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Epidemiologic transition in an isolated indigenous community in the Valley of Oaxaca Mexico.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 137:69–81 (2008)
Epidemiologic Transition in an Isolated Indigenous
Community in the Valley of Oaxaca, Mexico
Robert M. Malina,1,2* Maria Eugenia Peña Reyes,3 and Bertis B. Little4
1
Department of Kinesiology and Health Education, University of Texas at Austin
Department of Health and Physical Education, Tarleton State University, Stephenville, TX
3
Escuela Nacional Antropologia e Historia, Mexico DF
4
Department of Mathematics, Physics, and Engineering, Texas Data Mining Research Institute,
Tarleton State University, Stephenville, TX
2
KEY WORDS
prereproductive mortality; demographic transition; secular trends; gastrointestinal
disease; nutritional status; seasonal variation
ABSTRACT
The objective of the present study is to
analyze age-specific mortality in a rural indigenous community in the throes of a secular increase in size in the
Valley of Oaxaca, southern Mexico, over 30 years, 1970–
1999. Variation in mortality by age group was analyzed
over time for evidence of an epidemiological transition.
The seasonal rain pattern in the Valley of Oaxaca (83%
from May through September) was evaluated for its relationship with mortality in wet and dry months. Mortality and causes of death changed markedly over the 30year interval. Infant and preschool mortality, overall
mortality, and causes of death changed from the 1970s
through the 1990s. Prereproductive deaths (<15 years)
predominated in the 1970s and were largely due to gastrointestinal and respiratory diseases, with periodic out-
breaks of measles. Deaths of adults 651 years predominated in the 1990s and were largely due to degenerative
diseases usually associated with aging. The marked
changes in age and causes of death over the three decades (epidemiologic transition from Stage I to Stage II)
occurred concurrently with significant secular increases
in body size in children, adolescents, and young adults,
highlighting improved health and nutritional conditions
in the community which is in early Stage II of the demographic transition. The demographic transition to Stage
II is a leading indicator (15–25 years lag) for the onset of
the secular trend, while the epidemiologic transition to
Stage II is a predictor that the secular increase is in process in the study community. Am J Phys Anthropol
137:69–81, 2008. V 2008 Wiley-Liss, Inc.
Differential mortality is a driving force in human
populations, affecting population genetic structure, human
biology, and demographic characteristics. In particular,
differential prereproductive mortality is the most influential component of natural selection in preindustrial
societies, dwarfing the influence of variance in fertility
on natural selection. Mortality is also an indicator of
population health status. Infant mortality is accepted as
a sensitive barometer of community, regional and national health conditions, while elevated mortality among
preschool children is a widely recognized indicator of
compromised nutritional status.
Mortality rates relative to birth rates also indicate the
stage in the demographic transition. As high death rates
and high birth rates (Stage I) diverge and lower mortality and sustained high natality occur (Stage II), the first
demographic transition has occurred. The epidemiologic
transition is characterized by the change from high infectious disease mortality among young individuals to a
preponderance of mortality from degenerative disease
among the aged (Omran, 1971, 1983; Barrett et al.,
1998; Gage, 2005; Little et al., 2008). In Europe, the demographic transition occurred over approximately a 100year period during the industrial revolution, starting
about 1800 (Gage, 2005). Similarly, the epidemiological
transition occurred over a century (Barrett et al., 1998).
Population level investigations of mortality are frequently confounded by emigration, immigration, and exogenous factors such as socioeconomic variation within
and between populations. Isolation of specific effects on
mortality rates can be accomplished more straightforwardly among anthropological populations because
they are frequently closed or nearly closed to outside economic, genetic, and demographic influences. Moreover,
confounding effects can frequently be quantified and analyzed in such groups. Analysis of age-graded changes in
mortality over time can reveal changing patterns, especially in those populations undergoing the demographic
transition and/or secular changes in body size. In Stage I
of the demographic transition, mortality is typically high
and the birth rate is commensurately high. Mortality
declines absolutely and relatively (i.e., compared to birth
rates) during Stage II of the transition, leading to population growth and shift in structure (Gage, 2005).
The aim of the present investigation is to analyze
changes in age group-specific mortality over time and
C 2008
V
WILEY-LISS, INC.
C
Grant sponsor: National Science Foundation; Grant numbers:
BNS 78-10641, BCS 9816400; Grant sponsor: Institute of Latin
American Studies at the University of Texas at Austin.
*Correspondence to: Robert M. Malina, Department of Health and
Physical Education, Tarleton State University, Box T-0010, Stephenville,
Texas 76402-0010, USA. E-mail: rmalina@skyconnect.net
Received 8 August 2007; accepted 26 February 2008
DOI 10.1002/ajpa.20847
Published online 29 April 2008 in Wiley InterScience
(www.interscience.wiley.com).
70
R.M. MALINA ET AL.
seasonal patterns of mortality between 1970 and 1999 in
a genetically isolated rural indigenous Zapotec-speaking
community in the Valley of Oaxaca and to relate these
changes to the observed secular increase in body size in
children and young adults.
MATERIALS AND METHODS
The focus of the study is a rural Zapotec-speaking
community in the Valley of Oaxaca, an intermontane, Yshaped valley in southern Mexico. The city of Oaxaca is
located at the junction in the Y. The valley is geographically defined as the upper drainage basin of the Rio
Atoyac and its floor varies from 1,420 to 1,740 m above
sea level (Kirkby, 1973; Dilley, 1993, 1997). Mean annual
temperature is about 208C, with a difference of 58C
between the mean temperatures of the hottest and coldest months. Rainfall is more variable, with a sharp distinction between dry months (October–April) and wet
months (May–September) when about 83% of the average annual precipitation on the valley floor occurs
(Kirkby, 1973; World Climate Data, 2007).
Community
The community is located about 23 km northwest of
the city of Oaxaca at an altitude of about 1640 m in the
piedmont zone of the northern (Etla) branch of the Valley of Oaxaca (Granskog, 1974), and will be subsequently
referred to as the Etla community (see Fig. 1). The community was economically isolated until quite recently
and is still genetically isolated (Little and Malina, 1989;
Little et al., 2006). National census figures indicated a
population of 1,423 in 1970 (Secretaria de Industria y
Comercio, 1971), 1,823 in 1980, 1,954 in 1990, and 1,939
in 2000 (Instituto Nacional de Estadı́stica, Geografı́a e
Informática [INEGI], 1984, 1991, 2002). The annual
report of the community health center indicated a population of 2,037 for 2000 (Reyes Castellanos et al., 2000).
Population size has historically been influenced by outmigration, especially of males, starting in 1940 (Granskog, 1974). Community health center records indicated
93 emigrants in 1998 (Altamirano, 1999) while household interviews in 2000 indicated 98 emigrants, the majority of whom were males (79%).
The community is dependent largely on subsistence agriculture with families working small plots of individually or
communally owned land. About 90% of heads of households were full-time farmers (campesinos) in 1978, but
about 40% of households did not own land (Malina et al.,
1985). The proportion of full-time farmers declined to about
30% by 2000 (Reyes Castellanos et al., 2000; Martinez Julian et al., 2001), which reflects a breakdown in economic
isolation. By inference, many are now part-time farmers;
other occupations include vendors (which are a significant
component of the informal economy in Mexico), artisans,
construction workers, and industrial workers, who commute daily to the City of Oaxaca or adjacent centers.
The community is indigenous to the Valley of Oaxaca.
It was among communities listed as established in a
1536 census of Oaxaca commissioned by the Marquesado
de Cortéz (Iturribarria, 1955) and also appeared on tributary counts circa 1580, which presumably reflected the
preconquest situation in the Valley of Oaxaca (Welte,
1975). Census data indicated that among individuals of
5 years of age and older, Zapotec was spoken by 915 in
1960, 985 in 1970 (Secretaria de Industria y Comercio,
American Journal of Physical Anthropology
Fig. 1. Map of Oaxaca and location of study community.
1963, 1971), 1,390 in 1980, 1,379 in 1990, and 1,113 in
2000 (INEGI, 1984, 1991, 2002; Serrano Carreto et al.,
2002). The majority, however, spoke both Zapotec and
Spanish, and several spoke Mixtec.
It is estimated that the community has been relatively
isolated genetically since 900 A.D. (Little and Malina,
1989; Little et al., 2006). Estimated inbreeding was moderately high (0.01), and gene flow was very low (3.3%);
natural selection was slightly more intense (10%) than
would be predicted given population and subsistence
characteristics (Little and Malina, 1989, 2005). Natural
selection intensity was influenced largely by prereproductive mortality (Little and Malina, 1989), and there
was no selection for reduced body size in the community
(Little et al., 1989).
Health resources
No health center was present in the community at the
time of the first anthropometric survey of primary school
children in 1968 (Malina et al., 1972), although older
informants indicated availability of medical services. A
public health nurse visited the community once per
week at the time of the 1978 survey (Malina et al.,
1980), but there was no doctor in the community. The
public health nurse worked mostly with children and
young mothers. A mid-wife with some public health experience also lived in the community. The community
currently has a health center which dates to 1991 when
a program, ‘‘Solidaridad,’’ helped develop the health
infrastructure throughout the country (Velazquez, 1992).
The center is staffed by a public health nurse daily,
EPIDEMIOLOGIC TRANSITION IN AN ISOLATED ZAPOTEC COMMUNITY
while a physician attends the center daily during the
week but not on weekends. Recent reports of the medical
center indicate births, mortality, and frequencies of
medical consultations, including family planning and
child health (Reyes Castellanos et al., 2000; Martinez
Julian et al., 2001).
Birth and death records
The official records are handwritten and are kept by
the secretary to the community president for each year.
Residents of the community are required to register all
births and deaths, although a lag may occur between
actual events and official recording. Availability of professional health personnel likely influenced the quality
of more recent records.
Birth and death records for 1969 through 1978 were
transcribed from records in the community archive in
fall 1979 (Buschang, 1980), while records for 1979
through 1999 were transcribed at the district archive in
Etla in 2000 and 2002 by project researchers (Peña
Reyes et al., 2003; Malina et al., 2004a,b). The number
of births from the health center reports was complemented by the death records from the archives for the
interval 1995–1999 because the archives had more accurate accounting of mortality than the health center. Age
was generally reported in days or months for infants
and young children and in whole years (presumably age
at last birthday) for older individuals.
Fetal deaths were limited to the 1970s and were generally reported on both birth and death records. Three were
reported in 1980 and none thereafter. If a child was
reported as stillborn on both the birth and death records or
as a live birth on the birth records and a stillbirth on the
death records, it was considered to have been live born. In
some areas of Latin America in the 1960s and 1970s,
deaths occurring on the first day of life are considered stillborn (mortinatos) because legally they are not considered
live births (Puffer and Serrano, 1973). In the community
records for the 1970s, 39 newborn were reported as being
born alive but dying soon after birth and 22 were reported
as stillborn. Of the latter, gestational ages \9 months were
noted for 10 births and at 9 months for 9 births, while gestational age information was not reported for 3.
The accuracy of handwritten records is based upon the
actual registration of deaths and thoroughness of recording by secretaries. A lower ratio of reported to actual
events has been noted in areas where an indigenous language is spoken and where schooling is minimal (Sloan,
1971). As noted earlier, the population has a high proportion of Zapotec speakers, but the majority is presently
largely bilingual. The vast majority of the population
101 years of age did not advance beyond primary school
education, grades 1–6, in 1970 and 1980 (Secretario de
Industria y Comercio, 1971; INEGI, 1984). Among those
151 years of age in the 1990 and 2000 censuses, respectively, 22 and 9% had no schooling, 29 and 23% had
incomplete primary schooling, 35 and 43% completed primary school, and 14 and 25% had postprimary schooling
(INEGI, 1991, 2002; Serrano Carreto et al., 2002).
Recorded causes of death were rather general in the
1970s and early 1980s. It is likely that the most prominent symptoms, e.g., diarrhea, measles rash, respiratory
distress, etc. were reported at registration. Symptoms of
course are complicated and may not be equated with
cause of death. Diarrhea, for example, frequently occurs
with measles, being quite common before and during the
71
appearance of the rash (Scrimshaw et al., 1966). From
1985 on, however, recorded causes were more specific
which may reflect the presence of a public health nurse
in the late 1970s and 1980s and an attended medical
center since 1991.
Causes of death were grouped into several categories.
Gastrointestinal causes included diarrhea, vomiting, dysentery, colic, and gastroenteritis; specific parasitic infections are probably involved in several. Dehydration often
accompanied gastrointestinal conditions as a cause of
death. Respiratory causes of death included cold, pneumonia, whooping cough, bronchitis, acute respiratory distress (especially in neonates and the elderly), and pulmonary edema (especially in the elderly). Infectious causes
of death included primarily measles (especially in the
1970s) but also generalized fever and general inflammation (especially in the elderly), plus isolated cases of
typhoid, yellow fever, septicemia, encephalitis, gangrene,
and peritonitis. Several congenital conditions were noted
in infants and young children (meningocele, airway
obstruction, hemophilia, macrocephaly, cranial malformation, congenital heart disease, Down syndrome). Deaths
attributed to accidents, anemia, and pregnancy, childbirth
were few and simply noted as such. The term ‘‘hinchazon’’
(swelling, edema) was indicated as a cause between 1970
and 1984. A more specific definition for hinchazon was
not indicated in the available records. Other categories of
causes of death, largely in adults, included cardiovascular
complications (infarct, stroke, ‘‘cardiorespiratory insufficiency’’, heart disease and problems), diabetes, renal
insufficiency, cancers, cirrhosis (usually as a complication
of alcohol use), and old age (senilidad).
Deaths were tabulated by age group as follows: neonate—birth through 1 month; non-neonate—one through
11 months (not yet 1 year of age); infants—neonates plus
non-neonates (deaths before 1 year); early childhood—1
through 4 years of age (not yet 5 years of age); and subsequently by 10 year age groups (5–14, 15–24, 25–34,
and so on) up to 851 years. The age range 15–44 was
considered the reproductive years. Infant mortality rates
were calculated on the basis of deaths occurring during
the first year of life (neonatal plus postneonatal periods).
These and other calculations were also based on
accepted formulae (Keyfitz and Flieger, 1971). Deaths
occurring in the wet and dry seasons were compared
among age groups and across decades using Chi-square.
Statistics were computed using Primer of Biostatistics
(Glantz, 1996) and EpiInfo (CDC, Atlanta, GA, USA).
Growth stunting
The growth status of school children in the community
was surveyed in 1968, 1978, and 2000 (Malina et al.,
2004a). Z-scores for height were calculated relative to
reference values of the United States growth charts
(Center for Disease Control and Prevention, 2000), and
were subsequently classified as stunted (z-score below
22.00) and nonstunted (z-score equal to or above 22.00)
(de Onis and Blossner, 1997). Changes in the prevalence
of stunting among surveys are used as an indication of
changing health and nutritional conditions in the community paralleling changes in mortality.
RESULTS
A total of 1,727 births and 479 deaths were reported
from 1970 through 1999. Year-to-year variation in absoAmerican Journal of Physical Anthropology
72
R.M. MALINA ET AL.
lute numbers of births and deaths is illustrated in Figure 2. The downward trend in both births and deaths
over time is apparent. Information on sex is available for
1,650 newborns, 824 males, and 826 females, giving a
sex ratio of 0.998. Information on sex of those who died
is available for 476 individuals, 227 males, and 249
females, giving a sex ratio of 0.912. The sex ratio at
death, however, varies with age. It is highest in children
under 5 years, 1.12, indicating more deaths in young
males, and is then \1.0 at all other ages indicating more
deaths in females: 5–14 years, 0.92; 15–44 years (reproductive years), 0.79; 45–74 years, 0.87; and 751 years,
0.68. The sex ratio for deaths, of course, must be tempered with the emigration of males, many of whom do
not return to the community.
Births, deaths, crude population increase, and estimated infant and preschool death rates are summarized
by decade in Table 1. Live births were used as the denominator because census figures are not available for
the number of children 1–4 years. Births and deaths
decline over time; births decline more so from the 1980s
into the 1990s while deaths decline more so from the
1970s into the 1980s. The estimated crude increase rises
into the 1980s and declines in the 1990s. Estimated
infant and preschool mortality rates decline over time,
with the major decline in infant and preschool mortality
occurring from the 1970s into the 1980s.
Two trends are apparent among deaths by age group
as a percentage of all deaths in the three decades (see
Fig. 3). First, deaths of infants and children 1–4 years
decline from 53 and 11% of all deaths, respectively, in
1970–1979 to 9 and 4% of all deaths, respectively, in
1990–1999. Second, deaths of older adults 651 years of
age increase from 19% of all deaths in 1970–1979 to 65%
in 1990–1999 (see Fig. 4). Percentages of deaths in the
age groups between the young and old extremes are rea-
Fig. 2. Number of births and deaths from 1900–2000.
sonably stable over the three decades, although those in
adults 55–64 years triple from 3 to 9% from the 1980s
into the 1990s.
The changing mortality pattern is also reflected in
changes in causes of death over the three decades (Table
2). In the 1970s and 1980s, the primary contributors to
infant mortality are perinatal complications among neonates which likely reflect respiratory and cardiovascular
immaturity. Among postneonatal infants (1–11 months)
and children of preschool (1–4 years) and school (5–14
years) age, gastrointestinal conditions and respiratory
and other infections are the primary contributors to mortality. Measles is noted as a cause of death in 14 children
1–5 years of age in the 1970s, 12 in 1972, and 2 in 1977,
which suggests a measles epidemic in 1972. In the
1990s, however, absolute number of deaths attributed to
gastrointestinal conditions and other infections are
reduced considerably; nevertheless, among the relatively
few deaths in children older than 1 month of age, 10 of
17 (59%) are attributed to gastrointestinal conditions.
Deaths among individuals 15–54 years are relatively
few compared to younger and older age groups and show
no predominant cause. Four deaths are attributed to
cardiovascular conditions in those 25–44 years, one in
the 1970s and three in the 1980s. The former is simply
described as cardiac insufficiency while the latter appear
to be congenital: stroke (female, 27 years), hypertensive
heart disease (female 34 years) and mitral lesion (female
37 years). Several degenerative diseases appear among
causes of death in those 35–54 years in the 1980s and
1990s, including myocardial infarction (male, 46 years),
diabetes (male, 35 years; female, 48 years), and cirrhosis
(females, 40 and 47 years; male, 45 years) with alcohol
consumption indicated as a primary factor.
Among causes of death in those 55 years of age and
older, gastrointestinal conditions predominate as a major
cause in the 1970s, but cardiovascular conditions
increase as the major cause in the 1980s and 1990s.
Respiratory and gastrointestinal conditions are also indicated as causes of death in the 1980s and 1990s, especially among those 751 years of age. Renal insufficiency
appears as a cause of death in the 1980s (2 cases), but is
more common in the 1990s (9 cases). Dehydration is frequently associated with renal sufficiency. ‘‘Old age’’ also
appears as a ‘‘cause’’ of death in those 751 years old in
the 1980s and 1990s; it often has ‘‘desnutricion’’ (malnutrition) as an associated condition.
Hinchazon (swelling, perhaps edema) is indicated as
a cause of death in 28 individuals, 11 males, and 17
females, in the 1970s and early 1980s, and is last noted
in the records as a cause of death in January 1984. It is
noted most often in adults 601 years of age, 19 of 28
cases (68%), followed by six cases evenly distributed
between 16 and 55 years of age and 3 children 3, 4, and
6 years of age. Hinchazon is indicated without associated
conditions with the exception of 3 adults (females 30, 70
years; male, 73 years) for whom diarrhea is noted as an
associated condition. It is likely hinchazon reflects differ-
TABLE 1. Births, deaths, crude increase, and infant and preschool mortality rates per 1,000 live born from 1970–1999
Years
1970–1979
1980–1989
1990–1999
a
Births
Deaths
Crude increase (B minus D)
Infant mortalitya
1–4 year mortalitya
662
621
444
225
151
103
437
470
341
181
71
20
36
19
9
Per 1,000 live born infants.
American Journal of Physical Anthropology
EPIDEMIOLOGIC TRANSITION IN AN ISOLATED ZAPOTEC COMMUNITY
73
Fig. 3. Relative frequency of deaths by age group and decade: 1970–1999.
Fig. 4. Percentages of deaths among individuals <5 and
>65 years old: 1945–1999.
ent conditions at different ages. A clear shift in causes of
death among the elderly occurred, moving from acute infectious disease before 1980 to predominately chronic
and degenerative diseases by 1990 to 1999.
Variation in mortality by rainy versus dry seasons is
significantly different by age group (Table 3). Causes of
death in neonates (\1 month of age) differ from those
among older children (Table 2), but causes of death for
postneonates and preschool children 1–4 years of age are
similar and were combined for subsequent analysis. During the rainy season mortality among children 1 month
through 4 years of age is significantly higher (P \ 0.05)
compared to mortality during the dry season among individuals 15–65 years of age in 1970–1979 and 1990–1999,
but not 1980–1989. In the rainy season, gastrointestinal
conditions are the most frequent cause of death (64%)
among children 1 month through 4 years of age. This is
consistent with the observation that problems with
drainage and lack of sanitary food and water are major
factors in gastrointestinal infections as these problems
are exacerbated during the rainy season. The trend for
more frequent mortality during the rainy season persists
and the change in its composition (gastrointestinal vs.
other causes) over time reveals an epidemiologic transition process. During the rainy season the relative frequency of mortality among children 1 month through 4
years is greater in the 1990s (73%) compared to the
1970s (59%) and 1980s (60%). On the other hand, the
absolute number of deaths in the age group 1 month
through 4 years during the rainy season declines over
time. This indicates that 1) during the rainy season
other infectious diseases as a cause of mortality have
decreased in frequency over time, and 2) gastrointestinal
diseases predominate as a cause of death during the
rainy season since sanitary and food conditions are
aggravated. Nongastrointestinal infectious diseases
account for 29 and 14% of the deaths to children in this
age group during the rainy season in the 1970s and
1980s, respectively. Measles is the primary infectious
agent, accounting for 13 of 15 deaths attributed to infectious conditions during the rainy season in the 1970s
and 1980s.
DISCUSSION
The present study focused on birth and death records
over a 30-year interval, 1970–1999, for a single, indige-
nous, rural community in the Valley of Oaxaca, southern
Mexico. Natality and mortality statistics undoubtedly
vary among communities throughout the state as well as
the country. Nevertheless, the data highlight several
trends in dynamics of change in demographic, health,
and nutritional conditions in the community that parallel trends in the state of Oaxaca. Among the 32 states
and the Federal District of Mexico, Oaxaca ranks 30th
in an index of marginalization in 1995 (Consejo Nacional
de Poblacion, 2000), 32nd in an index of social malnutrition (indice de desnutricion social, Roldan et al., 2000),
31st in the Human Development Index in 2000 (Programa de las Naciones Unidas para el Desarrollo, 2003),
and 30th in mortality among children \5 years of age in
2000 (INEGI, 2005). Moreover, the State of Oaxaca has
ranked consistently below the national average in the
Human Development Index for Mexico since 1950: 30%
below in 1950 and 1960, 25% below in 1970, 20%
below in 1980, and 15% below in 1990 and 2000 (Programa de las Naciones Unidas para el Desarrollo, 2003).
Conditions in the state of Oaxaca are also reflected in
the growth status of children. At school entry, about 43%
of children in the state in 1994 had stunted heights, i.e.,
[ 2 standard deviations below that expected for age
(Dirección General de Estadistica e Informatica de la
Secretaria de Salud, 1998). Moreover, about 48% of
indigenous children \5 years of age in the south of
Mexico, including the state of Oaxaca, in the 1998–1999
national nutrition survey had heights that would classify
them as stunted (Rivera et al., 2003). All markers indicate the marginal and inequitable status of the state of
Oaxaca compared to other federal entities in Mexico,
suggesting conditions have been and continue to be relatively poor compared to other regions.
Mortality and causes of death in the Zapotec community changed markedly over the 30-year interval. Deaths
to individuals of prereproductive age, especially \5
years, predominated in the 1970s, while deaths to individuals 651 years of age predominated in the 1990s (see
Fig. 3). Perinatal complications accounted for the majority of neonatal deaths in the 1970s. The majority of
deaths in the 1970s were attributed to infectious diseases (respiratory, gastrointestinal, other) and occurred
mainly among infants and children. In contrast, after epidemiological transition stage II, the majority of deaths
American Journal of Physical Anthropology
74
R.M. MALINA ET AL.
TABLE 2. Indicated causes of death by age group and decade
TABLE 2. (Continued)
Decade (number of deaths)
Prior to
health center
1970–79
1980–89
Age group
Neonatal (B-1 mo)
Perinatal
Respiratory
Gastrointestinal
Other infections
Congenital
Subtotal
Postneonatal (1–11 mo)
Respiratory
Gastrointestinal
Other infections
Congenital
Subtotal
1–4 yrs
Respiratory
Gastrointestinal
Other infections
Congenital
Hinchazon
Subtotal
5–14 yrs
Respiratory
Gastrointestinal
Other infections
Hinchazon
Accident
Anemia
Subtotal
15–24 yrs
Respiratory
Gastrointestinal
Other infections
Hinchazon
Childbirth
Accident
Anemia
Subtotal
25–34 yrs
Respiratory
Gastrointestinal
Other infections
Hinchazon
Childbirth
Accident
Cardiovascular
Subtotal
35–44 yrs
Respiratory
Gastrointestinal
Other infections
Hinchazon
Childbirth
Accident
Anemia
Cardiovascular
Diabetes
Cirrhosis
Cancer
Subtotal
45–54 yrs
Respiratory
Gastrointestinal
Other infections
Hinchazon
Accident
Anemia
n
61
2
8
1
2
74
%a
11
n
3
9
7
1
1
21
8
27
10
1
46
17
59
22
4
16
2
1
23
4
11
7
1
1
24
17
46
29
1
7
2
1
1
12
–
3
4
1
1
–
9
2
2
2
–
–
2
8
%a
43
33
17
70
9
58
17
n
1
–
–
1
2
2
3
–
2
7
1
2
1
–
–
4
–
5
1
–
–
–
6
–
1
1
1
1
1
–
5
–
–
1
–
–
–
1
2
–
–
–
–
–
–
–
0
–
–
1
2
–
–
–
3
1
–
1
–
1
–
2
5
1
–
–
–
–
1
–
2
1
–
3
–
1
1
1
1
–
–
–
8
1
1
–
1
–
–
–
1
1
–
1
6
–
1
–
–
–
1
–
–
–
1
–
3
–
1
1
1
–
–
3
2
1
–
–
–
–
–
1
–
–
–
American Journal of Physical Anthropology
Decade (number of deaths)
Prior to
Health
health center
center
1970–79
1980–89
1990–99
Health
center
1990–99
%a
%a
%a
Age group
n
Cardiovascular
Diabetes
Cirrhosis
Other
Subtotal
55–64 yrs
Respiratory
Gastrointestinal
Other infections
Hinchazon
Cardiovascular
Cancer
Other
Subtotal
65–74 yrs
Respiratory
Gastrointestinal
Other infections
Hinchazon
Accident
Cardiovascular
Renal insufficiency
Cirrhosis
Cancer
Other
Subtotal
75–84 yrs
Respiratory
Gastrointestinal
Other infections
Hinchazon
Accident
Anemia
Cardiovascular
Diabetes
Renal insufficiency
Cancer
‘‘Old age’’
Subtotal
851 yrs
Respiratory
Gastrointestinal
Other infections
Hinchazon
Accident
Anemia
Cardiovascular
Renal insufficiency
‘‘Old age’’
Subtotal
Grand total
–
–
–
1b
4
1
–
1
–
8
–
1
1
–
3
–
2
3
2
1
–
–
8
–
1
1
1
1
–
–
4
3
1
–
–
3
1
1c
9
1
2
–
4
–
3
–
–
2
1c
13
3
–
–
–
1
8
3
2
1
–
18
1
7
3
5
1
1
–
–
–
1b
19
–
7
3
3
–
–
1
1
–
1
–
16
–
5
1
2
–
1
–
–
–
9
225
37
44
56
n
2
4
2
–
1
1
11
–
2
3
4
30
1
3
–
3
–
–
7
–
5
19
151
13
37
37
n
%a
44
4
4
2
–
–
–
10
–
4
1
2
27
15
15
5
1
–
–
–
–
9
2
5
22
103
23
37
15
41
a
Percentages refer to deaths in the age group by decade, broken
down by whether or not the village health center is present.
Hemorrhage.
c
Strangulated hernia.
b
in the 1990s occurred among adults and was due to
degenerative conditions usually associated with aging
(Table 2). Importantly, this transition which occurred
over a 1001 year period in Europe (Barrett et al., 1998)
occurred over a two or three decade interval in the study
community (Table 5).
75
EPIDEMIOLOGIC TRANSITION IN AN ISOLATED ZAPOTEC COMMUNITY
TABLE 3. Frequencies of deaths during the dry season (October–April) and rainy season (May–September) by age group within
decade and for the total interval 1970–1999
Frequencies
Age group
1970s
Neonates
1 mo–4 yrs
5–14 yrs
15–64 yrs
651 yrs
Total
1980s
Neonates
1 mo–4 yrs
5–14 yrs
15–64%
651 yrs
Total
1990s
Neonates
1 mo–4 yrs
5–14 yrs
15–64 yrs
651 yrs
Total
1970–1999
Neonates
1 mo–4 yrs
5–14 yrs
15–64 yrs
651 yrs
Total
Total
Dry
Rain
% Rainy seasona
ORb 0.95 CI
P-valuec
74
70
9
28
44
225
43
29
6
21
17
116
31
41
3
7
27
109
41.9%
58.6%
33.3%
25.0%e
61.4%
48.4%
2.2 (0.8–6.4)
4.2 (1.5–12.8)
1.5 (0.2–9.9)
–
4.8 (1.5–15.7)
–
NS (0.12)
0.003
NS (0.62)d
21
35
8
25
62
151
14
14
5
12
30
75
7
21
3
13
32
76
33.3%
60.0%
37.5%
52.0%e
51.6%
50.3%
0.2 (0.1–1.8)
1.4 (0.4–4.4)
0.6 (0.1–3.4)
–
1.0 (0.4–1.6)
–
NS (0.20)
NS (0.54)
NS (0.48)d
2
11
6
17
67
103
1
3
3
13
36
56
1
8
3
4
31
47
50.0%
72.7%
50.0%
23.5%e
46.3%
45.6%
3.3 (0.0–163.6)
8.7 (1.2–7.8)
3.3 (0.3–36.4)
–
2.8 (0.7–11.4)
–
NS (0.42)d
0.01d
NS (0.23)d
97
116
23
70
173
479
58
46
14
46
83
247
39
70
9
24
90
232
40.2%
60.3%
39.1%
34.3%e
52.0%
48.4%
1.3 (0.7–2.6)
2.9 (1.5–5.7)
1.2 (0.4–3.6)
–
2.1 (1.1–3.9)
–
NS (0.44)
0.0006
NS (0.67)
0.003
NS (0.97)
NS (0.09)
0.01
a
Percentage of deaths during the rainy season.
Odds ratio.
c
Chi-square or Fisher’s Exact test, where appropriate.
d
Fisher’s Exact test.
e
Reference group.
b
The pattern noted in the indigenous community from
1970 to 1999 is similar to that noted in other areas of
the world which have experienced a secular decline in
mortality. During the secular decrease in mortality, ages
at death and causes of mortality shift (Demetrius, 1989),
although data on age-specific mortality and causes of
death are often incomplete and limit analyses (Folger,
2004). In the study community, total mortality has
decreased over time (Little et al., 2008). The secular pattern has two aspects related to age and cause of death,
respectively: childhood mortality as a proportion of total
mortality decreases while mortality among those 651
years as a proportion of total mortality increases; and
causes of death tend to shift from infectious diseases
(with periodic epidemics) to degenerative diseases that
occur with aging (Alfonso-Sanchez et al., 2004). In contrast to the relatively rapid change in the community
under study, secular changes in mortality are usually
more gradual, occurring over 100 to 200 years, perhaps
reflecting the complex synergistic interaction of chronic
undernutrition and a high infectious disease load
(Folger, 2004).
The recent and relatively rapid shift in mortality in
the Zapotec community is perhaps more apparent when
the Etla data are combined with corresponding data for
another Zapotec community in the Tlacolula branch of
the Valley of Oaxaca, about 28 km southeast of the city
of Oaxaca, studied in the early 1970s (Malina and
Himes, 1977a,b, 1978). The Tlacolula community had a
population of 1,703 individuals in 1970 (Secretaria de
Industria y Comercio, 1971) which was slightly larger
than the community under study (1,423 individuals in
1970). Though located at opposite ends of the Valley of
Oaxaca, the two communities are generally similar in
subsistence (agriculture), diet and structure (endogamous), and growth status of school children (Malina and
Himes, 1978; Malina et al., 1981). Birth and death
records for the Tlacolula community for the interval
1945 through 1970 were evaluated in a manner similar
to the present study. Trends in mortality for the two
communities in the Valley of Oaxaca (Etla and Tlacolula)
are summarized in Table 4, providing a view of two indigenous Zapotec communities that spans approximately
55 years, 1945–1999. Relative mortality among children
\5 years of age was reasonably stable from the 1940s to
the 1970s and then declined (see Fig. 4), while mortality
among school age children 5–14 years of age was stable
across time (Table 4). Relative mortality among individuals 651 years was also stable through the 1960s,
increased slightly in the 1970s, but increased dramatically in the 1980s and 1990s (see Fig. 4).
High mortality among children 1–4 years of age is a
generally accepted indicator of chronic undernutrition in
a community (Wills and Waterlow, 1958). Estimated mortality in children 1–4 years in the Zapotec community
was highest in the 1970s, declined somewhat in the
1980s but decreased markedly in the 1990s (Table 1).
Note the estimated rates were expressed per 1000 live
born infants because annual census information was not
available. Overall, the decline in mortality among chilAmerican Journal of Physical Anthropology
76
R.M. MALINA ET AL.
TABLE 4. Deaths in specific age groups as a percentage of total deaths within intervals from 1945 to 1999 in two rural
Zapotec-speaking (Etla and Tlacolula) communities in the Valley of Oaxacaa
Years
Age group
1945–1949
1950–1959
1960–1969
1970–1979
1980–1989
1990–1999
\1
1–4
\5
5–14
15–24
25–34
35–44
45–54
55–64
65–74
751
65
23.8
32.9
56.7
4.2
2.1
5.6
8.4
4.9
5.6
3.5
8.4
11.9
31.7
24.3
56.0
4.4
3.2
5.6
3.2
6.1
6.6
5.1
9.5
14.6
22.9
30.8
53.7
6.4
3.7
8.2
4.0
4.0
4.0
7.3
8.5
15.8
53.3
10.7
64.0
4.0
2.2
1.3
3.6
1.8
3.6
8.4
11.1
19.5
29.1
7.9
37.0
5.3
1.3
3.3
4.0
5.3
2.6
8.6
32.5
41.1
8.7
3.9
12.6
5.8
0
1.9
2.9
2.9
8.7
17.5
47.6
64.1
a
Data for 1945–1969 are from Malina and Himes (1977b, 1978).
dren \5 years suggests improving nutritional conditions
over the 30-year interval beginning in the 1980s and
continuing into the 1990s.
Gastrointestinal conditions, especially diarrhea, were
indicated as the major cause of death in postneonatal
infants and children 1–4 years of age in the 1970s and
1980s (Table 2). Other infections, specifically measles in
the 1970s, were the second major cause of death at these
ages. As noted, causes of death were derived from nonmedically certified records, especially for the 1970s and
early 1980s. The reported cause of death given at the
time of registration was probably the most prominent
symptom, for example, diarrhea, measles rash, coughing,
and so on. Symptoms, of course, are complicated. Diarrhea, for example, occurs frequently with measles, particularly before and during the appearance of the rash
(Scrimshaw et al., 1966). Diarrhea and measles are associated with malnutrition, but symptoms of undernutrition per se are not ordinarily the most prominent at the
time of death and thus are seldom reported. However,
approximately 50% of deaths among preschool children
reported as due to infectious and parasitic diseases have
nutritional deficiency as an associated cause (Puffer and
Serrano, 1973). Of relevance, diarrheal diseases and
measles were the principal infectious disease-related
causes of death.
Hinchazon, a generic term that refers to swelling, was
indicated as the cause of death for 28 individuals in the
1970s and early 1980s, 14% of the deaths from 1970
through 1984. Individuals ranged in age from 3 to 851
years. It was the indicated cause for females (n = 17)
more often than males (n = 11) and among individuals
60+ years of age (19 of 28, 68%). Only three cases were
children 3–6 years, while the remainder was between 16
and 55 years of age.
The generic nature of the term hinchazon makes it difficult to relate it to specific conditions that contributed
more directly to mortality. The meaning of the term may
vary with age and sex. Among young children, it likely
reflects compromised nutritional status which is often
accompanied by edema. The term was also used in association with diarrhea in three adults in the community
(30, 70, 73 years) and may reflect abdominal swelling
with severe gastroenteritis. A recent news report in
Oaxaca included hinchazon with kidney malfunction,
edema, proteinuria, and hypertension during late pregnancy, subsiding soon after childbirth (Salanueva
American Journal of Physical Anthropology
Camargo, 2006). In clinical obstetrics, these symptoms
are consistent with pre-eclampsia, or eclampsia. Three
cases of hinchazon in the Zapotec community were in
females of reproductive age (16, 30, 43 years), two in the
1970s and one in the early 1980s.
Significantly higher mortality during the rainy season
remained apparent in the 1990s, affecting the young
(1 month to 4 years) and the elderly (651 years), but the
absolute magnitude of mortality decreased markedly
since the 1970s (Table 3). Across all years for which
causes of death were noted (1970–1999), 61% of deaths
attributed to gastrointestinal conditions (72 of 119) and
56% of deaths attributed to other infectious diseases (30
of 54) in individuals 1 month of age and older occurred
during the rainy season.
The shift in causes (Table 2), age-associated (see Fig.
3), and temporal patterns (Fig. 4 and Table 4) of mortality occurred concomitantly with major secular change in
size and maturity in the community (Malina et al.,
2004a,b). Surveys of growth status of school children 6–
14 years in 1968 and 1978 indicated no change over the
decade (Malina et al., 1980). Health and nutritional conditions in the birth years of the 1978 sample (1964–
1972) and years of their early growth were not apparently sufficient to support a secular increase. This was
reflected in the elevated preschool mortality during the
1970s, especially mortality associated with gastrointestinal (diarrheal) and infectious (measles) diseases (Table
2), which suggested marginal health and nutritional circumstances, especially during the rainy season. However, significant gains in height were found among primary school children 6–13 years in 2000 (6 cm in boys
and girls) and secondary school children 12–17 in 2002
(6 cm among boys, 3 cm in girls). Young adult males
and females 19–29 years of age showed smaller secular
gains in height between 1978 and 2000, 3 cm and 2
cm, respectively (Malina et al., 2004a). In addition, median age at menarche (probit estimates) declined by 1.8
years, from 14.8 years in 1978 to 13.0 years in 2000
(Malina et al., 2004b). The birth years of the recent
school children (1985–1994) and the years of their early
growth, as well as the adolescent years of young adults
(1980–1990) coincide with the dramatic reduction in
infant and preschool mortality in the community (Tables
1 and 2). Further, over the interval from 1978 to 2000,
the prevalence of growth stunting among primary school
children 6–13 years in the community declined from 76
EPIDEMIOLOGIC TRANSITION IN AN ISOLATED ZAPOTEC COMMUNITY
to 29%. It is reasonable to assume that health and nutritional conditions in the community were dramatically
improved during the interval of rapid linear growth during the preschool years.
The secular decline in infant and preschool mortality
during the 1970s and 1980s and secular gains in height
between 1978 and 2000 should be viewed in the context
of changes in the community during this interval.
Reduced mortality and enhanced growth suggest that
health and nutritional conditions and associated factors
improved over time in the community. As noted, there
was no health center in the community in the late
1960s. The community had no doctor at the time of the
1978 survey but a public health nurse visited the community once per week and a mid-wife with some public
health experience lived in the community. The public
health nurse worked mostly with children and young
mothers. The current health center dates to 1991 and is
apparently used on a regular basis by community residents. Records of use of the medical center were not
available to us for earlier years; however, about 85% of
the population used the official medical services in 2000
and 2001 (Reyes Castellanos et al., 2000; Martinez-Julian et al., 2001). Health center reports also provide
insights into current morbidity and services provided to
community residents. Acute respiratory infections and
intestinal amebiasis (dysentery) were the principal
causes of morbidity in the community between 1992 and
2000 (Altamirano, 1999; Reyes Castellanos et al., 2000).
Gastrointestinal problems were compounded by 89 cases
of shigellosis in 1998 (Altamirano, 1999) while 66 cases
of mild and moderate malnutrition were noted in 2000
(Reyes Castellanos et al., 2000). Burning of waste materials and smoke from kitchens (wood and charcoal are
major fuels for cooking) are likely implicated in respiratory complications and perhaps asthma (10 cases were
reported in 2000), while problems with drainage and
lack of sanitary food and water are major factors in gastrointestinal infections. Significantly elevated mortality
rates among the young and elderly during the rainy season reflect the problems with disinfection of water and
food (Table 3).
The relative predominance of individuals 651 years of
age in mortality records for the 1990s is suggested in
some of the conditions treated at the health center. In
addition to 80 cases of rheumatic infirmities, a large
number of adult and elderly individuals were examined
for diabetes mellitus (n 5 116) and hypertension (n 5
546) in 2000. Four new cases of diabetes were identified,
12 were under control and 13 were being treated; corresponding numbers for hypertension were 9 new cases, 13
cases under control and 15 cases under treatment (Reyes
Castellanos et al., 2000). The primary causes of mortality in the 1990s (Table 2) and recent health center statistics indicate the presence of degenerative conditions in
the adult and elderly population of the community.
Nutritional status was marginal in the 1960s with
estimated energy and protein intakes based on household surveys considerably below recommendations for
Mexico (Amdurer, 1978). This was consistent with the
relatively poor nutritional status that characterized the
rural south of Mexico including the state of Oaxaca in
the 1960s and 1970s (Perez Hidalgo et al., 1970, 1973;
Muñoz de Chavez et al., 1976). There was also a high
prevalence of stunting in children 1–5 years of age in
the region in the 1970s, 64% in 1974, and 56% in 1979
(Saucedo Arteaga et al., 2001). Among school children 6–
77
13 years of age in the study community, the prevalence
of stunting was 71 and 76% in 1968 and 1978, respectively, and the lack of change in growth status of school
children between 1968 and 1978 suggested persistence of
marginal health and nutritional conditions (Malina et
al., 1980). Comparison of foods consumed at the household level in 1968 and 1978 indicated little variety, limited sources of animal protein, and dependence upon
corn in the form of tortillas, beans, and salsa (Peña
Reyes et al., 1995). Household surveys in 2000 indicated
greater variety in diet. Corn in the form of tortillas,
beans, and salsa were still the main staples, but consumption of animal protein in the form of beef, cheese,
and eggs was reported by about 15% of the households
and consumption of tortillas was reported less often in
2000 than in 1978. This may suggest that the quality of
the diet recently improved (Table 6).
Improvements in housing, potable water, sanitation,
and personal hygiene probably contributed to a reduced
infectious and parasitic disease load. About 82% of the
houses were constructed of adobe in 1978, while the remainder was constructed of bamboo and other materials.
The houses typically had earthen floors (Buschang,
1980). Housing in 2000 indicated the following: walls
made of concrete or brick (53%), adobe (40%), and wood
and other materials (7%); roofs made of tile (42%), concrete (44%), and laminated board (12%); and cement or
concrete floors in the majority (66%) (Martinez-Julian
et al., 2001).
Potable water and sanitary facilities were generally
limited in the 1960s and 1970s. Two rivers that join each
other at about 500 m from the village are the primary
source of water, but the rivers often lacked water for a
good part of the year, except for the rainy season (May
to September). Piped water was available to 135 of 247
households (55%) in the 1970 census (Secretaria de
Industria y Comercio, 1971) and to 147 of 325 households (45%) in the 1980 census (INEGI, 1984). The relative decline likely reflected population growth over the
decade, 1,423 to 1,823 individuals, and new construction
on the periphery of the community. The situation
improved through the 1980s; 256 of 352 households had
piped water in the 1990 census (INEGI, 1991). A storage
unit for potable water obtained from deep wells now is
located about 500 m north of the community. Health center reports (Altamirano, 1999; Reyes Castellanos et al.,
2000; Martinez Julian et al., 2001) indicated the following recent trends: potable water was available for 89% of
households in 1998, 95% in 2000, and 98% in 2001;
latrines were available for 32% of households in 1998,
39% in 2000, and 47% in 2001; and septic tanks
increased from 15% in 1998 and 2000 to 17% in 2001.
Although the availability of sanitary facilities has
reduced the amount of open ground used for human
excrement, a significant portion of land area used for
excrement is in open areas with associated opportunity
for spread of disease and contamination.
Educational level in the community has also improved
from the 1970s through 2000. In the 1970s, only 35% of
the population over 15 years had completed 1–6 years of
school (primary school of 6 years is required by federal
law). In the 2000 census, 41% of individuals \18 years
completed 6 years of primary school and about 37% completed secondary school. Among individuals 18 years,
7% completed high school and 4% had some college education (INEGI, 2000, 2002). Only 6% of the population
was described as illiterate in 1999–2001.
American Journal of Physical Anthropology
American Journal of Physical Anthropology
Full secular increase
0.6
c
b
a
1991–1994
6–9 yrs
Adapted from Malina et al. (1983, 2004a).
Adapted from Malina et al. (1983, 2004b).
Omran (1971, 1983) and Barrett et al. (1998).
d
Adapted from Little et al. (2008).
6.4
0.7
1987–1990
10–13 yrs
6.1
1.0
6.7
0.9
1983–1987
13–17 yrs
6.6
0.9
3.3
1.4
1971–1981
19–29 yrs
6.2
–
Stage II, transition in
progress
Stage II, complete
degenerative disease
dominates mortality
–
13.0 yrs
13.9 yrs
Incipient secular
increase in size
Transitional secular
increase in size
Full secular increase
1.2
2.0
1.2
1955–1970
45–30 yrs
3.1
14.9 yrs
No change
–
0.0
–
1900–1954
100–46 yrs
0.0
Stage I, no sign of
change
Stage II, incipient
Stage I, high birth and
mortality rates
Stage II, mortality rate
decreases, birth rate
remains high
Stage II, 15–25 yrs
after transition
Stage II, 28–32 yrs
after transition
Stage II, 32–35 yrs
after transition
Stage II, 36–39 yrs
after transition
Stage I, High infectious
disease mortality
Stage I
15.0–15.4 yrs
No change
–
0.0
–
SE
Mean
SE
Mean
0.0
Epidemiological
transitionc
Secular
decrease in age
at menarcheb
Secular increase
in size stagea
Females
Males
Birth
years
Age
cohort
Secular gains in
stature (cm)
Out-migration is relatively common. The primary
motivation is economic. A health center survey in 1998
indicated 93 emigrants, while household interviews during 1999–2000 indicated 98 migrants. The destination of
the migrants was primarily Mexico City (60%), with a
smaller proportion going to the United States (30%).
Statistics for 2000 indicated about 4 million undocumented workers from Mexico in the United States, and
these migrant workers sent remittances equaling 12 billion dollars US back to Mexico (Authers and Dinmore,
2003). Using these data it is possible to estimate that
approximately $3000 US per migrant worker in 2000
was sent home to Mexico. If 30 emigrants from the community were in the United States and remitted the average amount, this would be a total remittance of $90,000
US per year. If 60 emigrants were in the Federal District
of Mexico and sent back the equivalent of $500.00 US,
this would be a total remittance of $30,000 US per year.
Overall, this would be $120,000 US per year flowing
back to the community (Malina et al., 2004a). These estimates take on added meaning when placed in the context of estimated family income. At the time of the study
in 2000, the daily minimum wage or minimum salary
was about 34.5 pesos for Mexico City and 30.0 pesos for
the state of Oaxaca, which corresponded, respectively, to
about 1035 pesos ($113 US) and 900 pesos ($96 US) per
month. An average salary of two times the minimum
wage is considered necessary to satisfy basic family
needs (INEGI, 2000). A large proportion of families in
the community had no income or had incomes 1 time
the minimum wage, 86, 84, and 65% in 1999, 2000, and
2001, respectively. Income 2 times the minimum wage
was present in 14, 15, and 35% of the families in 1999,
2000, and 2001, respectively (Altamirano, 1999; Reyes
Castellanos et al., 2000; Martinez-Julian et al., 2001).
Families vary in stage of the economic cycle associated
with migration which influences the flow of capital.
Occupational mobility alters family structure and
responsibilities within households so that women, children, and older members often undertake essential subsistence tasks during absence of the male head. Funds
received from family members also have an influence
beyond the immediate recipient families. In addition to
improving living conditions for the families, a portion of
the funds are used for community infrastructure and development, i.e., sanitary facilities, health and social programs, and schools. This reflects the concept of overhead
capital (Youngson, 1967), the network of social relationships which transcends the nuclear family and which
permits access to resources (funds, political, information)
for local improvement and development, i.e., for more
general social benefit.
Although the precise changes that have contributed
to the secular shift in age cohort-specific mortality in
the rural Zapotec community are difficult to specify,
data suggest that overall health, nutritional, and living
conditions have improved over the past 10–20 years.
The improvements were apparently sufficient to contribute to a major decline in and age-pattern shift of
mortality.
In a prior investigation in this community we reported
that circa 1955 high birth rates diverged from lower
mortality rates which implied better health and nutritional conditions in Stage II of the demographic transition. Increased growth status begins 15-to-25 years
(about one generation) after the demographic transition
to Stage II (Little et al., 2008). Mortality continued to
Demographic
transitiond
R.M. MALINA ET AL.
TABLE 5. Age-adjusted secular gains in stature, decrease in age at menarche, and epidemiological and demographic transitions in the study community
78
79
EPIDEMIOLOGIC TRANSITION IN AN ISOLATED ZAPOTEC COMMUNITY
a
TABLE 6. Comparison across time of 10 foods consumed most frequently: Household recall data
1968 (n 5 39)
Foods
1978 (n 5 175)
2000 (n 5 167)
Percentage
Foods
Percentage
Breakfast (Almuerzo)
1. Tortillasb
2. Black coffee
3. Salsa
4. Beans
5. Atole (gruel)
6. Carne de res
7. Chile
8. Herbs
9. Bread
10. Eggs
97%
67%
62%
21%
8%
8%
8%
8%
5%
5%
Tortillasb
Salsa
Black coffee
Beans
Bread
Eggs
Atole (gruel)
Chapulines (grasshoppers)
Tasajo (dry meat)
Water
100%
81%
77%
53%
29%
16%
16%
15%
11%
9%
Lunch (Comida)
1. Tortillasb
2. Salsa
3. Beans
4. Nopales (cactus)
5. Coffee
6. Dulces (pastries)
7. Chile
8. Plátano
9. Water
10. Beef
97%
64%
23%
21%
16%
10%
8%
8%
5%
5%
Tortillasb
Salsa
Beans
Soft-drinks
Coffee
Bread
Nopales (cactus)
Eggs
Tasajo (dry meat)
Orange
Dinner (Cena)
1. Tortillasb
2. Black coffee
3. Salsa
4. Beans
5. Bread
6. Nopales (cactus)
7. Soft drinks
8. Rice
9. Chile
10.–
85%
56%
23%
21%
8%
8%
5%
5%
5%
–
Tortillasb
Coffee
Salsa
Beans
Bread
Water
Eggs
Tesajo (dry meat)
Chapulines (grasshoppers)
Beef
a
b
c
Foods
Percentage
Tortillasc
Beans
Atole (gruel)
Black coffee
Bread
Water
Eggs
Salsa
Soft-drinks
Cheese
50%
35%
35%
25%
21%
17%
16%
15%
14%
11%
97%
72%
56%
26%
20%
19%
15%
11%
10%
10%
Tortillasc
Water
Beans
Soft-drinks
Beef
Eggs
Nopales (cactus)
Cheese
Salsa
Pasta soup
62%
48%
44%
36%
15%
15%
15%
14%
11%
10%
84%
56%
49%
30%
30%
14%
12%
12%
7%
6%
Tortillasc
Coffee w/ milk
Bread
Water
Beans
Soft drinks
Beef
Cheese
Atole (gruel)
Nopales (cactus)
15%
13%
11%
8%
8%
6%
5%
5%
5%
4%
Adapted from Little et al., 2006.
Maize was stone ground using mano and metate.
Maize was machine ground.
decrease at a rapid rate after 1955, indicating continuing
improvement of conditions in the community until some
critical threshold of improved nutrition and health was
reached in the 1980s resulting in moderately increased
growth status among the cohort born in the 1970s and
1980s. Greater gains in the growth status were observed
in the cohort born in the 1990s when mortality rates
decreased and the epidemiologic transition from high
childhood mortality from infectious disease to the elderly
mortality from degenerative disease occurred. Therefore,
changes in mortality rates and patterns are leading indicators associated with the onset of the secular increase in
child growth (and eventual adult height), and the progression of the incipient secular trend (2–3 cm) to a ‘‘full
blown’’ generational increase in height (6 cm).
The unique finding in this report is that the epidemiologic transition from Stage I to Stage II is predictive of
the onset of the secular trend, demonstrating an almost
‘‘dose-response’’ effect of the age shift in mortality (Table
5). Notably, the epidemiologic transition began the decade
(1980) before the health center attended by a physician
was established in the community. Nutrition changed
somewhat, with the major changes being a transition
from stone ground to machine-milled maize tortillas and
increased consumption of beef, cheese, and perhaps soft
drinks (Table 6). While public health interventions such
as the health center seem to be associated with the secular trend, the signal that seems most strongly associated
is the epidemiologic transition, which began the decade
before the health center was established. While the demographic transition to Stage II is a leading indicator (timelagged predictor) of the secular increase in size, the epidemiologic transition analyzed in the present investigation
is a predictor of the secular trend. These transitions are
signals of improved health and nutritional conditions in
the study community. The apparent response to the epidemiologic transition signal is incipiently increased growth
of school children during the transition and a ‘‘full blown’’
secular increase in child growth when the epidemiologic
transition is complete. Notably, in this anthropological
population the epidemiologic transition spanned two-tothree decades, in contrast to much longer times in 19th
and 20th century Europe.
In summary, improved health and nutritional conditions from 1970 to 1999 have resulted in 1) decreased
overall mortality, 2) markedly decreased mortality
among infants and children, and 3) a shift in the preponderance of mortality, from the very young in the 1970s
to the elderly in the 1990s. This is a classic demographic
pattern of response, epidemiologic transition, to improved conditions observed in a closed population over
30 years of investigation. Moreover, the changes are
American Journal of Physical Anthropology
80
R.M. MALINA ET AL.
associated with significant secular changes in body size
among children, adolescents, and young adults.
ACKNOWLEDGMENTS
The guidance and assistance of Professors Henry A.
Selby of the University of Texas at Austin and Peter H.
Buschang of the Texas A & M University System Health
Sciences Center at Dallas during the field phases of the
project are graciously recognized and appreciated. We
also thank Ann Pawlak for editorial assistance and John
Millet for assistance with the map and figures.
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