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International Journal of Paleopathology 5 (2014) 3445

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International Journal of Paleopathology


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

Research Article

Subadult scurvy in Andean South America: Evidence of vitamin C


deciency in the late pre-Hispanic and Colonial Lambayeque Valley,
Peru
Haagen D. Klaus a,b,c,
a

Department of Sociology and Anthropology, George Mason University, United States


Museo Nacional Sicn, Peru
c
Museo Nacional de Arqueologa y Etnografa Hans Heinrich Brning de Lambayeque, Peru
b

a r t i c l e

i n f o

Article history:
Received 3 September 2012
Received in revised form 5 September 2013
Accepted 5 September 2013
Keywords:
Vitamin C deciency
Rickets
Differential diagnosis
Eten

a b s t r a c t
Scurvy is a disease caused by vitamin C deciency and is a key paleopathological indicator of subadult
health and nutritional status in the past. Yet, little is known about scurvy in human remains from South
America and the Peruvian Central Andes in particular. In the Lambayeque Valley Complex on the north
coast of Peru, a sample of 641 archaeologically recovered subadults (A.D. 9001750) were scored for the
skeletal manifestations of vitamin C deciency, testing the hypotheses that scurvy was common in this
region and that prevalence increased following European contact. The ndings reveal only ve convincing cases of scurvy; overall prevalence appears extremely low, and scurvy did not become perceptibly
more common following conquest. Of diagnostic interest, complex ectocranial vascular impressions were
documented in two cases. Though rarely attributed to scurvy, examination suggests they formed during
scorbutic episodes. Another Colonial Period subadult may demonstrate comorbidity between scurvy and
rickets. This work also provides new questions for the investigation of scurvy in Andean South America.
2013 Published by Elsevier Inc.

1. Introduction
Scurvy is a metabolic disorder produced by chronic inadequate
intake of vitamin C. As one of the central goals of paleopathology
and bioarchaeology is to reconstruct health and nutrition in the
past, scurvy ranks as a key variable in the assessment of nutritional stress and dietary adequacy in human populations. While
scurvy has long been underreported in the paleopathological literature, it has received increasing perception, focus, and diagnostic
rigor, particularly over the last decade. This visibility is largely
due to the development of Donald Ortners diagnostic criteria of
scurvy in the skull (Ortner and Eriksen, 1997; Ortner et al., 1999,
2001) and postcranial skeleton (Ortner, 2003). Subsequent studies
have shed new light on dietary insufciency, subsistence economy, humanecology synergisms, urbanism, and socioeconomic
inequality (e.g., Melikian and Waldron, 2003; Lewis, 2004; Brickley
and Ives, 2006, 2008; Mays, 2008; Waldron, 2009; Lewis, 2010;
van der Merwe et al., 2010a,b; Brown and Ortner, 2011; Geber and
Murphy, 2012).

Correspondence to: Department of Sociology and Anthropology, Robinson Hall


B, Room 305, George Mason University, MSN 3G5 Fairfax, VA 22030-4444, United
States. Tel.: +1 703 993 1440; fax: +1 703 993 1446.
E-mail address: hklaus@gmu.edu
1879-9817/$ see front matter 2013 Published by Elsevier Inc.
http://dx.doi.org/10.1016/j.ijpp.2013.09.002

While the skeletal evidence for scurvy spans thousands of years


and almost the entire world, Brickley and Ives, 2008, Table A1), only
one study has emerged from Andean South America. Ortner and
colleagues (1999) examined 363 subadult crania from Peru curated
at the Smithsonian Institutions National Museum of Natural History (NMNH). This work found probable cases in just over 10.5%
of the examined crania to establish that scurvy was: (1) indeed
present in the ancient coastal and highland Andes, and; (2) was
evidently a common disease condition in pre-Hispanic Peru. However, most of these human remains were selectively collected from
the devastated landscapes of looted cemeteries along Perus central coast during the early 20th century expeditions of Hrdlicka
(1914). Key questions regarding cultural, spatial, temporal, and epidemiological variation could not be addressed as corresponding
contextual data were either destroyed by looting or lost by insufcient documentation during surface collections that focused mostly
on crania. Since no postcranial remains accompanied the NMNH
Peruvian crania, broader assessment of lesion distributions within
affected individuals was also inhibited.
Scurvy has yet to be assessed in the arid Lambayeque Valley
Complex of Perus north coast for additional contextual information regarding local Lambayeque ecology and cultural history,
see the Online Supplemental Materials.This region and its ve
rivers provided the setting for one of the independent centers
of Andean cultural development beginning around 1500 B.C. Key

H.D. Klaus / International Journal of Paleopathology 5 (2014) 3445

developments spanned Cupisnique, Moche, and Sicn cultures


that were characterized by complex socioeconomic organization,
diverse subsistence economies, and innovative technologies (Alva,
2012; Alva and Donnan, 1993; Alva Meneses, 2008; Dillehay, 2011;
Donnan, 1989; Donnan, 1990a,b, 2012; Elera, 1986; Hayashida,
2006; Heyerdahl et al., 1995; Klaus et al., 2013a,b; Shimada, 1990,
1995, 2013; Shimada, 1994, 1999, 2000; Shimada et al., 2013;
Tschauner, 2001; Wester, 2012). Following European conquest
in the 16th century, the region became central to the Colonial
viceroyalty. Emerging bioarchaeological reconstructions of late
pre-Hispanic and Colonial Lambayeque have revealed multifaceted
spatial and temporal patterns of health variation and a range of
pathological conditions endured by local communities (Farnum,
2002; Klaus, 2012; Klaus and Tam, 2009, 2010; Klaus et al., 2009,
2010; Shimada et al., 2004; Toyne, 2011a,b). Increasing focus has
been placed on reconstructing metabolic stress (Farnum, 2002;
Klaus and Tam, 2009), but scurvy has remained unreported.
In this report, two basic hypotheses are addressed. Using a sample of archaeologically documented remains, it is rst hypothesized
that as with the earlier work of Ortner et al. (1999) on remains
from Perus central coast, scurvy was equally common in the north
and will reect evidence of a comparable prevalence. Second, it is
hypothesized that scurvy became more common during the postcontact Colonial period when biological stress broadly increased
(Klaus and Tam, 2009).

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

Criteria

Cranial vault

Abnormal regions of porosity <1 mm in


diameter penetrating cortical bone; woven
bone deposition; impressions of vascular
rami or networks
Abnormal regions of porosity <1 mm in
diameter penetrating cortical bone
Abnormal regions of porosity <1 mm in
diameter penetrating cortical bone; new
bone deposition
Abnormal regions of porosity <1 mm in
diameter penetrating cortical bone
Abnormal regions of porosity <1 mm in
diameter penetrating cortical bone; new
bone deposition
Abnormal regions of porosity <1 mm in
diameter penetrating cortical bone; woven
bone deposition
New bone deposition
New bone deposition
New bone deposition

Greater wing of the


sphenoid bone
Orbital plate

Temporal bone
Zygomatic bone, internal
and external surfaces
Anterior maxilla

Infraorbital foramen
Hard palate
Coronoid process of the
mandible, medial surface
Long bone diaphyses
Long bone metaphyses
Supra- and infraspinous
fossa of the scapula
Ribs

2. Pathogenesis and lesion characteristics


Humans and other great apes share a mutation of the gene
that produces l-gluno--lactone oxidase, and we fail to produce
this nal enzyme crucial to the synthesis of ascorbic acid, or vitamin C (Nishikimi and Udenfriend, 1976, 1977; Stuart-Macadam,
1989; Brown and Ortner, 2011; Weinstein et al., 2001). Obtaining at least 10 mg/day of dietary vitamin C is required. Vitamin C
accomplishes hydroxylation of proline and lysine into hydroxyproline and hydroxylysine, which are necessary to form collagen bril
polypeptide precursors (Hodges, 1980). Insufcient dietary intake
of vitamin C leads to defective Type 1 collagen formation, which in
turn promotes production of defective osteoid, fragile blood vessels
prone to rupture, and periosteal membranes with a propensity to
tear. Depressed immune function, compromised blood formation,
and suboptimal metabolism of iron and folate are additional corollaries (Tamura et al., 2000; Weinstein et al., 2001; Akikusa et al.,
2003; Lewis, 2007).
Hemorrhage is a hallmark of scurvy. Outside the circulatory system, the body treats blood as an inammatory agent targeted for
removal. The inammatory reaction in response to hemorrhage
in subadults can affect both the cranial and postcranial skeleton.
The vascular response in the cranium may stimulate an incursion of osteoclasts into existing cortical bone that creates channels
for newly formed capillaries (usually less than 1 mm in diameter
[Ortner et al., 1999; Kozlowski and Witas, 2012]), thus providing pathways for white cells to remove extravasated blood. Yet,
such new vessels are themselves likely to be structurally compromised and decient in collagen, thus exacerbating hemorrhage and
inammation in a feedback loop (Brown and Ortner, 2011, 198).
Should hemorrhage elevate the periosteum, new, hypertrophic
bone will form hematomas; osteoblasts migrate via chemotaxis to
hematomas, which then begin to organize into connective tissue
(Ragsdale and Lehmer, 2012).
Common skeletal sites manifesting subadult scurvy include the
superior eye orbits, ecto- and endocranial regions of the cranial
vault, alveolar bone, the hard palate, and the posterior maxilla
and mandible (Table 1). Ortner and colleagues (1999, 2001) argue
abnormal bilateral porosity of the greater wing of the sphenoid

35

New bone deposition


Metaphysial fractures, cortical thinning,
deposition of new bone
Abnormal regions of porosity <1 mm in
diameter penetrating cortical bone; new
bone deposition
Fractures adjacent to oestochondral
junction; aring rib ends

bone is virtually pathognomonic for scurvy, produced by chronic


bleeding of ruptured connective or vascular tissue owing to minor
trauma or normal muscular functions such as chewing (Ortner,
2012). Endocranially, scurvy can produce epidural bleeding as
arteries in the dura rupture and leak into surrounding tissue space
such that hematoma separates the dura and periosteum from the
bone and tears bridging vessels between the arachnoid and dura
layers of the meninges (Kumar et al., 2009; also Lewis, 2004).
In the infra-cranial skeleton, movement of the muscles of the
rotator cuff is implicated in the formation of porous lesions and
new bone deposition in the supra- and infraspinatus fossa of the
scapula. Osteochrondral junctions of ribs and long bone metaphyses may fracture. New bone 1 cm thick may be deposited on
affected regions of long bone diaphyses. The most massive subperiosteal hematomas are observed on the weight-bearing long bones
of the lower limb, especially in children old enough to be walking
(Ortner, 2003, 384). Sharpeys bers, which attach periosteum to
bone, are shorter and less numerous in children and have less resistance to tearing and bleeding (Caffey, 1978; Lewis, 2007). Brown
and Ortner (2011) and Geber and Murphy (2012) recently identied the ilium and the foramen rotundum of the sphenoid bone as
potential sites of scorbutic inammation.
A common view holds that scurvy manifests in bone following
reintroduction of vitamin C into the diet following an episode of
deprivation (Brickley and Ives, 2008). In essence, skeletal signs of
this disorder may represent signs of recovery, implying that lesion
formation is akin to a Cartesian switch that is ipped upon the conclusion 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 contribute
to a progressive model of skeletal lesion formation in response
to insufcient vitamin C. Pathophysiologic and cellular functional
perspectives thus seem to involve a spectrum of responses, rst
spanning a period of progressive drawdown of bioavailable vitamin
C that promotes poor collagen formation, bleeding, and inammatory response. Only small amounts of vitamin C are needed for

36

H.D. Klaus / International Journal of Paleopathology 5 (2014) 3445

osteoblasts to produce considerable amounts of new periosteal


bone (Bourne, 1942), and total exclusion of ascorbic acid from
human diets is very rare. During this window of insufciency,
osteoblasts produce osteoid, though in progressively suboptimal
quality. Should insufciency lead to total deprivation, a second
window would follow, and osteoid and collagen production would
terminate. Third, should vitamin C sufciency be subsequently
regained, progressively elevated bone formation would occur in
response to hematomas formed during the rst and second modes
of pathophysiological manifestation.
3. Materials and methods
3.1. Archeological contexts
The Lambayeque Valley Biohistory Project has documented the
skeletal remains of 1968 individuals in the Lambayeque Valley
Complex at 19 sites (Fig. 1). The samples span what appears to be
both a demographically and socially representative cross section
of the native population from approximately A.D. 9001750
(Klaus et al., 2013a,b). Because of the overlapping macroscopic
characteristics of growth-related new bone and inammatory
changes to bone, subadults less than 12 months 3 months were
removed from the sample and alveolar processes were not scored.
A total of 641 subadults (015 years of age at death) were complete and sufciently old to examine for this study. Of these, ve
candidate cases of scurvy were identied. Detailed descriptions
of the biocultural setting, archaeological contexts, and complete
osteological descriptions of these ve individuals are present in
the online Supplementary Materials that accompany this article.
Case 1 comes from the site of Chornancap in the lower Lambayeque drainage. Founded around A.D. 900, Chornancap was a
monumental secondary political center from ca. A.D. 9001375
(Wester, 2010; Klaus et al., 2011). Chornancap South Platform
(CSP) Burial 2 included the skeleton of a child 57 years of age, who
had been interred in a commoner cemetery dating to the Chim
occupation (A.D. 13751470). Case 2 was identied at Jotoro,
near the northern margin of the Lambayeque Valley Complex in
the mid-La Leche valley. Jotroro was a large, stable, and prosperous
community occupied from A.D. 900 to the Early Contact period of
the 1530s (Martnez, 2011). Burial O1M1-E7 is one of more than
50 burials documented thus far at Jotoro. This funerary context
contained the virtually complete skeleton of a child 1621 months
of age. Decorated grave goods indicate the child, again an inferred
member of the commoner population, was buried during the
terminal pre-Hispanic Inka occupation (A.D. 14701532).
Cases 35 all originate from the Colonial period town of Santa
Maria de Magdalena de Eten (or simply Eten), which was established as a forced nucleated resettlement of multiple communities
during the mid 16th century. Its ruins are under extensive seaside sand dunes at the southwest corner of the Reque drainage.
Three church ruins were excavated, including an Early/Middle
Colonial cemetery containing the remains of native Muchik people
buried under the mission church in Eten (A.D. 15331620)
(;Alvarez-Caldern and Klaus, 2013). Case 3 was Burial CNS U2-36,
a 4.55.5-year-old child, and whose nearly complete skeleton
was located in the northeast corner the nave. Case 4 was Burial
CNS U4AE-2, a relatively complete subadult, 1621 months of
age at death. This was an intrusive Late Historic burial interred
sometime after A.D. 1776. Case 5 was Burial CNS U3-91. Based on
its deep stratigraphic position, this was one of the rst burials in
Eten, probably interred during the 1530s or 1540s. The skeleton
of this 11.5-year-old child was incomplete and was disturbed by
the subsequent interrment of an adult. The mandible, vertebral
column, sacrum, right ribs, entire upper left limb, both ilia, pubic
bones, ischia, and feet were absent from the funerary context.

3.2. Lesion scoring criteria


A subadult was dened as either any individual without a third
molar in occlusion or who possessed an unfused spheno-occiptial
synchondrosis. More specic age estimations were then calculated
based on the attainment of maturity stages relating to tooth crown
and root formation, tooth eruption, epiphyseal fusion, and long
bone length (Buikstra and Ubelaker, 1994). Potential signs of scurvy
included abnormal porosity and periosteal bone deposition in the
anatomical sites listed in Table 1 and were scored as present, absent,
or unobservable and observed macroscopically under 10 magnication using a hand-held loupe. Abnormal porosity was dened
following Ortner and Eriksen (1997) and Ortner et al. (1999, 2001)
as a localized phenomenon of dense penetrating holes usually less
than 1 mm in diameter. Surface porosity and new periosteal bone
deposition was scored as unobservable in any cranium that lacked:
(1) a sphenoid bone with an intact cortical area consisting of less
than 50% of its total surface, and (2) at least one orbital roof consisting of less than 50% of its total surface. Long bones were evaluated
for the presence or absence of abnormal periosteal or pathological
bone deposition along both diaphyses and metaphyses, which were
scored as unobservable if less than 50% of a diaphysis or metaphysis
could be observed.
4. Results
A visual summary of the results is presented in Table 2, while
detailed descriptions and additional images of the lesions are
supplied in online Supplementary Materials that accompany this
article.
4.1. Case 1: Chornancap South Platform Burial 2 (57 years old)
Case 1 exhibited a series of lesions that affected the cranium.
Abnormal porosity was observed bilaterally on the ectocranial surface of the greater wing of the sphenoid bone (Fig. 2). Porosity
extended posteriorly to the temporal bone and the inferiolateral
portions of the frontal bone. Fine bone deposits ringed both infraorbital foramen extending superiorly toward the frontal process of
the maxilla just inferior to the bottom of the orbital margin. Bilateral formations of thin new bone and porosity characterized the
orbital roofs. Superior to glabella, an irregularly shaped locus featured a mixture of concentrated abnormal porosity, extremely ne
woven bone, and traces of vascular impressions (Fig. 3). Vascular impressions were also observed on left and right nasal bones.
Superior to this, three irregular, shallow, smooth-walled, and contiguous bony channels were observed. These were supercial and
did not affect the diplo. These channels present as impressions
of a tortuous vascular network on the surface of the frontal bone;
the two largest channels may have even anastomosed (Fig. 4). They
resemble an endocranial phenomenon called a branched lysis by
Mays (2008: Fig. 8), formed as new bone proliferates and remodels
around capillaries. But instead of being lysis-like and destructive,
these structures more likely represent bone formation around new
or preexisting blood vessels, and therefore are best characterized
as a vascular ramus or as vascular impressions.
Posterior to the coronal suture, Case 1 exhibited additional
lesions. A raised oval region of hypertrophic bone was present on
the left parietal bone (Fig. 5). Consistent with a hematoma in the
process of organization, it was 4.2 cm long and 2.2 cm wide. The
surface of this formation was extremely porous, and its margins
were ringed by shallow vascular impressions. An area of wellremodeled new bone extended from the feature across to the right
parietal bone, locally obliterating the sagittal suture. Most of the
surfaces of the left and right parietal bones were covered with 25

H.D. Klaus / International Journal of Paleopathology 5 (2014) 3445

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) where
cases of subadult scurvy have been identied.

Fig. 2. Abnormal porosity observed bilaterally on the ectocranial surface of the


greater wing of the sphenoid bone of Case 1 (left lateral view of the skull shown
here).

+
+

Fig. 3. Anterior view of the skull, Case 1. Areas of abnormal porosity, along with
vascular impressions and patches of ne bone deposition, were observed superior
to glabella, on the left and right nasal bones, and in midfacial region.
Key: +, present; , absent; and n/o, not observable.

+
+
+

n/o
Case 1 (57 years old)
Case 2 (1621 months old)
Case 3 (4.55.5 years old)
Case 4 (1621 months old)
Case 5 (11.5 years old)

+
+

+
+

+
+
+
+
+

n/o

+
+

n/o

n/o

Long Bone
metaphyses:
fracture,
cortical
thinning, new
bone
formation
Long bone
diaphyses:
new bone
formation
Supra- and
infraspinous
fossa of the
scapula:
abnormal
porosity, new
bone
formation
Coronoid
process of the
mandible: new
bone formation
Infraorbtial
foramen, hard
palate: new
bone formation
Anterior and
posterior
zygomatic
bone:
abnormal
porosity, new
bone
formation,
vascular
impressions
Anterior and
posterior
maxilla:
abnormal
porosity, new
bone
formation,
vascular
impressions
Temporal
bone:
abnormal
porosity
Superior eye
orbits:
abnormal
porosity, new
bone formation
Greater wing
of the
sphenoid
bone:
abnormal
porosity
Cranial vault:
abnormal
porosity, new
bone
formation,
vascular
impressions

Table 2
Distribution of pathological loci, Cases 15.

H.D. Klaus / International Journal of Paleopathology 5 (2014) 3445

Ribs: fractures
adjacent to
oestochondral
junction;
aring rib ends

38

discrete vascular branch-like lesions. Less than 2 cm wide, each


focus was characterized by multiple shallow vascular branches that
radiated away from a central point. The posterior cranium (Fig. 5)
was characterized by two large bilateral lesions of the parietal
bones, superior to the midlamdoidal region. Remnants of dozens
of small vascular impressions ringed their margins, and each lesion
possessed islands of elevated surfaces. No postcranial abnormalities were present.
4.2. Case 2: Jotoro Burial 01M1-E7 (1621 months old)
The cranial vault in Case 2 was fragmentary, but at least one
greater 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) 3445

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.

Fig. 5. Case 1 also included a unilateral raised region of hypertrophic bone on


the superior aspect of the left parietal bone. Its margins were ringed by multiple
radiating vascular impressions.

new bone (Fig. 6a). While both orbits were affected, the degree of
porosity was asymmetrical and affected the left orbit in a more pronounced fashion than the right. Extensive and widespread deposits
of new bone covered much of this childs left and right anterior
maxillae, particularly at the attachment sites of the Quadratus labii
superioris, Caninus, Transverse nasalis, and Incisive muscles (Fig. 6b).
The left and right posterior maxillae featured very porous new
bone and bilateral blood vessel tracking within new bone deposits
(Fig. 6c). The right ascending ramus of the mandible showed evidence of minor inammation in areas associated with the insertion
of the Temporalis muscle, but this was not bilateral. Mild abnormal
porosity was also noted at the mental eminence of the mandible
near the origins of the Mentalis and Orbicularis oris muscles. No
postcranial abnormalities were present.

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

4.3. Case 3: CNS Burial U2-36 (4.55.5 years old)

In Case 4, abnormal porosity and hypertrophic new bone formation was observed in the eye orbits, posterior maxillae, and both
greater wings of the sphenoid bone (Fig. 8). Patches of ne new
bone formation were also observed on the endocranial surfaces of
the fontal bone. Upper limb bones were also affected (Fig. 9). The
posterior diaphysis of the right humerus was covered in a very ne
but irregular distribution of woven bone. Anteriorly, the superior
humeral metaphysis was characterized by ragged surfaces. Similar features were present on the metaphyses of both ulnae and
radii, qualitatively resembling a slit/strut morphology (Ortner

In Case 3, abnormal porosity was observed on the right temporal bone at the posterior root of the zygomatic arch along and
inferior to the attachment of the Temporalis m. Porosity of the
orbital roofs was noted, associated with irregular areas of wellorganized, smooth compact bone overlying the cortex, consistent
with a well-organized hematoma (Fig. 7A). Both left and right
posterior maxillae exhibit abnormal porosity and supercial vessel tracking. The superior and lateral aspects of the frontal bones

ectocranial surface was covered with remnants of multiple vascular ramus-like blood vessel impressions (Fig. 7B) and included
one prominent channel system extending into a raised region of
well-healed porosity. Both parietal bosses were characterized by
roughly circular, elevated, and bilateral porotic loci ringed by tortuous vascular impressions (Fig. 7C). These loci are in line with the
morphology and location of Parrotts swellings (Brickley and Ives,
2008). No postcranial abnormalities were observed.
4.4. Case 4: CNS Burial U4AE-2 (1621 months old)

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H.D. Klaus / International Journal of Paleopathology 5 (2014) 3445

Fig. 9. Abnormalities of upper limb bones were affected in Case 4, and included
bone formation on the posterior diaphysis and a porous olecranon fossa of the
right humerus. Metaphyses and diaphyses of left and right radii and ulnae also
demonstrated atypical porosity and new bone formation.

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

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

and Mays, 1998). The surface of the right olecranon fossa was
notably porous. This may be explained as a vascular response to
the presence of hemarthrosis. On the radii, pathological new bone
was present in the regions overlaid by the Flexor pollicis longus and
Pronator quadratus muscles. Also, the distal radial epiphyses were
cupped. On the ulnae, abnormal bone formation was present in
regions involved with the Abductor pollicis longus origin and the
Brachialis insertion.
4.5. Case 5: CNS Burial U3-91 (11.5 years old)
Case 5 presented abnormal porosity on sphenoid bone fragments, posterior maxillae, and on both superior orbital plates.
Cranial vault fragments displayed ne porosity. In this example,
inammatory response and new bone formation was present on the
endocranial surfaces of the frontal, temporal and occipital bones.
The frontal bone lesions featured very ne vascular impressions or
capillary lesions (Lewis, 2004) involving new bone organization
and formed around vasculature (Fig. 10).
On the postcranial remains of Case 5, porosity and new bone
was observed on the oor of the supraspinous fossa of the right
scapula (Fig. 11A). The diaphysis of the right ulna possessed areas
of ne and coarse porosity in a shell-like layer of pathological bone
that abnormally thickened most of the shaft (Fig. 11B). This was
most pronounced around the areas overlain by the Abductor pollicis
longus, Extensor pollicis longus, and Extensor indicis muscles.
Both femora and tibiae exhibited pronounced bilateral diaphyseal thickening due to massive pathological new bone deposition
(Figs. 12 and 13A). The margins demarcating ber bone formation from normal cortical surfaces were very sharply dened in
terms of texture and coloration, and the anterior tibial crests were

H.D. Klaus / International Journal of Paleopathology 5 (2014) 3445

41

Fig. 10. The endocranial surfaces of the frontal bone in Case 5 were marked by new
bone formation associated with an inammatory response.

irregular and undulating in some areas. Further, the margins of


the femora and tibiae possessed very ne (literally, razor-thin) but
clearly denable leading edges of newly calcied bone overhanging
healthy cortical surfaces (Fig. 13B). Periosteal bone formation margins were well-dened on the anterior femoral diaphyses and were
precisely located along the origin of the Vastus lateralis muscle.
5. Discussion
5.1. Differential diagnosis
The observations above illustrate a mosaic of multiple cranial
and postcranial lesions (Table 2). Several conditions, including
infectious processes, various kinds of chronic anemias, boneforming disorders, and metabolic disease can resemble the bony
changes observed here. Potential differential diagnoses include
chronic non-specied (or non-specic) infection, treponemal disease, chronic anemia, hypertrophic (pulmonary) osteoarthropathy,
infantile cortical hyperostosis (Caffeys disease), inammatory

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

Fig. 11. Abnormal porosity and new bone formation affected the oor of the
supraspinous process of the right scapula (A) in Case 5, in addition to areas of
ne and coarse porosity associated with a shell-like layer of pathological bone that
abnormally thickened most of the diaphysis of the right ulna (B).

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

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H.D. Klaus / International Journal of Paleopathology 5 (2014) 3445

meningitis, rickets, and scurvy. Further elaboration of these differential diagnoses is supplied in the online Supplementary Materials
that accompany this article.
Some cranial lesions, such as the anterior and posterior maxillae of Cases 1, 3, 4, and 5, and postcranial lesions in Cases 4
and 5, could reect the presence of chronic infectious processes.
Chronic infectious processes producing periosteal inammation
and pathological new bone formation (Larsen, 1997; Ortner, 2003)
may produce plaque-like, sclerotic, and elevated bone deposits.
Under such conditions, new bone can form on any osseous surface but commonly predilects tibial diaphyses bilaterally, such as
Case 5. Such responses due to infection are often more supercial,
patchy, and localized, not producing circumferential modication
of affected bone. Non-specied infection is also a poor explanation
for new bone formation observed on various anterior and posterior maxillae or long bones in Cases 4 and 5, especially since these
lesions are closely associated with muscle attachments and actions.
A differential diagnosis of congenital or acquired treponemal disease in Cases 4 and 5 can be rejected due to the lack of focused
bone apposition on the anterior tibiae (i.e., the sabre-shin deformity absence of caries sicca, and the absence of associated dental
stigmata.
Chronic anemias produced by hemoglobinopathies, hemolyises,
or vitamin deciencies can produce porotic lesions of the cranial vault via hypertrophy of the diplo and may closely resemble
scurvy. However, with every vault lesion reported here in Cases
15, it is possible to rule out marrow hypertrophy fairly easily.
Marrow hypertrophy and enlargement of the diplo occurs at the
expense of the outer table; in these crania, porosity penetrates an
intact outer table. Also, the greater wing of the sphenoid bone is
unlikely to become porous under anemic conditions because it contains minimal marrow space. The oval osseous prominence in Case
1 and the formation of bone atop the anatomical surface of eye
orbits in Cases 3 and 4 are defects that overlay the external lamina, consistent with an organized hematoma. They do not represent
enlarged marrow spaces.
Specic bone-forming disorders may also resemble scorbutic
changes. Hypertrophic (pulmonary) osteoarthropathy (or HO; also
known as Marie-Bamberger Syndrome) is a condition potentially
responsible for new postcranial bone formation in Cases 4 and 5. A
neurocirculatory mechanism associated with forms of pulmonary
inammation and cancers likely stimulates osteoblasts to produce pathological bone (Aufderheide and Rodrguez-Martin, 1998;
Resnik, 2002; Ortner, 2003). However, the onset of this syndrome
typically occurs during adolescence or yet later in life. Children
are rarely affected by the disorder. Cases 4 and 5 also lack the
expected dense candle wax formation on long bone diaphysis and
digital clubbing of hands and feet often associated with HO. Hypertrophic osteoarthropathy cannot account for the cranial lesions
since it typically spares the skull, and only may affect the inner table
(Aufderheide and Rodrguez-Martin, 1998, 91). HO spares muscle
attachment sites (Ortner, 2003, 354), in contrast to locations of
postcranial new bone formation seen in Cases 4 and 5.
Infantile cortical hyperostosis, or Caffeys disease, could t
many lesion descriptions here, as it involves long bone and cranial periosteal inammation and cortical thickening (Caffey, 1946;
Herring, 2007). Demographically, infantile cortical hyperostosis
is unlikely in all cases since it actively manifests in children
mostly between 0 and 6 months of age. The lesions further do
not match those associated with the persistent disease variant in
older children (Resnick, 2002). Infantile cortical hyperostosis disease also tends to produce asymmetrical and unilateral lesions of
the mandible, ribs, and metatarsals, none of which were present.
Endocranial lesions seen in Cases 4 and 5 could be a product
of inammatory meningitis that involves intracranial hemorrhage
(Nelson, 2006). Meningitis can form lesions through a similar

pathophysiological process and produce identical lesion morphology to those observed in Cases 4 and 5. While the presence of
multiple additional cranial and postcranial features all point to
scurvy in these two skeletons, comorbidity with inammatory
meningitis cannot be ruled out without a histological diagnosis
(e.g., Schultz, 2001; Walper et al., 2004).
Metabolic disorders, such as rickets, may produce near-identical
lesions to scurvy, but subtle distinguishing characteristics can help
discriminate between vitamin C and vitamin D deciency (Ortner
and Mays, 1998; Ortner, 2003; Brickley and Ives, 2008). Rachitic
cranial lesions tend toward ultra-ne deposits of porous periosteal
bone, and are often far ner than those recorded in Cases 1 thru
5. In all but Case 4, there is an absence of abnormal curvature of
long bones or other elements associated with weight bearing on
bones possessing inadequate mechanical strength. Other pathological morphologies associated with rickets, including thickened
rib diaphysis, rib attening at the costochondral junction (rachitic
rosary), and pelvic deformation was absent.
Scurvy represents the remaining differential diagnosis. The
specic constellations of lesions appear most consistent with a
diagnosis of scurvy in each case, including abnormal porosity of the
greater wing of the sphenoid bone in Cases 1, 2, 4, and 5 (lesions
considered by the Ortner criteria to be virtually pathognomonic
for scurvy), additional cranial and maxillary sites, and new bone
formation associated with the location and movement of various
muscles associated with mastication and movement of limbs. No
other known pathological condition of the skeleton is known to produce similar bony changes. Though the greater wing of the sphenoid
bone was not affected in Case 3, the combination of other lesions
in this childs remains is most consistent with mechanisms involving pathological inammation and subsequent new bone formation
associated with scorbutic hemorrhage.
However, in Case 4, co-morbidity between scurvy and rickets
should be considered. In addition to the apparent scorbutic lesions,
there was minor yet perceptible deection of the distal radius and
medial bowing of the ulnae and radial epiphyseal cupping. For
a child of this age, it may reect weight bearing on the upper
limbs associated with the locomotion of pushing up and crawling before walking commenced. Further, the morphology of the
affected upper limb long bone metaphyses in Case 4 bear strong
qualitative resemblance to the slit/strut morphology associated
with the metaphyseal ends of rachitic long bones (Ortner and Mays,
1998, Fig. 4). These formations represent parallel zones of alternatingly mineralized and unmineralized osteoid. These features
maximize biomechanical strength under adverse metabolic conditions. The struts provide greater resistance to bending and provide
a basis for rapid and full mineralization once vitamin D becomes
available again (Ortner and Mays, 1998, 53).
5.2. Scurvy in Lambayeque: rst assessment and questions for
future research
Both research hypotheses are rejected. The current data indicate
scurvy in Lambayeque was a rare disease condition, and prevalence did not evidently increase during the postcontact era. An
overall crude prevalence rate is currently calculated as 0.79% (or
5/641 subadults) for the combined late pre-Hispanic and Colonial eras. This stands in clear contrast to a crude prevalence rate
of 10.5% in the NMNH collection drawn from the Peruvian central coast and highlands (Ortner et al., 1999). Hrdlickas early 20th
century preferential bias for collecting pathological remains from
the surfaces of looted cemeteries quite likely skewed this gure upwards in the NMNH collection. In contrast, the very low
prevalence reported here is calculated from samples that were
generated mostly through attempts at regional representative
sampling strategies (and see below).

H.D. Klaus / International Journal of Paleopathology 5 (2014) 3445

The ectocranial vascular impressions in Cases 1 and 3 are of note.


Ranging in morphology from complex vascular networks to discrete, star-shaped radiating channels, their formation appears to
involve deposition and remodeling of bone around extant or newly
proliferating vasculature. This type of lesion is rarely reported in
the subadult scurvy literature (see Brown and Ortner (2011, Fig.
6) for another example). They appear fully consistent with the
behavior of blood vessels and new bone formation in response
to inammation. Hemarthrosis (such as that possibly documented
in the right elbow joint of Case 4) is emphasized in clinical literature but virtually never noted in subadult paleopathological
cases. Slit/strut metaphyseal organization is also an important
marker for rickets, but development of qualitative and quantitative standards for its documentation and formal comparison to
metaphyseal alterations produced by scurvy is an important future
task.
Archaeologically, these results indicate that during the late preHispanic era, most subadults consumed sufcient dietary vitamin
C to prevent manifestations of scurvy despite variation in social
status, ethnic group membership, or differential diets between
elites and non-elites (Klaus and Alvarez-Caldern, 2013). Paleobotanical data (Klaus, 2008, 99101) indicate various dietary staples
such as squash, lcuma, avocado, guava, and gaunbana contained
moderate to high vitamin C content. Our macro- and microbotantical study of midden contents of Colonial Eten reveal an
abundance of these foods later in time, and also include remains
of imported oranges (Citrus sp.). Despite a mosaic of negative biocultural changes in the Colonial era, consumption of long-standing
staples, and at least one introduced food, seems to have offered
sufcient ascorbic acid intake for the vast majority of people.
These rst documented cases of scurvy in Lambayeque represent a starting point for the study of vitamin C deciency on
the north coast of Peru, but there are currently more questions
than answers. First, the notion of such glaring differences in crude
prevalence between the NMNH remains and these archaeological skeletons needs to be further explored. While it is almost
certain that sampling bias surrounded Hrdlickas collection of
looted remains, a regional understanding of patterning and variation of Andean scurvy has yet to emerge. Could there be truly
stark differences in scurvy prevalence between the north and
central coast/highland regions of Peru? Were there differences
between individual coastal valleys? Did unique characteristics of
Lambayeque ecogeography (see online Supplemental Materials)
buffer against larger percentages of children being affected by
scurvy?
Second, what is the temporal and contextual patterning of
scurvy on the north coast of Peru? How does scurvy relate to the
development of increasingly complex subsistence economies and
adaptive transitions over time? Do the episodic environmental dis events impact prevalence patterns? If there
ruptions of El Nino
seems to be widespread dietary sufciency of vitamin C, was scurvy
then decoupled from the development of increasing social stratication and differential access to resources and other documented
increases in skeletal stress markers?
Third, what relationships might exist between scurvy and other
paleopathological reections of nutritional stress and stable isotope evidence of diet? How common was co-morbidity between
scurvy, rickets, and other conditions on the north coast of Peru?
At this equatorial latitude, sufcient synthesis of vitamin D from
cutaneous exposure to sunlight is easy to accomplish. Rickets was
probably exceedingly rare, and Case 4 represents the rst possible
paleopathological example of rickets from this region of the world
to be identied. Did cultural practices such as infant swaddling or
cradle boarding contribute to the development of rickets, or did
it reect rare inborn errors of metabolism (e.g., Brickley and Ives,
2008, Table 5.4)?

43

6. Conclusion
This study establishes the presence of scurvy in this region of the
South American Andes. However, scurvy appears as a rare disease
condition on the north coast of Peru. This work has underscored
careful description and differential diagnosis between multiple discrete sites in both the cranial and postcranial skeleton, the potential
co-morbidity between scurvy and rickets, and that ectocranial vascular impressions are consistent with scurvy. Also, it is argued that
identication of subadult hemarthoses deserves greater focus. The
future of research into the history, distribution, and signicance of
scurvy on the north coast of Peru is promising, as this disease represents an increasingly important component of paleopathological
reconstructions of Andean dietary adaptation, nutrition, and health.
Acknowledgements
Grants from the National Science Foundation (Grant BCS
1026169), the Wenner-Gren Foundation for Anthropological
Research (Grants 7302, 8009, 8132) and Utah Valley Universitys
College of Humanities and Social Sciences, The Center for Engaged
Learning, SCOP program, Presidential Scholar Award, Department
of Behavioral Science, and the International Center funded this
work from 2004 to 2012. I thank Peruvian project co-director
Rosabella Alvarez-Caldern (Harvard University) and all the contributors of the Lambayeque Valley Biohistory Project from Peru,
Japan, Canada, and the United States. Special thanks are owed
to Brian Birch, Steven Clark, Carlos Elera, Marco Fernndez, Juan
Carlos Wester, and David
Martnez, Raul Saavedra, Fausto Saldana,
Yells for their many contributions supporting this work. Scott
Applegate, Jenna Hurtubise, Marisa McKane, and Becky Ann Talpas worked out details of lesion patterning in the lab, while Judith
Arnett provided initial observations of lesions in CNS U4AE-2
during excavation. Figures 613 by Sam Scholes. I am grateful
to the editor, associate editor, Simon Mays, John Crandall, Clark
Larsen, Kate Teel, and the anonymous reviewers for their thoughtful
and constructive comments and corrections. Any remaining shortcomings are my own.
Most of all, I owe a debt of deepest gratitude to Don Ortner
for energizing my interest in scurvy (and for all the pathological
conditions of the human skeleton). This work is dedicated to his
memory.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at doi:10.1016/j.ijpp.2013.09.002.
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