Child nutrition and oral health in Ulaanbaatar

Child nutrition and oral health in Ulaanbaatar

Nutrition Research 23 (2003) 1165–1176 www.elsevier.com/locate/nutres Child nutrition and oral health in Ulaanbaatar Henna M. Karvonena, Outi Nuutine...

127KB Sizes 2 Downloads 145 Views

Nutrition Research 23 (2003) 1165–1176 www.elsevier.com/locate/nutres

Child nutrition and oral health in Ulaanbaatar Henna M. Karvonena, Outi Nuutinena,*, Ulla Uusitalob, Rita Sorvaric, Merja Ihanainend a

Department of Clinical Nutrition, University of Kuopio, P.O.B. 1627, 70211 Kuopio, Finland b University of Cornell, Ithaca, New York, USA c Department of Anatomy, University of Kuopio, Finland d Pohjois-Savo Polytechnic, Social and Health Care, Kuopio, Finland

Received 23 September 2002; received in revised form 26 March 2003; accepted 27 March 2003

Abstract This study investigated the nutritional status and eating habits of Mongolian children in relation to dental health. Growth and oral health of 151 Ulaanbaatarian children under age five were examined, and their parents were interviewed on child’s health and eating habits. Every tenth child had a low weight for age and the mean energy intake of the weaned children was 89%-96% of the recommendation by WHO. Frequent eating exposed the teeth of children to many acid attacks. Every third child over age three had serious developmental defects in their teeth, which might be associated with deficient intakes of energy and calcium, highly variable vitamin D supplementation and gastrointestinal infections. All of the examined 4 to 5 -year old children had caries and the average number of decayed teeth was 6.5. Severe caries was related to the abundant use of sugar, whereas proper dental health was related to use of hard cheese. © 2003 Elsevier Inc. All rights reserved. Keywords: Child; Oral health; Dental health surveys; Growth; Nutrition; Diet

1. Introduction Nutrition has a strong impact on oral health. A healthy, correctly fed child is more expected to have healthy teeth. Vitamin D, proteins and minerals, especially calcium and phosphorus, are essential for the development of teeth [1,2]. Both the lack and the excess of

* Corresponding author. Tel.: ⫹1-358-17-162-787; fax: ⫹1-358-17-162-792. E-mail address: [email protected] (O. Nuutinen). 0271-5317/03/$ – see front matter © 2003 Elsevier Inc. All rights reserved. doi:10.1016/S0271-5317(03)00088-5

1166

H.M. Karvonen et al. / Nutrition Research 23 (2003) 1165–1176

Table 1 The characteristics of the study subjects by age, sex and housing Age group (years)

N

Under 0.5 0.5–0.9 1.0–1.9 2.0–2.9 3.0–3.9 4.0–4.9 All age groups

33 27 33 17 29 12 151

Sex (n)

Housing (n)

Boys

Girls

Ger

Flat

15 10 19 6 10 5 65

18 17 14 11 19 7 86

21 17 20 9 14 8 89

12 10 13 8 13 4 62

these nutrients might be harmful. Protein as well as energy malnutrition may cause dental defects or hypoplasias [1,3]. In turn, malformations of teeth expose them to caries [4]. Poor oral health is a major problem in Mongolia [5]. Dental developmental defects are common in both rural and urban areas [5]. On the other hand, in rural areas children have nearly caries-free mouths, but in cities 6-year old children have an average of 6 carious teeth. Change from a traditional milk-meat based diet to a western-type diet might be one of the reasons for the high incidence of caries in cities. The most important factors affecting the development of caries are the eating frequency of fermentable sugars and the use of fluorides [6,7]. Eating frequency has a strong impact on oral health. When food containing fermentable sugar is eaten, the pH of the mouth decreases, and the dental enamel starts to dissolve. On average, the pH decrease lasts about half an hour after eating, but at night, when saliva production is reduced, pH decrease is longer. Normally, saliva remineralizes the dissolved enamel, but, if the eating frequency is high, there is not enough time for the remineralization process to occur. In early childhood, caries can quickly become a serious health problem because the newly erupted teeth are very sensitive to caries. The aim of this cross-sectional study was to investigate the nutritional status and eating habits of Ulaanbaatarian children in relation to oral health.

2. Materials and methods A randomized sample of 151 children aged under 5 years was drawn from the clients of family nurses in Ulaanbaatar, the capital of Mongolia (Table 1) and they represented about 2‰ of the children aged under 5 years in Ulaanbaatar. Children were from six different geographical areas of the capital. The study subjects were randomized out of the client register of the nurses on each geographical district. After randomization family nurses asked their clients to volunteer for the research and informed the families about the coming research. The dean of the Medical School approved the study due to lack of an ethics committee in Ulaanbaatar. The research group included a clinical nutritionist, a nurse as well as a dentist, who also worked as an interpreter for the nutritionist in dietary interviews. All together 15 local nurses

H.M. Karvonen et al. / Nutrition Research 23 (2003) 1165–1176

1167

and physicians guided the researchers during their visits at the homes of the study subjects in different areas of the town. Fieldwork was carried out in the summer of 1998. Families with children under 6 months old were visited only once whereas the families with 1⁄2 –5 year old children were visited twice. Parents were interviewed on child health and eating habits. The length and weight of the child was always measured by the nutritionist with the help of the nurse. Weight of children under 15 kg was measured to the nearest 50 grams with mechanical scale for children (SECA, Vogel & Falke GmpH & Co, Germany). Children weighing over 15 kg were measured to the nearest 100 grams with electronic scale. Children were weighed with light underclothes or naked. The function of both scales was confirmed three times during the research period. The weight-for-age growth chart was used to monitor the malnutrition, because the high prevalence of rickets reduces the reliability of height-for-age or weight-for-height charts [8]. Weight of the children was compared to the weight-for-age growth chart of the WHO (World Health Organization) [9]. Children under the third percentile were classified as underweight. Only the children with seriously bowed legs or chest or knocked knees were classified as having rickets. Food consumption of children over six months old was collected twice by 24-hour recall. The parents were interviewed with the aid of food models and dishes. In the beginning of each home visit the native Mongolian dentist-interpreter interviewed parents on the child’s habitual diet and then the nutritionist completed the data with additional questions on food quality and portion sizes. On the second visit, a 24-hour recall was repeated, and in addition 10 parents were asked about the seasonal differences in their children’s diet. During the study visit the mothers of under 1⁄2-year old infants were only interviewed on breastfeeding practices and the possible use of weaning foods. Eating frequency of children was calculated from 24-hour recalls. The daily intake of energy yielding nutrients, calcium, sugar and vitamin D was calculated with the MicroNutrica® dietary analysis software (The Social Insurance Institution, Helsinki, Finland). In order to calculate the nutrient intake the recipes of Mongolian dishes were saved on the dietary analysis database. Child’s oral health was examined by the dentist and the nutritionist collected the dental examination data on the Oral Health Assessment form of the World Health Organization [10]. Dmft-index (the number of decayed, missing and filled teeth) was calculated for each child. Nearly all of the teeth calculated on dmft-index were carious without fillings. All statistical analyses were done by SPSS statistical software package version 8.5 (SPSS Inc., Chicago, IL, USA). The results are given as means and standard deviations. Average dietary intakes of the children were compared to the recommendations of WHO [11]. Cross-tabulation was used to analyze the association of the gender of the child, breast feeding practise, number of the children in the family and family dwelling place with the growth of the child and the existence of hypoplastic teeth. Only children over 3 years of age were taken into account in statistical analysis on dental health. Correlation matrix was used to study the association of the age of the child, nutrient intake and dental health (indicators number of hypoplastic teeth and dmft-index) and the variables correlating (rp ⬎ 0.3) with dmft-index were selected for further examination. The association of rickets, relative weight and vitamin D supplementation with the prevalence of dental enamel defects was analysed by cross-

1168

H.M. Karvonen et al. / Nutrition Research 23 (2003) 1165–1176

Fig. 1. The percentage of children (total n ⫽ 151) being underweight if compared to the growth standards of WHO.

tabulation. Association of the use of candies, bakery products, refreshments and hard cheese with dental health was also analyzed by cross-tabulation. To test the association of sugar intake and dmft-index children were divided in three groups based on their daily sugar consumption. Normal distribution of the variable was tested with Shapiro-Wilk test. The variable was not normally distributed even after logarithmic or other mathematical transformations. Therefore Kruskal-Wallis test was used to compare the dmft-index between the groups.

3. Results 3.1. Nutritional status and health of children Most of the children had a normal birth weight. Only very few babies (1%) had a birth weight less than 2.5 kg, which is considered low birth weight [9]. However, every tenth child had a low weight for their age when compared to the growth standards of the World Health Organization (Fig. 1). Girls tended to be more often undernourished than boys and ger (traditional Mongolian tent) dwellers weighed less than flat dwellers (p ⬎ 0.06). Breastfeeding practice did not affect the weight of the study children. Mothers of children under 6 months reported 9% of their infants being sick on research day and of the children over 6 months, 18% were sick on at least one of the two research visits. The most common diseases were flu and gastrointestinal infections. Six percent of the

H.M. Karvonen et al. / Nutrition Research 23 (2003) 1165–1176

1169

children had diarrhea or had been vomiting on research day. Nurses and parents reported that 10 children (7%) had been diagnosed with rickets. Some of the children (3/10) who were diagnosed earlier with rickets had not received any vitamin D treatment. Upon examination, 23% of the children over 6 months of age had clear signs of rickets i.e. severely bowed legs or bent chest. Every eighth child (13%) had received some medicine during the week preceding the research visit. Antibiotics and cough syrups were the most common medicines used. Children received medicines both by prescription of physician and through parental consideration. Every tenth child received some vitamin preparation. The most common preparation was vitamin C solution given to infants. However, none of the children had received vitamin D during the week preceding the research visit. 3.2. Diet Breast-feeding was common and 57% of the children who participated in the research were still breast-fed. The average weaning age of the already weaned children was one year and four months. Most of the mothers (92%) gave breast milk to their children whenever they felt their children were hungry. On the average, children received breast milk twice a night and altogether eight times over a 24-hour period. Breast milk was the most important food of children under 6 months. Nearly all (87%) of the infants were breast-fed. The non-breast-fed infants and infants having insufficient amounts of breast milk received either infant formula, boiled cow’s milk, or milk tea. The first weaning foods introduced to an infant’s diet were normally liquids (tea or water with sugar or honey) and only infants over 3 months old received more solid baby foods like yogurt, bantan or kaash. Bantan and kaash are traditional Mongolian weaning foods; bantan is flour in meat soup, and kaash is semolina cooked in water with sugar, milk and butter. Six months to one-year old infants were breast fed frequently. The most popular baby foods given to 6 month - one-year old infants were yogurt, bantan, milk tea and kaash. All of the infants over 6 months received some baby food in addition to the breast milk, but quite often the amount of extra food was very small—maybe only one or two spoonfuls of milk tea or the cooking water of rice. Children over one-year old gradually adapted to the eating patterns of the family. However, they were still breast fed frequently. The most common extra foods were yogurt, bantan, milk tea and kaash, but more and more normal family food was also given. The main meal was family dinner containing meat, and only a few families served a hot lunch. Extra foods were commonly served during the day for all children under three years of age. In the evening and at night, many mothers gave breast milk to their children in order to get them to fall asleep. Children over 3 years old more often ate bread, donuts, cookies or leftovers from the previous dinner during the day (Table 2). Children also drank plenty of tea or milk tea. Most of the children over one year old had confections or baked goods as extra snacks during the day. Fifty-five percent of the children used sugar on their bread or did not eat any bread, but confections instead. Based on the 24-hour recall, nearly half of the children had eaten candies and one third had drunk soft drinks. One-fifth of the children had eaten cheese or aarul (dried Mongolian cheese).

1170

H.M. Karvonen et al. / Nutrition Research 23 (2003) 1165–1176

Table 2 Childrens’ habitual daily diet in various age groups Meal

Food item eaten by children under 3-year old

over 3-year old

Breakfast 7–10 a.m.

- Kaash or bread and milk tea - Breast milk

- Bread covered with sugar and butter - Milk tea

Lunch/snacks 10 a.m.–5 p.m.

- Kaash or bantan - Bread, yogurt, ice cream, donuts or cookies - Breast milk or milk tea

- Bread, yogurt, ice cream, donuts or cookies - Tea or milk tea - Occasionally soup or ravioli in milk tea or leftovers

Dinner 5 p.m.–8 p.m.

- Meat casserole or soup with potato, macaroni, or rice and onion, carrot, cabbage or turnip - Tea, milk tea or breast milk - Bread, donuts or cookies - Tea, milk tea or breast milk

- Meat casserole or soup with potato, macaroni, or rice and onion, carrot, cabbage or turnip - Tea or milk tea - Bread, donuts or cookies - Tea or milk tea

Late supper After 8 p.m.

Mongolian diet has some seasonal variation. Most of the 10 families interviewed reported that the greatest differences are in the use of milk and meat products: summer is the time of milk whereas winter is meat season. Some of the parents complained that it is very hard to afford or to find fresh vegetables or fruit in the winter. The use of grains, potatoes, bakery goods or confectionery had no significant seasonal variation. 3.3. Nutrient intake The mean (SD) of the weaned children’s energy intake was 5,000 kJ (⫾1,500 kJ) per day. When the energy intake was adjusted to the weigh of the child, children received on the average 94% of the WHO’s recommended energy intake, which is based on the minimum requirements. Almost every third two-to-three-year old child received less than 75% of the recommended daily energy intake. The protein intake of weaned children was, on average, 37 g (⫾13) per day. Protein intake of the children was twice the minimum amount considered to meet the physiological need of the child. Weaned children received, on average, 100 (⫾77) % of the calcium intake recommended by the WHO (Table 3). However, 44% of the children received less than 75% of the recommended daily intake of calcium. In the summer, children spent an average of 51⁄2 hours a day outside, whereas in the winter, children played outside less than one hour a day, and many of the children did not even go outside every day. Also, heavy clothing and swaddling practice minimize the exposure to sunlight. In spite of the summer, 27% of infants under 6 months old were always swaddled when outside, and 15% were swaddled occasionally. Vitamin D content of the Mongolian diet is very low. None of the children received even half of the recommended daily intake of vitamin D. On average children received only 7% (0.7 ␮g) of the recommended daily intake of vitamin D, which is 10 ␮g/day for children

H.M. Karvonen et al. / Nutrition Research 23 (2003) 1165–1176

1171

Table 3 Calcium intake of the children (mg/day) in various age groups. The mean (SD) and the recommendation of WHO [11] Age (years) 1/2–1 Weaned Breast-fed 1–3 Weaned Breast-fed 4–5 Weaned Breast-fed 1

N

Calcium intake (mg/day)

Recommendation (mg/day)

5 22

439 (220) 200 (160)1

600

45 34

420 (270) 360 (290)1

400

12 0

400 (470)

450

Does not include the calcium derived from breast milk.

under 5 years old [11]. In addition, breast milk does not contain enough vitamin D to protect infants from rickets [12]. More than half (56%) of the children had received vitamin D supplementation at least once in their lifetime. Most of the children received vitamin D orally, by solution or in capsules. Capsules included 50,000 IU of vitamin D. Some of the children received injections containing 300,000 IU of vitamin D. Child diagnosed with rickets might have received both injection and capsules. 3.4. Oral health Parents did not brush the teeth of the infants or toddlers. Half of the children over 2 years old were brushing their teeth. 86% of the children brushing their teeth used fluoridecontaining toothpaste. Although brushing frequency was not asked, some of the parents mentioned their children brushing teeth only in the morning before breakfast. Dental enamel defects were common. Nearly one-third of the children over 3 years old had at least one hypoplastic tooth. Family’s dwelling place, number of children in the family, or child’s gender did not affect the occurrence of hypoplasias (p ⬎ 0.3, ␹2 test). Almost all of the children over 3 years old had diffused or demarcated opacities. Every tenth child had mild or questionable fluorosis. Caries was a common problem, which increased by the age. Forty-two percent of the 3– 4 year old children were caries free, but all of the 4 –5-year old children had cavities and the mean dmft-index was 6.5. The dmft-index of the study children presents the actual number of decayed, non-filled teeth, since children seldom had any teeth missing for reasons other than caries and hardly any cavities had been filled. 3.5. Teeth and nutrition Breast-fed infants under one year of age ate at short intervals and their teeth were exposed to many acid attacks. With aging children ate less frequently; the children under one year of

1172

H.M. Karvonen et al. / Nutrition Research 23 (2003) 1165–1176

Fig. 2. Average number of meals for children (total n ⫽ 118) in various age groups.

age ate, on average, 9.7 times a day, while the children over 4 years old ate only 5.4 times a day (Fig. 2 ). Breast fed children ate more often than weaned children due to breastfeeding many times a day as well as at night. In total 18 children had received some medicine the day before the study visit. One-third of the medicines given to children contributed to increased number of acid attacks; six of the children received medicines containing sugar. Among over 3 year old children the age of the child, the use of sugar, and enamel defects were significantly related to the dmft-index (rp ⬎ 0.3, p ⬍ 0.035). Rickets, relative weight or vitamin D supplementation had no significant relation to the prevalence of dental developmental defects. There were no association between single sugar containing food product and dental health; the use of candies, bakery products or refreshments did not correlate with severity of caries or incidence of dental developmental defects (Table 4). However, the children using sugar most abundantly tended to have higher dmft-index. Children in the lowest sugar consumption tertile (average intake of sugar 9g/day) had dmft-index of 2.4 whereas children in the highest tertile (average intake of sugar 41 g/day) had dmft-index of 5.4 (p ⫽ 0.133) (Table 5.) Table 4 The percentage of children eating various food products in relation to dmft-index (n ⫽ 41)

Bakery products Candies Refreshments Mongolian cheese

Dmft 0 (%) (n ⫽ 12)

Dmft 1–5 (%) (n ⫽ 15)

Dmft over 6 (%) (n ⫽ 14)

p-value1

58 33 17 58

40 60 20 27

71 43 36 7

NS NS NS 0.0153

P-values ⬍0.05 were considered significant. Analysed with ␹2 test.

1

H.M. Karvonen et al. / Nutrition Research 23 (2003) 1165–1176

1173

Table 5 The association of nutrient intake and dmft-index in Mongolian children (n ⫽ 41). The mean (SD) dmftindex and intake of nutrients in tertiles based on daily intake of nutrients. Four of the children were not yet totally weaned Daily intake of nutrients

Energy/body weight Dmft-index Intake (kJ/kg) Protein/body weight Dmft-index Intake (g/kg) Saccharose Dmft-index Intake (g) Calcium Dmft-index Intake (g)

Lowest tertile (n ⫽ 14)

Middle tertile (n ⫽ 13)

Highest tertile (n ⫽ 14)

p-value1

2.6 (3.0) 240 (54)

4.4 (4.7) 353 (18)

5.5 (3.9) 478 (90)

NS

4.0 (4.1) 1.8 (0.4)

3.8 (3.8) 2.6 (0.2)

4.6 (4.3) 3.6 (0.5)

NS

2.4 (2.9) 9 (5)

4.6 (4.7) 22 (3)

5.4 (3.9) 41 (11)

NS

3.4 (3.9) 146 (59)

4.2 (4.3) 370 (69)

4.9 (3.9) 787 (333)

NS

P-values ⬍0.05 were considered significant. Analysed with Kruskal-Wallis test. 2 Analyzed with one-way analysis of the variance. 1

Children eating cheese or aarul had fewer cavities than the other children; children over three years old eating cheese or aarul had dmft-index of only 2.3 compared to 4.9 for the non-cheese- or-aarul-eaters. Children without caries ate aarul more often than the children with over 6 carious teeth (p ⫽ 0.0153) (Table 4).

4. Discussion This cross-sectional study showed that oral health and child feeding practices need further attention in Mongolia. Every third child over three years of age had serious developmental defects in their teeth, and all of the examined 4-5 -year old children had cavities. Every tenth child had a low weight for age compared to the WHO growth standards. The mean energy intake of the weaned children was 89%-96% of the minimum recommendation by WHO. However, the intake of protein was more than twice the minimum recommendation. The teeth of children under three years of age were exposed to many acid attacks due to frequent breastfeeding and use of sugar containing weaning foods. The study population of 151 subjects represented about 2 ‰ of the under 5 year old Ulaanbaatarian children [13, Census Department of Ulaanbaatar Administration 1998]. These children fairly represented six geographically and economically different areas of the capital. Repeated 24-h recall functioned well as a method of nutritional assessment. The reliability of the study could have been improved by more interviews, if there were more time and a larger research team. The nutritional status of infants under 6 months was good. Infants over 6 months had some

1174

H.M. Karvonen et al. / Nutrition Research 23 (2003) 1165–1176

nutritional problems. Many mothers prepared the baby foods so watery that the foods contained very little energy or other nutrients, which might impair the growth of the children. Some of the children were breastfed constantly, which might indicate the hunger of the child. Weaned children over one year old received energy slightly under the recommended figure and twelve percent of the children were underweight. In a 24-hour recall, about half of the children received less than what is considered to be a safe amount of energy. According to the nutrient intake calculations child malnutrition is caused by a lack of energy rather than by poor protein intake. Even the seasonal variation of diet is not likely to reduce protein intake, because increased use of meat compensates the reduced use of milk in the winter. Breast feeding practice or weaning age did not seem to affect the dental health. However, there were some feeding practices that may cause a lot of damage to teeth. After teeth have erupted, continual breast-feeding at night might cause caries [14]. After weaning, some children from poor families received sugary water instead of supplementary milk. This practice may cause both malnutrition and tooth decay [15]. Gastrointestinal infections were a common problem. It is very possible that the gastrointestinal infections and the liberal use of medicines in any sickness expose children to enamel defects [1]. There was lot of variation in the vitamin D supplementation practice and the supplements given had been recorded only occasionally. Some children may develop vitamin D toxicity while some do not get any vitamin D. Swaddling practice may also increase the risk of rickets. The large variation in the vitamin D supplementation practice can endanger the health of the teeth. Rickets due to lack of vitamin D supplementation may cause opacities and hypoplasias as well as the overload of vitamin D supplements may also lead to dental deformations [1,16]. Seasonal variation of diet is likely to affect the calcium intake. Scanty use of milk during the winter might reduce the calcium intake to a very low figure. The small calcium intake, together with extremely low vitamin D intake, increases the risk of hypoplasias [1]. Poor nutrition in early childhood can start a destructive downward spiral; malnourished children get malformed teeth [17,4]. Enamel defects expose them to dental caries. The malnutrition reduces the salivary flow, which increases the risk of caries even more. Saliva can not properly restore the dissolved enamel when the intake of calcium, phosphorus and fluorides are continually too little. Thus, the teeth of malnourished children decay easily. Especially the teeth of children under three years of age were exposed to many acid attacks due to frequent breastfeeding and use of sugar containing weaning foods. The more sugar children consumed, the more caries they had. In these data, the use of any specific food product did not worsen the occurrence of caries; the overall use of sugar seemed to be more important. Interestingly, the use of traditional Mongolian cheese was connected to better dental health. This might be because cheese contains lot of calcium and phosphorus. In addition, biting increases flow of saliva. Dental health care at homes was not systematic and tooth brushing did not become common until in those age groups which already had seriously decayed teeth. Beginning from the early childhood, oral health care practices could therefore be greatly improved by regular tooth brushing with fluoride containing toothpaste. In order to examine the associ-

H.M. Karvonen et al. / Nutrition Research 23 (2003) 1165–1176

1175

ation of dental care practices at home and dental health the tooth brushing practices should have been questioned more detailed. The fluoride content of the household water in Ulaanbaatar should be examined in order to plan the proper fluoride prophylaxis for the prevention of tooth decay. Further research is also needed on the childrens’ calcium-phosphorus balance with vitamin D levels in the blood. In conclusion, the present study showed that dental developmental defects and tooth decay are serious health problems among children in Ulaanbaatar. Deficient intakes of energy and calcium, highly variable vitamin D supplementation and gastrointestinal infections might be associated with dental developmental defects. Severe caries was related to the abundant use of sugar, whereas proper dental health was related to the use of hard cheese. For better oral health the growth of the children, their nutrition and the use of vitamin D supplements as well as the eating frequency need to be monitored.

Acknowledgments Nature of contribution of each author: Henna M Karvonen, M.Sc was responsible for planning the study, carrying out the field work and writing the manuscript. Outi Nuutinen, Ph.D was responsible for planning the study and writing the manuscript. Ulla Uusitalo, M.Sc served as statistical advisor and took part in planning the study and writing the manuscript. Rita Sorvari, D.D.S, Ph.D served as dental advisor. Merja Ihanainen, M.Sc took part in planning the study and writing the manuscript. The authors wish to thank dentist Mr Tserenbat for excellent technical assistance. The study was supported by FIDA International (development aid agency), Helsinki, Finland.

References [1] Pindborg JJ. Etiology of developmental enamel defects not related to fluorosis. Int Dent J 1982;32:123–34. [2] Alvarez JO, Caceda J, Woolley TW, Carley KW, Baiocchi N, Caravedo L, Navia JM. A longitudinal study of dental caries in the primary teeth of children who suffered from infant malnutrition. J Dent Res 1993;72:1573– 6. [3] May RL, Goodman AH, Meindl RS. Response of bone and enamel formation to nutritional supplementation and morbidity among malnourished Guatemalan children. Am J Phys Anthropol 1993;92:37–51. [4] Li Y, Navia JM, Bian JY. Caries experience in deciduous dentition of rural Chinese children 3-5 years old in relation to the presence or absence of enamel hypoplasia. Caries Res 1996;30:8 –15. [5] Salmenkivi S. Mongolian oral health survey. Finnish Free Foreign Mission, Helsinki, Finland, 1997. Unpublished survey. [6] Geddes D. Diet patterns and caries. Adv Dent Res 1994;8:221– 4. [7] Ismail AI. Prevention of early childhood caries. Community Dent Oral Epidemiol 1998;26:49S– 61S. [8] Kachondham Y, Dhanamitta S, Oyunbileg M, Brown L. Child health and nutritional status in Ulaanbaatar, Mongolia: a preliminary assessment. Asia Pac J Public Health 1992-93;6:226 –32. [9] WHO. The growth chart. A tool for use in infant and child health care. Geneva: World Health Organization, 1986.

1176

H.M. Karvonen et al. / Nutrition Research 23 (2003) 1165–1176

[10] WHO. Oral health surveys, Basic methods. 3rd ed. Geneva: World Health Organization, 1987. [11] Michaelsen KM, Weaver L, Brance F, Robertson A. Feeding and nutrition of infants and young children, guidelines for the WHO European Region, with emphasis on the former Soviet countries. WHO regional publications. European series; no. 87. Copenhagen: World Health Organization, Regional Office for Europe, 2000. [12] Feldman KW, Marcuse EK, Springer DA. Nutritional rickets. Am Fam Physician 1990;42:1311– 8. [13] Mongolian Annual report. Ulaanbaatar, Mongolia, 1997. [14] Matee M, van’t Hof M, Maselle S, Mikx F, van Palenstein Helderman W. Nursing caries, linear hypoplasia, and nursing and weaning habits in Tanzanian infants. Community Dent Oral Epidemiol 1994;22:289 –93. [15] Holt RD. Weaning and dental health. Proc Nutr Soc 1997;56:131– 8. [16] Dreizen. The mouth as an indicator of internal nutritional problems. Pediatrician 1989;16:139 – 46. [17] Alvarez JO. Nutrition, tooth development and dental caries. Am J Clin Nutr 1995;61:410S– 416S.