Anthropometric Measurements and Dental Caries in Children: A Systematic Review of Longitudinal Studies^,,

Abstract

There is growing interest in the association between anthropometric measurements and dental caries in childhood over time (life-course studies). The aim of this review was to identify and systematically review the evidence of the association between anthropometric measurements and dental caries in childhood over time. PubMed, Institute for Scientific Information (ISI) Web of Knowledge, the Cochrane Library, and 6 other databases were searched to identify effective articles. A systematic approach involving critical appraisal was conducted to examine the relation between anthropometric measurements and dental caries in preschool- and school-aged populations from longitudinal studies. An initial search identified 1338 studies, with 59 potentially effective studies (κ = 0.82) and 17 effective studies (κ = 0.88). The quality of reporting among the studies ranged from 19.5 to 30.0 according to the Strengthening the Reporting of Observational studies in Epidemiology (STROBE) criteria. Among the effective studies, 2 studies in which caries was used to predict anthropometric measurements consistently found an inverse association and 15 studies in which anthropometric measurements were used to predict caries were inconsistent, with results appearing to be influenced by nonuniformity of assessments, setting, and procedure of measurements; age and ethnicity of participants; and confounders of dental caries. In conclusion, among >1000 studies identified, 17 informed this systematic review. The quality of reporting of these studies varied considerably. Evidence of the association between anthropometric measurements and dental caries is conflicting and remains inconclusive.

Introduction

The individual growth of children and adolescence is influenced by both genetic and environmental factors (1). Many of these factors can give rise to dental caries; thus, growth/development and dental caries are thought to share a common pathogenesis in that nutrition, parenting, lifestyle, physical and social environments, as well as psychosocial factors influence both conditions (2). It has long been reported that dental caries and obesity coexist among children from families with lower income (3) and that high dental caries experience and high BMI share similar behavioral practices (4).

As one of the most prevalent diseases worldwide (5), dental caries is hypothesized to be a potential risk factor for general health. Positive associations between caries experience and children’s systemic health has been reported in several studies (6–8). Moreover, untreated dental decay is a neglected determinant of low BMI (9). It is also believed that treating dental caries can improve the growth rate and systemic health (10).

Anthropometry refers to “the measurement of the size, weight, and proportions of the human or other primate body” (11). It is widely accepted that anthropometric measurements are important indicators of children’s growth and development and are widely used because of their low cost, simplicity, and strong correlation with children’s nutritional status (12). Several anthropometric measurements are used as a proxy of a child’s nutritional state, such as BMI, weight for age, actual weight divided by the 50th percentile weight for age, and actual height divided by 50th percentile height for age (12).

Both childhood obesity and dental caries are public health concerns globally, and several systematic reviews examined the cross-sectional relation between anthropometric values (particularly BMI) and dental caries (13–15). For example, Kantovitz et al. (13) reported inconclusive associations and recommended further well-designed randomized studies to support or to refute their association. However, an updated systematic review undertaken by Hooley et al. (14) found a positive association when only studies involving normal-weight and overweight participants were included and concluded that dental caries was related with both high and low BMI in a U-shaped manner. A substantial positive association between dental caries and childhood obesity was also evident for permanent dentitions in a meta-analysis applying BMI as a standardized assessment of child obesity (15). However, to our knowledge, no systematic review has been attempted to establish the prospective association between anthropometric measures and dental caries.

There is a dearth of information on the long-term association between childhood obesity and dental caries, and no systematic review to date. The aim of this systematic review was to consider anthropometric measurements in its broadest sense (beyond simply BMI) and dental caries over time.

Methods

Search strategy and selection criteria.

We systematically searched the English-language literature to identify human studies examining the long-term association between anthropometric measurements and dental caries in children and adolescents. The review was restricted to longitudinal observational studies (cohort study, case-control study, or cross-sectional study nested in a cohort study). The initial search was conducted by using the following electronic bibliographic databases from their commencement to February 2014: PubMed, Institute for Scientific Information (ISI)⁶ Web of Knowledge, Cochrane Library, ProQuest Medical Library, ProQuest Research Library: Health & Medicine, British Nursing Index, ComDisDome, GenderWatch, and Health & Safety Science Abstracts (via Proquest). Our core search consisted of Mesh terms related to anthropometric measurements (e.g., “anthropometry,” “body constitution,” and “nutritional status”), combined with terms for dental caries (e.g., “dental caries,” “tooth decay,” “tooth cavity,” and “dental cavity”) and the Mesh terms for longitudinal studies (e.g., “cohort studies” and “case-control” studies). The full search strategy is provided in Supplemental Appendix 1. Additional studies were identified by reference linkage.

The inclusion criteria were as follows:

1. Sample characteristics: <18 y old; no sex, country, or socioeconomic restriction

2. Measurements of dental caries: caries experience with primary and/or secondary dentitions measured by the number of decayed, extracted, and filled primary teeth; the number of decayed and filled primary tooth surfaces; the number of decayed and filled approximal permanent tooth surfaces; the number of decayed and filled primary teeth; the number of decayed and filled permanent teeth; the number of decayed, missing, and filled primary tooth surfaces (dmfs); the number of dmfs according to International Caries Detection and Assessment System (ICDAS) codes 1–6, the number of dmfs according to ICDAS codes 3–6; the number of decayed, missing, and filled permanent tooth surfaces (DMFS); the number of decayed, missing, and filled primary teeth (dmft); the number of decayed, missing, and filled permanent teeth (DMFT); the number of DFMT of incisors and molars; the number of decayed primary teeth; the number of decayed permanent teeth; and any other indices

3. Measurements of human anthropometry: weight, height, and body fat measured by BMI, waist circumference, waist-to-hip ratio, and skinfold thickness, including BMI category and other nutritional status category

4. Evaluation of the association between dental caries and anthropometric measurements of the same sample over time (longitudinal studies)

5. Published and accessible English-language studies

Data extraction and quality assessment.

The abstract and full text of each relevant study were independently reviewed by 2 investigators (L-WL and S-MP). κ Statistics were used to evaluate inter-reader agreement. A third reviewer (HMW) was consulted to resolve disagreements. Review of abstracts and full texts followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. A data extraction sheet was developed, including the interpretation of the methodologies and results. The extracted information included the following: characteristics of the subjects (age, sex, socioeconomic status, and nationality), methodology (study design, setting, participants, variables, anthropometry type, caries index, data source/measurements, and statistical methods), and outcome (follow-up time, management of missing data, confounder-adjusted estimates). One reviewer (L-WL) extracted the data from the included studies. To reduce bias and minimize errors, the other reviewers (S-MP and HMW) were responsible for checking the extracted data. Disagreements were resolved by consensus of the 3 reviewers.

The quality of included articles was independently assessed by 2 investigators (L-WL and S-MP) by 2 methods. The Strengthening the Reporting of Observational studies in Epidemiology (STROBE) checklist determined the quality of reporting of the articles from different aspects (introduction, methods, results, discussion, and other information). Each item used a 4-score scale: “yes” = 1, “incomplete” = 0.5, “no” = 0, “NA” (not applicable) = 0. Thirty-four items were identified in the STROBE checklist, ranging from 0 to 34. Inter-reader agreement was also addressed by κ value. In addition, study design and analysis were assessed according to the criteria described by Hooley et al. (14) to provide specific information based on number of subjects, observational period, sample, attempts made to control confounders, and anthropometric measurement method (Table 1).

TABLE 1.

Quality assessment of the included studies

Study (reference)	Sample size, n	Follow-up, y	Sample method	Control of confounding factors	Anthropometric measures
Gerdin et al. (24)	2303	BMI: 6	Stratification/cluster sampling use to obtain sample representative of country/districts	Yes	Secondary data
		Dental status: 8
Lempert et al. (25)	280	6	Stratification/cluster sampling use to obtain sample representative of country/districts	Yes	Secondary data
Scheutz et al. (17)	145	6	Convenience sample	No	Primary data
Sánchez-Perez et al. (16)	88	4	Convenience sample	Yes	Primary data
Peres et al. (26)	339	12	Some form of cluster sampling use to obtain sample approximately representative of towns	Yes	Secondary data
Peres et al. (27)	352	6	Some form of cluster sampling use to obtain sample approximately representative of towns	Yes	Secondary data
Alvarez (32)	209	4	Random sample	No	Primary data
Kay et al. (28)	985	5.08	Some form of cluster sampling use to obtain sample approximately representative of towns	Yes	Primary data
Werner et al. (23)	230	1.8	Convenience sample	No	Secondary data
Delgado-Angulo et al. (30)	83	3.5	Random sample	Yes	Primary data
Seow et al. (22)	617	0–4	Convenience sample	No	Secondary data
Nelson et al. (18)	224	14	Convenience sample	Yes	Secondary data
Lai et al. (20)	50	4.33	Convenience sample	No	Secondary data
Ismail et al. (31)	788	2	Random sample	No	Not reported
Rajshekar and Laxminarayan (21)	500	3–5.5	Convenience sample	No	Secondary data
Zhou et al. (19)	225	2.67	Convenience sample	Yes	Secondary data
Shulman (29)	4207	2–6	Stratification/cluster sampling use to obtain sample representative of country/districts	No	Secondary data

Results

A total of 1338 citations were identified from the electronic databases (Pubmed, ISI Web of Knowledge, Cochrane library, and 6 other databases). Fifty-nine articles were eligible for full-text assessment after removal of duplications and screening of relevant articles; inter-reader κ agreement was 0.82 ± 0.04 (means ± SEs). The flow diagram of search process is shown in Figure 1. Seventeen articles formed the bases of this systematic review; inter-reader κ agreement was 0.88 ± 0.07.

FIGURE 1.

PRISMA flow diagram of the study selection process. PRISMA, Preferred Reporting Items for Systematic Reviews and Meta-Analyses.

Quality assessment and risk of bias

The mean quality of the articles was 23.91 ± 3.06, ranging from 19.5 to 30.0. Inter-reader agreement was reached after discussion. Inter-reader κ agreement was 0.90 ± 0.017. All of the articles covered >50% of the STROBE items. The quality assessments of the included studies are presented in Table 1. The sample size of included articles ranged from 50 to 4207. Eight studies collected the convenience sample either at local primary schools (16, 17) or hospitals (18–23). Six studies were from large community samples, e.g., records extracted from the Swedish child welfare centers and the school health service (24), the European Youth Heart Study (25), the Pelotas 1993 birth cohort in Brazil (26, 27), the Avon Longitudinal Study of Parents and Children in South West England (28), and the NHANES III (29). Only 3 studies applied the random sample design (30–32), and one of them did not elaborate on the selection procedures (32). Based on the nature of the study design, 5 studies collected primary anthropometric data (16, 17, 28, 30, 32), whereas only 4 of the included articles reported the dental caries experience as secondary data (23–25, 29). Most of the dental caries measurements followed the WHO criteria, with qualified examiner calibration, but only 3 studies assessed dental radiographs for more accurate diagnoses of caries (18, 23, 24). In addition, some dental assessments were performed by calibrated nondental personnel (28) or dental students (23) rather than dental surgeons. Only Sánchez-Perez et al. (16) presented the reliability of measurements with intraclass correlation.

Subjects in the included studies were followed at least 1.8 y, ensuring sufficient follow-up time to evaluate the longitudinal relation between change in body size and dental caries. Nine studies tried to control confounders, but the modified factors varied in each article, including age (16, 18, 25, 28, 30), sex (16, 18, 24–28, 30), socioeconomic status (16, 18, 19, 24–27), diet (25, 30), ethnicity (18, 25), baseline status of primary teeth (16, 30), child development (19, 26), and oral behaviors (19, 27, 30). Three articles reported the adjusted estimate and SE (18, 24, 25), whereas Sánchez-Perez et al. (16) reported the adjusted error only. Six articles presented RRs or risks ratios (17, 26), ORs (27, 28), incidence rate ratios (30, 31), or incidence density ratios (19, 29). Note that Peres et al. evaluated the same cohort with different statistical terms [RRs (26) and ORs (27)]. Alvarez (32) concluded that malnourishment during the first year of life was associated with increased caries in both primary and permanent dentition; however, no quantitative data were shown except for a line chart.

Study characteristics

All of the included articles were observational studies published in English after 1995. The follow-up time ranged from 1.8 to 14 y and involved 11,625 participants. Among the articles, the study conducted by Peres et al. was presented in 2 publications (26, 27). Because the primary outcomes in these 2 articles were slightly different, the data were not combined for analysis (26, 27). Seven studies were cohort studies (16–19, 24, 30, 31), whereas 7 studies had a case-control design (20–23, 25, 28, 29) and 2 were cross-sectional studies nested in birth cohorts (26, 27). One additional study reported both cross-sectional and longitudinal findings (32). Eleven articles reported anthropometric measurements and dental caries as a primary outcome (16, 18, 20, 21, 23–25, 28, 29, 30, 32), whereas 6 articles evaluated them as secondary outcomes (17, 19, 22, 26, 27, 31).

Results of included articles indicated disparate associations that might be influenced by several factors: for example, nonuniformity assessments, setting and procedure of measurements, age and ethnicity of participants, and confounders of dental caries. Three of the included studies reported a significant positive association between BMI or birth weight/height and dental caries (18, 24, 31). Six of them found no association between anthropometric measurements and dental caries (17, 20, 22, 23, 25, 29). Three studies demonstrated an inverse association either in primary or permanent dentition (26, 30, 32). Five additional studies reported that the relation was inconclusive (16, 19, 22, 27, 28). Among the included articles, early anthropometric measures were used to predict later dental caries in 14 studies, whereas only 1 study (25) used early oral status to predict later anthropometric measures. One additional study examined their mutual relation (28). Both of the authors who applied caries experience as a predictor agreed that high dental caries experience had a negative influence on children’s growth (25, 28). However, agreement was not reached when anthropometric measurements were used as the predictor. The results of the included 17 studies were evaluated according to their anthropometric categories and types of dentition. The variables and associations in these studies and literature reviews are presented in Tables 2 and 3, respectively. A meta-analysis was attempted, but the degree of heterogeneity between study designs, particularly with respect to the diversity of the indices of the anthropometric measurement and dental caries, made the quantitative data difficult to be summarized for meta-analysis.

TABLE 2.

Variables and associations in the included studies¹

Anthropometric measurements	Dental caries measurements (reference)	Association (reference)
BMI
isoBMI	deft (24), DFSa (24), DFT (24)	P (24)
BMI z score	dmfs (25), DMFT (25), DMFS (17)	N (17, 25)
BMI (CDC criteria)	dmfs (16), DMFS (16), dmft (16), DMFT (30), DMFS (30)	I [primary dentition (16), permanent dentition (30)]
		N [permanent dentition (16)]
No defined criteria	DT (23), dt (23), new caries lesion (23)	N (permanent dentition and new caries lesion) (23)
		I (primary dentition) (23)
No category	dmft (25), DMFT (25), dmft (28)	N (25, 28)
Height
Height-for-age z score	dmft (27), DMFT (26)	I (26, 27)
Birth height	dmft (28)	P (28)
Weight
Birth weight	dmft (28), ECC (22), DMFT-IM (18), DMFT (18)	P [primary dentition (28), permanent dentition (18)]
	dmft (20, 21), dmfs (19), dfs (29), dt (20, 21), ft (20, 21), mt (21)	N [primary dentition (19–21, 29)]
		I (21)
Weight by height	dmft (27), d1–6mfs (31), d3–6mfs (31)	N (27)
		P (31)
Weight by age	dmft (27)	N (27)
Other measurement
NCHS standard	DMFT (32), deft (32), DMFS (32), dft (32)	I (32)

¹deft, the number of decayed, extracted, and filled primary teeth; dfs, the number of decayed and filled primary tooth surfaces; DFSa, the number of decayed and filled approximal permanent tooth surfaces; dft, the number of decayed and filled primary teeth; DFT, the number of decayed and filled permanent teeth; dmfs, the number of decayed, missing, and filled primary tooth surfaces; DMFS, the number of decayed, missing, and filled permanent tooth surfaces; d_1–6mfs, the number of decayed, missing, and filled primary tooth surfaces according to International Caries Detection and Assessment System (ICDAS) codes 1–6; d_3–6mfs, the number of decayed, missing, and filled primary tooth surfaces according to ICDAS codes 3–6; dmft, the number of decayed, missing, and filled primary teeth; DMFT, the number of decayed, missing, and filled permanent teeth; DMFT-IM, the number of decayed, missing, and filled permanent teeth of incisors and molars; dt, the number of decayed primary teeth; DT, the number of decayed permanent teeth; ECC, early childhood caries; ft, the number of filled primary teeth; I, inverse association; isoBMI, international age- and sex-adjusted BMI; mt, the number of missing primary teeth; N, no association or inconclusive association; NCHS, National Center for Health Statistics; P, positive association.

TABLE 3.

Literature reviews of the included studies¹

Study (reference)	Study design	Initial data and follow-up scheme	Sample size, n	Measurements taken	Key findings
Gerdin et al. (24)	Cohort study	• Initial: 4-y-old	2303	• Caries: deft (6-y-old), DFT (10 and 12-y-old), and DFSa	• Children who were obese at age 4-y-old had more caries when they were 12-y-old compared with those who had normal weight at 4-y-old; DFT: 1.1 vs. 0.7*
		• Follow-up: BMI (4, 5, 7, and 10-y-old), dental status (6, 10, and 12-y-old) and socioeconomic status (10-y-old)		• Anthropometric: isoBMI	• Similar results were seen when comparing children who were not obese at 10-y-old
					• DFSa: overweight or obese at 4, 5, 7, and 10-y-old > normal weight from 4 to 10-y-old > overweight or obese at 4 y but with normal weight at 5, 7, and 10-y-old*
					• Childhood BMI had independent weak effect on caries prevalence at 12-y-old; adjusted estimate (β-value ± SE): BMI at 4-y-old: 0.048 ± 0.020*; 5-y-old: 0.050 ± 0.018**; 7-y-old: 0.032 ± 0.013*; 10-y-old: 0.024 ± 0.009*
Lempert et al. (25)	Case-control study	• Initial: 9.6-y-old	385	• Caries: dmft and DMFT	• No significant association was found between caries experience and BMI or △BMI; adjusted estimate (β-value ± SE) △BMI: −0.022 ± 0.020; △BMI z score: −0.010 ± 0.007
		• Follow-up: 6 y later (from 1997 to 2003)	280	• Anthropometric: BMI, BMI z score, and △BMI	• Inverse association was found between caries at baseline and subsequent changes in BMI over a period of 6 y later in children whose mothers were well educated; adjusted estimate (β-value ± SE) △BMI: −0.059 ± 0.024*; △BMI z score: −0.023 ± 0.009
Scheutz et al. (17)	Cohort study	• Initial: mean 7.6-y-old	145	• Caries: DMFS and new caries lesions in the permanent dentition	• No significant difference in new caries lesions was found between malnourished children (BMI z score ≤1.96 SDs) and those without malnutrition (BMI z score >1.96 SDs); crude RR: 1.42; adjusted RR: 1.55 (95% CI: 0.92, 2.62)
		• Follow up: 6 y later (from 1997 to 2003)		• Anthropometric: BMI (without clear criteria)
Sánchez-Perez et al. (16)	Cohort study	• Initial: 7-y-old	110 (7-y-old)	• Caries: dmft, DMFT, dmfs, and DMFS	• Children with a higher BMI had lower amounts of dental caries in primary dentition**
		• Follow-up: 4 y later (examination at each year)	88 (11-y-old)	• Anthropometric: BMI (CDC criteria)	• The effects of the risk of being overweight and actually being overweight were significantly negative when compared with thin children*; dmft: 7-y-old: 3.2 vs. 6.2 9-y-old: 2.1 vs. 5.8
					• No association was found between BMI and DMFS scores in permanent dentition
Peres et al. (26)	Cross-sectional study (nested in a birth cohort study)	• At birth: socioeconomic and demographics variables	359 (6-y-old for survey)	• Caries: DMFT	• No significant difference was found for caries between different groups of birth weight and gestation age
		• 6-y-old: oral health–related behaviors, dental service use, and primary dental caries	339 (12-y-old for oral examination)	• Anthropometric: height-for-age z score at 1 and 4-y-old and birth weight	• The prevalence of caries (DMFT ≥1) in 12-y-old children with height deficiency at 1-y-old (height-for-age z score ≤2) was significantly higher than for children with adequate height (height-for-age z score >2); prevalence of caries: 82.1% vs. 49.2%**
		• 12-y-old: family economic level, oral health–related behaviors, dental service use, and dental caries			• Mean DMFT of 12-y-old children with height-for-age z score ≤2 at 1-y-old was significantly higher than for children with height-for-age z score > 2; mean DMFT: 1.86 vs. 1.18**
					• The prevalence of caries (DMFT ≥1) in 12-y-old children with height deficiency at 4-y-old (height-for-age z score ≤2) was significantly higher than for children with adequate height (height-for-age z score >2); prevalence of caries: 82.1% vs.49.0%**
					• Mean DMFT of 12-y-old children with height-for-age z score ≤2 at 4-y-old was significantly higher than for children with height-for-age z score >2; adjusted RR: 1.50 (95% CI 1.03, 2.18)
					• No interactions were found between height-for-age deficiency at 1-y-old and dental caries at 6-y-old in primary dentition
Peres et al. (27)	Cross- sectional study (nested in a birth cohort study)	• Initial: at birth	352 (6-y-old)	• Caries: dmft	• No significant difference of high amount of dental caries (dmft ≥4) was found in 6-y-old children between the adequate (>2500 g) birth weight group and the low (≤2500 g) birth weight group
		• Follow up: 0.08, 0.25, 0.5, 1, and 6-y-old		• Anthropometric: birth weight, height by age at 1-y-old, weight by height at 1-y-old, and weight by age at 1-y-old	• Children with height deficiency for 1-y-old (height-for-age z score ≤2) had a significantly higher chance of having a high amount of dental caries (dmft ≥4) than those with adequate height for age at 1-y-old; adjusted OR (inadequate group): 4.5 (95% CI: 1.5, 13.6)*
					• No significant difference of a high amount of dental caries (dmft ≥4) was found in 6-y-old children between the group with adequate weight by age at 1-y-old (z score >2) and those with inadequate weight by age at 1-y-old (z score ≤2)
					• No significant difference of a high amount of dental caries (dmft ≥4) was found in 6-y-old children between the group with adequate weight by height at 1-y-old (z score >2) and those with inadequate weight by height at 1-y-old (z score ≤2)
Alvarez (32)	2 cross-sectional studies and a longitudinal study	For longitudinal study:	209	• Caries: deft, DMFT, DMFS, and dft	• The deft of stunted and wasted children at 4-y-old was significantly higher than the normal, wasted, stunted groups*
		• Initial: 0.5-y-old and 0.92-y-old		• Anthropometric: height and weight (classified into normal, wasted, stunted, and stunted and wasted groups by NCHS)	• The proportion of stunted and wasted children at 4-y-old with ≤3 caries was significantly lower than the normal, wasted, stunted groups; the percentage of children with 0–3 deft: 3.4% (stunted and wasted group) vs. 35% (normal group) vs. 20% (stunted group) vs. 37% (wasted group)
		• Follow-up: 4 y later			• The dft of stunted and wasted children at 6-y-old was significantly higher than the normal, wasted, stunted groups**
					• The DMFS of stunted and wasted children at 6-y-old was significantly higher than the normal, wasted, stunted groups**
					• The DMFT of stunted and wasted children at 6-y-old was significantly higher than the normal, wasted, stunted groups*
Kay et al. (28)	Case-control study	• Initial: at birth	985	• Caries: dmft	• No association was found between caries and current weight
		• Follow-up: 5.08 y later		• Anthropometric: weight, height, birth weight, birth height, and BMI	• Higher birth weight was associated with increased risk of caries; model a and c: OR: 1.05 (95% CI: 1.01,1.08)**; model d: OR: 1.08 (95% CI: 1.03,1.13)
					• No association was found between caries and current height
					• Higher birth height was associated with increased risk of caries; model a: OR: 1.08 (95% CI: 1.01,1.16)*; model c: OR: 1.09 (95% CI: 1.01,1.18)*; model d: OR: 1.14 (95% CI: 1.03,1.26)*
					• Children who had caries at 5.08-y-old had a smaller increase in weight (measured as change in SD score) than those without tooth decay; change in SD score (model d): “no caries” vs. “any caries”: 0.183 vs. −0.142**
					• Children who had caries at 61-mo-old had a smaller increase in height (measured as change in SD score) than those without tooth decay; change in SD score (not adjusted): “no caries” vs. “any caries”: 0.026 vs. −0.151*
					• No association was found between BMI1 and dental caries
Werner et al. (23)	Case-control study	• Initial: 6- to 9-y-old	230	• Caries: DT, dt, new caries lesion	• DT at the initial exam was not significantly different between different BMI groups
		• Follow-up: mean interval, 1.8 y later		• Anthropometric: height, weight, and BMI (categorized into underweight /healthy weight, overweight, and obese groups)	• Overweight and obese children had less dt than underweight/healthy children
					• Obese vs. overweight vs. underweight/healthy: 34% vs. 30% vs. 51%*
					• The presence of new carious lesions at recall exams in primary teeth and permanent teeth was not significantly different between different BMI groups
Delgado-Angulo et al. (30)	Cohort study	• Initial: 7- to 9-y-old	121	• Caries: net DMFS increment	• Stunting was related to net DMFS increment. CDC criteria: IRR: 1.61 (95% CI: 1.07, 2.44); WHO standards: IRR: 1.79 (95% CI: 1.28, 2.51)
		• Follow-up: 3.5 y later	83	• Anthropometric: height and weight (defined stunting using 2000 CDC and 2007 WHO criteria)
Seow et al. (22)	Case-control study	• Initial: at birth	617	• Caries: ECC-free or ECC	• The birth weight of ECC group was not significantly different from birth weight of non-ECC group
		• Follow-up: until 4-y-old		• Anthropometric: birth weight
Nelson et al. (18)	Cohort study	• Initial: at birth	224 (80 HR-VLBW, 59 LR-VLBW, and 85 term adolescents)	• Caries: DMFT-IM and DMFT	• The term adolescents had significantly increased DMFT-IM and DMFT scores compared with the LR-VLBW group; unadjusted means ± SDs: HR-VLBW vs. LR-VLBW vs. term DMFT-IM scores (means ± SDs): 1.06 ± 1.6 vs. 1.00 ± 1.5 vs. 1.49 ± 1.7; total DMFT scores (means ± SDs): 1.70 ± 3.1 vs. 1.56 ± 2.1 vs. 2.39 ± 2.9; adjusted estimated by race, sex, SES, age, sociodemographics DMFT-IM % increase: 26.1 vs. 26.2 (term vs. HR-VLBW), 60.1 vs. 35.4 (term vs. LR-VLBW); DMFT % increase: 33.5 vs. 29.6 (term vs. HR-VLBW), 71.6 vs. 36.8 (term vs. HR-VLBW)*
		• Follow-up: 14 y later		• Anthropometric: birth weight (HR-VLBW and LR-VLBW)
Lai et al. (20)	Case-control study	• Initial: at birth	50 (25 cases and 25 controls)	• Caries: dt, ft, and dmft	• Prevalence of dental caries in the VLBW children was not significantly different from that of NBW
		• Follow-up: 2.5-, 3.67-, and 4.33-y-old		• Anthropometric: birth weight (VLBW)	• VLBW vs. NBW (means dmft ± SDs): 2.5-y-old: 0 vs. 0 ± 0.2; 3.67-y-old: 0.6 ± 1.4 vs. 0.5 ± 1.5; 4.33-y-old: 0.8 ± 1.5 vs. 1.4 ± 3.2
Ismail et al. (31)	Cohort study	• Initial: 0- to 5-y-old	788	• Caries: d1–6mfs and d3–6mfs (ICDAS criteria)	• Children in the highest weight-for-age percentile group (84.3–100%) had a significantly higher d3–6mfs than the lowest weight-for-age percentile group (0–26.9%); IRR: 0.8 (95% CI: 0.6, 1.0)*
		• Follow-up: 2 y later		• Anthropometric: weight for age	• Children in the higher weight-for-age percentile group (27.0–56.4%) had a significantly higher d3–6mfs than the lowest weight-for-age percentile group (0–26.9%); IRR: 0.6 (95% CI: 0.4 1.0)*
Rajshekar and Laxminarayan (21)	Case-control study	• Initial: at birth	500 (250 FTNBW and 250 PTNBW)	• Caries: dmft, dt, mt, and ft	• The caries rate (dmft >0) in PTLBW was significantly higher than in the FTNBW group; caries rate: 48% vs. 38.8%*
		• Follow-up: 3–5.5 y later		• Anthropometric: birth weight (FTNBW, PTNBW)	• The mean dmft, dt, mt, and ft of FTNBW groups were not significantly different from the PTLBW group
					• Mean dmft was significantly higher in the PTLBW girl group than in the FTNBW girl group; mean dmft: 1.3 ± 1.9 vs. 0.7 ± 1.4**
					• The mean dmft was not significantly different between PTLBW and FTNBW boy groups
Zhou et al. (19)	Cohort study	• Initial: at birth	225	• Caries: dmfs	• ECC was not significantly related to birth weight (P = 0.128)
		• Follow-up: 0.67, 1.17, 1.67, and 2.67 y later		• Anthropometric: birth weight (≥2500 g, <2500g)	• ECC was significantly related to children’s z values of weight and height**; z values of weight: IDR: 0.77 (0.67, 0.88) (P < 0.001)**; z values of height: IDR: 1.41 (1.12, 1.78) (P < 0.003)**
Shulman (29)	Case-control study	• Initial: at birth	4207	• Caries: dfs	• Mean dft was not related to birth weight (P < 0.096)
		• Follow-up: 2–6 y later		• Anthropometric: birth weight

¹*P < 0.05, **P < 0.01. deft, the number of decayed, extracted, and filled primary teeth; dfs, the number of decayed and filled primary tooth surfaces; DFSa, the number of decayed and filled approximal permanent tooth surfaces; dft, the number of decayed and filled primary teeth; DFT, the number of decayed and filled permanent teeth; dmfs, the number of decayed, missing, and filled primary tooth surfaces; d_1–6mfs, the number of decayed, missing, and filled primary tooth surfaces according to ICDAS codes 1–6; d_3–6mfs, the number of decayed, missing, and filled primary tooth surfaces according to ICDAS codes 3–6; DMFS, the number of decayed, missing, and filled permanent tooth surfaces; dmft, the number of decayed, missing, and filled primary teeth; DMFT, the number of decayed, missing, and filled permanent teeth; DMFT-IM, the number of decayed, missing, and filled permanent teeth of incisors and molars; dt, the number of decayed primary teeth; DT, the number of decayed permanent teeth; ECC, early childhood caries; ft, the number of filled primary teeth; FTNBW, full term and normal birth weight; HR-VLBW: very low birth weight adolescents with high risk; ICDAS, International Caries Detection and Assessment System; IDR, xxx ; IRR, incidence rate ratio; isoBMI, international age- and sex-adjusted BMI; LR-VLBW, very low birth weight adolescents with low risk; mt, the number of missing primary teeth; NBW, normal birth weight; NCHS, National Center for Health Statistics; PTLBW, preterm and low birth weight; Δ, change.

Anthropometric measurements

Anthropometric measures predicting dental caries.

Five of the included articles applied BMI as the primary predictor of dental caries. One article indicated a positive association (24), whereas 1 reported an inconclusive association (16) and the other 3 reported no association (17, 18, 23). The results varied considerably when different categories of BMI were used (Table 2). Gerdin et al. (24) assessed child obesity using international age- and sex-adjusted BMI and reported that childhood BMI had an independent weak effect on caries prevalence at age 12. Using CDC criteria, Sánchez-Perez et al. (16) and Delgado-Angulo et al. (30) indicated that children with a high BMI had lower levels of dental caries in primary dentition; however, no association was shown between BMI and DMFS scores in permanent dentition. Using no defined criteria, Werner et al. (23) found an inverse association in primary dentition but no association in permanent dentition or new caries lesions; however, Kay et al. (28) and Lempert et al. (25) found no associations. When used as a continuous variable, Kay et al. (28) found no association between BMI and caries (P = 0.396) nor was an association found using BMI z scores by Lempert et al. (25) or Scheutz et al. (17).

Six of the included articles predicted caries experience by height and/or weight. The inverse relation was in agreement when assessing dental caries by height and weight (30, 32) or height only (19, 26, 27). However, reported results that considered only baseline weight and future caries experience indicated various types of relations: 1 article indicated a positive association (31), 1 reported an inverse association (19), whereas another article concluded no association (27). Alvarez (32) and Delgado-Angulo et al. (30) demonstrated that stunting (measured by height and weight) was a significant risk factor for dental caries in primary (32) and permanent (30, 32) dentition. Peres et al. (26, 27) reported that children who were shorter at 12 mo or 4 y had a higher prevalence of caries at ages 6 and 12 y (height-for-age z score ≤2). However, no significant difference for high amounts of dental caries (dmft ≥4) was found in 6-y-old children between groups of adequate weight by age and of inadequate weight by age. Ismail et al. (31) found that the severity of caries increased in children with higher weight for height. Zhou et al. (19) indicated that children with weight and height below the normal range had a greater risk of developing early childhood caries.

Birth weight and height are important factors for children’s early development. Seven of the included articles predicted caries experience by birth height and/or weight. Two articles supported a positive association (18, 28), 4 reported no association (19, 20, 22, 29), and only 1 reported an inconclusive association (21). Nelson et al. (18) and Kay et al. (28) showed that higher birth height (28) or birth weight (18, 28) was associated with increased risk of caries. Zhou et al. (19), Seow et al. (22), Lai et al. (20) and Shulman (29) agreed that caries experience of children with low birth weight was not significantly different from that of children with normal birth weight, whereas Rajshekar and Laxminarayan (21) reported inconclusive results in that different patterns existed in prevalence and severity of caries among different groups.

Anthropometric measures predicted by dental caries.

Two of the included studies used baseline caries as the predictor and agreed that high previous caries experience affected children’s BMI (25) or weight (28). Lempert et al. (25) found an inverse association between baseline caries and subsequent changes in BMI over a period of 6 y in children whose mothers were well educated. Kay et al. (28) also discovered that children who had caries at 61 mo had a smaller increase in weight than did those without decay.

Type of dentition

Subjects in most of the included studies were in their mixed dentition (a combination of primary and permanent teeth), ranging from birth to 16 y old. Lempert et al. (25) combined the primary and permanent caries index and revealed that early caries experience was not related to BMI. Werner et al. (23) reported that the presence of new carious lesions at recall examinations in primary and permanent teeth was not significantly different between various BMI groups.

Eleven articles reported the varied prospective association between anthropometric measurements and caries in the primary dentition. Two of them found that the severity of caries [dmft (16); number of decayed, extracted, and filled primary teeth (32)] was inversely related to anthropometric measurements. Opposite results were reported when dental caries experience was described by using the ICDAS index (31). No significant correlation was found between low birth weight and dental caries in primary dentition (20, 22, 29). Kay et al. (28) described that higher birth height or weight increased the risk of caries, whereas decayed teeth slowed a child’s development in terms of height and weight. However, some inconclusive patterns were found in other studies (19, 21, 27).

Eight articles assessed the relation between caries experience of permanent dentition and a child’s growth. Peres et al. (26), Alvarez (32), and Delgado-Angulo et al. (30) identified an association of deficient height or weight in early childhood with increased prevalence and/or severity of dental caries in permanent teeth. Gerdin et al. (24) reported that obese children (4 or 10 y old) would develop more caries at an older age (12 y old) and that adolescents who were born full term and were of normal birth weight had significantly more dental caries experience than did adolescents with low birth weight (18). However, no significant association between DMFS and BMI was detected in another 3 studies (16, 17, 23).

Discussion

The principal results of this systematic review indicated that agreement has not been reached because of the varied associations shown in the included studies. However, both of the articles (25, 28) that applied caries as the predictor of anthropometric measurements agreed that higher caries experience was a risk factor for children’s growth and development. Because both of the studies were observational prospective studies, we suggest that maintaining good oral health in early childhood should be included as a potential intervention for general health issues. With regard to anthropometric measures as an indicator, “height” may be a potential predictor of caries experience. There were 3 types of anthropometric measurements of children’s growth in this review, namely BMI, height and weight, and birth weight and height. Less than 1 in 5 studies identified a positive association between anthropometric measurements and dental caries, whereas 1 in 6 reported an inverse relation. However, approximately one-third of the articles found no significant relation between anthropometric measurements and dental caries, and more than a quarter observed conflicting findings. In terms of type of dentition, 2 articles revealed a positive association in primary dentition (28, 31), 4 found no association (20, 22, 23), 2 found an inverse association (16, 17), and 3 found an inconclusive association (19, 21, 27). A similar pattern was shown in the permanent dentition: 2 articles revealed a positive association (18, 24), 3 found no association (16, 17, 23), and 3 found an inverse association (21, 26, 32). In general, these results are consistent with the systematic review of Hooley et al. (14) that dental caries is not related to BMI in a simple linear association. Caries experience tends to be more related to both low and high anthropometric measurements (21, 24, 26, 27, 30–32). However, most of the studies that investigated low birth weight supported that there was no association between birth weight and future caries (19, 20, 22, 26, 29). As pointed out by Hooley et al. (14), some of the contradictory findings can be explained by methodologic factors. The use of sensitive measures (X-rays or the ICDAS index) tended to yield a positive relation (18, 24, 31). Although the results of Werner et al. (23) disagreed with this pattern, we found that the examiners in the study were dental students, which may have influenced the results. Socioeconomic factors appear to be significant moderators in the analyses, as concluded by the 2 other systematic reviews (14, 15). Lower socioeconomic status is a potential risk factor for high caries prevalence (19, 21, 22, 26–29, 31). The inverse relation is more apparent in the studies that were conducted in developing countries (16, 21, 26, 27, 30, 32), as Hooley et al. (14) suggested, although 2 studies from developing areas showed no significant relation (17, 19). It is not surprising to find that most of the reviewed articles that studied children with malnutrition in disadvantaged districts reached the conclusion that poor nutrition status was associated with increased caries experience. Some evidence was found to support this hypothesis: 1) protein-energy malnutrition in these children may lead to reduced salivary flow and a high count of lactobacilli (17) and Streptococcus mutans (33); 2) unfavorable socioeconomic status, including lower parental educational level and household income, was demonstrated to affect children’s oral health (34, 35); 3) poor chewing ability due to caries determined the wellness and quality of life of children, which affected their weight and height (36–38); and 4) poor oral hygiene and lack of public health service were prominent factors in stunted children (39, 40). Similar evidence was also found by Hooley et al. (14). Each study that supported a positive association (18, 24, 31) met >1 of the following conditions: 1) the sample underrepresented underweight children (24), 2) the studies were conducted in highly developed countries (18, 24, 31), or 3) examination was conducted by using a more sensitive method (18, 24, 31). This finding is consistent with the review of Hooley et al. (14). However, we also noticed that if the sample met only 1 of the conditions, a positive relation may not be detected. For example, although 5 studies included an underweight group and were conducted in an advantaged area with less sensitive examination methods, none of them proposed a positive association (20, 22, 23, 28, 29). Two articles (26, 27) absorbed the underweight group into the normal group and conducted the studies in developing countries with less sensitive examination, and neither of them reported a positive relation between caries and anthropometric measurements. In addition, 2 new patterns were detected in our review. With the exception of the studies of birth weight, studies that underrepresented the obese/overweight group were inclined to show a negative relation, whereas studies that covered all groups did not show any specific pattern.

With regard to dentition type, the meta-analysis by Hayden et al. (15) supported a strong relation between BMI (as the standardized assessment of child obesity) and dental caries in permanent dentition. However, no significant pattern was recognized in our review. Our review and the review of Hayden et al. had different included criteria of effective studies, which may have contributed to different conclusions.

In summary, we suggest that the following factors may explain the variety of the outcomes:

• Nonuniformity of anthropometric assessment breakdown and measurement of dental caries was observed among these studies. In terms of BMI, 1 study applied the 2000 CDC criterion, which defines stunting as height for age below the fifth percentile (equivalent to −1.645 SD) of the 2000 CDC reference population (30), whereas another study used the National Center for Health Statistics median as the reference (32). Furthermore, some articles did not provide clear “cutoff” points for underweight or normal or obese groups. In terms of measurement of dental caries, dental caries was measured at various levels across studies. Most studies recorded caries at the cavity level (16–19, 21, 22, 26–28, 30, 32); however, the inclusion of the initial stages of the caries (31) or no clear criteria for diagnosis of caries in some studies (23, 25, 29) may make comparison and combination of the outcomes more difficult.

• Dental examinations in 2 studies (23, 28) were not performed by dental surgeons, which may have affected the accuracy of the diagnosis of caries. Moreover, intra- or interexaminer reliability was not examined in 5 studies (18, 23–25, 29), and the κ value was not provided in 3 articles (19, 21, 32).

• The setting and procedure of the measurements were not standardized. Only 3 studies (18, 23, 24) had access to X-ray images. Some forms of caries, especially proximal caries, are not easily detected by only clinical examination. Thirteen articles did not provide detailed information of the setting of the anthropometric measurements (17–23, 26–28, 31, 32, 39), whereas the other 4 (16, 24, 25, 30) elaborated the standardized procedure of the measurements (a calibrated scale with the child wearing light clothing).

• Approximately two-thirds of the included studies used secondary anthropometric data, and 4 articles (23–25, 39) extracted dental caries data from previous dental reports. This may have hampered the accuracy of the information.

• The ages ranged from birth to 16 y old in the included studies. The amounts of growth hormone secreted during the adolescent growth spurt (41) would change formation of enamel (42). These factors might influence the comparison between anthropometric measurements.

• Ethnicity and/or country of the studies varied, and the socioeconomic status of the samples differed, which would likely affect children’s diet, health status, and access to health education and affect the children’s cariogenic and obesogenic environments.

• Nine articles tried to control for the confounders of dental caries; however, the factors they analyzed were different. Age (16, 18, 25, 28, 30), sex (16, 18, 24–28, 30), and socioeconomic status (16, 18, 19, 24–27) were the most frequent confounders; however, other important caries-related factors, such as dietary habits, oral health behaviors, and baseline status of decayed primary teeth were controlled in only 5 studies (16, 19, 25, 27, 30).

• Because the hypotheses varied between studies, the full spectrum of anthropometric measurements was often not investigated. Scheutz et al. (17), Alvarez (32), and Delgado-Angulo et al. (30) focused on dental caries in malnourished children who lived in underprivileged suburban areas and the sample size of the obese and overweight groups was much smaller than that of the malnourished group. The variables of dental caries also differed between these studies. Eleven articles reported both prevalence (percentage of children who suffered from caries) and severity (e.g., mean DMFS, DMFT) of dental caries (16–21, 24–28), whereas 6 articles assessed only prevalence (22, 23) or severity (29–32).

Our systematic review has several limitations. Only English-language publications were included, and thus selection bias may be an issue. The quality of the included studies varied in their reporting and study designs. The Cochrane Collaboration tool is recognized as one of the best checklists for randomized controlled trials (43). However, no widely accepted appraisal tools could be found for the observational studies (44). The critical appraisal checklist of this systematic review was modified from another similar review (14), which provides good criteria for rating the studies but has not been widely recognized.

From the articles reviewed in this study, we found a growing interest in the long-term association between anthropometric measurements and dental caries in children. Researchers tried to assess this question in different ways. A more accurate model of relation, which covers different aspects of multilevel analysis or structural equation modeling, should be provided in future studies. On the basis of the findings of our systematic review, the following recommendations are offered [many of which are consistent with Hooley et al. (14) and Hayden et al. (15)]: 1) attempts should be made to standardize caries measurements, including using trained and calibrated examiners and standardized clinical and radiographic examinations; 2) more confounders should be controlled for data analyses; 3) ensure that the reporting of the anthropometric categories covers a full range of measurements and the details of the variables are presented when making between-group comparisons; and 4) cohort studies that follow the children from birth to 18 y old are needed to explore long-term associations between children’s growth and dental caries.