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Intergenerational influences on the growth of Maya
children: The effect of living conditions experienced by
mothers and maternal grandmothers during their childhood


Journal: American Journal of Human Biology
Manuscript ID: Draft
Wiley - Manuscript type: Original Research Article
Date Submitted by the Author: n/a
Complete List of Authors: Azcorra, Hugo; Centro de Investigacin y de Estudios Avanzados del
Instituto Politecnico Nacional, Departamento de Ecologa Humana
Dickinson, Federico; Centro de Investigacin y de Estudios Avanzados del
Instituto Politcnico Nacional, Departamento de Ecologa Humana
Bogin, Barry; Loughborough University, Human Sciences
Rodriguez, Luis; Universidad Autonoma de Yucatan, Facultad de
Matematicas
Varela-Silva, Maria; Loughborough University, Human Sciences
Keywords: Maya, Yucatn, Growth, Intergenerational influences



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Intergenerational influences on the growth of Maya children: The effect of living
conditions experienced by mothers and maternal grandmothers during their
childhood

Hugo Azcorra
1
, Federico Dickinson
1
, Barry Bogin
2
, Luis Rodrguez
3
, and Maria
Ins Varela-Silva
2
.

1: Departamento de Ecologa Humana, Centro de Investigacin y de Estudios
Avanzados del Instituto Politcnico Nacional (Cinvestav)-Unidad Mrida, 97310
Mrida, Yucatn, Mxico; 2: Centre for Global Health and Human Development,
School of Sports, Exercise and Health Sciences, Loughborough University,
Loughborough, LE11 3TU United Kingdom; 3: Facultad de Matemticas,
Universidad Autnoma de Yucatn, Mrida, Yucatn, Mxico; : corresponding
author.

hugoazpe@hotmail.com

This research was funded by the National Council of Science and Technology
of Mexico (Conacyt grant no. 168047)

















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ABSTRACT
Objectives To test the hypothesis that living conditions experienced by
maternal grandmothers (F
1
generation) and mothers (F
2
generation) during their
childhood are related to height and leg length (LL: height sitting height) of their
6-to-8 year old children (F
3
generation). Methods From September 2011-June
2012 we obtained height and LL, and calculated z-scores values of these
measurements for all participants who are Maya living in Merida, Yucatan,
Mexico. Several socioeconomic parameters of maternal and grand-maternal
living conditions during childhood were examined. Multiple regression models
were adjusted to examine the relation of anthropometric and intergenerational
socioeconomic parameters of F
1
and F
2
with the z-score values of height and LL
of children. Results Childrens height and LL were positively predicted by the
height and LL of mothers, respectively, with LL influenced relatively more than
height. None of the mothers SES variables were significant. Grandmothers who
lived during their own childhood in transitional housing built with perishable
materials predicted significant reductions in childrens height and LL,
suggesting relevant intergenerational effects of household environment.
Grandmothers who lived in bigger families predicted significantly greater height
and LL in their grandchildren. Conclusions Our findings support the hypothesis
that living conditions experienced by maternal grandmothers during their growth
period influence the growth of their children and grandchildren. Results suggest
that LL is more sensitive to intergenerational influences than is total height and
that the transition from a traditional rural lifestyle to urban conditions results in
new exposures for risk in human physical growth.

Key words: Maya, Yucatan, growth, intergenerational influences.








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INTRODUCTION
The process of growth is a complex phenomenon strongly influenced by the
social, economic and political conditions surrounding the group (Bogin and
Loucky, 1997; Steckel, 2012; Stinson, 2012). It has been suggested that the
current biological status of a group can also be explained by ecological
conditions experienced by recent ancestors during their growth period. In 1986,
Irving Emanuel defined the intergenerational influences hypothesis (IIH) as
those factors, conditions, exposures and environments experienced by one
generation that relate to the health, growth and development of the next
generation (Emanuel, 1986, p 27). Subsequent theoretical contributions
suggest that growth trajectories of children are also influenced by factors that
trace the nutritional history of matrilineal ancestors, including their nutrition
during prenatal stage and first years of postnatal life (Kuzawa, 2005).
Most of the accumulated evidence of intergenerational influences on
growth is on the prenatal stage (Emanuel, 1986; Ounsted et al., 1986; Klebanoff
and Yip, 1987; Emanuel et al., 1992; Emanuel et al., 1999; Emmanuel et al.,
2004; Hypponen et al., 2004; Martin et al., 2004; Kuzawa, 2005; Jasienska,
2009; Alwasel et al., 2011; Alwasel et al., 2013). The intergenerational effects
on postnatal growth have been less studied. Some studies provide results about
the association between parental and offspring height. Correlation coefficients
show that associations between mothers and offspring are stronger than
associations between fathers and offspring in all ages (Alberman, 1991;
Hypponen et al., 2004; Ghosh and Malik, 2007; Gray et al., 2012). However,
parent-offspring correlations reflect both the effect of genes and shared
environmental factors such as diet and life style (Towne et al., 2012).
The Maya are one of the largest and most important ethnic groups in
Mesoamerica (Thompson, 1973). Merida, the capital city of the Yucatan state,
in Mexico, is the home of a great number of Maya people resident in poor
neighbourhoods (Lizama, 2012). Historically, the Maya from Yucatan have lived
under very unfavourable socioeconomic conditions (Bracamonte, 2007), and
continue to do so (Azcorra et al., 2013; Wilson et al., 2013). This has impacted
negatively the biosocial status of the Maya. Previous studies show that Maya
from Yucatan exhibit high rates of undernutrition (mainly short stature) during
the growing period (Kelley, 1991; Wolanski et al., 1993; Siniarska and Wolanski,
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1999; Azcorra et al., 2009; Varela-Silva et al., 2009; Varela-Silva et al., 2012),
and in adulthood. Despite overall improvements of social and economic
conditions since the end of the colonial period in Mexico (1821) research
indicates the absence of a positive secular change in stature for the Maya
people (McCollough, 1982; Siniarska and Wolanski, 1999).
In a previous article we described the nutritional status of a sample of
109 triads of Maya children, their mothers, and maternal grandmothers from
Merida, Mexico (Azcorra et al., 2013). We confirmed the hypothesis that leg
length-relative-to-stature is a more sensitive indicator of nutrition and health
than is total height or sitting height. In that study the analysis was based on the
examination of correlations between grandmothers and children and mothers
and children. In the present study we extend the analysis with a bio-cultural
model to test the IIH and ascertain the impact of biosocial background of urban
Maya grandmothers (F
1
generation) and mothers (F
2
generation) on the linear
growth and nutritional status of their children (F
3
generation). This study
contributes to the knowledge about the intergenerational influences on postnatal
growth in groups with a long adverse socioeconomic history.

METHODS
From September 2011 to June 2012 a cross-sectional study was undertaken on
a sample of 109 triads of urban Maya children (6-to-8 year old), their mothers
and their maternal grandmothers from the city of Merida. The number of triads
needed for the study was obtained through a power analysis calculation. Maya
surnames were used as a proxy for Maya ancestry; the requirement for
inclusion in the sample was that children, mothers and grandmothers had to
have at least maternal Maya surname. Schools (n = 20) where recruitment was
made were randomly selected from the south of Mrida, where Maya language
speakers and people with the lowest level of income are concentrated. To allow
for maximum geographic and socioeconomic variability in the sample, we
selected no more than 10 children from each school. More details of sample
size calculation and recruitment process of participants are described by
Azcorra et al (2013).


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Measurements We only focused, in this study, on height and sitting height of
the participants. Leg length (LL) was calculated by subtracting sitting height
from height. Height and LL were transformed to z-score values using the
Comprehensive references published by Frisancho (2008). Particularly in the
case of mothers and grandmothers, z-score values were useful to
accommodate the effect of loss of height with age. Additionally, grandmothers
were classified as short stature when their height-for-age was below 5
th

percentile of the reference, which for this sample corresponded to less than 150
cm. We focused on the intergenerational effects on the height and LL of
children because these measurements provide information about the nutritional
history of individuals (Bogin & Keep, 1999; Bogin & Varela-Silva, 2010), and are
related to the risk for adult mortality (Barker et al., 1990; Leon et al., 1995) and
health outcomes at adulthood such as obesity, insulin resistance, type 2
diabetes and heart diseases (Forsen et al., 2000; Lopez-Alvarenga et al., 2003;
Asao et al., 2006).
The biosocial background of mothers and grandmothers was analyzed
through 1) current anthropometric characteristics: height and LL (z-score
values) and, 2) socioeconomic indicators experienced during childhood.
Children were measured at schools and adult women at homes, all of
them by trained personal. Anthropometric measurements were taken following
standardized methods (Lohman et al., 1988).
Home visits were used to apply socioeconomic questionnaires to
mothers and grandmothers. Data on socioeconomic conditions experienced
during maternal and grand-maternal childhood were obtained through the same
questions. Some questions examined the general living conditions: place of
birth and growing up, family size, number of siblings, number of rooms used to
sleep, type of water to drink, availability of toilet at home, construction materials
of the house, household assets, parents occupation and work during childhood.
Other questions examined some conditions experienced by mothers and
grandmothers, such as: serious illness or death of parents, divorce or
separation of parents, job loss of parents and alcoholism in the immediate
family. Mothers and grandmothers were interviewed separately. In some cases
the assistance of the mothers was requested when grandmothers did not
understand the questions because they did not speak Spanish fluently.
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Three categories of maternal and grand-maternal house type were
defined according to the materials of construction: 1) traditional Maya rural type
(dirt floor, palm leaf ceilings and wattle and daub walls), 2) perishable materials
(dirt or cement floor, cardboard or metal sheets for walls and ceilings) and, 3)
durable materials (cement floor and cement blocks in walls and ceilings).

Ethical concerns The research was approved by the Bioethics Committee for
the Study of Human Beings of the Center for Research and Advanced Studies
of the National Poly- technic Institute of Merida, Mexico and by the
Loughborough University Advisory Ethical Committee. The mothers and
grandmothers signed consent forms for themselves and mothers on behalf of
their children. Those grandmothers who could not sign their name were asked
to provide their ngerprints as proof of consent. For ethical reasons, adult
women were measured only by women of the research team. All children
provided us verbal consent to be measured.

STATISTICAL ANALYSIS
Intergenerational influences of grandmothers and mothers on childrens growth
status were assessed through multiple regression models. Several models were
adjusted for the outcome variables of z-height and z-LL. Outcome variables
were normally distributed. Model building was done following an exploratory
approach. In order to decide which variables should be included in the final
models each predictor variable was regressed against each outcome variable.
The variables that showed a significant coefficient (p<0.05) were retained in the
model.
We consistently found that paternal job loss during maternal childhood,
grand-maternal home index and family size during childhood predicted the z-
height and z-LL of children and this result did not change with the inclusion of
any other independent variable in the model. For each analysis, model 1
included only the maternal stature or LL as predictors. In model 2 the variable
paternal job loss during childhood (0 = No, 1 = Yes) was added. In model 3,
three grand-maternal intergenerational predictors were added: 1) short stature
(0 = No, 1 = Yes), 2) home type (0 = Maya type, 1= perishable materials, 2 =
durable materials) and, 3) family size (continuous).
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The validity of the final models was assessed through several diagnostic
tests. All models met the assumptions for multiple regression model building.
Particular interest was given to collinearity between predictors included in the
models; variance inflation factor (VIF) values informed us that no cases violated
this assumption. Additionally, residuals of the models were normally distributed
and all predictors had linear relationships with outcomes. In all analyses, the
signicance level was set at = 0.05.

RESULTS
Nutritional status of participants has been described recently by Azcorra et al.
(2013). Short stature in adult women and stunting and short LL in children were
defined when height-for-age and LL-for-age were below the 5
th
percentile of the
Frisancho Comprehensive references (Frisancho, 2008). Mothers and
grandmothers exhibited very low heights (means of 147.91 cm [SD = 4.84] and
143.08 cm [SD = 4.77], respectively) and 71% and 90% of them were classified
as short stature. Stunting in children, defined as z-height less than -1.650 of the
reference, was present in 11% of the sample. The prevalence short LL, defined
as z-LL less than -1.650 was 29%.

Intergenerational influences The models of intergenerational influences on
childrens height and LL are shown in Tables 1 and 2. Maternal z-score for
height and LL positively predicted childrens growth in all models. Paternal job
loss during maternal childhood did not predict significantly the growth of
children. The presence of short stature in grandmothers did not predict
significantly the outcome variables. Grand-maternal home type significantly
impacted the growth of children. Those grandmothers who lived during their
childhood in a household built with perishable materials predicted a decrease in
their grandchildrens z-score for height and LL in comparison to children whose
grandmothers lived in a traditional rural type house. For LL we also found that
grandmothers who lived in a house built with durable materials positively
impacted the growth of the children, but this effect was marginally significant (P
= 0.059). Greater grand-maternal family size during childhood positively
predicted the childrens LL. The inclusion of grand-maternal predictors
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contributed to the increase of the explained variance for height by 8% and for
LL by 16%.

PLEASE INSERT TABLE 1 HERE

PLEASE INSERT TABLE 2 HERE

DISCUSSION
Our results suggest that living conditions experienced by mothers and
grandmothers during childhood contribute to shape the linear growth status of
children of F
3
generation. We developed our regression models based on our
previous findings (Azcorra et al. 2013) of significant correlations between child-
mother and mother-grandmother dyads in height, sitting height and LL, but not
between child-grandmother dyads. Accordingly, in the present analysis we
included first the maternal intergenerational predictors in models 1 and 2, and
then grand-maternal predictors in model 3.
Our previous analyses and our current multiple regression models
showed that childrens height and LL were positively predicted by maternal
height and LL respectively, and this effect did not change after the inclusion of
grand-maternal anthropometric and socioeconomic factors. We recognize that
genetic factors cannot be ignored in the context of our results. However two
relevant considerations should be pointed out: 1) recent evidence suggests that
while many genes influence the linear growth of our species, the variance in
height explained by the genome accounts for only a small proportion (currently
estimated at less than 10%) of the total variance of a given trait (Mortier and
Vandem Berghe, 2012), and 2) the expression of the genomic regulation of
growth in height tends to be lower in populations under disadvantaged living
conditions (Mueller 1976, Lauderdale and Rathouz, 1999; Silventoinen et al.,
2000). For instance, reviewing 24 studies of parent-child correlations, Mueller
(1976) found that the genetic component of such correlations tends to be low in
developing countries, in which the presence of several environmental factors
tend to induce variation in growth and reduce the phenotypical expression of
genes. The United States-born children of Guatemalan Maya immigrant parents
were found to be 11.5 cm taller, on average, and have longer legs, averaging
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6.8 cm longer than Guatemala-living Maya children of the same ages (5-12
years old, Bogin et al., 2002). The Maya-American children had body
proportions more like those of European-American children in the US than like
Maya children in Guatemala. Improvements in the environment for growth, in
terms of nutrition and health, seemed to explain both the trends in greater
stature and relatively longer legs for the Maya-Americans. Gene-environment
interaction seems to be more relevant in growth than only genes per se,
particularly in those populations exposed to chronic stress.
The intergenerational influences hypothesis (IIH) has been previously
tested by Varela-Silva et al (2009) in a sample of 206 Maya children (120 girls)
4-6 years of age and their mothers living in the south of Merida. In that study it
was found that Maya children whose mothers height was below 150 cm were
3.6 times more likely to be stunted than children whose mothers height was
above 150 cm. In addition, children with birth weights below 3,000 g were over
three times more likely to be stunted than children within the range of normal
birth weight (3,0003,500 g). The authors explained these results in the context
of IIH suggesting that the compromised conditions of mothers growth pass on
similar risk for their offspring.
Intergenerational influences have also been tested for body composition
in Maya populations. A study by Wilson et al (2014) aimed to determine whether
mothers adult height (used as an indicator of early life environment) had an
intergenerational influence on several adiposity parameters of their children.
The sample included Maya children (7-9 years of age) and their mothers. In
general mothers exhibited very low heights (mean = 146.84 cm, SD = 4.58 cm)
and children high levels of body fat (mean = 28.40%, SD = 6.81%). After
controlling for sanitation index of the family and maternal parity, maternal height
did not predict significantly the childrens BMI, waist circumference and
percentage body fat, which suggest that recent environment and lifestyles are
more relevant than the intergenerational legacy in this sample.
Our results suggest that the grandmothers house type is a good
indicator of environmental quality during their growing years. We suggest that
grandmothers who lived in a house type which was built with durable materials
(e.g., cement) belonged to families who experienced in general the best living
conditions relative to other families. The next best grandmaternal house type
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was found to be the Maya type - palm leaf roof, wattle and daub walls and dirt
floor. Finally, grandmothers who grew up in a house built with perishable
materials (cardboard and corrugated metal) belonged to families who
experienced the most disadvantaged conditions, probably because these
families were in a transition period from traditional to modern conditions.
Larger grand-maternal family size was another intergenerational
predictor of greater childrens linear growth. This finding makes sense in the
context of the demographic characteristics of rural societies, such as the Maya,
who depended on agricultural activities for subsistence. These rural societies
took advantage of larger family size to increase their economic productivity.
Ethnographic evidence for this is provided by Kramer (2005) who studied
Xculoc, a Maya farming village in the Yucatan. Kramer describes how family
size and the presence of offspring at home until 25 years of age contribute
significantly to increase the production of maize and other benefits for the
family. Maya families of Xculoc had, on average, 7 children and the presence of
grandparents at home was very common. Kramer also found that children were
assigned childcare activities and domestic chores from around three years of
age and then were involved in the laborious tasks of harvesting and transporting
the maize. Domestic work and childcare were gender-based, with females
allocating more time to these activities.
In our study 74% of the grandmothers reported that their fathers worked
for the most part of their lives in the milpa, a complex form of swidden
agriculture involving about 40 vegetal species (Tuxill et al., 2010). On average,
grandmothers family size was 8 and the number of their own offspring was 7.
Therefore we hypothesize that those grandmothers belonging to bigger families
experienced better conditions during growth, which in turn have positive
intergenerational impacts on the growth of their grandchildren.
The effect of grand-maternal home type and family size was more
evident on childrens LL than in total height. A growing body of research finds
that the leg, especially the tibia, is more sensitive to intergenerational influences
than total height (reviewed by Bogin & Varela-Silva 2010).
The biological condition shown by the Maya participating in the present
study, as well as our previous research articles, reveals the effects of chronic
deprivation along several generations. Our results suggest that early
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environments experienced by mothers and grandmothers impacted negatively
their own growth and have significant influences on their descendants growth
trajectories. The processes through which intergenerational influences operate
have been not completely elucidated. However, gestation seems to be a key
period which triggers complex biological processes, including epigenetic
modifications that help to explain some phenotypic traits and conditions in
individuals. Evidence suggests that epigenetic marks are established during
early stages of embryogenesis and exhibit environmental plasticity into the
postnatal period (Gluckman et al., 2011). It has been suggested that maternal
nutrients and hormones act as cues of environmental conditions which allow
offspring to adjust their growth and development (Gluckman and Hanson, 2005)
in utero. The exposure to hormones can induce durable epigenetic
modifications that potentially modify the offsprings physiology, metabolism and
functions during postnatal stages (Kuzawa and Thayer, 2011).
Accumulated evidence suggests that offspring biology is possibly less
sensitive to rapid changes in the current environment when adverse
intergenerational influences or signals are present. For instance, some studies
of nutritional interventions during pregnancy have shown little or moderate
impacts on the offspring development (Villar et al., 2007; Kramer and Kakuma,
2010). In contrast, larger effects have been found when nutritional interventions
have been done prior to pregnancy (Stein et al., 2003; Behrman et al., 2009).
Understanding the timescale at which intergenerational influences operate is
particularly important if we are interested in implementing effective interventions
to improve the nutritional and health status of the current and future
generations. Even if well planned interventions are implemented in populations
with long histories of deprivation and poverty, then positive results may require
two or more generations to be detected (Kuzawa and Tahyer, 2011; Bogin
2013).
We hypothesise that Maya people will not overcome the negative
intergenerational influences unless poverty levels are not substantially reduced.
According to official reports, by 2010, 46.2% (52 million) of the Mexican
population was classified as poor (CONEVAL, 2013). As in many other regions
of the world, poverty in Mexico tends to be more severe in indigenous groups,
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including the Maya, and this situation has been reflected in the biological
condition of indigenous Mexicans (Rivera-Domarco et al., 2013).
Historically, the south-east of Mexico has shown greater economic
poverty levels than the centre and the north of the country. The magnitude of
the problem is so great that despite the increase in social assistance programs
for indigenous communities in the last few years their net effect remain still
insufficient (INSP-SSP, 2007; INSP, 2013). In addition, the Yucatan has
remained in the last fifteen years among the states with the highest rates of
social inequality, measured as the concentration of the highest income
disparities (CONEVAL, 2014). We believe that reducing the poverty levels in
Mexico necessarily implies to reduce the levels of social inequality through a
more equitably wealth distribution.

ACKNOWLEDGMENTS
The authors would like to thank again the people who participated in the field
work of this research, especially to Biol. Graciela Valentin, research assistant of
Cinvestav and the students of nutrition Frida Gutierrez and Paulina Cauich. The
MSc. Ina Lopez generated the dataset and participated in the design of the
recruitment of participants. We also would like to thank the mothers,
grandmothers and children who accepted to participate in the study.

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Table 1 Intergenerational effects on children z-score values for height
Model 1 Model 2 Model 3
B (SE) p B (SE) p B (SE) p CI 95%
Maternal z-score of height 0.419 (0.093) <0.001 0.401 (0.093) <0.001 0.416 (0.094) <0.001 0.23 0.60
Paternal job loss during maternal childhood -0.317 (0.192) 0.103 -0.176 (0.187) 0.350 -0.55 0.20
Grandmaternal short height -0.271 (0.221) 0.221 -0.71 0.17
Grandmaternal home index (reference =
household Maya type
a
)

-Perishable materials (cardboard & metal) -0.439 (0.154) 0.005 -0.74 -0.13
-Durable material (cement) 0.412 (0.321) 0.203 -0.22 1.05
Grandmaternal family size during childhood 0.043 (0.023) 0.061 0.00 0.09
Constant 0.180 (0.200) 0.371 0.192 (0.199) 0.338 0.189 (0.323) 0.559 -0.45 0.83
R
2
adjusted 0.151 0.164 0.248
a
Household Maya type: palm leaf roof, wattle & daub walls and ground floor; S.E.: standard error; n = 109, F (6, 102) = 6.95, p<0.001, R
2
= 0.290; Shapiro-
Wilk residual normality test: w = 0.98, p = 0.126; Breusch-Pagan/Cook-Weisberg homoscedasticity test: X
2
(1)
= 0.04, p = 0.840.
















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Table 2 Intergenerational effects on children z-score values for leg length
Model 1 Model 2 Model 3
B (SE) p B (SE) p B (SE) p CI 95%
Maternal z-score of LL 0.369 (0.094) <0.001 0.352 (0.093) <0.001 0.353 (0.083) <0.001 0.19 0.52
Paternal job loss during maternal childhood -0.381 (0.220) 0.086 -0.093 (0.192) 0.630 -0.47 0.29
Grandmaternal short height -0.040 (0.224) 0.859 -0.48 0.40
Grandmaternal home index (reference =
household Maya type
a
)

-Perishable materials (cardboard & metal) -0.533 (0.155) 0.001 -0.84 -0.23
-Durable material (cement) 0.623 (0.326) 0.059 -0.02 1.27
Grandmaternal family size 0.073 (0.023) 0.002 0.03 0.12
Constant -0.498 (0.178) 0.006 -0.476 (0.177) 0.010 -0.767 (0.351) 0.031 -1.51 -0.28
R
2
adjusted 0.118 0.135 0.297
a
Household Maya type: palm leaf roof, wattle & daub walls and ground floor; S.E.: standard error; n = 106, F (6, 99) = 8.38, p<0.001, R
2
= 0.337; Shapiro-Wilk
residual normality test: w = 0.99, p = 0.693; Breusch-Pagan/Cook-Weisberg homoscedasticity test: X
2
(1)
= 0.19, p = 0.659


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