Systematic Review of the Effect on Caries of Sugars Intake: Ten-Year Update

Abstract

An update of the systematic review of evidence on the association between amount of sugars intake and dental caries, as well as on the effect of restricting sugars intake to <10% and <5% energy (E) on caries, was conducted, almost 10 y since the review that informed the World Health Organization (WHO) Guideline on Sugars. The aim was to systematically review epidemiological data published from 2011 to 2020 on the amount of sugars consumption and levels of caries and to report the findings for adults and children. Data sources included MEDLINE, EMBASE, Cochrane Database, Cochrane Central Register of Controlled Trials, Latin American and Caribbean Health Sciences, China National Knowledge Infrastructure, Scopus, and Google Scholar. Eligible studies reported the amount of sugars and caries, measured as prevalence, incidence, or severity. The review was conducted in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses statement. Risk of bias was assessed using the Office of Health Assessment and Translation tool. Vote counting and harvest plots provided the basis for evidence synthesis. From 488 new papers identified, 23 studies were eligible: 4 cohort, 1 case-controlled, 12 cross-sectional, and 6 ecological. Eleven of 15 studies in children and 6 of 8 studies in adults reported at least 1 positive association between sugars and caries. Six of 7 studies in children and 4 of 4 studies in adults, with data enabling comparison of caries levels with sugars intakes >10%E and <10%E, showed lower caries when sugars intake was <10%E. Amalgamating with original studies yielded 64 of 78 studies showing at least 1 positive association, 20 of 78 a null association, and 3 of 78 a negative association between sugars and caries. GRADE profiles of new and original cohort data confirmed “moderate-quality” evidence that caries is lower when sugars intake is <10%E. Furthermore, new cohort data upgraded the quality of evidence (from “very low” to “low”) for lower caries when free sugars are <5%E. The findings support and strengthen original evidence underpinning the WHO recommendations for sugars.

Keywords

nutrition policy oral health sucrose carbohydrates adult child

Introduction

The World Health Organization (WHO 2015) published its Guideline on Sugars Intake for Adults and Children, which was based on comprehensive systematic reviews of evidence. The underpinning systematic review on amount of sugars intake and risk of dental caries (Moynihan and Kelly 2014) included data published between 1950 and 2011. Based on moderate evidence, a strong recommendation was made to limit the intake of free sugars to <10% energy intake (E). Furthermore, based on very low-quality evidence, a conditional recommendation was made to limit the intake of free sugars to <5%E. The WHO guideline and the underpinning systematic review highlighted the need for more research pertaining to the relationship between sugars intake and risk of caries in adults, as well as on the impact of interventions to reduce sugars intake on caries risk. Ten years since the original review, the aim of this article is to report an update of the systematic review to include all data published between 2011 and 2020 pertaining to the relationships between the amount of sugars consumption and levels of dental caries and to report the findings for both adults and children.

The review was based on the original research questions previously developed by the WHO Nutrition Guideline Advisory Group (NUGAG) Subgroup on Diet and Health (WHO 2015), which related to the effect on caries of increasing or decreasing free sugars intake and of restricting free sugars intake to <10%E and <5%E (Table 1). This enabled consideration of any impact of new data on the original balance of evidence pertaining to the relationship between sugars and risk of caries and current recommended thresholds.

Table 1.

Review Questions and Corresponding Number of Studies with Data Addressing Each Question.

Review Question	Number and Type of Studies Identified
Question 1: What is the effect on dental caries of an increase/reduction in free sugars intake in adults?	Total studies: 8
	Cohort: 2
	Cross-sectional: 5
	Ecological: 1
Question 2: What is the effect on dental caries of an increase/reduction in free sugars intake in children?	Total studies: 15
	Cohort: 2
	Case-controlled: 1
	Cross-sectional: 7
	Ecological: 5
Question 3: What is the effect on dental caries of restricting sugars intake to below 10% energy to reduce risk of dental caries in adults?	Total studies: 4
	Cohort: 1
	Cross-sectional: 2
	Ecological: 1
Question 4: What is the effect on dental caries of restricting sugars intake to below 10% energy to reduce risk of dental caries in children?	Total studies: 7
	Cohort: 2
	Cross-sectional: 4
	Ecological: 1
Question 5: What is the effect on dental caries of restricting sugars intake to below 5% energy to reduce risk of dental caries in adults?	Total studies: 1
	Cohort: 1
Question 6: What is the effect on dental caries of restricting sugars intake to below 5% energy to reduce risk of dental caries in children?	Total studies: 5
	Cohort: 1
	Cross-sectional: 3
	Ecological: 1

Methods

The protocol for the update review was registered on PROSPERO (CRD42018086384) (Kelly et al. 2018). The systematic review was conducted and reported according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) 2020 statement (Page et al. 2021).

Eligibility Criteria

Studies eligible for inclusion were intervention or observational studies, including randomized and nonrandomized controlled studies, quasi-experimental studies, cohort, case-control, cross-sectional, and ecological studies published since November 2011. Reviews were eligible if they contained a new analysis of data not considered in the original review. Unpublished studies or non–peer review articles (e.g., theses, abstracts, and preprints) were excluded.

Information Sources

Seven databases were searched: Cochrane Database of Systematic Reviews, Cochrane Central Register of Controlled Trials (CENTRAL), China Academic Journals Full Text database (CJFD) via China National Knowledge Infrastructure (CNKI), EMBASE (Ovid/Elsevier), Google Scholar, LILACS (Latin American and Caribbean Health Sciences), Medline (Ovid), and Scopus (Elsevier). Databases searched in the original review but excluded from the update included the South African National Health Research Database (as no longer a database of publications) and Wanfang (as not available in English at the time of the searches).

Search Strategy

The search strategy applied in the original review (Moynihan and Kelly 2014) was used. Searches were executed in 2018 and repeated in July 2020 to retrieve publications from November 2011 to July 2020.

Participants were healthy humans (without acute illness but could include those overweight or with hypertension or diabetes) in low-, middle-, or high-income countries. All age groups were included. No language restrictions were used.

Studies were included if they reported any intervention intended to alter sugars intake in 1 study arm compared with diet with a different sugars content in another study arm, and they also included information on dental caries; change in caries prevalence, incidence, and/or severity; or comparisons of higher versus lower caries as an outcome, with a time scale of at least 1 y. Observational studies were included if they reported absolute sugars or change in sugars intake and included information on dental caries. All time scales were included.

Sugars included total sugars (and any component of)—that is, total, free, non-milk extrinsic, added sugars, or mono- and disaccharides, expressed as g or kg/d or /y or as a percentage of E or per-capita population intake/availability. Studies that reported solely on the frequency of sugars consumption were excluded.

Dental caries outcomes included caries prevalence, incidence, and/or severity, measured as indices (e.g., DMF, DMFT, dmft, DMFS, dmfs, deft, dft) or comparisons between caries and no caries or higher caries versus lower caries rates.

Study Selection

Titles and abstracts of search results were initially screened in duplicate to exclude studies outside the scope of the review. Abstracts not in English were translated using Google Translate for title/abstract screening. Potentially eligible papers underwent full-text review by independent duplicate assessment for inclusion. Articles not published in English were screened by the authors for eligible data, translating methods text as required. Articles written in Chinese (n = 20) were screened by a Chinese researcher. Differences between reviewers’ results were resolved by discussion. Data were extracted by 1 author, using the data collection form from the original review and checked by a second author. Data extracted included study population (country, sample size, age, gender), type of sugars exposure, and dietary assessment method, dental indices, information on confounders/modifiers of the sugars–caries relationship (e.g., socioeconomic status, fluoride exposure, oral hygiene), completion rate, statistical analysis, and funding source.

Risk of Bias

Risk of bias (RoB) of included new studies was assessed using the National Toxicology Program Office of Health Assessment and Translation (OHAT) tool (Division of the National Toxicology Program 2015). Studies were classified into 3 tiers, where tier 1 is low, tier 2 is moderate, and tier 3 high RoB (Appendix Table 1) based on a previously applied method (EFSA [European Food Safety Authority] 2021). RoB of cohort studies identified in the original review was reassessed using OHAT.

Synthesis Methods for New Data

Evidence was organized by study type/design and grouped according to the review questions (Figure 1 and Table 1). Evidence synthesis was conducted using a vote counting method that is suited to data from a heterogeneous group of studies (McKenzie and Brennan 2019). The vote counting approach weighed the evidence (number of studies) showing a positive relationship between exposure and outcome against that showing a null or negative association. Data were formulated into harvest plots to summarize study characteristics, including study type, RoB, and the weight of evidence (number of studies showing positive, no, or negative direction of effect) in relation to specific questions (Ogilvie et al. 2008).

Figure 1.

Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram.

Where a study reported more than 1 outcome with respect to a research question (e.g., different countries) showing contrasting effects, separate data points were used to depict both outcomes in the harvest plot. This approach was supplemented with a narrative synthesis of findings based on a “best available evidence” approach (Petticrew and Roberts 2006) that considers the best evidence in terms of study design to answer each question but with a lower level of relevant evidence still being considered for inclusion.

Process for Combining Original and New Data

The overall balance of data pertaining to a positive, null, or negative impact on caries of changing sugars intake from both original and new studies was considered using a vote counting approach. Using the best available data based on study design, new data were amalgamated with original data for GRADE profile analysis of the evidence pertaining to any effect on caries of restricting free sugars intake to <10%E and <5%E.

Results

Study Selection

Figure 1 presents the PRISMA flow diagram. From all databases combined, 4,629 unique new records were identified, following deduplication. Following title and abstract screening, 488 papers were retained for full-text review. Following full-text review, 23 new studies were included and 464 excluded. Reasons for exclusions are provided in Figure 1 and Appendix Table 2. Amalgamating the original and new searches resulted in a total of 78 papers published from 1950 to 2020, with data pertaining to amount of sugars and dental caries. Table 2 provides a summary of included new studies and assigned RoB tiers. Details on OHAT categories for each new study are given in Appendix Table 1. Data extraction forms for new studies are available in Appendix Table 3.

Table 2.

Summary of Included Studies: Characteristics and Exposure/Outcome Relationship: Positive (+), Neutral (0), or Negative (−).

Author (Year)	Country	n/Age^a	Sugars Exposure	Diet Assessment Method	Dental Outcome Measure	+/0/−^b	RoB Tier/Review Question Addressed^c
Studies of adults
Cohort studies
Bernabé et al. (2016)	Finland	n = 1,702Mean (SD) 47.6 (11.4) y	Total sugars	FFQ	DMFT	+	Low RoBQ1, Q3, Q5
Kaye et al. (2015)	United States	n = 53347–90 y	Sum of sucrose, fructose, and lactose	FFQ	Root caries (adjusted root caries increment)	0	High RoBQ1
Cross-sectional studies
Barrington et al. (2019)	Australia	n = 4,17015–91 y	Added sugars	Questionnaire on habitual intake of high sugar items	DMFT	+	Moderate RoBQ1
Christensen et al. (2015)	Denmark	n = 3,21254 (21–89) y	Total sugars; added sugars; sucrose	Internet-based semiquantitative food questionnaire (based on frequency recalled over past year)	Active root caries and restored root surfaces (fillings or crowns)	0	High RoBQ1
Kaye et al. (2020)	United States	n = 7,751Mean (SD) 47.4 (0.5) y	Added sugars	2 × 24-h recalls	Number of untreated coronal caries) visual assessment	+	Moderate RoBQ1, Q3
Rosier et al. (2017)	Netherlands	n = 26818–32 yMean (SD) 22.6 (2.6) y	Total sugars	FFQ	DMFS (ICDASx; ICDASvi)	+	Moderate RoBQ1
Saw et al. (2012)	Malaysia	n = 16820–59 y	“Sugar”	Multiple-pass 24-h recall	DMFT (WHO criteria)	+	High RoBQ1, Q3
Ecological studies
Sheiham and James (2014)	United Kingdom	Aged 20+ y	Sucrose	Per-capita availability from FAO	DMFT	+	High RoBQ1, Q3
Studies of children
Cohort studies
Devenish et al. (2020)	Australia	n = 9652–3 y	Free sugars	24-h recall and 2-d food record at age 1 y, FFQ at age 2 y	Incidence of ECC (based on NIDCR and ICDAS methods)	+	Low RoBQ2, Q4, Q6
Karjalainen et al. (2015)	Finland	n = 142 baseline (age 3 y) followed up to age 16 yn = 79	Sucrose	4-d food diary	D₃MFT/d₃mft (WHO criteria)	+	Moderate RoBQ2, Q4
Case-controlled studies
Evans et al. (2013)	United States	n = 381 with S-ECC, n = 427 caries free	Added sugars	FFQ	Severe ECC (3+ smooth surface plus 1+ pulpal)	+	Moderate RoBQ2
Cross-sectional studies
Chi et al. (2015)	United States	n = 516–17 y	Hair-based biomarker of corn and cane sugars	NA	Percent dmfs/DMFS (WHO criteria)	+	Moderate RoBQ2
Goodwin et al. (2017)	United Kingdom	n = 12812–13 y	Free sugars	3-d food diary	DMFT, with a threshold of ICDAS 4	0	High RoBQ2
Kaur et al. (2015)	Malaysia	n = 3127–11 y	Sucrose	Questionnaire on frequency and amount of high sugars foods and drinks in the past week	Dmft (WHO criteria)	0	High RoBQ2
Mitrakul et al. (2016)	Thailand	n = 1006–12 y	Total sugars	3-d dietary recall	DMFT (WHO criteria)	0	High RoBQ2, Q4, Q6
Palacios et al. (2016)	Puerto Rico	n = 72312 y	Total sugars	24-h recall	DT (decayed component of DMFT) NIDCR method	+	Low RoBQ2, Q4
Rego et al. (2020)	Brazil	n = 40612 y	Free sugars	FFQ	DMFT indexPUFA index	+	Moderate RoBQ2, Q4, Q6
Saido et al. (2016)	Japan	n = 5,1585–6 y	Free sugars	Diet history questionnaire	Parent/carer reported decayed and filled teeth	+	Moderate RoBQ2, Q4, Q6
Ecological studies
Davies et al. (2017)	England	NR0–5 y	Nonmilk extrinsic sugars g/d and %E	Data from national surveys	Caries prevalence and dmft count from dental surveys over same period (BASCD methods)	0	Moderate RoBQ2
Macigo et al. (2016)	Kenya	3–15 y	Sucrose	Per-capita availability	Dmft/DMFT index (WHO criteria)	+ dmft/+ DMFT	High RoBQ2, Q4
Masood et al. (2012)	73 countries	12 y	UNFAO “sugar and sweeteners” category (i.e., sucrose, glucose, honey, HFCS)	Per-capita availability	DMFT (WHO criteria)	− HIC/+ LMIC	High RoBQ2
Mukouyama et al. (2018)	Japan	n = 3,000/y5–15 y	Added sucrose	From Japanese national health and nutrition survey; method NR	DMFT	+	High RoBQ2
Olczak-Kowalczyk et al. (2016)	Poland	n = 185–919/survey year12 y	Sucrose	Per-capita availability	DMFT/caries prevalence (WHO criteria)	+	Moderate RoBQ2

BASCD, British Association for the Study of Community Dentistry; DMFT/dmft, decayed, missing, and filled permanent teeth (uppercase) and primary teeth (lowercase); D₃MFT/d₃mft, decay affecting dentine layer, missing and filled teeth; E, energy; ECC, early childhood caries; FAO, Food and Agricultural Organization; FFQ, food frequency questionnaire; HFCS, high fructose corn syrups; HIC, high-income countries; ICDAS, International Caries Detection and Assessment System; ICDASvi, International Caries Detection and Assessment System (visual assessment); ICDASx, International Caries Detection and Assessment System (by radiograph); LMIC, low- and middle-income countries; NA, not applicable; NIDCR, National Institute for Dental and Craniofacial Research; NR, not reported; PUFA, pulpal ulceration fistula abscess; Q, question; RoB, risk of bias; S-ECC, severe early childhood caries; UNFAO, United Nations Food and Agricultural Organization; WHO, World Health Organization.

Ages are listed as reported. If an age range is reported, the lower and upper limits are listed by a dash (−); if a mean is reported, that is indicated; if more than 1 age cohort is reported, the ages of each cohort are listed separated by a forward slash (/).

The + indicates a positive and significant relationship between sugars and dental caries, 0 indicates no significant relationship, and − indicates a negative and significant relationship. If results are reported for separate cohorts within the same study, all relationships are listed and separated by a forward slash (/).

RoB was assessed using the Office of Health Assessment and Translation tool: low = tier 1, moderate = tier 2, and high = tier 3.

Characteristics of New Studies

Fifteen studies had data from children and 8 from adults (of which 1 included participants aged 15–91 y). No randomized controlled trials (RCTs) or quasi-experimental studies were identified. Of the included studies, 4 were prospective cohorts, 1 was case-controlled, 12 were cross-sectional, and 6 were ecological studies. Studies were from Australia (n = 2), Brazil (n = 1), Denmark (n = 1), Finland (n = 2), Japan (n = 2), Kenya (n = 1), Malaysia (n = 2), Netherlands (n = 1), Poland (n = 1), Puerto Rico (n = 1), Thailand (n = 1), United Kingdom (n = 3), United States (n = 4), and multiple countries (n = 1).

Sugars exposure was measured by many different methods, including food frequency questionnaire (FFQ) (n = 5), other questionnaire (n = 4), food diary (n = 3), multiple (n = 2) or single (n = 1) 24-h recall, combination of methods (n = 1), per-capita availability (n = 4), national survey data (n = 2), and an added sugars biomarker (n = 1). The terminology used for reporting sugars varied, but most studies reported free sugars (WHO 2015) or a component of free sugars (e.g., sucrose or added sugars). Four studies reported total sugars (added sugars plus sugars in whole fruits, vegetables, grains, milk) (Bernabé et al. 2016; Mitrakul et al. 2016; Palacios et al. 2016; Rosier et al. 2017).

Due to methodological heterogeneity between studies, it was not appropriate to synthesize data using meta-analysis (Aromataris and Munn 2020). This was because of disparity in the reporting of outcomes (e.g., odds ratios, caries counts, proportion affected, continuous data), the RoB tier, participant age range, length of follow-up, the sugars measure, and differences in reporting and accounting for factors that modify the sugars–caries relationship (e.g., fluoride). Moreover, some studies compared caries between higher versus lower categories of sugars intake, and others compared sugars intake between higher versus lower caries groups. The dental outcome measures reported also varied across studies (dmfs, d₃mft, dft, dmft, severe early childhood caries, DMFT, % caries, caries incidence). Evidence synthesis was therefore conducted by vote counting and harvest plots. Effect size of individual studies is presented in Appendix Table 3.

Overall Findings

Overall, 17 of 23 new studies showed at least 1 positive association between amount of sugars and dental caries (Masood et al. 2012; Saw et al. 2012; Evans et al. 2013; Sheiham and James 2014; Chi et al. 2015; Karjalainen et al. 2015; Bernabé et al. 2016; Macigo et al. 2016; Olczak-Kowalczyk et al. 2016; Palacios et al. 2016; Saido et al. 2016; Rosier et al. 2017; Mukouyama et al. 2018; Barrington et al. 2019; Devenish et al. 2020; Kaye et al. 2020; Rego et al. 2020). Of these, 5 studies were classified as high RoB (see Table 2, Figure 2). Six studies reported at least 1 null association (Christensen et al. 2015; Kaur et al. 2015; Kaye et al. 2015; Mitrakul et al. 2016; Davies et al. 2017; Goodwin et al. 2017), of which 5 were classified as high RoB. One study (high RoB) reported a negative association between sugars intake and caries for high-income countries only (Masood et al. 2012).

Figure 2.

Harvest plot to illustrate weight of evidence for positive or negative effect of intake of sugars on dental caries in adults (question 1) and children (question 2). Height of bar represents study quality: 3 blocks = low risk of bias (RoB), 2 blocks = moderate RoB, and 1 block = high RoB, based on the Office of Health Assessment and Translation tool (details of individual studies provided in Appendix Table 1).

Question 1: What is the effect on dental caries of a reduction/increase in free sugars intake in adults?

The best available new evidence (based on study design) was provided by 2 cohort studies; 1 study (low RoB) reported a positive linear relationship between sugars intake and caries development (Bernabé et al. 2016). The other, rated high RoB, reported no association (Kaye et al. 2015). Figure 2 presents the evidence synthesis of all new data pertaining to dental caries in adults (question 1), which considered both study design and RoB. Six of 8 studies in adults reported a positive association between sugars intake and caries (Saw et al. 2012; Sheiham and James 2014; Bernabé et al. 2016; Rosier et al. 2017; Barrington et al. 2019; Kaye et al. 2020). Both studies that did not report an association were rated high RoB (Christensen et al. 2015; Kaye et al. 2015).

In the original review, 5 of 5 studies in adults reported a positive association between sugars intake and caries. Amalgamating these data with the new studies, the overall body of evidence shows 11 of 13 studies in adults report a positive association between amount of sugars and caries levels.

Question 2: What is the effect on dental caries of a reduction/increase in free sugars intake in children?

Based on study design, the best available evidence was provided by 2 cohort studies both reporting a positive association (1 low and 1 moderate RoB). Figure 2 presents the evidence synthesis of data for children. Eleven of 15 studies reported at least 1 positive association between amount of sugars and dental caries, of which 3 were rated high RoB. Three of the 4 studies showing no association, and the 1 study reporting a negative association, had a high RoB.

In the original review, 43 of 51 studies reported at least 1 positive association between amount of sugars and caries, 14 studies reported at least 1 null association, and 2 reported at least 1 negative association. Amalgamating these data with the new studies, the overall body of evidence shows 54 of 66 studies in children report at least 1 positive association, 18 of 66 studies report no association, and 3 of 66 studies report at least 1 negative association between sugars intake and caries.

Question 3: What is the effect on dental caries of restricting free sugars intake to <10% of energy intake in adults?

The best available evidence came from the 1 cohort study (low RoB) that had data enabling the comparison of caries development when sugars intake was equivalent to >10%E compared with <10%E (Bernabé et al. 2016) showing lower dental caries with intakes <10%E. This finding was supported by the next level of evidence, 2 cross-sectional studies (1 moderate and 1 high RoB), both showing lower caries when sugars intake was <10%E (Saw et al. 2012; Kaye et al. 2020). Details of the studies that provided data pertaining to question 3 are presented in Table 3 and Figure 3. There were no relevant data from adults in the original review to explore the 10%E threshold.

Table 3.

Summary of Studies with Data Pertaining to 5%E and 10%E Thresholds for Free Sugars Intake.

Author (Year) and RoB Tier^a	Population	Supports <5%E/<10%E from Sugars	Summary of Evidence
Cohort studies
Bernabé et al. (2016) Low RoB	Adults aged 30–89 y	<5%<10%	Analysis that explored the shape of the relationship between total sugars intake and DMFT increment using longitudinal data from 1,702 adults aged 30–89 y, who participated in at least 2 of 3 oral health surveys in Finland (up to 11 y follow-up). Analysis controlled for confounders and modifying factors (SES, sex, age, education, toothbrushing frequency, dental attendance, use of fluoride toothpaste, and sugars frequency). A linear dose response was found between sugars intake (from 13.7 g/d [~2% EI] to 442 g/d) and caries increment. For every 10-g/d sugars intake, DMFT increased by 0.09 (95% CI, 0.02–0.15), P = 0.14. Analysis therefore supports lower caries when sugars intake is below 10%E compared with >10%E and when <5%E compared with >5%E.
Devenish et al. (2020) Low RoB	Children aged 1–3 y	<5%	Study investigated dietary practices and dental caries in Australian preschool children. Intake of free sugars measured at 1 and 2 y and dental caries at 2–3 y. Multiple regression analysis generated PRs for the association between ECC and compliance with the WHO threshold for free sugars intake in 965 participants. After controlling for maternal education, SES, age at time for dental exam, and breastfeeding duration, those with free sugars intake of >10%E on both dietary assessments had significantly increased PR (1.97; 95% CI, 1.13–3.44) for caries compared with those who complied with the WHO threshold of <5%E from free sugars on both occasions.
Karjalainen et al. (2015) Moderate RoB	Children aged 3 y at baseline followed at 6, 9, 12, and 16 y	<10%	Study in which participants were dichotomized by sucrose intake (≥10%E and <10%E) at 3 y. Using GLM repeated measures, DMFT/dmft scores of the high-sucrose group (≥10%E) were significantly higher than those of the low-sucrose group (<10%E), P = 0.046. Difference was statistically significant at ages 9 and 16 y, when reported by age. HR for caries survival (percent caries free at end of follow-up or discontinued the study caries free) in <10%E sucrose versus ≥10%E sucrose was 1.22 (95% CI, 0.77–1.93) in relation to sucrose intake at age 3 y, and no significant differences were found in use of fluoride toothpaste between the sucrose intake groups at age 3, 6, 9, 12, or 16 y. Oral hygiene: No significant differences in toothbrushing habits at age 3, 6, 9, 12, or 16 y.
Cross-sectional studies
Kaye et al. (2020) Moderate RoB	Adults aged 20+ y	<10%	Analysis used data from the NHANES for adults aged 20+ y in the United States. The OR of having untreated coronal decay was derived for those adhering to an added sugars threshold of <6.5%E and those not. After controlling for age, gender, ethnicity, smoking, family income, education, and time since last dental visit, the OR for caries of those adhering to sugars threshold was 0.74 (95% CI, 0.58–0.93).
Saw et al. (2012) High RoB	Adults aged 20–59 y	<10%	Cross-sectional analysis of data from Malaysian adults aged 20–59 y. Compared the intake of added sugars between those that were caries free and those with caries. Added sugars intake was 35.2 (SD 20.6) g/d, equivalent to 9.3 (SD 5) %E in the caries-free group, compared with 45.9 (SD 27.1) g/d, equivalent to 11.9 (SD 6.3) %E in those with caries (P < 0.05). Analysis was not controlled for confounding. Analysis supports lower caries when intake of sugars is <10%E.
Palacios et al. (2016) Low RoB	Children aged 12 y	<10%	Cross-sectional study of children (n = 723) aged 12 y from Puerto Rico. Total sugars measured (which was close to WHO free sugars definition as intake of whole fruits and vegetables was very low). In a regression model that controlled for key modifying factors, including oral hygiene habits, children with ≥10%E from total sugars: OR for caries was 3.76 (95% CI, 1.03–13.7).
Saido et al. (2016) Moderate RoB	Children aged 5–6 y	<5%<10%	Cross-sectional study that examined the appropriateness of the WHO recommendation to limit free sugars to <5%E using data from 5,158 Japanese children aged 5–6 y. Participants were categorized into quintiles of free sugars intake with Q1 (<4.88%E from free sugars) the reference. Analyses were controlled for factors significantly associated with caries in bivariate analysis, including education of mother, frequency of toothbrushing, and residential area. Compared with the reference, those consuming between 7.89%E and 10%E from free sugars had an increased risk of caries of 1.28 (1.10–1.37), P < 0.05. Those consuming >10%E from free sugars had higher dental caries of 1.55 (95% CI, 1.44–1.66) than those consuming <5%E from free sugars.
Mitrakul et al. (2016) High RoB	Children aged 6–12 y	<5%<10%	Cross-sectional study of 100 Thai children that examined relationship between sugars intake (not defined) and DMFT using Spearman’s correlation. Bivariate analysis reported no association was found between amount of sugar consumed/d and DMFT (Spearman’s correlation: R = −0.128; P = 0.205) over intakes ranging from 0 to over 140 g, thus not supporting lower caries with intakes below 10% or 5% (crude analysis based on graphical data).
Rego et al. (2020) Moderate RoB	Children aged 12 y	<10%<5%	Brazilian children (n = 406) aged 12 y. Relationship between DMFT, decayed teeth (D), and PUFA and daily and annual free sugars intake assessed, and dose response reported. With a free sugars intake <10 kg/y (~5%E), mean (SD) D = 0.57 (1.10) and PUFA = 0.11 (0.42).With a free sugars intake 10–15 kg (<10%E), mean (SD) D = 0.86 (1.25) and PUFA = 0.24 (0.64).With a free sugars intake >15 kg/y, mean (SD) D = 0.90 (1.58) and PUFA = 0.30 (0.75).With a free sugars intake <25 g/d (~5%E), mean (SD) D = 0.67 (1.24) and PUFA = 0.19 (0.51).With free sugars intake 25–50 g/d (<10%E), mean (SD) D = 0.75 (1.20) and PUFA = 0.29 (0.63).With free sugars intake >50 g (>10%E), mean (SD) D = 0.92 (1.61) and PUFA = 0.29 (0.75).
Ecological studies
Sheiham and James (2014) High RoB	Adults aged 20+ y	<10%	Presents new analysis of data on DMFT from adults from 9 national dental surveys in Japan from 1957 to 2005 showing the increase in DMFT with age and links DMFT data to FAO sucrose intake data of 7%E in 1961, increasing to 11.2%E in 1985 and 9.6%E in 2005, showing higher DMFT in the mid-1980s compared with the early 1960s.
Macigo et al. (2016) High RoB	Children aged 3–15 y	<10%	Analysis of data from children aged 3–15 y in Kenya from published dental surveys that used WHO criteria for caries assessment. Compared with sucrose availability data from 1969 to 2009. Trends in dmft/DMFT followed trends in sucrose availability. Increase in per-capita sucrose availability from 35.5 g/d (<10%E) in 1969 to 60.8 g/d (>10%E) in 1989 then dropped again to 44.7 in 2009.In children aged 3–5 y, dmft/dft index increased from 1.5 in studies from the 1980s to 2.5 in studies after 2000.In 12-y-old children, DMFT increased from 0.2 in 1984 to 0.51 in 1986 to at least 0.92 after 2000 (another study reported 2.40).

CI, confidence interval; DMFT/dmft, decayed, missing, and filled permanent teeth (uppercase) and primary teeth (lowercase); E, energy; ECC, early childhood caries; EI, energy intake; FAO, Food and Agricultural Organization; GLM, general linear model; HR, hazard ratio; NHANES, National Health and Nutrition Examination Survey; OR, odds ratio; PR, prevalence ratio; PUFA, pulpal ulceration fistula abscess; Q, question; RoB, risk of bias; SD, standard deviation; SES, socioeconomic status; WHO, World Health Organization.

RoB was assessed using the Office of Health Assessment and Translation tool: low = tier 1, moderate = tier 2, and high = tier 3.

Figure 3.

Harvest plot to illustrate weight of evidence showing lower dental caries with sugars intakes below 10% energy (E) against evidence not showing lower dental caries with sugars intake below 10%E, in adults (question 3) and children (question 4). *Studies with additional evidence pertaining to <5%E from free sugars intake threshold (questions 5 and 6). Height of bar represents study quality: 3 blocks = low risk of bias (RoB), 2 blocks = moderate RoB, and 1 block = high RoB, based on the Office of Health Assessment and Translation tool (details of individual studies provided in Appendix Table 1).

Question 4: What is the effect on dental caries of restricting sugars intake to <10% of energy intake in children?

The best available evidence to address this question came from 2 cohort studies with data enabling comparison of caries development when free sugars intake was <10%E compared with >10%E: both showed lower caries when intake was <10%E (neither rated high RoB) (Karjalainen et al. 2015; Devenish et al. 2020). The next level of evidence came from 4 cross-sectional studies that had data enabling the comparison of caries when sugars intake was >10%E compared with <10%E: 3 studies reported lower caries with sugars intake <10%E (Palacios et al. 2016; Saido et al. 2016; Rego et al. 2020), and 1 study (Mitrakul et al. 2016), rated high RoB, showed no association (Figure 3, Table 3).

In the original review, 5 cohort studies had data comparing levels of caries >10%E and <10%E from sugars. Amalgamating these with the newly identified cohort studies gave a total of 7 cohort studies all showing lower levels of caries with sugars intake <10%E.

Question 5: What is the effect on dental caries of restricting free sugars intake to <5% of energy intake in adults?

The only available data on adults came from 1 cohort study (low RoB) with data supporting lower dental caries with sugars intake equivalent to <5%E (Bernabé et al. 2016). There were no data from adults in the original review to explore the 5%E threshold.

Question 6: What is the effect on dental caries of restricting sugars intake to <5% of energy intake in children?

The best available data came from 1 cohort study (low RoB) that had data that enabled comparison of caries development when free sugars was <5%E with >5%E and showed lower caries with intakes <5%E (Devenish et al. 2020). This was supported by 2 cross-sectional studies (moderate RoB), showing lower caries with sugars intake <5%E (Saido et al. 2016; Rego et al. 2020). One cross-sectional study (high RoB) had graphically presented data that did not support lower caries when total sugars intake was equivalent to <5%E (Mitrakul et al. 2016) (Figure 3, Table 3). The original review did not identify any cohort or cross-sectional data, with the best available data from 3 ecological studies all showing lower caries with sugars <5%E.

GRADE Profile Analysis

In line with the original review, data from cohort studies (best data in terms of study design) enabling comparison of development of caries with sugars intake >10%E with <10%E underwent GRADE profile analysis. Data from the original and updated review were combined for this purpose and showed the body of evidence pertaining to the effect on caries of restricting free sugars to <10%E was of “moderate” quality (Appendix Tables 4 and 5). A GRADE profile assessment of the cohort data (low RoB) was rated “low” quality for lower caries with free sugars intake <5%E, which for children was supported by data from 2 of 3 cross-sectional studies (both moderate RoB) (Appendix Tables 6 and 7).

Discussion

The WHO recommendation (WHO 2015) to limit free sugars to <5%E was a “conditional recommendation” underpinned by “very low” quality data from ecological studies with high RoB due to inability to control for modifying factors (e.g., fluoride) and crude assessment of sugars exposure (Moynihan and Kelly 2014). This updated systematic review has identified better quality data from well-designed cohort studies with low RoB to support the <5%E threshold for sugars intake. The updated information on the impact of amount of sugar consumed on the development of dental caries will help inform whether sugar taxes are a cost-effective means of caries prevention as part of the WHO Global Oral Health Strategy (WHO 2021).

This update of the systematic review of the effect on caries of amount of free sugars intake showed that most data (17/23 studies) indicate that increasing free sugars intake increases caries risk and that limiting free sugars intake to <10%E and to <5%E lowers caries risk. Moreover, excluding data from studies rated high RoB strengthened the balance of data in support of these WHO recommended thresholds: all data pertaining to the effect on caries of limiting free sugars intake to <10%E or <5%E not deemed to be high RoB supported the WHO thresholds.

Effect of Fluoride on the Sugars–Caries Relationship

Higher development of dental caries with sugars >10%E was observed despite exposure to fluoride. In 1 cohort study of children, participants were exposed to fluoridated water (Devenish et al. 2020), and another cohort reported uniform toothbrushing habits and exposure to fluoridated toothpaste between sugars intake groups (Karjalainen et al. 2015). Moreover, in the adult cohort, analysis showed that the use of fluoride toothpaste reduced but did not eliminate the linear dose response between sugars intake and caries (Bernabé et al. 2016). In support of an independent effect of limiting sugars intake and an additive effect of both limiting sugars and optimizing fluoride exposure, Ha et al. (2021) recently reported a combined effect of lack of fluoride exposure and high sugars led to greater caries risk than if there was no interaction.

Research Requirements

The original systematic review (Moynihan and Kelly 2014) highlighted the need for more data from adults, having identified only 5 studies of adults. This update identified data from a further 8 studies, but only 2 were cohort studies, of which only 1 did not have serious RoB. Consequently, there remains a need for more data from well-designed cohort studies in adults. The original review also identified a need for data on the impact of interventions to reduce free sugars intake on caries development, yet in the current update, no such studies were identified. In the past 10 y, evidence for the effectiveness of several public health measures in reducing sugars intake, for example, reformulation (Hashem et al. 2019) and fiscal measures (Colchero et al. 2017), has been reported, including modeling scenarios of the impact of sugar-sweetened beverage taxes on dental caries (Alhareky 2021). However, research into the impact of behavior change interventions (aiming to lower the intake of foods and drinks high in free sugars) on dental caries outcomes is also needed.

A key issue in both the original and updated systematic review was the heterogenous nature in which sugars exposure is measured and reported, with some studies reporting total sugars (of which the majority is added), some added sugars, some free sugars, and some sucrose (as a proxy for added sugars). Such diversity in exposure measures complicates data analysis across studies. Future studies should aim to report both total and free or added sugars. Moreover, many studies were excluded from the synthesis based on the way that sugars were either measured or reported. Of the 488 studies that underwent full screen, 382 were excluded because an absolute measure of sugars intake was not reported (even when it would have been possible to report this based on the dietary assessment method used). In many studies, the dietary assessment methodology was poorly reported, validation of dietary data was not conducted or reported, or only the frequency of intake of selected sugars-containing foods and drinks was reported. To assess risk and set guidelines on levels of intake for free sugars, authoritative bodies rely on evidence relating the absolute amount of intake to the disease outcomes (e.g., dental caries). Such data help inform recommendations such as those of the WHO. Future prospective studies should use a method that enables the quantification of sugars (preferably both total and free or added sugars), in g/d and %E (to control for energy intake), and should include dietary assessment expertise in the research team. Future studies should also consider important confounding and modifying factors, including socioeconomic status, age, frequency of sugars intake, and fluoride exposure in statistical analyses.

Limitations

This review has some limitations. The characteristics of the included studies were too diverse to allow pooling of data for meta-analysis. Therefore, in contrast to the original review, which included “crude” meta-analysis, evidence synthesis was conducted using vote counting. Evidence synthesis by vote counting is suited to data from a heterogeneous group of studies (McKenzie and Brennan 2019) and enables the weighting between the body of evidence showing a positive relationship between exposure (sugars) and outcome (caries) with that showing a negative association. Moreover, depicting the evidence in harvest plots enabled a visualization of evidence weighting that accounted for RoB and study design. In the current evidence synthesis, because of the absence of RCTs with which to conduct funnel plots and limited possibility to combine data, publication bias was difficult to assess. In the original review, RoB was assessed as part of the GRADE process without using a specific tool. This update used the OHAT tool to assess RoB in new studies and original cohort studies, which increased objectivity.

In line with the original remit of the WHO guideline, which was to set recommended quantitative thresholds for sugars intake, this systematic review was not concerned with the effect on caries of frequency of sugars consumption. Most studies that have considered both variables have found amount of sugars to be more strongly related to caries than frequency of sugars intake (Rugg-Gunn et al. 1984; Burt et al. 1988; Rodrigues et al. 1999). Interestingly, a study identified in this review showed frequency of consumption was not significantly associated with caries after adjusting for the amount consumed, but amount of sugars remained significantly associated with caries after adjusting for frequency of intake (Bernabé et al. 2016). This suggests that prevention should focus on reducing amount of sugars consumed, whereas the traditional focus has been on frequency. Most included studies measured free sugars (or components of), but 4 studies measured total sugars only. However, free sugars account for most total sugars, except for populations consuming high amounts of milk (e.g., young children) or fruits and vegetables.

In the updated review, the best available evidence (based on study design) for the GRADE profile analyses of the quality of evidence pertaining to the effect on dental caries of limiting the intake of free sugars to below 5%E was based on only 1 cohort study in adults and 1 in children. However, this is an acceptable approach (Guyatta et al. 2011) and was supported by lower-level evidence from cross-sectional studies. Moreover, the new data enabled the quality of evidence supporting the <5%E threshold from free sugars to be upgraded from “very low” (the original GRADE profile) to “low.”

Conclusion

This update of the evidence pertaining to the impact on risk of dental caries of the amount of free sugars intake has shown that new data are consistent in supporting a positive relationship between amount of free sugars consumed and dental caries. New data from 3 cohort studies add to the body of evidence supporting lower dental caries with free sugars intakes <10%E. Moreover, new data from 2 cohort studies support and strengthen the evidence underpinning the recommendation to limit intake of free sugars to <5%E.

Author Contributions

C.J. Moores, contributed to the data analysis, helped to draft and critically revised the manuscript; S.A.M. Kelly, contributed to the conception, design, data analysis, critically revised the manuscript; P.J. Moynihan, contributed to the conception, design, and data analysis, drafted the manuscript. All authors gave final approval and agree to be accountable for all aspects of the work.

Supplemental Material

sj-docx-1-jdr-10.1177_00220345221082918 – Supplemental material for Systematic Review of the Effect on Caries of Sugars Intake: Ten-Year Update

Supplemental material, sj-docx-1-jdr-10.1177_00220345221082918 for Systematic Review of the Effect on Caries of Sugars Intake: Ten-Year Update by C.J. Moores, S.A.M. Kelly and P.J. Moynihan in Journal of Dental Research

Footnotes

Acknowledgements

The authors thank Dr. Xiangqun Ju for her assistance in screening Chinese full-text articles.

A supplemental appendix to this article is available online.

Declaration of Conflicting Interests

The authors declared the following potential conflicts of interest with respect to the research, authorship, and/or publication of this article: P.J. Moynihan is a member of the EFSA working group on added sugars and a member of the UK Governments Scientific Advisory Committee on Nutrition Subgroup on Maternal and Child Nutrition, providing advice on the evidence pertaining to dietary sugars and dental caries to both. The other authors have no competing interests to declare. The views expressed in this article are the authors’ own.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

ORCID iDs

C.J. Moores

S.A.M. Kelly

P.J. Moynihan

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