American Journal of Physical Anthropology Volume 109 Issue 2 1999 B.M. Rothschild; B. Arriaza; R.J. Woods; Olivier Du

7/25/2019 American Journal of Physical Anthropology Volume 109 Issue 2 1999 B.M. Rothschild; B. Arriaza; R.J. Woods; Olivie

1/9

Spondyloarthropathy Identified as the Etiology of NubianErosive Arthritis

B.M. RO THSC H I L D, 1* B. ARRIAZA,2 R.J . WOODS,3

AND O L I VI E R D U TO U R 41Art hri t is Center of Northeast Ohi o and Nort heastern Ohio U niversit iesColl ege of Medici ne, Youngstown, Ohi o 445122Department of Anthr opology and Et hni c Studi es, University of Nevada,Los Vegas, Nevada 89154 and U niversidad d e Tarapaca, Arica, Chil e3Department of Anthr opology, Ohio State Un iversity,Columbus, Ohi o 432104U ni versit e de l a M edit er ra nee, F acul te de M edecine de M ar seil le, 13385Marseil le, France

K E Y W O R D S erosive ar thrit is ; spondyloar thropathy; rheumat oidar thrit is ; skeleta l pat hology

A B S T R A C T Slight variat ion in manifesta t ion of different diseases maya llow a single individual w ith one disease to mimic the classica ppea ra nce ofanother, as evidenced by the frequent confusion of spondyloarthropathy withrheumat oid ar thrit is . Ana lysis of populat ion occurrence of ar thrit is (rat hertha n isolated skeletons) facilita tes more precise diagnosis.

Northeast Africans living ar ound 2,000 years before present were clearlyafflicted w ith a form of spondyloart hropat hy. Lack of inclusion of spondyloar -t h r op a t h y i n t h e d if fe re nt i a l d ia g n os is of e ros iv e a r t h r i t is l ed t o p a s tmisclassifi cat ion of Nubians as ha ving rheumat oid a rthrit is . While evidenceof spondyloarthropathy abounds in th e literature of huma n skeleta l disease,pre-Columbian Old World rheumatoid arthritis is still elusive. The currents t u dy f u rt h e r do c u me n t s t h e a bs e n c e o f rh e u ma t o id a r t h ri t is in N u bia n s ,supporting the hypothesis that rheumatoid arthritis began in the New World.Am J P hy s Ant hr opol 109:259267, 1999. 1999 Wiley-Liss, I nc.

Sp on dy loa rt h ro pa t h y de fi n e s a g rou p o f

dise a s es wit h a t e n den cy t o re a c t ive n e w

(enthesial) bone forma tion, pauciar t icular

periphera l joint involvement, an d frequent

occurrence of a xial (spine and sacroiliac)

joint disease (Bywaters, l960; Martel, l968;

McEwen et al . , l971; Ortner and Putschar,

1985; Resnick a nd Niwa yam a, l988; Roths-

child, l982; St einbock, 1975). In cluded in t he

spondyloarthropathy group are Reiters syn-

drome (often referred to as react ive arthri-

tis), psoriatic arthritis, ankylosing spondyli-

t i s , a n d t h e a r t h r o p a t h y o f i n fl a m m a t o r y

bowel disease (ulcera tive colitis a nd C rohns

disea se) (McEw en et a l., l971).

I n t h e l 950s , i t w a s s o f a s h ion a b l e t o

lump rheumatoid arthritis with spondylo-

art hropat hy, tha t t he latt er received the a ppel-

lat ion rheuma toid spondylitis (Schilder eta l., l954; Toone et a l., l959). The r ecognit iont h a t t h e s e w e r e d i ff er e n t d i sor d e r s ( a l -though sha ring some chara cterist ics) led t otheir separa tion into tw o categories (rheuma -t oi d a r t h r i t i s a n d s pon d y loa r t h r o pa t h y )(Ka tz , l989; Kelly et a l., 1985; McCa rt y, l989;Rothschild, l982). Unfortunately, the termrh e uma t o id s p on dy lit is , a n d t h e orig in a lfailure to recognize this as a separate formof art hrit is, led to much diagn ostic confusion

in paleopathology (Bourke, 1967; Brothwelland Sa ndison, l967; D uncan, l979; H udsonet al . , l975; Klepinger, l979; Rothschild,

*Correspondence to: B.M. Rothschild,Arthrit is Center of North-east Ohio, 5500 Market St . , Youngstown, OH 44512. E-mail :[email protected]

Received 12 August 1997; accepted 7 Mar ch 1999.

AME RI CAN J OURNA L OF PH Y SICA L AN THR OPOL OGY 109:259267 (1999)

1999 WIL EY-L I SS, INC.


2/9

1997). The misdiagnosis by May (1898) ofagonal (death-related) ulnar deviat ion of theh a n ds ( in a mu mmy ) a s rh e uma t o id a r t h ri-tis is a classic illustration of the importance

of g re a t f a s t idiou s n es s in a s s e s sin g t h isquestion.

Although clinician s ra rely ha ve the oppor-t u n it y t o e x a min e ma c e ra t e d bo n e s ( f ro mindividuals with validated diagnoses), clini-cal X-rays afford a common ground for diag-nosis. Analyzing the nature and distributionof radiologic altera tions allows confid ent con-firmation of a differential diagnosis. Prelimi-nar y classifi cat ion is based on alterat ions inbon e s ize a n d con fi g u ra t ion , p res en ce oferosions, and evidence of reactive bone for-m a t i on or r e m od el in g (R es n ick a n d N i -wayama, l988; Rothschild, l982). However,bone is limited in the va riety of react ions itcan ma nifest . P erilesional, regiona l, or gen-eralized increases or decreases in bony den-s i t y c a n o c c u r . Ca lc ifi c a t io n ma y o c c u r a tsites of l igament, tendon, or capsule inser-tion. Erosions ma y occur solely a s resorptivephenomena or may have a react ive compo-nent .

Although such options would a ppear tolimit diagnostic ability, ana lyzing the a lter-at ions in light of the genera l skeletal distri-bution is more productive (Rothschild andWoods, l989, 1991a,b; Rothschild et al., l988;

Woods a nd Rothschild, l988). I solated osse-ous lesions, however, a re probably not a tt rib-utable to specific diagnoses. It is usually notpossible to accurat ely state tha t a part iculardise a s e e xis t ed in a s a mp led p op u la t io n(Bennike, l985), based on the lesions foundin a few isolated bones. Conversely, defi ni-tive diagnosis is facilita ted by ana lysis of thespectrum of disease in large populat ionsamples. Expanding analysis to include ra-diologic appeara nce, pa tt ern of involvement,nature of lesions, and association with otherdise a s e f e a t u re s , t h e ma n if es t a t io n o f dis -ease in a macerated skeletal populat ion is

often a t tr ibutable to a specifi c clinical diag-nosis (Rothschild and Woods, l989, 1991a,b;Rothschild et al . , l988; Woods and Roths-child, l988).

The report by Kilgore (1989) of erosivedisease in Nubians seemed compatible withthe specific diagnosis of spondyloarthropa-

thy. The lat ter is characterized by specificpatterns of erosive joint disease and a ten-dency to spine an d sacroiliac fusion (Mc-E we n e t a l ., l971; R es n ick a n d N iwa y a ma ,

l988; Rothschild l982; Rothschild et al., 1994;Woodrow, l985). The curr ent stu dy exa minesNubian populat ions with special at tentionto especially dia gnostic stru ctures (e.g., ver-tebra l an d sa croiliac joints ).

MATERIALS AND METHODS

O n e h u n dred a n d t h ir t y -e ig h t M eriot icN ub ia n s f rom t h e S e m n a S ou t h S i te i nN ort h e rn Su da n we re e xa min e d (Arizon aSt a te U niversity, Tempe, Arizona ). The s iteis o n t h e we s t ba n k o f t h e N ile R iv e r , 15miles south (Fig. 1) of Wadi Ha lfa (Zabkar

and Zabkar, l982). It is dated at 2,0001,600years before present . While dista l extremi-ties were less well-represented in this skel-eta l popula tion, a xial components (e.g., ver-t e bra e , s a c roi lia c join t s ) we re p res e rve d.Sixty-one individuals were examined fromt h e H a s s i e l A bio d s i t e s in N o rt h e rn M a li(Fig. 1). Fifteen individuals were dated at7,000 y ears before present (ybp), an d 46were dated at 4,500 ybp (Dutour, 1989).

Three other sit es, housed at the AmericanMuseum of Nat ura l Hist ory (New York, NewYork), were examined. Although skeletonsfrom the lat ter sites were reasonably com-plete, surviving field notes are quite limitedfor th ese 19th centur y collections. The la rg-est collect ion, designated El Hessa or thevon Luschan collection, comprised 115 indi-v idu a ls . A s e con d s i t e, iden t ifi e d on ly a snear P yra mids of Light , consisted of 10i nd iv id u a l s, a n d a t h i rd s it e , d e s ig n a t edNubian Egypt , comprised 7 individuals.These latter samples, though small in num-ber, a re included a s collabora tive evidence.

The skeletal remains were subjected tov is u a l e xa min a t io n of a l l a r t ic u la r re g ion sb y a t l ea s t t w o a n d g e n er a l ly t h r ee o f t h e

au thors, to identify a ll occurrences of a rticu-l a r a n d p er ia r t i cu la r b on y a l t er a t i on st h rou g h ou t e a ch s k elet o n , t o s pe cif y t h etypes of bony alt erat ions at ea ch occurrence,an d to ma p the distr ibution of occurrences ineach skeleton. In the event of disagreementas to wh ether a lesion represented erosion or

260 B .M . RO TH S C H ILD ET AL.


3/9

postmortem damage, for the purpose of thisstudy it wa s treated as postmortem dama ge.

R a dio g ra p h s we re s e le ct iv e ly o bt a in edwith the bones in normal anatomic position.One author (B.M.R.)was specifically respon-sible for their interpreta tion.

RESULTS

Isolated lesions

Isolated holes, of unclear significance, werefound in 10 Meriotic Nubia n sk eletons (7%;

a ffectin g 1 hip, 2 knees, 4 shoulders, 1 elbow,

and 2 wrists) , and 5 von Luschan skeletons(4%; affecting 4 shoulders a nd 1 meta ta rsa lphalan geal joint) . Isolated erosions (ma r-

ginal a rea gr ooves or disruptions)w ere foundin 14 Mer iotic Nub ia n skelet ons (10%; affect -ing 1 hip, 7 shoulders, 3 elbows, 2 wrists,and 1 metacarpal pha langeal joint). Similarisolated erosions were found in 4 von Luschanskeletons (3%; a ffecting 1 shoulder, 1 w rist, 1hip, an d 1 metat ar sal pha langeal joint).

Fig. 1. Map of northern Africa, noting locations of sites examined. A, Egyptia n sites; B, Meriotic site;C, Hassi el Abiod.

261NUBIAN EROSIVE ARTHRITIS


4/9

Definitive lesions

N o r t h er n S u d a n ese s p on d y l o a r t h r o p a -

t h y . Ana lysis of the Meriotic Nubia n sam-ple for axial joint involvement revealed 6individua ls (4%) wit h fusion of zy ga pophy-seal joints, associated with calcificat ion of

the a nulus fi brosis, resulting in syndesmoph-yte forma tion (Table 1) (Resnick an d Ni-wayama (l988) defined syndesmophytes asossificat ion w ithin th e a nulus fi brosus lead -ing to thin, vertical radiodense areas). Thethoracic spine was predominantly affected.Two insta nces were associat ed with a ca ndle-wa x-like calcificat ion of an terior a nd la terallongitudinal ligaments. Vertebral involve-ment was an isolated phenomena in 2 indi-v idu a ls , a s s ocia t e d wit h p a u cia r t icu la r a r-t hr it is in 3 in divid ua ls , a n d w it h amon a rt ic ula r (p rox ima l h u me ra l) h o le inone other.

P eripheral joint erosions were asy mmetr i-cal in distribution a nd a ssociat ed with exu-berant , reactive perilesiona l new bone forma -t ion . Alt h ou g h h a n ds a n d f ee t we re o n lyrarely represented in this collect ion, wristfusion wa s noted in one individua l. Erosionswere marginal and subchondral in distribu-tion, affecting t ha t zone of meta physea l bonewit h in t h e s y n o v ia l me mbra n e a n d o rig i-nally covered by cartilage, respectively. Ra-diographs revealed predominantly scleroticperilesional margins.

Sacroiliac erosions and fusion were pre-sent in 2 individuals with vertebral involve-

ment. One had unilateral sacroiliac involve-me n t a s s ocia t e d w it h w ris t a n d s h o u lde rerosions. The other had bilateral sacroiliacdisease with erosions of left wrist, erosionsof metacarpal phalangeal bilaterally and ofthe right meta ta rsal pha langeal joint . Aholewa s also present in a right dista l meta carpalof tha t individual.

M a l i sp o n d y l o a r t h r o p a t h y. Ana lysis of

the Mali sample for axial joint involvement

revea led one (MN27/H 1) ind ividu a l (2%) w ith

asymm etrical w rist fusion a nd proximal in-

t e rph a la n g e a l jo in t s u bch on dra l e ros ion s

(Table 1). Radiographs revealed predomi-

nantly sclerotic perilesional margins.

E g y p t i a n sp o n d y l o a r t h r o p a t h y. While

all other observations of spine involvement

w e r e m or e l im i t ed i n d i st r i b ut i on , z y g -

apophyseal joint fusion with syn desmophyte

f orma t io n , s imu la t in g t h e a p p ea ra n ce of a

piece of bamboo, was found in one (AMNH

6575) of 10 skeletons from the site desig-

nat ed near P yra mids of Light (Table 1).

Th e a n k le a n d p rox ima l in t erp h a la n g e a l

joint erosive disease in this individual, with

the classic ba mboo spine a ppea ra nce, wa s

associated with exuberant react ive perile-

s ion a l n e w bon e f orma t ion . Sa croi lia c in -

v ol vem e nt w a s a l s o n ot e d i n on e p a r t ia l

skeleton from the population labeled Nu-

bian Egypt.

Isolat ed asymm etrical proxima l interpha-

l a n g ea l a n d m et a c a r pa l p ha l a n g ea l joi n t

erosive disea se, a ssociat ed with rea ctive a nd

enthesial new bone forma tion, was noted in

one von Luschan skeleton. Proximal inter-

phalangeal joint fusion was noted in a sec-

ond individual from that site.

N u b i a n i n f ec t i o n a n d d i f f u s e i d i o p a t h i c

sk e l e ta l h yp e r o st o si s. O n e in f e ct io n(sternum) was noted in a Meriotic Nubian

skeleton, and isolated dripping candle-wax-

like calcification of the anterior longitudinal

ligament (diffuse idiopathic skeletal hyperos-

tosis) wa s present (Ta ble 1) in a n a dditiona l

18 (Arr ia za et a l., 1993). An infected h ip wa s

n ot e d in on e v on L u s ch a n s k elet o n , a n d

TAB LE 1. Fr equencies of pathologic condit i ons1

Si teSampl e

size

Spondyloarthropathy distribution

D I S H 2% za S I S ho Wrist MC P P I P D I P An kle MTP

Mer iot ic 138 4 6 2 1 3 1 1 18H a ssi el Abiod 61 2 1 1 1von L uscha n 115 3 1 1 1 1 2 3P y r a mids of L igh t 1 0 10 1 1 1Nubia n E gypt 7 14 1

1 %, frequency; za, zyga pophyseal a nd syndesmophytes; SI, sa croil iac ; Sho, shoulder; MCP, metacarpal phalangeal ; P IP, proximalinterphalangeal of hand; DIP, distal interphalangea l of hand; MTP, metatar sal phalangea l .2 Diffuse idiopathic skeletal hyperostosis.



5/9

diffuse idiopathic skeletal hyperostosis inthree.

DISCUSSION

Spondyloarthropathy

Sp on dy loa rt h ro pa t h y de fi n e s a g rou p o fdise a s es wit h a t e n den cy t o re a c t ive n e w(enthesial) bone forma tion, pauciar t icularperiphera l joint involvement, an d frequentoccurrence of a xial (spine and sacroiliac)joint disease (Arria za , 1993; B yw a ters, l960;Martel, l968; McEwen et al . , l971; Ortnerand Putschar, 1985; Resnick and Niwayama,l988; Rothschild, l982; Rothschild et al . ,1994; St einbock, 1975). Zyga pophysea l jointerosions and fusion appear pathognomonicfor spondyloarthropathy. They have not been

identified in other diseases (San Zhang andRothschild, 1993). The classical ba mboospine, with uniform smooth fusion of thespine, mimicking a piece of bamboo, is un-co mmon , a l t h o u g h h ig h ly c h a ra c t eris t ic.Limited in occurrence to individuals withspondyloar thropathy (Ka tz, l989; Kelly etal. , l985; McCarty, l989; Resnick and Ni-w a y a m a , l 988; R ot h s ch i ld , l 982), i t w a sclearly present (AMNH 6575) at the Pyra-mids of Light site. Northea st Africans clearlyhad an erosive arthropathy of the spondylo-arthropathy variety.

P re s e n ce o f s u bch on dra l a s we ll a s ma r-

ginal erosions, characteristic of spondyloar-thr opa thy (Rothschild a nd Woods, 1991a ),was observed both in this study and that ofKilgore (1989). L a ck of periar ticular loss ofbony density in this study a nd tha t of Kilgore(1989) is also characteristic of spondyloar-thr opa thy (By wa ters, l960; Ka tz, l989; Kellyet al . , l985; McCarty, l989; McEwen et al . ,l971; Resnick and Niwayama, l988; Roths-child, l982; Rothschild a nd Woods, 1991a,b).The observed prominent remodeling of ero-s ion ma rg in s in bot h s t u die s is p roba blyresponsible for the X-ray density findings,chara cteristic of spondyloart hropat hy (Roth-

schild and Woods, l989, 1991a). Punchedout lyt ic areas (holes) were also noted int h e s e s t u dies , of t en a s s o cia t e d wit h bon eremodeling (Rothschild a nd Woods, l989,1991a ). L a rg e r t h a n v a s cu la r iza t ion ch a n -nels (but of unclear etiology), they a re com-mon in spondyloart hropath y (Rothschild andWoods, l989, 1991a ). The er osive a rt hr itis in

northeast (Nubian) Africa is clearly of thespondyloar thropathy variety.

The next question is, which variety? OnlyR e it e r s s y n drome a n d p soria t ic a r t h ri t is

(among the variet ies of spondyloarthropa-thy) can occur with only limited spine in-volvement (yet spa ring t he lumbar spine)(K a t z , 1989; M cCa rt y, 1989; R o t h s ch ild ,1982). Spina l involvement in psoria tic ar th ri-t is a n d R e it e r s s y n drome ca n be di f fu s e(e.g., t he bam boo spine noted in AMNH7575), b ut t e nd s t o b e m or e l im i t ed , a sobserved in t his stu dy.

A s p s o ria t ic a r t h ri t is p re do min a n t ly a f -fects the hands and Reiters syndrome pre-domin a n t ly a f f ect s t h e f ee t (R e sn ick a n dNiwa ya ma , l988; Rothschild, l982), it is rea -sonable (in view of the observed distribut ionof peripheral joint disease) to consider adia g n os is of p soria t ic a r t h ri t is . H o we ve r,Reiters syndrome frequently complicatesinfect ious-agent diarrh ea (Colin and Fries,l976; Katz, l989; Leung et al., l980; McCarty,l989; Roth schild, l982). In view of Old Worlds a n it a ry con dit ion s , R e it e r s s y n drome isalso a reasonable diagnosis.

P opulat ion frequency of spondyloart hropa-thy in Nubia n populat ions is fully with in thera n g e p rev iou s ly re port e d in mo st N ort hAme rica n s i t e s (R o t h s ch ild a n d Wo ods ,1992) , bu t lo we r t h a n t h a t n o t e d in t h o s ecommunit ies in which sanitat ion was com-promised (Rothschild and Rothschild, 1993).Apparent exceptions at Pyramids of Lightan d Nubia n Egypt sites (Ta ble 1) refl ectt h e s ma ll de n omin a t o r a n d a re n o t s t a t is t i-cally different from the 24% frequenciesnoted at the Meriotic, Hassi el Abiod, andvon Luschan sites. While Morton (1995)described disposal of persona l and house-h o ld wa s t e a s p rimit iv e , t h e f re q u e n c y o fspondyloarthropathy suggests that at leastt h e wa t e r s o u rc e s h a v e n o t be e n c o n t a mi-nat ed by sewage disposal. While studies onmorta lity and impact of agriculture ar e ava il-able (Beckett a nd L ovell, 1994; Van G ervene t a l . , 1981) , we we re u n a ble t o fi n d p u b-lished studies direct ly addressing regionalsa nita tion in the time period of interest.

Differential diagnosis

E r o si ve d i se a s e m a y com p li ca t e ot h e rf o rms o f a r t h ri t is ( o t h e r t h a n rh e u ma t o id



6/9

art hrit is an d spondyloar thropathy), but on apopulat ion basis, t ends not t o be common orpolyarticular (Resnick and Niwayama, l988;Roth schild, l982).

R h eu m a t o i d a r t h r i t i s. The prominentsubchondral localization of erosions in thisstudy and that of Kilgore (1989) is at vari-ance with observations in rheumatoid arthri-t is (R e sn ick a n d N iwa y a ma , l988; R ot h s -child et al., l988, 1990, 1992a). Rheumatoida rt h ri t is p rodu ce s e ros ion s wit h s moot h ,rounded lesional edges and excavated inter-nal trabeculae. Lesions typically are distrib-uted along the mar ginal or bare a rea of bone(between the area of bone covered by carti-lage a nd the insertion of the joint capsule) a sa resorptive groove or front of resorption

(Leisen et al. , 1987; Resnick and Niw a ya ma ,l988; Rothschild et al . , l988, 1990). Thepunched outlesions observed in this studya n d by a ls o by K ilg o re ( F ig . 1 in K ilg o re ,l989) a re q u i t e dis t in ct f rom t h e ma rg in a lerosions noted in rheuma toid art hritis (Roth-schild et a l. , l988, 1990, 1992a ; Woods a ndRoth schild, l988).

Th e re a ct iv e n e w bon e f orma t io n in a f -flicted Nubian s is in marked contra st to theminimal or a bsent perierosional bone reac-t ion of rh e uma t o id a r t h ri t is . P e ri les ion a lloss of bony density (periarticular osteope-n ia ) is u n iformly p res en t in rh e uma t oida rt h ri t is (B o g och e t a l . , l988; K a t z , l989;McCa rty, l989; Ropes et al . , l958; Roths-child, l982; Rothschild et a l. , l988; Woodsa n d R o t h s ch ild , l988). (Sin c e a 3050%change in bone density is required (Resnickand Niwayama, l988) for radiologic recogni-t ion, perilesional bone r eact ion in rheuma-toid art hrit is is below tha t threshold.) Scle-rotic reactive bone noted here a nd in K ilgore(1989) is notably absent at the borders ofrheumat oid erosions (Bogoch et al . , l988;Katz, l989; McCarty, l989; Ropes et al., l958;Rothschild, l982; Rothschild et al . , l988;

Woods an d Rothschild, l988). The perile-sional bone (around t he erosions) wa s actu-ally increased in density in both studies, asexpected in spondyloar thr opa thy, but incom-p a t ible w it h a dia g n os is of rh e u ma t o id a r-thrit is .

Rheumatoid arthritis (on a population ba-sis) tends to affect almost every appendicu-

lar joint , with predilect ion especially forcarpal, ulnar st yloid, metacarpopha langeal,me t a t a rs op h a la n g e a l , a n d p rox ima l in t er-phalan geal joints. The mea n number of pe-

ripheral joints involved in rheuma toid art hri-t i s i s 12 (R es n ick a n d N iw a y a m a , l 988;Rothschild, l982; Rothschild a nd Woods,1990). This contrasts with the limited jointinvolvement in Meriotic and Egyptian Nu-bians and only wrists, shoulders, and meta-ca r p a l p ha l a n g ea l joi nt s i n t h e s t u d y b yKilgore (1989). Such limited erosive diseasewould be highly unusual in rheumatoid ar-thritis, but is quite characteristic of spondy-loarthropathy in primates (Rothschild andWoods, l989, 1991a,b).

The postcervical spine a nd sa croiliac joints

a r e u n a ff ect e d i n r h eu m a t o id a r t h r i t i s.Squaring, syndesmophytes, react ive enthe-sial remodeling, zygapophyseal, and sacro-iliac joint erosion or fusion are notably ab-sent in rheumatoid arthrit is . Ankylosis isalso absent in clinical populat ions with rh eu-ma toid art hrit is (prior to the a dvent of corti-costeroid therapy; see Rothschild et al., l988,1990; Woods a nd Roth schild, l988). P resenceof s u ch p h en ome n a in a f fl ict e d N u bia n se limin a t e s rh e u ma t o id a r t h ri t is a s a p os -sible cause (Katz, l989; Kelly et al . , l985;McCart y, l989; Resnick a nd Niw ay am a, l988;Rothschild, l982; Rothschild et al . , 1988,

1990).As involvement is not always pauciarticu-lar and axial joint disease is not present ina l l in div idu a ls wit h s pon dy loa rt h ro p a t h y,diagn ostic confusion wit h rheuma toid arth ri-t is does exist . Psoriat ic arthrit is (a form ofspondyloar thropathy) is often a source ofconfusion, a s 40%ma y ha ve a polyart icularpat tern (Moll, 1979; Rothschild a nd Woods,l989). D istinguishin g t his form of spondylo-a rt h ro pa t h y f rom rh e uma t o id a r t h ri t is in as in gle in div idu a l ca n be comp lica t e d, a sthere are fi ve pat terns of psoriat ic ar thrit is :a x ia l dis ea s e , dis t a l p redomin a n t , a r t h ri t is

mutilans, asymmetrical pauciart icular, andpolya rticula r (pseudo-rheuma toid).

G ou t a n d i n f ec t i ou s a r t h r i t i s . Gouta n d in f e c t io u s a r t h ri t is ma y p ro du c e e ro -sions with sclerotic margins. The isolatedinfectious lesions identifi ed in Nubians w erecle a rly dis t in g u is h a ble f rom s p on dy loa r-



7/9

thropathy. The predominant ly monoart icu-la r n a t u re o f in f e c t io u s a r t h ri t is a n d g o u t(Katz, l989; McCarty, l989; Rothschild, l982;Rothschild a nd H eat hcote, 1995; Rothschild

an d Woods, 1990) and lack of a periosteum-based overhanging lesional edge (character-istic of gout; see Katz, l989; McCarty, l989;Ortn er a nd P utscha r, l985; Rothschild, l982)are clear ly dist inct from the a rthrit is classi-fi ed as spondyloarthropathy in Nubians.

C a l c i u m p y r o p h o sp h a t e d e p osi t i o n d i s-

ease. Ca lcium pyrophospha te depositiondisease or pseudogout causes dista l meta car-pal sclerosis and fla t tening a nd joint surfa ceindentations (e.g., at the radiocarpal joint oft h e wris t ) (G e n a n t , l985; R e sn ick a n d N i-wayama, l988; Rothschild, l982; Rothschildet a l . , 1992b). G iant subchondral cysts an dcart ilaginous calcium deposit ion are com-monly present , often as a sheet of calciumwh ich para llels the art icular sur face (Ma rkeland Hart, 1982). Hemochromatosis (an irons t ora g e dis ea s e ) a n d h y p erp a ra t h y ro idis mar e causes of calcium pyrophospha te deposi-t ion disease which may have a pauciart icu-la r e ros ive c omp on e n t (R e sn ick a n d N i-wa ya ma , l988; Rothschild, l982; Schum a cher,l985). While hemochromatosis does indeedproduce ra diologic chan ges in the metacar-pal pha langeal joints, joint spa ce narrowing

(related to loss of cartilage) is the predomi-nant radiologic lesion. Erosions appear unde-scribed. The soft-tissue sw elling produces arheuma toid-like clinica l appear a nce, but t herad iogra ph is quite different . Chondrocalci-n os i s , b o n y o ve r g r ow t h , a n d c r um b l in gchanges of hemochromatosis a re ea sily dis-tinguished from marginal erosive lesions ofrheumatoid arthrit is .

O s t eo a r t h r i t i s . Ca rt ilage fi ssuring in os-teoarthrit is causes cart ilage damage, and isocca s ion a l ly re fe rred t o by p h y sicia n s a serosions. That use implies changes in carti-

lage, not bone. Osteoart hrit is (formerly r e-f erre d t o a s de ge n era t iv e join t dise a s e orDJ D) a ctually does not produce bone ero-sions (Resnick and Niwayama, 1988; Roths-child, 1982, Rothschild a nd Woods, 1987).While erosions or holes (disruption) may beobserved in the cart ilage, actual erosion ofsubchondral bone does not occur. The mar-

ginal ar ea (between t he cart ilage-coveredbone a nd t he site of insertion of the synovia lme mbra n e in t o t h e bo n e ) is u n a f f e c t e d inosteoarthrit is .

Isolated erosions

The significance of the observed isolatede ros ion s or h oles is u n clea r . As s k elet a lremains reflect a l ifet ime of potential dis-e a s e e x p o s u re , a n d a s mo s t a re be lo w t h elimits of radiologic resolution, their erosive(or h ole) n a t u re wo u ld p roba bly n ot h a v ebeen recognized in life. Common in popula-tions with spondyloarthropathy (Rothschildand Woods, 1993), their significance is un-clear a t this t ime.

Diffuse idiopathic skeletal hyperostosis

The sign ifi cance of diffuse idiopa thic skel-etal hyperostosis is as a protective phenom-ena, not a disease (Rothschild, l985). I t isunrelated to any other recognized skeletaldise a s e, a l t h ou g h t h e a p pe a ra n c e c a n bemimicked by fluorosis and by hypervitamin-osis A (Fa ccini a nd Teotia , l974; P ennes etal. , l985; Sea w right a nd En glish, l965; Singhet a l. , l962). P resent in 20%of men over a ge50 (Roth schild, l985), its pr esence in a ssocia-t ion with spondyloar thropathy in the popu-lat ion studied is not surprising (Arriaza etal., 1993).

Perspectives in paleopathology

Slight va riat ion in ma nifesta t ion of differ-e n t dis ea s e s ma y a l low a s in gle in div idu a lwith one disease to mimic the classic ap-pearance of another (e.g., the common confu-sion of spondyloarthropathy with rheuma-toid arthritis; see Wells, l962). Analysis ofthe population occurrence of arthritis (ratherthan isolated skeletons)facilitates more pre-cise diagnosis (Rothschild and Woods, l989,1991a,b; R othschild et a l., 1990).

North Africans were clearly afflicted witha form of spondyloarthropathy, perhaps of

the Reiters or psoriatic variety. While evi-de nce of s pon dy loa rt h ro p a t h y a bo un ds int h e l it e ra t u r e of h u m a n s ke le t a l d is ea s e(Arriaza, 1993; Kramar, l982; Ortner andP uts char, l985; Ruffer, l92l; Smit h a nd J ones,l910; St einbock, l975; Zora b, 1961), pre-Columbian Old World r heumatoid a rthrit ishas proven elusive (Appelboom, l987). The



8/9

cu rren t s t u dy f u rt h er docu me nt s t h e a b-s e n c e o f rh e u ma t o id a r t h ri t is in N u bia n s ,supporting t he hypothesis of Rothschild etal. (l988) tha t rh eumatoid art hrit is began a s

a New World disease.

ACKNOWLEDGMENTS

We e xp r es s ou r a p pr e ci a t i on t o D r s .Cha rles Merbs of the Arizona Sta te U niver-s it y a n d I a n Ta t t e r sa l l of t h e A me ri ca nMuseum of Natural History for facilitat ingaccess and logistics in the collections whichthey curate.

LITERATURE CITED

Appelboom T. l987. Art, hist ory a nd an tiquity of rheu-mat ic diseases. B russels: E lsevier Librico. 128 p.

Arria za BT. 1993. Seronegative spondyloarth ropathiesan d diffuse idiopat hic skeletal h yperostosis in a ncientnort hern C hile. Am J P hys Anth ropol 91:263278.

Arria za BT, Merbs CF, Rothschild B M. 1993. Diffuseidiopathic skeletal hyperostosis in Meroitic Nubiansf r om S e m n a S o ut h , S u d a n . A m J P h y s An t h r op ol92:243248.

Beckett S, Lovell N. 1994. Dental disease evidence forag ri c ul tural i nte nsi fic at i on i n the Nubi an C -g roup.Int J Osteoarchaeol 4:223240.

Bennike P. 1985. Paleopathology of Danish skeletons.Copenha gen: Akademisk Forag. 198 p.

Bog oc h E , Gsc hwe nd N, Bog oc h B, Rahn B, Pe rre n S.1988. J uxtaa rticular bone loss in experimenta l infla m-mat ory ar thrit is. J Orthop Res 6:648656.

Bourke J B. 1 96 7. A re vie w of pa l ae opathol og y of a r-thrit ic diseas e. In: B rothw ell D, Sa ndison AT, editors.D i s ea s e s i n a n t i q u it y. S p r in g fi e ld , I L : Th om a s . p352370.

Br othwell DR, Sa ndison AT. 1967. Diseases in an tiquity.Asu rvey of the diseas es, injuries, and s urgery of ear lypopulat ion. Springfi eld: Cha rles C. Thomas. 580 p.

Byw at ers E. 1960. The early r adiologic signs of rheuma-toid arthritis. Bull Rheum Dis 11:231234.

Colin A, Fries J F. 1976. An experiment a l epidemic ofReiter s revisit ed. Ann I nt ern Med 84:564566.

Dunca n H. 1979. Letter to th e editor. Pa leopat hol News-lett 25:1011.

D u t o u r O . 1 9 8 9 . H o m m e s f o s s i l e s d u S a h a r a . P a r i s :Centre Na tional de la Recherche Scientifi que. 342 p.

Fa ccini J M, Teotia SP. 1974. Histopat hological ass ess-ment of endemic skeletal fluorosis. Calcif Tissue Int16:4557.

Genant HK. 1985. Radiology of the rheumatic diseases.In :

McCart y DJ , editor. Arth ritis a nd a llied conditions, l0thed. P hiladelphia: L ea a nd F ebiger. p 76147.

Hudson C , Butl e r R, Si ke s D. 1 9 7 5 . Arthri t i s i n the

prehistoric southeast ern Un ited Sta tes: biological andcultural variables. Am J Phys Anthropol 43:5762.

Kat z WA. 1 98 9. Rhe umati c di se ase s: di a g nosi s andman agement. P hiladelphia: Lippincott. 1020 p.

Ke ll y WN, Harr i s E D J r , Ruddy S , S l edg e C B . 1 9 85 .Textbook of rheuma tology, 2nd ed. Ph iladelphia : Sa un-ders.

Kilgore L. 1989. Possible case of rheumatoid arthritisfrom Suda nese Nubia. Am J P hys Anthropol 79:177183.

Klepinger LL. 1979. Paleopathologic evidence for theevolution of rheumatoid arthritis. Am J Phys Anthro-pol 50:119122.

Krama r C . 1 98 2. A c ase of anky l osing spondy l i t is i nmedieval Geneva. OSSA8:115129.

Leisen J C, D uncan H, Riddle J M, P itchford WC. 1987.The erosive front: a topogra phic study of the junctionbe twe en the pan nus an d the subc hondral pl ate i n themac e rate d rhe umatoi d me tac arpal he ad. J Rhe uma-tol l5:l722.

Leung FY, Littlejohn GO, Bomba rdier C. 1980. Reiterssyndrome after Campylobacter jejunoenteritis. Arthri-tis Rheum 23:948950.

Marke l SF, H art WR. 1 98 2. Arthropath y i n c al c i umpy rophosphate di hy drate c ry stal de posit i on di sease .Arch P at hol 106:529533.

Ma rt el W. 1968. Ra diologic signs of rheuma toid ar th rit iswi th part i c ular re fere nce to the ha nd, wr i st , and foot .Med Clin North Am 52:655665.

May WP. 1 89 8. Rhe umatoi d a rthri t i s (ostei t i s de for-m a n s ) a f fe ct i n g b on e s 5 5 00 y ea r s o ld . B r M ed J2:16311632.

McCart y D J . 1989. Arth ritis a nd a llied conditions, 11thed. Ph iladelphia: Lea an d Febiger. 2100 p.

McEw en C, DiTat a D, Lingg C. 1971. Ankylosing spondy-litis and spondylitis accompanying ulcerative colitis,re g ional e nte ri t i s, psoriasi s, and Re ite rs di sease : acomparative study. Arthritis Rheum 14:291318.

Moll J M. 1979. The clinical spectrum of psoriatic arthri-tis. C lin Ort hop l43:6675.

Morton RS. 1 99 5. Se xual at t i tude s, pre fe renc es andinfections in ancient Egypt. Genitourin Med 71:180186.

Ortner DJ , Putschar WG. 1985. Identification of patho-logica l conditions in huma n skeletal rema ins. Was hing-ton, DC: Smithsonian Institution Press. 479 p.

P ennes D R, Ma rt el W, Ellis CN. 1985. Retinoid-inducedossi fic at i on of the poste ri or l ong i tudi nal l i game nt .Skeleta l Ra diol l4:191193.

Re snic k D, Ni wa y ama G. 1 98 8. Di a g nosis of bone andjoint disorders. P hiladelphia: S aun ders. 6250 p.

Ropes MW, B ennett GA, Cobb S, J acox R, J essar RA.1958. 1958 revision of diagnostic criteria for rheuma-toid arthritis. Bull Rheum Dis 9:175176. 416 p.

Rothschi l d B M. 1 9 82 . Rhe umatol og y : a pri mary c areapproach. New York: Yorke Medical Press.

Rothschild B M. 1985. Diffuse idiopat hic skeleta l hyper-ostosis: misconceptions and reality. Clin Rheumatol9/l0: 207211.

Rothschild B M. 1997. Two fa ces of rheumatoid a rthr i-tis: type A versus type B disease. J Clin Rheumatol3:334338.

Rothschild BM, Heathcote GM. 1995. Characterizationof gout in a skeletal population sample: presumptivediagnosis in Micronesian population. Am J Phys An-thropol 98:519525.

Rothschild BM, Rothschild C. 1993. 19th century spon-dyloarth ropath y independent of socioeconomic stat us:lack of skeletal collection bias. J Rheuma tol 20:314319.

Rothschild B M, Woods RJ . 1987. Osteoart hrit is in prehis-toric Na tive Americans . Age 10:161.

Rothschild B M, Woods RJ . 1989. Spondyloart hropath yin gorillas. Semin Arthritis Rheum 18:267276.

Rothschild BM, Woods RJ . 1990. Symmetrical erosivedisease in Archaic Indians: the origin of rheumatoidarth ri t i s i n the Ne w World. S e min Arthri t i s Rhe um19:278284.

Rothschild BM, Woods RJ . 1991a. Spondyloarthropathy.E rosive a rthri t i s i n re pre senta t i ve de fle she d bone s.Am J P hys Anth ropol 85:125134.

Rothschi l d BM, Woods RJ . 1 99 1b. Re ac t i ve e rosi vear thrit is in chimpanzees. Am J P rimat ol 25:4956.



9/9

Rothschi l d BM, Woods RJ . 1 99 2. C hara c ter of pre -C olumbi an North Ame ric an spondy l oarth ropathy . JRheumatol 19:12291235.

Roths child B M, Woods RJ . 1993. Implications of isolatedosseous erosions r elated to population skeletal h ealth.

Hist orical B iol 7:2128.Rothschi l d B M, Turne r KR, De L uca MA. 1 98 8. Sy m-me tri cal e rosi ve peri pheral pol y arthri t i s i n t he L a teArchaic period of Alab a ma . S cience 241:14981501.

Roths child B M, Woods RJ , Ort el W. 1990. Rh euma toidarthri t i s i n the buff : e rosi ve arthri t i s i n re pre se nta-tive defleshed bones. Am J P hys Anthropol 82:441449.

Rothschi l d BM, Woods RJ , Rothschi l d C , Se bes J I .1992a. Geographic distribution of rheumatoid arthri-tis in ancient North America: implications for patho-genesis. Semin Arthritis Rheum 22:181187.

Rothschild B M, Woods RJ , R othschild C. 1992b. C al-cium pyrophosphate deposition disease: description indefleshed skeletons. Clin Exp Rheumatol 10:557564.

Rothschi l d BM, P oteat GB , Wi l li ams E , C ra wford WL .1994. Infl am mat ory sacroiliac joint pa thology: evalua -t i on of ra di ol og i c asse ssme nt t e chni q ue s. C l i n E xpRheum at ol 12:267274.

Ruffe r MA. 1 92 1. Studi e s i n the pal ae opath ology ofEgypt. Chicago: University of Chicago Press. p 184l93.

San Zhang C, Rothschild BM. 1993. Zygapophyseal andc ostotra nsve rte bral /c ostove rte bral joi nts: a n an a-tomic asse ssment of a rthri t i s i mpac t . Br J Rhe umatol32:10661071.

Schilder DP, Harvey WP, Hufnagel CA. 1954. Rheuma-toid spondylitis and aortic insufficiency. N E ngl J Med255:1117.

Schumacher HR. 1985. Ochronosis, hemochromatosisan d Wilsons diseas e. In: McCa rty DJ , editor. Arthritis

and allied conditions, 10th ed. Philadelphia: Lea andFebig er. p 15651578.

Se awri g ht AA, E ng l i sh P B. 1 96 5. Hy pe rvitami nosi s Aand hyperostosis of the cat. Nature 206:11711172.

Singh A, Dass R, Singhhayreh S, J olly SS. 1962. Skel-

e tal c hang e s i n e ndemi c fluorosi s. J Bone J oi nt S urg[Br ] 44:806815.

Smit h G E, J ones FW. 1910. The a rcha eological sur vey ofNubia : Report for 19071908. Volume II: r eport on t heh u m a n r e ma i n s . C a i r o : N a t i on a l P r i n t i n g D e p a r t -ment . 100 p.

Steinbock RT. 1976. P ala eopat hological dia gnosis a ndinterpreta tion. Springfi eld: Thomas. 423 p.

Toone EC J r, P ierce EL, Henn igar G R. 1959. Aort itis a ndaortic regurgitation associated with rheumatoid spon-dylitis. Am J Med 21:255263.

Va n G e r v en D P , S a n f o rd M K , H u m m er t J R . 1 981 .M or t a l i t y a n d c ul t u r e ch a n g e i n N u bi a s B a t n e lHajar. J Hum Evol 10:395408.

Wells C. 1962. J oint pa th ology in a ncient Anglo-Sa xons.J B one J oint S urg [B r] 44:948949.

Woods R J , Rothschild B M. 1988. Populat ion an alysis ofsymmetrical erosive art hritis in Ohio Woodland Indi-

an s (1200 years before the present time). J Rh eumat ol15:12581263.

Woodrow J C. 1985. G enetic as pects of th e spondyloar-thropat hies. Clin Rheum D is 1:124.

Zabka r LV, Zabka r J . 1982. Semna South. A prelimina ryreport of the 19661968 excava tion of t he U niversityof Chicago Oriental Institute Expedition to SudaneseNubia. J Am Res Cent Egypt 19:2128.

Zorab PA. 1961. The historical and prehistorical back-g round of an ky l osi ng spondy li t i s. P roc R Soc Me d54:415420.


Documents

American Journal of Physical Anthropology Volume 109 Issue 2 1999 B.M. Rothschild; B. Arriaza; R.J. Woods; Olivier Du