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Familial aggregation of blood pressure and anthropometric variables in patrilocal households.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 79305-311 (1989)
Familial Aggregation of Blood Pressure and Anthropometric
Variables in Patrilocal Households
P.J. BYARD, B.N. MUKHERJEE, S.K. BHATTACHARYA,
J.M. RUSSELL, AND D.C. RAO
Departments of Pediatrics and Epidemiology and Biostatistics, Case
Western Reserve University, Cleweland, Ohio 44106 (P.J.B.);Anthropometry
& Human Genetics Unit, Indian Statistical Institute, Calcutta-35,India
(B.N.M.,S.K.B.);Division of Biostatistics (J.M.R.,D.C.R.),and Departments
of Psychiatry and Genetics (0.C.R.), Washington University School of
Medicine, St. Louis, Missouri 63110
KEY WORDS
folds
Anthropometrics, Familial correlations, India, Skin-
ABSTRACT
Fifty-three households in a small Indian fishing community
were surveyed for blood pressure, pulse rate, and anthropometric measurements
(height, weight, and three skinfolds). I n addition to nuclear family relationships, correlations for extended family members and in-laws living within a
common household were estimated by maximum likelihood. Based on likelihood ratio tests, the hypothesis that correlations among genetically unrelated
pairs from the same household are zero is rejected for systolic blood pressure.
Among genetically related individuals, the degree of relationship does not
affect the magnitude of the blood pressure correlations. For the anthropometric
measurements, family resemblance is significant only for first-degree relatives,
except that the correlation for uncle-child pairs is significant for subscapular
skinfold, and brother-in-law-sister-in-lawpairs resemble each other for height
and weight. The results suggest that common household environment is a
significant determinant of blood pressure but not fatness in this population.
Although familial aggregation of hypertension and obesity is well established in
western populations (Acheson and Fowler,
1967; Annest et al., 1979; Biron et al., 1976;
Hartz et al., 1977; Havlik et al., 1979;Johnson
et al., 1965; Miall and Oldham, 1963), the
effect of household environment on normal
variation in blood pressure and fatness levels
has not been demonstrated systematically.
In western populations, nuclear families living in a single household share both genes
and environment, and with the exception of
spouse pairs, twins, or adoptions, there are no
family relationships which allow examination of the role of household environment
independently of shared genes. I n cultures
which promote alternative types of household compositions, it is possible to study the
effects of shared household environment on
several types of genetically unrelated individuals. Here we describe one such arrangement found in patrilocal societies, where
@ 1989 ALAN R. LISS, INC.
wives take up residence with their husbands
and their extended families.
MATERIALS AND METHODS
Population
Data were collected in a small fishing
community located in the state of West Bengal, India, about 180 km southwest of Calcutta. The respondents comprise a nearly
complete sampling of household inhabitants
old enough to participate (generally, above 6
years of age). A total of 413 people in 53
households were measured for blood pressure, pulse rate, height, weight, and three
skinfolds (biceps, triceps, and subscapular).
Details of measurement technique have been
reported previously (Mukherjee et al., 1988).
Figure 1presents a typical household structure found in this group. The core of the
Received March 21, 1988; revision accepted September 22, 1988.
306
P.J. BYARD ET AL.
Fig. 1. Pedigree showing typical household composition. Males are shown as squares, females as circles. This
pedigree shows two brothers and their wives in the middle
generation, their mother and deceased father in the top
generation, and their unmarried sons and daughters in
the bottom generation.
household consists of a group of brothers,
their mother, more rarely their father, their
wives, sons, and unmarried daughters. The
greater representation of females in the older
generation is due either to greater longevity
in women or to age disparity among spouses
at marriage (wives were much younger than
their husbands, especially in earlier times).
Since most women marry and join the households of their husbands, the adult women in
a household are more often related to other
household members by marriage, not by
blood.
Familial correlations
Although many different types of relationships are found in these households, we
limited analysis to relationships with significant representation. Thus, ten familial correlations were estimated for each variable:
marital, parent-child, sibling, grandparentchild, cognate uncle-nephewhiece (genetically related), affinal aunt-nephewhiece (related by marriage), first cousins, parent in
law-daughter in law, brother in law-sister in
law, and wives of brothers.
Before estimating familial correlations,
measurements were adjusted for age and sex
(Mukherjee et al., 1988). This was done with
stepwise multiple regression of each variable
on age, age2, and age3 within each of four
groups: adult males (220 years), adult females
(220 years), young males (<20), and young
females (<20). The standardized residuals
were then normalized by assigning Blom
scores (Blom, 1958). Normalization was done
separately within each age-sex group to approximate a univariate normal distribution.
After age adjustment in this way, there is no
residual correlation between any of the anthropometric or blood pressure variables and age
(r ranges from -0.006 to 0.006, P > 0.8).
Correlations among household members
were estimated by maximum likelihood, using
a general purpose algorithm called MLECOR
(Rao et al., 1987) that, in turn, uses the
numerical optimization subroutine GEMINI
(Lalouel, 1979).A FORTRAN program called
PEDCOR was used to input pedigree structure. The PEDCOR program accepts any
arbitrary matrix of familial or other relationships, thus allowing estimation of correlations for any type of genetic or non-genetic
relationship.
Hypothesis testing
For each variable, we first estimated all 10
correlations listed above, calling this the
“general” model. In subsequent runs, we set
certain correlations equal to each other or
fixed them at zero in order to test hypotheses
about household resemblance. Statistical significance was evaluated by likelihood ratio
criterion. The log-likelihood value obtained
under the reduced model is subtracted from
the value obtained under the general model,
and doubled to yield a x2 statistic. The test
statistic has been shown to be distributed
asymptotically as a x2 with 10-k degrees of
freedom (df), where k is the number of correlations being estimated in the reduced set
(McGue et al., 1984).
Several simple hypotheses about the effects
of household environment can be tested in
this way. If common household environment
is the primary determinant of resemblance,
then we would expect all members of the
household to be similar, and all 10 correlations could be set equal. Thus, we estimate a
single correlation coefficient for all relationships, and test the hypothesis using a x2 with
10 - 1 = 9 df. Rejection of this hypothesis
need not, however, implicate a genetic effect,
since the household environment may have
different effects on different classes of relatives.
As a further test of the hypothesis of no
genetic effect, we set all the first-, second-,
and third-degree genetic relationships equal,
BLOOD PRESSURE AND ANTHROPOMETRICS
307
giving rise to a single parameter, all the nongenetic relationships equal to a second parameter, and the marital correlation to a third
parameter, and tested the fit of this model
against that obtained with the general model.
This hypothesis is tested using a x2 with 10 3 = 7 df.
Finally, if the genetic effect is the only
determinant of family resemblance, we could
fit a model in which all the nongenetic correlations (except marital, which may be affected by phenotypic assortment as well a s
by common household environment) are fixed
a t zero. This is tested using a x2 with 10 - 6 =
4 df. It should be pointed out that this is not a
specific test for no household environmental
effect, as the genetic relationships also share
such effects. While rejection of this hypothesis implies significant household environmental effect, failure to reject should not be
interpreted as a demonstration of genetic
effect.
Although a number of more complex models could be tested with this method, they
would be unlikely to yield much more information than could be obtained through examination of the familial correlations and their
standard errors (Table 1). Some testing of
specific hypothesis, however, guards against
the problem of multiple comparisons when a
large number of familial correlations is presented.
RESULTS
As shown in Figure 2, this sample is considerably leaner and has lower median systolic blood pressure than NCHS standards
for white Americans. In addition, fatness and
blood pressure levels are less variable in this
sample than in western groups, and the effect
of fatness level on blood pressure is minimal
(Mukherjee et al., 1988).
Estimates of correlations among household members, with their standard errors
and estimated sample sizes, are presented in
Table 1. Using twice the standard error as
the 95%confidence limit, marital correlations
are significantly different from zero only for
height and diastolic blood pressure. Correlations for first-degree relatives (parent-child
and sibling pairs) are significant for all variables. The grandparent-child correlations are
significant only for diastolic blood pressure.
Cognate uncle-child correlations are significant for subscapular skinfold and both blood
pressure measurements, whereas cousins are
significantly correlated for the blood pressure
variables only.
$- 1
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P.J. BYARL) ET AL
308
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Fig. 2. Median values of triceps skinfold and systolic
blood pressure compared to NCHS standards.
Among the nongenetic in-law relationships,
there are few significant correlations. None
of the affine aunt-child and or parent-in-lawdaughter-in-lawcorrelations is significantly
different from zero. Brother-in-law-sister-inlaw pairs are significantly correlated for
height and weight, with borderline statistical significance. Wives of brothers have a
significant correlation coefficient for diastolic
blood pressure only.
Table 2 presents the results of likelihood
ratio tests for the reduced hypotheses. The
hypothesis that all ten household correlations are equal (hypothesis 1, the household
environment model) is rejected for every variable except diastolic blood pressure. A model
allowing one correlation for all genetically
related individuals, one for spouse pairs, and
a third for all genetically unrelated pairs
(hypothesis 2, the three-correlation model) is
rejected for height, weight, biceps, and triceps
skinfold, for which genetic effects are there-
fore implicated, but not for subscapular skinfold or blood pressure, for which household
environment appears to be the major determinant. The hypothesis that all the nongenetic correlations (except marital) are zero
TABLE 2.
,yz values for likelihood ratio tests of
hypothesis'
Hypothesis Nos.
Variable
Height
Weight
Biceps skinfold
Triceps skinfold
Subscapular skinfold
Systolic blood pressure
Diastolic blood pressure
1
2
3
26.17*
26.31*
23.50*
29.16'
25.01*
27.35*
13.66
23.22*
17.44'
25.11*
14.51*
9.78
12.03
4.33
6.24
6.73
1.85
7.56
6.00
10.47*
3.52
'No. 1: Household environment only (a11 ten Correlations equal).
No. 2. Different household environment effects (three correlations:
marital, genetic, and nongenetic). No. 3 Genetic effect only
(nongenetic correlationsfixed at zero).
* P C 0.05.
RL001) PRESSURE AND ANTHROPOMETRICS
(hypothesis 3, the genetic model) is rejected
only for systolic blood pressure.
DISCUSSION
In this population, shared household environment appears to play a major role in family resemblance for systolic and diastolic
blood pressure. This is reflected in the likelihood ratio tests, in that the household environment model (1) cannot be rejected for
diastolic blood pressure, and the genetic
model (3) can be rejected for systolic blood
pressure. There is some suggestion of a
household effect for subscapular skinfold, in
that the three-correlation model (2), with all
genetic relationships constrained to have
equal correlations, cannot be rejected for that
variable. This results primarily from the fact
that resemblance for cognate uncle-child
pairs (r = .29) is as high as the resemblance
for first-degree relatives. However, caution
must be used when interpreting such results,
because failure to reject a hypothesis may, in
part, be due to lack of sufficient power. This is
especially true when sample size is small.
Nonetheless, the effect of household environment on body build has been documented
for several western samples of parents and
their adopted children (Garn et al., 1979;
Hartz et al., 1977), and it may be that differences between the results for subscapular
skinfold and the other indicators of body
composition in this sample occur because
there is too little variation in fat deposition at
sites other than subscapular in this lean
population.
The pattern of familial resemblance exhibited for blood pressure in this population
does differ considerably from that observed
in western populations, however. Chazan
and Winklestein (1964) found household aggregation of hypertension in a group of
American households, both in genetically
related and unrelated individuals, but most
studies have found no resemblance for normal blood pressure variation in genetically
unrelated household members. Adopted children and their adoptive parents have nearzero correlations, both in the Framingham
offspring study (Feinleib, 1979) and in the
Quebec study of Biron et al. (1976). Since
adopted children were born elsewhere and
probably have not yet reached adulthood, the
length of time spent with their adoptive parents is probably less than the length of
cohabitation for some of the genetically unre-
309
lated or distantly related pairs used in the
present analysis.
In the Framingham offspring study, correlations between spouses of the propositi and
their unrelated in laws are near zero (Feinleib, 1979). Of course, these in-laws live in
completely separate households. Similar results in the present analysis suggest that
either length of cohabitation has not been
sufficient to have a n effect on in-law pairs, or
that in-laws do not share enough common
environment at the proper stage of the life
cycle to have a significant effect, even when
they occupy the same household.
The marital correlation for diastolic blood
pressure is comparable to the correlations for
first-degree relatives in this populations. A
similar result is reported by Tseng (1967)in a
fishing community from Taiwan. Reports of
marital correlations from western populations are conflicting. Johnson et al. (1965)
found no significant correlation among
spouse pairs for blood pressure at all. Others
conclude that spouse resemblance for blood
pressure remains even when several indices
of household environment (and spouse similarity for them), such a s education, occupation, and dietary sodium intake, are
controlled (Speers et al., 1986). Length of
cohabitation for spouse pairs h a s been suggested as a n intervening factor, but length of
cohabitation does not affect the marital correlation for blood pressure in the Framingham study (Feinleib, 1979; Sackett et al.,
1975),or in Taiwanese agricultural or fishing
communities (Tseng, 1967). In the present
study, no accurate information on length of
cohabitation is available, but the length of
cohabitation for spouse pairs and in-law
pairs should be comparable. If cohabitation
is responsible for the spouse resemblance,
one would expect in-law pairs to have significant correlations for blood pressure as well.
On the other hand, assortative mating for
blood pressure seems unlikely, since blood
pressure is not detectable in normal social
interactions. Although there is some marital
resemblance for height in this group, there is
none for weight or skinfolds, and phenotypic
assortment for height alone cannot account
for the marital resemblance for blood pressure. One explanation for the discrepancy in
marital and in-law resemblance is that
household environment is shared unequally
by different types of relatives. This hypothesis would require detailed study of household
310
P.J. BYARU ET AL
structure and day-to-day functioning for and genetic and cultural heritabilities are
useful primarily for examining the possible
verification.
The fact that the wives-of-brothers correla- effects of shared environment on family
tion for systolic blood pressure is significant, resemblance for modifiable disease risk facwhereas the other in-law correlations are not, tors, not for establishing rigid standards for
requires some comment. The possibility of the effect of household environment on a trait
genetic relatedness among women marrying worldwide.
into a particular sibship was examined, and
ACKNOWLEDGMENTS
two pairs of related wives were excluded from
This research was supported in part by PHS
analysis. While the possibility of remote,
unknown relatedness exists, it would be grants GM28719, HL33973, and MH31302.
unlikely to have a detectable effect on the
LITERATURE CITED
correlation coefficient. Instead, the possibility that individuals who share the same gen- Acheson RM, Fowler GB (1967) On the inheritance of
stature and blood pressure. J . Chronic Dis. 20:731-745.
eration, status, and sex role expectations
JL, Sing CF, Biron P, and Mongeau J G (1979)
may react physiologically in similar ways Annest
Familial aggregation of blood pressure and weight in
must be entertained. It should be noted that
adoptive families. I. Estimation of the relative contributions of genetic and common environmental factors to
the similarity among wives of brothers for
blood pressure correlations among family members.
blood pressure does not appear to be mediated
Am. J . Epidemiol. 110:492-503.
by any similarity in weight or adiposity,
Biron P, Mongeau J, Bertand D (1976) Familial aggregasince their correlations are near zero for skintion of blood pressure in 558 adopted children. Can. Med.
folds and negative for weight. In fact, there is
Assoc. J . 115773-774.
no consistent relationship between family Blom G (1958) Statistical Estimates and Transformed
Beta Variables. New York John Wiley and Sons.
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suggesting that the resemblance for blood
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SM, Cole PE, and Bailey SM 91979) Living together
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RJ, Garrison RJ, Feinleib M, Padgett S, Castelli
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J-M (1979) GEMINI-A computer program for
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(1988) Blood pressure in a rural West Bengal fishing
degree, such a s first cousins. Although wives
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of brothers are significantly correlated for
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systolic blood pressure, none of the other in- Rao DC, Vogler GP, McGue M, and Russell J M (1987)
law relationships have significant correlaMaximum likelihood estimation of familial correlations
from multivariate quantitative data on pedigrees: A
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