THE MULTINATIONAL ANDEAN GENETIC AND
HEALTH PROGRAM: III. OPHTHALMIC DISEASE
AND DISABILITY AMONG THE AYMARA’p *, 3
Robert I. Goldsmith,* Francisco Rothhammer, and William J. Schul16
Direct ophthalmoscopy and slit lamp microscopy performed on 706 residents of the coastal, sierran, and Andean highland zones of Chile’s Department of Arica failed to disclose unusual
disorders of the eye or its adnexa attributable to the subjects’ biological origins. Most of the pathology that was encountered could be attributed to the dust, persistent wind, low humidity,
and other conditions that characterize the interior.
Introduction
Individuals unaccustomed to altitude
can and frequently do experience a kind of
psycho-physiological effect upon prolonged
exposure to the hypoxia which prevails at
high elevations. If oxygen deprivation is
sufficiently profound, memory falters, the
central visual field is impaired, and the
individual may be appreciably and perma-
nently handicapped (I, 2, 3). Ocular ac-
commodation, convergence, and stereo-
acuity are all reported to have been mea-
surably degraded at altitudes as low as
4,500 meters (4). Still more subtle visual
1Also appearing in Spanish in the Roletin de la Ofi- cina Sanitaria Panamericana, 1979.
*Part 1 of this series, entitled A Study of Adapta- tion to the Hypoxia of Altitude is contained in Physzologicat Varzation and its Genetic Basis Vol. 17. Society for the Study of Human Biology, Taylor and Francis Ltd., London, 1977, pp. 139-169. Part II, entitled Disease and Disability among the Aymara, appeared in the preceding issue of this journal, Rull Pun Am Health Organ lZ(3): 219-235, 1978.
3The authors gratefully acknowledge the support of the National Heart and Lung Institute through grant HL-15614.
4Unniversity of Michigan, Department of Ophthal- mology, Room 216, Michigan Theater Bld., Ann Arbor; Michigan 48109. -
5Universitv of Chile, Sede Norte, Faculty of Medi- cine, Department of Cellular Biology and Genetics, Casilla 6556, Santiago 7, Chile.
6University of Texas Health Science Center, Center for Demographic and Population Genetics, P.O. Box 20334, Houston, Texas 77025.
effects also occur; the sensitivity of color
perception, for example, decreases progres-
sively and systematically as hypoxia be-
comes more severe and extends over longer
periods (5). Engorgement, with tortuosity,
of the retinal vessels; an increase in venous
and arterial diameters; and retinal hemor-
rhages are frequently observed in moun-
tain climbers at altitudes as low as 3,600
meters (6-8), and a familial proclivity to
their development may exist (9).
These risks and the discomfiture expe-
rienced by lowland visitors notwithstand-
ing, more than 10 million individuals now
live in the Andes at altitudes of 3,000
meters or more. In fact, Andean men and
women are generally presumed to have
adapted effectively to the lessened oxygen
as well as to the rigors of temperature and
humidity that accompany life at the alti-
tudes where they reside (10-12). None-
theless, oxygen deprivation, extremely low
humidity for most of the year, persistent
wind, and high levels of ultraviolet radia-
tion at these elevations can all be viewed as
inimical to ophthalmic health.
Some of the adjustments associated with
Andean peoples that promote oxygen trans-
port and utilization may also have delete-
rious long-run ophthalmic consequences.
Thus, for example, polycythemia can lead
to retinal cyanosis; it can also lead to reti-
nal hemorrhages and papilledema that re-
,,’ I’
Goldsmith et al.
. OPHTHALMIC DISEASE AMONG THE AYMARA 59portedly have been so gross on occasion as
to result in blindness (13). Furthermore,
brain tissue is known to be more sensitive
to oxygen deprivation than any other tis-
sue; and since the eye is developmentally
and histologically an extension of the
brain, more profound eye tissue damage
might be expected at low oxygen levels
than would characteristically occur in
other tissues.
On the other hand, we are aware of few
studies of a systematic, community-wide
nature that provide a clear perspective on
chronic as well as acute ophthalmic disease
or disability among Andean peoples. Buck
and his colleagues (14) have reported on
the frequency of eye diseases and conditions
encountered in epidemiologic studies of
four Peruvian villages, one of which, Pusi,
is in the
altiplano.
Some 240 inhabitants ofthis village, all presumably of Quechua
origin, were studied. All of the findings
recorded involved the cornea, conjunctiva,
or lids-which suggests that ophthalmos-
copy was not done. The largest differences
among the four villages were observed with
regard to conjunctivitis and pterygium; in
both instances data from the altiplano
village were intermediate in value. A kera-
toconjunctival lesion allegedly restricted to
individuals indigenous to high altitudes in
Bolivia, said to resemble limbal vernal
catarrh has been described (1.5). We failed
to see this lesion at equally high altitudes
in Chile. Rennie and Morrissey (7) observed
no retinal hemorrhages in a limited number
of Sherpa at altitudes where one out of three
of their American coclimbers were affected,
and we likewise failed to find this phenome-
non increased among the Aymara of the
Chilean altiplano.
Methods
The study reported here was carried out
in northern Chile in the villages and towns
of the Department of Arica, which is
divisible into three sharply distinct ecologic
niches-the costa (sea level to a few hundred
meters), the sierra (generally 3,000-3,500
meters), and the
altiplano
(above 4,000meters). Each of these differs from the
others in terms of oxygen tension, tempera-
ture, and humidity; and associated with
these physical parameters are biotic con-
straints that impose different biologic
burdens and limit lifestyles (for a fuller
description see references I6 and 27).
In 1972 an investigation called the Multi-
national Andean Genetic and Health
Program was initiated in the Department to
appraise the impact of these parameters
upon disease and disability among the
Aymara, the indigenous people of the inte-
rior. Part of this investigation consisted of
ophthalmic examinations that tested visual
acuity, color vision, and tenometry, and
that also included slit lamp microscopy, an
external examination, and an ophthalmos-
topic examination. The slit lamp microsco-
py was carried out with a Marco (Model
MT-304~JSM) slit lamp and the ophthal-
moscopic examination was conducted with a
conventional Welch-Allyn ophthalmoscope.
Color vision tests were performed with A0
H-R-R pseudoisochromatic plates. Visual
acuity was determined with a Snellen Illite-
rate “E” Chart at ‘20 feet, each eye tested
separately.
After the color vision and visual acuity
examinations had been conducted, two
drops of 1 per cent mydracil were instilled
into the conjunctival sacs 20 to 25 minutes
before fundoscopy, save where medically
contraindicated, to enhance visualization of
the posterior chamber, fundus, and retina.
It was observed that dilation occurred less
frequently than it normally does among
non-Indian populations. Indeed, dilation
failed to occur in some 21 (8.8%) of 238
Aymara, in 17 (5.8%) of 292 Mestizos, and
in 4 (2.8%) of 143 non-Aymara. For a varie-
ty of reasons, no effort was made to dilate
the pupils of 33 individuals (11 Aymara, 19
mestizo, and 3 non-Aymara) who were
60
PAHO BULLETIN
l vol.13. no. 1. 1979
A good view of the fundus
is generally
ob-
tained
10 to 15 minutes
after instillation,
and at 20 minutes the average pupil diame-
ter is about 7.5 mm; little change in pupil-
lary diameter occurs in the succeeding hour
or two (18).
Elsewhere we have argued that examina-
tions at the various villages within
each eco-
logical
niche
were sufficiently
encompas-
sing (participation
averaged
over 70 per
cent of the eligible
individu,als)
so that sys-
tematic
biases in our
evaluation
of the
prevalence
of disease and disability
were
unlikely
(17). We accept, of course,
that
those disorders
(e.g., blindness)
incompati-
tified
by the American
Board of Ophthal-
mology. The former examination
was given
706 were examined
ophthalmologically.
each time a physical examination
occurred;
the latter,
the results of which
we report
here, involved
slightly
more than a third of
the 2,096 persons who were examined
in the
basic study. The individuals
who had this
more detailed ophthalmologic
examination
were all residents
of three
communities:
Lluta in the costa, Putre in the sierra, and
Visviri
in the
altiplano.
Each community
is
typical
of the ecologic
niche
to which
it
belongs;
among the 975 residents
of these
communities
(some 70 per cent of the com-
munities)
who were seen in the basic study,
ble with sufficient
mobility
to participate
in j
the examinations
described
create a bias,
insofar
as such
disorders
are
altitude-
dependent .
Tables
1 and 2 provide
data on the
ophthalmic
disorders seen in the adults and
children
examined
in the course of this
study. (For purposes of the study, children
were arbitrarily
defined
as individuals
less
than 15 years of age at the time of examina-
tion.) These findings
are grouped according
to each subject’s
ethnic
background
and
area of residence
(Costa, sierra,
or
altipla-
no).
For convenience,
the discussion
that
follows aggregates these findings
into those
affecting
(1) the globe and its adnexa;
(2)
the
cornea,
conjunctiva,
choroid,
and
sclera; (3) the anterior
chamber,
lens, and
uveal tract;
and (4) the retina
and optic
nerve. Normality
in this context implies no
Another
matter
basic to the study -the
algorithms
by which
each individual
was
designated,
first, to be Aymara,
Mestizo, or
non-Aymara,
and, second, to be a resident
of the
costa, sierra,
or
altifilano -
have been
extensively
described elsewhere
(17, 19).
Diagnosis of Disease and Disability
Two ophthalmic
examinations
were car-
ried out-one
by the physician
who per-
formed
the general
physical
examination
and the second by an ophthalmologist
cer-
Goldsmith et al.
l OPHTHALMIC DISEASE AMONG THE AYMARA61
Table 1. Distribution of ophthalmic disease and disability among children” by sex, ethnicity, itnd ecological niche.
Dngnosis
Costa Sierra Altiplano
NIXI- NW- Non- Total
Aymara Mestw Aymara Aymara Mestlzo Aymara Aymara Mesttzo Aymara
- - - - ---
Mb Fe M F M F M F M F M F M F M F M F
Globes and odnexa:
Blepharitis Cyst, meibomian Exotropia Hypertelorism
Lacrimal dramage system, inflammatton of
Corntw. conjunctiva. cloroid. and sclera:
Conjunctiva, hyperemla of Conjunctivitis
Melanoma, conjunctiva Opaaty, cornea1 Pseudopterygium Subconjunctival hemorrhage,
secondary to trauma
Anterior chamber. lens. and uveal met:
Cataract, unspecified Cyst, iris Opacity, vitreous Refractive error Uveltis
Retinn and optic nerve
Retina, cicatrot Retina, pigmentary deposits
Other c&m
Other anomalies: ‘Normal” eye exarmnations Total number of children
examined
1
- -
- -
2 - I - 3 1
- -
-
6
- - -
- I -
I
I
7 10
16 I6 26 30
-
2
1
I - 1
I 6 10
1 - 1 2 - - - - l---
l - - -
2 3 - IO 8 3 1 3 6 2 - - - - 1 - - - 1
l--2--11 I---
- - - - - I---
- - I 25 - 14 2
a 2 II II - 1 5 3 6 12 9 2018 5 6 26 20 9 22 I2 38 40 7 a 35 28
- - I
4 -
- - 2
-
2 7 12
I - -
1 - - - - - 1 - - - -
- - - - - - 3 1 -
- - - - - - I - - 8 - - 13 1 -
$2 2 3 6 I 1
1 1 1 24 1
64 I76 295 aSubjects less than 15 years of age.
bM = males. CF = females.
loss of function; that is, nothing was seen saw no clinical evidence of avitaminoses des-
that would limit ocular activity. No biopsies pite local government concern, particularly
were performed; clinically, the benign with respect to vitamin A deficiency; nor
neoplasms reported appeared to be papillo- did we see evidence of ocular changes sec-
mata. ondary to cardiovascular anomalies such as
patent ductus arteriosus that are known to
Disorders
ofthe Globe and Its
Adnexa be more common at higher altitudes.Surprisingly few instances of strabismus
Disorders
ofthe Conjunctiva,
Cornea,
or blindness were seen; and aside from epi-
Choroid, and Sclera
canthus, whi;h is to be expected in the
Aymara, few congenital anomalies affecting The most frequent disorders seen-ac-
the adnexa were noted. Indeed, much of the tinic and keratoconjunctivitis, pterygium,
pathology involving the globes as a whole or and cornea1 scarring-can all be ascribed
PAHO BULLETIN l
vol. 13, no. 1, 1979
Table 2. Distribution of ophthalmic disease and disability among adult+ by sex. etbnicity. and ecological niche.
Diagnosis
Costa Sierra Alt~plana
NO”- NO”. NO”.
Aymara MeStlZO Aymara Aymara Mestizo Aymara Aymara M&W0 Aymara Total
- - - __
Mb Fe M F M F M F M F M F M F M F M F
Globes and ndnexa:
Bum, eye Cyst, meibomian Exotrqxa
Lacrimal drainage system, mflammaton of Melanoma, bemgn, eyelids Neoplasm,benign, eyehds Ptosls
StI.?biS”W
Blindness. one eye Conjunctiva, hyperenua of Conjunctivitis
Embryotoxon Eye inflammation
(eplscleritls) Keratltls Melanoma, bemgn,
cqunctiva Nevi, charoid New. conjunctiva New. pigmented opacay. corncal Pteryglum Trachoma
Anterior chombcr. lens and uvcal tract
Blindness, one eye, CamaCt, traumatic Cataract, congenital Cataract, senile Caiarac1, traumat,C Cataract, other Lens, exfoliation of
CapSUle
Refractive errors Uveal tract, scar Uveitls
Retina and optic nerve’
Amblyopia Blindness, both eyes,
Retinopathy, artermsclerot~ primary optic atrophy Macula. dwneratmn of Optic I&, structural
Retmopathy, diabetic variants Retma, cicatrix
Retinopathy, hypertensive Retma,vascular changes of
Ved. glial
Other anomalies
Waardenburg syndrome Other specified anomalies
of the eyes
Other data:
“Normal” eye examinations
Total number of adults examined
I--- 2---,-,] l-,-*3---- I---,---
l--II--- I-l----m---
----I 1 --I ----~~___ l--- l---
I--- l---m---
122331234-l43--II
I--- l---3--- 11-l---2---
3 3 IO 5 II I2 5 7 9 I2 3 4 I6 I2 3 2 3 I 1-1--11~1---
l---l--- l--l---
~ - --- --I -- - - -__
I-13.2l32--221--- 2211-l----12----
---,2--- -~---__
----I---
l--- 11-1--1--1----
1 2 - I - - - - I - I - I - ---I---I---
- - ---I --- -__
l---
s 4 26 20 IO 8 7 I2 I2 I3 23 6 I6 I4 2 5 2 -
II 7 44 33 29 26 23 26 29 30 37 II 46 35 9 7 7 I I I2 2 3
I 109 I4 8 I 3 2
I I 31 I 4 5 121 5 2 2 I IO 3 I 5 I8 I 7 2 I I
I87 411 aSubjects IS years of age or older.
Goldsmith et al.
l OPHTHALMIC DISEASE AMONG THE AYMARA 63radiation, the dust and persistent wind to
which we have previously called attention,
or to neglect. No professional medical atten-
tion was consistently available in the sierra
and alti@lano villages studied. Four villages
were served by a firacticante, a member of
the Chilean police force (Curabineros) with
paramedical training. Little of this train-
ing, however, appeared to be directed at
alleviation of eye injuries, although clearly
some skill in the use of pressure dressing and
simple ophthalmic medications would be
helpful.
Conjunctival and cornea1 pigmentation
were common; in fact, the latter was re-
corded in 123 (49.4%) of 249 Aymara, 121
(38.9%) of 311 Mestizos, and 11 (7..5%) of
146 non-Aymara. Conjunctival hyperemia
was also frequent, but no significant dif-
ferences were observed in its distribution
among the three ethnic groups. (Hyperemia
was found in 58 of 249 Aymara, 67 of 311
Mestizos, and 36 of 146 non-Aymara-that
is, in 23.3%, 21.5%, and 24.7y0 of the re-
spective subjects). Increased cornea1 (or con-
junctival) pigment would not seem to
diminish the risk of conjunctival hypere-
mia. Only one case of trachoma was encoun-
tered, and it was of long standing.
Disorders
ofthe Anterior Chamber, Lens,
and Uveal Tract
Here two diagnoses prevailed, namely,
exfoliation of the lens and refractive errors.
The former was variously reported among
3.5 to 8% of the subjects, rates higher than
the rates usually thought to prevail in most
populations (20). In general, exfoliation of
the lens is most often seen in the 60 to 80
year age group, although it has been de-
scribed as occurring earlier. In our study all
of the cases seen occurred among subjects in
the customary group (ranging from 54 to 79
years of age).
Many of the refractive errors were pres-
byopic in nature; few people were encoun-
tered who regularly used glasses, though the
number who had conspicuous errors of re-
fraction but did not wear glasses was not
notably high. Tonometry was routinely
performed on subjects in the older age
groups, or where otherwise indicated.
Among 158 adults almost equally distrib-
uted among the three ethnic groups, not a
single case of elevated intraocular pressure
was seen.
Minor opacities of the lens were not con-
sidered cataracts; the latter term was used
only to describe an opacity of the lens that
decreased vision. Examination of the lens
was always performed after dilation.
Disorders
ofthe Retina
andOptic Nerve
Andean men and women are commonly
reputed (a) to have lower systolic and diasto- lic blood pressures than most non-Andean
populations, (b) to have blood pressures that
fail to exhibit the usual age-dependence,
and (c) to be free, or virtually free, of car-
diovascular disease. Elsewhere we present
data that support the belief that the blood
pressures of Andean peoples are generally
lower, but that fail to support a belief in
either the absence of hypertension or the
independence of blood pressure and age
(19). Pressures exceeding 160 mm of
mercury (systolic) and/or 95 mm (diastolic)
were encountered in all three ethnic
groups, albeit more commonly in the non-
Aymara than in either the Mestizos or the
Aymar a.
As indicated in Table 2, hypertensive
retinopathy was seen on no less than seven
occasions; these involved all three ethnic
groups, as well as individuals residing in
all three ecological niches. Of the 38 indi-
viduals examined ophthalmologically who
were judged to have hypertension solely on
the basis of blood pressure, eight were
found to have retinal changes, either of an
arteriosclerotic (two) or hypertensive (six)
nature. One person whose blood pressure at
the time of examination was 120/86 exhib-
64 PAHO BULLETIN .
vol. 13, no. 1, 1979
changes of the retina; he claimed not to be
on medications at the time, but he was a
user of coca. Among the 25 subjects with
retinal changes characteristic of circulato-
ry disease, 10 were Aymara, 9 were Mesti-
zos, and 7 were non-Aymara. The age
ranges at diagnosis were similar, namely,
40-71 years among the Aymara, 43-67
among the Mestizos, and 48-78 among the
non-Aymara. From these data we can
adduce no evidence of difference among
the three ethnic groups, regarding either
the frequency of these retinopathies or
their apparent distribution in different age
groups. Clearly, cardiovascular disease does
occur among the indigenous peoples of the
interior of the Department of Arica, even
at higher altitudes where these peoples had
been thought free of such disorders.
Only one case of diabetic retinopathy was
seen-in a somewhat obese (144 lbs, 64
inches) 36-year-old non-Aymara male who
resided in Arica’s coastal zone.
As previously stated, we saw no evidence
of an increased frequency of retinal hemor-
rhage among the Aymara of the
altiplano,
nor could we find evidence of retinal
changes secondary to the polycythemia of
altitude. To examine the latter issue, a care-
ful study was made of the ophthalmic find-
ings on 20 individuals with hemoglobins in
excessof 19.5 gm at the time of their exami-
nation and hematocrits of 50’$‘& or higher.
Approximately two-thirds of these hemato-
crits were in the 50-59% range, the remain- ing third being in the SO-69% range. None
of these subjects had retinal changes worthy
of comment, such as increased tortuosity or
vascular engorgement.
Other Disorders
One of the 706 people examined, an
Aymara female 15 years of age, exhibited a
well-defined inherited syndrome, that of
Waardenburg. Both of her parents were
examined, as were four of her siblings; all
of these individuals were normal. The
proposita’s hetiring was impaired bilaterally
and was especially poor at the lower fre-
quencies (500-1000 Hz).
ACKNOWLEDGMENTS
Studiesof this magnitude and complexity,
carried out under circumstances very alien
to most of those involved, clearly owe
whatever measure of success they achieve to
many individuals. This investigation was
no exception. We are indebted to numerous
people and many local and national institu-
tions in Chile, but we are especially be-
holden to the
Junta de Adelanto
of Aricaand its then president, Luis Beretta. With-
out the unqualified endorsement of this
body, as well as the enthusiastic support of
all members of the Departamento de Desa-
rrollo Comunal y Plan Andino-particular-
ly that of its chief, Carlos Solari -this study
would not have been possible. We also owe
much to the National Health Service of
Chile, the
@acticantes
of the Chilean Cara-bineros, and numerous teachers who gave
selflessly of their time and energies to make
our examinations a success. We are also
indebted to Dr. Merry Makela, Sara
Barton, Richard Allen, Susan Seybold, and
Paula Carlock, without whose help the data
presented would not be available for analy-
sis. Finally, we wish to express our gratitude
to the numerous Arica residents who in
patience and good humor tolerated our
Goldsmith et al. . OPHTHALMIC DISEASE AMONG THE AYMAR.4
65
SUMMARY
Direct ophthalmoscopy and slit lamp micros- ultraviolet radiation which characterizes much copy performed on 706 Aymara, Mestizo, and of this area of Chile, particularly the altiplano. non-Aymara residents of Chile’s Department of Retinal changes pathognomonic of arterioscle- Arica failed to disclose unusual disorders of the rosis and hypertension were seen in all three eye or its adnexa attributable to the subjects’ ethnic groups and in all three ecologic niches, biological origins. Much of the pathology that despite the reputed absence of cardiovascular was encountered could be logically ascribed to disease among indigenous Andean peoples. the dust, persistent wind, low humidity, and
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