Nutritional supplementation and the development enamel hypoplasias in children from Tezonteopan, Alan
H Goodman,
Celia
ABSTRACT effect ofnutritional subsequent in Mexican
Martinez,
and
The purpose of this study intake during tooth-crown
development nonsupplemented
of linear enamel (control)
Adolfo was
Chavez
to compare the formation on the
hypoplasias adolescents
(LEHs)
(n
42)
=
and adolescents who had received daily nutritional supplements since birth (n = 42). The proportion of individuals with LEHs was nearly two-fold greater (74.4%; 95% CI 64.7-84. 1%) in the control
than
50.4%;
in the
at formation, ofearly
supplemented
P
9.44;
=
X2
‘2-2.5
(before
group
0.001).
=
Although
y, is similar
crate
undernutrition
during
study
enamel
suggest
that
formation
to the formation 773-81.
of
LEHs.
Am
J Clin
KEY
Nutritional
status,
chronic
WORDS
dental
development,
oping
dental
enamel
mild
that
to modlinked
Nuir
1991 ;53:
with
the
ciency.
duration
of maternal,
Experimental
studies
devel-
A variety enamel These
opmental
characteristics.
of physiological ( 1-3). Because
It is highly
of the
a variety susceptible
of unique
devel-
to a wide
variety
perturbations (stressors) during enamel is unable to remodel, the
physiological perturbations pattern of developmental cause
with
regular
and
is semipermanently defects of enamel ring-like
nature
the locations of these developmental provides an estimate of individuals’ logical disruption (3, 4, 6). Because of enamel, it can yield record ofphysiological
recorded in the (2-5). Finally, beapposition,
defects on tooth crowns ages at the time of physioofthe unique characteristics
a relatively permanent stress, potentially useful
shown
vitamin
that
effects
eruption
protein
A defiand
energy
and reduced and colleagues
of protein
during
in
associated
key
and
energy
periods
of de-
of
studies
suggests
a relationship
and protein-energy been frequently noted believed
to be suffering
undernutrition. ofthese defects
population an increased
IL (‘-950-1300
AD).
1 7th-l9th-century
slaves
habitants
of a 19th-century shown
high
upper
prevalence
(PEM). and his-
mild
(17) related
a temporal increase such as a decreased
(2 1) have
from
Swardstedt was inversely
between
malnutrition in prehistoric
to moderate
showed that to socioeconomic
the
from Westerhus, and prevalence of defects
in other indicators of early growth velocity, at Dickson Analyses from
of the Barbados
New ofenamel
York
skeletons (20)
state
of
and
in-
poorhouse
hypoplasias.
Nearly
all (92.3%) permanent dentitions of African Americans (many ofwhom were former slaves) who were buried in the First African Baptist Church cemetery in Philadelphia (1823-1843) displayed
amelogenesis record of past
of enamel
of human
populations
degrees prevalence
Mounds,
tissue
was
pregestational
the separate size and
hypoplasias defects have
former is an epithelial
rats
lead to delayed dental development ofteeth (12-14). Work by Navia
on tooth
that paralleled undernutrition,
Introduction
disruption
A-deficient have
status in a medieval Swedish Goodman et al ( 1 8, 1 9) found
countries
Enamel
degree
of vitamin
roughly associated H Mellanby ( 1 1)
velopment.
toric
malnutrition, Mexico,
the
in offspring
restriction
is causally
hypoplasia,
of developmental
enamel
(1 5, 16) demonstrated
age
and in
of this
3.0 y) LEHs
demonstrated
peak
the proportion
the control group. LEH was also more common in females was associated with an increase in illness days and a decrease Results
(after
groups,
dental defect Similarly,
CI 28.6-
in
velocity.
late
in both
95%
estimated
in dogs, with the severity ofthe with the intensity of deficiency.
deficiencies can size and weights
was greater
growth
1.5 y) and
(39.5%; the
of linear Mexico3
one
or more
enamel
hypoplasias
temporary prevalence
populations. of enamel
Guatemalan
children
Sweeney hypoplasia with
whereas Sawyer and Nwoku in Nigeria for undernutrition
and chronologic in epidemiolog-
(22).
More direct evidence for the relationship between undernutrition and enamel hypoplasias has been noted in studies of con-
third-
et al (23) found on deciduous vs second-degree
(24) found displayed
that children an increased
an
increased incisors of
malnutrition, hospitalized prevalence
ical studies. However, for this potential to be more fully realized, the relationship between enamel development and common stressors velopment
affecting needs
Experimental micronutrients, physiological a developmental
infants and children to be better understood. studies along
stressors, defect
have with can caused
shown a wide lead
during that
tooth-crown
severe
variety
to an enamel by a disruption
de-
deficiencies
of
other
of
systemic
hypoplasia
(7-9),
in enamel-matrix
apposition (3-5). For example, M Mellanby (10) demonstrated that vitamin D deficiency could lead to an enamel hypoplasia Am
J
(Yin Nuir
1991:53:773-81.
Printed
in USA.
© 1991 American
Downloaded from https://academic.oup.com/ajcn/article-abstract/53/3/773/4731893 by Washington University, Law School Library user on 05 June 2018
Society
I From the School MA and the Division de Nutricion, Tlalpan, 2 Supported in part of Health and by the
of Natural Science, Hampshire College, Amherst, de Nutricion de Communidad, Instituto Nacional Mexico. by grant R03 DEO8607 from the National Institutes 3M Corporation, St Paul. 3 Address reprint requests to A Goodman, Natural Science, Hampshire College, Amherst, MA 01002. Received April 19, 1990. Accepted for publication July 18, 1990. for Clinical
Nutrition
773
774
GOODMAN
ofsevere enamel hypoplasia compared trol subjects. Enwonwu (25), in a study
Western
Nigeria,
deciduous
teeth
increased
did not find any gross in “well-fed”
prevalence
of defects
prominent
Studies
among
based
and on deciduous nutrition
and
et al (26). enamel Solis
and
children
of
noted
with
forms
an
poorer
of malnutrition
to milder
teeth
in a study
in Mexico
found
on
permanent
determined
a high
(46.7%)
of children
on the
basis
of mal-
by Goodman
prevalence
teeth
that
forms
of
from
of their
the
position
on the anterior teeth, most enamel hypoplasias developed in the second to third year. Also noted were statistical associations between the presence ofan enamel hypoplasia and low height-forage and socioeconomic status (27). Whereas all these studies suggest a causal relationship between enamel hypoplasias and poor nutrition (and other stresses associated
with
low
socioeconomic
status),
no
studies
have
cx-
amined nutritional intake or status at the time of enamel devclopment and related it in longitudinal fashion to the prevalence and pattern of enamel defects. This study is based on a followup of children from a long-term nutritional-supplementation study. It was designed to help answer the question of whether chronic mild development oping
areas
to moderate undernutrition and of a degree frequently ofthe
world
predisposes
at the time of enamel found in many devel-
people
to have
AL
gaging
(25). severe
extended
authors
hypoplasias Valley
he
were
permanent
These
factors
on the more
teeth
hypoplasias
whereas
in village
confrom
status. He concluded that enamel to disruptions from stressors asstatus, with severe malnutrition
these
mainly
enamel
children,
diets and lower socioeconomic development was susceptible sociated with low socioeconomic being
with well-nourished ofYoruba children
ET
in subsistence
and
In 1968,
the
year
in which
eating
a traditional
30% of families
diet
own
land,
1 5% rent land, and 15% are paved road is ‘-9 km from
the
first
study
participants
were
born, 1495 individuals resided in Tezonteopan (43.8% aged < 15 y), with natality and mortality rates of55.0/1000 and 14.5/1000, respectively, (28) and a mean yearly per capita income of $55 US(28).
The
without
electricity
0.5
fluoride/L
mg
majority
ofhouses
consisted
or plumbing
ofsingle
rooms
(28). The town’s
(samples
drawn
in June
(84.8%) contained
water
1988
and
January
1990; N Tinnanoff, unpublished observations). A 48-h weighted dietary survey that was completed at the start of the supplementation study indicated that 69% of energy was derived
from
sugar
(28).
tortillas, The
1 1% from
mean
daily
black
protein
beans,
and
and
energy
10%
nitrogen
intake)
X lOOJ
and
8280
Id,
from
intakes
individuals in the community was 55.6 g [net protein (NPU) 63%; NPU = ([nitrogen intake - nitrogen
for
all
utilization excretionj/
respectively.
Preschool
children consumed a similar diet with a daily average of 3030 Id and 19.2 g protein, far below recommended levels(28). Chavez and Martinez (28) suggested that the population’s mean energy and
protein
intakes
and that National Id
dren
are
10% and
37%
the preschoolers are Institute of Nutrition’s
and The
32 g protein. dietary data
study
an increased
agriculture
based on maize and beans. About 40% belong to collectives (ejidos), landless day laborers. The nearest the town (28).
are
undertaken 1 and
below
by a cross-sectional
growth
three-fourths
(n
levels Mexican of 5225
Almost
4 y ofage
recommended
further below the recommended levels
supported
in 1977.
between
even
426)
=
(73.7%)
were
found
of chil-
to be below
reference values for observations, 1972). to have mild malof75-90% of weight-
in the 2) to
90% of the Mexican population’s median weight-for-age (28; R Galvan, unpublished The majority ofthesc children was considered nutrition [47.4%; Gorncz classification (26) for-age] or moderate malnutrition (2 1 . 1%; age). A greater proportion of the females
in the
(21 .2%)
or third-degree
3) to compare the pattern and prevalence of LEH to both past and current anthropometric measures; and 4) to examine the role of respiratory and diarrheal disease as an additional variable that may further explain the relationship between nutritional status and the development of an enamel hypoplasia.
nutrition
frequency
poses
ofdifferent of this enamel
linear
characterized
with
same
community
estimate
and
Subjects
the and
and
to moderate
group
with
compare
nonsupplemented
The
specific
pur-
the risk of developing in a group of control children
(LEH) mild
a supplemented but
defects.
1) to examine
as having
pared
ofenamel
types
study are hypoplasia
improved age
malnutrition,
of children
at development
supplemented
corn-
residing
nutritional
a
status; of LEHs
children;
methods
The nutritional-supplementation
The child
growth,
physical
Indian
activity,
community
Mexico
City
and
little
migration,
cognition.
all reside
25 km ‘
to the
north
rural
180 km of Atlixco
Nahuatl
(Aztec)
to the south in the
central
made
child
adding
inhabitants
en-
Downloaded from https://academic.oup.com/ajcn/article-abstract/53/3/773/4731893 by Washington University, Law School Library user on 05 June 2018
study
nonsupplemented
18 and
height
mal-
and
and
to be within
cm) and
Newborns
(a measure
ofChavez
mothers had to be one and four preg-
36 y of age,
(137-154
community.
score
The
the
group as were
to match
± I
socioeconomic
needed
to
at birth,
of neonatal
following
were
maternal This
study
year,
recruited
used
have
a birth
and to receive
physiological
weight was
the
control
an
status)
and
Its protocol of Nutrition’s
of
nutritional
human
height,
milk
and
was
approved
by the
subjects vitamin
birth
weight
of a dearth
of
on the growing Mexican
committee
in the form
in-
socioeconomic
infant’s
because
malnutrition
with
for
effort
Great
family
mainly
supplement,
64 g powdered
supple-
criteria
the nonsupplemented
including
justified was
in the
same
subjects.
as possible
ofcritcria
on the affect ofmoderate
(28).
individuals
by use of the
for the
as closely
on a variety
knowledge
and
with
males
oftwo groups of mothergroup was recruited begin-
To be included in this group, diseases, to have had between
the
inclusion
Institute
poor,
supplementation
the recruitment
2.5 kg, to be free ofdisease
>
Beginning
(28).
of
second-
8 (28).
1600 m above sea level (28). Tezonteopan for study because it was relatively isolated,
typically
for
status,
in the
of Tezonteopan,
Mexican highlands, was originally selected with
and
study
The
to be between
dividuals
in this
dyads.
of the mean
undernutrition
resistance,
ofthe
Z score
chronic
as disease
design
(28) involved
APGAR
such
as having
nancies,
mented
Subjects
basic
fling in 1968. free ofobvious
The sample was derived from people enrolled in Proyecto Puebla, a continuously operating nutritional supplementation program named after the state of Puebla and initiated by the Mexican National Institute of Nutrition in 1968 (28). Proyecto Puebla was designed to provide information on the effect of on functions
classified
weight-for-
than
1 .5%)
(28).
Martinez
status weight
study
was
60-75%
(3
National (28).
of a drink fortification
made
by
and
fla-
UNDERNUTRITION voring
to
180
first missed
mL
water,
was
low
lactation
during
The
of
vitamin 000
100
200
IU vitamin
whole
1986).
9 1 5 Id and
2 1 .6 g protein/
17.7
g protein/d
contributed A, 20
during
an
mg thiamin,
The
extra
daily
10 mg
ribo-
100 mg ascorbic acid, and 20 000 LV Schlaepfer, unpublished observations,
mo
supplement
1986). After in the (180
‘-4 form
the
of a bottle
mL)
wiches
and
and
commercial
glasses
has
amount
consumed
nience
of having
clinic. Previous
given
directly 1254
a profound
showed on such
of days 1986).
ill (28-3 Physical
supplemented cidence
to the
group
after
of parasitic
nearly
and
mainly
that
the
The
The 1988.
field
because
things
=
the
first
Solis,
study to the
year
examined,
42; 2 1 male,
Mexico
(26),
before
and
of -0.70. defects
surfaces ofdefect
0.5
y, 0.5-1.0
and
ending
ogy
for
was
shown in
26).
nonsupof days
Differences differed by
Replicas
of enamel.
equally divided 2 1 female) and groups.
On
aged
in Mexico
high reliable whether an protocol
for
human
subject
and
polysiloxane. poured
brief
(3-5-mm)
of Nutrition
over
same
observer sample)
between the nonsupplemented basis
a 20%
detectible
recorded
12 anterior,
followed
with
by type permanent
dental and
and
due
in
(diarrhea.l)
to
ofthe
found
of both Hampshire
was
study the
on
The
was Mexican
for
enamel (DDE (32). Previous blind
approved National
tween
to The
by the In-
College.
Downloaded from https://academic.oup.com/ajcn/article-abstract/53/3/773/4731893 by Washington University, Law School Library user on 05 June 2018
Reliability
of the
randomly
to provide
super-hard subject
and field
to a
allowed
to
assessment
an assessment selected
dental
of
by the
anterior
teeth
casts.
completed,
height,
from
data
weight,
were
oh-
data
at the
include
the
upper-respiratory
from control
develop
presented
on the
prevalence
22). Statistical
different
and central
control incisors,
we
results
of
in the
between were
periods
prevalence
group
carried
and
of LEH
by tooth
groups.
of
and
hypoplastic the
relationship
be-
Second,
disruption
is presented
vary
(1, 3, 26, 38),
is pre-
antimeres (contralateral the chronology of LEH
the most
analyses
(36)
disruption
of developmental
supplemented
analyses
ofLEHs
measurements,
nonsupplemented
sented by combining data from and other sets of teeth. Third, the maxillary
ill
gastrointestinal
(37).
during
and
of dental ofdays
as well as associations
to developmental
the supplemented
cir-
22), and
time
distribution
groups,
software
=
head
=
number and
to 6 y (n
birth
chronological
and were
and
to 2 y (n
birth
circumference
and anthropometric
teeth
present
with
were
illness
and and
first
bubbles
include
head
susceptibility
are
remove
completed
by use of SPSS-X
data
to
data
illnesses
Because
was
from
prevalence
in their
with
pour
intervals
and
period
a summarized
method
always supplements.
out
re-
standard
this classification
recorder nutritional
follow-up
location
made
of 100
growth
78). The
=
3-mo
observer
made
Each
the
at 6-mo
supplemented
a statistical-
teeth.
the epidemiological
elsewhere
committees
of -60% decrease
per
same
were
observations
weight,
in
crowns
which subjects were in the supplement and growth and illness data on a subsample
The
(n
edge
methodolagreement
the
were
be(birth-
tooth
replicas
(AHG)
cumference study
on
by
by comparison
all dental
(n
a defect
in
period.
from
regarding groups,
height,
supple-
of research
prevalence
that
collected.
of 84 in-
cx-
incisal
The
to six layers.
vacuum a 24-h
(10%
10 y (1
di-
For
zones
the
(interobserver
Dental
was estimated
exami-
at (26).
teeth
were
develops
nine
line
(maxillary)
in four
LEH and illness were
(26, 33-35). The individual received this
and
A total
the
a LEH
determined
of all
were cleaning
upper
which
into
Mexico
et al half-
crowns
repeatable
studies
of
at formation.
zones.
crown,
of
also
of Massler
y) starting
location
were
record ofthe field observations. Two-stage impresinvolving a base and wash layer, were made with
resin, harden
4.0-4.5
.
onto
Missing
equal-width,
tooth
divided
to
chronologies
ages
canine
incisor
highly
of the
vinyl
tamed control
in June
.
be
data,
into
cemento-enamel
previous
a permanent sions (casts),
LEH
.
(26).
developmental
y, was
the
to
88.9%)
3 y of age was
y
estimating
(AHG;
in-
central
age 4.5
at the
and
The
undertaken
who
be statistically
type
was
and
and
year-long
maxillary
obserin the
unpublished
classification of developmental defects of dental index) of the Federation Dentaire International
stitute
birth
(28, 30). Height
for a dental
we expected
subjects
power measure Dental-enamel
studies
the
tween
group, and the twice the number
participants
2 1 female)
would
labial
ample,
29).
zones
drawn
were
or attrition
divided
on
likely to be due (2-4, 17-27).
standard
were
paper
focused
location
these
dental-development
equal-width,
the
most
eruption
crowns
diffuse
6). This
been
by developmental
development into
Sup-
levels,
the tooth
4 and have
and
From
and
bands of dean area of to-
all defects
size
diagram.
constructed
incisor
1986).
had
horizontal involving types
types,
their
opacities
fine lines,
of quantitative defects or groove, hypoplasias
which
of incomplete tooth
were
vided
inconve-
ofdefect
ofdental
types with
FDI
defects,
to reflect
areas
By following
Tezonteopan
(combined
LEH-type
the
however,
of life (28,
defects
clinic
=
control
cording
defects
supplement
of illness profound.
defects
the supplement
the
milk
activity
diseases
ofenamel
were
(n
42; 2 1 male,
the
whole
ofthe
nutritional
as growth,
diarrheal
for developmental
dividuals mented
on
year-long
at the
enamel
diagram
children
three
opacities
were most often thin, thickness, occasionally
identification
After
recording
All available
nation
After
and
found:
in previous studies and are stressors such as undernutrition
a tooth
study
1 5.5 y) came
age
the most systemic
and
1986).
dental
concerns
noted
20 g protein/
2 y of age (28, 3 1 ; LV Schlaepfer,
at
observations,
missing
only
teeth
1 ; LV Schlaepfer, unpublished activity was greatly increased
of increased duration between groups were
10 cm
tally
(36),
infants
were diffuse
LEHs enamel
child sand-
ofdefects opacities,
without lines) and two types hypoplasias and horizontal-line,
(LEHs)J. creased
children
adolescence;
30% greater in the nonsupplemented plemented group suffered from nearly ill because in growth
opacities [pits-type
to the Later,
an extra
supplement
types
to the
observations,
into the
foods. given
Id and
has decreased to ingest
effect
percent vations,
baby were
unpublished continued
studies
directly powdered
milk
an extra
LV Schlaepfer,
plementation
given
semisolid
of low-fat
contributed
d (28;
was
of reconstituted
(28). The supplement roughly
Five
nicotinamide,
775
HYPOPLASIAS
(demarcated
during
observations, and
fortification
and
ENAMEL
the
D (28;
mg
IU vitamin
Id
after
to the mother
thereafter, to the infant. and recorded (28). The
extra
1330
libitum
given
pregnancy
a mean and
ad
were
unpublished
contributed
lactation. flavin,
(1.5%)
pregnancy
daily
lactation and, was monitored
Schlaepfer,
supplement d during dose
fat
(LV
given
Supplements
during pregnancy and The amount consumed milk
was
menstruation.
AND
teeth) in the
compared teeth.
for Finally,
between
776
GOODMAN
LEH
and
past
and
present
anthropometric
status
and
and left central incisor, mandibular left canine, right lateral incisor, and right central incisor). The relative risk (RR) of a LEH in the control vs the supplemented groups ranged from 1.59 (mandibular left central incisor) to 6.96 (maxillary left lateral
Results
incisor). The proportions of individuals with LEHs in the same zone 1 zone to allow for developmental variation and measurement error) on contralateral teeth (such as left and right upper canines) are presented in Table 2. This method eliminates asymmetric defects that are less likely to be due to systemic stress (3, 5).
Reliability
(±
Ofthe
100
buccal
tooth
surfaces
examined
on casts,
of LEH were observed, compared with an original of 31 cases of LEH in the field. Twenty-seven times
recorded
in both
of specific
the field and on the casts,
agreement
of 0.83.
A LEH
yielding
was
not
34 cases
assessment a defect was
Nearly
a proportion found
Prevalence
oflinear
enamel
hypoplasias
The prevalence of LEHs was relatively similar for contralateral but greatly varied by individual tooth types (Table I). The lowest prevalence ofdefects in both the supplemented and control groups was found on the maxillary left canine (supplemented teeth
2.6%;
control
15.0%)
2.4%;
control
16.7%).
and The
maxillary
left
greatest
incisor
prevalence
(72.2%) (7 1.2%)
of defects
in the
the supplemented
group].
and control
lateral teeth with matching
were
supplemented
groups
defects
found
on both
group The
and
difference
in proportions
was significant
an-
72/99 between
of contra-
for all maxillary
teeth and approached significance for the mandibular canine and central incisor (Table 2). The relative risk of a LEH in the control vs the supplemented group ranged from 1.5 to 5.0 for the six anterior tooth types. The proportion of individuals with one or more matched LEHs on anterior maxillary and mandibular teeth, a combination of the maxillary central incisor and mandibular canine (the two most hypoplastic teeth), and on any of the anterior studied
was also
computed
(Table
2). Differences
between
were not significant for the mandibular tooth prevalence but were significantly different for the maxillary tooth prevalence (P = 0.009), the central incisor-canine combination (P = 0.001), and the total prevalence (P = 0.001). The proportion of mdividuals with LEHs is 39.5% (95% CI = 28.6-50.4%) in the supplemented group and 74.4% (95% CI = 64.7-84. 1%) in the control group. The supplemented and control groups clearly differed groups
was
found on the maxillary central incisor (supplemented 38. 1% for left and 40.5% for right; control 7 1.4% for left and 66.7% for right). The prevalence of defects in the control group was greater than in the supplemented group for all 12 teeth examined. The differences in prevalence between groups approached significance (Mantcl-Haenszel estimation of X2, one-tailed P < 0.10 and P > 0.05) for three teeth (mandibular right canine and left lateral and central incisors) and was significant (P < 0.05) for seven of nine remaining teeth (maxillary left canine, left lateral incisor,
TABLE
[37/52
(72.7%) in the nonsupplemented
teeth
(supplemented of defects
three-fourths
timeres
in either
the field or on the casts in the remaining 62 cases, yielding an overall proportion of observed agreement of 0.89 (39). The Kappa statistic (K), a measure of agreement, yielded a value of 0.75 (SE of K = 0. 12; Z = 6.25, P < 0.001). Landis and Koch (40) suggest that values > 0.75 represent excellent agreement.
in the
overall
Distribution
prevalence
oJLEH
of LEH.
by age at formation
To evaluate the pattern age at time ofdevelopmental
of LEH development by individuals’ disruption, the central incisor was
1
Proportion
of individuals
wit h linear
enamel
hypoplasia
( LEH)
Supplemented Maxilla Right
canine canine RightI2 Left 12 RightIlil Left Ii Mandible Right canine
2.6
in the supplement
ed and control
Control
10.5 (4/38)
Left
*
AL
right
past
illnesses.
(1/39)
11.9(5/42) 2.4 (1/42) 38.1(16/42) 40.5 (17/42)
groups
RRt
x2f
17.9 (7/39)
1.70
0.85
15.0
5.77
3.73
0.027
21.4(9/42) 16.7 (7/42) 71.4(30/42)
1.80 6.96 1.87
1.36 4.91 9.30
66.7
1.65
5.71
NS 0.0 13 0.001 0.008
(6/40)
(28/42)
One-tailed
20.0 (8/40)
34.1 (14/41)
1.71
2.02
0.077
12.5 (5/40)
29.3 (12/41)
2.34
3.39
0.033
Right 12 Left 12 Right Ii
16.7 (7/42) 14.3 (6/42) 16.7 (7/42)
33.3 (14/42) 26.2 (1 1/42) 33.3 (14/42)
2.00
3.07
0.040
1.83 2.00
1.82
0.089
3.07
0.040
Left Il
21.4 (9/42)
34.1 (14/41)
1.59
1.65
0.098
as a combination
of Federation
Dentaire
International
size.
t Relative
risk (control/supplemented). the Mantel-Haenszel
f Computed by § Lateral incisor. II Central
method.
incisor.
Downloaded from https://academic.oup.com/ajcn/article-abstract/53/3/773/4731893 by Washington University, Law School Library user on 05 June 2018
defect
types
4 and
6 (32).
Numbers
in parentheses
P
NS
Left canine
Defined
sample
ET
are frequencies
of LEHs/
UNDERNUTRITION TABLE 2 Proportion of LEHs matched lower canine (CI combination),
AND
Maxilla Canine
2.6 2.4 33.3 36.8
12
Ii Total maxilla Mandible Canine 12
Ii Total mandible CI combinationt Any combination Numbers
divided
central
into
successive,
tooth] defects
y for the
group
opment of a defect 2. 17 y in the control
is 2.03 group.
be significantly
different
corresponding y, and 3.5-4.0
to defects y.
Whereas is little tween
groups,
groups
occur
1). When three
roughly
in the
of6
zones
[0.76
before
defects
developmental
TABLE 3 Comparison
on
the
groups
upper
zones
of the chronological
2.5-3.0
was
0.5-
main
time incisor
distribution
that
differences
central
those
are
be-
between
of disruption divided
y, 1.5-3.0
y, 3.0-4.5
of LEHs
on maxillary
*
Numbers
in parentheses
are frequencies
1.59
1.43
NS
1.83 1.88
8.97
0.001
9.44
0.001
3). The
were 0.006) relative
differences
and
of formation
Gender,
1972),
the
frequency
of LEHs
groups
before
1 .5 y and
group were 2.7 and relative risk (1 . 14) was that
during
status,
and illness
girls from Tezonteopan were of secondand third-degree
than
were boys (28; R Galvan,
we compared
the
in our sample
there
in females
vs males.
y)
dibular
canine,
central
incisors
in the control
Downloaded from https://academic.oup.com/ajcn/article-abstract/53/3/773/4731893 by Washington University, Law School Library user on 05 June 2018
develops
developed
their
peak
in period
(1.5-3.0).
differences,
size.
that
supplemented
into
14.6 (6/41) 33.3 (14/42) 4.8 (2/42)
con-
of a LEH
control vs supplemented In comparison, a low
anthropometric
for-age)
and
risks
in comparing control
supplemented
for defects developing between birth and between 3.0 and 4.5 y (P 0.002) (Table
after 3.0 y in the 6.0, respectively. found
between
found and
(Fig
2.4 (1/41) 7.1 (3/42) 11.9(5/42) 1 1.9 (5/42) 23.8(10/42) 16.7 (7/42) 4.8 (2/42) 0.0 (0/42) 0.0 (0/42)
of LEHs/sample
significant
females
Supplemented Six-month developmental periods Birth-0.5 y 0.5-1.0 y l.O-l.Sy 1.5-2.0 y 2.O-2.Sy 2.5-3.0 y 3.0-3.5 y 3.5-4.0 y 4.0-4.5 y Eighteen-month developmental periods Birth-l.5 y 1.5-3.0 y 3.0-4.5 y
most
trol groups 1 .5 y (P
Because prevalence
there
of LEH
the
the
group and found to
zones,
suggest
the peak
y for
1 .0 y, 3.0-3.5
distribution
(birth-1.5
per
age at devel-
for three
tendency
and after
and
supplemented of defects
the
1 .07
±
mean
of central that
to
highest prevalence of to defects forming
around
it is apparent
corresponding
a total
group
chronological
NS
0.056
size.
1 hypoplastic [1 .45 ± 1 .30 (1 ± SD) per
y in the Frequency
P
canine.
developing
the measures
difference
0.054
9.22
2.54
estimated
between
5.65
0.026 0.046 0.001 0.009
1.90
Overall,
3). The
3.74 2.84
0.72
supplemented
(Table
5.92 4.96 2.00 1.74
2.59
of LEHs/sample
and
One-tailed
1.50
31.7(13/41) 31.7 (13/41) 73.2 (30/41) 74.4 (29/39)
incisor
x2
2.14
(9/42)
central
RR
21.4
zones, (26).
(6/39) (5/42) (28/42) (25.39)
upper
26.8 (1 1/41)
(6/42)
in the control group with 33 hypoplastic
2.0-2.5
control
15.4 1 1.9 66.7 64.1
teeth,
14.3
in the supplemented group. The was found for the zone corresponding
around the
777
12.5 (5/40)
and mandibular
horizontal periods
zones was found tooth], compared
(1/38) (1/42) (14/42) (14/38)
are frequencies
incisors
nine 6-mo
Control
16.7(7/42) 20.0 (8/40) 40.0 (16/40) 39.5 (15/38)
in parentheses
t Maxillary
HYPOPLASIAS
on antimeres and combined for anterior maxillary and anterior mandibular and all anterior teeth in the supplemented and control groups* Supplemented
*
ENAMEL
frequency
(Table
was a slight
where
This
4). Confirming increase
5.7
(2/35)
males
significant
times
of defects for the
0.52
One-tailed
NS
3.82 0.45 0.10 0.06 2.33 6.15
0.026 NS NS NS 0.064 0.006
9.5
(4/42)
4.15
0.021
0.0
(0/42)
-
-
40.0 (14/35) 38.1 (16/42)
6.18 0.20
28.6
8.47
0.006 NS 0.002
(9/42)
man-
the frequency
groups* 2
and
the anthropometric
had over three
and supplemented
a higher (weight-
observations,
between
in prevalence
was
Control
22.5 (9/40) 14.3(6/42) 14.3 (6/42) 26.2(11/42) 31.0 (13/42) 23.8 (10/42)
unpublished of LEHs
difference
females
history found to have malnutrition
P
778
GOODMAN LEH
PERCENT
ET AL with
5.9%
for the control
in the
current
cantly
different vs 8.2%;
(17.7% this
mean
between
2.
t
difference
was
percentiles
is a slightly
but
not
Mean OEVELOPMENTM..
AGE
head
different
ao.as
2.0.2.5 (YEARS)
1.50 and 53.04 head circumferences cantly
greater
difference mented from
compared
Overall,
60%
symmetrical pared idence
LEH
CI
males =
on one
(30.0%
or more
P
vs 9.8%,
49. 1-70.9%)
of females
pairs
=
0.01
1).
displayed
of anterior
a
teeth,
corn-
pattern
or for
a gender
difference
in the
chronological
of defects.
Head
circumferences,
time
ofthe
heights,
dental
evaluation.
and
weights
were
Whereas
the
mean
evaluated
at
weight-for-age (based on NCHS reference values) (41) was significantly greater in the supplemented (37.8%) than the control
5). In fact, studied
when separately,
the supplemented one finds a slight
for-age with LEH (Table 5). At the time of the dental height-for-age
of the
supplement
the
group
was
mean
percentile
18.5%,
compared
in weight.
For
12
II Total maxilla Mandible Canine 12
Ii Total mandible CI combination Any combination *
Numbers
in parentheses
groups
However, LEH
to 54.05
the
3.33,
weight
P
that
first
5.4(2/37)
12.5(5/40)
are
gain
small,
the
cm for those
group
and
formation
4.8(2/42)
(10-25%)
ill with
gastrointestinal
of LEHs
ofthose
without
the
(20/42)
these
but
on antimeres teeth
control
results formation association that
insignificantly
devel-
(2.84
± 1.59
sample
suggest
alone,
an association
of LEHs. between
illness
individuals
with
x2
and
Two-tailed
1.15
NS NS
(18/47)
52.5 (21/40)
1.12
of days
maxillary
0.71 1
0. 1 9
NS
0.1
NS
1
30.0 (12/40)
3.06
5.17
16.7
(7/42)
19.0
1.14
0.80
NS
24.4 19.5 53.7 54. 1
(10/41) (8/41) (22/4 1) (20/37)
23.8 (10/42) 32.5 (13/40)
0.98 1.67
0.04 1.76
NS NS
60.0
1 . 12
0.33
NS
1. 1 1
0.27
NS
(8/42)
(24/40)
60.0 (24/40)
the had and
illnesses. For that developed
2.31 0.9
and
illness,
and gastrointestinal individuals with LEH
for anterior
be-
LEHs
frequency
upper-respiratory
0.50
46.8
Downloaded from https://academic.oup.com/ajcn/article-abstract/53/3/773/4731893 by Washington University, Law School Library user on 05 June 2018
also es-
LEHs
LEHs group
greater
illnesses,
and combined
RR
47.6
size.
was
velocity,
with
of sup-
nearly a 50% lower mean gain in this same time period when corn-
For
and ofthe
of upper-respiratory nonsupplemented
(22/42)
of LEHs/sample
without
7 in the
in growth
individuals
also suggests
a slight
52.4
are frequencies
mean
the suppleincreased
2 y of life on a subset
decreases
example,
0.003).
=
ofLEHs
the total example,
Females
9.8 (4/41)
(53.43
the mean was signifi-
5). This
(Table
control
1 2-24 mo had ± 0.33 kg) during
sizes
formation
Males
9.5(4/42)
suggests
tween growth faltering Finally, an analysis
TABLE 4 Comparison of the prevalence of LEHs in males and females, with defects matched anterior mandibular teeth, upper central incisor and lower canine, and all anterior
Maxilla Canine
the
(12.1%)
to be significantly
control
LEH
during 15 in the
simultaneous
sample
weight(Table
and control groups were increase in mean weight-
observation
total;
group)
with
found
for
LEHs
of variation within head circumference
LEHs
with
t =
height-for-age with
and
with
associated
kg;
not
without
plemented
pared
mean
vs those
was
those
on growth (22
around (1.48
without LEHs are However, there
the mean weight gains were 1 .48 kg with concurrent LEH and 2.56 kg without concurrent LEH (t = 1 .78; P = 0. 10 1). Although
percentile
group (22.3%), there was no difference in mean percentile for-age for those with (30.5%) and without (32.5%) LEHs
data
oping weight
and
greater
by
5).
individuals
pecially
with 54. 1% (95% CI = 43.0-65.2%) of the males. No cvwas found for an interaction between gender and sup-
plementation,
the
with
(95%
with
supplemented
cm for those
(Table
The of LEHs
group
mean
LEHs
of height-for-age
± 1 . 18 cm, respectively). of individuals without
than
signifi-
the without
5.7%, respectively).
is entirely a function group, where the mean
52.80
LEHs
percentiles
significantly
the
and
mean
circumference
±
FIG 1 . Comparison ofthe chronological distribution oflinear enamel hypoplasias (LEHs) on the maxillary central incisors ofindividuals who received nutritional supplementation and those who did not. Data are based on dividing the crown into nine half-year developmental zones by following the developmental chronology of Massler et al (36).
The
with
LEHs (22.7%) group.
between
also
of supplementation,
in the control (6.0% and
individuals without in the supplemented
Differences
were
without and with LEHs Table 5). To assess whether
for those
status.
0.001).
=
height-for-age
individuals 19, P = 0.034;
were compared
of individuals nearly identical
3.58; P
(t =
independent
supplementation
1.0.1.5
group
percentile
0.022
P
UNDERNUTRITION TABLE 5 Comparison total sample
of current
anthropometric
measurements
AND
for individuals
ENAMEL
with and without
LEH Percentile weight-for-age (%)t Total Control Supplemented Percentile height-for-age (%)t Total Control Supplemented Head circumference (cm) Total Control Supplemented
30.5 25.4 38.9 8.2 6.0 12.1 53.12± 53.30 52.80
LEHs
for the supplemented
No LEH
and control
and the
groups
t value
Two-tailed
±
24.9
[40]
32.5
± 23.6
[31]
±
23.0
[25]
17.0
±
18.4
[91
0.35 -0.98
NS NS
±
26.3
[15]
38.8
± 22.9
[22]
-0.01
NS
±
ll.9[41]
±
9.5
[26]
±
14.8
[15]
5.7
l.l3[41] 0.88 [26] 1.46 [15]
± ±
2.19
17.7 ±2l.9[31J ±
6.0
[9]
-0.
0.034
11
NS NS
1.52
22.7
± 24.1
[22]
53.77± 53.10 54.05
±
l.23[3l] 1.30 [9]
±
1.12
2.33 -0.43
0.023 NS
2.93
0.006
[22J
P
SD. n in brackets.
S
t On the basis of NCHS
around period
reference
30-36 mo averaged compared with 174.9
values
214.5 illness
(41).
illness d during this 6-mo d for those without a LEH.
As in previous found
on the
viduals had
Discussion reliability
Intraobserver
Previous
studies
in clinical
and field settings
results
in demonstrating
sistent
with
fact,
that
but
on casts
field
from to their
to severe
are the
most
observations
LEHs
similar
eye-do
not appear
is needed
to formulate
depression
to score
systemic this
of defects in further
defects. FDI standard
with
high
symmetrical suggesting
minimum
physiological
study
the
Variation
defects
less
easily
in prevalence
ofLEH
some
de-
for recognizing
a linear
The
(and caused
method
by
employed teeth
is one
defects.
by tooth
type
differences
in time
susceptibility incisors
that
are
strongest
other periods. enamel
formation
oftheir Therefore,
teeth
as well as to variation
teeth
(38). Teeth such in developmental
control
of development
polar
genetic
nonpolar
the timing
ofcrown
to disruption
(38);
these
development they
are
polar
teeth
during more
likely
in
as upper central fields are under compared
are least
physiologically to develop
able
with to vary stressful defective
(38).
Downloaded from https://academic.oup.com/ajcn/article-abstract/53/3/773/4731893 by Washington University, Law School Library user on 05 June 2018
42 were
of analysis of upper were so assessed
ofthe
Effect
these
data
The
risk
ofdcveloping
decrease
However,
takes
because
nutrients
might previous
be
LEH
ofdefects
toward
as less senof which
the importance
twice
as great
intake
individuals to the
showed
specific
that
nutrient
sug-
and the develto variations have
it is difficult
critical
in the
group.
supplementation
dietary
appears to be sensitive order of 1200 kJ/d.
most
on the
formation
nearly with
between
studies
and
of all
data from
significance Regardless
on LEH was
of nutrients,
Although
44
of an analysis
point
supplemented
of a variety
on
whereas
as it was in the supplemented
relationship
of LEH. LEH intake on the
anwith-
(1, 3, 38).
a LEH
group in prevalence
a clear
opment nutrient
further
incisors
a LEH
alone,
incisors. Conversely, of confirming data
supplementation
nonsupplemented
central
mdi-
studies designed to gain may be able to focus on
additional disruption.
type
was
two
to have
incisors
on the basis
data
by tooth
ofnutritional
Only
individuals
recognized
central
of upper central provide a means
are studied,
of reporting
between
Consistent with previous studies, substantial differences were observed in the frequency of LEH among the anterior teeth (1, 3, 38). Variation in frequency of defects among teeth is due to
differently,
incisors and may have assays of physiological
teeth
of defects
38).
set of contralateral
teeth. These data suggest that assessment of nutritional status
central sitive
in way
on another
2). Stated teeth,
frequency
LEH on the upper
LEHs
(Table
observation other teeth
gests
research
highest
(1, 3, 19, 26,
a symmetrical
missing
anterior a rapid
The
to the human
meaningful,
on contralateral
discerned
(32)
repeatability.
Because
any
the basis individuals
the the
nor associated that they are not
hypoplasia
perturbation).
of matching
to eliminate
criteria
a true enamel
In
most defects are less by FDI. These mild
to be physiologically
as being
con-
replicas.
potential
by systemic physiological disruption. in enamel thickness (a hypoplasia)-visible
caused creases
highly
frequency
to the
However, presented
Additionally, they may be neither with histological irregularities (3),
these
are
and
developmental
scored
extends
dental
greater
dental
difficult
be reliably
This study
quality
are easily discerned in the field. severe than the standard types
defects
could
high-quality
not significantly
attests
of quantitative
Moderate
LEHs
(26, 33-35).
observations
the slightly
observed studies
that
the
incisors
symmetrical
teeth
out
showed
studies,
central
without
such
terior
the
779
HYPOPLASIAS
in
greater
in-
to ascertain
which of a LEH.
formation there
are
deficiencies
associations
(1, 7), these
studies only suggest that a specific deficiency might be etiologically significant and cannot be used to determine ifthe specific deficiency is a sufficient cause or how common a cause it is in
humans. this
A review
ofthe
further
suggest
perhaps
similar
study
in cause, tional
status,
current
roles.
disease
Further
is clearly of and
with
both
states
literature that
combined
LEH
to anthropometric intake
ofa
with
required
to begin
interactions
among
of nutrients
playing
significant
experimental to tease these
out
factors.
with the results
animals the
of
to be multifactorial
measures
variety
potentially
research
is likely
relative
of nutriand
con-
etiological
and humans importance
780
GOODMAN
Developmental
The
ages
estimated
central
at
LEH
peak
incisor
with
a slightly
the
supplemented
earlier
of a LEH
mean
age
at formation
upper groups,
(2.03-2.17
y) in dif-
ference in developmental age may actual difference in chronological age because
the
be relatively nutritional
groups.
small mean be somewhat less than
delayed status
developmental
in the control (42). Whereas
group poor
individuals
nutritional
can significantly delay eruption times, less is known of its on the timing of matrix formation. It is, however, likely to be less significant, especially for a highly canalized tooth. The peak age at formation ofa LEH in both groups is similar status effect
to that
found
ofstudies
in another
study
ofprehistoric
also follows
closely
in Mexico
and historical
(26)
and
populations
after the median
in a number
(3). This peak
age at completion
the
It is as if all children
are at great
risk
but the supplemented
protection
before
and
of LEH
individuals
after
weaning.
with
compromised
Male-ftmale
nutritional
differences,
study,
slightly
in the
more
females results
Mexican
The
variation
periods
illness,
males and
to severe
in association
and past anthropometric ical
than (26)
moderate
also
support
and LEH
studies has shown that LEH is females and vice-versa (3). In this had
are consistent
highlands
females with pan (28).
data
and gastrointestinal illespecially in individuals
anthropometry.
1%). These
after
greater
status.
A variety of epidemiological more common in males than (60.0-54.
immediately
are afforded
These
the hypothesis that common respiratory nesses are an immediate cause of LEH,
the
or more
between
greater
LEH
catch-up
study
proportion
of
in Tezonteoand
is explicable
and
LEHs
a previous
undernutrition
measures
of development
one
with
both
in terms
potential
current
of crit-
of the
of children
to catch
up
in weight
growth.
with
LEH.
Finally,
2 and 3 y is associated
a decrease with
in weight
a concurrently
velocity
LEH,
although, as noted above, this relationship does not carry through to weight at the time of dental examination. This paradoxical relationship is likely due to the sensitivity of weight to physiological
disruption.
When
a stressor
is virulent
enough
to cause
a LEH, it may also lead to a decrease in weight gain. Both upper-respiratory and gastrointestinal illnesses were moderately associated with the development ofa LEH. The potential
importance
noted commonality ages at formation etiology
of LU-I
In summary, in a population
ofillness
is indirectly
suggested
by the above-
in peak ages at incidence ofillness and peak of LEH. However, the role of illness in the needs
to be further
the prevalence after
nutritional
explored.
of LEH
was shown
supplementation
to be reduced during
perturbations,
of nutritional
study
confirms
the
Downloaded from https://academic.oup.com/ajcn/article-abstract/53/3/773/4731893 by Washington University, Law School Library user on 05 June 2018
mild
to moderate
under-
Keith
LEH
may
prove
to be a unique
U
status.
Dobney,
Debra
Martin,
Homero
Martinez,
and
Lorena Chapparro for assistance in the collection of the dental data and Arlene Perry and Yin-Chai Cheah for data management. We especially wish to acknowledge the efforts of the people of Tezonteopan who have contributed so unfailingly to Proyecto Puebla.
References Cutress TW, Suckling GW. The assessment of non-carious defects ofenamel. Int Dent I 1982;32:l 17-22. 2. Kreshover SI. Metabolic disturbance in tooth formation. Ann NY AcadSci 1960;85:l61-7. 3. Goodman AH, Rose JC. The assessment of systemic physiological perturbations from developmental defects of enamel and histological structures. Yearbook of physical anthropology I 990;3:59I 10. 4. Sarnat BG, Schour I. Enamel hypoplasias (chronic enamel aplasia) in relationship to systemic diseases: a chronological, morphological and etiological classification. I Am Dent Assoc 194 l;28:l989-2000. 5. Suckling G. Developmental defects ofenamel-historical and present-day perspectives of their pathogenesis. Adv Dent Res 1989;3: 87-94. 6. Goodman AH, Armelagos GJ, Rose JC. The chronological distri1.
bution 7.
of enamel
hypoplasias
from prehistoric
Dickson
populations. Am I Phys Anthropol l984;65:259-66. Jontell M, Linde A. Nutritional aspects on tooth formation.
Rev Nutr Diet l986;48:l
between
developing
physiological
indicator
Conversely,
LEH developing earlier in life is associated with adolescent head circumference (Table 5). Because head circumference is rapidly increasing during the time ofenamel formation, one might expect that a permanent decrease in mean head circumference is associated
longitudinal
The peak age at formation ofenamel defects, -24-36 mo, is also the age at which weaning has been completed and illness reaches its greatest incidence. The web of potential interactions involving socioeconomic conditions, feeding patterns, dietary intake, and illness patterns suggests that all of these variables need to be examined in concert if one is to better understand the causal relationship between nutritional status and LEH. Because of enamel’s ability to provide a chronological record of
an-
thropometric measures. The fact that there is no association between LEH and current weight-for-age is likely due to the ability
This
status further support the view that nutrition is a main cause of LEH.
We thank
The greatest relative difference in frequency of LEH between supplemented and control groups occurs before I .5 y and after 3.0 y, or before and after weaning and the time ofgreatest illness. weaning,
development.
from previous studies that examined the relationship between current nutritional status and the previous formation of enamel defects. Associations between LEH and both growth yelocity at the time of defect formation and current nutritional
past
of weaning
(“-20-24 mo) in this community (28) and is congruent with age at which the incidence of illness is greatest (28, 30).
ofenamel
results
This
timing may with poorer
control
on the
age in both
mo developmental
vs the
AL
time
development
age at formation
is ---24-36
ET
Mounds World
14-36.
8. Jenkins GN. The physiology and biochemistry of the mouth. 2nd ed. Oxford, England: Blackwell, 1978. 9. Navia JM. Nutrition in dental development and disease. In: Winick M, ed. Nutrition pre and postnatal development. New York: Plenum, 1979:333-62.
10. Mellanby structure [Medical 1 1. Mellanby 12.
M. Diet and the teeth: an experimental study. Part I: dental in dogs. London: His Majesty’s Stationery Office, 1929. Research Council special report series no. 140.] H. The effect of maternal dietary deficiency of vitamin A
on dental tissues in rats. J Dent Res 194 1;20:489-509. Tonge CH, McCance R. Normal development ofthejaws
and teeth
in pigs, and the delay and malocclusion produced by calorie deficiencies.I Anat l973;l 15:1-22. I 3. Holloway P1, Shaw JH, Sweeney EA. Effects of various sucrose: casein ratios in purified diets on the teeth and supporting structures ofrats. Arch Oral Biol 1961:3:185-200. 14. Shaw JH, Griffith D. Dental abnormalities in rats attributable to protein deficiency during reproduction. J Nutr l963;80: 123-41. 1 5. Aponte-Merced L, Navia JM. Pre-eruptive protein-energy malnutrition and acid solubility of rat molar enamel surfaces. Arch Oral Biol l980;25:70l-5.
UNDERNUTRITION
AND
DiOrio LP, Miller SA, Navia JM. The separate effects of protein and calorie malnutrition on the development and growth ofrat bones and teeth. I Nutr l973;103:856-65. 17. Swardstedt T. Odontological aspects ofa medieval population from the province oflamtland/Mid-Sweden. Stockholm:Tiden Barnangen, AB, 1966. 18. Goodman AH, Lallo I, Armelagos GJ, Rose IC. Health changes at Dickson Mounds, Illinois(AD 950-1 300). In: Cohen MN, Armelagos GJ, eds. Paleopathology at the origins of agriculture. New York: Academic Press, 1984:271-306. 19. Goodman AH, Armelagos GI, Rose IC. Enamel hypoplasias as indicators ofstress in three prehistoric populations from Illinois. Hum Biol 1980;52:5 I 5-28. 20. Corruccini RS, Handler iS, Jacobi KP. Chronological distribution ofenamel hypoplasias and weaning in a Caribbean slave population. Hum Biol 1985;57:699-71 I. 21. Lanphear KM. Frequency and distribution of enamel hypoplasias in a historic skeletal sample. Am I Phys Anthropol l989;8l:35-43. 22. Blakey ML. Fetal and childhood health in late 18th and early 19th century Afro-Americans: enamel hypoplasias and hypocalcifications in the FABC skeletal population. Am J Phys Anthropol l987;72: I 79 (abstr). 23. Sweeney EA, Saffir IA, de Leon R. Linear enamel hypoplasias of deciduous incisor teeth in malnourished children. Am I Clin Nutr 16.
197 l;24:29-3
ENAMEL 29.
30.
31.
32.
33.
34.
35.
36.
1.
24. Sawyer DR. Nwoku AL. Malnutrition and the oral health of children in Ogbomosho, Nigeria. I Dent Child 1985;52:l4l-5. 25. Enwonwu CO. Influence of socio-economic conditions on dental development in Nigerian children. Arch Oral Biol l973;l8:95-107. 26. Goodman AH, Allen LH, Hernandez GP, et al. Prevalence and age at development of enamel hypoplasias in Mexican children. Am I Phys Anthropol 1987;72:7-19. 27. Goodman AH, Pelto GH, Allen LH. Socioeconomic and nutritional status correlates of enamel developmental defects in mild-to-moderately malnourished Mexican children. Am I Phys Anthropol 1988;75:215 (abstr). 28. Chavez A, Martinez C. Growing up in a developing community. Guatemala City: Institute ofNutrition ofCentral America and Panama, 1982.
Downloaded from https://academic.oup.com/ajcn/article-abstract/53/3/773/4731893 by Washington University, Law School Library user on 05 June 2018
37.
38.
39. 40. 41.
42.
HYPOPLASIAS
781
Chavez A, Martinez C, Bourges H. Nutrition and development of infants from poor rural areas 2. Nutrition level and physical activity. Nutr Rep Int l972;5:139-44. Martinez C, Chavez A. Nutrition and development ofchildren from poor rural areas VII. The effect of the nutritional status on the frequency and severity of infections. Nutr Rep mt 1979;l9:307-l4. Chavez A, Martinez C, Ophuis A et al. Nutrition and development of children from poor rural areas VI. Effects of mild malnutrition on body morphology during early growth. Nutr Rep Internat 1977; 15:407-19. Federation Dentaire International. An epidemiological iidex of developmental defects of dental enamel (DDE Index). mt Dent I 1982;32:l59-67. (FDI technical report 15.) King N. Developmental defects ofenamel in Chinese girls and boys in Hong Kong. Adv Dent Res 1989;3:l20-5. Murray II, Gordon PH, Carmichael CL. Dental caries and enamel opacities in 10-year-old children in Newcastle and Northumberland. Br Dent I l984;l56:255-8. Suckling GW, Pearce EF. Developmental defects of enamel in a group ofNew Zealand children: their prevalence and some associated etiological factors. Community Dent Oral Epidemiol l984;12:17784. Massler M, Schour I, Poncher HG. Developmental pattern of the child as reflected in the calcification pattern of the teeth. Am I Dis Child l941;62:33-67. SPSS Inc. SPSS-X user’s guide. Chicago: SPSS Inc. 1983. Goodman AH, Armelagos GI. Factors affecting the distribution of enamel hypoplasias within the human permanent dentition. Am I Phys Anthropol 1985;68:479-93. Fleiss I. Statistical methods for rates and proportions, 2nd ed. New York: John Wiley and Sons, 1981. Landis R, Koch G. The measurement of observer agreement for categorical data. Biometrics l977;33:l59-74. Hamill PV, Drizd TA, Johnson CL, et al. NCHS growth curves for children, birth-18 years, United States. Vital Health Stat [I 1] 1977; 165. Alvarez JO, Navia JM. Nutritional status, tooth eruption, and dental caries: a review. Am I Clin Nutr 1989;49:417-26.