Nutrition, tooth development, and dental caries3

Jos#{233}
0 Alvarez

ABSTRACT Many studies involving small animals have caries experience in the deciduous teeth of undernourished
clearly shown that malnutrition affects tooth formation and Guatemalan children.
causes increased dental caries. We have conducted two cross- In 1986, we initiated a series of epidemiological studies in
sectional studies and one longitudinal study among Peruvian Peru to specifically address the question of whether malnutni-
children to investigate the effect of early malnutrition on oral tion in children caused changes in tooth development and led to
health. The cross-sectional studies have shown that in malnour- increased dental caries. We conducted two cross-sectional
ished children the pattern of caries development as a function studies and one longitudinal study in children living in a
of age is significantly altered as a result of a delayed eruption northern suburb of the city of Lima that have provided direct
and exfoliation of the deciduous teeth. This phenomenon has evidence linking nutritional status, tooth eruption, and dental

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made difficult the observation by other scientists of a clear caries.
effect of nutritional status on total caries experience because
the comparison of age-adjusted caries data between popula-
tions of children with different nutritional status is inappropri- Cross-sectional studies
ate. The use of peak caries activity has allowed the observation
The purpose of the two cross-sectional studies was to inves-
of a strong association between malnutrition and increased
tigate whether there is a significant association between current
dental caries. The longitudinal study has confirmed the results
nutritional status and dental caries. The first cross-sectional
of the cross-sectional studies and has demonstrated that one
study (14) was conducted in 285 children, 133 boys and 152
mild to moderate malnutrition episode occurring during the
girls, aged 3-9 y. They were chosen at random from children
first year of life is associated with increased caries in both the
attending two elementary schools and two daycane centers in
deciduous and permanent teeth many years later. Am J
Cantogrande, a poor suburb located 16 km north of Lima, Peru.
Clin Nutr 1995;61(suppl):410S-6S
This is a community nonfluonidatedwith water, established by
poor Andean migrants, that has grown to a population of
KEY WORDS Malnutrition, nutritional status, dental car- :5O0 000 in 15 y. Although electricity is generally available,
ies, tooth eruption, children, Peru
running water, sewage disposal systems, and other public sen-
vices are not available to the majority of the households. Child
malnutrition is a prevalent problem and can be found in 50%
Introduction of the population aged <5 y. Drinking water is bought by the
barrel by 90% of the households and has a low fluoride content
It has been well documented in animals that early malnutri- (<0.1 ppm). The protocol for this study was approved by the
tion affects tooth development and eruption (1-3) and results in human subjects committees at both the University of Alabama
increased dental caries later in life (3, 4). Rats undernourished at Birmingham and the Universidad Peruana Cayetano
during the time that molars are being formed and fed a caries- Heredia, Lima, Peru.
promoting diet develop 50% more caries than do the controls Oral examinations were conducted at midmorning by three
(3, 5). Also, a protein-deficient diet in young rats leads to dentists using mouth mirror, explorer, and direct sunlight. The
delayed tooth eruption (6). Many factors may be responsible World Health Organization basic methods for oral health sun-
for the effect of malnutrition on increased dental caries in veys (15) were used for dental-caries scoring and the National
animals. Protein-energy malnutrition in rats has been shown to Institutes of Health/National Institute of Dental Research (NIH!
reduce salivary flow (7), affect salivary composition (7), alter NIDR) Dental Calibration Manual (16) was used for dentist
the immune system (8), and increase the acid solubility of calibration. Weight and height measurements were taken for
enamel (9). each child (dressed in light clothes and no shoes) by a
In humans, a cause-effect relationship between nutritional
status and dental caries has not been directly demonstrated 1 From the Departments of International Health and Nutrition Sciences,
(10). Indirect evidence in support of this effect can be found in
University of Alabama at Birmingham.
studies showing a high prevalence of linear enamel hypoplasia 2 Supported in part by USPHS research grant DE-06424 from the Na-
and dental caries in the deciduous teeth of rural Guatemalan tional Institute of Dental Research, National Institutes of Health.
children and their association with early infectious episodes 3 Address reprint requests to JO Alvarez, Department of International
(1 1, 12). Infante and Gillespie (13) observed a strong correla- Health, University of Alabama at Birmingham, lidwell Hall Room 106,
tion between the degree of linear enamel hypoplasia and Birmingham, AL 35294-0008.

410S Am J Clin Nutr 1995;61(suppl):410S-6S. Printed in USA. 1995 American Society for Clinical Nutrition
 NUTRITION AND DENTAL CARIES 411S

nutritionist-dietitian. The classification of Waterlow et al (17) 20.

for chronic (stunting) and acute (wasting) malnutrition was
used and the National Center for Health Statistics (NCHS)
growth tables were used as the standard. Children whose ie
height-for-age was <95% of the NCHS median (50th percen- S
tile) were classified as stunted (mild, 90% < height for age <
16
95%; moderate, 85% < height-for-age < 90%; severe, height
for age < 85%). Children whose weight-for-height was <90%
of the NCHS median were classified as wasted (mild, 80% < 14
weight-for-height < 90%; moderate, 70% < weight-for-height
<80%; severe, weight-for-height <70%). Stunting is a mea-
sure of past or chronic malnutrition whereas wasting indicates 12
current or acute malnutrition.
The
(Figure
pattern of caries development
1) showed a significant shift
as a function
to the right in the
of age
mal-
I 1! 5 6 7 I

nourished children. This phenomenon appeared to be a direct

a
consequence of a delayed eruption and exfoliation of the de-
Ag.(yws)
ciduous teeth. Because of the age of the cohort no eruption data
were obtained; however, a clear delay in the exfoliation of the FIGURE 2. Number of deciduous teeth as a function of age in well-
nourished (#{149})
and chronically malnourished (0) (stunted) children. From
deciduous teeth was observed, as shown in Figure 2.

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reference 14.
Because no direct caries comparison at any particular age
could be made because of the shifted pattern of caries devel-
opment that existed between the two groups of children, we demonstrated again a significant shift to the right of the age
decided to compare the percent of canious teeth. This compar-
distribution of caries among all malnourished groups. Wasting
ison, shown in Figure 3, clearly demonstrated that malnoun-
and stunting and wasting were associated with a greater delay
ished children had 40% of the deciduous dentition affected by
than stunting alone, suggesting that acute malnutrition (ie, low
caries; ie, an average of eight canious teeth compared with only
weight-for-height) has a more pronounced effect on tooth ex-
six for the normal children.
foliation than does chronic malnutrition (ie, low height-for-
The second cross-sectional study (18) involved a larger
age). A delay in the eruption and exfoliation of the deciduous
sample, 1481 children aged 1-13 y (737 boys and 744 girls)
teeth was indeed confirmed in these children as shown in
from the same community. In this study, children were also
Figure 6.
classified according to anthropometnic indexes as either 1)
normal, 2) wasted (acute malnutrition), 3) stunted (chronic
malnutrition), or 4) stunted and wasted. Figures 4 and 5
40

7.
35,

6
30

5
25

I
0
0

U
0 3 I 15

2
10

I
5

I I I
.1_f I I I I I I
_3 4 5 6 7 1 9
3 4 5 6 7 I I

FIGURE 1. Mean decayed, extracted, and filled deciduous teeth FIGURE 3. Percent carious deciduous teeth as a function of age in
(DEFT) vs age in well-nourished (#{149})
and chronically malnourished (0) well-nourished (S) and chronically malnourished (0) (stunted) children.
(stunted) children. From reference 14. From reference 14.
412S ALVAREZ ET AL

8 20

7 18

6 .c 16
Wasted
0
(acute malnutrition) ! 14
5
V

w4 0 12
0

2 0
.0
E6
Z4
0
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14
2
Age (years)
0
FIGURE 4. Decayed, extracted, and filled teeth (DEFT) vs age in 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14
normal, well-nourished children (#{149})
and children suffering from acute Age (years)
malnutrition or wasting (0). From reference 16. FIGURE 6. Number of erupted deciduous teeth vs age in normal,
well-nourished children (#{149})
and wasted children (0) (acute malnutrition).
From reference 16.
A question that remained unclear was whether malnutrition
in children led to an increased caries experience. It is likely that

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the effect of nutritional status on the timing of tooth eruption made. Stunted and wasted children also had significantly
and caries development, described above, has been an impor- higher decayed, missing, and filled (DMF) values at ages 13
tant confounder that has prevented epidemiologists and clini- and 14 y than did normal, well-nourished children, as shown in
cians from observing a clear-cut effect of malnutrition on caries Figure 8. These findings suggest that malnutrition is associated
experience in children. One way to separate the effect of with increased dental caries in both the deciduous and the
nutritional status on the timing of caries development from that permanent teeth.
on the number of caries is to examine peak caries activity, as The significant changes in the age distribution of dental
shown in Figures 4 and 5. The peak caries activity in the caries in the deciduous teeth reported in this study of malnoun-
deciduous teeth of the malnourished children, particularly the ished children may have important implications for epidemio-
wasted (DEFT = 7, where DEFT is the number of decayed, logical studies of dental caries. First, comparisons of age-
extracted, and filled teeth) and the stunted and wasted (DEFT adjusted dental caries data between different countries on
= 7), was found to be higher than that in normal, well- between different regions within a country cannot be made
nourished children (DEFT = 5.5). These results indicate that without the nutritional factor (ie, skeletal growth) being taken
malnutrition is indeed associated with increased caries in the into account. Second, the fact that infected, carious molars stay
deciduous dentition. Furthermore, examination of the caries 2-3 additional years in the oral cavities of children with mal-
prevalence in specific teeth (Figure 7) shows that, at ages nutrition at an age when most of the permanent teeth emerge
8-1 1, first and second deciduous molars in malnourished chil- (8-i 1 y), particularly the first permanent molar, may increase
dren developed more caries than did first and second deciduous the amount of caniogenic bacteria in the mouth and thus may
molars in normal, well-nourished children. Malnutrition is in- increase the risk for caries development in the permanent
deed associated with increased dental caries in the deciduous dentition.
teeth. In conclusion, malnutrition in children not only delayed
When the caries experience of the permanent teeth was tooth development and affected the age distribution of dental
examined in these children, an important observation was

100

90
0 Normal

rII
-
, WastIng (acute malnutritIon)
80 Stunting (chronic malnutrition)

70
I Stunting and Wasting
6
60
5 50

w 4
0

0 1.3yrs 4-7yrs 8-1 lyrs 1-3yrs 4.7yrs 8-1 lyrs 1.3yrs 4.7yrs 8-1 lyrs
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Cuspids Ftrst Molars Second Molars
Age (years)
FIGURE 7. Percentage of carious deciduous teeth as a function of
FIGURE 5. Decayed, extracted, and filled teeth (DEFT) vs age in nutritional status (ie, wasting or acute malnutrition, stunting or chronic
normal, well-nourished children (S), stunted children (0) (chronic malnu- malnutrition, and stunting and wasting) and age range. Lines on bars
trition), and stunted and wasted children (E). From reference 16. represent SDs. From reference 16.
 NUTRITION AND DENTAL CARIES 413S

8 DecIdUOUS Teeth Permanent Teeth - 8 ing not only acute malnutrition but malnutrition that had oc-
7- -7
curred soon after birth.

8- -8
The degree of malnutrition in all cases was mild to moderate
and did not require hospitalization. Acutely malnourished chil-
5 5
Lu dren recuperated within 3 mo after recruitment solely on the
O 4 4
0 basis of nutritional and medical counseling provided by the
3 3
health personnel participating in the study. This counseling was
2 2
provided equally to the mothers of all children participating in
the study. The children in the study were followed until ap-
0
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 proximately 4 y and no additional episodes of acute malnutni-
Age (years) tion occurred after the initial one during infancy. Throughout
FIGURE 8. Left ordinate: decayed, extracted, and filled deciduous teeth the follow-up period, each child was given a dental examina-
(DEFT) as a function of age in normal children (#{149})
and stunted and wasted tion regularly, usually every 4-6 mo. Tooth eruption and DEFT
children (0). Right ordinate: decayed, missing, and filled permanent teeth were recorded. Caries criteria included both the visual and
(DMFT) as a function of age in normal children (U) and stunted and wasted tactile method according to the World
Organizations Health
(0) children. basic guidelines for oral health surveys (15). All examinations
were carried out under the same lighting conditions by one of
caries, but it was also associated with a higher number of three dentists. The examination techniques and diagnostic cni-
carious deciduous and permanent teeth. tenia were standardized, and the intra- and interobserver van-

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ability were minimized at the outset of the study by a series of
standardization procedures according to the NIH/NIDR Dental
Longitudinal study Calibration Manual (16).
The data, composed of 2700 examinations, were analyzed by
The longitudinal study (19) was conducted from 1986 to
using the Statistical Analysis System (SAS Institute Inc, Cary,
1990 in 209 children residing in Canto Grande, a poor, pen-
NC) General Linear Models (GLM) program to compute anal-
urban community of 500 000 located 16 km north of Lima,
Peru. ysis of variance (ANOVA) tables and statistical significance

The children were recruited as infants, aged 6-li mo, from was determined by the GLM procedure with Tukeys studen-
the outpatient population of the Canto Grande Health Center, tized range HSD and LSD t test options. The alpha level was
on from the outpatient population of the Universidad Peruana 0.05. The variables of interest included the number of teeth and
Cayetano Heredia Hospital and the Collique Hospital of moth- the number of DEFT, at specific ages, with the nutritional
ens residing in Canto Grande. All children in the study were of status of the child at the time of recruitment into the study,
full-term gestation and normal birth weight (>2500 g), and indexed by group, as the independent factor. Number of teeth
entered the study at age 6-1 1 mo. Upon recruitment into the and DEFT by group were analyzed at ages 1, 1.5, 2, 2.5, 3, and
project, each child was assigned to one of four study groups, 4 y. The examinations included in the analysis had an age range
dependent on his on her nutritional status, ascertained by of the specific age plus or minus 1 mo for all the ages except
weight and height measurements, employing the following 4 y. Age 4 had a range of plus or minus 2 mo to capture the
NCHS standards as the reference. majority of the final clinical exams.
1) Normal: children who were normal height-for-age (>95% The results of this study confirmed that the eruption
of standard) and normal weight-for-height (>95% of standard). of deciduous teeth is delayed by malnutrition, as shown in
2) Wasted: children aged 6-1 1 mo who were of normal Table 1. These findings are consistent with similar observa-
height-for-age but low weight-for-height (<90% of standard), tions made in several other studies. Researchers in India (20-
indicating current acute malnutrition. 23), Guatemala (1 1, 12), Tunisia (24), Australia (25), Norway
3) Stunted: children aged 6-11 mo who were of normal (26), Gambia (27), and Nigeria (28) among others have re-
weight-for-height, and low height-for-age (<95% of standard), ported that malnutrition is associated with a delayed eruption of
indicating past or chronic malnutrition. the deciduous teeth. Also, our previous cross-sectional studies
4) Stunted and wasted: children aged 6-1 1 mo who were from Cantogrande (Peru) have documented this effect (14, 18).
both of low weight-for-height and low height-for-age, indicat- The present study has shown that one malnutrition episode

TABLE 1
Number of teeth in the oral cavity as a function of age and nutritional status

ly 1.5y 2y 2.5y 3y 4y

Normal 7.4 2.3 [72]2 14.6 2.2 [6512 17.4 1.7 [69] 19.5 1.0 [69] 20.0 [65] 20 [80)
Wasted 5.7 2.8 [34) 13.5 2.6 [37) 16.9 2.0 [40] 19.5 1.3 [36] 19.9 0.4 [41] 20 [25]
Stunted 5.7 2.1 [46] 12.8 2.6 [46] 16.5 1.6 [48] 18.9 1.4 [52] 19.8 0.5 [50] 20 [55]
Stunted and wasted 5.9 2.2 [21] 12.9 2.6 [19] 16.3 1.6 [21] 19.3 1.1 [22] 19.8 0.5 [26] 20 [29]
, n in brackets.

2 Significantly different from the other three groups; P < 0.05.

3 Significantly different from the stunted and stunted and wasted groups, P < 0.05.
4 Significantly different from stunted, P < 0.05.
414S ALVAREZ El AL

occurring during the first year of life is sufficient to cause a

significant delay in the eruption of all deciduous teeth, even 8
though some of the teeth erupted 2 y after the malnutrition
episode (Figure 9). Moreover, it is apparent that stunting, ie,
retarded linear growth, is more strongly associated with de-
6
layed tooth eruption than is wasting. The smaller effect of
wasting on tooth eruption was observed until age 1 .5 y whereas
the effect of stunting only disappeared by age 3 y (Table 1). I:
w
It would be expected that chronic malnutrition (stunting)
would have a greater impact than acute malnutrition (wasting)
on tooth eruption. Stunted children suffered the nutritional
insult soon after birth, ie, before the age of 6 mo, and this insult 2
was more prolonged than that of wasting. At this time, most of
the teeth are still being formed, and therefore, a nutritional
injury at this age would likely have a deleterious effect on all
0
deciduous teeth. For the wasted children, the nutritional insult
occurred immediately before or during recruitment, right at or 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0
Age in Years
after 6 mo of age. An episode of malnutrition at this stage of a
childs development would likely affect the formation of the FIGURE 10. Decayed, extracted, and filled deciduous teeth (DEFT) as

second deciduous molars only, and partially that of first decid- a function of age for children who were either normal, wasted, stunted, or

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stunted and wasted before the age of 1 y. The DEFT for stunted and wasted
uous molars. This time difference in the onset and duration of
children at the age of 4 y is significantly different from the other three
stunting vs wasting may explain the difference in the extent of
groups (P < 0.01). From reference 17.
their effort on the eruption pattern of the deciduous teeth.
The caries data have clearly demonstrated that a nutritional
injury occurring early in the life of a child, when most of the malnutrition episode, sex, and age could not explain the dif-
deciduous teeth are still being formed (10), will make that child ferences in dental caries observed within the group (data not
more susceptible to dental caries 3-4 y later. Our study has shown). Despite the fact that the stunted and wasted group
shown that a prolonged malnutrition episode in infancy that showed a bimodal DEFT distribution, this group of children
leads to both stunting and wasting results in more caries by the showed not only a significantly higher mean DEFT but also a
age of4 y (Figure 10). It is important to note here that although significantly lower proportion of these children (3.4%) had 3
no differences in caries were observed by the age of 4 between caries compared with 20-29% in the other three groups, as
the normal, the stunted, and the wasted groups, the malnour- shown in Figure 12. This suggests that even though there were
ished children had a delayed tooth eruption that likely resulted two distinctly defined caries populations in the stunted and
in delayed caries development (14, 18). Therefore, additional wasted group, all of the children in this group had relatively
differences in DEFT could be expected at a later age. high numbers of caries. Additional studies of these children
This longitudinal study has confirmed the strong association may help to clarify this matter.
between malnutrition and increased dental caries in the decid-
uous teeth. Thus, children who suffered a single but prolonged More recent findings from the longitudinal study
malnutrition episode during infancy (ie, stunting and wasting)
had more caries by the age of 4 y than did children who either In 1992, we reexamined 94 of the children who participated
had no malnutrition at all or less severe forms of malnutrition. in the longitudinal study. The children were 6 y old at the time
Interestingly, the stunted and wasted cohort showed a bimodal
distribution of DEFT as presented in Figure 11, suggesting that NORMAL WASTED
#{190}
there was a subgroup of children who had an unusually high
incidence of caries. A closer examination of these childrens
nutritional and clinical data in terms of the severity of the
15

1
15

1 K#{149}#{149}Ii -

Lower CIntT Idaors -4

I 23 5 6 7 I 910111213141516 I 2 3 4 5 8 7 8 910111213141516
DEFT DEFT
Upper Central icisors -4

Upper Latsrai hclsors -4 I

STUNTED % STUNTED S WASTED

2C
Lower Lateral Icisors -.

#{149}

-
15
c_
1
let Molsts

StIdMolsrs

I I I I I I
I 2 3 4 5 6 7 8 910111213141516 1 2 3 4 5 6 7 8 910111213141516
200 300 400 500 600 700 800 DEFT
DEFT

Ag at Eruption (days)
FIGURE 11. Percent frequency distribution of decayed, extracted, and
FIGURE 9. Eruption pattern for the deciduous teeth according to filled teeth (DEFT) at the age of 4 y for children who were either normal,
nutritional status. (#{149}),
normal children; (0), wasted children; (U), stunted wasted, stunted, or stunted and wasted by the age of 1 y. From reference
children; (0), stunted and wasted children. 17.
 NUTRITION AND DENTAL CARIES 415S

25
w
-I
20
U)
U.
0 15
0
z
10
0
z
5

FIGURE 14. Decayed and filled deciduous teeth (DFT) and decayed
and filled deciduous surfaces (DFS) as a function of nutritional status in
6-y-old children. Statistically significant difference, P < 0.01.

DEFT Conclusion

FIGURE 12. Percent of children with low (0-3), high

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moderate (4-7),
Our cross sectional studies have shown that in malnourished
(-12), or very high ( 13) decayed, extracted, and filled teeth (DEFT)
children, the pattern of caries development as a function of age
values at the age of 4 y as a function of nutritional status before the age
is significantly altered, showing a delay that is the direct
of 1. From reference 17.
consequence of a delay in the eruption and exfoliation of the
deciduous teeth. This phenomenon has made difficult the ob-
servation by other scientists of a clear effect of nutritional
of this evaluation. Examinations included not only tactile and status on total caries experience because the comparison of
visual exams but also peniapical and bitewing radiographs to age-adjusted caries data between populations of children with
assess interproximal caries. different nutritional status is inappropriate. However, the use of
The results
of this study showed that, surprisingly, the erup- peak caries activity or percent of canious teeth has allowed us
tion of the permanent teeth (ie, incisors and first molars) is to demonstrate clearly that malnutrition is associated with
accelerated in malnourished children, as shown in Figure 13. increased dental caries in the deciduous teeth. Moreover, these
Also, a significantly higher number of caries was observed in studies also suggested that malnourished children develop
both the deciduous teeth (Figure 14) and the permanent teeth more caries in the permanent teeth.
(Figure 15). Our longitudinal study has confirmed the previous observa-
In summary, this longitudinal study has shown that a single, tions and has demonstrated a clean association between early
moderate malnutrition episode occurring in infancy (<1 y of malnutrition (ie, a malnutrition episode occurring during the
age) is associated with increased dental caries later in life, first year of life) and increased caries in the deciduous teeth.
possibly as a consequence of a deleterious effect on the for- Interestingly, our most recent findings suggest that although
mation of tooth enamel early in life. This finding agrees with malnutrition delays the eruption of the deciduous teeth, it
previous experimental studies in animals and confirms the appears to accelerate the eruption of the permanent teeth.
indirect evidence from cross-sectional epidemiological studies
in human populations that had suggested a cause-effect rela-
tionship between malnutrition and increased dental caries. 1.2

1.0

I-
6
I l __ * Cl)
0.8
w ____j D NORMAL
w 5 0
I-
IU WASTED 0
-H STUNTED -1 z 0.6
Im STUNTED

1
AND WASTED

I *
> 0.4 LH
I
INCISORS
LkMAX.
MOLARS
N.. ....).
MOLARS
0.2

0.0
DMFT DMFS
FIGURE 13. Number of permanent incisors, maxillary (max), and FIGURE 15. Decayed, missing, and filled permanent teeth (DMFT) and
mandibular (mand) permanent molars and total number of permanent teeth decayed, missing, and filled permanent surfaces (DMFS) as a function of
in 6-y-old children according to nutritional status. Statistically significant nutritional status in 6-y-old children. #{149}
Statistically significant difference,
difference, P < 0.01. P < 0.01. Statistically significant difference, P < 0.001.
416S ALVAREZ El AL

Nevertheless, malnutrition results in increased dental caries in linear hypoplasia of human deciduous incisors. J Dent Res 1969;48:
both the deciduous and the permanent dentitions. 1275-9.
Because our studies were conducted in children with mild to 13. Infante PF, Gillespie GM. Dental caries experience in the deciduous

moderate malnutrition, this effect is likely to be quite pervasive dentition of rural Guatemalan children ages 6 months to 7 years. J Dent
Res 1976;55:951-7.
among children of low socioeconomic condition in both devel-
14. Alvarez JO, Lewis CA, Saman C, et al. Chronic malnutrition, dental
oped and developing nations. Thus, these children are at higher
caries, and tooth exfoliation in Peruvian children aged 3-9 years. Am
risk for developing dental caries, and preventive measures
J Clin Nutr 1988;48:368-72.
should be applied early on. Also, future epidemiological stud-
15. World Health Organization. Oral health surveys: basic methods. 3rd
ies of dental caries prevalence, particularly comparisons of ed. Geneva: World Health Organization, 1986.
different populations, should take into consideration the con- 16. National Institute for Dental Research. NIH/NIDR dental calibration
founding effect of nutritional status. manual. Bethesda, MD: National Institute for Dental Research and
WESTAT, 1979.
17. Waterlow JC, Buzina R, Keller W, Lane JM, Nichaman MZ, Tanner
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