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Association of vitamin D and dental caries in children
ORIGINAL CONTRIBUTIONS
Association of vitamin D and dental caries in children Findings from the National Health and Nutrition Examination Survey, 2005-2006 Karin Herzog, DDS, MSD; JoAnna M. Scott, PhD; Philippe Hujoel, PhD, DDS, MSD; Ana Lucia Seminario, DDS, PhD
V
itamin D is a hormone precursor that controls calcium absorption into the small intestine, mediates skeletal mineralization, and maintains calcium hemostasis in the blood stream.1 Vitamin D is naturally produced in certain plants and fish,2 and can be found in supplements or fortified foods, such as milk products, juices, and breakfast cereals.3 It is also synthesized in the skin after exposure to sunlight. Although vitamin D is known mainly for its role in calcium hemostasis, it has been found to be associated with various conditions and diseases. Theodoratou and colleagues’4 umbrella review of vitamin D and health outcomes found suggestive evidence (evidence from randomized controlled trials with an effect at .001 # P # .05 or evidence from meta-analyses of observational studies showing an association of P # .001) of relation between high vitamin D concentrations or vitamin D supplementation and decreased risk of developing colorectal cancer, nonvertebral fractures, cardiovascular disease, hypertension, stroke, depression, body mass index, and type 2 diabetes. Vitamin D exposures in early life may also play a role in dental caries prevention.4-8 Dental caries has remained the most prevalent chronic disease of childhood, 5 times more frequent than asthma and 7 times more common than hay fever.9 Tanaka and colleagues5 found that higher maternal vitamin D intake during pregnancy was associated with a reduced risk of developing caries in children, and Schroth and colleagues6 found that mothers of children with early childhood caries had significantly lower prenatal concentrations of serum 25-hydroxyvitamin D (25[OH]D) levels than
ABSTRACT Background. The authors sought to determine associations between serum vitamin D levels and dental caries in noninstitutionalized children aged 5 to 12 years in the United States. Methods. The authors used National Health and Nutrition Examination Survey, 2005-2006, data to study childhood caries and vitamin D. Vitamin D deficiency and inadequacy were defined as serum 25-hydroxyvitamin D (25[OH]D) less than 30 nanomoles per liter and between 30 and 49 nmol/L, respectively. Associations between vitamin D and caries experience (a combined measure of untreated caries or restorations) were examined after adjustment for confounders using multivariate logistic regression at a critical value of 5%. Sample weights were used to generate nationally representative estimates. Results. The overall prevalence of serum 25(OH)D less than 30 nmol/L and 25(OH)D between 30 and 49 nmol/L among 5- to 12-year-olds was 3% and 16%, respectively. Prevalence of 25(OH)D less than 30 nmol/L and 25(OH)D between 30 and 49 nmol/L among children with caries experience was 2% and 16%, respectively. Multivariate logistic regression analysis found no significant association between vitamin D and caries experience (P ¼ .78). Furthermore, this association was not significant after adjusting for age, sex, race and ethnicity, ratio of family income to poverty threshold, and sugar consumption (P ¼ .46). Conclusions. The authors did not find a significant association between 25(OH)D status and caries experience in US children who participated in NHANES, 2005-2006. Practical Implications. The authors’ findings do not support existing evidence of an association between caries and vitamin D. Key Words. Dental caries; vitamin D; pediatrics. JADA 2016:-(-):--http://dx.doi.org/10.1016/j.adaj.2015.12.013
Copyright ª 2016 American Dental Association. All rights reserved.
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ORIGINAL CONTRIBUTIONS
those whose children were caries-free. Furthermore, caries-free children were twice as likely to have serum 25(OH)D concentrations of 75 nanomoles per liter or more, and those with severe early childhood caries were at nearly 3 times the odds of having levels below 35 nmol/L.7 Hujoel’s8 systematic review and meta-analysis of controlled clinical trials that were conducted in the early 20th century found that supplemental vitamin D was associated with a 47% reduced risk of developing caries. Theodoratou and colleagues4 categorized Hujoel’s findings as probable evidence (significant evidence from both observational studies and randomized controlled trials at P # .001) of relation between high vitamin D concentrations or vitamin D supplementation and decreased risk of developing dental caries in children. Vitamin D supplementation was ineffective after the age of 13 years, however, particularly for girls, suggesting that growth and variations in body fat may influence the way vitamin D is stored and metabolized, and alter the effectiveness of the fat-soluble vitamin D in caries prevention.8 Possible mechanisms by which vitamin D decreases dental caries includes improved tooth development,7,8 immunity, and better dentinal mineralization responses to caries. Ameloblasts and odontoblasts are target cells for 1,25-dihydroxyvitamin D, the active form of vitamin D. Thus, vitamin D plays a role in enamel and dentin formation.7 Vitamin D deficiency is associated with neonatal enamel hypoplasia and hypocalcification.7,10,11 Such developmental defects create a better environment for cariogenic bacteria to colonize and adhere to teeth, increasing susceptibility to dental caries.7,12,13 Vitamin D also plays a role in regulating innate and adaptive immunity7,14-15 and can induce the production of cathelicidin and defensins—antimicrobial peptides that reduce the risk of developing dental caries by attacking cariogenic bacteria.7,16 Multiple studies have analyzed the relationship between dental caries and vitamin D levels.5-8,16-19 A 2015 article by Schroth and colleagues20 explored this relationship with a national representative sample of Canadian children. Having these data and knowing the relationship between geographic location and sun exposure—and other factors affecting vitamin D—we conducted a study looking at dental caries and vitamin D on a national scale in the US pediatric population, who reside at lower latitude than Canadians. Our study sought to determine the association between serum vitamin D levels and dental caries in noninstitutionalized children in the United States, between the ages of 5 and 12 years. METHODS
Study population. For our study, we examined civilian, noninstitutionalized US children, between the ages of 5 to 12 years, who participated in the 2005-2006 National Health and Nutrition Examination Survey (NHANES). NHANES is a stratified, multistage, probability sample
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survey conducted annually by the National Center for Health Statistics.21 NHANES excludes all people in supervised care or custody in institutional settings, all active-duty military personnel, active-duty family members living overseas, and any other US citizens residing outside the 50 states and the District of Columbia.22 We chose the 2005-2006 data set because the newest released vitamin D NHANES data was from 2005-2006. We chose the age range of 5 to 12 years because children younger than 5 years were not eligible for NHANES oral health examinations, and investigators have found decreased effectiveness of vitamin D in caries prevention in those 13 years and older.8 Because NHANES data are deidentified, the institutional review board of the University of Washington, Seattle, WA, waived review of this study. Variables. Demographic variables. NHANES 20052006 collected demographic data for children younger than 12 years by parental and guardian report during inperson interviews. Demographic variables in the analysis included age, sex, race and ethnicity, health insurance, and ratio of family income to poverty threshold. We measured age in years. We categorized race as non-Hispanic white, non-Hispanic black, Hispanic, and other. We categorized health insurance into no health insurance, private health insurance, or public insurance. We categorized the ratio of family income to poverty threshold as below 1, 1 to less than 2, 2 to less than 5, and greater than 5. Dental variables. The dental examinations in NHANES were conducted by health technologists, who were trained and calibrated to do the oral health screenings.23 During the basic screening examination (BSE), the health technologist evaluated study participants using a disposable dental mirror (no tactile assessment with an explorer) and determined whether untreated decay and restorations were present, not present, or could not be assessed. The examining health technologist had access to a dental light for illumination and compressed air to assist in clearing the teeth of residual food debris. We used 4 dental variables in this study: untreated dental caries, dental restorations, overall caries experience, and sealants. All 4 were classified in NHANES as binary variables. The presence of dental caries was defined in NHANES as at least 1 tooth with untreated decay. The tooth or teeth could be primary or permanent. Untreated caries was decay in a tooth that appeared as a darkened fracture with irregular breakdown of the enamel surface of the tooth. The area may have appeared soft and spongy in texture. The following were not considered decay: teeth with stains or pigmentations; stained occlusal pit or fissures
ABBREVIATION KEY. BSE: Basic screening examination. DMFT: Decayed, missing, and filled teeth. NA: Not applicable. NHANES: National Health and Nutrition Examination Survey. 25(OH)D: 25-hydroxyvitamin D.
ORIGINAL CONTRIBUTIONS
TABLE 1
Prevalence of vitamin D deficiency among US children aged 5 to 12 years by demographic characteristics. DEFICIENT 25(OH)D* LESS THAN 30 nmol/L† PREVALENCE, % (95% CI‡)
INADEQUATE 25(OH)D 30 TO 49 nmol/L PREVALENCE, % (95% CI)
SUFFICIENT 25(OH)D 50 TO 125 nmol/L PREVALENCE, % (95% CI)
POSSIBLY HARMFUL 25(OH)D GREATER THAN 125 nmol/L PREVALENCE, % (95% CI)
5
0.73 (0.15-3.49)
10.05 (6.55-15.13)
89.22 (83.60-93.07)
0.00
6
0.85 (0.36-2.00)
14.25 (9.59-20.65)
84.90 (78.09-89.86)
0.00
7
0.85 (0.10-6.82)
11.35 (5.49-22.02)
87.80 (78.07-93.56)
0.00
8
1.54 (0.76-3.09)
9.22 (4.82-16.93)
89.24 (81.22-94.08)
0.00
9
2.49 (0.87-6.91)
22.60 (15.64-31.49)
73.30 (62.81-81.70)
1.61 (0.19-12.19)
10
2.23 (0.77-6.27)
13.68 (8.84-20.57)
84.09 (77.28-89.15)
0.00
11
5.39 (2.98-9.55)
19.80 (13.82-27.53)
72.93 (64.41-80.05)
1.88 (0.22-14.02)
12
5.88 (3.27-10.35)
27.89 (20.27-37.06)
65.13 (54.38-74.53)
1.10 (0.13-8.42)
Overall
2.54 (1.62-3.98)
16.20 (12.91-20.13)
80.71 (76.28-84.48)
0.55 (0.16-1.85)
Male
1.75 (0.66-4.58)
13.64 (10.41-17.67)
83.57 (79.71-86.81)
1.04 (0.31-3.44)
Female
3.42 (2.28-5.09)
19.03 (14.67-24.31)
77.56 (71.23-82.83)
0.00
CHARACTERISTIC
Age, y
Sex
Race and Ethnicity Non-Hispanic white
0.00
7.26 (4.07-12.63)
91.80 (87.05-94.91)
0.94 (0.29-3.01)
Non-Hispanic black
12.58 (8.03-19.17)
36.94 (32.36-41.76)
50.48 (43.05-57.90)
0.00
Hispanic
3.26 (1.85-5.71)
26.83 (20.24-34.62)
69.91 (61.37-77.26)
0.00
Other
1.89 (0.49-7.00)
19.61 (7.90-40.95)
78.51 (59.86-89.94)
0.00
Below 1
3.72 (2.20-6.23)
22.24 (17.31-28.10)
74.04 (66.81-80.17)
0.00
1 to less than 2
4.56 (2.26-8.99)
16.68 (11.07-24.36)
78.75 (69.40-85.83)
0.00
2 to less than 5
1.22 (0.70-2.14)
16.10 (11.62-21.87)
81.37 (75.94-85.80)
1.31 (0.38-4.41)
Greater than 5
1.31 (0.26-6.23)
8.07 (4.06-15.43)
90.62 (83.05-95.01)
0.00
None
1.76 (0.70-4.34)
22.73 (14.62-33.57)
75.52 (64.04-84.23)
0.00
Public
3.51 (2.02-6.02)
18.58 (13.43-25.14)
77.91 (69.94-84.24)
0.00
Private
2.22 (1.13-4.31)
13.74 (10.03-18.53)
83.13 (77.72-87.44)
0.91 (0.27-3.01)
Less than once a week
5.84 (1.75-17.72)
20.94 (8.15-44.16)
73.22 (49.93-88.23)
0.00
Once a week to less than once a day
4.14 (1.50-10.94)
25.32 (15.97-37.68)
70.54 (58.04-80.56)
0.00
Once a day
2.14 (1.31-3.47)
14.47 (11.43-18.16)
82.73 (78.63-86.18)
0.66 (0.19-2.20)
Ratio of Family Income to Poverty Threshold§
Health Insurance
Milk Consumption
* † ‡ §
25(OH)D: 25-hydroxyvitamin D. nmol/L: Nanomoles per liter. CI: Confidence interval. The poverty ratio level represents the ratio of family income to the appropriate poverty threshold. Ratios below 1.00 indicate that the family income is below the poverty threshold, whereas a ratio greater than 1.00 indicates income above the poverty level.26
with no apparent breakdown of the enamel structure; white-spot lesions; dark, shiny, and pitted areas of enamel; and tooth wear or erosion. According to NHANES, a dental restoration was defined as the presence of at least 1 tooth with a restoration. A dental restoration was a restoration in a tooth that could be amalgam, yellow or white gold, a metal crown, a temporary restoration, restorative materials using toothcolored porcelain, ceramic, or resin-based composite.
Fractured or missing restorations were scored as if the restoration was intact. The following were not considered restorations in NHANES: sealants, prosthetic teeth, and crowns that were placed because of malformations, esthetics, or traumatic injuries. We defined overall caries experience as the presence of at least 1 tooth with untreated decay or at least 1 tooth with a restoration, combining untreated dental decay and restorations into 1 variable. According
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ORIGINAL CONTRIBUTIONS
TABLE 2
Prevalence of vitamin D deficiency among US children aged 5 to 12 years by oral health measures. CHARACTERISTIC
DEFICIENT 25(OH)D* LESS THAN 30 nmol/L† PREVALENCE, % (95% CI‡)
INADEQUATE 25(OH)D 30-49 nmol/L PREVALENCE, % (95% CI)
SUFFICIENT 25(OH)D 50-125 nmol/L PREVALENCE, % (95% CI)
POSSIBLY HARMFUL 25(OH)D >125 nmol/L PREVALENCE, % (95% CI)
OVERALL PREVALENCE, % (95% CI)
MEAN (SD§) P VALUE¶ 25(OH)D nmol/L)
.869
Untreated Dental Caries Caries
2.75 (1.45-5.16)
18.00 (10.96-28.14) 79.25 (68.83-86.85)
0.00
19.62 (15.34-23.89) 67.68 (3.17)
No caries
2.48 (1.55-3.96)
15.93 (12.48-20.12) 80.89 (76.11-84.91)
0.69 (0.21-2.31)
80.38 (76.11-84.66) 66.47 (1.78)
Sealants
1.42 (0.69-2.91)
13.97 (10.07-19.06) 83.86 (79.06-87.73)
0.75 (0.08-6.82)
28.17 (23.61-32.72) 67.59 (3.03)
No visible sealants
2.99 (1.76-5.02)
17.30 (13.10-22.49) 79.23 (73.15-84.24)
0.48 (0.11-2.08)
71.83 (67.28-76.39) 66.34 (1.72)
Restoration
2.16 (1.22-3.79)
15.11 (10.77-20.78) 82.25 (75.91-87.21)
0.48 (0.06-3.76)
39.63 (35.21-44.04) 66.78 (2.02)
No restoration
2.78 (1.70-4.53)
17.13 (13.42-21.62) 79.47 (74.75-83.51)
0.61 (0.13-2.76)
60.37 (55.96-64.79) 66.66 (1.93)
.139
Sealants
.965
Restoration
.79
Caries Experience Caries experience
2.37 (1.37-4.05)
15.79 (11.67-21.02) 81.46 (75.73-86.09)
0.38 (0.05-3.00)
50.11 (44.78-55.44) 67.01 (2.00)
No caries experience
2.70 (1.64-4.42)
16.87 (12.70-22.06) 79.69 (74.39-84.12)
0.74 (0.16-3.32)
49.89 (44.56-55.23) 66.41 (1.90)
* 25(OH)D: 25-hydroxyvitamin D. † nmol/L: Nanomoles per liter. ‡ CI: Confidence interval. § SD: Standard deviation. ¶ P values calculated using the Fisher exact test.
to NHANES, the presence of a sealant was defined as the presence of at least 1 tooth with a visible sealant. Milk consumption. We assessed milk intake from the diet, behavior, and nutrition section of the NHANES sample person questionnaire. We determined preceding 30-day milk product consumption by the following question: “In the past 30 days, how often did you have milk to drink or on your cereal? Please include chocolate and other flavored milks as well as hot cocoa made with milk. Do not count small amounts of milk added to coffee or tea.” In this analysis, we categorized milk consumption as less than once per week, between once a week to less than once per day, and once per day. Sugar consumption. We assessed total sugar consumption in a 24-hour period from the NHANES dietary recall interview. Sugar consumption was measured in grams. Vitamin D. In NHANES, serum 25(OH)D measurements were performed on venous blood samples collected in mobile examination centers by using standardized protocols. Measurements were performed by using the DiaSorin radioimmunoassay kit at the National Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, GA. In this analysis, we defined vitamin D deficiency by using the Institute of Medicine 2011 report.24 We defined
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risk of developing vitamin D deficiency as serum 25(OH)D less than 30 nmol/L. We defined risk of developing vitamin D inadequacy as serum 25(OH)D between 30 and 49 nmol/L. We defined vitamin D sufficiency as serum 25(OH)D between 50 and 125 nmol/L. Serum 25(OH)D greater than 125 nmol/L may be a reason for concern and could indicate possibly harmful vitamin D levels.25 Data analysis. We used prevalences to examine the distribution of 25(OH)D less than 30 nmol/L, 25(OH)D between 30 and 49 nmol/L, 25(OH)D between 50 and 125 nmol/L, and 25(OH)D greater than 125 nmol/L. We used adjusted and unadjusted odds ratios (OR) from logistic regression to examine the association between vitamin D and caries experience. We adjusted this multivariate logistic regression model for age, sex, race and ethnicity, ratio of family income to poverty threshold, and sugar consumption; 95% confidence intervals were reported. We performed data analysis using statistical software (Stata version 12.1, StataCorp). We used survey sampling methods adjusted for appropriate sampling weights for all analysis. Weighting schemes allowed estimates to reflect the relative proportions in the population as a whole. For this analysis, a P value less than .05 was considered statistically significant.
ORIGINAL CONTRIBUTIONS
RESULTS
TABLE 3
The overall prevalence Multivariate logistic regression testing the association of 25(OH)D less than between vitamin D and caries experience. 30 nmol/L, and 25(OH)D ASSOCIATION BETWEEN VITAMIN D AND CARIES EXPERIENCE between 30 and 49 nmol/L CHARACTERISTIC among children aged Adjusted* Unadjusted 5 to 12 years was 2.54% P value Total OR (95% CI) P value Total OR† (95% CI‡) and 16.2%, respectively. .465 1,137 NA .777 Vitamin D 1,103 NA§ The prevalence of 760 Reference NA 784 Reference NA Sufficient (50-125 nmol/L¶) 25(OH)D less than 30 Inadequate (30-49 nmol/L) 279 0.69 (0.37-1.29) .224 285 0.83 (0.45-1.54) .538 nmol/L among 5- to Deficient (less than 30 nmol/L) 64 0.65 (0.27-1.52) .296 68 0.74 (0.31-1.79) .483 12-year-olds was greater Age (y) 1,103 1.00 (0.93-1.08) .991 1,325 1.03 (0.95-1.11) .440 among non-Hispanic Sex 1,103 NA .631 1,325 NA .579 blacks (12.58%), girls Male 546 Reference NA 658 Reference NA (3.42%), those with a Female 557 0.89 (0.55-1.45) .631 667 0.88 (0.56-1.40) .579 lower ratio of family Race and Ethnicity 1,103 NA .662 1,325 NA .367 income to poverty Non-Hispanic white 283 Reference NA 340 Reference NA threshold (4.56%), Non-Hispanic black 339 1.09 (0.63-1.89) .733 404 1.36 (0.86-2.13) .174 children who had Hispanic 410 1.21 (0.78-1.87) .362 495 1.30 (0.86-1.98) .198 public health insurance Other 71 0.88 (0.52-1.50) .612 86 0.99 (0.66-1.51) .984 (3.51%), and those who 1,103 NA .003 1,283 NA .024 Ratio of Family Income to consumed less than 1 Poverty Threshold# milk product per week Below 1 298 Reference NA 345 Reference NA (5.84%). The prevalence 1 to less than 2 301 0.96 (0.46-1.97) .899 350 1.05 (0.53-2.09) .876 of 25(OH)D between 2 to less than 5 388 0.58 (0.32-1.05) .069 449 0.75 (0.42-1.35) .316 30 nmol/L and 49 nmol/L Greater than 5 116 0.32 (0.18-0.57) .001 139 0.46 (0.25-0.83) .014 was greater among Total Sugar Consumed (Grams) 1,103 1.003 (1.001-1.005) .002 1,325 1.002 (1.001-1.003) .003 non-Hispanic blacks * The multivariate logistic regression models adjusted for age, sex, race and ethnicity, ratio of family income to (36.94%), girls (19.03%), poverty threshold, and sugar consumption. † OR: Odds ratio. children with a lower ‡ CI: Confidence interval. ratio of family income § NA: Not applicable. ¶ nmol/L: Nanomoles per liter. to poverty threshold # The poverty ratio level represents the ratio of family income to the appropriate poverty threshold. Ratios below (22.24%), those who 1.00 indicate that the family income is below the poverty threshold, whereas a ratio greater than 1.00 indicates had no insurance income above the poverty level.26 (22.73%), and those who consumed between 1 milk product per week to less than 1 milk product per Multivariate logistic regression analysis indicated no day (25.32%). Non-Hispanic whites (91.80%), boys significant association between vitamin D and caries (83.57%), those with a higher ratio of family income experience (P ¼ .78). Furthermore, this association was to poverty threshold (90.62%), children with private not significant after adjusting for age, sex, race and health insurance (83.13%), and those who consumed 1 ethnicity, ratio of family income to poverty threshold, and milk product per day (82.73%) had a higher prevalence of sugar consumption (P ¼ .46) (Table 3). This association 25(OH)D between 50 and 125 nmol/L (Table 1). was still not significant after stratifying by either having The overall prevalence of sealants, restorations, and no visible sealants or at least 1 tooth with a sealant (P ¼ .20 caries experience among 5- to 12-year-olds was 28.17%, and P ¼ .78, respectively) (Table 4). Additional analysis 39.63%, and 50.11%, respectively. The prevalence of looking at different thresholds of 25(OH)D, such as 25(OH)D less than 30 nmol/L, and 25(OH)D between 25(OH)D less than 30 nmol/L compared with 30 nmol/L 30 and 49 nmol/L among children with sealants, was 1.42% or more, and 25(OH)D less than 50 nmol/L compared and 13.97%, respectively. The prevalence of 25(OH)D less with 50 to 125 nmol/L, respectively, did not find any sigthan 30 nmol/L and 25(OH)D between 30 and 49 nmol/L nificant associations between vitamin D and caries among children with dental restorations was 2.16% and experience. 15.11%, respectively. The prevalence of 25(OH)D less than DISCUSSION 30 nmol/L and 25(OH)D between 30 and 49 nmol/L among children with untreated caries or restoration was This is the first study, to our knowledge, that examined 2.37% and 15.79%, respectively (Table 2). the association between vitamin D and dental caries in a
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TABLE 4
and caries was conducted by Mellanby in the 1920s and 1930s.7,18,27 Mellanby’s results showed an association between vitamin D supplementaCHARACTERISTIC ASSOCIATION BETWEEN VITAMIN D AND CARIES EXPERIENCE tion and reduced caries No Visible Sealants* 1 or More Teeth With a Sealant* risk.7,18,27 Other analyses P value Total OR (95% CI) P value Total OR† (95% CI‡) have found that children .198 279 NA .783 Vitamin D 822 NA§ with caries were signifi550 Reference NA 208 Reference NA Sufficient (50-125 nmol/L¶) cantly more likely to have Inadequate (30-49 nmol/L) 220 0.71 (0.47-1.07) .098 59 0.66 (0.16-2.65) .530 low vitamin D concenDeficient (less than 30 nmol/L) 52 0.56 (0.24-1.31) .166 12 1.19 (0.17-8.47) .853 trations.7 Kühnisch and Age (y) 822 1.04 (0.96-1.14) .292 279 0.88 (0.71-1.09) .236 colleagues28 found that a Sex 822 NA .686 279 NA .505 10 nmol/L increase in Male 409 Reference NA 137 Reference NA serum 25(OH)D concenFemale 413 0.90 (0.52-1.55) .686 142 0.87 (0.55-1.35) .505 trations was significantly Race and Ethnicity 822 NA .974 279 NA .339 associated with a lower Non-Hispanic white 192 Reference NA 91 Reference NA OR of having hypominNon-Hispanic black 268 1.09 (0.62-1.93) .745 70 0.88 (0.35-2.22) .777 eralized teeth, and higher Hispanic 309 1.05 (0.56-2.00) .862 100 1.62 (0.74-3.52) .207 25(OH)D values were Other 53 0.95 (0.58-1.56) .822 18 0.83 (0.26-2.64) .735 associated with a reduced 822 NA .009 279 NA .936 Ratio of Family Income to incidence of caries. In Poverty Threshold# addition, maternal preBelow 1 235 Reference NA 62 Reference NA natal 25(OH)D levels in1 to less than 2 228 1.01 (0.61-1.67) .969 73 1.06 (0.14-8.21) .953 fluence the development 2 to less than 5 274 0.53 (0.33-0.85) .013 113 0.86 (0.15-4.92) .855 of early childhood caries,6 Greater than 5 85 0.25 (0.13-0.49) .001 31 0.69 (0.10-4.60) .687 with higher prenatal Total Sugar Consumed 822 1.002 (0.999-1.005) .151 279 1.004 (0.999-1.009) .058 vitamin D intake associ(Grams) ated with a reduced risk * The multivariate logistic regression models adjusted for age, sex, race and ethnicity, ratio of family income to of developing caries in poverty threshold, and sugar consumption. † OR: Odds ratio. children.5 Schroth and ‡ CI: Confidence interval. colleagues20 looked at a § NA: Not applicable. nationally representative ¶ nmol/L: Nanomoles per liter. # The poverty ratio level represents the ratio of family income to the appropriate poverty threshold. Ratios below sample of Canadian chil1.00 indicate that the family income is below the poverty threshold, whereas a ratio greater than 1.00 indicates dren and found that income above the poverty level.26 children with 25(OH)D concentrations of nationally representative sample of US children. The 75 nmol/L or greater had a 39% lower odds of having findings of this study do not provide convincing evidence experienced caries, whereas children with levels of of a relationship between vitamin D exposure and overall 50 nmol/L or greater had a 47% lower odds for caries. caries experience. Our findings on vitamin D deficiency and dental caries were in the direction hypothesized; however, Because dental caries remains the most common we did not observe statistically significant associations chronic disease in childhood,9 efforts to prevent caries beyond clinical care of the oral cavity should be investi- between 25(OH)D less than 30 nmol/L and caries experience. This could be due to several important study gated. Published research has reported vitamin D may aid in preventing dental caries through its role in enamel limitations. We were limited by a lack of information on several potential important confounders, including the and dentin formation7 and production of antimicrobial season of measurement of 25(OH)D levels, lack peptides, which protect from oral pathogens.7,14-16 of information on sun exposure, fluoride exposure, water Furthermore, interventions that provide adequate levels fluoridation status, toothbrushing, detailed geographic of vitamin D are theorized to decrease the prevalence of dental caries in children, affecting other health data, and location of participants’ home. The accuracy of the sugar consumption variable was also a limitation outcomes. because total sugar consumption was based on particiHistorically, multiple studies have suggested that vitamin D can prevent caries onset and progression. pants’ 24 hour dietary recall and subject to recall bias. Early research assessing the relationship between vitamin D In addition, like most population-based sample surveys,
Multivariate logistic regression testing the association between vitamin D and caries experience stratified by visible sealants.
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NHANES experiences both participant and component nonresponse biases.22 Another limitation of the study was the way caries and restorations were diagnosed and classified in NHANES 2005-2006. Beginning in 2005, NHANES switched from a dentist-based oral health examination protocol to an oral health screening conducted by health technologists.23 Studies on the quality assurance for the oral health component of NHANES have supported the use of health technologists in assessing person-based estimators of dental caries and sealant prevalence, citing the high interrater reliability statistics for the BSE between health technologists and the survey reference examiner (Cohen k scores of 0.80 and 0.78 for untreated caries, 0.92 and 0.83 for dental restorations, and 0.79 and 0.85 for dental sealants, respectively).23 Furthermore, starting in 2005, NHANES changed from tooth-surface to person-based estimators of dental caries, restorations, and sealants. The presence of caries or restorations was diagnosed by visual examination, without the aid of radiographs or tactile exploration of teeth. Untreated caries, restorations, and sealants were binary variables, coded as either having the presence of at least 1 tooth with untreated caries, restorations, or sealants or no teeth with untreated dental caries, restorations, or sealants, respectively. Thus, the results underestimate the true prevalence of untreated caries and restorations. It was also not possible to model caries, restorations, or sealants as a continuous variable or know which tooth, type of tooth (primary or permanent) or tooth surface had caries, restorations, or sealants. Furthermore, given this NHANES data set, it was not possible to obtain a total count of the number of decayed, missing, and filled teeth (DMFT), or assess the relationship between 25(OH)D and DMFT. With more detailed information, the relationship between vitamin D and caries could have been further explored. Vitamin D deficiency affects multiple health outcomes, especially in children. Thus, interventions that provide adequate levels of vitamin D, as well as ongoing investigations on the role of vitamin D, can help improve the overall well-being of children. Further studies are needed to explore these areas. CONCLUSIONS
Our findings add to a growing body of knowledge of childhood vitamin D levels and dental caries. We were unable to determine a true association between vitamin D and caries experience in US children participating in the 2005-2006 NHANES. More interventional studies are needed to further examine this topic. n Dr. Herzog was a pediatric dental resident, Department of Pediatric Dentistry, University of Washington, Seattle, WA, when this article was written. She now is a clinical instructor, Department of Dentistry, Oral and
Maxillofacial Surgery, New York Presbyterian Hospital-Weill Cornell Medical College, New York, NY. Address correspondence to Dr. Herzog, The Center for Pediatric Dentistry, 6222 NE 74th St, Seattle, WA 98115, e-mail [email protected]. Dr. Scott is an acting assistant professor and the director of graduate research, Department of Pediatric Dentistry, University of Washington, Seattle, WA. Dr. Hujoel is a professor, Department of Oral Health Sciences, University of Washington, Seattle, WA. Dr. Seminario is an assistant professor, Department of Pediatric Dentistry, University of Washington, Seattle, WA. Disclosure. None of the authors reported any disclosures. 1. Kulie T, Groff A, Redmer J, Hounshell J, Schrager S, Vitamin D: an evidence-based review. J Am Board Fam Med. 2009;22(6):698-706. 2. Holick MF. Vitamin D deficiency. N Engl J Med. 2007;357(3):266-281. 3. Bailey RL, Dodd KW, Goldman JA, et al. Estimation of total usual calcium and vitamin D intakes in the United States. J Nutr. 2010;140(4): 817-822. 4. Theodoratou E, Tzoulaki I, Zgaga L, Ioannidis JP. Vitamin D and multiple health outcomes: umbrella review of systematic reviews and metaanalyses of observational studies and randomised trials. BMJ. 2014;348: g2035. 5. Tanaka K, Hitsumoto S, Miyake Y, et al. Higher vitamin D intake during pregnancy is associated with reduced risk of dental caries in young Japanese children. Ann Epidemiol. 2015;25(8):620-625. 6. Schroth RJ, Lavelle C, Tate R, Bruce S, Billings RJ, Moffatt ME. Prenatal vitamin D and dental caries in infants. Pediatrics. 2014;133(5): e1277-e1284. 7. Schroth RJ, Levi JA, Sellers EA, Friel J, Kliewer E, Moffatt ME. Vitamin D status of children with severe early childhood caries: a case-control study. BMC Pediatr. 2013;13:174. 8. Hujoel PP. Vitamin D and dental caries in controlled clinical trials: systematic review and meta-analysis. Nutr Rev. 2013;71(2):88-97. 9. U.S. Department of Health and Human Services. Oral Health in America: A Report of the Surgeon General. Rockville, MD: U.S. Department of Health and Human Services, National Institute of Dental and Craniofacial Research, National Institutes of Health; 2000. 10. Cockburn F, Belton NR, Purvis RJ, et al. Maternal vitamin D intake and mineral metabolism in mothers and their newborn infants. Br Med J. 1980;281(6232):11-14. 11. Purvis RJ, Barrie WJ, MacKay GS, Wilkinson EM, Cockburn F, Belton NR. Enamel hypoplasia of the teeth associated with neonatal tetany: a manifestation of maternal vitamin-D deficiency. Lancet. 1973;2(7833): 811-814. 12. Hong L, Levy SM, Warren JJ, Broffitt B. Association between enamel hypoplasia and dental caries in primary second molars: a cohort study. Caries Res. 2009;43(5):345-353. 13. Pascoe L, Seow WK. Enamel hypoplasia and dental caries in Australian aboriginal children: prevalence and correlation between the two diseases. Pediatr Dent. 1994;16(3):193-199. 14. Griffin MD, Xing N, Kumar R. Vitamin D and its analogs as regulators of immune activation and antigen presentation. Annu Rev Nutr. 2003;23:117-145. 15. Hewison M. Vitamin D and the immune system: new perspectives on an old theme. Endocrinol Metab Clin North Am. 2010;39(2):365-379. 16. Grant WB. A review of the role of solar ultraviolet-B irradiance and vitamin D in reducing risk of dental caries. Dermatoendocrinol. 2011;3(3): 193-198. 17. Mellanby M. Diet and the Teeth: An Experimental Study. Part III. The Effect of Diet on Dental Structure and Disease in Man. London, UK: His Majesty’s Stationery Office; 1934:1-180. 18. Mellanby M, Pattison CL. The action of vitamin D in preventing the spread and promoting the arrest of caries in children. Br Med J. 1928; 2(3545):1079-1082. 19. Schroth RJ, Jeal NS, Kliewer E, Sellers EA. The relationship between vitamin D and severe early childhood caries: a pilot study. Int J Vitam Nutr Res. 2012;82(1):53-62. 20. Schroth RJ, Rabbani R, Loewen G, Moffatt ME. Vitamin D and dental caries in children [published online ahead of print Nov. 9, 2015]. Journal Dent Res. http://dx.doi.org/10.1177/0022034515616335.
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21. Centers for Disease Control and Prevention, National Health and Nutrition Examination Survey 2005-2006. Available at: http://wwwn.cdc. gov/nchs/nhanes/search/nhanes05_06.aspx. Accessed September 26, 2015. 22. Johnson CL, Paulose-Ram R, Ogden CL, et al. National Health and Nutrition Examination Survey: analytic guidelines, 1999-2010. Vital Health Stat 2. 2013;(161):1-24. 23. Dye BA, Barker LK, Li X, Lewis BG, Beltrán-Aguilar ED. Overview and quality assurance for the oral health component of the National Health and Nutrition Examination Survey (NHANES), 2005-08. J Public Health Dent. 2011;71(1):54-61. 24. Institute of Medicine, Committee to Review Dietary Reference Intakes for Vitamin D and Calcium. Dietary Reference Intakes for Calcium and Vitamin D. Washington, DC: National Academies Press; 2011.
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25. Looker AC, Johnson CL, Lacher DA, Pfeiffer CM, Schleicher RL, Sempos CT. Vitamin D status: United States, 2001-2006. NCHS Data Brief. 2011;(59):1-8. 26. United States Census Bureau. Definitions. Available at: http://www. census.gov/hhes/www/poverty/methods/definitions.html#ratio of income to poverty. Accessed January 15, 2016. 27. Mellanby M. The role of nutrition as a factor in resistance to dental caries. Br Dent J. 1937;62(5):241-252. 28. Kühnisch J, Thiering E, Kratzsch J, Heinrich-Weltzien R, Hickel R, Heinrich J; GINIplus study group; LISAplus study group. Elevated serum 25(OH)-vitamin D levels are negatively correlated with molar-incisor hypomineralization. J Dent Res. 2015;94(2): 381-387.
Association of vitamin D and dental caries in children Findings from the National Health and Nutrition Examination Survey, 2005-2006 Karin Herzog, DDS, MSD; JoAnna M. Scott, PhD; Philippe Hujoel, PhD, DDS, MSD; Ana Lucia Seminario, DDS, PhD
V
itamin D is a hormone precursor that controls calcium absorption into the small intestine, mediates skeletal mineralization, and maintains calcium hemostasis in the blood stream.1 Vitamin D is naturally produced in certain plants and fish,2 and can be found in supplements or fortified foods, such as milk products, juices, and breakfast cereals.3 It is also synthesized in the skin after exposure to sunlight. Although vitamin D is known mainly for its role in calcium hemostasis, it has been found to be associated with various conditions and diseases. Theodoratou and colleagues’4 umbrella review of vitamin D and health outcomes found suggestive evidence (evidence from randomized controlled trials with an effect at .001 # P # .05 or evidence from meta-analyses of observational studies showing an association of P # .001) of relation between high vitamin D concentrations or vitamin D supplementation and decreased risk of developing colorectal cancer, nonvertebral fractures, cardiovascular disease, hypertension, stroke, depression, body mass index, and type 2 diabetes. Vitamin D exposures in early life may also play a role in dental caries prevention.4-8 Dental caries has remained the most prevalent chronic disease of childhood, 5 times more frequent than asthma and 7 times more common than hay fever.9 Tanaka and colleagues5 found that higher maternal vitamin D intake during pregnancy was associated with a reduced risk of developing caries in children, and Schroth and colleagues6 found that mothers of children with early childhood caries had significantly lower prenatal concentrations of serum 25-hydroxyvitamin D (25[OH]D) levels than
ABSTRACT Background. The authors sought to determine associations between serum vitamin D levels and dental caries in noninstitutionalized children aged 5 to 12 years in the United States. Methods. The authors used National Health and Nutrition Examination Survey, 2005-2006, data to study childhood caries and vitamin D. Vitamin D deficiency and inadequacy were defined as serum 25-hydroxyvitamin D (25[OH]D) less than 30 nanomoles per liter and between 30 and 49 nmol/L, respectively. Associations between vitamin D and caries experience (a combined measure of untreated caries or restorations) were examined after adjustment for confounders using multivariate logistic regression at a critical value of 5%. Sample weights were used to generate nationally representative estimates. Results. The overall prevalence of serum 25(OH)D less than 30 nmol/L and 25(OH)D between 30 and 49 nmol/L among 5- to 12-year-olds was 3% and 16%, respectively. Prevalence of 25(OH)D less than 30 nmol/L and 25(OH)D between 30 and 49 nmol/L among children with caries experience was 2% and 16%, respectively. Multivariate logistic regression analysis found no significant association between vitamin D and caries experience (P ¼ .78). Furthermore, this association was not significant after adjusting for age, sex, race and ethnicity, ratio of family income to poverty threshold, and sugar consumption (P ¼ .46). Conclusions. The authors did not find a significant association between 25(OH)D status and caries experience in US children who participated in NHANES, 2005-2006. Practical Implications. The authors’ findings do not support existing evidence of an association between caries and vitamin D. Key Words. Dental caries; vitamin D; pediatrics. JADA 2016:-(-):--http://dx.doi.org/10.1016/j.adaj.2015.12.013
Copyright ª 2016 American Dental Association. All rights reserved.
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those whose children were caries-free. Furthermore, caries-free children were twice as likely to have serum 25(OH)D concentrations of 75 nanomoles per liter or more, and those with severe early childhood caries were at nearly 3 times the odds of having levels below 35 nmol/L.7 Hujoel’s8 systematic review and meta-analysis of controlled clinical trials that were conducted in the early 20th century found that supplemental vitamin D was associated with a 47% reduced risk of developing caries. Theodoratou and colleagues4 categorized Hujoel’s findings as probable evidence (significant evidence from both observational studies and randomized controlled trials at P # .001) of relation between high vitamin D concentrations or vitamin D supplementation and decreased risk of developing dental caries in children. Vitamin D supplementation was ineffective after the age of 13 years, however, particularly for girls, suggesting that growth and variations in body fat may influence the way vitamin D is stored and metabolized, and alter the effectiveness of the fat-soluble vitamin D in caries prevention.8 Possible mechanisms by which vitamin D decreases dental caries includes improved tooth development,7,8 immunity, and better dentinal mineralization responses to caries. Ameloblasts and odontoblasts are target cells for 1,25-dihydroxyvitamin D, the active form of vitamin D. Thus, vitamin D plays a role in enamel and dentin formation.7 Vitamin D deficiency is associated with neonatal enamel hypoplasia and hypocalcification.7,10,11 Such developmental defects create a better environment for cariogenic bacteria to colonize and adhere to teeth, increasing susceptibility to dental caries.7,12,13 Vitamin D also plays a role in regulating innate and adaptive immunity7,14-15 and can induce the production of cathelicidin and defensins—antimicrobial peptides that reduce the risk of developing dental caries by attacking cariogenic bacteria.7,16 Multiple studies have analyzed the relationship between dental caries and vitamin D levels.5-8,16-19 A 2015 article by Schroth and colleagues20 explored this relationship with a national representative sample of Canadian children. Having these data and knowing the relationship between geographic location and sun exposure—and other factors affecting vitamin D—we conducted a study looking at dental caries and vitamin D on a national scale in the US pediatric population, who reside at lower latitude than Canadians. Our study sought to determine the association between serum vitamin D levels and dental caries in noninstitutionalized children in the United States, between the ages of 5 and 12 years. METHODS
Study population. For our study, we examined civilian, noninstitutionalized US children, between the ages of 5 to 12 years, who participated in the 2005-2006 National Health and Nutrition Examination Survey (NHANES). NHANES is a stratified, multistage, probability sample
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survey conducted annually by the National Center for Health Statistics.21 NHANES excludes all people in supervised care or custody in institutional settings, all active-duty military personnel, active-duty family members living overseas, and any other US citizens residing outside the 50 states and the District of Columbia.22 We chose the 2005-2006 data set because the newest released vitamin D NHANES data was from 2005-2006. We chose the age range of 5 to 12 years because children younger than 5 years were not eligible for NHANES oral health examinations, and investigators have found decreased effectiveness of vitamin D in caries prevention in those 13 years and older.8 Because NHANES data are deidentified, the institutional review board of the University of Washington, Seattle, WA, waived review of this study. Variables. Demographic variables. NHANES 20052006 collected demographic data for children younger than 12 years by parental and guardian report during inperson interviews. Demographic variables in the analysis included age, sex, race and ethnicity, health insurance, and ratio of family income to poverty threshold. We measured age in years. We categorized race as non-Hispanic white, non-Hispanic black, Hispanic, and other. We categorized health insurance into no health insurance, private health insurance, or public insurance. We categorized the ratio of family income to poverty threshold as below 1, 1 to less than 2, 2 to less than 5, and greater than 5. Dental variables. The dental examinations in NHANES were conducted by health technologists, who were trained and calibrated to do the oral health screenings.23 During the basic screening examination (BSE), the health technologist evaluated study participants using a disposable dental mirror (no tactile assessment with an explorer) and determined whether untreated decay and restorations were present, not present, or could not be assessed. The examining health technologist had access to a dental light for illumination and compressed air to assist in clearing the teeth of residual food debris. We used 4 dental variables in this study: untreated dental caries, dental restorations, overall caries experience, and sealants. All 4 were classified in NHANES as binary variables. The presence of dental caries was defined in NHANES as at least 1 tooth with untreated decay. The tooth or teeth could be primary or permanent. Untreated caries was decay in a tooth that appeared as a darkened fracture with irregular breakdown of the enamel surface of the tooth. The area may have appeared soft and spongy in texture. The following were not considered decay: teeth with stains or pigmentations; stained occlusal pit or fissures
ABBREVIATION KEY. BSE: Basic screening examination. DMFT: Decayed, missing, and filled teeth. NA: Not applicable. NHANES: National Health and Nutrition Examination Survey. 25(OH)D: 25-hydroxyvitamin D.
ORIGINAL CONTRIBUTIONS
TABLE 1
Prevalence of vitamin D deficiency among US children aged 5 to 12 years by demographic characteristics. DEFICIENT 25(OH)D* LESS THAN 30 nmol/L† PREVALENCE, % (95% CI‡)
INADEQUATE 25(OH)D 30 TO 49 nmol/L PREVALENCE, % (95% CI)
SUFFICIENT 25(OH)D 50 TO 125 nmol/L PREVALENCE, % (95% CI)
POSSIBLY HARMFUL 25(OH)D GREATER THAN 125 nmol/L PREVALENCE, % (95% CI)
5
0.73 (0.15-3.49)
10.05 (6.55-15.13)
89.22 (83.60-93.07)
0.00
6
0.85 (0.36-2.00)
14.25 (9.59-20.65)
84.90 (78.09-89.86)
0.00
7
0.85 (0.10-6.82)
11.35 (5.49-22.02)
87.80 (78.07-93.56)
0.00
8
1.54 (0.76-3.09)
9.22 (4.82-16.93)
89.24 (81.22-94.08)
0.00
9
2.49 (0.87-6.91)
22.60 (15.64-31.49)
73.30 (62.81-81.70)
1.61 (0.19-12.19)
10
2.23 (0.77-6.27)
13.68 (8.84-20.57)
84.09 (77.28-89.15)
0.00
11
5.39 (2.98-9.55)
19.80 (13.82-27.53)
72.93 (64.41-80.05)
1.88 (0.22-14.02)
12
5.88 (3.27-10.35)
27.89 (20.27-37.06)
65.13 (54.38-74.53)
1.10 (0.13-8.42)
Overall
2.54 (1.62-3.98)
16.20 (12.91-20.13)
80.71 (76.28-84.48)
0.55 (0.16-1.85)
Male
1.75 (0.66-4.58)
13.64 (10.41-17.67)
83.57 (79.71-86.81)
1.04 (0.31-3.44)
Female
3.42 (2.28-5.09)
19.03 (14.67-24.31)
77.56 (71.23-82.83)
0.00
CHARACTERISTIC
Age, y
Sex
Race and Ethnicity Non-Hispanic white
0.00
7.26 (4.07-12.63)
91.80 (87.05-94.91)
0.94 (0.29-3.01)
Non-Hispanic black
12.58 (8.03-19.17)
36.94 (32.36-41.76)
50.48 (43.05-57.90)
0.00
Hispanic
3.26 (1.85-5.71)
26.83 (20.24-34.62)
69.91 (61.37-77.26)
0.00
Other
1.89 (0.49-7.00)
19.61 (7.90-40.95)
78.51 (59.86-89.94)
0.00
Below 1
3.72 (2.20-6.23)
22.24 (17.31-28.10)
74.04 (66.81-80.17)
0.00
1 to less than 2
4.56 (2.26-8.99)
16.68 (11.07-24.36)
78.75 (69.40-85.83)
0.00
2 to less than 5
1.22 (0.70-2.14)
16.10 (11.62-21.87)
81.37 (75.94-85.80)
1.31 (0.38-4.41)
Greater than 5
1.31 (0.26-6.23)
8.07 (4.06-15.43)
90.62 (83.05-95.01)
0.00
None
1.76 (0.70-4.34)
22.73 (14.62-33.57)
75.52 (64.04-84.23)
0.00
Public
3.51 (2.02-6.02)
18.58 (13.43-25.14)
77.91 (69.94-84.24)
0.00
Private
2.22 (1.13-4.31)
13.74 (10.03-18.53)
83.13 (77.72-87.44)
0.91 (0.27-3.01)
Less than once a week
5.84 (1.75-17.72)
20.94 (8.15-44.16)
73.22 (49.93-88.23)
0.00
Once a week to less than once a day
4.14 (1.50-10.94)
25.32 (15.97-37.68)
70.54 (58.04-80.56)
0.00
Once a day
2.14 (1.31-3.47)
14.47 (11.43-18.16)
82.73 (78.63-86.18)
0.66 (0.19-2.20)
Ratio of Family Income to Poverty Threshold§
Health Insurance
Milk Consumption
* † ‡ §
25(OH)D: 25-hydroxyvitamin D. nmol/L: Nanomoles per liter. CI: Confidence interval. The poverty ratio level represents the ratio of family income to the appropriate poverty threshold. Ratios below 1.00 indicate that the family income is below the poverty threshold, whereas a ratio greater than 1.00 indicates income above the poverty level.26
with no apparent breakdown of the enamel structure; white-spot lesions; dark, shiny, and pitted areas of enamel; and tooth wear or erosion. According to NHANES, a dental restoration was defined as the presence of at least 1 tooth with a restoration. A dental restoration was a restoration in a tooth that could be amalgam, yellow or white gold, a metal crown, a temporary restoration, restorative materials using toothcolored porcelain, ceramic, or resin-based composite.
Fractured or missing restorations were scored as if the restoration was intact. The following were not considered restorations in NHANES: sealants, prosthetic teeth, and crowns that were placed because of malformations, esthetics, or traumatic injuries. We defined overall caries experience as the presence of at least 1 tooth with untreated decay or at least 1 tooth with a restoration, combining untreated dental decay and restorations into 1 variable. According
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TABLE 2
Prevalence of vitamin D deficiency among US children aged 5 to 12 years by oral health measures. CHARACTERISTIC
DEFICIENT 25(OH)D* LESS THAN 30 nmol/L† PREVALENCE, % (95% CI‡)
INADEQUATE 25(OH)D 30-49 nmol/L PREVALENCE, % (95% CI)
SUFFICIENT 25(OH)D 50-125 nmol/L PREVALENCE, % (95% CI)
POSSIBLY HARMFUL 25(OH)D >125 nmol/L PREVALENCE, % (95% CI)
OVERALL PREVALENCE, % (95% CI)
MEAN (SD§) P VALUE¶ 25(OH)D nmol/L)
.869
Untreated Dental Caries Caries
2.75 (1.45-5.16)
18.00 (10.96-28.14) 79.25 (68.83-86.85)
0.00
19.62 (15.34-23.89) 67.68 (3.17)
No caries
2.48 (1.55-3.96)
15.93 (12.48-20.12) 80.89 (76.11-84.91)
0.69 (0.21-2.31)
80.38 (76.11-84.66) 66.47 (1.78)
Sealants
1.42 (0.69-2.91)
13.97 (10.07-19.06) 83.86 (79.06-87.73)
0.75 (0.08-6.82)
28.17 (23.61-32.72) 67.59 (3.03)
No visible sealants
2.99 (1.76-5.02)
17.30 (13.10-22.49) 79.23 (73.15-84.24)
0.48 (0.11-2.08)
71.83 (67.28-76.39) 66.34 (1.72)
Restoration
2.16 (1.22-3.79)
15.11 (10.77-20.78) 82.25 (75.91-87.21)
0.48 (0.06-3.76)
39.63 (35.21-44.04) 66.78 (2.02)
No restoration
2.78 (1.70-4.53)
17.13 (13.42-21.62) 79.47 (74.75-83.51)
0.61 (0.13-2.76)
60.37 (55.96-64.79) 66.66 (1.93)
.139
Sealants
.965
Restoration
.79
Caries Experience Caries experience
2.37 (1.37-4.05)
15.79 (11.67-21.02) 81.46 (75.73-86.09)
0.38 (0.05-3.00)
50.11 (44.78-55.44) 67.01 (2.00)
No caries experience
2.70 (1.64-4.42)
16.87 (12.70-22.06) 79.69 (74.39-84.12)
0.74 (0.16-3.32)
49.89 (44.56-55.23) 66.41 (1.90)
* 25(OH)D: 25-hydroxyvitamin D. † nmol/L: Nanomoles per liter. ‡ CI: Confidence interval. § SD: Standard deviation. ¶ P values calculated using the Fisher exact test.
to NHANES, the presence of a sealant was defined as the presence of at least 1 tooth with a visible sealant. Milk consumption. We assessed milk intake from the diet, behavior, and nutrition section of the NHANES sample person questionnaire. We determined preceding 30-day milk product consumption by the following question: “In the past 30 days, how often did you have milk to drink or on your cereal? Please include chocolate and other flavored milks as well as hot cocoa made with milk. Do not count small amounts of milk added to coffee or tea.” In this analysis, we categorized milk consumption as less than once per week, between once a week to less than once per day, and once per day. Sugar consumption. We assessed total sugar consumption in a 24-hour period from the NHANES dietary recall interview. Sugar consumption was measured in grams. Vitamin D. In NHANES, serum 25(OH)D measurements were performed on venous blood samples collected in mobile examination centers by using standardized protocols. Measurements were performed by using the DiaSorin radioimmunoassay kit at the National Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, GA. In this analysis, we defined vitamin D deficiency by using the Institute of Medicine 2011 report.24 We defined
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risk of developing vitamin D deficiency as serum 25(OH)D less than 30 nmol/L. We defined risk of developing vitamin D inadequacy as serum 25(OH)D between 30 and 49 nmol/L. We defined vitamin D sufficiency as serum 25(OH)D between 50 and 125 nmol/L. Serum 25(OH)D greater than 125 nmol/L may be a reason for concern and could indicate possibly harmful vitamin D levels.25 Data analysis. We used prevalences to examine the distribution of 25(OH)D less than 30 nmol/L, 25(OH)D between 30 and 49 nmol/L, 25(OH)D between 50 and 125 nmol/L, and 25(OH)D greater than 125 nmol/L. We used adjusted and unadjusted odds ratios (OR) from logistic regression to examine the association between vitamin D and caries experience. We adjusted this multivariate logistic regression model for age, sex, race and ethnicity, ratio of family income to poverty threshold, and sugar consumption; 95% confidence intervals were reported. We performed data analysis using statistical software (Stata version 12.1, StataCorp). We used survey sampling methods adjusted for appropriate sampling weights for all analysis. Weighting schemes allowed estimates to reflect the relative proportions in the population as a whole. For this analysis, a P value less than .05 was considered statistically significant.
ORIGINAL CONTRIBUTIONS
RESULTS
TABLE 3
The overall prevalence Multivariate logistic regression testing the association of 25(OH)D less than between vitamin D and caries experience. 30 nmol/L, and 25(OH)D ASSOCIATION BETWEEN VITAMIN D AND CARIES EXPERIENCE between 30 and 49 nmol/L CHARACTERISTIC among children aged Adjusted* Unadjusted 5 to 12 years was 2.54% P value Total OR (95% CI) P value Total OR† (95% CI‡) and 16.2%, respectively. .465 1,137 NA .777 Vitamin D 1,103 NA§ The prevalence of 760 Reference NA 784 Reference NA Sufficient (50-125 nmol/L¶) 25(OH)D less than 30 Inadequate (30-49 nmol/L) 279 0.69 (0.37-1.29) .224 285 0.83 (0.45-1.54) .538 nmol/L among 5- to Deficient (less than 30 nmol/L) 64 0.65 (0.27-1.52) .296 68 0.74 (0.31-1.79) .483 12-year-olds was greater Age (y) 1,103 1.00 (0.93-1.08) .991 1,325 1.03 (0.95-1.11) .440 among non-Hispanic Sex 1,103 NA .631 1,325 NA .579 blacks (12.58%), girls Male 546 Reference NA 658 Reference NA (3.42%), those with a Female 557 0.89 (0.55-1.45) .631 667 0.88 (0.56-1.40) .579 lower ratio of family Race and Ethnicity 1,103 NA .662 1,325 NA .367 income to poverty Non-Hispanic white 283 Reference NA 340 Reference NA threshold (4.56%), Non-Hispanic black 339 1.09 (0.63-1.89) .733 404 1.36 (0.86-2.13) .174 children who had Hispanic 410 1.21 (0.78-1.87) .362 495 1.30 (0.86-1.98) .198 public health insurance Other 71 0.88 (0.52-1.50) .612 86 0.99 (0.66-1.51) .984 (3.51%), and those who 1,103 NA .003 1,283 NA .024 Ratio of Family Income to consumed less than 1 Poverty Threshold# milk product per week Below 1 298 Reference NA 345 Reference NA (5.84%). The prevalence 1 to less than 2 301 0.96 (0.46-1.97) .899 350 1.05 (0.53-2.09) .876 of 25(OH)D between 2 to less than 5 388 0.58 (0.32-1.05) .069 449 0.75 (0.42-1.35) .316 30 nmol/L and 49 nmol/L Greater than 5 116 0.32 (0.18-0.57) .001 139 0.46 (0.25-0.83) .014 was greater among Total Sugar Consumed (Grams) 1,103 1.003 (1.001-1.005) .002 1,325 1.002 (1.001-1.003) .003 non-Hispanic blacks * The multivariate logistic regression models adjusted for age, sex, race and ethnicity, ratio of family income to (36.94%), girls (19.03%), poverty threshold, and sugar consumption. † OR: Odds ratio. children with a lower ‡ CI: Confidence interval. ratio of family income § NA: Not applicable. ¶ nmol/L: Nanomoles per liter. to poverty threshold # The poverty ratio level represents the ratio of family income to the appropriate poverty threshold. Ratios below (22.24%), those who 1.00 indicate that the family income is below the poverty threshold, whereas a ratio greater than 1.00 indicates had no insurance income above the poverty level.26 (22.73%), and those who consumed between 1 milk product per week to less than 1 milk product per Multivariate logistic regression analysis indicated no day (25.32%). Non-Hispanic whites (91.80%), boys significant association between vitamin D and caries (83.57%), those with a higher ratio of family income experience (P ¼ .78). Furthermore, this association was to poverty threshold (90.62%), children with private not significant after adjusting for age, sex, race and health insurance (83.13%), and those who consumed 1 ethnicity, ratio of family income to poverty threshold, and milk product per day (82.73%) had a higher prevalence of sugar consumption (P ¼ .46) (Table 3). This association 25(OH)D between 50 and 125 nmol/L (Table 1). was still not significant after stratifying by either having The overall prevalence of sealants, restorations, and no visible sealants or at least 1 tooth with a sealant (P ¼ .20 caries experience among 5- to 12-year-olds was 28.17%, and P ¼ .78, respectively) (Table 4). Additional analysis 39.63%, and 50.11%, respectively. The prevalence of looking at different thresholds of 25(OH)D, such as 25(OH)D less than 30 nmol/L, and 25(OH)D between 25(OH)D less than 30 nmol/L compared with 30 nmol/L 30 and 49 nmol/L among children with sealants, was 1.42% or more, and 25(OH)D less than 50 nmol/L compared and 13.97%, respectively. The prevalence of 25(OH)D less with 50 to 125 nmol/L, respectively, did not find any sigthan 30 nmol/L and 25(OH)D between 30 and 49 nmol/L nificant associations between vitamin D and caries among children with dental restorations was 2.16% and experience. 15.11%, respectively. The prevalence of 25(OH)D less than DISCUSSION 30 nmol/L and 25(OH)D between 30 and 49 nmol/L among children with untreated caries or restoration was This is the first study, to our knowledge, that examined 2.37% and 15.79%, respectively (Table 2). the association between vitamin D and dental caries in a
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TABLE 4
and caries was conducted by Mellanby in the 1920s and 1930s.7,18,27 Mellanby’s results showed an association between vitamin D supplementaCHARACTERISTIC ASSOCIATION BETWEEN VITAMIN D AND CARIES EXPERIENCE tion and reduced caries No Visible Sealants* 1 or More Teeth With a Sealant* risk.7,18,27 Other analyses P value Total OR (95% CI) P value Total OR† (95% CI‡) have found that children .198 279 NA .783 Vitamin D 822 NA§ with caries were signifi550 Reference NA 208 Reference NA Sufficient (50-125 nmol/L¶) cantly more likely to have Inadequate (30-49 nmol/L) 220 0.71 (0.47-1.07) .098 59 0.66 (0.16-2.65) .530 low vitamin D concenDeficient (less than 30 nmol/L) 52 0.56 (0.24-1.31) .166 12 1.19 (0.17-8.47) .853 trations.7 Kühnisch and Age (y) 822 1.04 (0.96-1.14) .292 279 0.88 (0.71-1.09) .236 colleagues28 found that a Sex 822 NA .686 279 NA .505 10 nmol/L increase in Male 409 Reference NA 137 Reference NA serum 25(OH)D concenFemale 413 0.90 (0.52-1.55) .686 142 0.87 (0.55-1.35) .505 trations was significantly Race and Ethnicity 822 NA .974 279 NA .339 associated with a lower Non-Hispanic white 192 Reference NA 91 Reference NA OR of having hypominNon-Hispanic black 268 1.09 (0.62-1.93) .745 70 0.88 (0.35-2.22) .777 eralized teeth, and higher Hispanic 309 1.05 (0.56-2.00) .862 100 1.62 (0.74-3.52) .207 25(OH)D values were Other 53 0.95 (0.58-1.56) .822 18 0.83 (0.26-2.64) .735 associated with a reduced 822 NA .009 279 NA .936 Ratio of Family Income to incidence of caries. In Poverty Threshold# addition, maternal preBelow 1 235 Reference NA 62 Reference NA natal 25(OH)D levels in1 to less than 2 228 1.01 (0.61-1.67) .969 73 1.06 (0.14-8.21) .953 fluence the development 2 to less than 5 274 0.53 (0.33-0.85) .013 113 0.86 (0.15-4.92) .855 of early childhood caries,6 Greater than 5 85 0.25 (0.13-0.49) .001 31 0.69 (0.10-4.60) .687 with higher prenatal Total Sugar Consumed 822 1.002 (0.999-1.005) .151 279 1.004 (0.999-1.009) .058 vitamin D intake associ(Grams) ated with a reduced risk * The multivariate logistic regression models adjusted for age, sex, race and ethnicity, ratio of family income to of developing caries in poverty threshold, and sugar consumption. † OR: Odds ratio. children.5 Schroth and ‡ CI: Confidence interval. colleagues20 looked at a § NA: Not applicable. nationally representative ¶ nmol/L: Nanomoles per liter. # The poverty ratio level represents the ratio of family income to the appropriate poverty threshold. Ratios below sample of Canadian chil1.00 indicate that the family income is below the poverty threshold, whereas a ratio greater than 1.00 indicates dren and found that income above the poverty level.26 children with 25(OH)D concentrations of nationally representative sample of US children. The 75 nmol/L or greater had a 39% lower odds of having findings of this study do not provide convincing evidence experienced caries, whereas children with levels of of a relationship between vitamin D exposure and overall 50 nmol/L or greater had a 47% lower odds for caries. caries experience. Our findings on vitamin D deficiency and dental caries were in the direction hypothesized; however, Because dental caries remains the most common we did not observe statistically significant associations chronic disease in childhood,9 efforts to prevent caries beyond clinical care of the oral cavity should be investi- between 25(OH)D less than 30 nmol/L and caries experience. This could be due to several important study gated. Published research has reported vitamin D may aid in preventing dental caries through its role in enamel limitations. We were limited by a lack of information on several potential important confounders, including the and dentin formation7 and production of antimicrobial season of measurement of 25(OH)D levels, lack peptides, which protect from oral pathogens.7,14-16 of information on sun exposure, fluoride exposure, water Furthermore, interventions that provide adequate levels fluoridation status, toothbrushing, detailed geographic of vitamin D are theorized to decrease the prevalence of dental caries in children, affecting other health data, and location of participants’ home. The accuracy of the sugar consumption variable was also a limitation outcomes. because total sugar consumption was based on particiHistorically, multiple studies have suggested that vitamin D can prevent caries onset and progression. pants’ 24 hour dietary recall and subject to recall bias. Early research assessing the relationship between vitamin D In addition, like most population-based sample surveys,
Multivariate logistic regression testing the association between vitamin D and caries experience stratified by visible sealants.
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NHANES experiences both participant and component nonresponse biases.22 Another limitation of the study was the way caries and restorations were diagnosed and classified in NHANES 2005-2006. Beginning in 2005, NHANES switched from a dentist-based oral health examination protocol to an oral health screening conducted by health technologists.23 Studies on the quality assurance for the oral health component of NHANES have supported the use of health technologists in assessing person-based estimators of dental caries and sealant prevalence, citing the high interrater reliability statistics for the BSE between health technologists and the survey reference examiner (Cohen k scores of 0.80 and 0.78 for untreated caries, 0.92 and 0.83 for dental restorations, and 0.79 and 0.85 for dental sealants, respectively).23 Furthermore, starting in 2005, NHANES changed from tooth-surface to person-based estimators of dental caries, restorations, and sealants. The presence of caries or restorations was diagnosed by visual examination, without the aid of radiographs or tactile exploration of teeth. Untreated caries, restorations, and sealants were binary variables, coded as either having the presence of at least 1 tooth with untreated caries, restorations, or sealants or no teeth with untreated dental caries, restorations, or sealants, respectively. Thus, the results underestimate the true prevalence of untreated caries and restorations. It was also not possible to model caries, restorations, or sealants as a continuous variable or know which tooth, type of tooth (primary or permanent) or tooth surface had caries, restorations, or sealants. Furthermore, given this NHANES data set, it was not possible to obtain a total count of the number of decayed, missing, and filled teeth (DMFT), or assess the relationship between 25(OH)D and DMFT. With more detailed information, the relationship between vitamin D and caries could have been further explored. Vitamin D deficiency affects multiple health outcomes, especially in children. Thus, interventions that provide adequate levels of vitamin D, as well as ongoing investigations on the role of vitamin D, can help improve the overall well-being of children. Further studies are needed to explore these areas. CONCLUSIONS
Our findings add to a growing body of knowledge of childhood vitamin D levels and dental caries. We were unable to determine a true association between vitamin D and caries experience in US children participating in the 2005-2006 NHANES. More interventional studies are needed to further examine this topic. n Dr. Herzog was a pediatric dental resident, Department of Pediatric Dentistry, University of Washington, Seattle, WA, when this article was written. She now is a clinical instructor, Department of Dentistry, Oral and
Maxillofacial Surgery, New York Presbyterian Hospital-Weill Cornell Medical College, New York, NY. Address correspondence to Dr. Herzog, The Center for Pediatric Dentistry, 6222 NE 74th St, Seattle, WA 98115, e-mail [email protected]. Dr. Scott is an acting assistant professor and the director of graduate research, Department of Pediatric Dentistry, University of Washington, Seattle, WA. Dr. Hujoel is a professor, Department of Oral Health Sciences, University of Washington, Seattle, WA. Dr. Seminario is an assistant professor, Department of Pediatric Dentistry, University of Washington, Seattle, WA. Disclosure. None of the authors reported any disclosures. 1. Kulie T, Groff A, Redmer J, Hounshell J, Schrager S, Vitamin D: an evidence-based review. J Am Board Fam Med. 2009;22(6):698-706. 2. Holick MF. Vitamin D deficiency. N Engl J Med. 2007;357(3):266-281. 3. Bailey RL, Dodd KW, Goldman JA, et al. Estimation of total usual calcium and vitamin D intakes in the United States. J Nutr. 2010;140(4): 817-822. 4. Theodoratou E, Tzoulaki I, Zgaga L, Ioannidis JP. Vitamin D and multiple health outcomes: umbrella review of systematic reviews and metaanalyses of observational studies and randomised trials. BMJ. 2014;348: g2035. 5. Tanaka K, Hitsumoto S, Miyake Y, et al. Higher vitamin D intake during pregnancy is associated with reduced risk of dental caries in young Japanese children. Ann Epidemiol. 2015;25(8):620-625. 6. Schroth RJ, Lavelle C, Tate R, Bruce S, Billings RJ, Moffatt ME. Prenatal vitamin D and dental caries in infants. Pediatrics. 2014;133(5): e1277-e1284. 7. Schroth RJ, Levi JA, Sellers EA, Friel J, Kliewer E, Moffatt ME. Vitamin D status of children with severe early childhood caries: a case-control study. BMC Pediatr. 2013;13:174. 8. Hujoel PP. Vitamin D and dental caries in controlled clinical trials: systematic review and meta-analysis. Nutr Rev. 2013;71(2):88-97. 9. U.S. Department of Health and Human Services. Oral Health in America: A Report of the Surgeon General. Rockville, MD: U.S. Department of Health and Human Services, National Institute of Dental and Craniofacial Research, National Institutes of Health; 2000. 10. Cockburn F, Belton NR, Purvis RJ, et al. Maternal vitamin D intake and mineral metabolism in mothers and their newborn infants. Br Med J. 1980;281(6232):11-14. 11. Purvis RJ, Barrie WJ, MacKay GS, Wilkinson EM, Cockburn F, Belton NR. Enamel hypoplasia of the teeth associated with neonatal tetany: a manifestation of maternal vitamin-D deficiency. Lancet. 1973;2(7833): 811-814. 12. Hong L, Levy SM, Warren JJ, Broffitt B. Association between enamel hypoplasia and dental caries in primary second molars: a cohort study. Caries Res. 2009;43(5):345-353. 13. Pascoe L, Seow WK. Enamel hypoplasia and dental caries in Australian aboriginal children: prevalence and correlation between the two diseases. Pediatr Dent. 1994;16(3):193-199. 14. Griffin MD, Xing N, Kumar R. Vitamin D and its analogs as regulators of immune activation and antigen presentation. Annu Rev Nutr. 2003;23:117-145. 15. Hewison M. Vitamin D and the immune system: new perspectives on an old theme. Endocrinol Metab Clin North Am. 2010;39(2):365-379. 16. Grant WB. A review of the role of solar ultraviolet-B irradiance and vitamin D in reducing risk of dental caries. Dermatoendocrinol. 2011;3(3): 193-198. 17. Mellanby M. Diet and the Teeth: An Experimental Study. Part III. The Effect of Diet on Dental Structure and Disease in Man. London, UK: His Majesty’s Stationery Office; 1934:1-180. 18. Mellanby M, Pattison CL. The action of vitamin D in preventing the spread and promoting the arrest of caries in children. Br Med J. 1928; 2(3545):1079-1082. 19. Schroth RJ, Jeal NS, Kliewer E, Sellers EA. The relationship between vitamin D and severe early childhood caries: a pilot study. Int J Vitam Nutr Res. 2012;82(1):53-62. 20. Schroth RJ, Rabbani R, Loewen G, Moffatt ME. Vitamin D and dental caries in children [published online ahead of print Nov. 9, 2015]. Journal Dent Res. http://dx.doi.org/10.1177/0022034515616335.
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21. Centers for Disease Control and Prevention, National Health and Nutrition Examination Survey 2005-2006. Available at: http://wwwn.cdc. gov/nchs/nhanes/search/nhanes05_06.aspx. Accessed September 26, 2015. 22. Johnson CL, Paulose-Ram R, Ogden CL, et al. National Health and Nutrition Examination Survey: analytic guidelines, 1999-2010. Vital Health Stat 2. 2013;(161):1-24. 23. Dye BA, Barker LK, Li X, Lewis BG, Beltrán-Aguilar ED. Overview and quality assurance for the oral health component of the National Health and Nutrition Examination Survey (NHANES), 2005-08. J Public Health Dent. 2011;71(1):54-61. 24. Institute of Medicine, Committee to Review Dietary Reference Intakes for Vitamin D and Calcium. Dietary Reference Intakes for Calcium and Vitamin D. Washington, DC: National Academies Press; 2011.
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25. Looker AC, Johnson CL, Lacher DA, Pfeiffer CM, Schleicher RL, Sempos CT. Vitamin D status: United States, 2001-2006. NCHS Data Brief. 2011;(59):1-8. 26. United States Census Bureau. Definitions. Available at: http://www. census.gov/hhes/www/poverty/methods/definitions.html#ratio of income to poverty. Accessed January 15, 2016. 27. Mellanby M. The role of nutrition as a factor in resistance to dental caries. Br Dent J. 1937;62(5):241-252. 28. Kühnisch J, Thiering E, Kratzsch J, Heinrich-Weltzien R, Hickel R, Heinrich J; GINIplus study group; LISAplus study group. Elevated serum 25(OH)-vitamin D levels are negatively correlated with molar-incisor hypomineralization. J Dent Res. 2015;94(2): 381-387.