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International Journal of Paleopathology 5 (2014) 34–45

Contents lists available at ScienceDirect

International Journal of Paleopathology

j ourna l ho me pa ge: www.elsev ier .com/ locate / i jpp

esearch Article

ubadult scurvy in Andean South America: Evidence of vitamin Ceficiency in the late pre-Hispanic and Colonial Lambayeque Valley,eru

aagen D. Klausa,b,c,∗

Department of Sociology and Anthropology, George Mason University, United StatesMuseo Nacional Sicán, PeruMuseo Nacional de Arqueología y Etnografía Hans Heinrich Brüning de Lambayeque, Peru

r t i c l e i n f o

rticle history:eceived 3 September 2012eceived in revised form 5 September 2013ccepted 5 September 2013

eywords:

a b s t r a c t

Scurvy is a disease caused by vitamin C deficiency and is a key paleopathological indicator of subadulthealth and nutritional status in the past. Yet, little is known about scurvy in human remains from SouthAmerica and the Peruvian Central Andes in particular. In the Lambayeque Valley Complex on the northcoast of Peru, a sample of 641 archaeologically recovered subadults (A.D. 900–1750) were scored for theskeletal manifestations of vitamin C deficiency, testing the hypotheses that scurvy was common in this

itamin C deficiencyicketsifferential diagnosisten

region and that prevalence increased following European contact. The findings reveal only five convinc-ing cases of scurvy; overall prevalence appears extremely low, and scurvy did not become perceptiblymore common following conquest. Of diagnostic interest, complex ectocranial vascular impressions weredocumented in two cases. Though rarely attributed to scurvy, examination suggests they formed duringscorbutic episodes. Another Colonial Period subadult may demonstrate comorbidity between scurvy andrickets. This work also provides new questions for the investigation of scurvy in Andean South America.

. Introduction

Scurvy is a metabolic disorder produced by chronic inadequatentake of vitamin C. As one of the central goals of paleopathologynd bioarchaeology is to reconstruct health and nutrition in theast, scurvy ranks as a key variable in the assessment of nutri-ional stress and dietary adequacy in human populations. Whilecurvy has long been underreported in the paleopathological liter-ture, it has received increasing perception, focus, and diagnosticigor, particularly over the last decade. This visibility is largelyue to the development of Donald Ortner’s diagnostic criteria ofcurvy in the skull (Ortner and Eriksen, 1997; Ortner et al., 1999,001) and postcranial skeleton (Ortner, 2003). Subsequent studiesave shed new light on dietary insufficiency, subsistence econ-my, human–ecology synergisms, urbanism, and socioeconomicnequality (e.g., Melikian and Waldron, 2003; Lewis, 2004; Brickley

nd Ives, 2006, 2008; Mays, 2008; Waldron, 2009; Lewis, 2010;an der Merwe et al., 2010a,b; Brown and Ortner, 2011; Geber andurphy, 2012).

∗ Correspondence to: Department of Sociology and Anthropology, Robinson Hall, Room 305, George Mason University, MSN 3G5 Fairfax, VA 22030-4444, Unitedtates. Tel.: +1 703 993 1440; fax: +1 703 993 1446.

E-mail address: hklaus@gmu.edu

879-9817/$ – see front matter © 2013 Published by Elsevier Inc.ttp://dx.doi.org/10.1016/j.ijpp.2013.09.002

© 2013 Published by Elsevier Inc.

While the skeletal evidence for scurvy spans thousands of yearsand almost the entire world, Brickley and Ives, 2008, Table A1), onlyone study has emerged from Andean South America. Ortner andcolleagues (1999) examined 363 subadult crania from Peru curatedat the Smithsonian Institution’s National Museum of Natural His-tory (NMNH). This work found probable cases in just over 10.5%of the examined crania to establish that scurvy was: (1) indeedpresent in the ancient coastal and highland Andes, and; (2) wasevidently a common disease condition in pre-Hispanic Peru. How-ever, most of these human remains were selectively collected fromthe devastated landscapes of looted cemeteries along Peru’s cen-tral coast during the early 20th century expeditions of Hrdlicka(1914). Key questions regarding cultural, spatial, temporal, and epi-demiological variation could not be addressed as correspondingcontextual data were either destroyed by looting or lost by insuffi-cient documentation during surface collections that focused mostlyon crania. Since no postcranial remains accompanied the NMNHPeruvian crania, broader assessment of lesion distributions withinaffected individuals was also inhibited.

Scurvy has yet to be assessed in the arid Lambayeque ValleyComplex of Peru’s north coast for additional contextual infor-

mation regarding local Lambayeque ecology and cultural history,see the Online Supplemental Materials.This region and its fiverivers provided the setting for one of the independent centersof Andean cultural development beginning around 1500 B.C. Key

al of Paleopathology 5 (2014) 34–45 35

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Table 1Diagnostic criteria for scurvy used in this study, drawn from Ortner (2003), Ortneret al. (1999), and Brickley and Ives (2008).

Anatomical site Criteria

Cranial vault Abnormal regions of porosity <1 mm indiameter penetrating cortical bone; wovenbone deposition; impressions of vascularrami or networks

Greater wing of thesphenoid bone

Abnormal regions of porosity <1 mm indiameter penetrating cortical bone

Orbital plate Abnormal regions of porosity <1 mm indiameter penetrating cortical bone; newbone deposition

Temporal bone Abnormal regions of porosity <1 mm indiameter penetrating cortical bone

Zygomatic bone, internaland external surfaces

Abnormal regions of porosity <1 mm indiameter penetrating cortical bone; newbone deposition

Anterior maxilla Abnormal regions of porosity <1 mm indiameter penetrating cortical bone; wovenbone deposition

Infraorbital foramen New bone depositionHard palate New bone depositionCoronoid process of the

mandible, medial surfaceNew bone deposition

Long bone diaphyses New bone depositionLong bone metaphyses Metaphysial fractures, cortical thinning,

deposition of new boneSupra- and infraspinous

fossa of the scapulaAbnormal regions of porosity <1 mm indiameter penetrating cortical bone; newbone deposition

H.D. Klaus / International Journ

evelopments spanned Cupisnique, Moche, and Sicán cultureshat were characterized by complex socioeconomic organization,iverse subsistence economies, and innovative technologies (Alva,012; Alva and Donnan, 1993; Alva Meneses, 2008; Dillehay, 2011;onnan, 1989; Donnan, 1990a,b, 2012; Elera, 1986; Hayashida,006; Heyerdahl et al., 1995; Klaus et al., 2013a,b; Shimada, 1990,995, 2013; Shimada, 1994, 1999, 2000; Shimada et al., 2013;schauner, 2001; Wester, 2012). Following European conquestn the 16th century, the region became central to the Colonialiceroyalty. Emerging bioarchaeological reconstructions of latere-Hispanic and Colonial Lambayeque have revealed multifacetedpatial and temporal patterns of health variation and a range ofathological conditions endured by local communities (Farnum,002; Klaus, 2012; Klaus and Tam, 2009, 2010; Klaus et al., 2009,010; Shimada et al., 2004; Toyne, 2011a,b). Increasing focus haseen placed on reconstructing metabolic stress (Farnum, 2002;laus and Tam, 2009), but scurvy has remained unreported.

In this report, two basic hypotheses are addressed. Using a sam-le of archaeologically documented remains, it is first hypothesizedhat as with the earlier work of Ortner et al. (1999) on remainsrom Peru’s central coast, scurvy was equally common in the northnd will reflect evidence of a comparable prevalence. Second, it isypothesized that scurvy became more common during the post-ontact Colonial period when biological stress broadly increasedKlaus and Tam, 2009).

. Pathogenesis and lesion characteristics

Humans and other great apes share a mutation of the genehat produces l-gluno-�-lactone oxidase, and we fail to producehis final enzyme crucial to the synthesis of ascorbic acid, or vita-

in C (Nishikimi and Udenfriend, 1976, 1977; Stuart-Macadam,989; Brown and Ortner, 2011; Weinstein et al., 2001). Obtain-

ng at least 10 mg/day of dietary vitamin C is required. Vitamin Cccomplishes hydroxylation of proline and lysine into hydroxypro-ine and hydroxylysine, which are necessary to form collagen fibrilolypeptide precursors (Hodges, 1980). Insufficient dietary intakef vitamin C leads to defective Type 1 collagen formation, which inurn promotes production of defective osteoid, fragile blood vesselsrone to rupture, and periosteal membranes with a propensity toear. Depressed immune function, compromised blood formation,nd suboptimal metabolism of iron and folate are additional corol-aries (Tamura et al., 2000; Weinstein et al., 2001; Akikusa et al.,003; Lewis, 2007).

Hemorrhage is a hallmark of scurvy. Outside the circulatory sys-em, the body treats blood as an inflammatory agent targeted foremoval. The inflammatory reaction in response to hemorrhagen subadults can affect both the cranial and postcranial skeleton.he vascular response in the cranium may stimulate an incur-ion of osteoclasts into existing cortical bone that creates channelsor newly formed capillaries (usually less than 1 mm in diameterOrtner et al., 1999; Kozłlowski and Witas, 2012]), thus provid-ng pathways for white cells to remove extravasated blood. Yet,uch new vessels are themselves likely to be structurally compro-ised and deficient in collagen, thus exacerbating hemorrhage and

nflammation in a feedback loop (Brown and Ortner, 2011, 198).hould hemorrhage elevate the periosteum, new, hypertrophicone will form hematomas; osteoblasts migrate via chemotaxis toematomas, which then begin to organize into connective tissueRagsdale and Lehmer, 2012).

Common skeletal sites manifesting subadult scurvy include the

uperior eye orbits, ecto- and endocranial regions of the cranialault, alveolar bone, the hard palate, and the posterior maxilland mandible (Table 1). Ortner and colleagues (1999, 2001) arguebnormal bilateral porosity of the greater wing of the sphenoid

Ribs Fractures adjacent to oestochondraljunction; flaring rib ends

bone is virtually pathognomonic for scurvy, produced by chronicbleeding of ruptured connective or vascular tissue owing to minortrauma or normal muscular functions such as chewing (Ortner,2012). Endocranially, scurvy can produce epidural bleeding asarteries in the dura rupture and leak into surrounding tissue spacesuch that hematoma separates the dura and periosteum from thebone and tears bridging vessels between the arachnoid and duralayers of the meninges (Kumar et al., 2009; also Lewis, 2004).

In the infra-cranial skeleton, movement of the muscles of therotator cuff is implicated in the formation of porous lesions andnew bone deposition in the supra- and infraspinatus fossa of thescapula. Osteochrondral junctions of ribs and long bone metaphy-ses may fracture. New bone ≤1 cm thick may be deposited onaffected regions of long bone diaphyses. The most massive subpe-riosteal hematomas are observed on the weight-bearing long bonesof the lower limb, especially in children old enough to be walking(Ortner, 2003, 384). Sharpey’s fibers, which attach periosteum tobone, are shorter and less numerous in children and have less resis-tance to tearing and bleeding (Caffey, 1978; Lewis, 2007). Brownand Ortner (2011) and Geber and Murphy (2012) recently identi-fied the ilium and the foramen rotundum of the sphenoid bone aspotential sites of scorbutic inflammation.

A common view holds that scurvy manifests in bone followingreintroduction of vitamin C into the diet following an episode ofdeprivation (Brickley and Ives, 2008). In essence, skeletal signs ofthis disorder may represent signs of recovery, implying that lesionformation is akin to a Cartesian switch that is flipped upon the con-clusion of a scorbutic episode. However, multiple animal, clinical,and experimental studies (i.e., Dalldorf, 1929; Hamm and Elliot,1938; Brailsford, 1952; Hodges et al., 1971) abundantly contributeto a progressive model of skeletal lesion formation in responseto insufficient vitamin C. Pathophysiologic and cellular functionalperspectives thus seem to involve a spectrum of responses, first

spanning a period of progressive drawdown of bioavailable vitaminC that promotes poor collagen formation, bleeding, and inflamma-tory response. Only small amounts of vitamin C are needed for

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6 H.D. Klaus / International Journ

steoblasts to produce considerable amounts of new periostealone (Bourne, 1942), and total exclusion of ascorbic acid fromuman diets is very rare. During this window of insufficiency,steoblasts produce osteoid, though in progressively suboptimaluality. Should insufficiency lead to total deprivation, a secondindow would follow, and osteoid and collagen production would

erminate. Third, should vitamin C sufficiency be subsequentlyegained, progressively elevated bone formation would occur inesponse to hematomas formed during the first and second modesf pathophysiological manifestation.

. Materials and methods

.1. Archeological contexts

The Lambayeque Valley Biohistory Project has documented thekeletal remains of 1968 individuals in the Lambayeque Valleyomplex at 19 sites (Fig. 1). The samples span what appears to beoth a demographically and socially representative cross sectionf the native population from approximately A.D. 900–1750Klaus et al., 2013a,b). Because of the overlapping macroscopicharacteristics of growth-related new bone and inflammatoryhanges to bone, subadults less than 12 months ± 3 months wereemoved from the sample and alveolar processes were not scored.

total of 641 subadults (0–15 years of age at death) were com-lete and sufficiently old to examine for this study. Of these, fiveandidate cases of scurvy were identified. Detailed descriptionsf the biocultural setting, archaeological contexts, and completesteological descriptions of these five individuals are present inhe online Supplementary Materials that accompany this article.

Case 1 comes from the site of Chornancap in the lower Lam-ayeque drainage. Founded around A.D. 900, Chornancap was aonumental secondary political center from ca. A.D. 900–1375

Wester, 2010; Klaus et al., 2011). Chornancap South PlatformCSP) Burial 2 included the skeleton of a child 5–7 years of age, whoad been interred in a commoner cemetery dating to the Chimúccupation (∼A.D. 1375–1470). Case 2 was identified at Jotoro,ear the northern margin of the Lambayeque Valley Complex inhe mid-La Leche valley. Jotroro was a large, stable, and prosperousommunity occupied from A.D. 900 to the Early Contact period ofhe 1530s (Martínez, 2011). Burial O1M1-E7 is one of more than0 burials documented thus far at Jotoro. This funerary contextontained the virtually complete skeleton of a child 16–21 monthsf age. Decorated grave goods indicate the child, again an inferredember of the commoner population, was buried during the

erminal pre-Hispanic Inka occupation (A.D. ∼1470–1532).Cases 3–5 all originate from the Colonial period town of Santa

aria de Magdalena de Eten (or simply Eten), which was estab-ished as a forced nucleated resettlement of multiple communitiesuring the mid 16th century. Its ruins are under extensive sea-ide sand dunes at the southwest corner of the Reque drainage.hree church ruins were excavated, including an Early/Middleolonial cemetery containing the remains of native Muchik peopleuried under the mission church in Eten (∼A.D. 1533–1620);Alvarez-Calderón and Klaus, 2013). Case 3 was Burial CNS U2-36,

4.5–5.5-year-old child, and whose nearly complete skeletonas located in the northeast corner the nave. Case 4 was BurialNS U4AE-2, a relatively complete subadult, 16–21 months ofge at death. This was an intrusive Late Historic burial interredometime after A.D. 1776. Case 5 was Burial CNS U3-91. Based onts deep stratigraphic position, this was one of the first burials inten, probably interred during the 1530s or 1540s. The skeleton

f this 1–1.5-year-old child was incomplete and was disturbed byhe subsequent interrment of an adult. The mandible, vertebralolumn, sacrum, right ribs, entire upper left limb, both ilia, pubicones, ischia, and feet were absent from the funerary context.

aleopathology 5 (2014) 34–45

3.2. Lesion scoring criteria

A subadult was defined as either any individual without a thirdmolar in occlusion or who possessed an unfused spheno-occiptialsynchondrosis. More specific age estimations were then calculatedbased on the attainment of maturity stages relating to tooth crownand root formation, tooth eruption, epiphyseal fusion, and longbone length (Buikstra and Ubelaker, 1994). Potential signs of scurvyincluded abnormal porosity and periosteal bone deposition in theanatomical sites listed in Table 1 and were scored as present, absent,or unobservable and observed macroscopically under 10× magni-fication using a hand-held loupe. Abnormal porosity was definedfollowing Ortner and Eriksen (1997) and Ortner et al. (1999, 2001)as a localized phenomenon of dense penetrating holes usually lessthan 1 mm in diameter. Surface porosity and new periosteal bonedeposition was scored as unobservable in any cranium that lacked:(1) a sphenoid bone with an intact cortical area consisting of lessthan 50% of its total surface, and (2) at least one orbital roof consist-ing of less than 50% of its total surface. Long bones were evaluatedfor the presence or absence of abnormal periosteal or pathologicalbone deposition along both diaphyses and metaphyses, which werescored as unobservable if less than 50% of a diaphysis or metaphysiscould be observed.

4. Results

A visual summary of the results is presented in Table 2, whiledetailed descriptions and additional images of the lesions aresupplied in online Supplementary Materials that accompany thisarticle.

4.1. Case 1: Chornancap South Platform Burial 2 (5–7 years old)

Case 1 exhibited a series of lesions that affected the cranium.Abnormal porosity was observed bilaterally on the ectocranial sur-face of the greater wing of the sphenoid bone (Fig. 2). Porosityextended posteriorly to the temporal bone and the inferiolateralportions of the frontal bone. Fine bone deposits ringed both infraor-bital foramen extending superiorly toward the frontal process ofthe maxilla just inferior to the bottom of the orbital margin. Bilat-eral formations of thin new bone and porosity characterized theorbital roofs. Superior to glabella, an irregularly shaped locus fea-tured a mixture of concentrated abnormal porosity, extremely finewoven bone, and traces of vascular impressions (Fig. 3). Vascu-lar impressions were also observed on left and right nasal bones.Superior to this, three irregular, shallow, smooth-walled, and con-tiguous bony channels were observed. These were superficial anddid not affect the diploë. These channels present as impressionsof a tortuous vascular network on the surface of the frontal bone;the two largest channels may have even anastomosed (Fig. 4). Theyresemble an endocranial phenomenon called a “branched lysis” byMays (2008: Fig. 8), formed as new bone proliferates and remodelsaround capillaries. But instead of being “lysis-like” and destructive,these structures more likely represent bone formation around newor preexisting blood vessels, and therefore are best characterizedas a “vascular ramus” or as vascular impressions.

Posterior to the coronal suture, Case 1 exhibited additionallesions. A raised oval region of hypertrophic bone was present onthe left parietal bone (Fig. 5). Consistent with a hematoma in theprocess of organization, it was 4.2 cm long and 2.2 cm wide. Thesurface of this formation was extremely porous, and its margins

were ringed by shallow vascular impressions. An area of well-remodeled new bone extended from the feature across to the rightparietal bone, locally obliterating the sagittal suture. Most of thesurfaces of the left and right parietal bones were covered with 25

H.D. Klaus / International Journal of Paleopathology 5 (2014) 34–45 37

Fig. 1. The Lambayeque Valley Complex on the north coast of Peru, showing the location of key archaeological sites including Chornancap (1), Jotoro (2), and Eten (3) wherecases of subadult scurvy have been identified.

38 H.D. Klaus / International Journal of Paleopathology 5 (2014) 34–45

Tab

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Fig. 2. Abnormal porosity observed bilaterally on the ectocranial surface of thegreater wing of the sphenoid bone of Case 1 (left lateral view of the skull shownhere).

Fig. 3. Anterior view of the skull, Case 1. Areas of abnormal porosity, along withvascular impressions and patches of fine bone deposition, were observed superiorto glabella, on the left and right nasal bones, and in midfacial region.

discrete vascular branch-like lesions. Less than 2 cm wide, eachfocus was characterized by multiple shallow vascular branches thatradiated away from a central point. The posterior cranium (Fig. 5)was characterized by two large bilateral lesions of the parietalbones, superior to the midlamdoidal region. Remnants of dozensof small vascular impressions ringed their margins, and each lesionpossessed islands of elevated surfaces. No postcranial abnormali-ties were present.

4.2. Case 2: Jotoro Burial 01M1-E7 (16–21 months old)

The cranial vault in Case 2 was fragmentary, but at least onegreater wing of the sphenoid bone exhibited abnormal porosity.Similar lesions were present on the left and right orbital plates,but both surfaces also presented extensive plaque-like deposits of

H.D. Klaus / International Journal of Paleopathology 5 (2014) 34–45 39

Fig. 4. Vascular impressions on the ectocranial surface of the frontal bone of Case 1.These appear to be bony impressions of abnormal and tortuous vascular networks,the two largest of appear to have anastomosed.

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ig. 5. Case 1 also included a unilateral raised region of hypertrophic bone onhe superior aspect of the left parietal bone. Its margins were ringed by multipleadiating vascular impressions.

ew bone (Fig. 6a). While both orbits were affected, the degree oforosity was asymmetrical and affected the left orbit in a more pro-ounced fashion than the right. Extensive and widespread depositsf new bone covered much of this child’s left and right anterioraxillae, particularly at the attachment sites of the Quadratus labii

uperioris, Caninus, Transverse nasalis, and Incisive muscles (Fig. 6b).he left and right posterior maxillae featured very porous newone and bilateral blood vessel tracking within new bone depositsFig. 6c). The right ascending ramus of the mandible showed evi-ence of minor inflammation in areas associated with the insertionf the Temporalis muscle, but this was not bilateral. Mild abnormalorosity was also noted at the mental eminence of the mandibleear the origins of the Mentalis and Orbicularis oris muscles. Noostcranial abnormalities were present.

.3. Case 3: CNS Burial U2-36 (4.5–5.5 years old)

In Case 3, abnormal porosity was observed on the right tem-oral bone at the posterior root of the zygomatic arch along and

nferior to the attachment of the Temporalis m. Porosity of therbital roofs was noted, associated with irregular areas of well-

rganized, smooth compact bone overlying the cortex, consistentith a well-organized hematoma (Fig. 7A). Both left and rightosterior maxillae exhibit abnormal porosity and superficial ves-el tracking. The superior and lateral aspects of the frontal bone’s

Fig. 6. In Case 2, abnormal porosity and new bone formation was present on theleft and right orbital plates (A) and the left and right anterior (B) and posterior (C)maxillae.

ectocranial surface was covered with remnants of multiple vas-cular ramus-like blood vessel impressions (Fig. 7B) and includedone prominent channel system extending into a raised region ofwell-healed porosity. Both parietal bosses were characterized byroughly circular, elevated, and bilateral porotic loci ringed by tor-tuous vascular impressions (Fig. 7C). These loci are in line with themorphology and location of Parrott’s swellings (Brickley and Ives,2008). No postcranial abnormalities were observed.

4.4. Case 4: CNS Burial U4AE-2 (16–21 months old)

In Case 4, abnormal porosity and hypertrophic new bone forma-tion was observed in the eye orbits, posterior maxillae, and bothgreater wings of the sphenoid bone (Fig. 8). Patches of fine newbone formation were also observed on the endocranial surfaces ofthe fontal bone. Upper limb bones were also affected (Fig. 9). Theposterior diaphysis of the right humerus was covered in a very fine

but irregular distribution of woven bone. Anteriorly, the superiorhumeral metaphysis was characterized by ragged surfaces. Sim-ilar features were present on the metaphyses of both ulnae andradii, qualitatively resembling a “slit/strut” morphology (Ortner

40 H.D. Klaus / International Journal of Paleopathology 5 (2014) 34–45

Fig. 7. The cranium of Case 3 was characterized by: (A) abnormal porosity and well-organized new bone on the orbital roofs; (B) complex blood vessel impressionson the frontal bone, and (C) elevated and bilateral porotic loci ringed by tortuousvascular impressions on the left and right parietal bosses.

Fig. 8. Multiple sites of the cranium in Case 4 exhibited abnormal porosity and boneformation, including the superior eye orbits.

Fig. 9. Abnormalities of upper limb bones were affected in Case 4, and includedbone formation on the posterior diaphysis and a porous olecranon fossa of the

right humerus. Metaphyses and diaphyses of left and right radii and ulnae alsodemonstrated atypical porosity and new bone formation.

and Mays, 1998). The surface of the right olecranon fossa wasnotably porous. This may be explained as a vascular response tothe presence of hemarthrosis. On the radii, pathological new bonewas present in the regions overlaid by the Flexor pollicis longus andPronator quadratus muscles. Also, the distal radial epiphyses werecupped. On the ulnae, abnormal bone formation was present inregions involved with the Abductor pollicis longus origin and theBrachialis insertion.

4.5. Case 5: CNS Burial U3-91 (1–1.5 years old)

Case 5 presented abnormal porosity on sphenoid bone frag-ments, posterior maxillae, and on both superior orbital plates.Cranial vault fragments displayed fine porosity. In this example,inflammatory response and new bone formation was present on theendocranial surfaces of the frontal, temporal and occipital bones.The frontal bone lesions featured very fine vascular impressions or“capillary lesions” (Lewis, 2004) involving new bone organizationand formed around vasculature (Fig. 10).

On the postcranial remains of Case 5, porosity and new bonewas observed on the floor of the supraspinous fossa of the rightscapula (Fig. 11A). The diaphysis of the right ulna possessed areasof fine and coarse porosity in a shell-like layer of pathological bonethat abnormally thickened most of the shaft (Fig. 11B). This wasmost pronounced around the areas overlain by the Abductor pollicislongus, Extensor pollicis longus, and Extensor indicis muscles.

Both femora and tibiae exhibited pronounced bilateral diaphy-

seal thickening due to massive pathological new bone deposition(Figs. 12 and 13A). The margins demarcating fiber bone forma-tion from normal cortical surfaces were very sharply defined interms of texture and coloration, and the anterior tibial crests were

H.D. Klaus / International Journal of Paleopathology 5 (2014) 34–45 41

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5

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ig. 10. The endocranial surfaces of the frontal bone in Case 5 were marked by newone formation associated with an inflammatory response.

rregular and undulating in some areas. Further, the margins ofhe femora and tibiae possessed very fine (literally, razor-thin) butlearly definable leading edges of newly calcified bone overhangingealthy cortical surfaces (Fig. 13B). Periosteal bone formation mar-ins were well-defined on the anterior femoral diaphyses and wererecisely located along the origin of the Vastus lateralis muscle.

. Discussion

.1. Differential diagnosis

The observations above illustrate a mosaic of multiple cranialnd postcranial lesions (Table 2). Several conditions, includingnfectious processes, various kinds of chronic anemias, bone-orming disorders, and metabolic disease can resemble the bony

hanges observed here. Potential differential diagnoses includehronic non-specified (or non-specific) infection, treponemal dis-ase, chronic anemia, hypertrophic (pulmonary) osteoarthropathy,nfantile cortical hyperostosis (Caffey’s disease), inflammatory

ig. 11. Abnormal porosity and new bone formation affected the floor of theupraspinous process of the right scapula (A) in Case 5, in addition to areas ofne and coarse porosity associated with a shell-like layer of pathological bone thatbnormally thickened most of the diaphysis of the right ulna (B).

Fig. 12. Anterior view of the left and right femora and tibiae of Case 5, demonstratingabnormal new bone formation and significant diaphyseal thickening of the tibiae.

Fig. 13. Detail views of regions of new bone formation on the tibiae of Case 5.Extremely fine deposits of new bone (A) suggest an active condition at the timeof death, and in some areas, the leading edge of bone formation possessed very fine(literally, razor-thin) but clearly definable margins of newly mineralized bone (B,arrow) overhanging healthy cortical surfaces.

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eningitis, rickets, and scurvy. Further elaboration of these differ-ntial diagnoses is supplied in the online Supplementary Materialshat accompany this article.

Some cranial lesions, such as the anterior and posterior max-llae of Cases 1, 3, 4, and 5, and postcranial lesions in Cases 4nd 5, could reflect the presence of chronic infectious processes.hronic infectious processes producing periosteal inflammationnd pathological new bone formation (Larsen, 1997; Ortner, 2003)ay produce plaque-like, sclerotic, and elevated bone deposits.nder such conditions, new bone can form on any osseous sur-

ace but commonly predilects tibial diaphyses bilaterally, such asase 5. Such responses due to infection are often more superficial,atchy, and localized, not producing circumferential modificationf affected bone. Non-specified infection is also a poor explanationor new bone formation observed on various anterior and poste-ior maxillae or long bones in Cases 4 and 5, especially since theseesions are closely associated with muscle attachments and actions.

differential diagnosis of congenital or acquired treponemal dis-ase in Cases 4 and 5 can be rejected due to the lack of focusedone apposition on the anterior tibiae (i.e., the “sabre-shin” defor-ity absence of caries sicca, and the absence of associated dental

tigmata.Chronic anemias produced by hemoglobinopathies, hemolyises,

r vitamin deficiencies can produce porotic lesions of the cra-ial vault via hypertrophy of the diploë and may closely resemblecurvy. However, with every vault lesion reported here in Cases–5, it is possible to rule out marrow hypertrophy fairly easily.arrow hypertrophy and enlargement of the diploë occurs at the

xpense of the outer table; in these crania, porosity penetrates anntact outer table. Also, the greater wing of the sphenoid bone isnlikely to become porous under anemic conditions because it con-ains minimal marrow space. The oval osseous prominence in Case

and the formation of bone atop the anatomical surface of eyerbits in Cases 3 and 4 are defects that overlay the external lam-na, consistent with an organized hematoma. They do not representnlarged marrow spaces.

Specific bone-forming disorders may also resemble scorbutichanges. Hypertrophic (pulmonary) osteoarthropathy (or HO; alsonown as Marie-Bamberger Syndrome) is a condition potentiallyesponsible for new postcranial bone formation in Cases 4 and 5. Aeurocirculatory mechanism associated with forms of pulmonary

nflammation and cancers likely stimulates osteoblasts to pro-uce pathological bone (Aufderheide and Rodríguez-Martin, 1998;esnik, 2002; Ortner, 2003). However, the onset of this syndromeypically occurs during adolescence or yet later in life. Childrenre rarely affected by the disorder. Cases 4 and 5 also lack thexpected dense “candle wax” formation on long bone diaphysis andigital clubbing of hands and feet often associated with HO. Hyper-rophic osteoarthropathy cannot account for the cranial lesionsince it typically spares the skull, and only may affect the inner tableAufderheide and Rodríguez-Martin, 1998, 91). HO spares musclettachment sites (Ortner, 2003, 354), in contrast to locations ofostcranial new bone formation seen in Cases 4 and 5.

Infantile cortical hyperostosis, or Caffey’s disease, could fitany lesion descriptions here, as it involves long bone and cra-

ial periosteal inflammation and cortical thickening (Caffey, 1946;erring, 2007). Demographically, infantile cortical hyperostosis

s unlikely in all cases since it actively manifests in childrenostly between 0 and 6 months of age. The lesions further do

ot match those associated with the persistent disease variant inlder children (Resnick, 2002). Infantile cortical hyperostosis dis-ase also tends to produce asymmetrical and unilateral lesions of

he mandible, ribs, and metatarsals, none of which were present.

Endocranial lesions seen in Cases 4 and 5 could be a productf inflammatory meningitis that involves intracranial hemorrhageNelson, 2006). Meningitis can form lesions through a similar

aleopathology 5 (2014) 34–45

pathophysiological process and produce identical lesion morphol-ogy to those observed in Cases 4 and 5. While the presence ofmultiple additional cranial and postcranial features all point toscurvy in these two skeletons, comorbidity with inflammatorymeningitis cannot be ruled out without a histological diagnosis(e.g., Schultz, 2001; Walper et al., 2004).

Metabolic disorders, such as rickets, may produce near-identicallesions to scurvy, but subtle distinguishing characteristics can helpdiscriminate between vitamin C and vitamin D deficiency (Ortnerand Mays, 1998; Ortner, 2003; Brickley and Ives, 2008). Rachiticcranial lesions tend toward ultra-fine deposits of porous periostealbone, and are often far finer than those recorded in Cases 1 thru5. In all but Case 4, there is an absence of abnormal curvature oflong bones or other elements associated with weight bearing onbones possessing inadequate mechanical strength. Other patho-logical morphologies associated with rickets, including thickenedrib diaphysis, rib flattening at the costochondral junction (“rachiticrosary”), and pelvic deformation was absent.

Scurvy represents the remaining differential diagnosis. Thespecific constellations of lesions appear most consistent with adiagnosis of scurvy in each case, including abnormal porosity of thegreater wing of the sphenoid bone in Cases 1, 2, 4, and 5 (lesionsconsidered by the Ortner criteria to be virtually pathognomonicfor scurvy), additional cranial and maxillary sites, and new boneformation associated with the location and movement of variousmuscles associated with mastication and movement of limbs. Noother known pathological condition of the skeleton is known to pro-duce similar bony changes. Though the greater wing of the sphenoidbone was not affected in Case 3, the combination of other lesionsin this child’s remains is most consistent with mechanisms involv-ing pathological inflammation and subsequent new bone formationassociated with scorbutic hemorrhage.

However, in Case 4, co-morbidity between scurvy and ricketsshould be considered. In addition to the apparent scorbutic lesions,there was minor yet perceptible deflection of the distal radius andmedial bowing of the ulnae and radial epiphyseal cupping. Fora child of this age, it may reflect weight bearing on the upperlimbs associated with the locomotion of pushing up and crawl-ing before walking commenced. Further, the morphology of theaffected upper limb long bone metaphyses in Case 4 bear strongqualitative resemblance to the “slit/strut” morphology associatedwith the metaphyseal ends of rachitic long bones (Ortner and Mays,1998, Fig. 4). These formations represent parallel zones of alter-natingly mineralized and unmineralized osteoid. These featuresmaximize biomechanical strength under adverse metabolic condi-tions. The struts provide greater resistance to bending and providea basis for rapid and full mineralization once vitamin D becomesavailable again (Ortner and Mays, 1998, 53).

5.2. Scurvy in Lambayeque: first assessment and questions forfuture research

Both research hypotheses are rejected. The current data indicatescurvy in Lambayeque was a rare disease condition, and preva-lence did not evidently increase during the postcontact era. Anoverall crude prevalence rate is currently calculated as 0.79% (or5/641 subadults) for the combined late pre-Hispanic and Colo-nial eras. This stands in clear contrast to a crude prevalence rateof 10.5% in the NMNH collection drawn from the Peruvian cen-tral coast and highlands (Ortner et al., 1999). Hrdlicka’s early 20thcentury preferential bias for collecting pathological remains fromthe surfaces of looted cemeteries quite likely skewed this fig-

ure upwards in the NMNH collection. In contrast, the very lowprevalence reported here is calculated from samples that weregenerated mostly through attempts at regional representativesampling strategies (and see below).

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The ectocranial vascular impressions in Cases 1 and 3 are of note.anging in morphology from complex vascular networks to dis-rete, star-shaped radiating channels, their formation appears tonvolve deposition and remodeling of bone around extant or newlyroliferating vasculature. This type of lesion is rarely reported inhe subadult scurvy literature (see Brown and Ortner (2011, Fig.) for another example). They appear fully consistent with theehavior of blood vessels and new bone formation in responseo inflammation. Hemarthrosis (such as that possibly documentedn the right elbow joint of Case 4) is emphasized in clinical lit-rature but virtually never noted in subadult paleopathologicalases. Slit/strut metaphyseal organization is also an importantarker for rickets, but development of qualitative and quantita-

ive standards for its documentation and formal comparison toetaphyseal alterations produced by scurvy is an important future

ask.Archaeologically, these results indicate that during the late pre-

ispanic era, most subadults consumed sufficient dietary vitamin to prevent manifestations of scurvy – despite variation in socialtatus, ethnic group membership, or differential diets betweenlites and non-elites (Klaus and Alvarez-Calderón, 2013). Paleob-tanical data (Klaus, 2008, 99–101) indicate various dietary staplesuch as squash, lúcuma, avocado, guava, and gaunábana containedoderate to high vitamin C content. Our macro- and microb-

tantical study of midden contents of Colonial Eten reveal anbundance of these foods later in time, and also include remainsf imported oranges (Citrus sp.). Despite a mosaic of negative bio-ultural changes in the Colonial era, consumption of long-standingtaples, and at least one introduced food, seems to have offeredufficient ascorbic acid intake for the vast majority of people.

These first documented cases of scurvy in Lambayeque rep-esent a starting point for the study of vitamin C deficiency onhe north coast of Peru, but there are currently more questionshan answers. First, the notion of such glaring differences in cruderevalence between the NMNH remains and these archaeolog-

cal skeletons needs to be further explored. While it is almostertain that sampling bias surrounded Hrdlicka’s collection ofooted remains, a regional understanding of patterning and vari-tion of Andean scurvy has yet to emerge. Could there be trulytark differences in scurvy prevalence between the north andentral coast/highland regions of Peru? Were there differencesetween individual coastal valleys? Did unique characteristics ofambayeque ecogeography (see online Supplemental Materials)uffer against larger percentages of children being affected bycurvy?

Second, what is the temporal and contextual patterning ofcurvy on the north coast of Peru? How does scurvy relate to theevelopment of increasingly complex subsistence economies anddaptive transitions over time? Do the episodic environmental dis-uptions of El Nino events impact prevalence patterns? If thereeems to be widespread dietary sufficiency of vitamin C, was scurvyhen decoupled from the development of increasing social stratifi-ation and differential access to resources and other documentedncreases in skeletal stress markers?

Third, what relationships might exist between scurvy and otheraleopathological reflections of nutritional stress and stable iso-ope evidence of diet? How common was co-morbidity betweencurvy, rickets, and other conditions on the north coast of Peru?t this equatorial latitude, sufficient synthesis of vitamin D fromutaneous exposure to sunlight is easy to accomplish. Rickets wasrobably exceedingly rare, and Case 4 represents the first possiblealeopathological example of rickets from this region of the world

o be identified. Did cultural practices such as infant swaddling orradle boarding contribute to the development of rickets, or didt reflect rare inborn errors of metabolism (e.g., Brickley and Ives,008, Table 5.4)?

aleopathology 5 (2014) 34–45 43

6. Conclusion

This study establishes the presence of scurvy in this region of theSouth American Andes. However, scurvy appears as a rare diseasecondition on the north coast of Peru. This work has underscoredcareful description and differential diagnosis between multiple dis-crete sites in both the cranial and postcranial skeleton, the potentialco-morbidity between scurvy and rickets, and that ectocranial vas-cular impressions are consistent with scurvy. Also, it is argued thatidentification of subadult hemarthoses deserves greater focus. Thefuture of research into the history, distribution, and significance ofscurvy on the north coast of Peru is promising, as this disease rep-resents an increasingly important component of paleopathologicalreconstructions of Andean dietary adaptation, nutrition, and health.

Acknowledgements

Grants from the National Science Foundation (Grant BCS1026169), the Wenner-Gren Foundation for AnthropologicalResearch (Grants 7302, 8009, 8132) and Utah Valley University’sCollege of Humanities and Social Sciences, The Center for EngagedLearning, SCOP program, Presidential Scholar Award, Departmentof Behavioral Science, and the International Center funded thiswork from 2004 to 2012. I thank Peruvian project co-directorRosabella Alvarez-Calderón (Harvard University) and all the con-tributors of the Lambayeque Valley Biohistory Project from Peru,Japan, Canada, and the United States. Special thanks are owedto Brian Birch, Steven Clark, Carlos Elera, Marco Fernández, JuanMartínez, Raul Saavedra, Fausto Saldana, Carlos Wester, and DavidYells for their many contributions supporting this work. ScottApplegate, Jenna Hurtubise, Marisa McKane, and Becky Ann Tal-pas worked out details of lesion patterning in the lab, while JudithArnett provided initial observations of lesions in CNS U4AE-2during excavation. Figures 6–13 by Sam Scholes. I am gratefulto the editor, associate editor, Simon Mays, John Crandall, ClarkLarsen, Kate Teel, and the anonymous reviewers for their thoughtfuland constructive comments and corrections. Any remaining short-comings are my own.

Most of all, I owe a debt of deepest gratitude to Don Ortnerfor energizing my interest in scurvy (and for all the pathologicalconditions of the human skeleton). This work is dedicated to hismemory.

Appendix A. Supplementary data

Supplementary data associated with this article can be found, inthe online version, at doi:10.1016/j.ijpp.2013.09.002.

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Further reading

Alva, W., Donnan, C.B., 1993. Royal Tombs of Sipán. Fowler Museum of CulturalHistory. University of California, Los Angeles.

Alva Meneses, I., 2008. Los complejos de Cerro Ventarrón y Collud-Zarpán: del Pre-cerámico al Formativo en el valle de Lambayeque. In: Kaulike, P., Onuki, Y. (Eds.),Boletín de Arqueología PUCP No 12. El periodo Formativo: enfoques y eviden-cias recientes. Cinquenta anos de la Misión Arqueológica Japones y su vigencia.Primera parte. Fondo Editorial Pontifica. Universidad Católica del Peru, Lima, pp.97–117.

Barlow, T., 1883. On cases described as “acute rickets” which are probably a combi-nation of scurvy and rickets, the scurvy being an essential, and the rickets as avariable, element. Med. Chururgical Trans. 66, 159–219.

Brüning, E., 1922 [1989]. Estudios Monográphicas del Departmento de Lamabyeque.Fasciculo 1: Lambayeque, compiled by Vreeland, J. M. Sociedad de Investigacíonde la Ciencia, Cultura, y Atre Norteno, Chiclayo.

Cabello Balboa, M., 1586 [1951]. Miscelánea Antártica: Una Historia del PeruAntiguo. Instituto de Ethnología. Universidad Nacional Mayor de San Marcos,Lima.

Dillehay, T.D. (Ed.), 2011. From Foraging to Farming in the Andes: New Perspec-

tives on Food Production and Social Organization. Cambridge University Press,Cambridge, UK.

Donnan, C.B., 1989. En busca de Naylamp: Chotuna Chornancap y el valle de Lam-bayeque. In: Antonio de Lavalle, J. (Ed.), Lambayeque. Coleccion Arte y Tesorosdel Peru. Banco del Credito, Lima, pp. p.105–p.136.

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