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Effect of undernutrition on deciduous tooth emergence among Rajput children of Shimla District of Himachal Pradesh India.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 000:000–000 (2012)
Effect of Undernutrition on Deciduous Tooth
Emergence Among Rajput Children of Shimla
District of Himachal Pradesh, India
Rajan Gaur and Pawan Kumar
Department of Anthropology, Panjab University, Chandigarh 160014, India
KEY WORDS
dental eruption; nutritional status; sequence; timing
ABSTRACT
This article examines the influence of
nutritional status on the emergence of deciduous dentition
in a cross-sectional sample of 510 rural Rajput children from
the Jubbal and Kotkhai Tehsils, Shimla District, Himachal
Pradesh, India. The nutritional status of each child was
evaluated using Z-scores of height/supine length-for-age
(HAZ), weight-for-age (WAZ), and weight-for-height (WHZ).
The effects of sex and side on deciduous dental emergence
were not statistically significant. Partial correlation indicates that the number of emerged teeth (T) was more
strongly correlated with height than with other anthropo-
metric variables. In most age groups, the stunted boys and
girls (HAZ <22) had fewer emerged teeth than nonstunted
age peers (HAZ >22). The mean T in underweight children
was also less than that of the normal children, with a few
exceptions. The stunted children have a significantly greater
likelihood of delayed emergence of deciduous dentition.
Measures of linear growth status are more closely related to
dental development than measures of growth in mass. The
findings indicate that even moderate undernutrition can
delay deciduous tooth emergence. Am J Phys Anthropol
000:000–000, 2012. V 2012 Wiley Periodicals, Inc.
Tooth emergence is of interest to physical anthropologists, dental professionals, biologists, and forensic scientists. It provides a reliable indication of maturation and
biological age (Zadzinska et al., 2000) and thus serves as
a useful tool to determine age of children in populations
without birth records (Folayan et al., 2007). Most of the
authors define the time of clinical emergence as the
instant at which any part of the crown emerges through
the gingival surface, even though eruption continues as
each tooth moves into occlusion (Hillson, 1998; Bastos
et al., 2007b). Emergence is different from tooth calcification, which is the process whereby calcium salts are
deposited in the dental enamel (Zwemer, 1993).While the
former may be significantly delayed by undernutrition,
the latter is less affected by nutrition.
It is now widely accepted that dental emergence is to
a major extent under genetic control (Garn, 1977; Gaur
and Singh, 1994; Hughes et al., 2007; Gaur et al., 2011).
However, several environmental factors have been
reported to influence tooth emergence. Studies show that
underprivileged children have retarded eruption relative
to their higher socioeconomic peers (Enwonwu, 1973;
Saleemi et al., 1994). However, Folayan et al. (2007) did
not find any significant impact of socioeconomic status
on primary tooth emergence in Nigerians. Delayed
emergence of deciduous teeth was reported by a few
workers in low birth weight children (Viscardi et al.,
1994; Lawoyin et al., 1996; Sajjadian et al., 2010).
Emergence of deciduous dentition may also be retarded in
stunted children as was demonstrated by Bastos et al.
(2007b) in a sample of stunted Brazilian children. A couple of studies report that preterm children may have
fewer teeth as compared with their full-term counterparts
(Magnusson, 1982; Fadavi et al., 1992). A few studies,
however, suggest that deciduous dentition develops independent of general body development (Voors, 1957;
Shuper et al., 1986). Accelerated primary tooth emergence
was reported among children born to mothers who
smoked during pregnancy (Rantakallio and Makinen,
1984). Several studies report delayed emergence among
children with poor nutritional status (Kitamura, 1942;
Infante and Owen, 1973; Delgado et al., 1975; Ulizaszek,
1996; Kodali, 1998; Agarwal et al., 2003; Holman and
Yamaguchi, 2005; Bastos et al., 2007b; Psoter et al.,
2008). These studies suggest that apart from genetics,
dental emergence may be influenced by some environmental factors also.
Undernutrition in children is commonly assessed from
derived indices of height/supine length and weight,
namely weight-for-age (WAZ), height/supine length-forage (HAZ), and weight-for-height/supine length (WHZ),
expressed as Z-scores. Low WAZ may reflect both past
(chronic) and/or present (acute) undernutrition (Cogill,
2003) and is diagnostic of an ‘‘underweight child.’’ HAZ
is an indicator of past or long-term (chronic) growth failure resulting in ‘‘stunting.’’ WHZ detects ‘‘wasting" that
is a measure of current or acute very severe nutritional
stress leading to weight falling significantly below the
expected weight for same height/supine length.
The sequence and timing of emergence of deciduous
dentition have been examined in many human populations (Liversidge, 2003). However, several issues related
to deciduous tooth emergence, such as degree of population variability, the influence of growth, and effect of
nutritional status have yet to be fully resolved. Several
C 2012
V
WILEY PERIODICALS, INC.
C
*Correspondence to: Prof. Rajan Gaur, H. No. 1452, Sector: 44-B,
Chandigarh 160047, India. E-mail: rajan_gaur7@yahoo.com
Received 3 January 2011; accepted 20 January 2012
DOI 10.1002/ajpa.22041
Published online in Wiley Online Library
(wileyonlinelibrary.com).
2
R. GAUR AND P. KUMAR
Fig. 1. Generalized location map of the area.
TABLE 1. Distribution of sample children in various age groups according to sex
Boys
Girls
0.00–0.49
0.50–0.99
1.00–1.49
31
25
30
29
46
31
Age group (in years)
1.50–1.99
2.00–2.49
27
31
studies indicate that only severe undernutrition delays
the emergence of deciduous dentition (Jelliffe and
Jelliffe, 1973; Mukherjee, 1973; Billewicz and McGregor,
1975; el Lozy et al., 1975; Arvystas, 1976; Khan et al.,
1981; Rao, 1985; Kodali et al., 1993; Saleemi et al., 1994;
Kodali, 1998; Agarwal et al., 2003; Bastos et al., 2007a).
These studies also suggest that moderate undernutrition
did not have any substantial delaying effect on primary
tooth emergence. However, a set of studies reports that
even moderate undernutrition may result in delayed
emergence of primary teeth (McLaren et al., 1964; Rao
et al., 1973; Truswell and Hansen, 1973; Delgado et al.,
1975; Hull, 1983; Shuper et al., 1985; Fadavi et al.,
1992; Holman and Yamaguchi, 2005). A few workers
found no effect of undernutrition on deciduous tooth
emergence (Graham and Morales, 1963; Pindborg et al.,
1967; Jelliffe and Jelliffe, 1968; McGregor et al., 1968;
Trupkin, 1974). In contrast to these studies, Cifuentes
and Alvarado (1973) reported early emergence in undernourished Guatemalan children. There are, thus, varied
results with respect to the effect of undernutrition on
deciduous tooth emergence and the issue remains unresolved. This article examines a sample of Rajput children
from the state of Himachal Pradesh of India to assess
American Journal of Physical Anthropology
33
34
2.50–2.99
3.00–3.49
3.50–3.99
Ages combined
31
32
33
33
34
30
265
245
the influence of undernutrition on the emergence of
deciduous dentition.
MATERIALS AND METHODS
This investigation is based on a cross-sectional sample
of 510 rural Rajput children (265 boys and 245 girls).
The subjects included in the study were clinically
healthy and ranged in age from birth to 48 months. The
data were collected from the villages of Jubbal and Kotkhai Tehsils of the Shimla District of Himachal Pradesh
(Fig. 1), through a house-to-house survey. The dates of
birth of the subjects were taken either from the birth
certificates or from the parents. The decimal age was
calculated from the date of birth and date of examination (Tanner and Whitehouse, 1966). The children in this
sample were grouped into eight age groups of 6 months
each. The age-wise distribution of the sample children is
given in Table 1.
The study area and the people
The Shimla District of Himachal Pradesh in North
India lies between the longitudes 778 00 and 788 190 east
3
EFFECT OF UNDERNUTRITION ON DECIDUOUS TOOTH EMERGENCE
TABLE 2. Median ages (MD) and interquartile ranges (IR) of emergence of deciduous dentition among Rajput children (years)
Left
Tooth
Males
i1
i2
c
m1
m2
Females
i1
i2
c
m1
m2
Maxilla
MD (IR)
Right
Mandible
MD (IR)
Maxilla
MD (IR)
Combined
Mandible
MD (IR)
Maxilla
MD (IR)
Mandible
MD (IR)
1.16
1.24
1.86
1.58
2.31
(0.28)
(0.47)
(0.81)
(0.64)
(1.39)
1.13
1.59
1.97
1.69
2.51
(0.39)
(0.76)
(1.01)
(0.60)
(1.18)
1.16
1.27
1.86
1.60
2.45
(0.28)
(0.48)
(0.81)
(0.45)
(1.22)
1.12
1.55
1.95
1.69
2.54
(0.43)
(0.74)
(0.95)
(0.60)
(1.07)
1.16
1.26
1.86
1.59
2.28
(0.28)
(0.48)
(0.81)
(0.52)
(0.90)
1.12
1.57
1.96
1.69
2.46
(0.42)
(0.75)a
(0.94)
(0.60)
(1.01)
1.17
1.25
1.88
1.64
2.37
(0.36)
(0.50)
(0.61)
(0.49)
(0.80)
0.93
1.47
2.04
1.64
2.34
(0.66)
(0.56)
(0.74)
(0.72)
(0.60)
1.17
1.27
1.88
1.62
2.34
(0.36)
(0.43)
(0.61)
(0.43)
(0.93)
1.00
1.47
1.97
1.71
2.24
(0.57)
(0.56)
(0.57)
(0.79)
(0.58)
1.17
1.25
1.88
1.63
2.35
(0.36)
(0.41)
(0.61)
(0.44)
(0.88)
0.96
1.47
2.00
1.68
2.34
(0.62)a
(0.56)
(0.71)
(0.74)
(0.59)
Significant interjaw difference (Bonferroni adjusted alpha level of P \ 0.01).
Values in parentheses represent the interquartile ranges.
a
and latitudes 308 450 and 318 440 north. The area is
mountainous with altitude ranging from 1200 to 2700 m
above mean sea level. The staple food of the villagers of
this area generally consists of wheat, rice, and maize. In
addition, pulses like ‘‘Urd" (Black Lentil), ‘‘Lobia" (Blackeyed Bean), ‘‘Moong" (Green Lentil), and ‘‘Kulth" (Brown
Lentil) are used almost daily. The people usually take
three to four meals a day. They are very fond of rice,
which is consumed at least once a day. The people also
like meat and those who can afford consume it occasionally at dinner. A large majority (89%) of the children of
this sample belong to the lower middle income families
with a per capita income of \Rs. 800 per month.
METHODS
For this investigation, a cross-sectional study design
was used. The subjects were examined only once for gingival emergence of deciduous dentition. The sequence and
number of emerged deciduous teeth were recorded on a
specially designed proforma. Each child was examined in
daylight or, if necessary, with the help of a torch to record
the number of emerged teeth (T). The appearance of any
part of the cusp or crown through the gingiva was considered to be an emerged tooth (Demirjian, 1986; Holman
and Jones, 1998, 2003; Suri et al., 2004; Bastos et al.,
2007b; Folayan et al., 2007; Woodroffe et al., 2010). The
teeth that had erupted but subsequently clinically
extracted were also counted as emerged (only four such
cases were recorded). In addition to dental emergence
data, height/supine length and weight of each subject
along with some general information reflecting the socioeconomic status were also recorded. The supine length,
height, and weight of the children were measured using
standard methods (Weiner and Lourie, 1981). Supine
length was measured in children below the age of 18
months, height in children above this age. Median ages of
emergence of permanent teeth were calculated employing
the probit transformation (Mayhall et al., 1978).
Height was measured with a Harpenden anthropometer with subject standing, with head in Frankfort plane,
on a horizontal surface with heels together, stretching
upward to the fullest extent, aided by gentle pressure on
the mastoid processes by the measurer, with back as
straight as possible. The horizontal arm of the anthropometer was brought down to touch the highest point on
the subject’s head (vertex) in the mid sagittal plane.
Supine length was measured with an infant measuring
table, with infant lying supine. The infant’s head, in the
vertical Frankfort plane, was brought to touch the fixed
headboard by one measurer, while the infant’s feet, with
toes pointing directly upward, were held by the second
measurer who also brought the moveable footboard to
rest firmly against the infant’s heels. Weight was measured with a portable field survey scale.
The nutritional status of each subject was assessed
with the help of height/supine length and weight, which
are the two basic measurements for the assessment of
nutritional status (WHO, 1986). As per the recommendations of World Health Organization (WHO, 1983), the following derived indices were calculated for each child to
assess the nutritional status: WAZ, HAZ, and WHZ. The
reference data of the World Health Organization (WHO,
2006) was used to assess the nutritional status. For each
individual, the nutritional status was calculated as
Z-scores or S.D. scores, following Waterlow et al. (1977).
The cut-off point for undernourished children was taken
as 22 SD scores below the reference median, as recommended by the WHO (1983). Stunting, underweight and
wasting were defined as Z-scores 22 SD or less of HAZ,
WAZ and WHZ, respectively, of WHO (2006) reference
standards. The usual cut-off points for moderate and
severe undernutrition are: Z-scores of 22 S.D. and 23
S.D., respectively, below the reference median (WFP,
2005). The interjaw, bilateral, and gender differences,
which were, largely, not significant, were evaluated
using Mann-Whitney test. The relationship between anthropometric parameters and T and its significance was
calculated using partial correlation. Where multiple ttests were involved, a Bonferroni adjusted alpha level
was used to reduce the possibility of Type-I errors.
RESULTS
Table 2 shows the median age of emergence of deciduous teeth among the Rajput children according to sex,
side, and jaw. The mandibular central incisors were the
earliest set of teeth to emerge. The maxillary central
incisors emerge next followed by the maxillary lateral
incisors and mandibular lateral incisors. Next, emerge
the maxillary and mandibular first molars, canines, and
last the second molars. The overall sequence of emergence of the full complement of deciduous teeth among
Rajput children of this sample was i1, i1, i2, i2, m1, m1,
American Journal of Physical Anthropology
4
R. GAUR AND P. KUMAR
TABLE 3. Descriptive statistics (Mean 6 SD) of weight, height/supine length, and Z-scores of HAZ, WAZ, and WHZ
of Rajput children according to age and sex
Age (years)
Males
0.00–0.49
0.50–0.99
1.00–1.49
1.50–1.99
2.00–2.49
2.50–2.99
3.00–3.49
3.50–3.99
Females
0.00–0.49
0.50–0.99
1.00–1.49
1.50–1.99
2.00–2.49
2.50–2.99
3.00–3.49
3.50–3.99
a
Z-Scores
Height/Supine
Length (cm)
Weight (kg)
HAZ
WAZ
WHZ
61.1
67.3
75.6
80.2
85.1
88.3
93.2
96.8
6
6
6
6
6
6
6
6
5.37
2.89
4.67
3.70
3.76
3.90
4.07
4.23
5.46
7.59
9.47
10.76
11.47
12.30
13.56
13.78
6
6
6
6
6
6
6
6
1.26
1.41
1.35a
1.53
1.62
1.09
1.47
1.26
20.51
21.20
21.39
21.43
21.39
21.76
20.95
21.15
6
6
6
6
6
6
6
6
1.42
0.87
1.48
1.17
1.04
1.12
1.00
0.96
20.95
21.11
21.29
20.99
21.24
21.23
20.94
21.38
6
6
6
6
6
6
6
6
0.73
1.22
1.15
1.22
1.29
0.74
0.81
0.65
20.84
20.42
20.58
0.36
20.42
20.39
20.42
20.88
6
6
6
6
6
6
6
6
0.90
1.08
0.89
1.03
1.08
1.00
0.73
0.90
61.4
67.3
73.9
79.4
83.5
86.4
91.3
95.2
6
6
6
6
6
6
6
6
3.53
2.90
4.17
5.63
4.67
3.39
4.16
3.39
5.41
7.56
8.65
10.73
11.11
11.55
12.96
13.37
6
6
6
6
6
6
6
6
0.90
1.18
0.99
1.74
1.60
1.37
1.26
2.78
0.14
21.07
21.36
21.39
21.58
22.01
21.31
21.17
6
6
6
6
6
6
6
6
1.04
0.96
1.99
1.74
1.33
0.91
1.02
0.89
20.56
20.92
21.44
20.55
21.01
21.38
21.09
21.14
6
6
6
6
6
6
6
6
0.72
1.14
0.78
1.44
1.17
1.03
0.77
0.96
20.80
20.18
20.81
20.04
20.45
20.59
20.29
20.45
6
6
6
6
6
6
6
6
0.63
1.36
0.69
1.20
0.87
0.97
0.79
0.98
Significant sex difference (Bonferroni adjusted alpha level of P \ 0.01).
TABLE 4. Incidence (%) of undernourished children (<22 SD
scores) based on the Z-scores of HAZ, WAZ, and WHZ
Age (years)
Males
0.00–0.49
0.50–0.99
1.00–1.49
1.50–1.99
2.00–2.49
2.50–2.49
3.00–3.49
3.50–3.99
Combined
Females
0.00–0.49
0.50–0.99
1.00–1.49
1.50–1.99
2.00–2.49
2.50–2.49
3.00–3.49
3.50-3.99
Combined
Stunting
(\22 HAZ)
Underweight
(\22 WAZ)
Wasting
(\22 WHZ)
19.4
30.0
47.9
55.5
54.3
54.9
21.2
41.1
40.7
(6)
(9)
(22)
(15)
(18)
(17)
(7)
(14)
(108)
22.6
33.4
45.7
40.7
48.6
38.7
24.2
41.1
37.3
(7)
(10)
(21)
(11)
(16)
(12)
(8)
(14)
(96)
32.3
13.3
17.4
18.5
21.2
9.7
9.1
29.4
18.9
(10)
(4)
(8)
(5)
(7)
(3)
(3)
(10)
(50)
8.0
37.9
45.2
51.6
61.8
71.9
48.5
46.6
47.8
(2)
(11)
(14)
(16)
(21)
(23)
(16)
(14)
(117)
4.0
34.5
35.5
16.1
32.4
40.6
27.3
26.6
27.8
(1)
(10)
(11)
(5)
(11)
(13)
(9)
(8)
(68)
16.0
24.1
19.4
9.7
11.7
18.7
9.1
13.4
15.1
(4)
(7)
(6)
(3)
(4)
(6)
(3)
(4)
(37)
Values in parentheses represent the number of individuals.
c1, c1, m2, and m2 for males and i1, i1, i2, i2, m1, m1, c1,
c1, m2, and m2, for females. The average length of time
from the eruption of the first tooth to the last tooth in
mandible was 1.34 years in males and 1.38 years in
females. In maxilla, it was 1.12 years in males and 1.18
years in females. On an average, deciduous dentition
was almost complete by the age of 2.5 years.
Table 3 shows the age and sex specific descriptive statistics of height/supine length, weight, and Z-scores of
HAZ, WAZ, and WHZ. As expected, the mean height/
supine length and weight increase with increase in age
in both boys and girls. The mean Z-scores of HAZ
broadly increased up to the age of three in both sexes.
The mean Z-scores of WAZ increased up to the age of 1.5
years in the boys as well as the girls; the trend was not
clear thereafter. A clear trend could not be noticed for
WHZ. A student’s t-test with Bonferroni adjusted alpha
American Journal of Physical Anthropology
level of 0.01 revealed that, on the average, the sex differences in mean height/supine length, weight, HAZ, WAZ,
and WHZ were statistically not significant.
Table 4 depicts the rates (%) of undernutrition (\22
SD scores) based on Z-scores of HAZ, WAZ, and WHZ,
according to age and sex, among the Rajput children of
this sample. It can be seen in the table that 40.7% boys
and 47.8% girls were stunted (\22 HAZ); of these 12.8%
boys and 13.1% girls were severely undernourished (\23
HAZ). The incidence of underweight children (\22 WAZ)
was 37.4 and 27.8% in boys and girls, respectively. The
prevalence of wasting (\22 WHZ) was distinctly less
(18.9% in boys and 15.1% in girls). It is also clear from
the table that broadly, in both sexes, the percentage of
stunted children was clearly higher than that of underweight children. The rate of wasting was the minimum.
In this sample, a majority of the children were suffering
from chronic or long-term rather than acute undernutrition. On the average, the rate of stunting increased up
to 2.5 years. The percentage of underweight children
broadly increased up to 1.5 years. The trend was not
clear for wasting.
An examination of Table 4 reveals that, up to 2 years,
the rate of stunting was higher in boys; the girls overtook the boys thereafter. The percentage of underweight
boys was higher up to 2.5 years. The pattern was not
clear for rates of wasting. To evaluate the overall significance of sex differences in rates of undernutrition a Chisquare (v2) test was used. The test resulted in v2 values
of 38.97 for stunting, 142.99 for underweight, and 60.4
for wasting. The results of the test indicate that overall
rate of stunting was significantly (P \ 0.05) higher in
the girls, while the rate of wasting and underweight
individuals was significantly (P \ 0.05) more in boys.
Table 5 depicts the values of partial correlation
between the T and height/supine length (Ht), weight
(Wt), and Z-scores of HAZ, WAZ, and WHZ. The partial
correlation for Ht/T was significant (P \ 0.05) at 1–2
years for boys and 1–3 years in girls. The partial correlation for Wt/T was significant (P \ 0.05) from 1 to 2 years
in boys and from 1.5 to 2.5 years in case of girls. The
Z-scores of HAZ showed significant partial correlation
(P \ 0.05) with T from 1 to 2 years in boys and from
5
EFFECT OF UNDERNUTRITION ON DECIDUOUS TOOTH EMERGENCE
ber of emerged deciduous teeth was more strongly correlated with height/supine length than with weight.
Table 6 displays the mean T among normal (>22 SD
scores) and undernourished (\22 SD scores) children as
specified by the Z-scores of HAZ, WAZ, and WHZ. Since
multiple t-tests were employed, to reduce Type-I errors,
a Bonferroni adjusted alpha level of 0.01 is used to evaluate the statistical significance of t-tests. It is evident
from the table that the stunted (\22 HAZ) boys and
girls had less mean T as compared with their normal
peers in most age groups. The differences were significant (P \ 0.01) in 1.50–1.99 and 2.00–2.49 age groups in
girls and 1.00–1.49, 1.50–1.99, 2.50–2.99, and 3.00–3.49
age groups in boys.
The mean T in underweight children (\22 WAZ) was
slightly less than that of their normal counterparts, with
a few exceptions. However, the differences were not significant in both sexes. Children with low WHZ show a variable pattern. The low WHZ girls from 0.5 to 3 years
showed a slightly less mean T than normal girls. However,
low WHZ boys below the age of 1.5 years had slightly
more mean T than even normal boys. These results are
found in young age groups, and there is high variation. A
closer examination of Table 6 reveals that in only one age
group each in boys (2.00–2.49) and girls (1.00–1.49), the
low WHZ or severely undernourished children showed
significant retardation in dental emergence.
The mean T of the stunted (\–2 HAZ) and underweight (\–2 WAZ) boys was less than that of the girls in
a majority of the age groups, which indicates that emergence delay was more among the undernourished boys
than the girls. Interjaw differences were not clear in this
respect.
1 to 3 years in girls. The partial correlation of Z-scores
of WAZ was significant from 1 to 2 years in boys and
from 1 to 2.5 years in girls. The partial correlation of
Z-scores of WHZ with the T was broadly not significant
in both sexes.
Overall, the girls displayed a stronger correlation of
the T with a majority of the parameters considered here.
Table 5 further indicates that, overall, the partial correlation of the T was significant at more age groups with
height/supine length and Z-scores of HAZ than with
weight and Z-scores of WAZ and WHZ. Thus, the numTABLE 5. Results of partial correlation (r) of number of
emerged teeth (T) with Height/Supine length (Ht), Weight (Wt),
and Z-scores of HAZ, WAZ, and WHZ of Rajput children
Age
(years)
Males
0.00–0.49
0.50–0.99
1.00–1.49
1.50–1.99
2.00–2.49
2.50–2.99
3.00–3.49
3.50–3.99
Females
0.00–0.49
0.50–0.99
1.00–1.49
1.50–1.99
2.00–2.49
2.50–2.99
3.00–3.49
3.50–3.99
r
(Ht/T)
r
(Wt/T)
r
(HAZ/T)
r
(WAZ/T)
r
(WHZ/T)
0.157
0.179
0.661a
0.702a
0.229
0.084
0.271
–
0.347
0.185
0.442a
0.635a
0.093
0.032
0.179
–
0.140
0.250
0.622a
0.679a
0.006
0.166
0.136
0.017
0.003
0.243
0.402a
0.636a
0.069
0.003
0.061
0.109
0.197
0.142
0.026
0.333
0.107
0.047
0.036
0.178
–
0.026
0.451a
0.644a
0.456a
0.559a
–
–
–
0.071
0.225
0.454a
0.437a
0.256
–
–
–
0.038
0.496a
0.630a
0.456a
0.563a
0.150
–
–
0.092
0.405a
0.448a
0.440a
0.240
0.070
–
–
0.109
0.096
0.012
0.246
0.034
0.042
–
DISCUSSION
Significant partial correlation (P \ 0.05).
–: Correlation not computable because either no tooth had
emerged in any individual of the age group or all individuals in
the age group had a complete complement of 20 teeth.
a
Timing of tooth emergence is multifactorial (Alvarez and
Navia, 1989). Several factors have been reported to influence the time and sequence of emergence of deciduous
TABLE 6. Age and sex specific means 6 S.D. of T, according to nutritional status, as specified by Z-scores of HAZ, WAZ, and WHZ
among Rajput children
HAZ
Age (years)
Males
0.00–0.49
0.50–0.99
1.00–1.49
1.50–1.99
2.00–2.49
2.50–2.99
3.00–3.49
3.50–4.00
Females
0.00–0.49
0.50–0.99
1.00–1.49
1.50–1.99
2.00–2.49
2.50–2.99
3.00–3.49
3.50–4.00
22 S.D. scores
or less
(undernourished)
WAZ
[22 S.D.
scores
(normal)
22 S.D. scores
or less
(undernourished)
WHZ
[22 S.D.
scores
(normal)
22 S.D. scores
or less
(undernourished)
[22 S.D.
scores
(normal)
0.00
1.00
5.90
10.70
16.33
17.92
18.50
20.00
6
6
6
6
6
6
6
6
0.00
2.13
1.96a
2.83a
1.80
1.62a
1.91a
0.00
0.19
0.77
9.41
15.12
16.46
19.37
19.81
19.83
6
6
6
6
6
6
6
6
0.87
1.90
4.98
4.01
2.66
1.38
0.58
0.76
0.00
0.86
7.53
12.37
15.88
18.80
19.00
19.60
6
6
6
6
6
6
6
6
0.00
2.27
3.90
4.86
3.05
1.78
1.73
0.89
0.25
0.83
8.82
15.63
16.88
19.53
19.73
19.97
6
6
6
6
6
6
6
6
1.00
1.87
5.07
3.25
2.23
1.21
0.83
0.18
0.26
2.00
11.00
11.00
13.75
20.00
19.00
19.75
6
6
6
6
6
6
6
6
1.03
3.46
8.18
7.07
3.30a
0.00
0.00
0.50
0.00
0.70
8.23
14.96
17.00
19.40
19.75
19.97
6
6
6
6
6
6
6
6
0.00
1.75
4.54
3.76
2.12
1.32
080
0.18
0.00
1.50
6.09
12.00
14.91
19.25
20.00
20.00
6
6
6
6
6
6
6
6
0.00
0.83
1.81
3.26a
3.12a
2.17
0.00
0.00
0.00
1.73
8.45
15.80
17.72
20.00
20.00
20.00
6
6
6
6
6
6
6
6
0.00
2.14
3.54
3.23
2.64
0.00
0.00
0.00
0.00
1.80
6.88
12.66
15.50
19.11
19.97
20.00
6
6
6
6
6
6
6
6
0.00
0.44
4.25
3.05
4.72
2.66
0.19
0.00
0.00
1.56
8.00
15.00
17.73
19.82
20.00
20.00
6
6
6
6
6
6
6
6
0.00
2.06
3.35
3.72
2.20
0.83
0.00
0.00
0.00 6
0.00 6
1.00 6
–
10.00 6
20.00 6
20.00 6
–
0.00
0.00
1.41a
0.00
1.67
8.14
14.77
17.42
19.59
19.97
20.00
6
6
6
6
6
6
6
6
0.00
1.96
3.22
3.68
2.81
1.64
0.18
0.00
0.00
19.58
0.00
a
Significant difference in the T between undernourished (22 S.D. or less) and normal children (Bonferroni adjusted alpha level of
P \ 0.01).
–: No undernourished individual in the age group.
American Journal of Physical Anthropology
6
R. GAUR AND P. KUMAR
teeth, which include weight, height, nutritional status,
ethnicity, socioeconomic status, and disease (Al-Jasser and
Bello, 2003; Gaur et al., 2011).
Some studies have indicated marked sex differences in
malnutrition in India, with a higher prevalence of undernutrition among girls (Sen and Sengupta, 1983; Tarozzi
and Mahajan, 2007). Some reports linked this with gender inequalities in nutrient intake because of nutritional
neglect of girls (Behrman, 1988; Borooah, 2004). This
may not hold true for whole of India because of regional
differences in nutritional status as has been reported by
Tarozzi and Mahajan (2007) and Lancaster et al. (2006).
The gender differences are reported to be more striking
in northwest and east India where the presence of widespread son preference has been documented (Tarozzi and
Mahajan, 2007). This sample did not show any nutritional neglect of girls. The rate of stunting, an indicator
of long-term undernutrition, was higher in girls but the
rates of underweight and wasting, indictors of acute and
severe undernutrition, respectively, were higher in boys.
Thus, the rates of undernutrition do not reflect any clear
gender bias in this sample.
The relationship between deciduous tooth emergence
and height and weight has been the subject of several
investigations. It has been reported that low-birth
weight infants have delayed emergence (Fadavi et al.,
1992; Harris and Barcott, 1993; Viscardi et al., 1994)
and eruption is advanced in higher birth weight infants
(Delgado et al., 1975; Khan et al., 1981; Sajjadian et al.,
2010). Holman and Yamaguchi (2005) suggested that
earlier emergence in higher birth weight children may
be due to heavier infants being born at later gestational
ages. There are, however, a few studies, which suggest
that deciduous tooth emergence was an independent process and not related to height and weight (Falkner,
1957; Shuper et al., 1985, 1986; Haddad and Correa,
2005). In this study, a positive correlation was noticed
between the number of emerged deciduous teeth and
height/supine length and weight in some age categories.
This is consistent with several other studies that report
a positive correlation between height and weight and
deciduous tooth emergence with taller and heavier children having a greater T at a given age (Billewicz, et al.,
1973; Enwonwu, 1973; Infante and Owen, 1973; Jelliffe
and Jelliffe, 1973; Rao, 1985, 1992). Infante and Owen
(1973) suggested that since stature and weight are
related to nutritional status, deciduous tooth emergence
might be an indicator of nutritional status.
Overall, the correlations in this sample were not significant in the younger age groups and the oldest two
age groups for a majority of the parameters considered
here. It should be noted that the critical ages for assessing variation in emergence patterns are from 0.5 to
3.0 years. This is because, before 0.5 years, very few
infants have any teeth, whereas after 3 years, almost all
the children have a complete complement of 20 deciduous teeth. This probably accounts for poor correlation in
the youngest and the older two age groups.
The correlations were stronger with stature as compared to weight, which is consistent with the findings of
Rao (1992) who reported that the correlation of height
and T was more distinct. McGregor et al. (1968) and
Infante and Owen (1973) also reported a strong positive
association between stature and number of emerged
deciduous teeth, with children having more deciduous
teeth present for a given age being taller than those
with fewer teeth. Spier (1918) noted that there was a
American Journal of Physical Anthropology
functional relationship between stature and physiological status as defined by dentition. Garn et al. (1965)
reported that taller children were slightly advanced in
permanent tooth formation and movement. Sutow et al.
(1954) and Lee et al. (1965) demonstrated a significant
positive association between permanent tooth emergence
and skeletal maturation. Thus, a stronger correlation
with stature could be because of the fact that development of dentition, a skeletal element, is more likely to
be influenced by factors that affect skeletal growth. A
better correlation with stature rather than weight may
exist because there is a strong relationship between
eruption and skeletal growth (Psoter et al., 2008). In
view of a stronger correlation between tooth emergence
and stature, Tanguay et al. (1986) suggest that clinical
standards for emergence of deciduous teeth were more
accurate and efficient when scaled to height rather than
chronological age. The results of this study suggest that
deciduous dental emergence was more strongly correlated with linear growth (i.e., skeletal) as compared to
growth in mass.
Nutrition is an important environmental factor that
influences deciduous tooth emergence. Yun (1957) concluded that deciduous tooth eruption may be greatly
delayed by nutritional disturbance. Psoter et al. (2008)
found that early childhood malnutrition not only delays
emergence of deciduous teeth but could delay emergence
of permanent dentition because of its delaying effect on
the exfoliation of primary teeth.
Previous studies have reported in the past that only
severe undernutrition resulted in delayed emergence of
deciduous dentition while moderate undernutrition had
no significant effect (Jelliffe and Jelliffe, 1973; Mukherjee, 1973; Billewicz and McGregor, 1975; el Lozy et al.,
1975; Arvystas, 1976; Khan et al., 1981; Rao, 1985;
Kodali et al., 1993; Saleemi et al., 1994; Kodali, 1998;
Agarwal et al., 2003; Bastos et al., 2007a). Our findings
are not consistent with these studies.
In this case, even moderately undernourished (\22
Z-scores) Rajput children had, on the average, less T than
their normal counterparts. Our findings are consistent
with findings of several other studies, which also indicate
that even moderate and less severe undernutrition could
delay emergence of primary dentition (McLaren et al.,
1964; Truswell and Hansen, 1973; Rao et al., 1973;
Delgado et al., 1975; Hull, 1983; Shuper et al., 1985;
Fadavi et al., 1992; Holman and Yamaguchi, 2005).
In this sample, stunted children had significantly less
T as compared with their normal peers. In a sample of
Brazilian children, Bastos et al. (2007b) had also
reported fewer emerged deciduous teeth in stunted children as compared with their normal counterparts. Thus,
it can be safely concluded that, in this sample, ‘‘chronic
or long-term" undernutrition as indicated by low HAZ
significantly retards dental emergence. The impact of
‘‘acute/severe" undernutrition (low WHZ) on deciduous
tooth emergence in this case was not clear. It emerges
that the stunted children had a significantly greater
likelihood of having fewer emerged deciduous teeth at a
given chronological age than their normal peers and that
even moderate undernutrition may delay deciduous
tooth emergence.
These findings have implications for anthropologists,
demographers, public health workers, and other
researchers who use primary tooth emergence data for
estimation of chronological age of infants and children
from undernourished populations, particularly in rural
EFFECT OF UNDERNUTRITION ON DECIDUOUS TOOTH EMERGENCE
and tribal areas of the developing world, in which the tradition of maintaining birth records does not exist. The
findings may also be relevant to dental clinicians as a
delay in eruption can directly affect the accurate diagnosis, planning, and timing of treatment in orthodontic
patients (Suri et al., 2004). Since these findings are based
on a cross-sectional sample, these may require further
confirmation through additional longitudinal studies.
CONCLUSIONS
The results indicate a relationship between stature,
weight, and the emergence of deciduous dentition. The
number of emerged deciduous teeth is better correlated
with stature than weight. We conclude from these
findings that nutritional status may be an important
factor that can influence the timing of deciduous tooth
emergence. Delayed deciduous tooth emergence is more
pronounced in stunted children. Measures of linear
growth status are, thus, more strongly correlated with
dental development than measures of growth in mass/
weight. Emergence can be delayed in children with
even moderate undernutrition. In addition to genetic
factors, some extraneous factors such as nutrition may
also influence the timing of emergence of deciduous
dentition.
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