Patricia Smith Ronald A. Bloom* Judith Berkowitz

Department of Anatomy and Embryology, Hebrew University-Hadassah Faculties of Medicine and Dental Medicine, Jerusalem, Israel

* Department of Radiology, Hadassah Hospital, Jerusalem, Israel

Received 14 May 1983 and accepted 18 May 1984

Keywords: humerus, combined cortical thickness, bones, Epi-Paleolithic.

Diachronic Trends in Humeral Cortical Thickness of Near Eastern Populat ions

Humeral cortical thickness measurements (CCT) were taken from radio- graphs of four Near Eastern skeletal samples dated to the Epi-Paleoli-~bic (Natufian), Middle Bronze I (MBI), Roman/Byzantine and Early Arab periods. Epi-Paleolithic CCT values in both sexes were signiticantly higher than those of any other group. In the males, Epi-Paleolithic CCT values were extremely high when compared with those of living populations, while CCT values in the MBI to Early Arabs were within the range considered normal for living populations. In the females, Natufian and MBI CCT values fell within the range considered normal for living females, while the Roman/ Byzantine and Early Arab CCT values were diagnostic of severe osteopenia. We consider that in the males, the exceptionally high Epi-Paleolithic values reflect functional demands associated with techno- logical constraints and activity patterns of males at that time. In the same female groups, function presumably changed less drastically over time. The exceptionally low CCT values observed in the later groups were attributed to the combination of poor health status and calcium drain caused by pregnancy and lactation.

1. I n t r o d u c t i o n

C h a n g i n g modes of p roduc t ion , resul t ing from the in t roduct ion of fa rming are associa ted with, among o ther changes, marked changes in the pa t t e rn and intensi ty of phys ica l act ivi ty, nut r i t ion and disease pa t te rns . These, as well as o ther less well defined var iables associa ted with changing lifestyles, may be assumed to affect the physical character is t ics of popula t ions . Env i ronmen ta l pressures opera t ing th roughout the lifetime of ind iv idua ls affect growth and robust ic i ty , and on a long- term basis may modify the pheno type of popula t ions . In studies car r ied out in the Nile Val ley (Greene & Armelagos , 1972; Car lson , 1976) Nor th Afr ica (Fe rembach , 1962; Chamla , 1980), and Europe (Frayer , 1980), ma rked changes in s ta ture , skeletal robus t ic i ty and d imorph i sm, as well as in the craniofacial complex and dent i t ion, have been documen ted over this per iod of change which da tes from the te rmina l Pleis tocene to recent times.

In the Near East , few changes seem to have occurred in the physical make -up of popula t ions over this same per iod (Arensburg , 1973; Fe rembach , 1977; Smith e/al. , 1984). This m a y be pa r t ly due to the fact tha t the te rminal Pleistocene popula t ions , the Natuf ians , are considered to be inc ip ient agr icul tura l is ts . They were, for example , extensive collectors incorpora t ing larger quant i t i es of cereals into their diet than was the case for their predecessors or con tempora r i e s elsewhere (Sillen, 1981; Smith, 1972; Smith et al., 1984; Schoeninger , 1982).

The overal l lifestyle and, specifically, pa t te rns of physical act ivi ty and social s t ruc ture in the Natuf ians , was, however , essent ial ly tha t of their contemporar ies and predecessors . T h e archeological record (Bar-Yosef, 1983; Davis, 1983) indicates that they con t inued to rely heavi ly on hunt ing, wi th gazelle the main large m a m m a l hunted. The i r tool kit was l imi ted to l i thic and bone implements , and no evidence has yet been found of the use of ar rows or nets for hunt ing-accessor ies which may reduce the amoun t of physical act ivi ty needed for t r app ing and s laugh te r ing game.

Journal of Human Evolution (1984) 13, 603 611

0047-2484/84/080603 + 09 $03.00/0 �9 1984 Academic Press Inc. (London) Limited

604 P. SMITH E T A L .

Finally, the Natufians were nomadic or semi-sedentary, living in small bands with no anciliary form of transport or porterage. Their lifestyle was then very different from that of later populations in the Near East. These later populations show two main trends: one of settled villages based on mixed farming and animal husbandry and one of nomadic pastoratists, based on herds of sheep and goats, but with both donkeys and camels for transport and porterage.

Since only minor changes in anthropometric variables have been detected over this t2,000 year period, we have searched for a more sensitive method of detecting changes in the skeleton of prehistoric communities in this region, and their relation to changing subsistence patterns. One of the methods we have adopted is estimation of bone mass from cortical thickness.

Epidemiological studies have produced a large body of data on factors affecting bone mass in living populations. These include age, sex, diet and patterns of physical activity, as well as genetic factors, and nutritional, hormonal and metabolic disorders (Solomon, 1960; Chalmers & Ho, t970; Garn 1970, 1972; Nordin et al., 1975; Dequeker, 1976; Mayor et at., 1976; Pogrund et al., 1977; Mazess, 1982).

The methods that have been developed for the study of bone mass include bone biopsy, photon densitometry and radiographic studies of cortical thickness. All three can be directly applied to the study of skeletal remains, and provide a reliable means of investigating health status and patterns of physical activity in early populations.

For this purpose, radiographic studies have some advantages over the other methods, in that they are easily standardized, non-destructive and are not affected by post-mortem changes in bone composition. They have been used by Ericksen (1976, 1982) and Ruff & Jones (1981) for the examinations of different North American skeletal series and we have used a similar approach, based on the method developed by Bloom & Laws (1970) for the investigation of bone mass in skeletal populations from Israel.

The initial study on cortical thickness of bone using radiographs, was carried out on the femur and metacarpal by Barnett & Nordin (1960). They found that the endosteal margin of the femoral shaft was indistinct, introducing a large measure of error. Subsequently, this measurement was abandoned, and most measurements of cortical thickness have since been carried out on the metacarpal and usually at the midpoint of the second metacarpal (Dequeker, 1976). However at this site large inter- and intra-observer errors have also been reported (Adams et al., 1969; Noar et al., 1972), and have led to the examination of the humerus as an alternative. This bone is large, and so small errors of measurement are less critical than is the case with a smaller bone. It is non weight-bearing and so less subject to variation because of differences in body weight than is the femur. It also possesses a shaft which is roughly cylindrical distal to the bicipital tubercle. In this region the endosteal margin is sharp and parallel to the outer surface for 2-3 cm, so that the exact point at which measurements are made is not critical (Bloom & Laws, 1970). Furthermore, in post-mortem humeri the cortical cortex calculated as combined cortical thickness to total bone width, shows a very high correlation with the dry weight of the bone per unit volume (Virtma & Talkka, 1962 ).

This latter value is a measure of bone substance per unit volume, the cortical index thus being directly related to the degree of mineralization of the humerus. Barnett & Nordin (1960), questioned the validity of using information based on examination of a single bone to infer mineralization status of the whole body, since axial and appendicular osteoporosis

H U M E R A L C O R T I C A L T H I C K N E S S 605

may develop at different rates. A high correlation between bone mass in the peripheral and axial skeleton has however been reported by both Dequeker (1976) and Bloom (1980).

Bloom (1980), compared CCT of the upper limb bones in women and found that the CCT of the lower shaft of the humerus gave the lowest coefficient of variation in a homogenous female population. He suggested that the humeral site was significantly superior to both metacarpal and ulna sites for measuring CCT and that the intra-group variability was small enough to give clinically useful information for the diagnosis of osteoporosis.

From these and other studies (Bloom et al., in prep.) normal values for humeral CCT have been determined in living populations in relation to age and sex. In males, humeral CCT values average 10"0 mm and show little change between the ages of 20-70, when a significant reduction occurs and is followed by sequential loss in later years (Bloom et al., in prep.). The findings in healthy females are that mean values for CCT between the ages of 20-49 are 8'5 mm but that in extreme conditions of ill-health CCT values show a significant reduction in women in the years of 25-34 with oesteoporosis defined as present when CCT values are 7'0 mm or less. At approximately 55 years of age all women examined show a significant reduction in CCT compared with earlier values, and subsequently CCT values continue to reduce throughout life.

Measurement of humeral CCT then has advantages for use in the comparison of bone mass in adult skeletal remains in that it is not affected by minor variations in age within the age groups 20-49 in healthy females, and 20-70 in males, as defined above, which covers the age limit of most Near Eastern skeletal samples (Arensburg, 1973).

For skeletal populations, the humerus offers some additional attractions, in that it is also one of the best preserved long bones, and since all dimensions are influenced by use (Nilson & Westlin, 1971, Stevenson, 1952; Ruff& Jones, 1981; Plato et al., 1980),, comparison of right-left differences can provide a useful index of activity patterns both between and within populations. We have accordingly selected the humerus for the estimation of bone mass in Near Eastern populations.

For the present study, we have compared humeral CCT values in skeletal populations in the Near East associated with different adaptations.

The samples studied include the Natufians (10,500-8500 B.C.E.) (Bar-Yosef, 1982) who were nomadic or semi-sedentary hunter-gatherers exploiting a wide variety of food staples including wild cereals. They were compared with an Middle Bronze I (MBI) sample (2000 B.C.E.) who were nomadic pastoralists with herds of sheep and goats. The Roman and Byzantine samples were derived from sedentary villagers with a simple economy derived from mixed farming and animal husbandry a ad date from 50 B.C.E.-400 C.E. The early Arab group, dated at 1400 C.E. to 1800 C.E., also falls into this category of subsistence basis.

2. Methods and Materials

Specimens examined in this study were excavated from sites in the Galilee, Judean Hills, and coastal plain of Israel. They comprise Natufian remains from El-Wad (Garrod & Bates, 1937) and Eynan (Perrot, 1966; Valla, 1981), MBI specimens from Jebel Qa'akiir (Smith, 1982) and Givon (Davis, n.d.), Roman remains fi~om Sasa (Davis n.d.), Byzantine remains from Meiron (Smith el al., 1981), and an Arab sample excavated from Dor (Dauphin, 1979). Only adult specimens were included in this study. They were aged and

606 p. SMITH E T A L .

sexed according to Krogman (t 962). All measurements were carried out as described by Bloom & Laws (1970).

Humerus length was measured using a bone board and the diameter of the head of the humerus measured with Vernier calipers. Radiographs were taken of the humeri with the posterior surface flat against the cassette and with the source of a distance of 1-0 m. Medial and lateral cortical thickness and shaft diameter were measured three times at 0"5 cm intervals along the distal portion of the shaft where outer and inner cortical borders were narrowest and parallel. Medial and lateral cortical measurements were summed to give CCT and averaged scores for CCT and shaft diameter calculated fbr each individual.

3. Resu l t s

Descriptive statistics generated for each group are shown in Table 1. Mean age was slightly higher in males than in females and varied little between the sites. Less than 10% of those studied were age 50 or more. Significant sex differences in humerus length, diameter of head, shaft diameter and CCT were present in all samples, with male values larger than those of females. Both humerus size and CCT values varied between the groups. Humerus length, shaft diameter and diameter of the head of the humerus was greatest in the MBI and Early Arab groups, followed by the Natufians, with humeri in the Roman/Byzantine group significantly smaller in all dimensions. (P <0'05).

Values obtained for CCT and CCT ratios showed a different ranking. The Natufians had the highest CCT values and the Early Arab females the lowest CCT values. In the males, significant differences in CCT were present between the Natufian and MBI and all other groups studied (P <0-05). In the females no significant differences were present between them and the Roman/Byzantine and Early Arab groups (P <0'01).

Intergroup differences in these parameters were greater for right humeri than fbr left humeri. This finding could not, however,, be used to test for inter-group differences in assymetry since many of the individuals examined were represented by one humerus only. No constant association was found between the sites for humerus length and CCT, or shaft diameter and CCT. Patterns of association differed and CCT length and CCT/diameter ratios emphasize this dissonance. The two groups most similar in humerus length and shaft diameter (the Natufians and Roman/Byzantine samples) have very difl~rent CCT values and ratios.

Osteoporosis as defined by CCT values of 7"0 or less was diagnosed in 53% of Arab females; 23% of females in the Roman/Byzantine sample; 15% of MBI females and 10% of Natufian females. The percentage of Arab females affected was significantly higher than that affected at any other site (Table 2). The condition was much less common in males, affecting one to two males in the MBI and later samples. It was not found in any Natufian m a l e .

4. D i s c u s s i o n

Smith & Walker (1964) havc stated that CCT may be expected to reduce as shaft diameter increases since increased diameter produces a tube with improved resistance to bending forces. This explanation does not explain the high Natuiian CCT values fbund here. The Roman/Byzantine humeri which are similar to those of the Natufians in external dimensions, have very different and thinner CCT values that are similar to CCT values

Tab

le 1

M

ean

mea

sure

men

ts a

nd

rat

ios

calc

ula

ted

for

hu

mer

i in

sk

elet

al s

amp

les

from

dif

fere

nt

per

iod

s

Gro

up

Sha

ft d

iam

eter

C

CT

C

CT

/Dia

met

er

Mal

es

Fem

ales

M

ales

F

emal

es

Mal

es

Fem

ales

S

ide

No.

Yr

S

.D.

No.

Y~

S

.D.

No.

~

S.D

. N

o.

Yc

S.D

. N

o.

Yc

S.D

. N

o.

Yc

S.D

.

Nat

ufi

an

MB

I

Ro

man

/ B

yza

nti

ne

Ear

ly A

rab

R

10

I8.5

1-

2 9

16.3

1.

3 L

I1

18

.1

I-3

12

16'3

1.

0

R

8 19

.9

1.9

12

18.1

1.

5 L

13

19

-4

1-2

11

17.2

1.

8

R

10

18.7

1.

6 12

15

-9

0"5

L

14

18-5

1.

4 19

15

-5

0-8

R

23

18.8

1.

8 17

16

-0

1.4

L

21

18-8

1.

7 14

16

-0

1.3

I0

12-1

1.

2 9

10.0

1-

7 11

11

"3

1.9

12

8.9

1-7

8 9-

6 1'

8 12

9.

0 2.

0 12

9-

8 1.

2 I1

7.

6 2"

2

10

9-9

1.9

12

8.0

1.4

14

I0.5

2"

7 19

8-

1 1.

3

23

9.4

1.7

17

7.0

1.6

21

9.5

1.7

14

7.3

1.7

10

6.59

0

"07

9

6.10

0.

09

11

6.21

0'

08

12

5.41

0-

09

8 4

"78

0-

07

12

4.98

0.

11

12

5"0

8

0"05

11

4.

50

0-14

10

5.27

0-

08

12

5.07

0.

09

14

5.66

0.

12

19

5.21

0.

10

23

4-98

0-

08

17

4.39

0"

10

21

5"0

6

0-08

14

4.

57

0-10

Gro

up

CC

T/L

en

gth

M

axim

um

len

gth

D

iam

eter

of h

ead

C

CT

/Le

ng

th

Mal

es

Fem

ales

M

ales

F

emal

es

Mal

es

Fem

ales

S

ide

No.

~c

S

.D.

No.

Jr

S.D

. N

o.

5r S

.D.

No.

Yr

S

.D.

No.

Yr

S

.D.

No.

7r

S.D

.

Nat

ufi

an

MB

I

Ro

man

/ B

yza

nti

ne

Ear

ly A

rab

R

4 31

6 16

2

281

ll

L

3 31

3 8

2 28

3 8

R

6 31

9 ll

5

311

12

L

4 31

8 6

4 30

8 12

R

4 29

8 16

5

290

9 L

6

302

12

11

287

13

R

21

324

21

15

300

18

L

18

326

20

11

301

18

4 44

-3

0.1

2 40

.3

0.6

4 43

.5

0-2

2 40

.0

0.0

6 46

-2

0-5

7 41

.0

0-3

5 47

-7

0-4

6 41

-0

0.2

4 43

.3

0-4

7 38

.7

0.1

5 42

-8

0.3

12

38-0

0-

2

21

46-7

0.

3 16

40

.6

0-2

17

45.5

0.

3 12

40

.9

0.3

4 3.

66

0.02

1

3.66

0.

00

3 3.

39

0.05

2

3.25

0.

04

6 3.

03

0.06

5

2.89

1.

66

3 2

-91

0.

04

4 2.

38

0.08

4 2.

86

0.04

5

2-87

0-

06

6 3.

68

0.11

11

2.

75

0-05

21

2.88

0.

05

15

2.40

0-

05

18

2.90

0.

05

11

2-40

0.

06

6O8

Table 2

P. SMITH E T A L .

Frequency of osteoporot ie humer i* in different g roups

Males Females

Group Side No. examined % osteoporotic No. examined % osteoporotic

Natufian R 10 0 9 0 I, 11 0 12 17

MBI R 8 12 12 18 L 12 0 11 27

Roman/Byzantine R i 0 0 12 25 L 14 14 19 26

Early Arab R 23 5 17 53 L 21 13 14 43

* Osteoporosis delined as present where CCT = 7"0 or less.

obtained tbr the larger humeri of the Arab group. Male Natufian CCT values are not only significantly higher than those of any of the groups studied here, they are also significantly higher than those of adult males in living populations of Caucasians or Negroids which have mean values of 10"0 mm (Bloom et al., in prep.). Female Natufian CCT values, although significantly higher than those of the Roman/Byzantine and Early Arab samples, are comparable with C C T values obtained for female Caucasians and Negroids in the 20-49 year age group (8"6 ram) studied by the same authors.

In the males, the chronological differences observed in C C T are due to the exceptionally high mean values recorded in the Natufians, with later groups showing no significant change over time, and C C T values in them all comparable to those of living populations. In the females, Natufian females fall within the range of normal values characteristic of living populations, while C C T values in the Roman/Byzantine and the MBI to Early Arab t~males are markedly osteopenic in comparison to the same standards. The question then arises as to the contribution of differences in function, health status and gene pool to the findings observed here.

Ethnographic data on contemporary hunters and gatherers (Lee & De Vore, 1968) indicates that use of missiles in large game hunting is an exclusively male occupation. Such hunting at close quarters in the absence of long-range weapons requires considerable expenditure of strength as well as agility. As previously described, this type of hunting seems to have been practiced by the Natufians. Functional differences both between the two sexes in Natufian society and between male Natufians and male agriculturalists were then presumably greater than functional differences between females in the same societies, as collecting was replaced by farming.

The findings for C C T obtained in this study do demonstrate more extreme dimorphism in the Natufians than in the other groups examined. They also suggest that at least in relation to norms derived from living populations, the Natufian males have exceptionally high CCT values. The additional finding, that differences between the Natufian males and other groups are greater for the right arm than for the left arm, provides further support for the hypothesis that functional differences contribute to the group differences in CCT.

In the females it is the Roman/Byzantine and Early Arab groups that deviate from the norms of living populations, with C C T values lower than those of living urban populations. It is unlikely that function in the populations sampled by us was less than that of these

H U M E R A L C O R T I C A L T H I C K N E S S 609

l iving u rban groups, so that funct ional differences would not seem to explain the observed differences in C C T values.

Hea l t h s tatus of Nea r Eas te rn Chalco l i th ic and la ter popula t ions has been found to be poorer than tha t of the Natuf ians (Smith et al., 1984). Th is f inding is based on changes in the prevalence of deve lopmen ta l lesions such as denta l hypopas i a and growth ar res t lines, as well as on the incidence of c r ibra orb i ta l ia and other pathological lesions. I t has been sugges ted that increase in g roup size and poor sani ta t ion in sedentary popula t ions may have con t r ibu ted to an increase in the endemic disease load. I t has, however, also been pos tu la ted tha t the assoc ia ted changes in diet may have also affected hea l th status. Inc reased rel iance on cereals, a ccompan ied by reduct ion in the quant i ty of p ro te in and range of food staples ut i l ized has been inferred from the archaeological record and early wri t ten sources. Cereal foods are not only a poorer source of prote in and minerals , but in addi t ion , unrefined flour has a high fiber, phy ta te and phosphorus content that cont r ibu tes to minera l deple t ion (Re inhold et al., 1981). In I r an ian communi t ies where f la tbread made from lightly mi l led flour is one of the main d ie ta ry staples calc ium deficiency has been noted in chi ldren (Reinhold et al., 1973). No overt cases of rickets or os teomalac ia have been found in any of our series (Smith et al., in prep.) , however, in pat ients suffering from tuberculosis , os teopenia is c o m m o n dur ing the ma in chi ldbear ing years (Bocquet & Bergat , 1977; Bloom et al., in prep.) . In the R o m a n / B y z a n t i n e and Ear ly A r a b women s tudied here, the deleter ious effects of a high cereal diet may have been agg rava t ed by negat ive ca lc ium ba lance associa ted with p regnancy and lacta t ion to cause the observed osteopenia .

Th is s tudy was suppor t ed by a g ran t from the Israel A c a d e m y of Sciences.

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