International Journal of Paleopathology 5 (2014) 917

Contents lists available at ScienceDirect

International Journal of Paleopathology

journal homepage: www.elsevier.com/locate/ijpp

Research Article

Analysis of nutritional disease in prehistory: The search for scurvy

in antiquity and today
George J. Armelagos a, , Kendra Sirak a , Taylor Werkema a , Bethany L. Turner b
a
b

Emory University, Atlanta, GA 30322, United States

Georgia State University, Atlanta, GA 30302-3998, United States

a r t i c l e

i n f o

Article history:
Received 11 March 2013
Received in revised form 8 September 2013
Accepted 17 September 2013

a b s t r a c t
In this paper, we discuss the issues surrounding the study of scurvy, or vitamin C deciency, in paleopathology, and highlight the work of Donald Ortner in advancing this area of research. This micronutrient
deciency impacts collagen formation and results in damage to a variety of bodily tissues. While clinical
manifestations are observed routinely, the lack of specic signatures on bone makes paleopathological
diagnosis difcult. Rapid growth in infants, children, and subadults provides abundant remodeled tissue
and an increase in vascularization that makes identication possible in younger segments of the population. However, diagnosis of scurvy in adults remains problematic, given that diagnostic lesions are
strikingly similar to those associated with rickets, osteomalacia, and other conditions. We argue that
this confounding factor underscores the need for a broader anthropological approach to scurvy research
that expands beyond differential diagnosis to include more accurate reconstruction of diets and available
resources, greater consideration of the possibility even likelihood of multiple nutrient deciencies
simultaneously affecting an individual, and the patterning of these deciencies along lines of status, sex,
and age.
2013 Elsevier Inc. All rights reserved.

1. Introduction
Circumstantial evidence is a very tricky thing, answered
Holmes thoughtfully. It may seem to point very straight to one
thing, but if you shift your own point of view a little, you may nd
it pointing in an equally uncompromising manner to something
entirely different. (Doyle, 1891, p. 402)
We have three objectives in this essay: to describe the history of the search for markers of scurvy and similar diet-related
pathologies, to celebrate Donald J. Ortners1 role in unraveling the
role of nutritional deciencies in the adaptation and well-being
of human populations, and to suggest broader anthropological
perspectives useful in the study of these deciencies. Over the
course of his long and productive career, Ortner investigated

Corresponding author. Tel.: +1 14047249597.

E-mail address: antga@emory.edu (G.J. Armelagos).
1
Donald J. Ortner, in addition to be a major force in paleopathology, was the
epitome of a scientist and gentleman. While Don and I (GJA) were frequently at
opposite ends of controversial issues in paleopathology, these were always dealt
with as scientic matters and were never taken personally. No matter how heated
the debate, we always greeted each other in a genuinely friendly manner. Don also
played a signicant role in mentoring three of my former students: Michael Blakey
and Mark Mack were mentored by Don as undergraduates before they enrolled at the
University of Massachusetts, and Molly Zuckerman before she enrolled as a graduate
student at Emory. I will miss him and our scientic and social interactions.
1879-9817/$ see front matter 2013 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.ijpp.2013.09.007

tooth mutilation (Ortner, 1966), osteon remodeling (Ortner, 1975),

hypothyroidism (Ortner and Hotz, 2005), carcinomas (Ortner et al.,
1991), and nutritional diseases such as scurvy, rickets (Ortner and
Mays, 1998), and iron deciency anemia (Von Endt and Ortner,
1982). While we note limitations in the descriptive and diagnostic
tradition of paleopathology that might limit more meaningful
study of an elusive skeletal condition like scurvy, we also review
the progress that has been made in scurvy diagnosis and highlight
encouraging directions in broader anthropological research on this
condition in antiquity.
2. Contextual background
Donald Ortner was a major force in the development of
methodological and theoretical issues in paleopathology (Ortner,
1991, 2002, 2009; Ortner and Aufderheide, 1991). Ortner and
Arthur C. Aufderheide organized a symposium held at the International Congress of Anthropological and Ethnological Sciences in
Zagreb, Yugoslavia in July, 1988 that reviewed the then-current
state of paleopathology with an eye to future developments. The
proceedings of the conference, Human Paleopathology: Current
Syntheses and Future Options (Ortner and Aufderheide, 1991)
offers insights into a critical period in method and theory in
paleopathology.
Ortner (1991) framed the theoretical and methodological
perspective that denes his contribution to the discipline of

10

G.J. Armelagos et al. / International Journal of Paleopathology 5 (2014) 917

paleopathology. According to Ortner, the paleopathologist must

answer two deceptively simple questions that require complex
answers: What is it? and What does it mean? The answer to
each question is fundamental. Given the difculties of diagnosis
in contemporary biomedicine despite its advanced technology,
it is not surprising that paleopathologists would nd diagnosis
essential but also incredibly. This problem is compounded by
the fact that paleopathologists have, until recently, frequently
diagnosed pathological conditions without describing them in
detail or discussing their distribution among skeletal elements.
Naming a lesion without completing a differential diagnosis
makes it difcult for other researchers to evaluate the validity of
the original pathological determination and to standardize the
diagnostic criteria for conditions with similar manifestations.
An important aspect of paleopathology research, and one often
glossed over by more descriptive, case-oriented approaches, is the
second question: What does it mean? This question should extend
beyond mechanisms and a list of associated symptoms to include
a broader discussion of causal factors.
One research area that would benet from this more inclusive
approach is the study of scurvy. Ortner had an abiding interest in
scurvy (Ortner et al., 2001; Ortner and Ericksen, 1997; Ortner et al.,
1999) that served as a stimulus for renewed interest in the disease
among paleopathologists. Unfortunately, there are only a few new
techniques for diagnosing scurvy in skeletal remains. While the use
of collagen extraction and analysis shows promise (Koon, 2010;
Travis, 2008b), the application of standard macroscopic and microscopic techniques remain the current tools of choice (Brickley and
Ives, 2006, 2008; Murray and Kodicek, 1949; Ortner and Ericksen,
1997). Even so, a review of health and disease in Britain (Roberts
and Cox, 2003), with indisputable documentary evidence of morbidity and mortality from scurvy from the post-Medieval period
(15501850 CE), found no skeletal evidence for vitamin C deciency
(Brickley and Ives, 2006). This creates a riddle for the paleopathologist, and the search for scurvy in earlier time periods has been just as
elusive. Wells (1975, p. 756) describes the difculties in diagnosing
scurvy:
It is not an easy disease to recognize in skeletal remains because
its chief features are swollen, spongy, infected gums, and multiple subcutaneous and perifollicular hemorrhages giving rise
to extensive purpuric and ecchymotic areas, anemia, lassitude
and loss of muscle tone, and a tendency to sudden death on
slight exertion. Since these are all manifestations which affect
soft tissues rather than bones, it is understandable that its paleopathological recognition is very rare.
3. The scurvy enigma
Almost all animals, except for Homo sapiens, higher primates,
fruit bats, bulbul birds, guinea pigs, and sh metabolically synthesize the enzyme l-gulonolactone oxidase that is required to
convert glucose to vitamin C. Without the enzyme, vitamin C
must be consumed from food sources. Vitamin C, a simple watersoluble molecule, is found in many plants, with especially high
concentrations in citrus, tomatoes, potatoes, cabbages, and green
peppers (Garca-Closas et al., 2004). This vitamin is essential for
its capacity as an antioxidant and facilitator of many metabolic
pathways. Healthy humans have stores of vitamin C that allow
them to endure total dietary deprivation for 160200 days (Hodges
et al., 1971), after which symptoms of scurvy will manifest. Scholars have suggested that scurvy has caused more suffering among
humans throughout history than any other disease of nutritional
deciency, aside from generalized famine (Carpenter, 1988). In fact,
Stone (1966, p. 345) argued, In the long period of human prehistory
and history, scurvy has caused more deaths, created more human

misery and has altered the course of history more than any other
single cause.
Scurvy manifests as a generalized condition with a variety of
symptoms that progress over time and can vary between individuals (Table 1). Evidence from clinical settings is measured
primarily in behavioral features and changes in soft tissue. Behavioral features include fatigue (Hodges et al., 1971), loss of strength
(asthenia) (Fain, 2005) and changes in emotion (Hodges et al.,
1971). There are changes in soft tissue such as inammatory hypertrophy of the gingiva (Fain, 2005) that leads to swollen gums
(Hodges et al., 1971) and periodontal bleeding (Hirschmann and
Raugi, 1999). Weakness in the vascular system leads to pinpoint
bleeding of the skin (petechiae bleeding) (Hirschmann and Raugi,
1999) that causes dermal bleeding appearing as bruises or vascular purpura (Fain, 2005). Edema occurs as uid accumulates in
tissue (Hirschmann and Raugi, 1999; Hodges et al., 1971) with
signicant bleeding into the joint spaces as hemarthroses (Fain,
2005; Hirschmann and Raugi, 1999; Maat, 2004) and muscle as
hematomas (Fain, 2005), leading to joint pain (arthralgia) and muscle pain (myalgia). Changes in hair with follicular hyperkeratosis
(Hirschmann and Raugi, 1999) and congested follicles (Hodges
et al., 1971) round out the soft tissue changes (Table 1).
Deciency of vitamin C impacts the formation of collagen, the
building block of connective tissue and the majority of the protein
phase of bone. The bodys global response to vitamin C deciency
is not surprising given its importance in collagen synthesis and
the ubiquitous presence of collagen in human tissue. Collagen is
created by broblasts and comprises over 25% of the bodys total
proteins; it is also the primary component of connective tissues.
Collagen can form elongated brils that are the basic structure of
brous tissues such as tendons, ligaments, and skin. Signicant
amounts of collagen provide structure to the cornea, cartilage, bone,
blood vessels, intestines, and intervertebral discs. Collagen also
forms the endomysium of muscle tissue. Impaired collagen structure results in defective formation of bone osteoid and blood vessel
walls, resulting in weakened arteries and veins. Initially, there is a
state of fatigue with malaise and lethargy, followed by hemorrhaging of small blood vessels that leave petechial spots on the skin,
swollen joints with muscular aches and pains, and bleeding gums.
Advanced stages of the condition are characterized by suppurating pus-producing wounds, neuropathy, and death (Hodges et al.,
1971). Untreated scurvy is invariably fatal, but, death from scurvy
is rare in modern times.
While the symptoms of vitamin C deciency can be widespread
and dramatic, the treatment is remarkably straightforward. All that
is required for a full recovery is the resumption of normal vitamin
C intake; as little as 6.5 mg of vitamin C will result in a slow but
steady decline in symptoms of scurvy (Hodges et al., 1971). Given
that the most diagnostic features (see below) of scurvy are found
in soft tissue, the impact on bone is difcult to decipher. However,
skeletal signs (Table 1) include antemortem tooth loss, abnormal
dentin production, altered bone formation in subadults due to the
inability of osteoblasts to produce the osteoid seam, and possibly
elevated iron levels from increased absorption (Fain, 2005).
Though humans and human ancestors have long been susceptible to scurvy, attempts to determine the sources of scurvy
in human populations came surprisingly late. Though most commonly attributed to European maritime explorers seeking out new
lands through oceanic travel, scurvy was common in sailors long
before the Age of Discovery (Wells, 1975). It appears to have been
described initially during the fth and fourth centuries BCE by Hippocrates (Stone, 1966), who documented the physical symptoms of
pain in the lower extremities and gangrene of the gums (Hess, 1920;
Hirsch, 1885). In the three centuries between 1500 and 1800 CE, a
period characterized by an explosive increase in long duration maritime travel, scurvy is thought to have caused the death of at least

G.J. Armelagos et al. / International Journal of Paleopathology 5 (2014) 917

Table 1
Clinical and paleopathological diagnostic features of scurvy.
Diagnostic symptoms of scurvy
Clinical manifestations of scurvy
Behavioral features
Fatigue (Hodges et al., 1971)
Asthenia (loss of strength) (Fain, 2005)
Emotional changes (Hodges et al., 1971)
Soft tissue changes
Gingival hypertrophy (inammatory enlargement of gingiva) (Fain, 2005)
Swollen gums (Hodges et al., 1971)
Periodontal bleeding (Hirschmann and Raugi, 1999)
Petechiae bleeding (pinpoint bleeding of the skin) (Hirschmann and Raugi,
1999)
Vascular purpura (sub epidermal bleeding appearing as bruise) (Fain, 2005)
Edema (Hirschmann and Raugi, 1999; Hodges et al., 1971)
Haemarthroses (bleeding into joint spaces) (Fain, 2005; Hirschmann and
Raugi, 1999; Maat, 2004)
Musculoskeletal symptoms (Fain, 2005)
Arthralgia (joint pain) (Fain, 2005)
Myalgia (muscle pain) (Fain, 2005)
Muscular hematomas (accumulation of blood in muscles) (Fain, 2005)
Follicular hyperkeratosis (Hirschmann and Raugi, 1999)
Congested follicles (Hodges et al., 1971)
Skeletal changes, histological radiographic and chemical
Joint space loss (radiographic image) (Fain, 2005)
Osteolysis (radiographic image) (Fain, 2005)
Collagen with alteration in hydroxylation process (Fain, 2005; Koon, 2010;
Travis, 2008a, 2008b)
Musculoskeletal symptoms (Fain, 2005)
Defective osteoid matrix formation (Fain, 2005)
Increased bone resorption (Fain, 2005)
Trabecular and cortical osteoporosis (Fain, 2005)
Osteonecrosis (radiographic image) (Fain, 2005)
Skeletal changes, macroscopic
Hematoma formation and subperiosteal swellings in the lower extremities
Hematoma formation on the tibiae in particular (Aschoff and Koch, 1919)
Osteopenia, and/or periosteal proliferation (radiographic image) (Fain, 2005)
Porous, hypertrophic orbital lesions (Fraenkel, 1929; Ortner and Ericksen,
1997)
Cranial bosses enlargement (Parrots swellings) (Barlow, 1883; Ortner and
Ericksen, 1997)
Paleopathology, children
Porous and proliferative lesions cranial bones and scapula (Brickley and Ives,
2006)
Cranial vault, greater wing of the sphenoid (Ortner and Ericksen, 1997; Ortner
et al., 1999)
Lamellar porosity less than 1 mm in diameter (Ortner and Ericksen, 1997)
Cranial vault, orbit, frontal (roof) (Ortner et al., 1999)
Cranial vault, orbit, zygomatic (lateral) (Ortner et al., 1999)
Cranial vault, maxilla, posterior surface (Ortner and Ericksen, 1997; Ortner
et al., 1999)
Cranial vault, zygomatic bone, internal surface (Ortner et al., 1999)
Cranial vault, infraorbital foramen (Ortner et al., 1999)
Cranial vault, alveolar processes (Ortner et al., 1999)
Cranial vault, alveolar sockets (Ortner et al., 1999)
Cranial vault, palate (Ortner et al., 1999)
Mandible, coronoid process, medial surface (Ortner et al., 1999)
Mandible, alveolar processes (Ortner et al., 1999)
Mandible, alveolar sockets (Ortner et al., 1999)
Porous lesions on the ilium (Brown and Ortner, 2011)
Paleopathology, adults
Bilateral inammatory lesion of the greater wing of sphenoid (Ortner and
Ericksen, 1997)
When bilateral on the sphenoid, other sites on skull effected (Ortner and
Ericksen, 1997)
New bone formation at the foramen rotundum in sphenoid bone (Geber and
Murphy, 2012)
Porous and proliferative bone lesions affecting the cranial bones and scapulae
(Brickley and Ives, 2006)
Abnormal porosity occurring throughout the skeleton

11

two million sailors (Drymon, 2008, p. 114). In 1499, Vasco de Gama

lost 116 men of his crew of 170, and in 1520, Ferdinand Magellans crew was almost completely annihilated, with scurvy killing
208 out of 230 sailors (Lamb, 2000). The diet of sailors was the
source of the problem. While de Gama noticed that his men were
healthier at certain port cities, he attributed this variation in health
to good air in these regions, consistent with the foul air theory
of disease held by many at this time (Cuppage, 1994; Ravenstein,
1898). No further thought was given to a dietary deciency as the
cause of illness, though there are multiple anecdotes describing a
desolate crew that became well after the consumption of fruits and
vegetables at port. Ships were cold, damp, and unwholesome,
and sailor diets consumed diets of putrid beef, rancid pork, moldy
biscuits and foul water (Dunn, 1997, p. F64). The situation for many
sailors became dire on long sea voyages after the onboard supply of
perishable fruits and vegetables were depleted, at which point the
symptoms of scurvy appeared. Scurvy was a scourge for crew and
passengers on long voyages from the fteenth century until World
War I (Carpenter, 1988).
Vitamin C deciency treatment is simple with almost immediate amelioration with the consumption of fresh food, especially
citrus; this successful treatment for scurvy was discovered by James
Lind (Baron, 2009; Dunn, 1997), a surgeon in the Royal Navy and
the rst to carry out a systematic analysis of the disease (Lind,
1753). Lind was assigned as a surgeon to the HMS Salisbury and
was concerned with the living conditions of sailors. He believed
that scurvy was caused by purication and could be treated by consuming acidic foods. In A Treatise of the Scurvy, he described what
can now be called a clinical trial in which 12 sailors were placed
into six experimental groups and given different remedies that
were thought to improve health. Lind demonstrated that citrus prevented scurvy, though he thought it was only one of many remedies
(Baron, 2009). Though accredited with the discovery, Lind argued
that the anti-scorbutic effects of citrus fruits had been known for
at least 200 years before his time. While there have been revisions
of the Lind story (Baron, 2009), it was his research that eventually
convinced the Royal Navy to implement citrus juice in the daily
rations of sailors. However, citrus is only one of the many remedies applied since antiquity. Herbals, trephination (Mogle and Zias,
1995), bloodletting, laxatives, root extracts, baths with brooklime,
mallow and hog weed have been prescribed (De Luca and Norum,
2011), but the causal mechanism of scurvy was not known until
1932 (King, 1953). Consequently, treatment was inconsistent, with
many ineffective approaches used well into the 20th century.
4. Paleopathological approaches to studying scurvy
A combination of lesions (Brickley and Ives, 2008; Brown and
Ortner, 2011; Ortner et al., 1999), assessed using a weighted system of diagnostic criteria based on clinical and paleopathological
features (Brickley and Ives, 2006), provide the basis for a scurvy
diagnosis in skeletal remains. Fragmentary remains that are common features of the archeological record make diagnosis difcult,
which may contribute to an under-representation of the disease in
prehistory (Geber and Murphy, 2012).
According to Ortner et al. (1999), indisputable evidence of
subadult scurvy is not well documented in archeological remains.
There may be a number of reasons for this. For example, children
with scurvy may die of other causes, or may not manifest observable
skeletal changes in all cases. While pathological conditions associated with scurvy have been identied for nearly a century, these
features may be rare or difcult to differentiate from other pathological conditions and may thus be attributed to other ailments
such as anemia (Ortner et al., 1999).
A number of skeletal changes are relevant to the diagnosis
of scurvy from biopsy or autopsy samples that are subject to

12

G.J. Armelagos et al. / International Journal of Paleopathology 5 (2014) 917

histological, radiographic and chemical analyses. Radiographic

imaging reveals joint space loss, osteolysis, defective osteoid matrix
formation, bone resorption, trabecular and cortical osteoporosis,
and osteonecrosis (Fain, 2005). Chemical analysis of collagen shows
alteration to the hydroxylation process, appearing as a deciency
in proline hydroxylation (Fain, 2005; Koon, 2010; Travis, 2008a).
Building on these ndings, recent research in archeological humans
and modern guinea pigs (Koon, 2012) has successfully differentiated between individuals with unaffected versus scorbutic bone,
nding less proline hydroxylation in certain collagen peptides in
the latter via mass spectrometry analysis. Macroscopic observation
of skeletal changes in clinical cases is more relevant to diagnosis
in skeletal populations. Hematoma formation and subperiosteal
swellings in the lower extremities with bilateral involvement are
often observed on the tibiae (Aschoff and Koch, 1919). The orbits
of some scorbutics (vitamin C decient individuals) may show
porous, hypertrophic orbital lesions (Fraenkel, 1929; Ortner and
Ericksen, 1997) that are similar to cribra orbitalia (a skeletal sign
of anemia). While the porous lesion may indeed be diagnostic of
scurvy, it can difcult to distinguish it from anemia, which often
complicates a differential diagnosis based on porous lesions alone.
Ortner et al. (1999) described the distinct distribution of skeletal
porosity in scurvy and anemia, arguing that a differential diagnosis
of anemia in skeletal remains is possible based on evidence of
marrow hyperplasia. Distinguishing this is easier said than done,
since in the early stages of anemia, symptomatic lesions can be
difcult to differentiate from scurvy; however, recent microscopic
analyses (Brickley and Ives, 2006; Wapler et al., 2004) suggest that
distinguishing between pathogenic bone processes in anemia and
scurvy is possible: anemia creates porous lesions of the cranial
and orbital bones caused by a widening of the diple associated
with marrow hypertrophy and cortical bone thinning, whereas
scanning electron microscopy suggests that scorbutic hemorrhaging stimulates periosteal deposition on the orbits that may be
penetrated to varying degrees by proliferating vasculature, both in
response to hemorrhage.
Ortner et al. (2001) suggested that comorbidity between scurvy
and anemia is possible; Walker et al. (2009) echoed this notion and
argued that porous lesions may also result from hemoblastic anemia stemming from B-vitamin deciency. Given that individuals at
risk for scurvy in antiquity were likely at risk for other micronutrient deciencies as well, it is entirely reasonable to expect a
certain degree of comorbidity. Indeed, anemia is often a secondary
response to scurvy in modern clinical settings (Burk and Molodow,
2007; Larralde et al., 2007; Tamura et al., 2000) due to bleeding that
results from scurvy and reduction in the ability to absorb nonheme
iron that results in anemia (Fain, 2005). Ortner (2003) said that
archeological samples offer few example of comorbidity, though
he described one such case. While scurvy and cribra orbitalia have
macroscopically similar features in the orbit, only scurvy promotes
changes in the sphenoid bone, the mandible, and the hard palate.
The enlargement of the cranial bosses, known as Parrots swellings
(Barlow, 1883; Ortner and Ericksen, 1997), and osteopenia, and/or
periosteal proliferation (Fain, 2005) are also found in scurvy but are
not necessarily diagnostic by themselves (see Fig. 1). However, anemia and scurvy may in fact form an interacting relationship in that
vitamin C deciency inhibits the absorption of non-heme iron (Fain,
2005, p. 125). Plants (which contain varying amounts of vitamin C)
contain only non-heme iron and in animal esh about 60% the iron
content is none-heme in nature. Given the difculty in absorbing
non-heme iron, scurvy could result in lesions characteristic of both
vitamin C deciency and iron deciency anemia that reect in vivo
co-morbidity (Fig. 2).
The bones of infants and children in prehistory provide perhaps
the best evidence for diagnosing scurvy. The rapid growth of infants
and small children increases rates of bone remodeling as well as

Fig. 1. Sir Thomas Barlow attributed the lesion (Museum of the Royal College of Surgeons of England, Wellcome Museum, Catalog no. S56.4.) Ortner and Ericksen (1997)
note the vaults enlargement of the frontal and parietal bosses with the interior view
exhibits less porosity in the areas underlying the bosses.

the production of soft tissues such as muscles and blood vessels,

which also require collagen. The key feature that denes scurvy
is porosity on the greater wing of the sphenoid bone (Ortner and
Ericksen, 1997; Ortner et al., 1999). The lamellar porosity on the
sphenoid bone is characterized by lesions less than 1 mm in diameter (Ortner and Ericksen, 1997). Frequently, porosity on the roof of
the orbits has also been found (Ortner et al., 1999) (Fig. 3). Infants
and children also display porosity on the lateral, internal and inferior surfaces of the zygomatic bone (Ortner et al., 1999) and the
posterior area of the maxillary surface (Ortner and Ericksen, 1997;
Ortner et al., 1999) (Fig. 4); porosity has also been found around
the area of the infraorbital foramen (Ortner et al., 1999). Given the
clinical evidence of gingival involvement with scurvy, it is not unexpected to nd evidence of changes in the alveolar bone. Alveolar
processes, alveolar sockets, the hard palate, and the coronoid process are marked with abnormal porosity (Ortner et al., 1999) (Fig. 5).
In some cases, there are also lesions on the scapula (Brickley and

Fig. 2. This 12-year-old child (Pachacama, Peru) shows porous lesions in the region
of the right greater wing of the sphenoid. Specimen date between 1000 and 1530 CE.
From the biomedical collections of the National Museum of Natural History, Smithsonian Institution, Catalog no. 266599 (Ortner and Ericksen, 1997).

G.J. Armelagos et al. / International Journal of Paleopathology 5 (2014) 917

13

Fig. 3. According to Ortner, the left orbital surface displays dense, porous, abnormal
bone growth with vessel impressions on the medial third of the supraorbital margin.
The bony overgrowth is 1.5 mm at thickest point. This gure is available in color
online at http://wileyonlinelibrary.com/journal/oa (Brown and Ortner, 2011).

Fig. 5. Porosity involving the medial surface of the mandibular coronoid process
extending posterior to the mandibular foramen and to the edge of the ramus. This gure is available in color online at http://wileyonlinelibrary.com/journal/oa (Brown
and Ortner, 2011).

Ives, 2006) (Fig. 6) and porous lesions on the ilium (Fig. 7) (Brown
and Ortner, 2011) (Table 1).
Ortner et al. (2001) examined subadult human skeletons from
Native American archeological sites in the United States (midAtlantic, Florida, American Southwest and Plains) for skeletal
evidence of scurvy. The prevalence of probable scurvy in sub
adults ranged from 38% (Florida) to none (Plains). Unfortunately,
they were only able to speculate about differences in prevalence.
They suggested seasonal and regional variation in type and quantity of food, differences in storage and use, periodic shortages, and
the quantity of corn in the diet (Ortner et al., 2001).
Van der Merwe et al. (2010) describe clinical evidence of scurvy
in preparation for an analysis of the deciency in 19th-century

miners from Kimberly, South Africa. Differential diagnosis was

made through observation of gingival hypertrophy and petechial
bleeding, (pinpoint bleeding of the skin), follicular hyperkeratosis, hematoma formation and subperiosteal swelling in the lower
limbs (Fain, 2005). Maat and coworkers (Maat, 1981, 2004; Maat
and Uytterschaut, 1984), examining remains of Dutch whalers
who were recorded as being aficted with scurvy (Stoney, 1900),
found lesions suggestive of vitamin C deciency in 39 of 50 individuals. Differential diagnosis included subperiosteal hematomas,
hemarthroses and periodontal bleeding (Maat, 2004). Bilateral tibial and bular subperiosteal hematomas were also recorded. When
hematomas were identied on the upper extremities, they were
usually unilateral, which could also suggest the presence of scurvy
and subsequent opportunistic infection. The quality of these ndings reects extremely well-preserved remains. The diagnosis was
made primarily on the basis of soft tissue that displayed hemorrhaging. Interestingly, only a single individual had bony lesions
associated with healed vitamin C deciency. According to Van der
Merwe, this suggests that whalers who died of scurvy did not manifest skeletal lesions, which only developed with the restoration of
normal vitamin C levels (Murray and Kodicek, 1949).
Although skeletal lesions associated with infantile scurvy have
been well described by many authors such as Stuart-Macadam
(1989), Ortner and Ericksen (1997) and Brickley and Ives (2006),
very little literature is available on adult scurvy and the resulting
skeletal lesions (Van der Merwe, 2007). The evidence of paleopathology of scurvy in adults is more difcult to diagnose (but see
Crist and Sorg, this issue). Abnormal porosity occurring throughout the skeleton is common in scurvy. Unfortunately, the skeletal
response is so general that supporting evidence to assure that
scurvy was the actual source of the porosity is required.
More indicative of scurvy is the bilateral inammatory lesion
of the greater wing of sphenoid bone indicated by porotic hypertrophic bone (Ortner and Ericksen, 1997). When there is bilateral
porosity on the sphenoid bone, other sites on skull are usually
affected (Ortner and Ericksen, 1997). More promising is evidence
of new bone formation at the foramen rotundum of the sphenoid bone (Geber and Murphy, 2012). When there are proliferative
porotic bone lesions affecting the cranium, the scapula may also be
involved (Brickley and Ives, 2006).

Fig. 4. Ortner reports abnormal porosity involving the infraorbital foramen of the
maxilla extending medially to the lateral border of the nasal aperture (a). On the
palatal surface of the maxilla exhibiting dense porosity (b). This gure is available in
color online at http://wileyonlinelibrary.com/journal/oa (Brown and Ortner, 2011).

5. Theoretical issues in the paleopathology of scurvy

The complexity of describing and interpreting lesions indicative of scurvy is due, in part, to issues of comorbidity and the fact

14

G.J. Armelagos et al. / International Journal of Paleopathology 5 (2014) 917

Fig. 6. Composite image of abnormal porosity on supraspinous process of scapula. On the left is the macroscopic appearance of porosity. In the middle is a SEM image of
porosity while on the right is an age-matched SEM image of normal scapula (Brickley and Ives, 2006). AJPA. Detail of posterior left parietal showing a porous lesion with
hypertrophic bone formation (Schreiner Collection, Catalog no. 4733 from Ortner and Ericksen, 1997). (Left) Young infants maxilla showing porosity extends well beyond
alveolar processes and toward frontal process. (Right) Lateral view of maxilla showing normal, small, localized porosity restricted to alveolar pits and infraorbital foramen
Brickley and Ives (2006). AJPA.

that lesions may remain conned to soft tissues without skeletal

presentation. However, this complexity has also been due to a
historical trend in paleopathology whereby pathological conditions were described and diagnosed without fully standardizing
descriptive criteria. Ortner highlighted the considerable variability
that exists in the quality of observations, diagnosis and interpretation, and was at the forefront of developing protocols for
pathological diagnosis (Ortner and Putschar, 1981; Buikstra, 1977;
Steinbock, 1976). In Human Paleopathology, Ortner, a biological anthropologist, and Aufderheide, a physician, combined the
study of paleopathology with clinical perspectives from modern medicine rather than with a biocultural perspectives from
anthropological science (Ortner and Aufderheide, 1991). This was
a profound distinction that has signicantly impacted the eld of
paleopathology and has sparked a productive theoretical debate
(Armelagos, 1994). The issue of developing methodologies for
assigning a clinical diagnosis to archeological skeletal conditions
was considered by Ortner (1992, p. 6) to be so critical that he advocated suspending hypothesis testing until standardized protocols

are produced. While it is critically important for each study to

clearly state the methodology and descriptive criteria employed,
the push to make paleopathology essentially atheoretical unless
or until uniform diagnostic criteria are established has seriously
restricted its interpretive scope in understanding ancient patterns
of disease in human populations and of humanpathogen coevolution (Zuckerman et al., 2012).
A second important factor in limiting the growth and scope of
paleopathology was a reliance on the newest technology to drive
the research with the result that any substantive research questions became secondary to the technology applied (reviewed in
Armelagos et al., 1982). The application of new technology without
an overarching theoretical framework is only an illusion of progress
if that innovative technology is not applied to solve a problem
beyond diagnosis. There are now many studies that demonstrate
the application of pioneering technology to solve interesting questions. For example, ancient DNA extraction (Cooper and Poinar,
2000; Pbo, 1989) has been used to solve population relationships (Pbo et al., 2004) and the detection (Donoghue et al., 2008,

G.J. Armelagos et al. / International Journal of Paleopathology 5 (2014) 917

15

one devises alternative hypotheses; second, one designs experiments that exclude or falsify one or more of the hypotheses; third,
one carries out experiments to get clean results and nally, one
recycles the procedure by repeating the process.
While strong inference is most effectively applied to sciences with experimental possibilities, it can be useful in
non-experimental, or reconstructive sciences such as paleopathology. There is obviously a need to modify the methods of
paleopathological analysis. Ultimately, the paleopathologist must
rely on comparative analysis for natural experiments. It is possible to select samples that highlight differences in biotic or cultural
environment. Strong inference can be applied to archeological evidence of scurvy by seeing how diagnostic features are used in
formulating falsiable hypotheses, thus engaging in differential
diagnosis. Given the difculty with differential diagnosis, however,
this remains a formidable task.
6. Toward an anthropological study of ancient scurvy

Fig. 7. The external surface of the left ilium showing dense porosity without evidence of abnormal bone growth (a). The internal surface of the left ilium shows
dense porosity and bone hypertrophy (b). This gure is available in color online at
http://wileyonlinelibrary.com/journal/oa (Brown and Ortner, 2011).

2004) and spread of a diseases (Fletcher et al., 2003), while analyses

of pathogen DNA have made signicant strides in understanding the origin and evolution of major diseases (Armelagos et al.,
2005; Harper et al., 2008a, 2008b). Similarly, stable isotopes have
been used as part of osteological analyses to reconstruct diet and
estimate nutritional status in archeological populations related
to changes in fertility (White and Armelagos, 1997; White and
Schwarcz, 2005), variation in life histories (Turner and Armelagos,
2012), and the physiological effects of acute disease stress (Fuller
et al., 2005).
The analysis of pathology in prehistoric populations often follows a deductive methodology in which the researcher attempts
to reconstruct the factors that cause the skeletal lesions. In this
view, the paleopathologist is much like the detective who has to
reconstruct the crime from the evidence long after the criminals
have left the scene. Instead of a crime scene, the paleopathologist
attempts to reconstruct the broader lifeways of a population after
they lived and died. While the deductive approach has been useful,
it has certain inherent limitations, one of which is that it is usually
not possible to select from alternative conclusions (i.e., differential
diagnosis in the case of scurvy and other pathologies).
There is, however, a methodology that can systematically falsify
or exclude alternative hypotheses. Platt (1964) proposed the use of
an inductive approach to test hypotheses, which he called strong
inference. Although inductive inference has been known for many
years, it has only recently penetrated the methodology of paleopathology. Strong inference can be very effective when applied
to paleopathology in that it acts as the means for transforming a
scientic diagnostic endeavor into a more strongly theoretical one,
without sacricing methodological rigor. There are four stages in an
analysis using the approach of strong inference (Platt, 1964). First,

The preceding pages center primarily on Ortners rst question

as it pertains to scurvy; in order to study what it is, one must rst
nd and describe it. In turning our attention to the second question, of what scurvy means, we argue that it is as important to push
ourselves in thinking about the implications of scurvy in ancient
populations, as it is to move forward in developing new diagnostic techniques. If the skeletal signs of scurvy are ambiguous or
absent, a broader anthropological study of ecological and cultural
contexts in which affected individuals lived may provide critical
insights into assessing the likelihood of incidence and possible signicance of scurvy in antiquity. For instance, given that wild plants
in a number of global regions have much higher concentrations of
vitamin C and other antioxidants than do cultivated domesticates
(Guil et al., 1997; Halvorsen et al., 2002; Simopoulos, 2004), paleobotanical analyses of surrounding soils at archeological sites would
contribute a great deal to understanding what wild food resources
were available to different populations (e.g., Klaus, this issue). In
concert with isotopic and trace elemental methods of paleodiet
reconstruction to estimate what resources were actually consumed
(Price, 2012), paleopathologists could approach assessing scurvy
incidence with a much stronger set of contextual data.
In modern contexts, scurvy is seen in poorly nourished and
economically disadvantaged groups including alcoholics, the isolated elderly, and those who have been institutionalized (Pimentel,
2003). Bioarchaeology has a long tradition of studying aspects of
social inequality, marginalization, cultural transitions, and behavior, making it well-suited to round out studies of scurvy. Since
scurvy by itself may not leave visible or unambiguous traces
in bone, one strategy of investigating its presence in ancient
remains would be to identify those individuals who exhibit signs
of general malnutrition, other micronutrient deciencies (particularly anemias), or mortuary contexts suggesting relative poverty,
marginalization, or violence (e.g. Crandall, this issue). Subjecting
these individuals to more in-depth analyses such as those developed for collagen analysis by Koon (2012) would provide feasible
ways to more accurately identify scurvy in individuals who exhibit
no visible skeletal signs.
7. Conclusion
Solutions to the scurvy enigma may soon be within reach,
given the advancements in specic diagnostic tools for studying
subtle changes in collagen structure, identifying microscopic variation in bony reactions to different deciencies. In the future, it
may be possible to differentiate between collagen amino acid proles in affected versus unaffected individuals and better identify
divergence in the cellular and molecular processes associated with

16

G.J. Armelagos et al. / International Journal of Paleopathology 5 (2014) 917

different conditions. However, it is argued here that a more holistic

approach to paleopathology that draws on theories and methods
in archeology and social bioarchaeology is needed alongside technologically driven strides. Attending to co-morbidity and to the
social and ecological factors that can either buffer individuals or
exacerbate their suffering and open the door to various infectious
and noninfectious diseases may prove as useful to identifying what
scurvy is and its various signs as it is central to better understanding what it means in reconstructing the lives of ancient groups.
Given the exciting research happening in paleopathology, and the
potential for incorporating broader anthropological perspectives,
Don Ortner would be pleased to see the progress that has been
made since his pioneering research on scurvy.
Acknowledgements
We would like to thank Haagen Klaus, John Crandall, and an
anonymous reviewer for their helpful and insightful comments on
earlier versions of this manuscript. We would also like to thank
Don Ortner and his students for their immeasurable contributions
to paleopathology and biological anthropology.
References
Armelagos, G.J., 1994. In: Ortner, D.J., Aufderheide, A.C. (Eds.), Review of Human
Paleopathology: Current Synthesis and Future Options. Smithsonian Press,
Washington, DC, Journal of Field Archeaology 21, 239243.
Armelagos, G.J., Harper, K.N., Ocampo, P.S., 2005. On the trail of the twisted treponeme: searching for the origins of syphilis. Evolutionary Anthropology: Issues,
News, and Reviews 14 (6), 240242.
Armelagos, G.J., Carlson, D.S., Van Gerven, D.P., 1982. The theoretical foundations
and development of skeletal biology. In: Spencer, F. (Ed.), A History of American
Physical Anthropology, 19301980. Academic Press, New York, pp. 305328.
Aschoff, L., Koch, W., 1919. Skorbut Eine Pathologish-Anatomische Studie. Gustav
Fischer, Jena.
Barlow, T., 1883. On cases described as Acute Rickets which are probably a combination of scurvy and rickets, the scurvy being an essential, and the rickets a
variable, element. Medico-Chirurgical Transactions 66, 159220.
Baron, J.H., 2009. Sailors scurvy before and after James Linda reassessment. Nutrition Reviews 67 (6), 315332.
Brickley, M., Ives, R., 2006. Skeletal manifestations of infantile scurvy. American
Journal of Physical Anthropology 129 (2), 163172.
Brickley, M., Ives, R., 2008. The Bioarchaeology of Metabolic Bone Disease. Academic
Press, Oxford, UK.
Brown, M., Ortner, D.J., 2011. Childhood scurvy in a medieval burial from Macvanska
Mitrovica, Serbia. International Journal of Osteoarchaeology 21 (2), 197207.
Buikstra, J., 1977. Differential diagnosis: an epidemiological model. Yearbook of
Physical Anthropology 20, 316328.
Burk, C.J., Molodow, R., 2007. Infantile scurvy: an old diagnosis revisited with a
modern twist. American Journal of Clinical Dermatology 8 (2), 103106.
Carpenter, K.J., 1988. The History of Scurvy and Vitamin C. Cambridge University
Press, Cambridge.
Cooper, A., Poinar, H.N., 2000. Ancient DNA: do it right or not at all. Science 289
(5482), 1139.
Cuppage, F.E., 1994. James Cook and the Conquest of Scurvy. Greenwood Press,
Westport, CT.
De Luca, L.M., Norum, K.R., 2011. Scurvy and cloudberries: a chapter in the history
of nutritional sciences. Journal of Nutrition 141 (12), 21012105.
Donoghue, H., Spigelman, M., Zias, J., Gernaey-Child, A., Minnikin, D., 2008. Mycobacterium tuberculosis complex DNA in calcied pleura from remains 1400 years
old. Letters in Applied Microbiology 27 (5), 265269.
Donoghue, H.D., Spigelman, M., Greenblatt, C.L., Lev-Maor, G., Kahila Bar-Gal, G.,
Matheson, C., Vernon, K., Nerlich, G., Zink, A., Zink, R., 2004. A tuberculosis:
from prehistory to Robert Koch, as revealed by ancient DNA. Lancet Infectious
Diseases 4 (9), 584592.
Doyle, A.C., 1891. The Boscombe valley mystery. The Strand Magazine 2 (11),
4014116.
Drymon, M.M., 2008. Disguised as the Devil: How Lyme Disease Created Witches
and Changed History. Wythe Avenue Press, Brooklyn.
Dunn, P.M., 1997. James Lind (171694) of Edinburgh and the treatment of scurvy.
Archives of Disease in ChildhoodFetal and Neonatal Edition 76 (1), F64F65.
Fain, O., 2005. Musculoskeletal manifestations of scurvy. Joint Bone Spine 72 (2),
124128.
Fletcher, H.A., Donoghue, H.D., Holton, J., Pap, I., Spigelman, M., 2003. Widespread
occurrence of Mycobacterium tuberculosis DNA from 18th19th century Hungarians. American Journal of Physical Anthropology 120 (2), 144152.
Fraenkel, E., 1929. Infantiler Skorbut (Mo ller-Barlowsche Krankheit). Handbuch
der Speziellen Pathologischen Anatomie und Histologie 9 (1), 222239.

Fuller, B.T., Fuller, J.L., Sage, N.E., Harris, D.A., OConnell, T.C., Hedges, R.E.M., 2005.
Nitrogen balance and 15N: why youre not what you eat during nutritional
stress. Rapid Communications in Mass Spectrometry 19 (18), 24972506.
Garca-Closas, R., Berenguer, A., Tormo, M.J., Snchez, M.J., Quiros, J.R., Navarro, C.,
Arnaud, R., Dorronsoro, M., Chirlaque, M.D., Barricarte, A., 2004. Dietary sources
of vitamin C, vitamin E and specic carotenoids in Spain. British Journal of
Nutrition 91 (06), 10051011.
Geber, J., Murphy, E., 2012. Scurvy in the great Irish famine: evidence of vitamin
C deciency from a mid-19th century skeletal population. American Journal of
Physical Anthropology 148 (4), 512524.
Guil, J.L., Rodrguez-Garc, I., Torija, E., 1997. Nutritional and toxic factors in selected
wild edible plants. Plant Foods for Human Nutrition 51 (2), 99107.
Halvorsen, B.L., Holte, K., Myhrstad, M.C.W., Barikmo, I., Hvattum, E., Remberg, S.F.,
Wold, A.-B., Haffner, K., Baugerd, H., Frost Andersen, L., et al., 2002. A systemic screening of total antioxidants in dietary plants. Journal of Nutrition 132,
461471.
Harper, K.N., Liu, H., Ocampo, P.S., Steiner, B.M., Martin, A., Levert, K., Wang, D.,
Sutton, M., Armelagos, G.J., 2008a. The sequence of the acidic repeat protein (arp) gene differentiates venereal from nonvenereal Treponema pallidum
subspecies, and the gene has evolved under strong positive selection in the subspecies that causes syphilis. FEMS Immunology and Medical Microbiology 53 (3),
322332.
Harper, K.N., Ocampo, P.S., Steiner, B.M., George, R.W., Silverman, M.S., Bolotin, S.,
Pillay, A., Saunders, N.J., Armelagos, G.J., 2008b. On the origin of the treponematoses: a phylogenetic approach. PLoS Neglected Tropical Diseases 2 (1), e148.
Hess, A.F., 1920. Scurvy Past and Present. J.B. Lippincott Company, Philadelphia.
Hirsch, A., 1885. Handbook of Geographical and Historical Pathology, Volume II. The
New Sydenham Society, London.
Hirschmann, J.V., Raugi, G.J., 1999. Adult scurvy. Journal of the American Academy
of Dermatology 41 (6), 895906.
Hodges, R.E., Hood, J., Canham, J.E., Sauberlich, H.E., Baker, E.M., 1971. Clinical
manifestations of ascorbic acid deciency in man. American Journal of Clinical
Nutrition 24 (4), 432443.
King, C.G., 1953. The discovery and chemistry of vitamin C. Proceedings of the Nutrition Society 12 (03), 219227.
Koon, H.E., 2012. A biochemical marker for scurvy in archaeological bones. American
Journal of Physical Anthropology 147, 184185.
Koon, H., 2010. Scurvy bones: a collagen biomarker to detect vitamin C deciency
in archaeological bone. In: Fourth International Symposium on Biomolecular
Archaeology Conference Programme and Abstracts, p. 79.
Lamb, J., 2000. The rime of the Ancient Mariner, a ballad of the scurvy. Clio Medica/The Wellcome Series in the History of Medicine 56 (1), 157177.
Larralde, M., Munoz, A.S., Boggio, P., Di Gruccio, V., Weiss, I., Schygiel, A., 2007. Scurvy
in a 10-month-old boy. International Journal of Dermatology 46, 184198.
Lind, J., 1753. A Treatise on the Scurvy: In Three Parts Containing an Inquiry into the
Nature, Causes, and Cure, of that Disease. Together with a Critical and Chronological View of What has been Published on the Subject. Crowder, London.
Maat, G.J.R., 1981. Human remains at the Dutch whaling stations on Spitsbergen.
A physical anthropological study. In: van Holk, A.G.F., sJacob, H.K., Temmingh,
A.A.H.J. (Eds.), Early European Exploitation of the Northern Atlantic 8001700.
Arctic Centre, Groningen, Netherlands, pp. 153201.
Maat, G., 2004. Scurvy in adults and youngsters: the Dutch experience. A review
of the history and pathology of a disregarded disease. International Journal of
Osteoarchaeology 14 (2), 7781.
Maat, G., Uytterschaut, H., 1984. Microscopic observations on scurvy in Dutch
whalers buried at Spitsbergen. Sienna University Press, Sienna, pp. 211218.
Mogle, P., Zias, J., 1995. Trephination as a possible treatment for scurvy in a Middle
Bronze Age (ca 2200 BC) skeleton. International Journal of Osteoarchaeology 5
(1), 7781.
Murray, P., Kodicek, E., 1949. Bones, muscles and vitamin C: 2. Partial deciencies of
vitamin C and mid-diaphyseal thickenings of the tibia and bula in guinea-pigs.
Journal of Anatomy 83 (Pt 3), 205223.
Ortner, D., 1991. Theoretical and methodological issues in paleopathology. In: Ortner, D., Aufderheide, A. (Eds.), Human Paleopathology: Current Syntheses and
Future Options. Smithsonian University Press, Washington, DC, pp. 511.
Ortner, D.J., 1966. A recent occurrence of an African type tooth mutilation in Florida.
American Journal of Physical Anthropology 25 (2), 177180.
Ortner, D.J., 1975. Aging effects on osteon remodeling. Calcied Tissue International
18 (1), 2736.
Ortner, D.J., 2002. Palaeopathology in the twenty-rst century. In: Bones and the
Man: Studies in Honour of Don Brothwell. Oxbow, Oxford, pp. 513.
Ortner, D.J., 2003. Identication of pathological conditions in human skeletal
remains. Academic Press, San Diego.
Ortner, D.J., 2009. Issues in paleopathology and possible strategies for dealing with
them. Anthropologischer Anzeiger 67 (4), 323340.
Ortner, D.J., 1992. Skeletal Pathology: Probabilities, Possibilities and Impossibilities.
In: Verano, J.W., Ubelaker, D.H. (Eds.), Disease and Demography in the Americas.
Smithsonian Institution Press, Washington, DC, pp. 514.
Ortner, D.J., Aufderheide, A.C., 1991. Human Paleopathology: Current Syntheses and
Future Options. Smithsonian Institution Press, Washington, DC.
Ortner, D.J., Butler, W., Cafarella, J., Milligan, L., 2001. Evidence of probable scurvy
in subadults from archeological sites in North America. American Journal of
Physical Anthropology 114 (4), 343351.
Ortner, D.J., Ericksen, M.F., 1997. Bone changes in the human skull probably resulting
from scurvy in infancy and childhood. International Journal of Osteoarchaeology
7 (3), 212220.

G.J. Armelagos et al. / International Journal of Paleopathology 5 (2014) 917

Ortner, D.J., Hotz, G., 2005. Skeletal manifestations of hypothyroidism from
Switzerland. American Journal of Physical Anthropology 127 (1), 16.
Ortner, D.J., Kimmerle, E.H., Diez, M., 1999. Probable evidence of scurvy in subadults
from archeological sites in Peru. American Journal of Physical Anthropology 108
(3), 321331.
Ortner, D.J., Manchester, K., Lee, F., 1991. Metastatic carcinoma in a leper skeleton from a Medieval cemetery in Chichester England. International Journal of
Osteoarchaeology 1 (2), 9198.
Ortner, D.J., Mays, S., 1998. Dry-bone manifestations of rickets in infancy
and early childhood. International Journal of Osteoarchaeology 8 (1),
4555.
Ortner, D.J., Putschar, W.G.J., 1981. Identication of Pathological Conditions
in Human Skeletal Remains. Smithsonian Institution Press, Washington,
DC.
Pbo, S., 1989. Ancient DNA: extraction, characterization, molecular cloning, and
enzymatic amplication. Proceedings of the National Academy of Sciences 86
(6), 19391943.
Pbo, S., Poinar, H., Serre, D., Jaenicke-Desprs, V., Hebler, J., Rohland, N., Kuch, M.,
Krause, J., Vigilant, L., Hofreiter, M., 2004. Genetic analyses from ancient DNA.
Annual Review of Genetics 38, 645679.
Pimentel, L., 2003. Scurvy: historical review and current diagnostic approach. American Journal of Emergency Medicine 21 (4), 328332.
Platt, J.R., 1964. Strong inference. Science 146 (3642), 347353.
Price, T.D., 2012. The Chemistry of Prehistoric Bone. Cambridge University Press,
Cambridge.
Ravenstein, E.G., 1898. A Journal of the First Voyage of Vasco da Gama 1497-1499.
Burt Franklin, New York, USA (translated and edited with notes).
Roberts, C.A., Cox, M., 2003. Health and Disease in Britain: From Prehistory to the
Present Day. Sutton Publishing, Thrupp, UK.
Simopoulos, A.P., 2004. Omega-3 fatty acids and antioxidants in edible wild plants.
Biology Research 37, 263277.
Steinbock, R.T., 1976. Paleopathological Diagnosis and Interpretation: Bone Diseases
in Ancient Human Populations. C.C Thomas, St. Louis.
Stone, I., 1966. On the genetic etiology of scurvy. Acta Geneticae Medicae et Gemellologiae 15 (4), 345350.
Stoney, W., 1900. Report of the Medical Ofcer of Health, Kimberley, for the years
1898. Unpublished report.

17

Stuart-Macadam, P., 1989. Nutritional deciency diseases: A survey of scurvy,

rickets, and iron-deciency anemia. In: Iscan, M.Y., Kennedy, K.A.R. (Eds.),
Reconstruction of Life from the Skeleton. Alan R. Liss, New York, pp. 201222.
Tamura, Y., Welch, D.C., Zic, J.A., Cooper, W.O., Stein, S.M., Hummell, D.S., 2000.
Scurvy presenting as a painful gait with bruising in a young boy. Archives of
Pediatrics and Adolescence Medicine 154, 732735.
Travis, J., 2008a. Old bones reveal new signs of scurvy. Science 322 (5900), 368369.
Travis, J., 2008b. Third International Symposium on Biomolecular Archaeology. Old
bones reveal new signs of scurvy. Science (New York, NY) 322 (5900), 368.
Turner, B.L., Armelagos, G.J., 2012. Diet, residential origin, and pathology at machu
picchu. American Journal of Physical Anthropology 149 (1), 7183.
Van der Merwe, A., Steyn, M., Maat, G., 2010. Adult scurvy in skeletal remains of late
19th century mineworkers in Kimberley, South Africa. International Journal of
Osteoarchaeology 20 (3), 307316.
Van der Merwe, A.E. (2007)Human Skeletal Remains from Kimberley: An Assessment of Health in a 19th Century Mining Community. Unpublished M.Sc. Thesis,
University of Pretoria.
Von Endt, D.W., Ortner, D.J., 1982. Amino acid analysis of bone from a possible case
of prehistoric iron deciency anemia from the American Southwest. American
Journal of Physical Anthropology 59 (4), 377385.
Walker, P.L., Bathurst, R.R., Richman, R., Gjerdrum, T., Andrushko, V.A., 2009. The
causes of porotic hyperostosis and cribra orbitalia: a reappraisal of the irondeciency-anemia hypothesis. American Journal of Physical Anthropology 139
(2), 109125.
Wapler, U., Crubzy, E., Schultz, M., 2004. Is cribra orbitalia synonymous with anemia? Analysis and interpretation of cranial pathology in Sudan. American Journal
of Physical Anthropology 123, 333339.
Wells, C., 1975. Prehistoric and historical changes in nutritional diseases and associated conditions. Progress in Food and Nutrition Science 1, 729779.
White, C.D., Armelagos, G.J., 1997. Osteopenia and stable isotope ratios in bone collagen of Nubian female mummies. American Journal of Physical Anthropology
103 (2), 185199.
White, C.D., Schwarcz, H.P., 2005. Temporal trends in stable isotopes for Nubian
mummy tissues. American Journal of Physical Anthropology 93 (2), 165187.
Zuckerman, M.K., Turner, B.L., Armelagos, G.J., 2012. Evolutionary thought in paleopathology and the rise of the biocultural approach. In: Grauer, A.L. (Ed.), A
Companion to Paleopathology, pp. 3457.