Abstract
Severe early childhood caries (SECC) is a public health problem among preschool children. Malnutrition is a condition commonly prevalent in children with SECC. This study investigated the nutritional status among preschool children with SECC. Children with SECC (n = 101) aged 2–5 years from the Division of Pediatric Dentistry in an academic hospital in Southern Taiwan were recruited for our cross‐sectional study. The nutritional status of the children was assessed based on anthropometric measurements and clinical tests. By applying the criteria established by the World Health Organization, we found that 9% and 46% of the children with SECC were diagnosed as being anemic and iron deficient, respectively. Using national standards for the body mass index, 30% of children with SECC were classified as underweight. The relationship between the caries status of the children and anemia was examined using multivariable logistic regression analysis (p < 0.05). Our results show that SECC is strongly associated with anemia (7.25‐fold), indicating that clinicians and dentists should provide treatment to improve both the oral hygiene and the nutritional status of children with SECC.
Keywords: Anemia, Iron deficiency, Malnutrition, Severe early childhood caries, Underweight
Introduction
Early childhood caries (ECC) and severe early childhood caries (SECC) describe the status of caries present in children under the age of 6. SECC has been defined as any sign of smooth surface caries in children younger than 3 years. As shown in Table 1, SECC is defined for 3–5‐year‐old children by the following criteria: (1) one or more cavities, (2) one or more missing teeth as a result of caries, (3) one or more filled surfaces in primary maxillary teeth, or (4) For primary teeth index, def surfaces index (defs) which measures the severity of dental caries, “d” which is mean decayed tooth, “e” which is mean tooth indicated for extraction, “f” which is mean filled tooth. There are a decayed, missing, or filled surfaces (defs) score that is ≥4 at 3 years of age, ≥5 at 4 years of age, or ≥6 at 5 years of age [1].
Table 1.
Definition of early childhood caries and severe early childhood caries.
| Age (mo) | Early childhood caries | Severe early childhood caries |
|---|---|---|
| <12 | One or more defs surface | One or more defs surface |
| 12–23 | One or more defs surface | One or more defs surface |
| 24–35 | One or more defs surface | One or more defs surface |
| 36–47 | One or more defs surface | One or more cavitated, filled, or missing (due to caries) defs surface; smooth surfaces in primary maxillary anterior teeth or defs score ≥ 4 |
| 48–59 | One or more defs surface | One or more cavitated, filled, or missing (due to caries) defs surface; smooth surfaces in primary maxillary anterior teeth or defs score ≥ 5 |
| 60–71 | One or more defs surface | One or more cavitated, filled, or missing (due to caries) defs surface; smooth surfaces in primary maxillary anterior teeth or defs score ≥ 4 |
defs = d: decayed (noncavitated or cavitated lesions), e: extracted; f: filled tooth surfaces; ECC = early childhood caries; S‐ECC = severe early childhood caries, as classified by the American Academy of Pediatric Dentistry.
The prevalence rate of ECC in England, Finland, the United States, Indonesia, Western China, and Hong Kong were reported to be 4%, 6%, 20.2%, 48%, 20.2%, and 31.5%, respectively [2]. In Taiwan, it was reported to be 56% [3]. Thus, ECC can be considered as a highly prevalent dental disease in Taiwan. ECC has been associated with frequent consumption of fermentable carbohydrates and improper bottle‐ or breast‐feeding practices [[1], [4], [5], [6], [7], [8]]. Other nutrition‐related complications have also been reported [9]. Young children with extensive caries were found to be physically underdeveloped, especially in height and weight [[10], [11], [12]], symptoms that may be caused by aversions to eating because of tooth pain [[9], [12]] or a high sucrose diet that can compromise the intake of other nutrients [[9], [12], [13]]. In addition, cytokines and other inflammatory factors that are released from damaged tissues during pulpitis and chronic dental abscess are known to suppress erythropoiesis and the synthesis of hemoglobin (Hgb). Similar mediators of inflammation have also been shown to be prevalent in SECC [12], making SECC a possible risk factor for iron deficiency‐related anemia [9].
Because the prevalence rate of SECC in Taiwan is high and the nutritional status of children with SECC has not been studied in Taiwan, we performed an anthropometric and biochemical survey of children with SECC in an academic hospital setting in Southern Taiwan.
Materials and methods
Participant selection
We used a cross‐sectional approach to recruit young children between 2 and 5 years of age who visited the Department of Pediatric Dentistry of Kaohsiung Medical University Hospital (KMUH) for the treatment of SECC. The study protocol was approved by the Institutional Review Board of KMUH. Written informed consent was obtained from the parents or guardians of all participants. We excluded children with medical problems, mental or physical disabilities, and those who had been born prematurely.
Dental examination and diagnosis
The children in our study were diagnosed with SECC according to the diagnostic criteria established by the American Academy of Pediatric Dentistry [1]. One examiner performed oral examinations to determine the defs scores of the participants. None of the participants was found to have received prior dental treatments, including extractions, restorations, and endodontics.
Demographic information
The parent or the caregiver of each child was provided a questionnaire that recorded the demographic and socioeconomic data.
Anthropometric measurements
The body weight and height of each child were recorded, and the body mass index (BMI) was calculated (in kg/m2). The children were classified as obese, overweight, normal weight, or underweight based on the standards established by the Centers for Disease Control, Department of Health, Taiwan, R.O.C. (2008) [14].
Biochemical measurements
Before administering general anesthesia, blood samples were collected from each participant. There were missing data if the sum of sample does not equal 101. The blood samples were analyzed by the Department of Laboratory Medicine at KMUH. Blood analysis included examining common clinical parameters, anemia‐related parameters, and levels of mineral micronutrients, all of which are listed with the results of the analysis in Table 3. Common clinical parameters including levels of albumin, glutamate oxaloacetate transaminase (GOT), gamma‐glutamyl transpeptidase (GGT), alkaline phosphatase (ALP), blood urea nitrogen (BUN), and creatinine were obtained from medical charts. Anemia‐related measurements included an evaluation of red blood cell (RBC) count, hematocrit (Hct) value, concentration of Hgb, mean corpuscular volume (MCV), mean corpuscular hemoglobin (MCH), mean corpuscular hemoglobin concentration (MCHC), serum iron, total iron‐binding capacity (TIBC), transferrin (TSF) saturation, and the mineral status measures including calcium (Ca), magnesium (Mg), sodium (Na), and potassium (K).
Table 3.
Clinical parameters in children with severe early childhood caries (n = 101).
| Clinical parameters | Standard range b | Abnormal prevalence N (%) | ||
|---|---|---|---|---|
| Mean (SD) a | Median (range) | |||
| Common clinical parameters | ||||
| Albumin (g/dL) | 4.48 (0.26) | 4.48 (3.28–5.14) | 3.5–5.5 | 1 (1) |
| GOT (IU/L) | 32.26 (6.62) | 32.00 (23.00–61.00) | 10–42 | 0 (0) |
| GGT (IU/L) | 13.52 (3.30) | 13.50 (7.00–28.00) | 7–64 | 0 (0) |
| ALP (IU/L) | 224.55 (109.05) | 21.00 (138.00–1200.00) | 32–92 | 0 (0) |
| BUN (mg/dL) | 12.64 (9.62) | 11.40 (5.90–105.00) | 7.0–18.0 | 1 (1) |
| Anemia‐related measures | ||||
| Serum iron (μg/dL) | 63.32 (33.67) | 61.00 (9.00–246.60) | Male: 45–182 | 24 (25) |
| TIBC (μg/dL) | 390.17 (251.71) | 364.60 (229.30–2774.40) | Female: 28–170 | 1 (1) |
| TSF (%) | 17.54 (9.68) | 16.49 (2.81–75.27) | Male: 257–421 | 44 (46) |
| MCV (fmol) | 79.40 (5.29) | 80.4 (59.50–88.90) | Female: 254–450 | 11 (11) |
| MCH (Pg) | 27.08 (2.13) | 27.40 (19.00–30.40) | 16% | 11 (11) |
| MCHC (g/dL) | 34.07 (0.74) | 34.10 (34.10–36.40) | 74.9–84.6 | 5 (5) |
| RBC (×106/μL) | 4.70 (0.42) | 4.66 (3.66–6.12) | 25.2–29.1 | 13 (13) |
| Hct (%) | 37.15 (2.60) | 37.10 (30.8–47.70) | 32.6–35.1 | 14 (14) |
| Hgb (g/dL) | 12.60 (0.92) | 12.7 (10.3–15.20) | 4.28–5.05 | 15 (15) |
| 34.2–39.8 | ||||
| 11.6–13.7 | ||||
| Mineral status measures | ||||
| Ca (mg/dL) | 10.92 (9.53) | 9.60 (8.50–9.50) | 8.4–10.2 | 0 (0) |
| Mg (mg/dL) | 2.20 (0.15) | 2.18 (1.88–2.58) | 1.8–2.5 | 0 (0) |
| Na (mmol/L) | 137.86 (1.70) | 138.00 (134.00–144.00) | 136–145 | 7 (7) |
| K (mmol/L) | 4.32 (3.31) | 3.90 (3.17–37.00) | 3.5–5.1 | 8 (8) |
ALP = alkaline phosphatase; BUN = blood urea nitrogen; GGT = gamma‐glutamyl transpeptidase; GOT = glutamate oxaloacetate transaminase; Hct = hematocrit; Hgb = hemoglobin; MCH = mean corpuscular hemoglobin; MCHC = mean corpuscular hemoglobin concentration; MSV = mean corpuscular volume; RBC = red blood cell; TIBC = total iron‐binding capacity; TSF = transferrin.
Data are expressed as mean (SD) and median (range). Because of nonparticipation, missing values are noted while measuring albumin concentration (n = 29); calcium, magnesium, iron, and TIBC (n = 6); MCV, MCH, MCHC, RBC, Hct, Hgb (n = 2); GGT (n = 1).
Standard ranges used are those suggested by Kaohsiung Medical University Hospital.
Statistical analysis
The data were analyzed using JMP statistical software (version 7.0; SAS Institute, Cary, NC, USA). Statistical analyses included both descriptive and analytical tests. Descriptive data are presented as the number/percent of distributions in a tabular format. Biochemical measures were described as the median and standard deviation (SD) of the results of the blood analysis. Examinations of the relationships between the defs scores and participants' iron deficiency/anemia/growth impairment status were performed using a Chi‐square analysis and statistical significance was set at P < 0.05. Multivariate logistic analysis was used to estimate the independent effects of the malnutrition status in the children. Each participant's age and sex and the mother's education level were used in the regression models to control for confounding factors.
Results
We selected 101 participants for our study. Questionnaires were completed by the parents or the caregivers of 96 participants. Parents of 50 participants did not provide information about their income. The demographic characteristics of the participants are presented in Table 2. The mean age of the participants was 3.58 ± 0.95 years. Overall, 62% (63/101) of the participants were male, and 38% (38/101) were female.
Table 2.
Demographic characteristics of children with severe early childhood caries (n = 101). a
| Item | N | Percentage (%) |
|---|---|---|
| Gender | ||
| Female | 38 | 38.0 |
| Male | 63 | 62.0 |
| Age (y) | ||
| 2 | 13 | 13.0 |
| 3 | 36 | 36.0 |
| 4 | 32 | 31.0 |
| 5 | 20 | 20.0 |
| Body mass index for age category b | ||
| Underweight | 30 | 29.7 |
| Optimal | 50 | 49.5 |
| Overweight | 13 | 12.9 |
| Obese | 8 | 7.9 |
| Age of mother (y) | ||
| ≤29 | 33 | 35.0 |
| 30–39 | 56 | 60.0 |
| ≥40 | 5 | 5.0 |
| Age of father (y) | ||
| ≤29 | 11 | 12.0 |
| 30–39 | 57 | 60.0 |
| ≥40 | 27 | 28.0 |
| Maternal education | ||
| ≤Elementary school | 5 | 5.0 |
| High school | 55 | 57.0 |
| ≥College | 36 | 38.0 |
| Paternal education | ||
| ≤Elementary school | 1 | 1.0 |
| High school | 60 | 63.0 |
| ≥College | 35 | 36.0 |
| Yearly income in USD < 7576 | 9 | 10.0 |
| 7576–15,151 | 19 | 21.0 |
| 15,152–30,303 | 18 | 20.0 |
| >30,304 | 5 | 5.0 |
All data are expressed as N (%). There were missing data if the sum of participants does not equal 101.
Classification based on the standards by Department of Health, Executive Yuan (Taiwan 2008).
Dental diagnosis
The mean ± SD of decayed, missing, or filled teeth was 12.46 ± 4.23, while the mean ± SD of the defs scores was 35.68 ± 14.75.
Anthropometric measurement
The distribution of BMI categories is shown in Table 2. The BMI results for 50% of the participants were within the optimal ranges for their respective categories of age and gender, based on the standards set by the Centers for Disease Control, Department of Health, Taiwan, R.O.C. [14]. The prevalence rates of underweight, overweight, and obesity were 30% (30/101), 13% (13/101), and 8% (8/101), respectively.
Biochemical measurements
Quantities of blood that were sufficient to complete the blood analysis could not be obtained from all participants because of their refusal to cooperate, and therefore, the test results for RBC count, Hct value, concentration of Hgb, MCV, MCH, and MCHC were not obtained for two participants. Likewise, the results of the blood tests for iron, calcium, magnesium, and the TIBC could not be obtained for six participants; additionally, we could not perform blood tests for albumin on 29 participants.
The median, mean, and SD of the biochemical measurements are listed in Table 3. The results of blood analysis are shown as the median, mean ± SD. Standard ranges of RBC, Hgb, and MCV test results are described according to age‐specific thresholds (from 6 months to 6 years), and the ranges of the serum iron concentration and the TIBC tests are described according to gender‐specific thresholds, each based on standards previously established by KMUH.
The definitions of iron deficiency and anemia according to age‐ and gender‐specific thresholds were used based on standards established by the World Health Organization (WHO) [15]. Anemia was defined as (1) an Hgb concentration below 11 g/dL or an Hct value below 33% for children aged 6–59 months or (2) an Hgb concentration below 11.5 g/dL or an Hct value below 34% for children aged 5–11 years. TSF was calculated as (serum iron/TIBC) × 100%, while iron deficiency was defined as TSF saturation below 16%.
As shown in Table 3, the concentrations of GOT, GGT, and ALP were within standard ranges for all the participants. The concentration of serum albumin was below the standard range (minimum 3.5 g/L) in 1% (1/72) of the children. In the same way, 1% (1/101) of the children had a BUN level that was below the standard range (minimum: 7 mg/dL).
All of the anemia‐related measurements were below the standard ranges. The median ± SD for the test results of the serum iron concentration, TIBC, TSF, MCV, MCH, MCHC, RBC, Hct value, and Hgb concentration were 61.00 ± 33.67 μg/dL, 364.60 ± 251.71 μg/dL, 16.49 ± 9.68%, 80.40 ± 5.29 fmol, 27.40 ± 2.13 Pg, 34.10 ± 0.74 g/dL, (4.66 ± 0.42) × 106/μL, 37.10 ± 2.60%, and 12.70 ± 0.92 g/dL, respectively. Forty‐six percent of the children (44/95) were iron‐deficient [15]. Eleven percent (11/99) had an MCV below the reference range (minimum: 74.9 fmol), and were diagnosed with iron‐deficiency anemia. The test results of RBC count, Hct value, and Hgb concentration were below the reference range in 13% (13/99), 14% (14/99), and 15% (15/99) of the children, respectively, and all the children within these groups were diagnosed as having anemia. As shown in Table 4, 9% (9/99) and 46% (41/95) were diagnosed as being both anemic and iron‐deficient based on the WHO definitions [15].
Table 4.
Analysis of dental status and anemia/iron‐deficiency/malnutrition status in children with severe early childhood caries (n = 101).
| Clinical parameters | ≥35 defs | <35 defs | Chi‐square test | ||
|---|---|---|---|---|---|
| N a | (%) | N a | (%) | P | |
| Body mass index for age category b | |||||
| Underweight | 18 | 17.8 | 12 | 11.9 | 0.082 |
| Optimal | 16 | 15.8 | 34 | 33.7 | |
| Overweight | 7 | 6.9 | 6 | 5.9 | |
| Obese | 3 | 3.0 | 5 | 5.0 | |
| Anemia c | |||||
| Yes | 7 | 7.1 | 2 | 2.0 | 0.024* |
| No | 35 | 35.3 | 55 | 55.6 | |
| Iron deficiency d | |||||
| Yes | 18 | 19 | 23 | 24.2 | 0.681* |
| No | 26 | 27.4 | 28 | 29.5 | |
*p < 0.05 had a statistically significant difference.
defs = d: decayed (noncavitated or cavitated lesions), e: extracted; f: filled tooth surfaces.
There were missing data if the sum of participants does not equal to 101. Chi‐square test was used for analysis.
Classification based on standards by Department of Health, Executive Yuan (Taiwan 2008).
Based on the standards established by the World Health Organization (WHO 2001), anemia was defined as Hgb < 11 g/dL or Hct < 33% for children 6–59 months old and Hgb < 11.5 g/dL or Hct < 34% for children ≥ 5 years of age.
Based on the standards established by the World Health Organization (WHO 2001), iron deficiency was defined as transferrin concentration <16%.
The concentrations of calcium and magnesium were within the respective reference ranges for all the participants. The respective concentrations of sodium and potassium were 138 ± 1.70 mmol/L and 3.90 ± 3.31 mmol/L, with 7% (7/101) and 8% (8/101) of the children possessing levels of sodium and potassium below the standard ranges, respectively (Na minimum: 136 mmol/L; K minimum: 3.5 mmol/L).
Chi‐square analysis of associations between the defs score and malnutrition status (anemia/iron‐deficiency/underweight)
A defs score ≥ 35 was significantly associated with anemia (7.1%, p < 0.024) (Table 4). Although no significant differences were observed in malnutrition and iron‐deficiency status, 17.8% of the children with defs scores ≥ 35 were underweight, whereas 11.9% of the children with defs scores <35 were underweight.
Multivariable logistic regression analysis of associations between defs score and anemia
Multivariable logistic regression showed that defs scores ≥35 significantly correlated with anemia while adjusting for age, gender, BMI, and mother's education level to control for confounding factors (Table 5). Children with a defs score ≥ 35 were shown to be at a 7.25‐fold higher risk for anemia, compared with those with defs scores <35 (95% CI = 1.38–68.27; p = 0.0365).
Table 5.
Multivariable logistic regression analysis on risk factors associated with iron deficiency and anemia among children with severe early childhood caries.
| Variable | Iron deficiency/anemia | OR (95% CI) | p a | OR (95% CI) | p a | |
|---|---|---|---|---|---|---|
| Yes N (%) | No N (%) | |||||
| Anemia b | ||||||
| defs < 35 | 7 (77.8) | 35 (38.9) | 1 | 0.0401* | 1 | 0.0365* |
| defs ≥ 35 | 2 (22.2) | 55 (61.1) | 5.50 (1.25–38.34) | 7.25 (1.38–68.27) | ||
*p < 0.05 had a statistically significant difference.
CI = confidence interval; defs = d: decayed (noncavitated or cavitated lesions), e: extracted; f: filled tooth surfaces; OR = odds ratio.
Fisher exact t test was used if N < 5 in univariate analysis.
Based on the standards established by the World Health Organization (WHO 2001), anemia was defined as Hgb < 11 g/dL or Hct < 33% for children 6–59 months old and Hgb < 11.5 g/dL or Hct < 34% for children ≥ 5 years of age.
Discussion
This study described the nutritional status of children with SECC. Children with SECC were found to be at risk for anemia and iron deficiency. Nine percent were diagnosed with anemia, and 46% were diagnosed with iron deficiency [15]. Using multivariable logistic regression, we also found that the status of caries (defs score ≥ 35) was independently associated with anemia. To date, only one study has investigated the status of anemia and iron deficiency in children with SECC [6]. Clarke et al. (2006) reported a higher prevalence of anemia (28%, Hgb < 110 g/L) and lower prevalence of iron deficiency (24%, serum ferritin < 10 μg/L) in children with SECC than were observed in the children with SECC in our study [9]. Although the prevalence of anemia reported by Clarke et al. (2006) was higher than that obtained from our results, consideration should be given to the differences between the methodologies and the standards of the anemia‐related biochemical indices that were used in the two studies. Moreover, our study uses the definitions and standards of anemia and iron deficiency established by the WHO criteria, indicating that conclusions based on our findings may be extended to populations elsewhere.
According to the Nutritional and Health Survey in Taiwan (NAHSIT), the prevalence rate of iron deficiency in children between 4 and 6 years of age was 0.2–6.2% [16]. Forty‐six percent of children with SECC in our study had iron deficiencies, which was much higher than the rate reported by the NAHSIT. This outcome may be influenced by both dietary habits and socioeconomic status.
Anemia can be caused by several factors, including dietary factors, genetic (congenital) factors, environmental factors [[17], [18]], and inflammatory processes. Children with SECC may have higher rates of anemia and iron deficiency for various reasons. Children with SECC may consume cow's milk excessively, which reduces the absorption of iron [[19], [20], [21]]. In addition, children with SECC have untreated caries that often cause pain or discomfort, and they may thus have difficulty in chewing certain iron‐ and vitamin C‐rich foods, such as red meat and citrus fruits, respectively [[19], [20]]. Furthermore, children with SECC may suffer from acute or chronic inflammation, resulting from pulpitis and periapical abscess and fistula, and such inflammatory complications may induce the production of cytokines that suppresses the synthesis of Hgb [12]. In our study, children with anemia suffered a greater amount of injury to their teeth, as reflected in their defs scores, compared with the children without anemia. Such greater injury is likely to have a greater effect on their health, based on the preceding status.
In our study, 30% of participants were underweight (30/101). A recent study showed that the prevalence rate of underweight children with SECC was 4% [9]. Other studies report that children with SECC are significantly shorter and possess lower average weights than children with complete dental rehabilitation [[10], [11]]. Poor sleep quality resulting from dental pain may contribute to decreases in the production of glucosteroids, which may also impair growth [12].
Although 46% of our participants had iron deficiencies, almost none had calcium levels below the reference range. The concentration of serum iron is often influenced by dietary factors [[17], [19]], and iron absorption can be depressed by excessive calcium intake. Prolonged breastfeeding and the early introduction or increased consumption of cow's milk was associated with an increased risk of iron deficiency in children in Australia, Canada, New Zealand, and the United Kingdom [19]. Excessive milk intake (more than 750 mL/day) after 1 year of age is a risk factor for iron deficiency [[19], [20]]. One recent study [21] reported that bottle‐feeding of cow's milk at night was a significant determinant for ECC (odds ratio = 5.5), compared with breastfeeding. In our study, the frequency of milk intake (≥1 feeding/day) for children with SECC was 68%, and 73% of parents were unaware that their children had been previously weaned. Thus, a high frequency of milk consumption may have been a contributing factor for the high prevalence of iron deficiency observed in children with SECC in our study.
Our study has some limitations. First, our study population may not have been representative of all children with SECC in Taiwan. We were unable to use a systematic random sampling approach because young children with SECC were difficult to recruit, and difficulties were encountered in obtaining blood samples. In addition, the application of our findings may be limited to populations with extreme dental disease (DMFS score ≥ 35). Furthermore, because of the cross‐sectional approach used in our study, a causal relationship between SECC and anemia cannot be confirmed. Further investigations to determine causal relationships and lifestyle risk factors are warranted.
Conclusion
SECC may be a contributing factor for iron deficiency, anemia, and impaired weight gain in young children. SECC (defs score ≥ 35) may represent a risk factor for anemia in preschool children. Further studies are needed to examine lifestyle and socioeconomic risk factors that may be associated with the malnourished status of these children. Preventive strategies should be developed to reduce the risk of anemia, iron deficiency, and impaired weight gain in children with SECC.
Acknowledgments
This study was supported by a grant from Kaohsiung Medical University Hospital (Grant No. KMUH97‐7G40). The authors would like to thank Jhang Hui‐Ru (Department of Nutrition and Dietetics, Kaohsiung Medical University Hospital), Dr Hong‐Sen Chen (Department of Pediatric Dentistry, Kaohsiung Medical University Hospital), and Dr Fu‐Hsiung Chuang (Department of Conservative Dentistry, Kaohsiung Medical University Hospital).
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