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CHAPTER 1: INTRODUCTION
Biological anthropologists are presented with the unique ability to analyze human
skeletal remains to address questions of health, nutrition, environmental stress, disease,
and mortality in past populations. Historic skeletal collections present a wealth of data to
their reviewers: sex, age, health, origin, economic success, and diet. Ethnographic and
historical accounts provide a poignant perspective of many aspects of past cultures, but
often focus on certain subsets of the population or specific events. Analysis of skeletal
remains enables researchers to reconstruct or verify accounts in prehistory and shed light
on questions not yet answered.
To reconstruct the health and demographic patterns of a past population is no easy
task. However, sub-fields in biological anthropology attempt just that. Paleodemography
is the study of the population structure and dynamics of past cultures through the lens of
sex and age-at-death information. In compliment, paleopathology is the study of diseases
and indicators of poor health that can be identified in individual skeletons. Similarly,
paleoepidemiology is the study of population level interaction with illness using disease
and health indicators within and across entire skeletal assemblages. Collectively, these
sub-disciplines have allowed researchers to produce a comprehensive review of the
relationship between individuals and their culture, environment, health, disease, and
mortality. The field of paleopathology is not without interdisciplinary theoretical and
methodological debate. Interpretation of health from skeletal remains often generates as
many questions as are answered.
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Many pathological conditions have endures interdisciplinary debate. For example,
anemia is a condition that may arise from a variety of etiologies. A condition
characterized by a lack of iron in the blood, anemia may result from nutritional
deficiencies, congenital inheritance, or an excessive parasite load (Walker et al. 2009).
More recent research suggests anemia should be viewed as a symptom of a larger issue
rather than the end of the diagnosis (Holland and O'Brien 1997; Stuart-Macadam 1987a).
Overall, anemia is a condition that has afflicted populations for generations across varied
subsistence strategies, socioeconomic status, and geographic origin.
Osteologically, an anemic individual is identified by the presence of porotic
hyperostosis and cribra orbitalia. In a clinical setting, anemia may suggest broader
medical issues. The lack of iron in the blood affects the form and function of the red
blood cells and subsequently creates an expansion of diploë along the external table of
the cranial vault and the eye orbits (Ortner 2003).
The link between porotic hyperostosis and cribra orbitalia has been debated with
varied results as to each sample used. Porotic hyperostosis studies have explored links to
stress, diet, and parasitism (Holland and O'Brien 1997; Stuart-Macadam 1985; Walker
1986) and studies of cribra orbitalia studies have also explored these causes (Walker et al.
2009; Wapler et al. 2004). Techniques ranging from macroscopic to microscopic, cross
sectioning and DNA sampling have been explored in the analysis of these cranial lesions.
Research has caught the interest of clinical, forensic, and bioarchaeological studies alike
and investigations into the correlation between these lesions and temporal change have
given insight into how to diagnose and view health at the population level.
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Pathologies related to dietary deficiencies, such as porotic hyperostosis, emerge as
a result of a weakened immune system but are driven by several etiologies. In a 1992
study, Stuart-Macadam confirmed iron deficiency anemia, the associated physiological
affects, and the adaptive response. Wood et al. (1992) demonstrate that traditional
methods for determining the health of a population from human skeletal remains can
produce conflicting estimates. Stuart-Macadam (2006) suggests iron deficiency anemia is
not necessarily a disease but a symptom underlying a greater condition. Iron metabolism
is a complex process with a number of contributing factors, including status, diet,
physiology, and genetics. Therefore, anemia could be considered an adaptive response to
disease or infection. In this model, the body’s automated reduction in blood iron content
is designed to repel iron-hungry parasites.
1.1 Osteological Paradox
There is debate as to whether the presence of skeletal lesions is uniformly
expressed across populations. In the Osteological Paradox, Wood et al. (1992) highlight
that there are inherent problems in inferring past health from skeletal samples in the
archaeological record. There is a belief that there should be a correlation between the
disease we see in burials and the prevalence of said disease in past populations. The use
of a known demographic sample helps alleviate unknowns encountered in archaeological
samples.
However, this conclusion fails to account for selective mortality and hidden
heterogeneity. As defined by Wood et al. (1992), selective mortality refers to the
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unearthed sample only representing a portion of the greater whole, therefore data would
not inform all individuals at risk for the disease, or those who suffered from it, but only
those who succumbed to the disease within specific age cohorts. It is only possible to
infer health from individuals whose remains have survived in the archaeological record.
Hidden heterogeneity refers to the idea that past populations were composed of a mixture
of individuals with varied susceptibility to infection, whereby individuals may have been
infected but died before skeletal lesions could develop. Increased vulnerability could be
due to a host of factors: genetics, socioeconomic factors, or stressors associated with the
temporal period that an individual lived. Under this convention, some skeletons with
lesions may have been the healthier subset of the population during life because they
were able to survive the lesion-causing event before death (Wood et al. 1992). These
issues highlight that if an event or catalyst of similar force affected two populations,
evidence of that force may present differently by population. Some researchers suggest
variation in lesion patterns within populations should be minimal, and age-specific
mortality rates are comparable across populations suggesting lesions would always
indicate poor health (Goodman 1993).
Convention assumes that the average infant is at a high risk of death in early years
but risk declines steadily with age. This interpretation ignores life hazards not pertaining
to diarrheal disease or breast milk supply. Under current models of paleodemography and
paleopathology hazards are aggregated when some hazards far exceed others in
likelihood of impact (Wood et al. 1992). Populations should be cautiously compared if
their distributions of risk and mortality hazards are divergent.
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On morbidity, Wood et al. (1992) illustrate how the concept of health is arbitrary.
It is important to distinguish between healed and inactive lesions on the skeleton to
enhance the understanding of biological response to disease. Perception of morbidity is
likely much different than actual morbidity.
In essence, skeletal lesions represent only a portion of afflicted individuals in a
population and some individuals will display a greater propensity for lesion development
than others (Wood et al. 1992). If the parasite model is valid (Stuart-Macadam 2006), and
agricultural women and children suffer from iron deficiency for the same reasons as
people of the industrialized world, then analysis could conclude that anemic prehistoric
individuals were among the healthiest members of their communities. In theory, a
hypoferremic state protects the individual’s immune system from a variety of additional
pathological insults. Stuart-Macadam (2006) explains that even in anemia brought on by
parasitic infection, the severity is the product of at least three factors: the iron content of
the host’s diet, the host’s stored iron reserves, and, the intensity and duration of the
infection. When demographic data is absent and/or sparsely represented in archaeological
collections, it is difficult to confirm relationships between human life expectancy and
health status of a population when a propensity for anemia can be related to gene flow,
environmental selection (parasitism), and social selection.
The state of research in skeletal biology necessitates continued theoretical
expansion into issues of hidden risk, individual frailty, mortality, and pathological
processes. Publications continue to mount in support of, and seeking to delineate, the
variable expression of pathological processes, subsequent implications for a broader
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understanding of disease in prehistory, and to better understand transmission and
prevalence in modern society. Analysis of stress on the living that is known to impact the
skeleton and is visible in the deceased is a way in which this risk relationship can be
explored. Examining the remains of individuals of known demographic data can verify
the implications of pathological expression and underscores the importance of
demographic data in paleopathology (Wood et al. 1992).
1.2 Statement of Problem
Osteology is a sample driven science, where the scientific potential is enhanced
by the breadth of the population represented. Bioarchaeologists have documented porotic
hyperostosis and cribra orbitalia in both prehistoric and historic contexts worldwide and
commonly use both conditions to assess health and nutritional status on a population
scale (Armelagos and Cohen 1984; El-Najjar et al. 1975; El-Najjar and Robertson 1976;
El-Najjar et al. 1976; Mittler and Van Gerven 1994; Pechenkina et al. 2002; Steckel and
Rose 2002; Walker 1985; Walker 1986; Zaino and Zaino 1975). Since mid-century, iron
deficiency has been the widely held explanation for incidence of cranial lesions. Modern
clinical studies of iron-deficiency anemia (Kent et al. 1994) and radiographic evidence
for cranial vault marrow hypertrophy (e.g., changes in diploë) support these data (StuartMacadam 1987b). Epidemiological studies have also been used in support of porotic
hyperostosis and cribra orbitalia as responses of iron-deficiency anemia (Cook 1990).
More recent studies suggest these cranial lesions have a more complicated etiology
beyond iron deficiency, to include megaloblastic anemia (Walker et al. 2009). Regardless
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of a unifying catalyst, porotic hyperostosis and cribra orbitalia appear as correlated
indicators in the skeletons of individuals who have endured compromised conditions
whether they be tied to nutrition, sanitation, or infectious disease. Under this
interpretation anemia is seen as a pathological symptom not an isolated disease.
This particular study explores incidence of porotic hyperostosis and cribra
orbitalia in an attempt to verify the connection between skeletal stress and anemia. The
project tests a large historic population of Portuguese to identify incidence of porotic
hyperostosis and cribra orbitalia during a period of documented social, environmental,
and economic disparity (Cardoso 2006). The macroscopic scoring methods for porotic
hyperostosis and cribra orbitalia identified by the Global Health History Project (GHHP)
(Steckel et al. 2006) are duplicated so as to contribute to standardized data collection
efforts in the field of skeletal biology. In sum, this study explores the incidence and
prevalence of porotic hyperostosis and cribra orbitalia as an indicator of population health
within a Portuguese sample with known demographic data.
Most diseases do not directly impact the skeleton, or, only do so after afflicting
the individual for a prolonged period of time. As a result, disease may not be evident
from singular review of skeletal material. A skeletal sample may not show any markers
of disease, or those who do display lesions may represent individuals who survived with
the disease long enough for skeletal impact to occur. In line with the osteological
paradox, hidden heterogeneity in risk and selective mortality are factors that may explain
the conflicting interpretations derived from skeletal data (Wood et al. 1992). To address
these issues, a model of analysis outlined by Wood et al. (1992) will be utilized to
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maximize understanding of the mortality relationship between porotic hyperostosis,
cribra orbitalia and age-at-death. The model of analysis applies an age specific hazards
function in order to find corresponding functions in subpopulations that inform nonstationarity, selective mortality, and individual heterogeneity in the risk of death and
disease.
The reason for conducting a study into the macroscopic prevalence of cranial
lesions and their applicability to diagnoses of anemia is three-fold: 1) to document
presence and severity in a population exposed to periods of significant stress, 2) to verify
the claims within the bioarchaeological community that porotic hyperostosis and cribra
orbitalia can be viewed as a sign of population adaptation to adverse conditions, and
lastly 3) to document cranial lesions using methods that are easily repeatable in
subsequent studies. Comparing a record of cranial lesions to known demographic and
health data will allow for a better understanding of the social, economic, and
environmental stresses endured by this historic population.
This study examines the practicality of using iron deficiency anemia as a tool for
bioarchaeological analysis of status, health, sanitation, and genetic robusticity, while
identifying corollaries between health, diet, lifestyle, and geography in the prevalence of
porotic hyperostosis and cribra orbitalia as related to iron deficiency anemia. The Bocage
collection in Lisbon is an ideal sample in which to examine porotic hyperostosis and
cribra orbitalia given the composition, preservation, and breadth of demographic data.
This information tells us more about populations in transition and gives insight into the
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preservation and understanding of lifeways in recent history with implications for older
populations. Specifically, the following hypotheses will be addressed:
1. Both males and females will display the same distribution of cribra orbitalia
and porotic hyperostosis.
2. Based on existing bioarchaeological and clinical research of iron deficiency
related to pregnancy, child rearing, and early childhood development, adult
females and children will show a greater frequency of lesions than adult males.
3. Age-at-death cohorts will exhibit a fluctuation in lesion frequency over the
span of a lifetime as hazards of disease and dying increase.
4. Lesion frequency will provide diagnostic utility when comparing mortality to
cause of death categories. If lesions are a sign of poor health, then lesion
expression will reflect an elevated mortality hazard. If lesions are a sign of
survivorship, then lesion frequency will be a sign of adaptation.
5. Differences will be seen between lesion presence and severity to sex, age-atdeath, and cause of death data. Individuals subjected to the greatest stress are
expected to display higher severity scores as related to stress manifested from
lifestyle patterns reflected by economic and social changes.
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CHAPTER 2: LITERATURE REVIEW
Stress can be produced by forces of malnutrition, psychological stress, metabolic
or infectious disease, environmental stress, or resource depletion and adverse climatic
conditions (Goodman et al. 1988). Reaction to and survival of stressors involves factors
such as age, sex, and resiliency. If the body was unable to effectively respond to
stressors, physiological changes may affect the bones (Goodman et al. 1988).
Physiological changes are a way of countering stressors interfering with the body’s
performance. Not all stressors result in physiological manifestations, but duration may
contribute to likelihood of indicators on bone (Wood et al. 1992). For example, Harris
lines, dental enamel hypoplasia, periostitis, and non-specific indicators are all osteoindicators of stress.
Stress can manifest in a number of ways as a force that can have a significant
impact on the human body if it is not buffered. Physiological disruptions such as
interruption of bone development, growth, and maintenance may occur. There are many
examples of non-specific indicators of health but this study will focus on cribra orbitalia
and porotic hyperostosis. In previous work, cranial lesions were seen as specific
indicators of nutritional health (Walker 1986), but recent research has offered alternative
hypotheses (Holland and O'Brien 1997; Stuart-Macadam 1992; Walker et al. 2009).
Cranial lesions viewed in conjunction with the archaeological record can lend insight to
the health and behavior of past populations.
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Most diseases do not directly impact the skeleton, or, only do so after afflicting
the individual for a prolonged period of time. As a result, disease may not be evident
from singular review of skeletal material. A skeletal sample may not show any markers
of disease, and those that do display lesions may represent individuals who survived with
the disease long enough for skeletal impact to occur. In line with the osteological
paradox, hidden heterogeneity in risk and selective mortality are factors that may explain
the conflicting data skeletal samples sometimes yield (Wood et al. 1992).
2.1 Osteology
Cribra Orbitalia
Skeletally, cribra orbitalia are characterized as pitting lesions that develop in the
orbital roofs of the frontal bone. Lesions vary in appearance and distribution, but are
usually bilateral and symmetrical (Stuart-Macadam 1989). Macroscopically, the lesions
range from fine porous holes that impact compact bone to large openings that
compromise the integrity of compact bone. Microscopically, the trabeculae create a “hairon-end” appearance and the spaces between trabeculae enlarge to expand the surface of
the ectocrania (Stuart-Macadam 1992).
Biologically, the formation of cribra orbitalia is tied to the conversion of red and
yellow bone marrow. Red marrow (hematopoietic) is located where red blood cells
(RBC) are produced. During embryological development, RBC production occurs in the
liver and spleen but moves to the red bone marrow prior to birth. Subsequently, during
childhood and young adult development the red marrow begins conversion to yellow
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marrow until isolated repositories of red marrow remain in the spine, ribs, and parts of
the skull (Ortner 2003).
Typically, cribra orbitalia forms in children since they have a greater plasticity
and susceptibility to stress, and a greater concentration of red marrow remains throughout
the skeleton in youth. Cribra orbitalia develops when blood-producing bone marrow in
the orbital roofs expands, increasing RBC production (Stuart-Macadam 1985). The
porous or thickened bone lesions are created from the expansion of the diploë in response
to increased RBC. Lesions found in the orbital roofs of adult individuals are less
common, but when found are often characterized by remodeling.
Cribra orbitalia is classified as a non-specific indicator, but its presence can often
lead to assumptions about etiology (Ortner 2003). Commonly, cribra orbitalia may be
associated with incidence of anemia, subperiosteal hemorrhage, or a vitamin D deficiency
(“rickets”). Not all anemias produce or result in the same severity of cribra orbitalia seen
in iron-deficiency anemia. Incidence of differential expression is discussed in Section 2.3.
Porotic Hyperostosis
Skeletally, porotic hyperostosis is a paleopathological condition that affects the
skull vault, the frontal, parietal, and occipital bones (Ortner 2003). Summarily, Ortner
(2003) outlines the skeletal response seen in porotic hyperostosis at the macro- and
microscopic levels. Macroscopically, a number of foramina of varying size and
distribution penetrate the outer compact bone. The diploë table experiences a thickening,
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and the outer table thins. Lesions may vary from fine to porous and leave intact
coalescing foramina that destroy the integrity of the compact bone.
Biologically, porotic hyperostosis is the result of an imbalance of red blood cell
homeostasis. In response to vitamin, iron, or amino acid imbalances, the marrow cavities
where red blood cells travel respond by expansion. Walker et al. (2009) outlines the
response the body makes to the imbalance. Anemic conditions cause hemoglobin levels
to fall, which leaves the body oxygen-starved. As a result, the kidneys are triggered to
produce erthropoietin, a hormone that facilitates RBC production and maturation. If these
measures fail to right the imbalance, the cranial vault marrow expands to stimulate RBC
production within the diploë of the skull as a systemic response to insufficient
hemoglobin levels. In the crania the expansion of the diploë elevates the outer table. The
compact bone of the outer table eventually resorbs if red blood cell levels are corrected,
thus creating the porotic “spongy” lesion appearance on the ectrocranial surface.
Similar to cribra orbitalia, porotic hyperostosis is classified as a non-specific
indicator, and presence may also lead to assumptions about etiology (Ortner 2003).
Commonly, porotic hyperostosis may be associated with incidence of anemia,
subperiosteal hemorrhage, or a vitamin D deficiency (“rickets”).
Scoring Methods
Porotic hyperostosis and cribra orbitalia are commonly scored lesions in skeletal
analysis, primarily because both are typically associated with anemia (El-Najjar et al.
1976; Kent et al. 1994; Stuart-Macadam 1985). The identification of and method of
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scoring porotic hyperostosis and cribra orbitalia have evolved since first documented in
the 1800s, and macroscopic conditions can be subject to inter-observer biases of severity
and prevalence (Jacobi and Danforth 2002).
A number of scoring methods have been proposed, but most methods are
organized into four categories: scattered fine foramina, large and small isolated foramina,
foramina that have linked into trabecular structure, and lastly, outgrowth of trabecular
bone from the outer table. Vault and orbital lesions frequently occur bilaterally and
symmetrically. Stuart-Macadam (1982) was one of the first to present specific definitions
for degrees of expression of porotic hyperostosis, and subsequent publications explored
associated pathologies. Stuart-Macadam (1985) was the first to incorporate diploë
thickening into her evaluations on a scale of three severity levels:
1) light: with scattered fine foramina,
2) medium: large and small isolated foramina with some of the foramina
coalesced to form trabeculae, and
3) severe: outgrowth in trabecular structure from the normal contour of the outer
bone table.
Buikstra and Ubelaker (1994) adapted the work of Stuart-Macadam to develop a
recording system for porotic hyperostosis and cribra orbitalia collectively. In Standards
for Data Collection for Human Skeletal Remains, Buikstra and Ubelaker (1994) outline a
popularly used recording system to document various degrees of expression. They
subsume cribra orbitalia under scoring methods for porotic hyperostosis and allow for
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locational distinction of scoring. In the event multiple stages of expression are present,
Buikstra and Ubelaker indicate the most extreme stage should be coded.
6.1.0 Degree
6.1.1 Barely discernible.
6.1.2 Porosity only.
6.1.3 Porosity with coalescence of foramina, no thickening.
6.1.4 Coalescing foramina with increased thickness.
6.2.0 Location
6.2.1 Orbits
6.2.2 Adjacent to sutures
6.2.3 Near bosses or within squamous portion of occipital
6.2.4 Both adjacent to suture and within orbits
6.2.5 Both adjacent to suture and near bosses/in squamous
6.3.0 Activity
6.3.1 Active at time of death
6.3.2 Healed
6.3.3 Mixed reaction: evidence of healing + active lesions
In 2006, Steckel et al. produced a Data Collection Codebook for the Global History
of Health Project (GHHP) to document and analyze health in various populations across
temporal and spatial boundaries. The project was designed to archive skeletal data
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collected by the protocol into a central database augmented by archaeological, historical,
and ecological data. Of particular interest to the project is diagnosis of conditions that had
significant impact on the morbidity and mortality of historic and pre-historic populations.
Definitive diagnostic techniques were presented for a variety of paleopathological
conditions, including porotic hyperostosis and cribra orbitalia. Under GHHP, the scoring
system is as follows (see Figures 1 and 3):
0
No parietals present for observation
1
Absent with at least one observable parietal
2
Presence of slight pitting or severe parietal porosity
3
Gross parietal lesion with excessive enlargement of bone
Figure 1. Standard for scoring porotic hyperostosis. Courtesy of GHHP Codebook Figure
9, page 14. Note: images depict ectocranial surface of the cranial vault.
To score cribra orbitalia, the roof of at least one eye orbit must be present. Under GHHP,
the scoring system is as follows (see Figures 2 and 3):
0
No orbits present for observation
1
Absent with at least one observable orbit
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2
A cluster of mostly fine foramina covering a small area (< 1cm3)
3
Substantial areas (> 1cm3) covered by a small and/or larger foramina with
a tendency to cluster together.
Figure 2. Standard for scoring cribra orbitalia. Courtesy of GHHP Codebook Figure 8,
page 13. Note: images depict superior aspect of left eye orbit.
Figure 3. Example of porotic cranial lesions. Porotic hyperostosis (left) and cribra
orbitalia (right) from Walker et al. 2009, page 110.
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2.2 Diagnosis
Stuart-Macadam (1987b) conducted a radiographic study of living populations in
effort to link porotic hyperostosis and cribra orbitalia to a diagnosis of anemia. In
response to anemia, the immune system attempts to produce more red blood cells in the
cranial diploë. Expansion of the diploë puts pressure on the outer table of the skull,
resulting in a thinning of the cortical layer and producing a porous appearance (Wright
and Chew 1998). Because red marrow is not present in the developed cranial bones of
adults, porotic lesions in response to anemia is limited to juveniles, and sub-adults.
However, healed lesions may be present on adult skeletons whereby evidence of
remodeling would indicate the individual survived a stressful, anemic episode. StuartMacadam (1987b) confirmed a relationship does exist between the two cranial lesions
using anthropological and clinical data. The pattern of bone changes seen in radiographs
of skulls with porotic hyperostosis corresponded to patterns of bone changes seen in
clinical radiographs of patients diagnosed with a form of anemia.
As mentioned in earlier sections, iron deficiency anemia that causes porotic
hyperostosis and cribra orbitalia is thought to be the result of several factors, to include:
malnutrition, unsanitary living conditions, infectious disease, and parasite load (Blom et
al. 2005; Holland and O'Brien 1997; Palkovich 1987; Reinhard 1988). Iron deficiency
anemia is more common than genetic anemia and B12 disruption and refers to situations
of dietary stress, transition, and shifts in socio-economic norms. The association between
cribra orbitalia and porotic hyperostosis has been confirmed through clinical and
archaeological research, but presence of one does not guarantee the other. In some
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skeletal collections cribra orbitalia predominates over porotic hyperostosis, and in others
it is the reverse. For example, two studies conducted by Walker (1985; 1986) compare
skeletal insult in terrestrial and marine based subsistence communities. Overall, cribra
orbitalia occurs with greater frequency than porotic hyperostosis (Walker et al. 2009).
Re-evaluation of the etiology of cribra orbitalia and porotic hyperostosis has profound
implications for present interpretation of paleoepidemiology and nutrition in past
populations. Walker et al. (2009) present convincing hematological data to suggest a
vitamin-B12 deficient diet is a likely nutritional catalyst for the collaborative expression
of porotic hyperostosis and cribra orbitalia.
The diagnosis of vitamin B12 deficiency rather than an iron deficiency has
interesting implications for associated physiological symptoms. A vitamin B12 deficiency
would produce megaloblastic anemia (see description of the condition, below), but in
modern populations is also tied to neurological problems (Hector and Burton 1988). An
onset of neurological problems in concert with periods of agricultural transition in
prehistory may be telling about incidence of interpersonal violence in the archaeological
record. Walker et al. (2009) provide the example of outbreaks of violence among
Ancestral Puebloans in the American Southwest where osteological research has
identified a significant relationship between violent encounters and incidence of anemic
conditions.
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2.3 Anemia
Anemia literally translates to “without blood”, which suits its clinical definition of
leaving a pathological deficiency of either red blood cells or hemoglobin carried by red
blood cells. Specifically, anemia is a term utilized to describe the physiological defects
that occur to red blood cells that affects exchange of oxygen in the circulatory system
(Ortner 2003). Osteological changes may occur to allow space for hematopoietic marrow
to expand (Ortner 2003; Stuart-Macadam 1989).
Genetic
Ortner (2003) outlines the two types of anemia: genetic and acquired. Genetic
anemias (thalassemia and sicklemia) are rare in comparison to acquired anemias caused
by nutritional deficiencies or blood loss. Acquired anemia is characterized by inadequate
intake or absorption of iron to an individual’s system. Hemoglobin concentration, serum
iron, and storage iron are all low, while the lack of available iron produces a high total
iron-binding capacity in the circulating proteins that are responsible for transporting iron
to various bodily tissues. Iron is essential for healthy blood transport in the maintenance
of the circulatory and organ systems.
Thalassemia is a condition that results when the DNA coding for hemoglobin
molecules undergoes mutation. Originally, thalassemia was identified in populations of
the Mediterranean Sea (Angel 1966), but has subsequently been documented globally in
the archaeological record (Lewis 2012). There are multiple forms of thalassemia, the
most common of which is B-thalassemia affecting the B-globin genes. Thalassemia can
be differentiated by major, minor and intermediate severity. The most severe is inherited
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from both parents (B-thalassemia major). Within the first two years of life, symptoms
present with fatigue, growth deficiencies, paleness, and facial deformities. Blood
transfusions are necessary for survival otherwise bones become thin and fragile.
Childhood death results from heart failure or stroke due to the excess of iron stores that
thalassemia produces.
The presence of thalassemia in the archaeological record in the New World is
disputed. In past populations it would be uncommon for infants to survive inheriting
thalassemia (Ortner 2003). In 1964, Zaino identified porotic hyperostosis in preColumbian sub-adult skulls from Peru and speculated thalassemia responsible for their
origin. In the 1960s and 1970s, researchers began reporting porotic hyperostosis at
Pueblo sites in the American Southwest (El-Najjar et al. 1975; El-Najjar et al. 1976). It is
unlikely, however, that thalassemia reached the New World before Europeans arrived
(Ortner 2003).
Thalassemia has been tentatively identified in select archaeological sites.
Diagnosis is dependent upon the presence of porotic hyperostosis and cribra orbitalia in
concert with geographic origin of the remains. The non-specificity of skeletal changes
means a diagnosis of thalassemia is nearly impossible. Differential diagnosis of infant
remains is highly unlikely due to poor preservation or concurrent malnutrition (Lewis
2012).
In the Old World, identification of thalassemia is more convincing given modern
clinical evidence and DNA analysis. In the 1960s, Angel presented the possibility of
thalassemia in ancient Greece through a combination of skeletal evidence and ecological
22
evidence for the presence of mosquito born malaria in the region. Thalassemia is present
in modern Greek populations, which lends credence to Angel’s early speculation. More
recent analyses have bolstered the probability of identifying thalassemia in the skeletal
record (Lewis 2012; Ortner 2003).
Sickle cell anemia is characterized by skeletal involvement similar to that of
thalassemia, and is more commonly identified in the symptoms of the living. Sickle cell
anemia is a condition which has ensured the survival of individuals in malarial areas of
the world, where absence would serve as a selective force to cull individuals without the
mutation (Maat 1991). Foreign pathogens require a specific blood iron content to survive
in a host body. If iron stores are low due to genetic predisposition for malformed red
blood cells, individuals who display this inherited inability to transport sufficient oxygen
necessary to transport iron have a higher chance of survival in regions prone to iron
hungry parasites, pathogens, and infection. Sickle cell anemia is a genetic anemia that
occurs when the abnormal gene is present in a homozygous recessive condition, which is
almost exclusively found in individuals of African descent with pocket populations in
nearby Mediterranean regions (Ortner 2003). There is speculation that evidence of sickle
cell anemia can be identified on a global scale. Recent research has examined
pathological changes in red blood cells preserved in skeletons from as far back as the
Hellinistic Period in the Persian Gulf to modern individuals in clinical studies diagnosed
with a form of anemia (Maat 1991).
The skeletal impact of sickle-cell anemia is seen in three ways: 1) changes
secondary to increased demand of space for hematopoietic marrow; 2) sequelae of
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vascular obstruction of smaller or larger blood vessels; 3) secondary infections
superimposed on ischemic areas. The skeletal changes incurred from sickle cell anemia
are not obvious or specific but first occur in the crania. Enlargement of the diploë is
typically bilateral, symmetrical, and is seen along the parietal, frontal and occipital bones
in the deceased as well as radiographs (Stuart-Macadam 1987b). Unlike thalassemia, the
hair-on-end appearance is uncommon in sickle cell anemia (Ortner 2003). However,
skeletal changes associated with sickle cell anemia are seen in the vertebrae, pelvis, long
bones, hands and feet, locations not affected by thalassemia. Vertebral bodies experience
a widening and flattening, and necrosis of the head of the femur may occur. However,
most changes in the lower limb occur in the tibia and fibula due to a compromised
marrow cavity that results in an expanded diameter of the long bone shaft(s). Metacarpals
and phalanges may widen similar to thalassemia, complete with development of enlarged
vascular foramen (Ortner 2003). Regional, osteological, and genetic data are necessary to
determine whether pathological insults are the result of a genetic anemia in place of an
iron-deficiency (Ortner 2003).
Dietary
Anemia influenced by dietary fluctuations include megaloblastic anemia and irondeficiency anemia. Megaloblastic anemia is characterized by inadequate intake or
absorption of vitamin B12 or B9 (folic acid). The body produces oversized, malproportioned red blood cells that cannot adequately perform the function of oxygen
transport. This form of anemia is typical of infestation by high B12 consumption and fish
24
borne parasites. Foods that are rich in iron include red meats, mussels and other shellfish,
prunes, spinach, varieties of beans, eggs, and iron in animal products are more readily
absorbed than iron found in plant foods (Stuart-Macadam 2006).
Vitamin B12 and folic acid are necessary for DNA synthesis. Deficiencies are
common causes of megaloblastic anemia. Patients with a vitamin B12 deficiency that
develop megaloblastic anemia display symptoms of nervous system demylination to
include irritability, abnormal reflexes, psychiatric disorders, and lethargy progressing to
coma (Walker et al. 2009). Specifically, demyelination is a condition of the nervous
system characterized by damage to the myelin sheath that protects neurons, and thus
impairs signal conduction of affected nerves.
Curiously, iron overload can negatively impact physiological responses, as well.
Healthy people need very little supplementary iron to maintain proper iron balance, and
increased stores can be as harmful as the depletion of stores. The toxic nature of too
much iron is seen at the molecular level (Kent and Weinberg 1989). Excess iron cannot
be easily excreted and therefore accumulates in the body. Iron stores can develop in the
joints, liver, spleen, pancreas, pituitary, heart muscles, and causes arthritis, diabetes, liver,
pancreatic, cardiac, and endocrine system failures and has potential to contribute to
conditions such as heart disease and cancer (Stuart-Macadam 2006). On the contrary, too
little iron can result in severe anemia, which impairs quality of life and immune system
productivity.
Research of uterine development shows that fetuses exposed to B12 deficiencies
develop postnatal immune functional problems that increase their susceptibility to
25
infections (Molloy et al. 2008). Vitamin B12 is found almost entirely in foods of animal
origin, and therefore a B12 deficiency is common among individuals with diets restricted
of animal foods (Stabler and Allen 2004). There is a sharp contrast in how a vitamin B12
deficiency is expressed in adults versus children. In normal adults, livers maintain
substantial vitamin B12 stores, which deplete very slowly. Infants have not developed
reserve stores of vitamin B12 and can exhibit symptoms shortly after birth especially if
breastfed by a B12 deficient mother.
Populations with restricted access to animal products exhibit greater risk of
megaloblastic anemia, especially in nursing aged infants. Expectant women with personal
or situational restriction to animal products in their diet will translate vitamin B12
deficiency during pregnancy and lactation to their infants. Megaloblastic mothers may
not display physical symptoms but their offspring are likely to develop severe
megaloblastic anemia. Ethnographically, food taboos and gender-based limitations on
diet may have contributed to incidence of megaloblastic anemia.
Osteological changes attributed to megaloblastic anemia are difficult to discern,
as vitamin B12 deficiencies are difficult to identify without the use of stable nitrogen
isotope analyses (Pearson et al. 2010). The reaction to infant weaning would be
pronounced during famine. Additionally, gastrointestinal parasite infection may also
serve as the etiology for diarrheal disease and subsequent nutritional deficiencies leading
to anemia (Pearson et al. 2010; Walker et al. 2009).
Similar to megaloblastic anemia, iron deficiency anemia is an acquired anemia
that causes porotic hyperostosis and cribra orbitalia. These cranial lesions are thought to
26
be the result of several factors, to include: malnutrition, infection, and parasite load as
demonstrated by studies of Holland and O’Brien (1997), Stuart-Macadam (1989), and
Roberts and Manchester (2005) among others. Iron-deficiency anemia is a condition
characterized by insufficient levels of iron needed for the development of red blood cells
needed to transfer oxygen through the circulatory system. Iron is additionally important
for nerve response, protein synthesis, and overall strength of the immune system (StuartMacadam 1989). Iron absorption is affected by the physiological need for iron, dietary
intake of iron, bioavailability of dietary iron, and adaptation (Kent et al. 1994).
Adaptability is the most important factor that can affect absorption, and refers to the
ability of the cells in the intestines to adjust to the available stores of dietary iron as well
as physiological demands. Levels may fluctuate in response to the physiological demands
for iron. During pregnancy, infancy, and childhood, the body requires higher levels of
iron to support physiological changes. Subsequently, the body will adapt in effort to
maintain balanced iron levels when greater stores are required.
If iron levels fall below what the body requires, oxygen levels in the tissue
decrease as well. Subsequently, the red marrow is stimulated in effort to generate a
greater number of red blood cells and replenish oxygen levels (Mensforth et al. 1978).
This process causes the bone marrow to expand. The cranial diploë thickens in the cranial
vault and along the orbital roofs, also known as porotic hyperostosis and cribra orbitalia.
Debate remains about the post-cranial impact of iron-deficiency (Walker et al. 2009), but
more data is needed to reduce differential diagnosis of iron-deficiency anemia as
interpreted in skeletal material. Stuart-Macadam (1985) noted that the condition is most
27
common in younger individuals, and may not express all the skeletal indicators given
their early demise. Evidence of skeletal impact may be minimized by bone remodeling in
older aged individuals (Holland and O'Brien 1997). As a result, iron deficiency anemia
has become an overly diagnosed condition, when other pathological conditions such as
rickets, scurvy or related deficiencies could be considered to explain the same skeletal
pathologies (Walker et al. 2009)
As summarized by Stuart-Macadam (2006), iron overload – or hyperferremia –
occurs as a result of a reduction in iron absorption in the diet. In individuals experiencing
an increased physiological need for iron, such as pregnant women or young children, an
increased absorption of iron may occur in the gastrointestinal tract. A study by
Wadsworth (1975) explained the three laws of red blood cell production and destruction,
referred to as “laws of erythrokinetics”:
1. The body conserves its iron; once in the body very little can get out under
normal circumstances;
2. The amount of iron entering from the intestine is inversely related to the
amount of nonheme iron in storage in tissues; as these stores decrease, the amount
absorbed by the intestine increases;
3. The amount of iron entering the body from the intestines is directly related to
the rate of erythropoiesis (red blood cell formation); the greater the rate of red cell
production, the greater the amount of iron absorbed.
28
Environment
Incidence of anemia can also attributed to environment and hygiene related
etiologies. These include iron deficiencies related to diet breadth availability in a given
ecosystem, and also parasitism. Parasite driven infections are closely linked with
sedentism, which often correlates with agricultural practices, animal domestication, and
aspects of environment, sanitation, personal hygiene, education, poverty, and economic
structures (Bouchet et al. 2003). Parasitic infections may produce a broad spectrum of
diseases of major pathogenic and social importance. The subsequent osseous impact is
seen in the human skeletal record, but the etiology can be complicated (Ortner 2003).
Some infections are fatal if untreated and others may produce significant acute or chronic
disease in high proportions of segments of the populations. Helminths, or worm
endoparasites, tend to produce episodic periods of diagnosable ill health against a
background of slow cumulative morbidity, and chronic pathological response
(Aufderheide 2003). Emerging research in parasitism is challenging earlier views of the
role of iron in health and infection, and has implications for the significance of
understanding porotic hyperostosis in the balance of diet and adaptation to disease.
The parasite model reassesses the role of iron in health and disease and explores
the complexity of iron absorption explained by two tenants: (1) except in cases of
outright malnutrition, diet plays a minor role, if any, in the development of iron
deficiency anemia; and (2) mild iron deficiency, or hypoferremia, is not necessarily a
negative condition; in fact, it is one of the body’s defenses against disease. Essentially,
anemia can be considered an adaptive response to disease, infection, or parasites. In this
29
model, the body’s automated reduction in blood iron content is designed to repel ironhungry parasites.
Diagnosis of skeletal pathology resulting from parasitic infection can be
problematic. A holistic analysis of diet and skeletal pathology has enabled researchers to
identify the role of parasites to the incidence of skeletal lesions. Parasitic infection often
results in the organism burrowing into the tissue or organ systems of its host, which
results in nutrient deficiencies and subsequent osseous response. Iron deficiency anemia
associated with parasitic infection results in porotic hyperostosis, cribra, orbitalia, and
marrow hypertrophy. All three skeletal conditions have been documented by a number of
studies (Blom et al. 2005; El-Najjar et al. 1976; Holland and O'Brien 1997; StuartMacadam 1989; Walker et al. 2009), whereby anemia is a pathological symptom and not
a specific disease (Walker et al. 2009). The parasite model is an excellent example of the
osteological paradox (Wood et al. 1992), whereby skeletal lesions may represent only a
portion of afflicted individuals in a population and some individuals are more sensitive to
lesion development.
2.4 Archaeological Literature
The pathological connection between cribra orbitalia and porotic hyperostosis has
been explored for over 100 years. In the early 20th century, researchers began to suggest a
link between cranial lesions and nutritional deficiencies associated with anemia. In recent
years, clinical studies have confirmed a relationship between cribra orbitalia, porotic
hyperostosis, and anemia. However, the etiology of anemia and the associated cranial
30
lesions have shifted the focus to a better understanding of how different modes of stress
affect individuals skeletally. Research has involved archaeological skeletal collections
and collections with known demographic data, supported by clinical and radiological
research involving both deceased and living subjects.
Studies Identifying Lesions
The earliest attempts to identify the severity of lesions in cribra orbitalia began
with Welcker in 1888, as discussed by Jacobi and Danforth (2002). Welcker focused on
relative porosity size while severity was categorized as weak, stronger, and strongest.
Some of the earliest explorations into the etiology of cranial lesions involved the
paleopathological riddle of symmetrical osteoporosis, particularly in the young adult
members of society. Moseley (1965) examined remains for clues to congenital or
acquired pathological abnormalities. Moseley cites the early work of Ales Hrdlička
documenting presence and absence of skull pathology in pre-Columbian Peruvian Indians
of contrasting environmental habitation. Whether or not an absence of post-cranial
involvement was expected, findings generated much theoretical consternation among
Hrdlička and subsequent researchers. Moseley speculated that the involvement of
radiographic techniques later used by numerous studies, would provide critical diagnostic
data of ancient skeletons to confirm the relationship between porotic hyperostosis, cribra
orbitalia, and genetic or inherited anemias.
Subsequent work by Nathan and Haas (1966) characterized cranial lesions in
primates, identifying three degrees of cribra orbitalia development, including: 1) porotic
31
type with small pores, 2) cribrotic type with larger aggregated but still separated
openings, and 3) trabecular type with openings that are coalesced and form trabeculae. In
a collection of 106 crania of various primates, over 14 percent exhibited lesiatic activity.
As in humans, incidence was greater in younger animals. Interestingly, porosity was
documented on aspects of the temporal bone, as well.
Efforts to score porotic hyperostosis have also endured various standards. One of
the original descriptions of porotic hyperostosis was recorded by Hooton (1930) in his
seminal research at Pecos Pueblo. Hooten described the lesions as occurring in
symmetrical patches, usually on the parietals but occasionally impacting adjacent
elements. Hooten observed that diploë thickening varied from 10 to 15 mm and evidence
of healing by evidence of bone remodeling could be identified. Jacobi and Danforth
(2002) note that since Hooton, research has mainly focused on the presence of lesions
rather than adopt a universal scale to evaluate expression criteria. Bioarchaeologists have
documented both types of lesions in prehistoric and historic contexts on a global scale
and commonly use both as a proxy for health and nutritional status of populations.
Similar studies emerged from the American Southwest, exploring porotic
hyperostosis at New World sites prior to European contact in Arizona and New Mexico.
El-Najjar et al. (1975) explored the relationship between cranial pathologies such as
porotic hyperostosis to nutritional based iron deficiency anemia. Analysis examined 539
crania excavated from Anasazi (Ancestral Pueblo) sites. Contrasting diets of maize based
and animal and vegetable based revealed a greater incidence of lesions in the maize based
diet. Age differences were identified in the maize based diet but none in the alternative
32
diet. Lesions were scored for presence of small porous openings on the ectocranial
surfaces. Crania exhibiting one or more clusters greater than 5 mm in diameter were
characterized as porotic hyperostosis. A total of 185 adults and 87 children under ten
years of age were diagnosed with porotic lesions. El-Najjar et al. (1975) suggested that if
iron deficiency anemia accounts for the presence of porotic hyperostosis then the
pathology will persist in populations where animal protein is absent from the diet. In sum,
a heavy dependence on a single food source may have hematologic consequences and
thus explain social reorganization on a landscape (El-Najjar et al. 1976).
Walker (1985) reviewed osseous changes associated with anemia in skeletal
remains of the southwest American Indians. Walker speculates a combination of nutrition
and infectious disease are responsible for the lack of iron in the diet and diarrheal and
helminth infections. The 17 collections examined are located primarily in northern
Arizona and New Mexico and date from the later Pueblo periods. Age categories were
compromised due to inconsistent aging criteria between studies. Documented severity of
lesions was also variable, but it was still clear that a greater incidence of porotic
hyperostosis was displayed in children (26%) than adults (15%). Analysis excludes the
possibility of genetic origin for incidence of anemia due to the gradient of symptoms
documented, the lack of marrow hypertrophy in facial bones, and restriction of lesions to
the cranium. Walker also noted a significant increase of porotic hyperostosis in maize
dependent groups that were canyon-dwelling over plains people with access to game.
Walker acknowledges the impact that dietary deficiencies, culinary practices, prolonged
breast-feeding, diarrheal infections, and demographic variables may have on the
33
incidence of iron deficient anemia. However, helminth infections are recognized as
important causes of iron deficiency anemia in many parts of the world. Walker (1985)
discusses how parasites consume host blood, cause internal bleeding, and a general loss
of nutrients through the aforementioned diarrhea. It is highly possible that helminth
infections contributed to anemic conditions in the prehistoric Southwest. Documentation
of pinworms, tapeworms, and spiny-headed worms in coprolite materials from the sample
sites confirms the presence in the archaeological record. Infection likely occurred through
consumption of insects, which served as parasite’s intermediate hosts (Reinhard et al.
2012). At the time of this publication, Walker acknowledged the new field of isotopic
analysis, where documentation of a lack of animal protein in the diet could be highlighted
as an important factor contributing to porotic hyperostosis in place of parasite infestation.
In 1986, Walker followed up with an examination of the incidence of porotic
hyperostosis in marine resource dependent populations of Native Californians. Analysis
of 432 crania comparing mainland coast of California populations to nonagricultural, fish
dependent populations on the Channel Islands suggests the prevalence of porotic
hyperostosis and cribra orbitalia are the result of heavy dietary dependence of marine
resources infected with water-borne parasites. Lesions were scored on a scale of zero to
three, where zero indicates no evidence and three involves considerable linkage
involvement between foramina. Females displayed a higher rate of cribra orbitalia, likely
due to women’s cycles of menstruation and pregnancy resulting in iron loss. Islanders
displayed a higher frequency of skeletal lesions than mainlanders by fifteen percent.
Walker reviews the impact of dietary deficiencies, prolonged breast-feeding, weanling
34
diarrhea, and protein-calorie malnutrition as contributors to cranial lesions associated
with iron deficiency. However, in discussion of helminth infections there is a distinct
difference in exposure to fish borne parasites between island-mainland and inter-island
groups. Studies of kelp fish species and sea mammals show heavy infestation of larval
roundworms and tapeworms, which, if ingested, penetrate the digestive tract and cause
vomiting, diarrhea, ulcers, blood in the stools and megaloblastic anemia. A known
preference for a diet of raw fish and sea mammal meat on the Channel Islands
significantly contributed to the pathogen load and subsequent prevalence of iron
deficiency anemia in Native Californians on the coast. The incidence of symptomatic
lesions in agriculturalist mainlanders further proves that anemia is not solely the result of
nutrient deficiency in the diet, but exposure to parasites and pathogens in contaminated
resources or waterways. In 2009, Walker et al. followed up with previous research and
argued for a reappraisal of the iron deficiency anemia hypothesis. Research identified
porotic hyperostosis and cribra orbitalia in a broad sense of epidemiology with strong
physiological association with hypertrophic response related to pathogen load and diet
restrictions.
In 1996, Wright and White examined the Classic Maya collapse in light of
human skeletal biology and isotopic dietary construction to find ecological explanations.
Analyses examined paleopathological and paleo-dietary data independently but within a
single model. A correlation between diet and pathology suggests dietary choices have
health consequences as seen in prevalence of anemia and δ13C. Overall, this study sought
to establish ecological explanations for the collapse of a large empire, and found that the
35
nutritional argument for demise is weaker than assumed. Biological evidence for
malnutrition as an agent of demographic collapse fails to acknowledge the dietary
diversity of Mayan regions. Wright and White conduct a regional synthesis of existing
data, documenting porotic hyperostosis in three quarters of sub-adults and more than
sixty percent of adults. Wright and White argue that if dietary iron deficiency is
responsible for the collapse, then an increase in lesions is expected over time. If food
quantity, not diet composition, is responsible for collapse, then increased iron deficiency
is expected over time. If diet focus leads to maize in exclusion of other resources then
iron deficiency should increase. However, if maize is scarce and is substituted, then iron
deficiency should reduce. Through isotopic data, Wright and White observe only a slight
increase in porotic hyperostosis as maize consumption rises over time. However, porotic
hyperostosis increases significantly with the arrival of foreign infection and disease
during Spanish Conquest. Note that the period of Spanish Conquest was a period
socioeconomic change not accompanied by alterations in diet, which suggests increased
stress is a significant contributor to skeletal lesions.
In 1998, Wright and Chew examined porotic lesions resulting from childhood
anemia in the ancient Maya. Data collection looked for evidence of poor nutrition and
parasite infection to confirm speculation that more anemic children survived to adulthood
in the past than they do today. The study explores ethnographic analogy to evaluate the
broader implications of poor health on past cultures, with emphasis on skeletal evidence
for anemia. Analysis reviewed lesions on 47 individuals from modern forensics context
believed to be of Mayan decent, and compared these with 11 skeletal collections
36
comprising 761 ancient Mayans including both adult and sub-adult remains. A noticeable
absence of porotic hyperostosis on crania of modern forensic skeletons in the Maya
region is speculated to be the result of increased childhood mortality than compared to
the prehistoric condition. Individuals that reach adulthood in modern times are perceived
to have survived the burden of infectious disease and weaning. Wright and Chew support
their conclusions that childhood health is more compromised in current times than it was
in the past by stature reduction data.
In a 2005 study, Blom et al. explored environmental stressors such as parasites
associated with childhood anemia through regional variation in biocultural practices
among Pre-Columbian villages in Peru. Parasites and disease were found to have a more
significant impact on prevalence of cribra orbitalia and porotic hyperostosis than specific
dietary practices associated with the two types of lesions. Blom et al. focused on
incidence of childhood anemia to draw comparative conclusions about the association
between childhood anemia and mortality. The study sample included 1465 individuals
from two collections spanning three horizons: Early Intermediate (ca. 200 BC – AD 600),
Middle (ca. AD 600 – 1000), and Late Intermediate (ca. AD 1000 – 1476). The
collections contain twice as many males as females and the majority of individuals were
under 10 years of age at death. The collections span the peaks of the Andes to the coast of
Peru across more than 30 sites and 11 valleys, with contrasting communities of marinebased to maize-based subsistence strategies. The authors recorded porotic hyperostosis,
cribra orbitalia, and evidence of marrow hyperplasia in relation to dietary patterns with
implications for the study of anemia.
37
Blom et al. (2005) used Ba/Sr ratios of stable isotope analysis to measure food
consumption. Blom et al. speculate that if childhood anemia and childhood mortality are
correlated then the prevalence of porotic hyperostosis in a juvenile mortality sample will
overestimate the prevalence in the living sample, and in adult samples there will be a bias
toward individuals who survived anemia and other childhood illnesses. Therefore, it is
important to account for all age ranges. Overall, 30.1% of individuals exhibited lesions.
Adults exhibited lesions at a rate of 23.1% and 81.8% children. Along the coastal sites,
individuals in the south had significantly fewer lesions than the central coast, indicating
geographical influence. When anemia was viewed by time period, a trend of increasing
lesion frequency emerged. Overall, evidence confirms iron-deficiency anemia as the
probable cause of lesions and marrow hyperplasia seen in the samples.
Blom et al. (2005) explored the stressors that may have contributed to the
prevalence of anemia: access to resources, exposure to diet, parasite load, and infectious
disease. Analysis shows that marine dependent populations exposed to contaminated
water sources or marine mammal borne parasites may explain prevalence. Chronic
intestinal conditions cause abdominal bleeding, diarrhea, blood loss, and decreased iron
absorption. In this study, anemia is most frequently seen in marine and maize based
subsistence strategies, suggesting diet related sanitation inadequacies may be contributing
to prevalence of porotic hyperostosis and cribra orbitalia. Further, bouts of disease can
result in anemia because gastrointestinal infections increase susceptibility, and parasites
and bacteria need iron to survive and thus decrease iron content of the blood. Blom et al.
38
confirm a relationship between disease, sendentism, dietary practices, and population
density.
Studies Identifying Lesions as Disease
A breadth of literature discusses the biological meaning and social implications
for incidence of iron deficiency anemia found in skeletal material. The inferred
implications of anemia are varied, to include indicators of genetic robusticity, sanitation
and parasite load, dietary needs and malnutrition, socio-historic stress, and underlying
illnesses. Patterns of cranial lesions in the New World and Old World led researchers to
draw corollaries between incidence and nutrient deficiencies. Angel (1966) hypothesized
that genetic anemia was the cause of the skeletal lesions found in Old World skeletal
collections, especially individuals in malarial areas. Subsequent research in New World
collections generated dietary-based hypotheses (El-Najjar et al. 1975; El-Najjar et al.
1976; Walker 1985).
One of the earlier examinations of the relationship between cribra orbitalia blood
disorders involved a cross population comparison of Hawaiian and Australian infants and
children. Zaino and Zaino (1975) documented presence and absence of orbital lesions in
existing pre-colonial skeletal collections from Mokapu, Oahu and New South Wales,
Australia. Lesions were documented on children ranging from 2 – 12 years of age. This
study was the first attempt to document cranial lesions in Native Hawaiians. Existing data
on Australian aborigines had reported an incidence of zero percent. Of the 53 subadult
crania examined from the Mokapu collection, 23% show cribra orbitalia with the greatest
39
porotic activity seen in the youngest individuals. Zaino and Zaino acknowledge the
contrast in frequency of cribra orbitalia between populations could have serious
implications for health in the youngest members of a population. Drawing on studies in
the mainland southwest, Zaino and Zaino speculate a relationship may exist not only
between cribra orbitalia and symmetrical osteoporosis (porotic hyperostosis) but also an
associated blood disorder.
Studies Identifying Lesions as Adaptation
Additional studies have examined whether cribra orbitalia and porotic
hyperostosis are indicative of an adaptation of the immune system to avoid infectious
disease. In 1992, Stuart-Macadam explored iron deficiency anemia as a nutritional stress
indicator of less successful adaptation to a given environment. A new perspective on the
adaptability and flexibility of iron metabolism made it clear that diet plays a minor role in
the development of anemia, whereby anemia is an adaptation to disease and organismal
invasion. Stuart-Macadam (1992) argues that the skeletal lesions associated with anemia
are evidence of a population attempting to adapt to a pathogen load in the environment
rather than a nutrient deficiency. Examination of the relationship between cultural
groups, sanitation, and intestinal parasitism has provided evidence for porotic
hyperostosis and cribra orbitalia as a response to pathogen load over nutritional stress.
Data analysis indicated a strong relationship between the number of species of parasite
found per population and the complexity of the ecosystem in which they resided.
Acceptance of environment as more important than diet in the prevalence of anemia has
40
profound effects for the perception of porotic hyperostosis and cribra orbitalia, and
attempts to adapt to environment at the skeletal level.
In a 2005 study, Sullivan dissected three models for the development of anemia:
1) iron deficiency anemia produced by inadequate iron absorption, 2) anemia of chronic
disease caused by body’s natural iron withholding defense against invaders, and 3)
megaloblastic anemia caused by insufficient intake and/or absorption of vitamin B12 or
folic acid. This analysis reviewed evidence of anemia among adults interred at the
Medieval Gilbertine Priory of St Andrew, Fishergate, York. The study of 147 individuals
identified a relationship between decreased status and increased anemia in both men and
women, and a greater incidence in women. Evidence of porotic hyperostosis and cribra
orbitalia in groups of lower rank or reproductive aged women supports the hypothesis
that lack of sanitation and being a reproductive aged female subjected to high pathogen
loads will result in any of the three models for the development of anemia. Analysis of
the York collection documented remodeling of porotic regions, suggesting individuals
survived severe periods of anemia. Or, remodeling also suggested skeletal lesions inline
with anemic conditions could be evidence for an adaptive response to the environment
and exposure to pathogens. Sullivan (2005) discusses the complicated nature of
characterizing aggregated anemia within a site and whether prevalence represents hidden
heterogeneity in the risk of morbidity. The osteological paradox of whether high evidence
of anemic skeletal lesions in the population represents an adaptive gene pool responding
to heavy pathogen loads requires additional review of coprolite and diet data to more
fully understand the etiology of parasite driven iron deficiency anemia.
41
In 2006, Keenleyside and Panayotova addressed whether incidence of cribra
orbitalia and porotic hyperostosis in Greek skeletal remains are the result of a genetic
anemia or pathological response to parasite infection. Their analysis reviewed 184
complete or nearly complete skeletons of a Greek colonial population from the Black
Sea. Individuals were examined macroscopically for cribra orbitalia and porotic
hyperostosis, recorded in four stages with increasing severity, originally outlined by
Stuart-Macadam (1992). Cribra orbitalia was seen in twenty-eight percent of the
collection, four percent exhibited porotic hyperostosis, and sub-adults were affected in
greater frequency than adults. Keenleyside and Panayotova (2006) argued that poor iron
intake in childhood and a high pathogen load explains the adaptive response seen in
parasite driven iron deficiency anemia. To confirm speculation that parasite load
contributed to anemia, analysis was conducted to rule out scurvy and rickets as the
etiology for increased porosity in cranial lesions. Isotopic analysis determined diet
breadth relied heavily on iron and vitamin rich resources.
Stuart-Macadam has generated numerous studies exploring the significance of
porotic hyperostosis and cribra orbitalia as a stress marker to assess health and nutritional
status (Stuart-Macadam 1985; 1989; 1992; 2006). In 1985, Stuart-Macadam examined
the etiology of cranial lesions for clues to duration and severity of anemic episodes.
Stuart-Macadam acknowledged that using porotic hyperostosis as an investigative tool
has led to researchers assuming a priority of diseases.
Often, porotic hyperostosis seen in adults is assumed to represent adulthood
anemia rather than lingering affects from nutritional deficiencies or ailments in
42
childhood. Analysis by Stuart-Macadam(1985), examined 752 individuals from a
Romano-British site Poundbury Camp located in Southwest England. The site is a Bronze
Age settlement and the burials date to the 4th century A.D. Burials included 206 juveniles
and 546 adults. All were assessed for presence and severity of porotic hyperostosis,
dental enamel hypoplasia, and metopism (retention of the metopic suture beyond the
normal age of closure). Severity was scored based on work of Haas and Nathan (1966)
and involves a gradient of light (scattered foramina), medium (large and small isolated
foramina and foramina that have linked to form a trabecular structure), and severe
(outgrowth in trabecular structure from the normal contour). Dental enamel hypoplasias
and metopism were scored as present or absent. Results indicated the more severe lesions
in the orbits and on the vault are seen almost exclusively on juvenile individuals. Further,
almost 40 percent show dental enamel hypoplasia. While there is no significant
difference in enamel hypoplasia between males and females, data indicates incidence of
hypoplasia is seen most frequently in individuals with porotic hyperostosis. StuartMacadam synthesizes clinical, anthropological, and physiological research to document a
relationship between skeletal indications of childhood stress.
The ability to assess the etiology of porotic hyperostosis and cribra orbitalia with
anemia is complicated. In the skeletal record, these cranial lesions are documented as
both disease and adaptation. More commonly seen in infants and juveniles, cranial
porosity is common in populations impacted by environmental, social, and economic
stressors. Reevaluating the etiology of these cranial lesions has implications for current
interpretations of disease and malnutrition in earlier populations as well as treatment in
43
modern clinical settings. The documentation of prevalence and severity of porotic
hyperostosis and cribra orbitalia across temporal and spatial boundaries will help clarify
the etiology of anemia as disease or as adaptation.
44
CHAPTER 3: HISTORICAL BACKGROUND
3.1 Geography of Portugal
Portugal is a small country rich in geographic and population diversity,
characterized by a tumultuous history of exploration, economic expansion, famine and
fortune. Portugal is a small coastal country that covers an area of 35,383 square miles,
including adjacent islands, the archipelagos of Madeira, and the Azores (Robinson 1979).
Portugal is bordered by the Atlantic Ocean to the north and west, and bordered by the
Mediterranean Sea to the south. Spain borders Portugal to the east, and shares the Iberian
Peninsula to the southeast (Figures 4 and 5). The boundaries of Portugal were fixed in
1297, before any other European country, making it Europe’s first “nation state”
(Birmingham 2003).
Figure 4. The Geography and Provinces of Portugal (Google Earth, accessed 04-01-13).
45
Figure 5. The Geography of Portugal in 1937 (Google Earth, accessed 04-01-13).
Geographically, Portugal shares the Castilian plateau, the Serra da Estrela, and the
Douro and Tagus rivers with Spain. Portugal is divided into eighteen districts (distritos)
in mainland Portugal: Aveiro, Beja, Braga, Braganca, Castelo Branco, Coimbra, Evora,
Faro, Guarda, Leiria, Lisbo, Portalegre, Porto, Santarem, Setubal, Viana do Castelo, Vila
Real, and Viseu (Birmingham 2003). Lisbon is the main port city in Portugal, located
where the Tagus River empties into the Atlantic Ocean along the central portion of the
western coastline (Figures 4 and 5).
3.2 Portuguese Landscape
The Portuguese landscape is divided into northern and southern regions along the
40th parallel. The topography varies from mountainous to lowlands, with most of the
lowlands in the southern region and the mountainous terrain to the north. Valleys are
46
carved between the mountains, with deep humid zones that receive considerable rainfall
per year. The country is characterized by a Mediterranean climate, vegetation, and
lifestyle. Fruit trees, vineyards, wheat, maize, barley and rye are commonly produced
resources. As a result of geography, northern habitation patterns are dense, scattered
settlements while the southern plains region is developed with large, separated
settlements.
3.3 History of Portugal
Cardoso (2006; 2007) presents a summary of the economic, social, and political
development of Portugal. Agriculture dominated the economic scene until 1900, and over
60 percent of the labor force was devoted to agricultural production. By the late 1800s,
industrial growth emerged in Lisbon. A drive to expand the domestic market occurred
slowly, with low productivity in all branches of textiles, metalworking, and food
production. Low productivity was due to national tradition of small familial or traditional
sectors that comprised industry (Cardoso 2007). As the main port city, Lisbon increased
more rapidly in industrial production. The development of Lisbon was a direct result in
emigration from outlying agricultural districts to supplement the labor force.
Birmingham (2003) outlines the development of the nation, whereby Portugal
began industrialization well after the rest of Europe. In the 1900s, the majority of farmers
were still engaged in subsistence level farming, while only the largest cities, such as
Lisbon, had developing industries – the majority of which were small and manufactured
traditional products of tiles, pottery, etc. Urban growth accelerated during the first half of
47
the 20th century due to large migrations of rural farmers into cities in search of work. As a
result, overcrowding produced poor living conditions for the working class and highly
impoverished. Portuguese society is largely Catholic and was reflected in the social and
cultural norms. For the most underprivileged members of society such as the sick, poor,
widows, and orphans, the family was still the basis for their support and survival. As a
result of urbanization, migration increased the disease load of city inhabitants where
overcrowding coincided with water sanitation issues. Stratification of classes punctuated
the period, whereby the middle class was subsumed into the elite and the working class
morphed into a peasantry.
A coastal city, Lisbon relied primarily on marine resources for protein and
consumed a variety of cereals such as wheat, barley, maize, and rye (Cardoso 2006).
Inland towns relied more on domesticated livestock such as cattle and sheep for protein,
and maize for starch (Cardoso 2006). Subsequently, nutritional disparities are evident
between port cities and inland towns in the historical and skeletal records. Shifts in
population health can be documented multiple ways in the skeletal record, to include:
higher morbidity and mortality rates, developmental disturbances, decreased stature, and
increased pathologies. The negative effects of urbanization have been documented in
various Portuguese collections from this time period, to include increased mortality rates
and decreased stature development (Cardoso 2008a; Cardoso 2008b; Matos 2009; Rios
and Cardoso 2009; Rogers 2009). Porotic hyperostosis and cribra orbitalia may help
illuminate the degree of disease stress and highlight health patterns related to
urbanization and diet breadth.
48
3.4 History of Luis Lopes Collection
The Lisbon identified skeletal collection, also known as the Luis Lopes
Collection, is housed at the Bocage Museum (National Museum of Natural History), in
Lisbon, Portugal. Cardoso (2006) describes the historical development of the collection.
The Luis Lopes Collection was started in 1981, when the Bocage Museum requested
permission from the Lisbon City Hall to collect the remains of individuals destined for
communal graves at select local cemeteries. Three Lisbon cemeteries provided the
majority of the skeletal material: Alto de S. Joao, Prazeres, and Benfica. At the time,
custom predicated the exhumation of individuals from temporary graves after 5 years
and/or complete skeletonization to allow for reuse of gravesites. If family failed to claim
the remains or failed to pay the fee for ossorio storage, remains were destroyed via
incinerator and included in a communal grave. For investigative purposes, the Bocage
Museum stepped in to collect and curate unclaimed remains and remains of individuals
where fees were unable to be paid (Cardoso 2006). Collection of skeletal material ceased
in 1991 with the retirement of the lead curation technician, Luis Lopes. Additional
collection and curation was reinitiated in 2000 by museum staff to alleviate data
organizational issues (Cardoso 2006).
As of 2006, the collection consists of over 1,692 skeletons at various stages of
curation. According to Cardoso (2006) demographic data is readily available for
approximately 700 individuals, which are the primary set available for study. Individuals
were collected between the late 1980s and 1991, and represent the remains of Portuguese
individuals who died in Lisbon between 1880 and 1975. Individuals were born between
49
the years of 1805 and 1972. A wealth of demographic data is available (i.e., sex, age-atdeath, cause of death, and birthplace). The collection includes individuals of Portuguese
nationality but some may have been born outside the country, or in Portuguese colonies
such as Mozambique, Portuguese India, or Brazil, Spain, France, or Italy. Common male
occupations include service and sales workers, skilled workers, craftsmen, and similar
occupations. Female occupations are most frequently recorded as housewife, but also
maid, teacher or student. The individuals in the Luis Lopes Collection represent the
middle to low socioeconomic classes, as seen by occupation of parents and place of
residence within Lisbon.
A review of the collection presented by Cardoso (2006) provides age, sex, and
demographic data. Ages at death range from birth to 98 years and both sexes are equally
represented. The highest frequency of age is 50 years or older, with a slight
overrepresentation of females (1:1.14). Sub-adults account for 126 skeletons (< 21 years)
of the 700 available for study (Cardoso 2006). Most of the individuals represented are of
middle to low socio-economic status of the city of Lisbon, a conclusion supported by
occupation data and the method of acquisition of the remains. During the early 20th
century, the health conditions in Portugal were notably among the lowest in Western
Europe (Cardoso 2007). The period for this study sample is approximately 1900-1960, a
period of history in Portugal characterized by isolation and an underdeveloped society
(Birmingham 2003). For individuals who died after 1959, demographic data is not
available in cemetery books, and must be located in death registration records (Cardoso
50
2006). To note, collection events between the late 1980s and 1991 were not selective, and
materials retrieved may represent the total population of the cemeteries (Cardoso 2006).
Since the Luis Lopes Collection became available for research, researchers have
descended upon it with fervor. Studies have addressed research related to stature
(Cardoso 2008b), pathology (Cardoso 2007; Matos 2009; Matos and Santos 2006), age
estimation (Cardoso 2008a; Rios and Cardoso 2009), entheses (Campanacho and Santos
2013), and sexing of juvenile remains (Albanese et al. 2005; Rogers 2009; Vlak et al.
2008). The breadth of demographic and historical data available in the collection
provides a unique opportunity for researchers to explore skeletal patterns.
3.5 Project Specifications
This study proposed that porotic hyperostosis and cribra orbitalia were markers of
stress related to social, economic, and environmental insult. Further, it explored iron
deficiency anemia by examination of porotic hyperostosis and cribra orbitalia on the large
historic modern sample of Portuguese nationals from the urban community of Lisbon.
Porotic lesions and cribra orbitalia were scored macroscopically according to the
procedures for data collection outlined by the codebook for the Global History of Health
Project (GHHP), modified from the Western Hemisphere Project (Steckel and Rose
2002). Buikstra and Ubelaker (1994) as adapted from Stuart-Macadam (1985) outline
additional standards for data collection useful in locational distinction of active or healed
lesions.
51
The methodology set forth by the GHHP was utilized as closely as possible, so as
to contribute to standardized data collection efforts. Thus, this study explores the level of
intra-population pathological variation within an historic Portuguese community. Data
collection is used to assess prevalence, severity, and cause of iron deficiency in a historic
population as a mark of adaptation.
The Luis Lopes collection in Lisbon was an ideal sample in which to examine
porotic hyperostosis and cribra orbitalia given the composition, preservation, and breadth
of demographic data. The reason for conducting a study into prevalence of porotic
hyperostosis and cribra orbitalia as related to iron deficiency anemia is to identify
corollaries between prevalence and diet, lifestyle, and geography. This information will
tell us more about populations in transition and give insight into the preservation and
understanding of lifeways in recent history with implications for older populations.
In an attempt to address the concerns outlined by Wood et al. (1992), a life table and
hazard model were generated from the sample in an effort to relate the prevalence of
anemic lesions to mean age-at-death and survivorship.
52
CHAPTER 4: MATERIALS AND METHODS
This study examined the presence and severity of cribra orbitalia and porotic
hyperostosis in the Luis Lopes indentified skeletal collection. Analyses completed
regarding porotic hyperostosis and cribra orbitalia in the Luis Lopes collection include:
1. A comparison of sub-populations by sex, age-at-death, and cause of death
(COD) to determine if there were differences in lesion presence and severity
among groups.
2. A comparison of known COD to incidence and severity of lesions to determine
diagnostic utility of scored lesions.
3. An investigation of mortality rates related to lesion incidence and severity.
4.1 Materials and Methods
This study utilizes the Luis Lopes collection of identified historic Portuguese
skeletons at the Bocage Museum in Lisbon, Portugal. The Luis Lopes collection
originates from modern cemetery sources and is comprised of 1,692 skeletons with basic
demographic data available for 700 individuals, to include age-at-death, place of birth,
occupation, and date and COD.
In all, the remains of 540 individuals were examined from the Luis Lopes
collection. Skeletal remains were in moderate to good condition. All individuals are
curated at the Bocage Museum and were collected from four cemeteries in Lisbon: Alto
de S. Joao, Prazeres, Benfica, and S. Joao da Pesqueira. The known age-at-death
53
distribution for all identified individuals in the sample is given in Figure 6. The sample is
skewed toward middle to later adult age.
Figure 6. Age-at-death distribution of total sample (n = 540). Note panel A is for 1-50
years of age while panel B is for 51-98 years of age.
For analysis, age cohorts were organized into cohorts of five-year increments,
except the first and last decade whereby cohorts are organized in ten-year cohorts (see
Table 1). The first and last cohorts were expanded to ten years to ensure adequate sample
size. All age cohorts were assigned a unique numerical code (see Appendix A). The
youngest individual was one year of age-at-death and the oldest individual was 98 years
of age-at-death. Year of birth ranges from 1806 to 1950, and year of death ranges from
1880 to 1970. Sexes were approximately equal in representation and include 281 females
(52% of total population) and 259 males (48% of total population).
54
Table 1. Age distribution of the total sample.
Age (years)
Count
% of Pop.
0-10
11-15
16-20
21-25
26-30
31-35
36-40
41-45
46-50
51-55
56-60
61-65
66-70
71-75
76-80
81-85
86-90
91-100
Total
17
9
17
22
16
22
11
19
39
46
34
46
49
54
54
52
27
6
540
3.15%
1.67%
3.15%
4.07%
2.96%
4.07%
2.04%
3.52%
7.22%
8.52%
6.30%
8.52%
9.07%
10%
10%
9.63%
5.00%
1.11%
100%
In this study, each cranium was examined for porotic hyperostosis and cribra
orbitalia. Measurement of lesions can be examined macroscopically, microscopically, and
via radiographic techniques. This investigation examined the level of physiological
impact at the macroscopic level. Data collection and analysis followed the standard set by
Global Health History Project (GHHP) codebook (2006) adapted from an earlier version
created for the Western Hemisphere Project (Steckel and Rose 2002). The presence and
stages of severity were visually assessed on the cranial elements, to include ectocranial
55
surfaces and roof of eye orbits. Presence/absence and severity of expression were
recorded according to the GHHP scale of 0-3.
The progression of porosity for cribra orbitalia was scored in four stages:
0
No orbits present for observation.
1
Absent with at least one observable orbit.
2
A cluster of mostly fine foramina covering a small area (</= 1cm3).
3
Substantial areas (> 1cm3) covered by a small and/or larger foramina with
a tendency to cluster together.
The progression of porosity for porotic hyperostosis was scored in four stages:
0
No parietals present for observation.
1
Absent with at least one observable parietal.
2
Presence of slight pitting or severe parietal porosity.
3
Gross parietal lesion with excessive enlargement of bone.
Original data collection differentiated between right and left sides for both types
of lesions. The GHHP handbook indicates lesions need only be present in one orbit or
one portion of the cranial vault in order to generate a cumulative porosity score for the
individual. If only one orbit or one parietal exhibited lesions and the other did not, the
highest score assigned was used for this study. For example, take scores for Individual X:
right orbit = “0”, left orbit = “1”, whereby 0 indicates absent and 1 indicates present, then
cribra orbitalia was scored as “1” or “present” for Individual X. The same methodology
56
applies to severity scale, where if the right orbit = “3” and left orbit = “1”, the individual
receives a cumulative cribra orbitalia severity score of “3”.
In paleopathology studies, cribra orbitalia and porotic hyperostosis are commonly
reported in concert with one another due to the perceived relationship between diploë
expansion, porosity, and iron metabolism. Both types of lesions are viewed as indicators
of general health. To review cranial lesions more generally, the presence and severity of
cranial lesions was explored by differentiating individuals who show the same lesion or
combination of lesions into separate categories. Individuals were assigned a numerical
score according to a four-code “PHCO” system, whereby:
0
no cribra orbitalia; no porotic hyperostosis
1
only cribra orbitalia
2
only porotic hyperostosis
3
both cribra orbitalia and porotic hyperostosis are present
This study examined the practicality of the use of macroscopic analysis of porotic
hyperostosis and cribra orbitalia as a tool for bioarchaeological analysis of environmental
insult, status, genetic robusticity, and overall health.
4.2 Statistics
A Kruskal-Wallis (KS) nonparametric ANOVA was performed to test the null
hypothesis that there was no significant difference in age-at-death distribution between
males and females. ANOVAs are well suited to assessing a continuous variable in
57
conjunction with a categorical variable, like the tests here. For analyses comparing lesion
presence or severity to sex, a Pearson’s Chi-square was used to detect concordance
between porosity and sex. A chi-square will assess two categorical variables to test for
significance. Chi-square was selected for these analyses as both variables are categorical.
For these tests, a significant chi-square value indicates that porosity differs between
males and females. Significance of all chi-square tests is assessed at an alpha level of
0.05 ( < 0.05).
For analyses comparing lesion presence or severity to age-at-death or COD data, a
one-way analysis of variance (ANOVA) or Kruskal-Wallis (KS) rank sum test was
applied. The one-way ANOVA assumes that samples are independent, normally
distributed, and have equal within-group variances, whereas the KS test is nonparametric
and does not make assumptions about the underlying distribution of data. For these tests,
a significant p-value indicates that porosity differs among age-at-death or COD
categories. Significance of ANOVA or KS tests was assessed at an alpha level of 0.05. If
an ANOVA or KS test yielded a p-value of < 0.05, a post-hoc Tukey’s HSD test for
comparison of means was applied to determine which pairwise comparisons might have
contributed to the overall significance.
As described in Wood et al. (1992), there are documented patterns in human
mortality. Life begins with a high hazard of dying and fluctuates relative to subsequent
age. The hazard decreases to a low hazard in young adulthood, and increases with age as
degenerative illnesses and compromised immunity increase. To assess mortality rates, a
life table and Gompertz Hazard model were calculated. A Gompertz hazard model was
58
generated to describe human mortality and inform individual risks of disease and death as
seen in Wood et al. (1992). The Gompertz law states that the force of mortality increases
exponentially over time, whereby the hazard rate function:  > 0 and  > 0. The alpha
parameter controls the absolute value of the increasing hazard (mortality), while the beta
parameter controls the curvature of the hazard (senescence). A Gompertz model
distribution is preferable when demographic sample age cohorts are differentially
represented in the sample such as the Luis Lopes collection. Results were matched to
census and mortality data.
All statistical analyses were performed using Microsoft Excel (2008) and R
Statistical Computing software, version 3.0.2. Scripts for the Gompertz model were
provided by Dr Kanya Godde who modified them from coding written by Dr. Lyle
Konigsberg. Dr Lyle Konigsberg’s R programs are available at http://konig.la.utk.edu
(Konigsberg 2013).
59
CHAPTER 5: RESULTS
5.1 Demographic Data
Distribution of sexes across age intervals was not equal, but reflective of a natural
mortality sample. Sexes were approximately equal in representation and include 281
females (52% of total population) and 259 males (48% of total population). The mean
age-at-death differed between males (53.980 years) and females (61.953 years). A KS
rank sum test showed a statistically significant difference at the p < 0.05 level in age for
both sexes (p-value < .0001) indicating differences in survivorship in favor of female
longevity by approximately eight years.
Fifty-nine COD categories were established from formal death registration
records available at the Bocage Museum (see Appendix B). COD categories are
represented by as few as one individual (e.g. asthma, category 59) to a maximum of
eighty-two individuals (e.g., tuberculosis, category 52), with a mean representation of
9.152 individuals per category. COD categories were consolidated according to major
illness or disease. For example, death registration records indicated generalized
tuberculosis, pulmonary tuberculosis, and also acute tuberculosis. All documented forms
of tuberculosis were included under the collective COD category 52, tuberculosis (n=82).
5.2 Lesions
In this study, each cranium was examined for porotic hyperostosis and cribra
orbitalia according the GHHP scale of 0-3. In the Luis Lopes sample, cribra orbitalia was
60
documented with greater frequency than porotic hyperostosis. Some form of lesion(s)
was present in approximately half of the sample. Of the 540 individuals, a total of 289
individuals display no lesions, 160 individuals display only cribra orbitalia, 35
individuals display only porotic hyperostosis, and 56 individuals display a combination of
both cribra orbitalia and porotic hyperostosis (see Figure 7). These sums account for all
lesion activity, regardless of severity. While many of the lesions are small in size, others
are large and produce ectocranial expansion of the affected area (see Figure 8).
Figure 7. Summary incidence of lesions.
According to the GHHP scale of severity, individuals with severe taphonomic
impact to the orbit or vault regions were scored as zero on the severity scale, indicating
61
the element was not present or unable to be scored. A score of zero was reported for 17
cases. Of the 540 individuals scored, cribra orbitalia was unable to be scored on 10
individuals with no orbits, and porotic hyperostosis was unable to be scored on seven
individuals with cranial vault absence or taphonomic disruption. These 17 individuals
represent three percent of the total sample and were maintained in the study for their
contribution to the respective lesion type displayed.
Figure 8. Cranial lesions. From top left: cribra orbitalia in right and left orbits, stage 3;
top right: cribra orbitalia in left orbit, stage 2; bottom right: cribra orbitalia in right and
left orbits, stage 3; bottom left: porotic hyperostosis on cranial vault; stage 2. Photo 1-4
of lesion severity. Scale in centimeters.
62
5.3 Statistical Analyses
Statistical analyses were conducted using Pearson’s Chi-square, one-way analysis
of variance (ANOVA), Kruskal-Wallis (KS) nonparametric analysis of variance, and
Tukey’s HSD test for comparison of means. Statistical analyses were conducted to
investigate the interaction between porosity and sex, age, and COD categories in relation
to mortality. Differences in and between cribra orbitalia and porotic hyperostosis were
assessed by type, presence, and severity and yielded significant results in only ten tests.
Statistical results are reported in Table 2.
Table 2. Summary statistics from all comparisons between cribra orbitalia and porotic
hyperostosis to sex, age-at-death, and COD variables.
Comparison
Test
df
F-value/chi square value
p-value
CO presence by Sex
Chi-sq
1
0.0606
0.8056
CO severity by Sex
Chi-sq
2
0.1476
0.9289
CO presence by Age
ANOVA
1
1.2889
0.2568
CO presence by Age
KS
17
31.0990
0.0194*
CO severity by Age
ANOVA
1
3.2355
0.0726
CO severity by Age
KS
17
37.5138
0.0029*
CO presence by COD
KS
57
76.2356
0.0453*
CO severity by COD
KS
57
84.1888
0.0111*
PH presence by Sex
Chi-sq
1
6.3830
0.0115*
PH severity by Sex
Chi-sq
2
6.6836
0.0354*
PH presence by Age
KS
17
50.2272
0.0000*
PH severity by Age
KS
17
50.1409
0.0000*
PH presence by COD
KS
58
60.1975
0.3962
PH presence by COD
KS
58
60.1975
0.3962
63
Table 2. continued
PH severity by COD
KS
58
59.8944
0.4068
PHCO presence by Sex
KS
1
2.3492
0.1254
PHCO severity by Sex
KS
1
0.5052
0.4772
PHCO presence by Age
KS
17
39.0189
0.0018*
PHCO severity by Age
KS
17
39.8919
0.0013*
PHCO presence by COD KS
58
71.2962
0.1128
PHCO severity by COD
15
15.2066
0.4366
KS
* Significant value (<0.05)
Cribra Orbitalia
According to KS tests, there were no significant differences in presence or
severity of cribra orbitalia lesions between the sexes (see Table 2). One-way analysis of
variance (ANOVA) and Kruskal-Wallis (KS) tests were applied to comparisons of cribra
orbitalia presence and severity to age-at-death. According to the one-way ANOVA there
was no significant difference in presence and severity among age-at-death categories. In
contrast, the KS test results show significant differences in both presence and severity
among age-at-death categories. The KS test may be picking up on the higher than average
frequency of cribra orbitalia in two age cohorts: 11-15 and 91-100 years of age-at-death
(see Figures 9 and 10).
64
Figure 9. Average presence of cribra orbitalia by age–at-death cohort. Note, panel A
represents age cohorts 1-9 (ages 0-50), and panel B represents age cohorts 10-18 (ages
51-100).
Initial application of a KS nonparametric rank sum test between cribra orbitalia
and COD data yields significant results (see Figures 11 and 12). A post-hoc Tukey’s
HSD test indicates no significant differences at the alpha level (0.05) in any crosswise
comparisons, thus suggesting the KS test is picking up on the unequal distribution of
individuals across COD categories. Fibrosis (COD category 2, Appendix B) is one of the
65
Figure 10. Average severity of cribra orbitalia by age-at-death cohort. Note, panel A
represents age cohorts 1-9 (ages 0-50), and panel B represents age cohorts 10-18 (ages
51-100). Severity measured according to GHHP 0-3 scale, whereby “0” indicates absence
of skeletal element and “1” indicates element presence but absence of lesions.
lowest represented categories (n = 2), and the high severity scores seen in both
individuals may be skewing the KS and Tukey’s HSD significance tests. When COD
categories representing less than five individuals are removed from analysis, the KS test
yielded no significant differences in crosswise comparisons.
66
Figure 11. Average presence of cribra orbitalia by COD category. Note, panel A
represents categories 1-20, panel B represents categories 21-40, and panel C represents
categories 41-59.
67
Figure 12. Average severity of cribra orbitalia by COD category. Note, panel A
represents categories 1-20, panel B represents categories 21-40, and panel C represents
categories 41-59. Severity measured according to GHHP 0-3 scale, whereby 0 indicates
absence of skeletal element and 1 indicates element presence but absence of lesions.
68
Porotic Hyperostosis
According to chi-square comparisons, porotic hyperostosis presence and severity
of expression are positively associated with sex (see Table 2). Twenty-three percent
(23%) of males and thirteen percent (13%) of females display porotic lesions on the
cranial vault. The null hypothesis that the mean presence of lesions is equal between
sexes is therefore rejected. Porotic hyperostosis is infrequent in the sample and the degree
of severity is also notably low. Mean severity score ranges from 1.15 (female) to 1.2
(male) on the GHHP severity scale of 0-3, whereby a score of ”1” indicates the skeletal
element is present but the lesions are not present. This means that the population trends
towards barely discernible porotic lesions.
Figure 13: Average porotic hyperostosis presence by sex.
69
Figure 14: Average porotic hyperostosis severity by sex.
Severity measured according to GHHP severity scale of 0-3.
Porotic hyperostosis is present in 10 of 18 age-at-death cohorts (Figure 15).
Comparison of lesion presence and severity to age-at-death data showed differential
presence and severity among age-at-death categories ( < 0.05). Initial application of a
KS test between porotic hyperostosis and age-at-death data yielded significant results
(see Table 2). Post-hoc comparisons using the Tukey’s HSD test indicated that the mean
score for age-at-death cohort 7 (36-40 years) was significantly different from other age
categories (see Tables 3 and 4). Post-hoc Tukey’s HSD comparison of severity also
indicates the mean score for age-at-death cohort 7 was significant and displayed the
greatest overall severity of porotic hyperostosis (see Table 4).
70
Figure 15. Average porotic hyperostosis presence by age-at-death cohort. Note, panel A
represents age cohorts 1-9 (ages 0-50), and panel B represents age cohorts 10-18 (ages
51-100).
Table 3. Significant results yielded from Tukey’s HSD crosswise comparison between
porotic hyperostosis and age-at-death cohort.
Cohort Comparison
Age cohort 1
Age cohort 2
P-value
3-1
7-1
16-20
36-40
0-10
0-10
0.0173779
0.0008673
15-3
76-80
16-20
0.0237474
16-3
81-85
16-20
0.0071705
17-3
86-90
16-20
0.0570122
71
Table 3. continued
7-6
36-40
31-35
0.0249444
9-7
46-50
36-40
0.0074464
11-7
56-60
36-40
0.0070367
12-7
61-65
36-40
0.0419644
13-7
66-70
36-40
0.0151805
14-7
71-75
36-40
0.0073262
15-7
76-80
36-40
0.0010913
16-7
81-85
36-40
0.0003160
17-7
86-90
36-40
0.0030634
Table 4. Significant results yielded from Tukey’s HSD crosswise comparison between
porotic hyperostosis severity and age-at-death cohort.
Cohort Comparison
Age cohort 1
Age cohort 2
P-value
3-1
7-1
16-20
36-40
0-10
0-10
0.0541296
0.0047758
16-3
81-85
16-20
0.0266525
9-7
46-50
36-40
0.0274752
11-7
56-60
36-40
0.0262512
13-7
66-70
36-40
0.0783357
14-7
71-75
36-40
0.0271173
15-7
76-80
36-40
0.0098975
16-7
81-85
36-40
0.0020798
17-7
86-90
36-40
0.0133918
According to nonparametric KS tests, there are no significant differences in
presence or severity of expression between porotic hyperostosis and COD.
72
Cribra Orbitalia and Porotic Hyperostosis
To review cranial lesions more generally, the following section explores the
presence and severity of cranial lesions by differentiating individuals who show the same
lesion or combination of lesions into separate categories. Pearson’s Chi-square and
Kruskal-Wallis (KS) rank sum tests were applied to assess the frequency of lesion
combinations to sex, age, and COD variables, according to the four-code PHCO system.
Overall, porotic hyperostosis is seen far less frequently than cribra orbitalia in the Luis
Lopes collection, but when lesions are documented together on the same cranium, they
occur twenty-five percent more frequently in males.
Figure 16. Frequency of lesion type organized by sex.
73
A KS test comparing PHCO presence to age-at-death data yielded a significant pvalue of 0.0018 (see Table 2). The distribution of lesion type across age cohorts is seen in
Figure 17. In early life, it appears uncommon for individuals to exhibit only porotic
hyperostosis. It is more common to show both types of lesions or cribra orbitalia alone
than to exhibit only porotic hyperostosis. Approaching middle age to later adulthood, the
proportion of individuals showing no lesions is notable for two reasons: 1) the frequency
of individuals not showing lesions far outnumbers the number of individuals with lesions,
but 2) the age cohorts representing middle to late adult years are better populated. More
individuals were dying in the age cohorts where the greatest number of individuals
showing no lesions is seen. This pattern of equal numbers of people dying with and
without lesions may be attributed to healing of lesions or a shift in population
distribution.
For age-at-death, the Tukey’s post-hoc comparison showed a statistically
significant difference at the p < 0.05 level between age cohorts 7 and 16 (Table 5). Posthoc Tukey’s comparison of means and review of Figure 17 indicates 36-40 years (cohort
7) was the only age cohort where individuals that only exhibited cribra orbitalia represent
lowest within-cohort frequency. All other age cohorts consistently display cribra orbitalia
with greater frequency than other within cohorts lesion combination possibilities. Cribra
orbitalia is more than twice as common as porotic hyperostosis in the Luis Lopes
collection, which makes the low distribution in age cohort 7 notable.
74
Table 5. Significant results yielded from Tukey’s HSD crosswise comparison between
PHCO lesions to age-at-death cohort.
Cohort Comparison
Age cohort 1
Age cohort 2
P-value
9-7
46-50
36-40
0.0665720
15-7
76-80
36-40
0.0733939
16-7
81-85
36-40
0.0240227
Figure 17. Frequency of lesion type organized by age-at-death cohort. Note, panel A
represents age cohorts 1-9 (ages 0-50), and panel B represents age cohorts 10-18 (ages
51-100).
75
No association is seen between presence of both lesion types and age-at-death, but
KS tests do identify a trend between concurrent severity and age-at-death cohort (p-value
= 0.0013). Figure 18 illustrates the distribution of severity across age intervals. Note that
not all age cohorts are equally represented. A post-hoc Tukey’s comparison of means
indicates age-at-death cohort 2 (11-15 years) is different than most other age cohorts, in
particular middle to older adult age (see Table 6). Mortality between the ages of 11-15 is
low (< .02 of total population), but level of lesion severity is consistently higher (see
Figure 18).
Table 6: Significant results yielded from Tukey’s HSD crosswise comparison between
PHCO lesion severity to age-at-death cohort.
Cohort Comparison
Age cohort 1
Age cohort 2
P-value
6-2
31-35
11-15
0.0179713
9-2
46-50
11-15
0.0091285
11-2
56-60
11-15
0.0144681
12-2
61-65
11-15
0.0337509
13-2
66-70
11-15
0.0053978
14-2
71-75
11-15
0.0089055
15-2
76-80
11-15
0.0120131
16-2
81-85
11-15
0.0046894
No significant difference was seen among COD categories and combined PHCO
severity (Table 2). It is worth noting that there was a highly unequal distribution of
76
individuals among COD categories. Figure 19 illustrates the sum of individuals that
displayed each level of lesion severity by COD.
Figure 18. Distribution of lesion severity across age-at-death cohorts. Note, panel A
represents age cohorts 1-9 (ages 0-50), and panel B represents age cohorts 10-18 (ages
51-100).
77
Figure 19. Distribution of lesion severity across COD categories. Note, panel A
represents categories 1-20, panel B represents categories 21-40, and panel C represents
categories 41-59.
78
Figure 20. Average lesion severity by COD category when porotic hyperostosis and
cribra orbitalia are reviewed collectively. Note, panel A represents categories 1-20, panel
B represents categories 21-40, and panel C represents categories 41-59.
Gompertz Hazard Model
A Gompertz model is preferable when age cohorts are differentially represented
as in this study. The Gompertz model produced  and  parameters of = 0.001449602
and = 0.053574250. The Gompertz hazard model appeared to have a good fit to
survivorship (see Figure 21).
79
Figure 21. Survivorship by Age for the Luis Lopes Collection using a Gompertz hazard
model.
The stepped line indicates the confidence interval for survivorship and the solid
line indicates the Gompertz hazard curve. The survivorship curve produced for the Luis
Lopes collection by the Gompertz hazard function indicates moderate population decline
from birth to early adulthood. In early life, survivorship is lower than the expected
hazards. Survivorship declines steadily from birth to middle age. Approaching middle
80
age (~ 40 years), survivorship intersects with the Gompertz hazard curve, and
survivorship saddles the curve into late adulthood. Near age sixty, survivorship rises
above the hazard curve suggesting individuals who reach late adulthood have overcome
many hazards. After age eighty, the hazard of dying increases exponentially and
survivorship falls below the hazard curve.
Life Table
Many individuals survive past age seventy in the Luis Lopes collection. The
mortality pattern has important implications for our understanding of the living
population that produced the study sample. Demographic records denote place of birth
for individuals in this sample, which indicate regional movement occurred in the lifetime
of this population. City of birth spans the country of Portugal, but all individuals died in
Lisbon, which characterizes a population that was neither insular nor stationary. The sex
ratio of the collection includes 259 males per 281 females. The age distribution of the
population is outlined in Table 7. Approximately 3% of the population is under age 10;
12% is under age 25; 39% is under age 50; and 84% is under age 80. The life table shows
age-specific mortality and indicates mortality is low in early life, drops in middle age,
and evens out in later adulthood. Life expectancy at birth is strong (ex = 63.67 years), and
maintains a consistent survivorship prediction through adulthood. The mortality rate
steadily increases from birth, but between 45-50 years of age the mortality rate doubles
from approximately 4-10%. At age sixty, mortality decreases slightly and then continues
on an upward trend.
81
Table 7: Life Table for the Luis Lopes Collection.
x
Dx
dx
lx
qx
0
0
0.0000
1.0000
0.0000
10
17
0.0306
1.0000
15
9
0.0162
20
17
25
Lx
Tx
ex
cx
agetest
10.0000 63.6667
63.67
0.1571
0.0157
0.0306
4.9234
53.6667
53.67
0.0773
0.0155
0.9694
0.0167
4.8063
48.7432
50.28
0.0755
0.0151
0.0306
0.9532
0.0321
4.6892
43.9369
46.10
0.0737
0.0147
22
0.0396
0.9225
0.0430
4.5135
39.2477
42.54
0.0709
0.0142
30
16
0.0288
0.8829
0.0327
4.3423
34.7342
39.34
0.0682
0.0136
35
22
0.0396
0.8541
0.0464
4.1712
30.3919
35.59
0.0655
0.0131
40
11
0.0198
0.8144
0.0243
4.0225
26.2207
32.20
0.0632
0.0126
45
19
0.0342
0.7946
0.0431
3.8874
22.1982
27.94
0.0611
0.0122
50
39
0.0703
0.7604
0.0924
3.6261
18.3108
24.08
0.0570
0.0114
55
46
0.0829
0.6901
0.1201
3.2432
14.6847
21.28
0.0509
0.0102
60
34
0.0613
0.6072
0.1009
2.8829
11.4414
18.84
0.0453
0.0091
65
46
0.0829
0.5459
0.1518
2.5225
8.5586
15.68
0.0396
0.0079
70
49
0.0883
0.4631
0.1907
2.0946
6.0360
13.04
0.0329
0.0066
75
54
0.0973
0.3748
0.2596
1.6306
3.9414
10.52
0.0256
0.0051
80
54
0.0973
0.2775
0.3506
1.1441
2.3108
8.33
0.0180
0.0036
85
52
0.0937
0.1802
0.5200
0.6667
1.1667
6.47
0.0105
0.0021
90
27
0.0486
0.0865
0.5625
0.3108
0.5000
5.78
0.0049
0.0010
100
6
0.0108
0.0378
0.2857
0.1892
0.1892
5.00
0.0030
0.0003
Key: x = age interval; Dx = # of deaths in the interval x; dx = proportion of deaths for the
interval x; lx = survivorship, proportion of pop that is alive at the beginning of the age
interval; qx = age specific probability of death; Lx = people years live in the age interval;
Tx = total people years to be lived; ex = life expectancy, mean age-at-death; cx =proportion of individuals alive in the interval, the living population structure; age test =
the population pyramid, divide by the width of the interval.
82
CHAPTER 6: DISCUSSION
Diagnostic utility of lesions is important for paleopathological studies. Without an
understanding of how the body responds to stress, and an accurate understanding of how
reliable analyses are, then scoring of cribra orbitalia and porotic hyperostosis frequency
lacks validity in making determinations of population health. In archaeological and
clinical studies, stress related to poor iron metabolism has been linked to genetic, dietary,
and environmental factors. Confronting the significance of these lesions provides a more
rounded understanding of skeletal stress as related to anemia.
This study examined the practicality of macroscopic analysis of porotic
hyperostosis and cribra orbitalia as a tool for bioarchaeological analysis. This study
explored the level of intra-population pathological variation to understand the
relationship between health and mortality as a mark of adaptation. The project examined
a large historic population alive during a period of documented social, environmental,
and economic disparity (Cardoso 2006). The results of several hypotheses are addressed
here.
It was hypothesized that both sexes would have the same distribution of cribra
orbitalia and porotic hyperostosis with no significant difference of distribution. Instead,
analyses determined males exhibited a greater frequency and severity of porotic
hyperostosis than their female counterparts, and males were twenty five percent more
likely to exhibit concurrent display of porotic hyperostosis and cribra orbitalia.
83
The hypothesis that females and children would show a greater frequency of
lesions was based on existing bioarchaeological and clinical research of iron deficiency
related to pregnancy, child rearing and early childhood development. Analyses
determined that sub-adults showed a higher overall mean frequency of cribra orbitalia per
age cohort. Of all age cohorts, the subadult age cohort of 11-15 year olds showed the
most consistent within-cohort severity of cribra orbitalia. All but one of nine individuals
exhibited cribra orbitalia, and all eight who did display cribra orbitalia yielded the highest
severity score of “3” on the GHHP severity scale. These results confirm the hypothesis
that children will show a greater frequency of cranial lesions.
Another hypothesis stated that age-at-death cohorts would exhibit a
fluctuation in lesion frequency over the span of a lifetime. Frequency did fluctuate, but
showed a good correlation to the Gompertz Hazard curve (Figure 21). Between the ages
of 51-70 years the number of individuals who were free of lesions is conspicuously
higher than those who did exhibit lesions (age cohorts 10-13, Appendix A). The number
of individuals without lesions outweighed the frequency of those with lesions until ageat-death reaches 85 years. If individuals survived to age 85, lesions dramatically
increased and were present on fifty percent or more of the age sample. In Figure 21, the
Gompertz Hazard curve declines and survivorship increases between the ages of
approximately 50-80 years of age-at-death.
It was also hypothesized that frequency of lesions would provide diagnostic
utility in comparison of mortality to COD categories. Statistical analyses used in this
study were unable to clearly determine a relationship between lesion frequency and COD.
84
Significance tests indicated COD category 2 consistently yielded the most severe lesions,
however, these results were biased as numbers of individuals among COD categories
were not consistent. Category 2 (n=2) represents a disproportionate segment of the total
population (n=540) where fifty-nine COD categories were represented (see Appendix B).
The significance of category 2 (fibrosis) may be interpreted in two ways: 1) COD
category 2 validates an association between lesion severity and COD, or 2) a larger
sample of category 2 needs to be included to balance and/or confirm the results.
Additional KS tests comparing lesions to COD categories where n > 5 and n > 10
contradict the significance values seen when all COD categories were included.
The diagnostic utility of lesions as a mark of individual adaptation to stress
yielded significant results. It was hypothesized that expression of lesions would reflect an
elevated mortality hazard if lesions were a sign of poor health, or that increased lesion
frequency would be associated with survivorship if lesions were a sign of adaptation.
Analyses found that mean frequency and mean severity are higher in young adulthood
through middle age, a period where mortality is lowest in the age span of the population
(see Table 7). More people were surviving, but those who are dying in young adulthood
through middle adulthood were showing a greater incidence of lesions. Individuals who
did not show lesions in later adulthood may be explained in one of three different ways:
1) these individuals have experienced remodeling of affected areas from earlier life and
represent the healthiest of the population who overcame compromised health; 2) these
individuals may have never experienced the skeletal impact of poor iron metabolism; or,
85
3) these individuals succumbed to injury or ailment before immunodeficiencies could be
displayed skeletally; selective mortality as discussed by Wood et al. (1992).
It was hypothesized that differences would be seen between lesion presence and
severity to sex, age-at-death, and COD data. Individuals subjected to the greatest stress
were expected to display higher severity scores as related to stress manifested from
lifestyle patterns reflected by economic and social changes. Regarding severity, only
fifty-six individuals display both cribra orbitalia and porotic hyperostosis at the time of
death; thirty-five are male (62.5%) and twenty-one are female (37.5%). Either cribra
orbitalia or porotic hyperostosis was present in each age cohort, but concurrent affliction
is infrequent. Age cohorts 10 and 12 yield the highest incidence of concurrent lesions at
eight cases per cohort. Lesion presence and severity compared to sex and COD data
yielded non-significant results (Figures 19 and 20).
In sum, this study was designed to explore the relationship between prevalence,
severity, and cause of iron deficiency related to health and mortality. The use of a known
demographic sample helped alleviate unknowns typically encountered in archaeological
samples. Statistical analyses yielded significant differences in the frequency and severity
of cribra orbitalia and porotic hyperostosis across sex, age, and COD categories.
86
CHAPTER 7: CONCLUSIONS
This study explored the relationship between skeletal stress and anemia in a
modern historic population. The Luis Lopes skeletal collection at the Bocage Museum in
Lisbon, Portugal was chosen because it represented the middle to low socioeconomic
classes historically subjected to higher incidence of socioeconomic stress. In addition, the
composition, preservation, and breadth of demographic data available in the Luis Lopes
collection provided an added degree of confidence to findings. The goal of this study was
to gather information about a population in transition to give insight into lifeways in
recent history, which may have implications for a better understanding of older
populations.
Bioarchaeologists have documented porotic hyperostosis and cribra orbitalia in
both prehistoric and historic contexts worldwide and commonly use both conditions to
assess health and nutritional status on a population scale (Armelagos and Cohen 1984;
El-Najjar et al. 1975; El-Najjar and Robertson 1976; El-Najjar et al. 1976; Mittler and
Van Gerven 1994; Pechenkina et al. 2002; Steckel and Rose 2002; Walker 1985; Walker
1986; Zaino and Zaino 1975). Since mid-century, iron deficiency has been the widely
held explanation for incidence of cranial lesions. Modern clinical studies of irondeficiency anemia (Kent et al. 1994) and radiographic evidence for cranial vault marrow
hypertrophy (Stuart-Macadam 1987b) support these data. Regardless of a unifying
etiology, porotic hyperostosis and cribra orbitalia appear as unifying indicators in the
87
skeletons of individuals who have endured compromised conditions whether they be tied
to nutrition, sanitation, or infectious disease.
Clinical studies have confirmed the link between cribra orbitalia and porotic
hyperostosis, (Cook 1990; Stuart-Macadam 1987b). Stress can manifest in a number of
ways, but it is a force that can have a significant impact on the human body if it is not
buffered. Physiological disruptions such as interruption of bone development, growth,
and maintenance may occur. Reaction to and survival of stressors involves the whole
body system. If the body is unable to effectively respond to stressors, physiological
changes such as porotic hyperostosis and cribra orbitalia may affect the bones (Goodman
et al. 1988). It is important to remember that a sample may not show any markers of
disease, and those who do display lesions may represent individuals who survived with
the disease long enough for skeletal impact to occur. In line with the Osteological
Paradox, hidden heterogeneity in risk and selective mortality are factors that may explain
the conflicting data skeletal samples sometimes yield (Wood et al. 1992).
The results of this study can be related back to the concepts presented by Wood et
al. (1992) in the Osteological Paradox. Two questions posed in their paper were
addressed in this project and will be explained below: 1) do skeletal lesions always
indicate an elevated risk of death or might they actually indicate healthy individuals who
were able to elicit a bony response to a stress event, and 2) to what extent does variation
of well-being in a living population affect the patterns of skeletal lesions seen in a
skeletal assemblage. The implication of these two topics is that if a skeletal lesion varies
in its relationship to risk of death, both by age cohort and across populations, then
88
comparing health across past populations using skeletal lesions will be confounded and
disputed by this variation.
The Luis Lopes collection yields complex data that, in the absence of genetic
analysis, may best be explained by the Osteological Paradox. Males in the Luis Lopes
collection showed a higher incidence of porotic hyperostosis and combined lesions, while
also exhibiting a younger mean age-at-death. However, porotic hyperostosis is the least
represented form of lesion in the population. Therefore, data suggests porotic
hyperostosis is the strongest informant of increased mortality when looking at sex. Cribra
orbitalia is highly prevalent in the collection, but proportionally distributed among sexes.
Age cohorts which showed the highest mean incidence of porotic hyperostosis or
concurrent expression of lesions are of early adolescence (age category 2, 11-15 years)
and early adulthood (age category 7, 36-40 years). The mortality risk associated with
these lesion types correspond to the Gompertz Hazard model, which plotted a
survivorship curve below the overall hazard of dying, until approximately age forty.
Broadly, COD data failed to illuminate any significant patterns between lesion
presence and severity related to mortality. At this time, knowledge of known COD data in
this collection does not contribute to a greater understanding of how cranial lesion
presence and severity relate to the overall health of the population.
This collection represents a sample of individuals of the lowest socioeconomic
status in early historic urban Lisbon where diet and environment driven stressors were
expected. The country was experiencing a sociopolitical upheaval that would have
contributed to compromised economic viability of working class individuals and
89
compromised nutritional access and health care. The younger mean age-at-death and
higher incidence of concurrent lesion expression in males suggests lesion activity may be
an indication of increased stress rather than a sign of health and ability to withstand
external stressors.
7.1 Future Directions
The state of research in skeletal biology necessitates continued theoretical
expansion into issues of hidden risk, individual frailty, mortality, and pathological
processes. This study provides insight into skeletal stress and intra-population mortality,
but more work needs to be done across populations. Further study would benefit from
examination of inter-populational data to better illuminate how variables impacting
mortality such as sex, age, and COD are impacted by diet and geography.
Further study with the Luis Lopes collection is necessary. While macroscopic
analyses are informative and methodologically more approachable to replicate, future
research would benefit from microscopic and genetic data in investigation of the etiology
of iron metabolism in the skeletal record. More detailed examination of COD data at the
level of organ system may yield finer conclusions. Causes of death related to circulatory
and respiratory system failure were prevalent in this study, therefore an exploration into
COD from a generalized systems approach may yield new information that COD
specificity overlooks. To better understand the relationship between cranial lesions and
risk of death, incorporation of occupational data may inform the relationship between
occupational hazard and mortality.
90
Most important, analysis of covariance and regression analysis is necessary to
understand how the variables of sex, age-at-death, and COD interact to impact the
presence and severity of cribra orbitalia and porotic hyperostosis. The singular impact of
each variable is informative, but fails to weave together the collaborative impact
socioeconomic factors impacting health over time.
91
Appendix A. Date Code: Age Cohort
Cohort No.
Age range (years)
1
0-10
2
11-15
3
16-20
4
21-25
5
26-30
6
31-35
7
36-40
8
41-45
9
46-50
10
51-55
11
56-60
12
61-65
13
66-70
14
71-75
15
76-80
16
81-85
17
86-90
18
91-100
92
Appendix B. Data Code: Cause of Death
COD #
Cause of Death
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
Anemia
Aneurysm
Appendicitis
Arteriosclerosis
Bronchitis
Bronchopneumonia
Cancer
Carbon Monoxide Poisoning
Carcinoma
Diabetes
Dystrophy
Edema
Embolism/clot
Emphysema
Encephalitis
Epilepsy
Fibrosis
Flu
Fracture
Gangrene
Gunshot
Heart Attack
Heart Failure
Hemorraghe
Hepatitis
Hypertension
Infection
Inflammation
Intestinal Failure
30
Kidney failure
COD #
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
Cause of Death
Leprosy
Lesions
Leukemia
Liver failure
Meningitis
Myocarditis
Neoplasia
Nephritis
Paralysis
Pneumonia
Polio
Prolapsed Uterus
Rheumatism
Sclerosis
Senility
Septicemia
Stroke/Thrombosis
Suicide
Syphilis
Thrombosis
Trauma
Tuberculosis
Tumor
Typhoid
Ulcer
Unknown
Anorexia
Asphyxiation
Asthma
93
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