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

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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.

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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.

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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

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and teeth

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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.

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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.

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37.

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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.

Nutritional supplementation and the development of linear enamel hypoplasias in children from Tezonteopan, Mexico.

The purpose of this study was to compare the effect of nutritional intake during tooth-crown formation on the subsequent development of linear enamel ...
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