes in food

choices, providing benefits across all socioeconomic groups. Mandatory approaches face a range of barriers, because they can be politically unpopular, require a long-term commitment to monitoring and enforcement, and have unintended consequences. Legislation to control levels in a country may spill over to affect other countries, either beneficially through exporting foods that contain lower levels of artificial TFAs or detrimentally if manufacturers export artificial TFAs abroad in search of new and permissive markets.16 We examined how different types of regulations have affected levels of artificial TFAs in food worldwide. Our primary outcome was the availability of artificial TFAs in food. Secondary outcomes included any other measured outcomes the studies reported; these could be changes to individuals’ food purchasing or consumption behaviors or manufacturers’ responses such as reformulation, substitution of ingredients, promotional activities, or price changes.

METHODS We systematically searched for studies of legislative initiatives to reduce levels of artificial TFAs in food. This was part of a larger systematic scoping review of government regulation, rules, and legislation to influence healthy eating. As a systematic scoping review, it differed from established systematic review methods in how we designed the search and

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synthesized the data. We followed Cochrane Collaboration, Centre for Reviews and Dissemination, and Evidence for Policy and Practice Information and Co-ordinating Centre guidance for conducting systematic reviews with reference to recommendations for good practice.17---20 We selected studies for review using modified PICOS (population, intervention, comparison group, outcome, study design) criteria (Table 1). A study was eligible if (1) it examined a regulation or piece of legislation that was enforced or enforceable; (2) the regulation or legislation had a direct aim to influence the healthiness of food or diets, for example, by directly manipulating ingredients used in food or by influencing individual choices about which foods are eaten; (3) it had a recognizable research design, which included some description of methods; and (4) the impact of the regulation was assessed. We excluded studies if they did not meet all 4 criteria, unless the reviewer decided there

was insufficient information. If so, studies remained in the review until we acquired further information. The results of the scoping review are reported elsewhere.21 Studies had to meet an additional inclusion criterion: the intervention explicitly specified artificial TFAs as a target of the regulation.

Information Sources and Search Strategy In our systematic scoping review, we searched Medline, Embase, ISI Web of Knowledge, and EconLit from January 1980 to the end of December 2012. We also searched for gray literature, such as unpublished research or government reports, via Google Scholar, and we hand-searched bibliographies. We did not restrict the searches by language, country, or any other dates. When necessary, we obtained translations for titles or abstracts in languages other than English. Searching by population, outcome, or comparison group was not possible because our review

was designed to capture a broad range of eligible types of study. We used the modified PICOS criteria to develop a search strategy including relevant medical subject headings and text words. To accurately capture the diversity of regulations to directly influence diet or diet-related behavior, we broke the intervention concept down into 3 groups of key terms: (1) terms associated with regulation, rules, or legislation; (2) terms describing what was being regulated by type of food, drink, or nutrient; and (3) terms for the settings subject to the regulation, including a wide variety of locations, vendors, organizations, and other types of environments. Eligible study designs included quantitative or qualitative primary research studies with a recognizable research design. We excluded commentaries, editorials, and opinion pieces. We excluded a set of regulations we considered to have only an indirect effect on healthy eating, such as those pertaining to food safety, agriculture,

TABLE 1—Description of Research Question Components by Population, Interventions, Comparisons, Outcomes, Study Designs, and Excluded Regulations: Regulatory Interventions to Reduce Intake of Artificial Trans–Fatty Acids, 1980–2012 Criteria

Description

Population

Population-wide initiatives

Interventions

Regulation or legislation

Comparisons

Any, if available

Outcomes

Long term (e.g., mortality, morbidity, obesity) Intermediate and short term (e.g., food purchasing practices, consumption of specific foods, overall diet)

Study designs

Experimental designs (e.g., controlled trial), before–after design, interrupted time series, regression

Subgroups (e.g., age, gender, ethnicity, socioeconomic status, weight status)

Economic and cost data, if available discontinuity, natural and quasiexperiments, cohort, or longitudinal study, cross-sectional or survey, economic model, or qualitative studies such as focus groups, interviews, in-depth case studies, participant observation, and documentary analysis Excluded regulations

Food hygiene or health and safety; sustainability; agricultural and transportation policies; micronutrients, additives, and flavorings such as fluoride in water, fortifying flour with folic acid, or adding iodine to salt; alcohol control policies; voluntary agreements and guidelines; organization-level interventions; and legislation preventing antiobesity lawsuits

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transportation, or sustainability (Table 1). (Data available as a supplement to the online version of this article at http://www.ajph.org provide an example of a search strategy, which we designed to be sensitive rather than specific to ensure that we identified all relevant studies in a diverse and variably described literature.)

Study Selection and Data Extraction Three of the authors (V. H., P. M., E. A. R.) screened titles and abstracts using the eligibility criteria. In the first round of screening, we independently double screened a subsample to assess the level of agreement between the reviewers. We retained articles if the title and abstract were unclear about whether the study met the inclusion criteria or reviewers disagreed. We then independently screened full texts using the same eligibility criteria of 5 of the authors (V. H., P. M., E. A. R., S. B. N., D. O.). All authors discussed disagreements between reviewers at any stage to reach a consensus, and we sought further information about studies if necessary before reaching a final decision (Figure 1).22 The same 5 authors extracted data. We derived the data extraction form from Cochrane Effective Practice and Organization of Care guidelines and piloted it on a sample of studies.23 We assessed a subsample of studies in duplicate to assess consistency between reviewers. We extracted data on country; location of the intervention; characteristics of the intervention; study population characteristics, including socioeconomic status of study participants; baseline and follow-up measures; study design; results for primary and all secondary outcomes, including costs; and any subgroup analyses, limitations, and conclusions.

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Records identified through database searching (n=42 894)

Included

Eligibility

Screening

Identification

SYSTEMATIC REVIEW

Additional records identified through other sources (n=31)

Records after duplicates removed (n=38 162)

Records screened (n=974)

Records excluded (n=840)

Full-text articles assessed for eligibility (n=134)

Full-text articles excluded, with reasons (n=120)

Studies included in synthesis (n=14)

FIGURE 1—PRISMA flow23: regulatory interventions to reduce intake of artificial trans–fatty acids, 1980– 2012.

Reviewers also recorded their own interpretation of the results, limitations, and conclusions. We assessed risk of bias using Cochrane Effective Practice and Organization of Care guidelines and integrated it into the synthesis to moderate our interpretation of the results.22 The studies were distinctly heterogeneous with respect to design and reporting of results (Tables 2 and 3). Metaanalysis was not appropriate, and we therefore combined results in a narrative synthesis.

studies that did not meet our criteria for inclusion (Figure 1). We found 14 studies that examined artificial TFA controls.24---37 Seven studies examined the impact of maximum limits on the use of artificial TFAs in Denmark; New York City, NY; and British Columbia (Table 2). Seven studies assessed government-mandated explicit labeling of artificial TFAs provided separately from general nutrition information on food in the United States, Canada, and Korea (Table 3).

RESULTS

Studies of Limits on Artificial Trans–Fatty Acids

The searches identified 38 162 studies after we removed duplicates (Figure 1); the vast majority did not address government regulation to influence the healthiness of food, diets, or dietary behaviors. Thus, we eliminated 38 148

Interventions. In the 7 articles we examined, the regulations either set maximum upper limits on the finished product or banned the use of artificial TFAs during food manufacture (Table 2). Denmark legislated a 2% artificial TFAs

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maximum for all oils and fats used in food available for sale in 2004. New York City followed in 2006 with a ban on the use, storage, or serving of foods with a total of 0.5 grams or more artificial TFAs per serving in all licensed food service establishments including restaurants, schools, caterers, senior centers, and street food vendors. British Columbia restricted the use of artificial TFAs to 2% of total fat content for margarines and spreads and 5% of total fat for all other foods sold in food service establishments. Limitations and study quality. Six of the 7 studies assessed a change in TFA levels pre- and postregulation,24---26,28---30 whereas 1 assessed compliance postregulation only.27 Five studies used independently measured TFA levels in food samples26---30; the other 2 studies relied on food labels for

their primary outcome.24,25 Analysis predicated on the Cochrane Effective Practice and Organisation of Care guidelines for assessing bias suggested that the study designs used presented a moderate to high risk of bias. Only 2 studies included control groups.29,30 Across all studies, little consideration was reported to have been given to the potential influence of missing data, and there was inadequate reporting of whether efforts had been made with regard to the adequate blinding of assessors, protecting the data from contamination (such as confounding from other interventions or mislabeling), or selective reporting. Availability of artificial trans--fatty acids in food. All 7 studies consistently reported good compliance to a mandated artificial TFA limit, either measured in purchased foods or reported on food labels.24---30 Four of the 7 studies examined Denmark’s regulations. Before the limit was introduced, about 25% of Danish foods did not comply with the proposed maximum, whereas by 2006 and 2007 this proportion had fallen to 9%.26 Measurements of Danish popcorn indicated that artificial TFA levels decreased from 30 grams of TFAs per 100-gram serving before the regulation to less than 1 gram per 100-gram serving afterward.29 In the third evaluation, when compared with more than 20 other countries, Denmark had the lowest or among the lowest measured artificial TFA content in different types of fast food and below the maximum permitted levels.29,30 Similarly, when Leth et al. tested a wide range of food samples, the majority complied with the Danish regulation, although Leth et al. did not report an exact figure.28 In New York City, prevalence of artificial TFA use in

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information for French fries sold in 4 major fast food chains

establishments, including

restaurants, schools,

in 2007; 7 885 purchases in 2009

licensed food

establishments, including

shop-bought snacks from 2002 to 2003; 148 foods 2004–2005; 45 foods 2006–2007

and fats used in food

imposed from January

2004

Leth et al. 28 and 148 food samples in 2005

imposed from January

2004

253 food samples in 2003 Denmark

and fats used in food

service establishments;

2% maximum TFAs in oils

service establishments

British Columbia food

produced TFAs in all

30 000 inspections of food British Columbia

253 domestic or imported

2% maximum TFAs in oils

when saturated fats were

bought snacks

comparison of shop-

Pre- and postlegislation

health officers) of compliance

assessment (environmental

legislation: “much fewer” (number not reported)

> 2% TFAs; post-

legislation contained

25% of samples pre-

legislation

reported

Postregulation figures not

worse fatty acid profiles

lines and importers

Postregulation independent 90% compliance after

reformulation resulted in

directly from production

regulation

Continued

complied with the

Majority of foods tested

the foods measured

controlled TFA levels in

and fast foods Regulation effectively

were more likely in sweet

used; unsaturated fats

in 2006–2007;

Enforcement Office

with the maximum before

products did not comply

Food Control and

Not reported

each comparison time

neighborhoods Reduced TFAs: 25% of

the ban, down to 11% in 2004–2005 and 9%

legislation (1 time point)

Different sample sizes at

and low-poverty

transition; samples collected by the Regional

during, and after

time points: before,

TFAs in foods after

saturated or total fat; no difference in TFAs per purchase between high-

to significantly increase

not associated with TFA per purchase

chains without appearing

purchased from major

content of fast food

successfully reduced TFA

Local regulation

to TFAs

reducing exposure levels

Policy was successful at

Conclusions

neighborhood poverty was

TFA content of foods at 3

section shows association

(P £ .001); saturated fat only

representative; cross-

down by 0.55 g but total

Restaurants may not be

decreased by 2.4 g 60.4 g

self-report

derived from restaurant

examined; data were

Only 1 type of food was

Limitations

Mean TFA per purchase

decreased by a mean of 54%

plus saturated fat

< 2%; total reported trans

use fell from 50% to

Estimated restaurant TFA

Results

and street food

fast food purchases

consumers’ lunchtime

sectional study of

Pre– and post–cross-

postregulation

composition pre- and

Ecological study of food

Design

fat down by 1.9 g;

Denmark

New York City, NY

New York City, NY

Country or Setting

caterers, seniors’ centers,

restaurants, schools,

6 969 fast food purchases

Ban in 2006 for all

caterers, seniors’ centers, and street food

Web site nutrition

licensed food

Foods Tested

Ban in 2006 for all

Intervention

Forster-Coull and Kendall27 Restrict industrially

Bysted et al.26

Angell et al.25

Angell et al.

24

Author

TABLE 2—Study Characteristics of Artificial Trans–Fatty Acids (TFAs) Limits: Regulatory Interventions to Reduce Intake of Artificial TFAs, 1980–2012

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Hendry et al. | Peer Reviewed | Systematic Review | e35

bought in 26 countries imposed from January 2004

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countries. A low average

daily intake (1 g) for

a population did not

preclude a high intake

among subgroups

Czech Republic, Finland,

France, Germany, Hungary,

Italy, Netherlands, Norway,

Peru, Poland, Portugal,

Romania, Russia, South

Turkey, United Kingdom, United States

Africa, Spain, Sweden,

“high trans menu”

composed of popular foods in 18 out of 19 used

in popular foods were from 30 g in a high-TFA

menu in 2001 to < 1 g in 2005 comparison: Austria, Bulgaria, Canada, China,

Denmark reduced exposure The highest values for TFAs Possible to get 20–30 g Kingdom, United States

cross-sectional multinational and shop-bought snacks and fats used in food

and September 2005 2004

542 samples of fast food

between November 2004 imposed from January

2% maximum TFAs in oils Stender et al.30

bought in 20 countries and fats used in food

Denmark

Spain, Sweden, United

Denmark pre– and post–

legislation Russia, South Africa,

Peru, Poland, Portugal,

had among the lowest

levels of TFAs compared with countries without laboratory for analysis > 5% TFAs

permitted level

below maximum

postlegislation; Denmark

Germany, Hungary, Italy, Netherlands, Norway,

distance transportation to all servings contained Republic, Finland, France,

unknown effects of longChicken products; 50% of Bahamas, Czech

within-country variation; 2% in Kentucky Fried comparison: Austria,

Unrepresentative samples

from each country and McDonald’s products and

Denmark: 1% TFAs in Cross-sectional 43 fast food servings 2% maximum TFAs in oils Stender et al.29

TABLE 2—Continued

Denmark

multinational

TFAs in Denmark were

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food service establishments fell from 50% to 2% after the legislation was introduced in 2008.24 A follow-up study of artificial TFA content per fast food purchase reported lower mean levels of artificial TFAs, which decreased by 2.4 grams 60.4 grams (P £ .001) between 2007 and 2009.25 Lastly, a report from British Columbia found 90% postregulation compliance after 30 000 inspections by independent environmental health officers following the introduction of restrictions.27 Overall, there was consistent evidence that regulations to set maximum lower level limits of artificial TFAs in individual food items achieved good compliance. Secondary outcomes. Two studies examined the types of fats that were used to replace artificial TFAs. For fast food purchases in New York City, mean saturated fat content increased by 0.6 grams (confidence interval [CI] = 0.1, 1.0; P = .001), although combined saturated plus TFAs decreased by 1.9 grams; changes in total fat and other types of fats were not reported.25 Bysted et al. reported that in Denmark, 68% of paired before---after food samples showed an increase in saturated fat; saturated fat tended to increase in chocolates, sweets, and baked goods, whereas unsaturated fat increased in popcorn and fried potato products.26 Mandated limits on TFAs in manufactured food do not guarantee intakes below dietary recommendations if consumers have a diet high in processed or fried food. Stender et al. highlighted that despite Denmark’s legislated 2% maximum for any food product, it remained possible to consume a “high trans menu” of 20 to 30 grams—equivalent to about 8% to 12% of daily energy intake. 29 This study further

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Ratnayake et al.34

Niederdeppe et al.33

Mozaffarian et al.32

Lee et al.

31

Author

containing TFAs in Los Angeles County

margarine, cookies, and hot dogs) merged with news

reformulation: 75% of a subsample of 32 products decreased TFAs from 26% 613% to 2% 64%

cross-sectional design with repeated measures for a subsample of 32 products

2005–2007

TFAs at baseline;

for reformulated products

total fat 0.8% 63.0%

fats; mean change in

TFAs with unsaturated

products replaced

food composition;

likely to contain TFAs

contained ‡ 5%

laboratory testing of

restaurant foods

introduced in 2005

96% of reformulated

3 wk

Effects dissipated after

90% of restaurant foods

supermarket and

unchanged in 65% of

food labeling

consumers without

empowered

Generalizability to less

consumption

data not food

news influence sales

Indirect measure of

Continued

generally unchanged

total fat content was

than saturated and

unsaturated fats replaced TFAs rather

to reformulate products;

influence the decision

publicity appeared to

supported by

Mandatory labeling

labeling

TFAs after the launch of federally mandated

of products containing

consumer purchases

influenced short-term

News coverage

decreased saturated fat

exceeded any

decreased TFAs

Postreformulation:

fat levels

Saturated fat lower

decreased saturated

and cookies showed

by unsaturated fatty acids although cakes

foods TFAs replaced

labeling; in fried

reduced after

TFAs significantly

Conclusions

unsaturated fat None reported

None reported

Limitations

decreased

replaced by

fat in cakes and cookies; frying oil

decrease in saturated

categories; marked

and across

Wide variation within

Secondary Results

42% of products

221 grocery and

postlegislation

reduced sales

Linear trend showing

restaurant foods

(92%) for 25

supermarket foods; 3.3 g per serving

(84%) for 58

1.8 g per serving

Mandatory TFA labeling Postregulation

sales of products

Crisco, cookies,

Canada

media coverage on

data (popcorn,

introduced in 2006

coverage data

series regression of

Grocery store sales Cross-sectional time

analysis and food composition databases

restaurant foods 1993–2006 and

United States

through documentary

supermarket and

2008–2009

foods identified

brand-name

Mandatory TFA labeling

introduced in 2006

respectively)

2005 and 2008 Mean decrease of TFAs

and 0.64 g/100.00 g,

coffee) tested in

Pre- and postlegislation;

except 2 categories (0.53 g/100.00 g

cakes, instant soup powder, and canned

83 reformulated major

g/100.0 g for all

By 2008 below 0.5

0.01–6.88 g/100.00 g.

Baseline TFA range:

Primary Results

chicken, cookies,

United States

composition and lipids

French fries, fried

Mandatory TFA labeling

testing of fatty acid

Pre- and postlaboratory

(breakfast cereal,

Korea

Design

7 food categories

Country

introduced in 2007

Foods Tested

Mandatory TFA labeling

Intervention

TABLE 3—Study Characteristics of Artificial Trans–Fatty Acids (TFAs) Labeling: Regulatory Interventions to Reduce Intake of Artificial Trans–Fatty Acids, 1980–2012

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Van Camp et al.37

Ricciuto et al.36

Ratnayake et al.35

food composition, 448 label based; cross-sectional design; unclear

identified as high in TFAs in 2004, from 2005 to 2009

testing

introductions in 2001–2002 and

introduced in 2006

Database

New Product

in the Minitel Global

2008–2009 reported

5 012 product

Mandatory TFA labeling

supermarkets in the greater Toronto area

United States content

Changes in labeled fat

and average price

and in 2006 (274 margarines) by major

labeled fat composition

2002 (229 margarines)

introduced in 2005

Pre- and posttesting of

Margarines sold in

Mandatory TFA labeling Canada

672 products for

cafeteria foods

extent of repeated

laboratory testing of

Postregulation

chain restaurant and

introduced in 2005

Canada

1 120 grocery and

Mandatory TFA labeling

TABLE 3—Continued

saturated fat

at baseline; decreased

decreased saturated fat; mandatory labeling decreased the price premium of low-TFA products

to 43% (P £ .001); mean labeled TFAs decreased significantly from 0.80 g/10.00 g

“TFA-free” in 2009, but only 55% and 23% did so

fat; cookies decreased palm oil, significantly decreased saturated fat, % of total fat

and 77% of cookies were eligible to claim

unsaturated fat, no change to saturated

Potato chips

(P £ .001)

85% of potato chips

replaced TFAs with

decreased from 28%

serving to 0.34 g

6 of 18 margarines

“TFA-free” margarines

to 78% by 2009

decreased TFAs and

“Most”’ products

contained ‡ 5% TFAs

58% of products

labeling errors

and potential

sampling technique

new products, unsystematic

Did not capture all

sample size in 1 city

time points; small

composition at the 2

estimating margarine

Different methods for

None reported

brand image

also beneficial to

claims are used when

products; “TFA-free”

TFAs in most

reformulated to virtually eliminate

New launches were

disparities

population health

potentially decreased

mandatory labeling,

decreased after

higher in price and this premium

free” margarines

than doubled; “TFA-

margarines more

The range of “TFA-free”

frying with partially hydrogenated oils

sources by discouraging

restaurant and cafeteria)

and unregulated (chain

regulated (prepackaged)

Reduced TFAs in

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stated, “The [TFA] legislation had no noticeable effect on availability, price, or quality of food items previously containing high amounts of TFA” in Denmark following the regulation. 29(p51) In terms of variations in exposure to TFAs postregulation, only the study by Angell et al. looked for potential neighborhood differences.25 They found no statistically significant differences in the change in artificial TFA content of restaurant chain purchases between high- and low-poverty neighborhoods in New York City, suggesting the effects of mandated maxima for TFAs were equitably distributed.25

Studies of Mandatory Labeling of Artificial Trans–Fatty Acids

Interventions. Mandated TFA labeling has been introduced in many countries worldwide. These regulations were implemented in Canada in 2005, the United States in 2006, and Korea in 2007. They required all packaged foods to make a back-of-pack nutrition facts statement and allowed an additional front-of-pack declaration, with variation between countries. In the United States, a product containing less than 0.5 grams of TFAs per serving could be labeled as “0g trans fat,” whereas for Canada and Korea, the lowest declarable value is 0.2 grams or less of TFAs per serving. Limitations and study quality. As with the studies of maximum limits, we judged the risk of bias in the studies on labeling to be moderate. 31---37 All studies reported pre- and postcomparisons, with a variety of study designs including 2 time series.33,37 Three studies used nutrient declarations on food packs purchased for the study as the primary outcome,32,36,37 2 used measured

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artificial TFAs in purchased food samples,31,34 1 used both laboratory-based and label-based information,35 and 1 used sales data for a prespecified set of products high in artificial TFAs.33 None of the pre- and poststudies included a comparison group, and there was little or no assessment of the impact of potential missing data, lack of blinding, or protection from contamination or selective reporting. Both time series studies reported concomitant changes that might have influenced the perceived impact of the intervention, including education campaigns, consumer interest, and media publicity on efforts to ban or reduce artificial TFAs worldwide over the same period.33,37 Availability of artificial trans--fatty acids in food. Six of the 7 studies found that mandating TFAs declarations on labels reduced the artificial TFA content across a wide variety of food products, whether measured by laboratory tests or from labeled fat content (Table 3). One of the studies, that of Niederdeppe and Frosch, did not have a primary outcome on the basis of the availability of artificial TFAs but examined changes in consumer behavior.33 A Korean study found that before the labeling regulation, levels of up to 6.88 grams per 100.00 grams were measured in laboratory tests of packaged foods, which decreased to a maximum of 0.5 grams per 100.0-gram postregulation.31 Ricciuto et al. examined margarines in Canada, reporting that the proportion labeled with less than 0.2 grams artificial TFAs per 10.0 grams increased from 31% to 69% after the labeling regulation was introduced in 2006.36 Ratnayake et al., in their 2 Canadian studies, measured changes in fat content following artificial TFA

labeling.34,35 The authors found that 75% to 76% of measured products were reformulated to reduce artificial TFAs,34,35 with average levels decreasing from 26% 613% to 2% 64% of total fat.34 Lastly, 2 of the 3 US studies evaluated changes to labeled packaged foods, including the proportion using a “0g trans fat” declaration. Van Camp et al. measured the use of partially hydrogenated vegetable oil, an important source of artificial TFAs, which fell by 45% in chips and 42% in cookies after labeling legislation.37 Similarly, in a study of foods, Mozaffarian et al. found that 95% of supermarket products and 80% of restaurant products had been reformulated to reduce total TFAs to below 0.5 grams per serving.32 Secondary outcomes. Reported total fat changed very little, on average, across all the studies. In general unsaturated fats appeared to replace artificial TFAs,31---37 although there were some reports of small increases in saturated fat. Three studies examined differences between product categories and found that there was noticeable variation in the types of fats used for reformulation.31,35,37 Fried foods were consistently reformulated to replace artificial TFAs with higher levels of unsaturated fats, whereas bakery goods such as cakes and cookies, used saturated fats, including palm oil.31,35,37 Apart from reformulation, a single study assessed the impact of media coverage of the labeling mandate and consumer responses using sales data for 7 products.33 During a period of high media coverage postlegislation, consumers reduced purchases of 3 of the 7 foods containing labeled TFAs, but the trend for reduced sales faded after 3 weeks.33 Van Camp et al. found that manufacturers were not using TFA-free claims on foods that

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were entitled to do so unless it was also perceived as beneficial to the brand image to market the product as such.37 One of the Canadian studies examined the impact on price following the labeling mandate.36 Products labeled “TFA free” carried a price premium, whereby a decrease of 1 gram artificial TFA per 10-gram serving of margarine doubled in price from CAN $1.00 per kilogram in 2002 to CAN $2.00 per kilogram in 2006.36

DISCUSSION We have shown that maximum limits and mandatory labeling reduced the availability of artificial TFAs in food items for sale or reported on food labels since 2004. This suggests that governments have access to interventions that have the potential to reduce average population consumption of artificial TFAs. We found that the studies of maximum limits on artificial TFAs reported good compliance with the regulation, which appeared to effectively reduce artificial TFA levels in individual food items. The studies of labeling mandates also found good compliance levels in that labeled TFAs were lower subsequent to the ruling. The aim of labeling is to inform consumers, raising their awareness, and ultimately to alter market supply through consumer demand. Consumers can encourage food manufacturers to reformulate their products. Without unmonitored controls for comparison, it cannot be established whether monitoring encourages compliance for either maximum limits or mandatory labeling, although other studies have identified monitoring as an important feature of best practice.14 We did not identify any evaluations that addressed other outcomes such as food choices, dietary

behavior, nutritional intake, obesity or cardiovascular disease risk factors, or disease prevalence. We have not reported the costs of introducing, enforcing, or maintaining regulations because of a lack of data. A single study examined socioeconomic differences, reporting similar effects in more and less affluent neighborhoods. Even after the introduction of a new regulation, some individuals may still consume a diet that exceeds dietary recommendations for TFAs by selecting a high proportion of foods that continue to contain them. Labeling rules may have unintended consequences, for example, in the United States, levels below 0.5 grams can be labeled as 0 grams of artificial TFAs, leading to reductions in suggested serving sizes to meet labeling criteria.38 By disclosing information about a product’s desirable attributes, labeling is a form of advertising for food manufacturers whereby selective disclosure can be used to manipulate consumers’ choices.39 Ricciuto et al. reported that manufacturers’ decisions to label margarines “TFA free” also depended on the perceived value of labeling as a marketing tool.36 Labeling rules may have less desirable consequences if they lead to an increase in price, as Ricciuto et al. found.36 When there are underlying socioeconomic differences in consumer purchasing patterns and desires to avoid artificial TFAs, price differences could exacerbate inequalities, although we did not identify evidence of this in the studies we included in our review. The finding that mandating the content of labeling of TFAs in food is an effective strategy to reduce population TFA intake concurs with a World Health Organization report, although it was grounded on studies identified from a slightly

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different set of databases for studies and used a less comprehensive search strategy. However, the World Health Organization report, usefully, also examined the impact of voluntary initiatives. These were reported to be more variable in their success and often depend on the category of food targeted; margarines and bakery products were among the least affected unless specific initiatives were reinforced with a national ban.15

Secondary Findings For both maximum limits and labeling, it appears to be more difficult to find reliable healthy substitutes for the industrially hardened fats used in baked goods than it is for the oils used for frying, and the choice of replacement may have implications for public health.31 Palm oil is the replacement oil typically used by food producers, and a widespread switch to palm oil could raise future ecological and public health challenges, because increased palm oil farming has led to the destruction of tropical rainforests, and the oil itself is high in saturated fat.4,15,40 Replacing artificial TFAs with saturated fats is less desirable from a public health perspective than is a strategy that reduces both types.41 It is therefore important to consider the public health implications of the fatty acid profile of the oils used in reformulated products.

Implications for Research It is challenging to develop robust study designs to examine the impact of national-level reformulation or labeling and most of the available data are from pragmatic before---after studies in which policy changes were evaluated as a “natural experiment.”42,43 Cochrane criteria for assessing the

risk of bias were often not readily applied to studies of this type. Studies examining trends in purchasing TFA-containing foods before and after the enforcement of a regulation could shed light on how consumers respond to these strategies. As governments worldwide take steps to reduce the use of artificial TFAs, there is a need for more primary research to examine whether the anticipated population health benefits are realized, particularly changes to long-term cardiovascular risk and disease burden, and for more research that goes beyond secondary sources such as labeled TFA content. Future research should examine the impact on inequalities of different types of regulation as well as the costs and unintended consequences to society of reducing the artificial TFA content of food.

Implications for Policy and Practice Mandated limits and labeling reduce the presence of an undesirable substance in the food supply overall, although they may do little to influence individual behaviors and food choices. However, this can be an advantage, because mandated controls do not necessarily need to engage with consumers or behavior change to have an impact. It also creates the opportunity to engage with and inform the public about the health impact of artificial TFAs, using the legislation as a prompt for promoting healthier lifestyles. Limits or bans create a standard policy and could be attractive to industry, because they reduce potentially unfair competitive advantages for noncompliers. The sparse evidence suggests that limits do not appear to worsen inequalities, but the majority of studies did not examine this issue and further

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research is warranted, because it has been suggested that labeling initiatives may inadvertently exacerbate inequalities.36 Labeling is intended to help individuals make healthier choices, particularly as public knowledge increases about the detrimental health effects of artificial TFAs.44 This approach involves a relatively high level of consumer personal responsibility. The success of any labeling scheme is likely to be strongly associated with any concomitant health promotion in the media and educational strategies.33 Understanding the impact on inequalities is important because when average TFA intake is low there may be little incentive for governments to take further action unless it can be shown to specifically reduce inequalities. Evidence beyond that which we reviewed suggests that some gains can be made with voluntary action by the food industry.45 In such cases, public pressure and the threat of stronger government action could be used to encourage closer compliance with voluntary agreements. Poor cooking practices, especially frying, remain an important contributor to TFA intake. Regulations to limit TFAs, such as those implemented in Denmark, New York City, and British Columbia, have addressed this issue by requiring food service establishments to meet the mandated maxima as sold.24,29 However, introducing a labeling standard for all types of food service establishments relating to food as sold would be challenging to implement and monitor.

Strengths and Limitations of the Review Our methods were derived from the most up-to-date, robust, and valid systematic review techniques as disseminated by

Cochrane, Centre for Reviews and Dissemination and the Evidence for Policy, and the Practice Information and Co-ordinating Centre.17---20 We carried out an extensive search of the literature and screened more than 38 000 records without language or publication date limits. We were able to retrieve all the identified research studies. We restricted the review to a narrative synthesis; meta-analysis was not appropriate because of the small sample and the heterogeneity of the studies identified. We excluded voluntary agreements between industry and governments to reduce artificial TFAs in the food supply. Studies have suggested that food producers will voluntarily and effectively reduce levels in specific food items when they see the business case.45 For example, in the Netherlands an industry-led initiative in 1995 and 1996 reduced artificial TFAs from 18 grams to less than 2 grams per 100 grams in margarines through working with government and engaging social groups.13,46 Our findings were independently reached and are consistent with other reviews, such as the World Health Organization report on policies for reducing dietary TFAs.15

Strengths and Limitations of the Evidence There are numerous potential sources of bias in the studies included in our review. These were nonrandomized studies, so there was a risk of selection bias as well as performance and detection biases because of a lack of blinding. It was frequently unclear whether attrition in the form of incomplete outcome data was a concern because of the way data were selected for analysis. Similarly, it was rarely reported whether there had been

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any steps to protect the study from contamination by external, concomitant initiatives. Only a subsample of the artificial TFA limits and labeling mandates that have been introduced have been evaluated, a common issue in this field.15 Although the directions of the principal findings provided a consistent message, the risk of bias in the evidence available was moderate to high overall. We did not identify any controlled trials, few studies included a comparison or control group, and none were able to randomize exposure to the intervention. Effects on population health or on individual behavior have not been measured. The existing research tends to assume that reducing the availability of artificial TFAs will also reduce consumption, although no studies measured this in practice. For example, a Canadian study that did not meet our inclusion criteria found total TFAs in human milk decreased over time, from 7.1 grams 60.32 grams per 100 grams in 1998 to 4.6 grams 60.32 grams per 100 grams in 2006. This suggests that lactating women had reduced their intake, although dietary information was not collected and it is not clear whether the reduction was directly attributable to the mandate itself, arose from other factors such as better information and consumer awareness, or was part of a general population-wide trend.47 No study assessed whether reformulation included wider changes, for example to sugar or salt levels, which could be a potential concern, because there is related evidence that low-fat versions of processed foods that target dieters appear to be higher in salt and sugar than are the original products they replace.48 Furthermore, no study evaluated whether

reformulation may have increased consumption of the reformulated foods. Reformulation and the resulting “TFA free” labels may provide these products with a health halo, leading some consumers to increase their intake in the belief that they are selecting healthy options.49 We were not able to establish the absolute costs of artificial TFA controls or what the relative costs would be compared with alternative approaches to changing diets. The example of a price premium for margarines labeled lower in artificial TFAs suggests that some types of controls may exacerbate health inequalities across socioeconomic groups if those with lower incomes consider a premium product unaffordable. Although efforts to control artificial TFAs are important, they remain only 1 aspect of a comprehensive strategy to influence healthy eating.

all types of food for sale. This suggests that a mix of policies to target different sources may be necessary to substantially reduce artificial TFAs in the food supply or eliminate them altogether. j

Human Participant Protection About the Authors Vivien L. Hendry, Pablo Monsivais, Sara E. Benjamin Neelon, Simon J. Griffin, and David B. Ogilvie are with the UK Clinical Research Collaboration Centre for Diet and Activity Research, University of Cambridge School of Clinical Medicine, Cambridge, UK. Eva Almíron-Roig and Susan A. Jebb are with the Medical Research Council Human Nutrition Research, Cambridge, UK. Correspondence should be sent to Vivien L. Hendry, Behaviour and Health Research Unit, Forvie Site, University of Cambridge School of Clinical Medicine, Box 113, Cambridge Biomedical Campus, Cambridge CB2 0SR, UK (e-mail: [email protected]. ac.uk). Reprints can be ordered at http://www. ajph.org by clicking the “Reprints” link. This article was accepted September 28, 2014.

Contributors Conclusions This systematic review has demonstrated that when artificial TFAs are restricted, their general availability in the food supply decreases within the specific jurisdiction. There was insufficient evidence to determine which of 2 alternative strategies, maximum level limits or mandatory regulation for limiting use of artificial TFAs, was more effective. The approaches we examined tended, with the unique exception of Denmark, to focus on different and not necessarily overlapping sources of artificial TFAs. Labeling has been attached to packaged and pre-prepared foods, whereas maximum limits differed by national or local jurisdictions; locally mandated maximum limits such as those in New York dealt predominantly with foods eaten away from home, and only Denmark’s nationally mandated limit encompassed

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We acknowledge our colleague Alvaro Ullrich for creating and maintaining the database. Note. The views expressed in this article are solely those of the authors. S. A. J. is the chair of the Public Health Responsibility Deal Food Network.

V. L. Hendry planned the study; collected, analyzed, and synthesized the data; and wrote the article. E. AlmíronRoig, P. Monsivais, S. A. Jebb, and S. J. Griffin contributed to study planning. E. Almíron-Roig, P. Monsivais, and S. E. Benjamin Neelon assisted in data collection, analysis, and synthesis. E. Almíron-Roig, P. Monsivais, S. A. Jebb, S. E. Benjamin Neelon, and D. B. Ogilvie contributed to the writing of the article. S. A. Jebb, S. E. Benjamin Neelon, and S. J. Griffin assisted in data synthesis. D. B. Ogilvie supervised the study planning and assisted in data collection and analysis.

Acknowledgments Funding from the British Heart Foundation, Cancer Research UK, Economic and Social Research Council, Medical Research Council, the National Institute for Health Research, and the Wellcome Trust, under the auspices of the UK Clinical Research Collaboration, is gratefully acknowledged. The work was undertaken by the Centre for Diet and Activity Research, a UK Clinical Research Collaboration Centre Public Health Research Centre of Excellence, and by the UK Medical Research Council (Programme U105960389). The review was registered with Prospero (http://www.crd. york.ac.uk/PROSPERO; registration number CRD42013002998).

No protocol approval was required because the data were obtained from secondary sources.

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