International Journal of Paleopathology 5 (2014) 917

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International Journal of Paleopathology

j ourna l ho mepage: www.elsev ier .co

Research Article

Analysis of nutritional disease in prehistory: Thein antiquity and today

George J. Armelagosa,, Kendra Siraka, Taylor Werkemaa, Betha Emory University, Atlanta, GA 30322, United Statesb Georgia State

a r t i c l

Article history:Received 11 MReceived in reAccepted 17 S

urrouDona

andy, thefantsat ma

in a withhe nenosis e po

simultaneously affecting an individual, and the patterning of these deciencies along lines of status, sex,and age.

2013 Elsevier Inc. All rights reserved.

1. Introdu

CircumHolmes thing, buit pointientirely

We havtory of the pathologiesrole of nutrof human perspectivecourse of h

CorresponE-mail add

1 Donald J. epitome of a sopposite endswith as scientithe debate, weplayed a signiand Mark MackUniversity of Mstudent at Em

1879-9817/$ http://dx.doi.oction

stantial evidence is a very tricky thing, answeredthoughtfully. It may seem to point very straight to onet if you shift your own point of view a little, you may ndng in an equally uncompromising manner to somethingdifferent. (Doyle, 1891, p. 402)

e three objectives in this essay: to describe the his-search for markers of scurvy and similar diet-related, to celebrate Donald J. Ortners1 role in unraveling theitional deciencies in the adaptation and well-beingpopulations, and to suggest broader anthropologicals useful in the study of these deciencies. Over theis long and productive career, Ortner investigated

ding author. Tel.: +1 14047249597.ress: antga@emory.edu (G.J. Armelagos).Ortner, in addition to be a major force in paleopathology, was thecientist and gentleman. While Don and I (GJA) were frequently at

of controversial issues in paleopathology, these were always dealtc matters and were never taken personally. No matter how heated

always greeted each other in a genuinely friendly manner. Don alsocant role in mentoring three of my former students: Michael Blakey

were mentored by Don as undergraduates before they enrolled at theassachusetts, and Molly Zuckerman before she enrolled as a graduate

ory. I will miss him and our scientic and social interactions.

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 andMays, 1998), and iron deciency anemia (Von Endt and Ortner,1982). While we note limitations in the descriptive and diagnostictradition of paleopathology that might limit more meaningfulstudy of an elusive skeletal condition like scurvy, we also reviewthe progress that has been made in scurvy diagnosis and highlightencouraging directions in broader anthropological research on thiscondition in antiquity.

2. Contextual background

Donald Ortner was a major force in the development ofmethodological and theoretical issues in paleopathology (Ortner,1991, 2002, 2009; Ortner and Aufderheide, 1991). Ortner andArthur C. Aufderheide organized a symposium held at the Inter-national Congress of Anthropological and Ethnological Sciences inZagreb, Yugoslavia in July, 1988 that reviewed the then-currentstate of paleopathology with an eye to future developments. Theproceedings of the conference, Human Paleopathology: CurrentSyntheses and Future Options (Ortner and Aufderheide, 1991)offers insights into a critical period in method and theory inpaleopathology.

Ortner (1991) framed the theoretical and methodologicalperspective that denes his contribution to the discipline of

see front matter 2013 Elsevier Inc. All rights reserved.rg/10.1016/j.ijpp.2013.09.007 University, Atlanta, GA 30302-3998, United States

e i n f o

arch 2013vised form 8 September 2013eptember 2013

a b s t r a c t

In this paper, we discuss the issues sopathology, and highlight the work of deciency impacts collagen formationmanifestations are observed routineldiagnosis difcult. Rapid growth in inand an increase in vascularization thulation. However, diagnosis of scurvystrikingly similar to those associatedthis confounding factor underscores tthat expands beyond differential diagresources, greater consideration of thm/locate / i jpp

search for scurvy

any L. Turnerb

nding the study of scurvy, or vitamin C deciency, in pale-ld Ortner in advancing this area of research. This micronutrient

results in damage to a variety of bodily tissues. While clinical lack of specic signatures on bone makes paleopathological, children, and subadults provides abundant remodeled tissuekes identication possible in younger segments of the pop-dults remains problematic, given that diagnostic lesions are

rickets, osteomalacia, and other conditions. We argue thated for a broader anthropological approach to scurvy researchto include more accurate reconstruction of diets and availablessibility even likelihood of multiple nutrient deciencies

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

paleopathology. According to Ortner, the paleopathologist mustanswer two deceptively simple questions that require complexanswers: What is it? and What does it mean? The answer toeach question is fundamental. Given the difculties of diagnosisin contempit is not suessential bthe fact thdiagnosed detail or dNaming a makes it dithe originadiagnostic An importaglossed ovesecond quebeyond mea broader d

One reseapproach isscurvy (Ort1999) that samong paletechniques of collagenTravis, 2008scopic techIves, 2006, 1997). Evenand Cox, 20bidity and (15501850(Brickley angist, and theelusive. Wescurvy:

It is not aits chieftiple subto extenand lossslight exsoft tissuopatholo

3. The scur

Almost afruit bats, bthesize theconvert glumust be cosoluble moconcentratipeppers (Gits capacitypathways. them to endet al., 1971)lars have suhumans thrdeciency, Stone (1966and history

misery and has altered the course of history more than any othersingle cause.

Scurvy manifests as a generalized condition with a variety ofsymptoms that progress over time and can vary between indi-

s (Taily inaturia)

Ther of ts et1999g ofthat urpu(Hirsant Hirscomasn (mman971)cieng bloof bosurpiquit

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charraveorary biomedicine despite its advanced technology,rprising that paleopathologists would nd diagnosisut also incredibly. This problem is compounded byat paleopathologists have, until recently, frequentlypathological conditions without describing them iniscussing their distribution among skeletal elements.lesion without completing a differential diagnosisfcult for other researchers to evaluate the validity ofl pathological determination and to standardize thecriteria for conditions with similar manifestations.nt aspect of paleopathology research, and one oftenr by more descriptive, case-oriented approaches, is thestion: What does it mean? This question should extendchanisms and a list of associated symptoms to includeiscussion of causal factors.arch area that would benet from this more inclusive

the study of scurvy. Ortner had an abiding interest inner et al., 2001; Ortner and Ericksen, 1997; Ortner et al.,erved as a stimulus for renewed interest in the diseaseopathologists. Unfortunately, there are only a few newfor diagnosing scurvy in skeletal remains. While the use

extraction and analysis shows promise (Koon, 2010;b), the application of standard macroscopic and micro-

niques remain the current tools of choice (Brickley and2008; Murray and Kodicek, 1949; Ortner and Ericksen,

so, a review of health and disease in Britain (Roberts03), with indisputable documentary evidence of mor-mortality from scurvy from the post-Medieval period

CE), found no skeletal evidence for vitamin C deciencyd Ives, 2006). This creates a riddle for the paleopatholo-

search for scurvy in earlier time periods has been just aslls (1975, p. 756) describes the difculties in diagnosing

n easy disease to recognize in skeletal remains because features are swollen, spongy, infected gums, and mul-cutaneous and perifollicular hemorrhages giving risesive purpuric and ecchymotic areas, anemia, lassitude

of muscle tone, and a tendency to sudden death onertion. Since these are all manifestations which affectes rather than bones, it is understandable that its pale-gical recognition is very rare.

vy enigma

ll animals, except for Homo sapiens, higher primates,ulbul birds, guinea pigs, and sh metabolically syn-

enzyme l-gulonolactone oxidase that is required tocose to vitamin C. Without the enzyme, vitamin Cnsumed from food sources. Vitamin C, a simple water-lecule, is found in many plants, with especially highons in citrus, tomatoes, potatoes, cabbages, and greenarca-Closas et al., 2004). This vitamin is essential for

as an antioxidant and facilitator of many metabolicHealthy humans have stores of vitamin C that allowure total dietary deprivation for 160200 days (Hodges, after which symptoms of scurvy will manifest. Scho-ggested that scurvy has caused more suffering amongoughout history than any other disease of nutritionalaside from generalized famine (Carpenter, 1988). In fact,, p. 345) argued, In the long period of human prehistory, scurvy has caused more deaths, created more human

vidualprimarioral fe(asthen1971).trophy(HodgeRaugi, bleedin1999) cular ptissue signic2005; hematcle pai(Hirschet al., 1

Debuildinphase is not the ubcreatedproteinCollagebrousamounblood forms ture rewalls, state oing of swolleAdvaning pu1971).is rare

Whand dris requC intaksteadythat thin softskeletadentininabilielevate

Thoceptibin hummonlylands tbeforedescribpocratpain inHirschperioditime tble 1). Evidence from clinical settings is measured behavioral features and changes in soft tissue. Behav-es include fatigue (Hodges et al., 1971), loss of strength(Fain, 2005) and changes in emotion (Hodges et al.,e are changes in soft tissue such as inammatory hyper-he gingiva (Fain, 2005) that leads to swollen gums

al., 1971) and periodontal bleeding (Hirschmann and). Weakness in the vascular system leads to pinpoint

the skin (petechiae bleeding) (Hirschmann and Raugi,causes dermal bleeding appearing as bruises or vas-ra (Fain, 2005). Edema occurs as uid accumulates inchmann and Raugi, 1999; Hodges et al., 1971) withbleeding into the joint spaces as hemarthroses (Fain,hmann and Raugi, 1999; Maat, 2004) and muscle as

(Fain, 2005), leading to joint pain (arthralgia) and mus-yalgia). Changes in hair with follicular hyperkeratosisn and Raugi, 1999) and congested follicles (Hodges

round out the soft tissue changes (Table 1).cy of vitamin C impacts the formation of collagen, theck of connective tissue and the majority of the proteinne. The bodys global response to vitamin C deciencyrising given its importance in collagen synthesis andous presence of collagen in human tissue. Collagen isbroblasts and comprises over 25% of the bodys total

is also the primary component of connective tissues.n form elongated brils that are the basic structure ofues such as tendons, ligaments, and skin. Signicant

collagen provide structure to the cornea, cartilage, bone,ls, intestines, and intervertebral discs. Collagen alsondomysium of muscle tissue. Impaired collagen struc-

in defective formation of bone osteoid and blood vesselting in weakened arteries and veins. Initially, there is ague with malaise and lethargy, followed by hemorrhag-l blood vessels that leave petechial spots on the skin,nts with muscular aches and pains, and bleeding gums.tages of the condition are characterized by suppurat-ducing wounds, neuropathy, and death (Hodges et al.,eated scurvy is invariably fatal, but, death from scurvyodern times.e symptoms of vitamin C deciency can be widespreadic, the treatment is remarkably straightforward. All thatfor a full recovery is the resumption of normal vitamins little as 6.5 mg of vitamin C will result in a slow butine in symptoms of scurvy (Hodges et al., 1971). Givenst diagnostic features (see below) of scurvy are founde, the impact on bone is difcult to decipher. However,ns (Table 1) include antemortem tooth loss, abnormaluction, altered bone formation in subadults due to the

osteoblasts to produce the osteoid seam, and possiblyn levels from increased absorption (Fain, 2005).humans and human ancestors have long been sus-

scurvy, attempts to determine the sources of scurvyopulations came surprisingly late. Though most com-buted to European maritime explorers seeking out newgh oceanic travel, scurvy was common in sailors longge of Discovery (Wells, 1975). It appears to have beenitially during the fth and fourth centuries BCE by Hip-one, 1966), who documented the physical symptoms ofower extremities and gangrene of the gums (Hess, 1920;5). In the three centuries between 1500 and 1800 CE, aacterized by an explosive increase in long duration mar-l, scurvy is thought to have caused the death of at least

G.J. Armelagos et al. / International Journal of Paleopathology 5 (2014) 917 11

Table 1Clinical and paleopathological diagnostic features of scurvy.

Diagnostic symptoms of scurvy

Clinical manifestations of scurvyBehavioral featuresFatigue (Hodges et al., 1971)

Asthenia (loss of strength) (Fain, 2005)Emotional changes (Hodges et al., 1971)

Soft tissue changesGingival 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 chemicalJoint 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, macroscopicHematoma 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, childrenPorous 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, adultsBilateral inammatory lesion of the greater wing of sphenoid (Ortner and

Ericksen, 1997)When bilateral on the sphenoid, other sites on skull effected (Ortner andEricksen, 1997)

New bone formation at the foramen rotundum in sphenoid bone (Geber andMurphy, 2012)

Porous and proliferative bone lesions affecting the cranial bones and scapulae(Brickley and Ives, 2006)

Abnormal porosity occurring throughout the skeleton

two million sailors (Drymon, 2008, p. 114). In 1499, Vasco de Gamalost 116 men of his crew of 170, and in 1520, Ferdinand Magel-lans crew was almost completely annihilated, with scurvy killing208 out of 230 sailors (Lamb, 2000). The diet of sailors was thesource of thhealthier atto good aof disease h1898). No fcause of illndesolate crevegetables and sailor dbiscuits andsailors becaperishable symptoms passengersWar I (Carp

Vitamindiate amelicitrus; this sLind (Baronthe rst to1753). Lindwas concerthat scurvysuming acidcan now beinto six exwere thougvented scur(Baron, 200that the anat least 200of the Lind convinced rations of sdies applied1995), bloomallow and2011), but 1932 (King,many ineffe

4. Paleopa

A combiOrtner, 201tem of diagfeatures (Bdiagnosis inmon featurwhich mayprehistory (

Accordinsubadult scThere may with scurvyskeletal chaated with sfeatures malogical consuch as ane

A numbof scurvy fe problem. While de Gama noticed that his men were certain port cities, he attributed this variation in healthir in these regions, consistent with the foul air theoryeld by many at this time (Cuppage, 1994; Ravenstein,urther thought was given to a dietary deciency as theess, though there are multiple anecdotes describing aw that became well after the consumption of fruits andat port. Ships were cold, damp, and unwholesome,iets consumed diets of putrid beef, rancid pork, moldy

foul water (Dunn, 1997, p. F64). The situation for manyme dire on long sea voyages after the onboard supply offruits and vegetables were depleted, at which point theof scurvy appeared. Scurvy was a scourge for crew and

on long voyages from the fteenth century until Worldenter, 1988).

C deciency treatment is simple with almost imme-oration with the consumption of fresh food, especiallyuccessful treatment for scurvy was discovered by James, 2009; Dunn, 1997), a surgeon in the Royal Navy and

carry out a systematic analysis of the disease (Lind, was assigned as a surgeon to the HMS Salisbury andned with the living conditions of sailors. He believed

was caused by purication and could be treated by con-ic foods. In A Treatise of the Scurvy, he described what

called a clinical trial in which 12 sailors were placedperimental groups and given different remedies thatht to improve health. Lind demonstrated that citrus pre-vy, though he thought it was only one of many remedies9). Though accredited with the discovery, Lind arguedti-scorbutic effects of citrus fruits had been known for

years before his time. While there have been revisionsstory (Baron, 2009), it was his research that eventuallythe Royal Navy to implement citrus juice in the dailyailors. However, citrus is only one of the many reme-

since antiquity. Herbals, trephination (Mogle and Zias,dletting, laxatives, root extracts, baths with brooklime,

hog weed have been prescribed (De Luca and Norum,the causal mechanism of scurvy was not known until

1953). Consequently, treatment was inconsistent, withctive approaches used well into the 20th century.

thological approaches to studying scurvy

nation of lesions (Brickley and Ives, 2008; Brown and1; Ortner et al., 1999), assessed using a weighted sys-nostic criteria based on clinical and paleopathologicalrickley and Ives, 2006), provide the basis for a scurvy

skeletal remains. Fragmentary remains that are com-es of the archeological record make diagnosis difcult,

contribute to an under-representation of the disease inGeber and Murphy, 2012).g to Ortner et al. (1999), indisputable evidence ofurvy is not well documented in archeological remains.be a number of reasons for this. For example, children

may die of other causes, or may not manifest observablenges in all cases. While pathological conditions associ-curvy have been identied for nearly a century, thesey be rare or difcult to differentiate from other patho-

ditions and may thus be attributed to other ailmentsmia (Ortner et al., 1999).er of skeletal changes are relevant to the diagnosisrom 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. Radiographicimaging reveals joint space loss, osteolysis, defective osteoid matrixformation, bone resorption, trabecular and cortical osteoporosis,and osteonecrosis (Fain, 2005). Chemical analysis of collagen showsalteration tin proline hBuilding onand modernated betwending lessthe latter viof skeletal in skeletal swellings inoften obserof some scporous, hypEricksen, 19of anemia).scurvy, it ccomplicatesOrtner et aporosity in of anemia marrow hysince in thedifcult to danalyses (Bdistinguishscurvy is pand orbitalwith marroscanning eling stimulapenetrated response to

Ortner eand anemiaargued thatmia stemmrisk for scutrient deccertain degresponse to2007; Larraresults fromiron that rearcheologiche describemacroscopichanges in The enlarge(Barlow, 18periosteal pnot necessamia and scuvitamin C d2005, p. 125contain onlcontent is nnon-heme ivitamin C dco-morbidi

The bonthe best eviand small c

ir Tho Engla

vault less p

oduc alsosity n, 1id brtneits hildrerfaceior ar

et aa of l evid

to nd evidence of changes in the alveolar bone. Alveolarses, alveolar sockets, the hard palate, and the coronoid pro-e marked with abnormal porosity (Ortner et al., 1999) (Fig. 5).e cases, there are also lesions on the scapula (Brickley and

his 12-year-old child (Pachacama, Peru) shows porous lesions in the regionht greater wing of the sphenoid. Specimen date between 1000 and 1530 CE.

e biomedical collections of the National Museum of Natural History, Smith-nstitution, Catalog no. 266599 (Ortner and Ericksen, 1997).o the hydroxylation process, appearing as a deciencyydroxylation (Fain, 2005; Koon, 2010; Travis, 2008a).

these ndings, recent research in archeological humans guinea pigs (Koon, 2012) has successfully differenti-

en individuals with unaffected versus scorbutic bone, proline hydroxylation in certain collagen peptides ina mass spectrometry analysis. Macroscopic observationchanges in clinical cases is more relevant to diagnosispopulations. Hematoma formation and subperiosteal

the lower extremities with bilateral involvement areved on the tibiae (Aschoff and Koch, 1919). The orbitsorbutics (vitamin C decient individuals) may showertrophic orbital lesions (Fraenkel, 1929; Ortner and97) that are similar to cribra orbitalia (a skeletal sign

While the porous lesion may indeed be diagnostic ofan difcult to distinguish it from anemia, which often

a differential diagnosis based on porous lesions alone.l. (1999) described the distinct distribution of skeletalscurvy and anemia, arguing that a differential diagnosisin skeletal remains is possible based on evidence ofperplasia. Distinguishing this is easier said than done,

early stages of anemia, symptomatic lesions can beifferentiate from scurvy; however, recent microscopic

rickley and Ives, 2006; Wapler et al., 2004) suggest thating between pathogenic bone processes in anemia andossible: anemia creates porous lesions of the cranial

bones caused by a widening of the diple associatedw hypertrophy and cortical bone thinning, whereasectron microscopy suggests that scorbutic hemorrhag-tes periosteal deposition on the orbits that may beto varying degrees by proliferating vasculature, both in

hemorrhage.t al. (2001) suggested that comorbidity between scurvy

is possible; Walker et al. (2009) echoed this notion and porous lesions may also result from hemoblastic ane-ing from B-vitamin deciency. Given that individuals atrvy in antiquity were likely at risk for other micronu-iencies as well, it is entirely reasonable to expect aree of comorbidity. Indeed, anemia is often a secondary

scurvy in modern clinical settings (Burk and Molodow,lde et al., 2007; Tamura et al., 2000) due to bleeding that

scurvy and reduction in the ability to absorb nonhemesults in anemia (Fain, 2005). Ortner (2003) said thatal samples offer few example of comorbidity, thoughd one such case. While scurvy and cribra orbitalia havecally similar features in the orbit, only scurvy promotesthe sphenoid bone, the mandible, and the hard palate.ment of the cranial bosses, known as Parrots swellings83; Ortner and Ericksen, 1997), and osteopenia, and/orroliferation (Fain, 2005) are also found in scurvy but arerily diagnostic by themselves (see Fig. 1). However, ane-rvy may in fact form an interacting relationship in thateciency inhibits the absorption of non-heme iron (Fain,). Plants (which contain varying amounts of vitamin C)

y non-heme iron and in animal esh about 60% the ironone-heme in nature. Given the difculty in absorbingron, scurvy could result in lesions characteristic of botheciency and iron deciency anemia that reect in vivoty (Fig. 2).es of infants and children in prehistory provide perhapsdence for diagnosing scurvy. The rapid growth of infantshildren increases rates of bone remodeling as well as

Fig. 1. Sgeons ofnote theexhibits

the prwhichis poroEricksesphenoeter (Othe orband chrior suposterOrtnerthe areclinicapectedprocescess arIn som

Fig. 2. Tof the rigFrom thsonian Imas Barlow attributed the lesion (Museum of the Royal College of Sur-nd, Wellcome Museum, Catalog no. S56.4.) Ortner and Ericksen (1997)s enlargement of the frontal and parietal bosses with the interior vieworosity in the areas underlying the bosses.

tion of soft tissues such as muscles and blood vessels, require collagen. The key feature that denes scurvyon the greater wing of the sphenoid bone (Ortner and997; Ortner et al., 1999). The lamellar porosity on theone is characterized by lesions less than 1 mm in diam-r and Ericksen, 1997). Frequently, porosity on the roof ofas also been found (Ortner et al., 1999) (Fig. 3). Infantsn also display porosity on the lateral, internal and infe-s of the zygomatic bone (Ortner et al., 1999) and theea of the maxillary surface (Ortner and Ericksen, 1997;l., 1999) (Fig. 4); porosity has also been found aroundthe infraorbital foramen (Ortner et al., 1999). Given theence of gingival involvement with scurvy, it is not unex-

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, abnormalbone 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 coloronline at http://wileyonlinelibrary.com/journal/oa (Brown and Ortner, 2011).

Ives, 2006) (Fig. 6) and porous lesions on the ilium (Fig. 7) (Brownand Ortner, 2011) (Table 1).

Ortner et al. (2001) examined subadult human skeletons fromNative American archeological sites in the United States (mid-Atlantic, Florida, American Southwest and Plains) for skeletalevidence of scurvy. The prevalence of probable scurvy in subadults 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 quan-tity of food, differences in storage and use, periodic shortages, andthe quantity of corn in the diet (Ortner et al., 2001).

Van der Merwe et al. (2010) describe clinical evidence of scurvyin preparation for an analysis of the deciency in 19th-century

Fig. 4. Ortnermaxilla extendpalatal surfacecolor online at

Fig. 5. Porositextending posure is availabland Ortner, 20

miners frommade throubleeding, (psis, hematolimbs (Fainand Uytterwho were rfound lesioviduals. Difhemarthrosial and buhematomasusually uniand subseqings reect

primg. Inted w, thiseletal vitaougell

, Ortttle ll leslogynd Smade rhaginassociaMerweifest sknorma

Althbeen w(1989)very liskeletaopathoCrist a reports abnormal porosity involving the infraorbital foramen of theing medially to the lateral border of the nasal aperture (a). On the

of the maxilla exhibiting dense porosity (b). This gure is available in http://wileyonlinelibrary.com/journal/oa (Brown and Ortner, 2011).

out the skeresponse isscurvy was

More inof the greattrophic bonporosity onaffected (Oof new bonnoid bone (porotic boninvolved (B

5. Theoret

The comtive of scury involving the medial surface of the mandibular coronoid processterior to the mandibular foramen and to the edge of the ramus. This g-e in color online at http://wileyonlinelibrary.com/journal/oa (Brown11).

Kimberly, South Africa. Differential diagnosis wasgh observation of gingival hypertrophy and petechialinpoint bleeding of the skin), follicular hyperkerato-ma formation and subperiosteal swelling in the lower, 2005). Maat and coworkers (Maat, 1981, 2004; Maatschaut, 1984), examining remains of Dutch whalersecorded as being aficted with scurvy (Stoney, 1900),ns suggestive of vitamin C deciency in 39 of 50 indi-ferential diagnosis included subperiosteal hematomas,es and periodontal bleeding (Maat, 2004). Bilateral tib-lar subperiosteal hematomas were also recorded. When

were identied on the upper extremities, they werelateral, which could also suggest the presence of scurvyuent opportunistic infection. The quality of these nd-s extremely well-preserved remains. The diagnosis wasarily on the basis of soft tissue that displayed hemor-terestingly, only a single individual had bony lesions

ith healed vitamin C deciency. According to Van der suggests that whalers who died of scurvy did not man-l lesions, which only developed with the restoration ofmin C levels (Murray and Kodicek, 1949).h skeletal lesions associated with infantile scurvy havedescribed by many authors such as Stuart-Macadamner and Ericksen (1997) and Brickley and Ives (2006),iterature is available on adult scurvy and the resultingions (Van der Merwe, 2007). The evidence of pale-

of scurvy in adults is more difcult to diagnose (but seeorg, this issue). Abnormal porosity occurring through-

leton is common in scurvy. Unfortunately, the skeletal

so general that supporting evidence to assure that the actual source of the porosity is required.dicative of scurvy is the bilateral inammatory lesioner wing of sphenoid bone indicated by porotic hyper-e (Ortner and Ericksen, 1997). When there is bilateral

the sphenoid bone, other sites on skull are usuallyrtner and Ericksen, 1997). More promising is evidencee formation at the foramen rotundum of the sphe-

Geber and Murphy, 2012). When there are proliferativee lesions affecting the cranium, the scapula may also berickley and Ives, 2006).

ical issues in the paleopathology of scurvy

plexity of describing and interpreting lesions indica-vy 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. Compoporosity whilehypertrophic balveolar proceBrickley and Iv

that lesionspresentatiohistorical ttions were descriptivethat exists pretation, apathologicaSteinbock, cal anthropstudy of pern medicianthropoloa profoundpaleopatho(Armelagosassigning awas considecated suspesite image of abnormal porosity on supraspinous process of scapula. On the left is the m on the right is an age-matched SEM image of normal scapula (Brickley and Ives, 2006)one formation (Schreiner Collection, Catalog no. 4733 from Ortner and Ericksen, 1997).sses and toward frontal process. (Right) Lateral view of maxilla showing normal, small, les (2006). AJPA.

may remain conned to soft tissues without skeletaln. However, this complexity has also been due to arend in paleopathology whereby pathological condi-described and diagnosed without fully standardizing

criteria. Ortner highlighted the considerable variabilityin the quality of observations, diagnosis and inter-nd was at the forefront of developing protocols forl diagnosis (Ortner and Putschar, 1981; Buikstra, 1977;1976). In Human Paleopathology, Ortner, a biologi-ologist, and Aufderheide, a physician, combined thealeopathology with clinical perspectives from mod-ne rather than with a biocultural perspectives fromgical science (Ortner and Aufderheide, 1991). This was

distinction that has signicantly impacted the eld oflogy and has sparked a productive theoretical debate, 1994). The issue of developing methodologies for

clinical diagnosis to archeological skeletal conditionsred by Ortner (1992, p. 6) to be so critical that he advo-nding hypothesis testing until standardized protocols

are producclearly statthe push toor until unrestricted itof disease evolution (Z

A seconpaleopathothe researctions becamArmelagos an overarchif that innobeyond diathe applications. For e2000; Pbships (Pbacroscopic appearance of porosity. In the middle is a SEM image of. AJPA. Detail of posterior left parietal showing a porous lesion with

(Left) Young infants maxilla showing porosity extends well beyondocalized porosity restricted to alveolar pits and infraorbital foramen

ed. While it is critically important for each study toe the methodology and descriptive criteria employed,

make paleopathology essentially atheoretical unlessiform diagnostic criteria are established has seriouslys interpretive scope in understanding ancient patternsin human populations and of humanpathogen co-uckerman et al., 2012).

d important factor in limiting the growth and scope oflogy was a reliance on the newest technology to driveh with the result that any substantive research ques-e secondary to the technology applied (reviewed in

et al., 1982). The application of new technology withouting theoretical framework is only an illusion of progressvative technology is not applied to solve a problemgnosis. There are now many studies that demonstratetion of pioneering technology to solve interesting ques-xample, ancient DNA extraction (Cooper and Poinar,o, 1989) has been used to solve population relation-o et al., 2004) and the detection (Donoghue et al., 2008,

G.J. Armelagos et al. / International Journal of Paleopathology 5 (2014) 917 15

Fig. 7. The exdence of abnodense porosityhttp://wileyon

2004) and sof pathogeing the orig2005; Harpbeen used aestimate nuto changesSchwarcz, 22012), and et al., 2005)

The analows a deduto reconstrview, the preconstructhave left thattempts tothey lived ait has certainot possiblediagnosis in

There is,or exclude aan inductivinference. years, it haopathologyto paleopatscientic diwithout sacanalysis usi

one devises alternative hypotheses; second, one designs experi-ments that exclude or falsify one or more of the hypotheses; third,one carries out experiments to get clean results and nally, onerecycles the procedure by repeating the process.

ile swithperihereatho

comelecnmenof scatingsis. Gmain

ard

precrtaind de

whaes intionshniq, a brts ins intce ofmben C at al., 1l anute ternal surface of the left ilium showing dense porosity without evi-rmal bone growth (a). The internal surface of the left ilium shows

and bone hypertrophy (b). This gure is available in color online atlinelibrary.com/journal/oa (Brown and Ortner, 2011).

Whences non-exogy. Tpaleoprely onble to senvirodence formuldiagnothis re

6. Tow

Theas it pend antion, ofourselvpopulatic tecabsentcontexinsightnicanin a nuvitami(Guil eotanicacontribpread of a diseases (Fletcher et al., 2003), while analysesn DNA have made signicant strides in understand-in and evolution of major diseases (Armelagos et al.,er et al., 2008a, 2008b). Similarly, stable isotopes haves part of osteological analyses to reconstruct diet andtritional status in archeological populations related

in fertility (White and Armelagos, 1997; White and005), variation in life histories (Turner and Armelagos,the physiological effects of acute disease stress (Fuller.lysis of pathology in prehistoric populations often fol-ctive methodology in which the researcher attempts

uct the factors that cause the skeletal lesions. In thisaleopathologist is much like the detective who has to

the crime from the evidence long after the criminalse scene. Instead of a crime scene, the paleopathologist

reconstruct the broader lifeways of a population afternd died. While the deductive approach has been useful,n inherent limitations, one of which is that it is usually

to select from alternative conclusions (i.e., differential the case of scurvy and other pathologies).

however, a methodology that can systematically falsifylternative hypotheses. Platt (1964) proposed the use ofe approach to test hypotheses, which he called strongAlthough inductive inference has been known for manys only recently penetrated the methodology of pale-. Strong inference can be very effective when appliedhology in that it acts as the means for transforming aagnostic endeavor into a more strongly theoretical one,ricing methodological rigor. There are four stages in anng the approach of strong inference (Platt, 1964). First,

were availaconcert witreconstruct(Price, 2012incidence w

In modeeconomicallated elderl2003). Bioasocial inequior, makingscurvy by in bone, oremains woof general mlarly anemimarginalizathese indivoped for coways to mono visible s

7. Conclus

Solutiongiven the asubtle chanation in bomay be posles in affedivergencetrong inference is most effectively applied to sci- experimental possibilities, it can be useful in

mental, or reconstructive sciences such as paleopathol- is obviously a need to modify the methods oflogical analysis. Ultimately, the paleopathologist mustparative analysis for natural experiments. It is possi-t samples that highlight differences in biotic or culturalt. Strong inference can be applied to archeological evi-urvy by seeing how diagnostic features are used in

falsiable hypotheses, thus engaging in differentialiven the difculty with differential diagnosis, however,s a formidable task.

an anthropological study of ancient scurvy

eding pages center primarily on Ortners rst questions to scurvy; in order to study what it is, one must rstscribe it. In turning our attention to the second ques-t scurvy means, we argue that it is as important to push

thinking about the implications of scurvy in ancient, as it is to move forward in developing new diagnos-

ues. If the skeletal signs of scurvy are ambiguous oroader anthropological study of ecological and cultural

which affected individuals lived may provide criticalo assessing the likelihood of incidence and possible sig-

scurvy in antiquity. For instance, given that wild plantsr of global regions have much higher concentrations ofnd other antioxidants than do cultivated domesticates997; Halvorsen et al., 2002; Simopoulos, 2004), paleob-

alyses of surrounding soils at archeological sites woulda great deal to understanding what wild food resourcesble to different populations (e.g., Klaus, this issue). Inh isotopic and trace elemental methods of paleodietion to estimate what resources were actually consumed), paleopathologists could approach assessing scurvyith a much stronger set of contextual data.rn contexts, scurvy is seen in poorly nourished andly disadvantaged groups including alcoholics, the iso-y, and those who have been institutionalized (Pimentel,rchaeology has a long tradition of studying aspects ofality, marginalization, cultural transitions, and behav-

it well-suited to round out studies of scurvy. Sinceitself may not leave visible or unambiguous tracesne strategy of investigating its presence in ancientuld be to identify those individuals who exhibit signsalnutrition, other micronutrient deciencies (particu-

as), or mortuary contexts suggesting relative poverty,tion, or violence (e.g. Crandall, this issue). Subjectingiduals to more in-depth analyses such as those devel-llagen analysis by Koon (2012) would provide feasiblere accurately identify scurvy in individuals who exhibitkeletal signs.

ion

s to the scurvy enigma may soon be within reach,dvancements in specic diagnostic tools for studyingges in collagen structure, identifying microscopic vari-ny reactions to different deciencies. In the future, itsible to differentiate between collagen amino acid pro-cted versus unaffected individuals and better identify

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 holisticapproach to paleopathology that draws on theories and methodsin archeology and social bioarchaeology is needed alongside tech-nologically driven strides. Attending to co-morbidity and to thesocial and eexacerbate and noninfescurvy is aning what itGiven the epotential foDon Ortnermade since

Acknowled

We wouanonymousearlier versDon Ortnerto paleopat

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Analysis of nutritional disease in prehistory: The search for scurvy in antiquity and today1 Introduction2 Contextual background3 The scurvy enigma4 Paleopathological approaches to studying scurvy5 Theoretical issues in the paleopathology of scurvy6 Toward an anthropological study of ancient scurvy7 ConclusionAcknowledgementsReferences