bilateral absence of the lesser trochanter in a late epigravettian skeleton from arene candide...

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 83:42,5-437 (1990)

Bilateral Absence of the Lesser Trochanter in a Late Epigravettian Skeleton From Arene Candide (Italy)

VINCENZO FORMICOLA, DAVID W. FRAYER, AND JULIE A. HELLER Sezione di Antropologia, Dlartimento di Scienze del Comportamento Animale e dell’Uomo dell’ niversita, 56100 Pisa, Italy (V.F.); Department ofdnthropology, University of Kansas? Lawrence, Kansas 66045 (D.W.F.); Department of Anthropology, IJniversity of New Mexico, Albuquerque, New Mexico 87131 (J.A.H.)

KEY WOfiIhs’ Paleopathology, Late Upper Faledithic, Arene Candide, Avulsion fracture, Femur

ABSTRACT A virtually complete skeleton recovered from excavations in a Late Upper Paleolithic context by Cardini between 1940 and 1942 at the Arene Candide cave (NW Italy) lacks the normal development of the left and right lesser trochanters. The specimen is a short-statured male about 25 years old and shows no other especially peculiar skeletal irregularities, except for high negative angles of femoral torsion. We discuss a number of possible etiologies for the anomalous absence of the lesser trochanters. The condition is most likely a result of an epigenetic effect or a traumatic avulsion of both lesser trochanters. If the absence of normal development of the lesser trochanters involves a congenital condition, it is an extremely rare, previously undescribed trait. If the condition results from bilateral traumatic avulsion, it is probably the result of excessive muscular stress on the proximal femur and provides further evidence of hardship of life in Paleolithic populations and of the ability of these people to survive debilitating trauma.

Arene Candide is a large cave on the Lig- urian coast near Finale Ligure in northwest Italy. Excavations by Bernabo Brea (1946, 1956: and Cardini in the early 1940’s and again in 1970 (1946, 1980) produced a rich archaeological assemblage with multiple archaeological levels, running from the Gravettian phase of the Upper Paleolithic to the Romaflyzantine period. Numerous skeletal remains were found scattered through these strata, with a single burial from the Gravettian level and about 20 individuals from the late Epigravettian period. The ori ’nal description of the Epigravettian level ( # ) referred to this zone as Mesolithic or Holocene (Cardini, 1946, 1980; Oakley et al., 1971) based on the high frequency of temperate fauna and C1* dates of about 10,000 B.P. (Alessio et al., 1966). Frayer (1978, 1981, 1984), Mussi (1986), and Paoli et al. (1980) followed this Mesolithic attribu- tion, but evaluation of the avifauna (Cassoli, 1980) and new radiocarbon dates for level M ranging between 10,910 i: 90 B.P. and

11,750 ? 95 B.P. (Bietti, 1987) indicate that the material is best considered as terminal Upper Paleolithic.

Much of the skeletal material from level M derives from prepared graves located near the eastern part of the cave. Pierced deer teeth, pendants and other evidence of per- sonal adornment, perforated shells, oblong pebbles, red and yellow ochre nodules, and diffuse animal bones are abundant in graves of infants and adults. Single and multiple interments occur in level M, the graves were generally delimited by stones, and most individuals were buried in the supine position with the u per limbs extended along the

heavy concentration of red ochre on all the human bones attest to the importance of complex mortuary practices in the Paleo- lithic levels (Mussi et al., 1989).

hips. Buria lp position, gravegoods, and the

Received January 3,1990; accepted April 17,1990

0 1990 WILEY-LISS, INC

426 V. FORMICOLA ET AL

Formal description of the E igravettian human remains was publishe 8 by Parenti (1946a) and Paoli et al. (1980), but these authors do not mention the anomaly re- viewed here. Additional material has been recently described by Formicola (1986a,b) and Formicola and Scarsini (1987).

DESCRIPTION OF ARENE CANDIDE 2

The specimen buried in Tomb 2 was dis- covered by Cardini between 1940 and 1942 lying on its back with the head turned to the left, and all bones heavily stained with red ochre (Fig. 1). Stones of various sizes v;ere placed at the lower periphery of the grave, near the right shoulder and head. Two lines of large stones arallel the length of the

incomplete at the left lower and right upper extremities. Associated with the skeleton were perforated marine shells of Patella, Nassa, and Pectunculus, two semi-lunar, polished fragments of Pectunculus, two round, flat stones stained with red and yellow ochre, and two small blocks of hematite (Cardini, 1980). Burial treatment is similar to other individuals at the site (Mussi, 1986:552), although this grave lacked deer tooth pendants, oblong pebbles, and animal bones.

The skeleton is nearly complete, with only minor damage (which has been reconstructed with plaster) affecting some skeletal elements. Based on the form of the pubic symphysis and sciatic notch, the individual was clearly male, although cranial features

body, forming si c! es of a tomb which is only

are gracile (e.g., the mastoids and brow- ridges are small), more typical of a female (Paoli et al., 1980; Frayer, pers. observ.). The long bones are also short and stature is reconstructed between 163 and 165 cm, which is small for male specimens deriving from the Late Upper Paleolithic (Formicola, 1983; Frayer, 1981). Despite some incongru- ence between the sex determined from the elvis and that from the skull and body size,

Lke Paoli et al. (1980:43), we consider the specimen a male. Based on the fusion of all but medial clavicle epiphyses, sternal rib caditinn, r b i c symphysis morphology, and moderate ental wear, age is estimated at about 25 years.

During the course of measuring the specimen at the Museo Civico di Finale Ligure (Savona) we noted that both femurs lacked normal development of the lesser trochanters. On the left in the place of a lesser trochanter is a -40 mm-long, sagitally ori- ented ridge which projects only slightly (<5 mm) in the dorsal-medial direction (Fig. 2a,c). The superior portion of this ridge blends into the intertrochanteric crest and its inferior aspect ends in the medial branch of a weak linea aspera. There is a shallow depression on the anterior medial aspect of the ridge which contributes to some dorsal- medial projection of the region. However, the slight accentuation of this region by a small tubercle-like projection does not come close to a proximating the normal projection of

somewhat resembles the juvenile condition, the P esser trochanter. In general, this area

Fig. 1. Arene Candide 2 in its reconstructed grave as exhibited at the Museo Civico di Finale Ligure (Savona).

ABSENCE OF LESSER TROCHANTERS

Fig. 2. Posterior and medial views of the proximal femur of Arene Candide 2. A Left posterior. B: Right posterior. C: Left medial. D: Right medial.

427

428 V. FORMICOLA ET AL.

before the fusion of the epiphysis for the lesser trochanter, yet there is no indication of an epiphyseal plate nor a remnant of an ossification junction. On the right side (Fig. 2b,d), the morphology close1 matches

ridge is interrupted by a postmortem break (and plaster reconstruction) along its inferior border. In the -20 mm present, the ridge takes the appearance of a small tubercle with a dorsal-medial projection? accentu- ated by a shallow depression anterior to the ridge. As on the left, the ridge is situated lateral to the medial waii ofthe femoral shaft and in a location approximating the position of a normal1 developed lesser trochanter. This bilaterafabsence of the lesser trochanters is not the result of postmortem breakage, since the periosteal surface is intact, and evidence is clearly present for a muscular insertion along the low ridges. Based on the morphology of this region, it appears that the psoas major and iliacus muscles inserted anomalously on the left and right sides.

Other than the absence of the lesser trochanters, the femurs and other skeletal elements show no especially peculiar metric or anatomical features, except for high angles of retroversion. Metric dimensions for Arene Candide 2 are compared to the male, female, and unsexed (combined) Late Upper Paleo- lithic sample (viz, dating after the Solutrean or less than about 18,000 B.P.) and to a “male only” Late Upper Paleolithic sample in Tables 1 and 2. Maximum femur length of 429 mm is shorter than the combined and the male Late Upper Paleolithic sample means, but within the male range. Limb ratios show

the general features of the left, alt yh ough the

no significant deviation from the comparative samples, although the crural index for Arene Candide 2 is just below the range of both samples. With the exce tion of the

the distance from the superior femur head to the middle of the lesser trochanter or, in this case, a proximately to where the middle of

Bramblett, 1988:229), all femur dimensions fall within the range of the combined Upper Paleolithic sample. The substantially longer Steele 1-2 dimension in Arene Candide 2 (taken on the left side) seems to indicate the iliopsoas muscle insertion was more distally located on the femoral shaft than in specimens with a patent lesser trochanter. Com- pared to the “male only” sample, the Steele 1-2 dimension remains long and outside the male range. Diaphyseal length, as measured between Steele’s points 2 and 4, is below the male minimum, again reflecting what would appear to be a lower iliopsoas muscle insertion point. Subtrochanteric cross sections and the circumference are not substantially different from either late Upper Paleolithic samples, while midshaft dimensions are con- siderably smaller than the male Late Upper Paleolithic sample and below the means for the combined sex sample. Femur neck diam- eters? maximum breadth of the gluteal tuberosity, and maximum shaft A-P are all at the lower end of the male Late Upper Paleo- lithic range.

While most femur shaft dimensions tend to be comparatively small, joint size of Arene Candide 2 is equivalent to (or larger than! the mean of the combined or male Late Vp-

Steele 1-2 measurement (whic K represents

the ri dp ge protmdes the most; Steele and

TABLE I. Maximum long bone lengths and limb ratios of Arene Candide 2 and the comparative samples

Late Upper Paleolithic Late Upper Paleolithic AC males, females and unknowns males2 21 Mean Range n Mean Range n

Limb lengths Maximum clavicle length 129 144 1119-1601 (15) 148 1135-1601 (9) Maximum humerus length 305 30 1 1262-3311 (21) 315 1297-3311 (10) Maximum radius length 237 235 1195-2531 (11) 248 1245-2531 (6) Maximum ulna length 244 259 1222-2771 (12) 268 1256-2771 (7)

Maximum tibia length 348 368 [334-4001 (14) 380 1365-4001 (9) Maximum fibula length 337 353 1327-3751 (9) 362 1351-3751 (5)

Maximum femur length 429 436 [370-4821 (21) 448 1408-4821 (15)

1,imh ratins . . .. . . . .

Humerus/femur 71.1 70.7 t66.8-74.71 (15) 70.4 [66.8-74.71 (10) Tibia/femur 81.1 84.5 181.3-90.51 (14) 84.9 [81.3-90.51 (9)

‘Average of left and right sides. “Not including Arene Candide 2

ABSENCE OF LESSER TROCHANTERS 429

TABLE 2. Metric dimensions of the femur and tibia for Arene Candide 2 and the comaarative samales

Late Upper Paleolithic Late Upper Paleolithic AC males, females and unknowns males2 2‘ Mean Range n Mean Range n

Femur dimensions Steele 1-2 Steele 2-4 Steele 4-5 Max. head circumference Perpendicular head diameter Max. head A-P diameter Min. neck perpendicular diameter Min. neck horizontal diameter Max gluteal tuberosity breadth Suhtrochanteric circumference Suhtrochanteric A-P Subtrochanteric M-I, Midshaft circumference Midshaft A-P Midshaft M-L Max. shaft A-P Bi-epicondylar breadth Max. distal articular breadth

Steele 1-2 Steele 2-5 Steele 5-6 Max. platform breadth Medial condyle length Medial condyle breadth Lateral condyle length Lateral condyle breadth Midshaft circumference Midshaft A-P Midshaft M-L Inferior articular facet A-P Inferior articular facet M-L

Innominate dimensions Acetahulum height Acetabulum breadth Pubis length Pubis breadth Pubis height

Tibia dimensions

86 301 42

160 48.6 49.3 30.8 24.7 8.6

94 26.2 35.1 84 26.9 25.5 29.9 84.8 77.0

27 304

19 78.2 49.1 31.4 42.6 34.2 87 33.9 18.8 32.9 34.2

57.5 56.2 68.2 13.1 19.2

71 327 38

146 46.0 45.6 29.8 23.7 10.8 YZ 25.9 3’2.5 87 29.2 26.1 29.6 82.6 71.6

29 331

16 72.5 43.7 31.8 41.0 31.6 83 30.8 20.6 29.4 29.2

53.8 50.6 62.3 15.9 16.0

[SO-781 [275-3681 131-431

[39.5-52.01 140.3-51.01

rl29- 16 11

125.2-33.91 120.3-29.81 17.9-15.51 LT4-LGTj

120.7-31.11 [26.1-38.91

[70-1031 [22.5-38.01 121.2-32.91 123.8-35.81 172.5-89.01 164.0-81.21

125-371 [303-3631 114-171

[66.9-76.61 139.7-46.91 [28.5-34.21 L38.8-43.11

167-971 125.7-42.01 115.5-26.01 124.6-34.01 [26.4-33.91

149.0-59.21 143.5-55.11 [53.3-70.71 113.6-19.81

126.3-37.31

111.4-19.11

74 340 39

155 48.7 48.1 32.7 26.6 11.4 3: 27.7 34.9 95 32.1 27.8 32.5 83.6 73.8

29 338

16 74.7 44.3 33.4 40.8 34.4 88 34.0 21.7 31.4 30.1

56.5 52.8 62.5 17.0 16.7

170-781 [312-368] 131-431

1147-1611 [45.9-52.01

[31.0-33.91 145.8-51.01

r24.1-29.81 [8.1-15.51 :a 1”;

125.0-31.11 129.1-38.91

[82- 1031 [27.9-38.01 122.7-32.91 128.6-36.81 [76.4-89.01 167.4-81.21

[27-341 1320-3631 [ 15- 171

171.2-76.61 139.7-46.91 132.2-34.21

131.6-37.41 t38.8-43.11

(78-971 [29.4-42.01 [19.1-26.01 [29.3-34.01 [27.4-33.91

[52.4-59.21 151.5-55.11 158.2-67.01 113.6-19.81 r 13.6-19.11

‘Left or right side depcriding on prwwrvatinr, and wconstructinn. 2Not including Arene Candide 2.

er Paleolithic samples. Maximum femur E ead circumference, A-P head diameter, and maximum articular breadth are near the top of the range of the male Late Upper Paleo- lithic sample. Large articular size is also shown by the acetabular measurements which exceed the means for the combined and male Late Upper Paleolithic samples (Table 2). Pubis length and ramus midpoint height are also above the male range, while the ramus midpoint anterior-posterior breadth is below the comparative sample ranges.

Femur indices of Arene Candide 2 further illustrate the specimen’s relatively large joint dimensions and relatively small neck

and shaft cross sections and circumferences (Table 3). Relative to maximum femur length, head circumference, maximum head diameter, and relative bi-epicondylar breadth in Arene Candide 2 are at the top (or above) the range of both the combined and male samples. Except for the subtrochanteric M-L and circumference dimensions, all neck and shaft dimensions for Arene Can- dide 2 are relatively smaller than Late Up- per Paleolithic males and generally below the means for the combined sample. Finally, the Arene Candide 2 femur shows greater flattening of the subtrochanteric region and greater rounding at the midshaft compared to the means of either sample.


In addition to these features, both femurs show a well-developed greater trochanter, inter-trochanteric line and crest, a narrow (but rugose) gluteal tuberosity, and a large adductor tubercle. Neckhhaft and bicondy- lar angles of -121" and -lo", respectively, are not abnormal, while the angle of torsion is eculiar in that the left is -9" and the rig K t is - 30". According to Brouwer's survey of 28 studies culled from the literature, (1981:35-36), angles of anteversion average "about 12"" with a range of -25" to 54" in recent Western European and North Ameri- caii adtilt f e m ~ ~ . Kate (1976) also reports 3 12" average in a large sample of East Indian femurs, with negative angles occurring in only 7% of his sample. Finally, Parenti (1946b) found an average of 19.4" with a range of +4-+40 in 50 modern adult Sicil- ians. Thus, the right side of Arene Candide 2 is somewhat anomalous, completely outside Parenti's reported range and slightly exceed- ing those published by Brouwer and Kate. Also, the high amount of negative torsion (retroversion) in this specimen is distinct from the other skeletal material from the site, since Paoli et al. (1980) report torsion

angles between 2" and 18" for all other adult femurs from Arene Candide. There is also some slight medial bowing of the shaft, and the linea aspera only barely rises from the rear face of the femur. The small posterior projection of the latter accounts for the comparatively low pilasteric index. The femurs, then, represent a mixture of robust and gracile features, although, individually, none of these (with the exception of the torsion angles) are strikingly aberrant compared to the bilateral absence of the lesser trochanters.

Compared to the femur, the tibia and fibula af Arene Candide 2 are much more robust. Both bones show pronounced muscular attachments represented by the very promi- nent inter-osseous crests, tibia1 anterior crest and popliteal line, and various fibular crests. Also, laterally positioned "squatting" facets occur on both tibias. Maximum lengths of the tibia and fibula are very short, both about 15 mm below the minimum of the male Late Upper Paleolithic range (Table 1) and about 20 mm below the means for the combined Late Upper Paleolithic sample. For the tibia, the reduced length in Arene Candide 2 seems to be primarily due to the

TABLE 3. Femur and tibia indices for Arene Candide 2 and the comparative samples

Late Upper Paleolithic Late Upper Paleolithic AC males, females and unknowns males2 Z1 Mean Range n Mean Range n

Femur Max. head circum./max. It. Max. head diameterimax. It. Nerk perpendicular dia.imax. It. Neck horizontal dia./max. It. Subtrochanteric circum./max. It. Subtrochanteric A-P/max. It. Subtrochanteric M-L/max. It. Subtrochanteric A-P/M-L Midshaft circum./max. It. Midshaft A-P/max. It. Midshaft M-L/max. It. Midshaft A-P/M-L Bi-epicondylar br/max. It.

Max. platform br./max. It. Medial condyle Wmax. It. Medial condyle br./max. It. Lateral condyle It./max. It. Lateral condyle br./max. It. Midshaft circum./max. It. Midshaft A-P/max. It. Midshaft M-Limax. It. Midshaft M-L/A-P Distal Articular A-P/max. It.

Tibia

37.3 11.3

1.L 5.6

21.9 6.1 8.2

74.6 19.6 6.3 5.9

105.5 19.8

22.5 14.1 9.0

12.2 9.8

25.0 9.7 5.4

55.5 9.5 9.8

- .- 33.8 10.6 6.9 5.6

21.2 6.1 7.5

79.9 20.5

6.9 6.1

121.1 18.6

19.8 11.9 8.7

11.1 8.7

22.9 8.3 5.6

66.8 8.1 7.9

[31.7-36.01 110 0-1151

u6.2-7.73 i5.1-6.7]

[ 19.5-24.21

l6.4-8.81 15.3-6.91

165.6-90.91 117.5-23.33

15.0-7.41

[16.3-19.91

[17.8-20.81

18.0-9.31

[5.3-8.51

193.3-135.71

[9.9-12.81

110.6-11.71 17.5-10.01

120. 1-25.11 [7.4-9.71 14.9-6.41

155.6-83.51 17.4-9.23 17.5-8.61

(10) 34.7 (11) 10.8 (8) 7.3 (9) 5.9

(121 21.4

[33.3-36.01 (6) [10.4-ll.5] (7)

i7.0-7.71 (4) i5.2-6.7; (4:

r 19.5-24.21 i 71 i i s i 6.2 [5.3-6.91' is j (16) 7.8 16.4-8.81 (9) (20) 79.8 165.6-90.91 (9) (18) 21.3 117.6-23.31 (11) (18) 7.2 (18) 6.3 (24) 116.3 (11) 18.8

(7) 19.9 (6) 11.8 (8) 8.9 (3) 11.1 (8) 9.2

(11) 23.4 (11) 8.7 (12) 5.6 (16) 63.5 (9) 8.2 (91 7.9

[5.8-8.9]- (11) 15.0-7.41 (11)

t16.3-19.91 (10) [93.3-135.71 (12)

[17.8-20.81 (4) 19.9-12.81 (4) 18. 1-9.31 (4) r 10.6-11.71

Distal Articular M-L/max. It. . , ' [7.5-8.51 'Left or right side depending on preservation and reconstruction. 'Not including Arene Candide 2.


short diaphyseal length (Steele 2-5), which is at the bottom of the combined sample range and well below the male range (Table 2). As in the femur, joint surfaces of the tibia generally are at (or above) the means of the combined and Late Upper Pa- leolithic samples, while midshaft dimensions are in most cases at (or below) these comparative sample means. Relative to maximum tibia length, greatest platform breadth, medial condyle length, lateral condyle length and breadth, midshaft A-P and circtmrference, and dist,al articular facet A-P and M-L lengths are each substantially greater than the male Late Upper Paleo-

generally at the top of

found separate from the femurs, it is doubtful they would have been associated with each other, given the great differences in indicators of muscu- larity and robusticity.

In addition to these features in the lower limb of Arene Candide 2, the specimen has a short (but robust) clavicle, and humerus, radius, and ulna maximum lengths which are well below the male Late Upper Paleo- lithic sample means (Table 1). Of these, only maximum humerus length falls within the male range. Extreme lateral bowing of the humeral diaphysis occurs bilaterally, and the distal end of the humerus is strongly bent in the anterior direction. The vertebral column is virtually complete from the atlas to the sacrum. In the lumbars the centrums ap ear small, but the transverse processes

are weli-developed. dhe sacrum is cranial- caudally elongated with a breadtMength index of 76.0, which is well below the mean (87.2) of four other adult s ecimens from the

ment shows some sign of being transitional between the lumbar and sacral column. Fi- nally, the talus, calcaneus, and other foot bones show no abnormalities or pathology.

iw R ere the psoas ma’or muscle originates!

site (Paoli et al., 1980). T I! e first sacral seg-

POSSIBLE DIAGNOSES The morphological features associated

with the bilateral absence of the lesser trochanters in Arene Candide 2 appear to have no modern analogue, either in the clinical experiences of orthopedists and radiologists or in the recollections (or collections) of osteologists we have consulted. Clearly, the absence of both lesser trochanters occurred well before the death of the individual, and

throughout his life the individual remained ambulatory, despite the anomaly. Below we discuss five possibilities which may account for this condition. Some appear to be more likely than others.

(1) Paralysis of the iliopsoas muscle The iliopsoas muscle is composed of two

parts, psoas major and iliacus, which merge to a common tendon inserting into the lesser trochanter with additional fibers extending along the femoral shaft just below the lesser trochanter. The separate muscles arise from the transverse processes, bodies and septa vf the 12th thoracic and all lumbar vertebrae (psoas major) or the internal iliac basin (iliacus). Both act to flex the thigh (Cartmill et al., 1987; Gray and Goss 1968). According to Keagy et al. (1966) the iliacus muscle is silent while sitting and standing, so that activity is associated only with deviations from the rest position. The role of the iliopsoas muscle as a hi flexor is evidenced by its

gait, but electromyography also shows some minor involvement in rotation, abduction, and adduction of the hip, suggesting a “sta- bilizing function” (Keagy et al. 1966:1382). The muscle set is innervated from the lumbar plexus by the femoral nerve along with fibers of L2-L3 (Gray and Goss, 1968:492.).

We have found no clinical description for the isolated paralysis of the iliopsoas muscle, and we suspect this is unlikely, given the source of innervation. If trauma (or possibly, some kind of tumor) occurred in the lumbar plexus, it would certainly affect other muscles in the lower limb; causing major defi- ciency in lower limb function. The radio- graphic evidence of Arene Candide 2 (Fig. 3) indicates normal anatomy in trabecular pat- terns, bone density, and cortical thickness of the roximal femur, so it is clear this individ-

immobilized. Additionally, the iliopsoas muscle origins are regularly developed on the lower vertebrae and pelvic basin, and there is a well-developed iliopsoas groove between the anterior inferior iliac spine and the iliopectineal eminence (Fig. 4). There is also a low ridge which apparently represents the insertion of the iliopsoas muscle in the region where the lesser trochanter should be located (Fig. 2). All these provide evidence for the normal development and activity of the iliopsoas muscle. In the absence of a realistic mechanism for partial (or complete)

very active state (f uring the swing phase of

ual K ad no major gait dysfunction nor was he


Fig. 4. dide 2.

Fig. 3. Posterior/anterior radiographs of left (a) and right (b) proximal femur of Arene Candide 2.

paralysis of the iliopsoas muscle and bilateral indications for presence of this muscle in Arene Candide 2, we conclude paralysis is an unlikely explanation for the absence of the lesser trochanters.

(2) Avascular necrosis The principal arteries supplying the lesser

trochanter region include the medial femoral circumflex and the trochanteric branches of the first perforating artery, a branch from the femoral artery (Howe et al., 1950). Given the extensive anastomosis of the arteries around the lesser trochanter, it seems unlikely that a cutoff of blood supply (due to a fracture) could affect the lesser trochanter alone. Loss of the blood supply to the femoral head can result in necrosis (Ortner and Put- . schar, 1981:237), for which there is no evidence in Arene Candide 2. Moreover the condition of the region where the lesser trochanters should be shows little resemblance to illustrations of necrosis by Ortner and Putschar (1981: Figs. 371-374). If the femoral artery was damaged or occluded, there

rest of the lower limb. Thus, there is no Medial view of left innominate ofhene Can- would likely be serious consequences for the


support for the notion that the absence of the lesser trochanters is due to avascular necrosis.

(3) Rickets Some aspects of the skeletal morphology of

Arene Candide 2 resemble the pathological effects of rickets. There is bilateral humeral bowing, some slight medial bowing of both femurs, enlargement of the metaphyses (com ared to the maximum long bone lengt K s), and minor frontal bossing. One other specimerr fran Arme Candide (#3) shows clear evidence of rickets (Formicola, ers. observ.), but for Arene Candide 2 these r! imited features make rickets a remote pos-

sibility. Despite the occurrence of a few rickets-like signs, the specimen shows no dental hypoplasia, little bowing of weight-bearing bones, no reduction in cortical and trabecular bone, no marked shortening of the femur, and no evidence of rib or vertebral deformities (see Ortner and Putschar, 1981:274- 280, 444). The only possibility of rickets ac- counting for the anomaly would be if the individual suffered a brief deprivation, which permanently interrupted the ossification (or fusion) of the lesser trochanter apophyses. Since the secondary ossification centers for the lesser trochanters appear in late childhood and fuse in late adolescence, a short bout of rickets would have had to occur during this developmental period. However, other secondary ossification centers (such as the humeral epicondyles) also ossify and fuse during the same develo mental episode, and

the lack of concordance with other similarly timed secondary ossification centers and mi- nor evidence of typical rickets skeletal mark- ers, this explanation appears unlikely.

(4) Genetic anomalyfdiscrete trait It is possible the missing lesser trochant-

ers in Arene Candide 2 are an epigenetic trait resulting from the absence of appearance (or bony development) of the secondary ossification center and the underlying su -

rare condition since it is not included in lists of postcranial non-metric traits (Finnegan and Faust, 1974; Finnegan, 1978) nor in McKusick’s (1986) most recent compilation of genetic anomalies. In addition, we consulted numerous human osteologists, radiologists, and orthopedic surgeons and none have encountered the condition. If the miss-

these show no unusua P morphology. Given

porting platform. If so, this is an extreme P y

ing lesser trochanters are the result of epigenetic variation, the trait appears to be limited to a bony abnormality and not to a failure in the development of the iliopsoas muscle, since, as discussed above, this muscle was patent. Finally, given the occurrence of other graves in level M at Arene Candide and the likelihood these individuals probably shared some type of kin relationship, if the anomaly is explained as a discrete trait, it mi ht be expected to occur in other skele-

(10 infants and adults), all other adults from Arene Candide have well-dt.v&qed lesser trochanters and skeletons of children show regular impressions of the lesser trochanter platform. It is also possible that the missing trochanters are related to a clinically (and osteologically) undescribed syndrome which includes the severe femoral retroversion, absence of the linea aspera, and relatively short diaphyseal length. While it is impossi- ble to eliminate this epigenetic explanation for the bilateral absence of the lesser trochanters, one of the authors (D.W.F.) feels this is an unlikely explanation.

(5) Trauma Avulsion of each lesser trochanter (not

necessarily simultaneously), followed by non-union of the apophysis and subsequent remodelling of the muscular attachment, is another possible explanation for this phe- nomenon. Fractures of the lesser trochanter are rarely (if ever) reported in paleopathological analyses; for example, this type of trauma is not mentioned in Ortner and Put- schar 119811 nor in a recent review of os- teoporotic fractures in the Hamann-Todd collection (Mensforth and Latimer, 1989). In orthopedic medicine Dimion (1972) has re- viewed evidence from 30 cases which primarily involved teenage boys. Avulsion also is reported for elderly individuals in associa- tion with inter-trochanteric fractures (Ku- mar, 1973; Norcross and Pearson, 1966), sometimes as a symptom of metastatic ma- lignancy (Adler, 1984; Bertin et al., 1984; Lower et al., 1988; Phillips et al., 1988; Wilkinson, 19791, and even as a conse uence of a severe coughing episode (Gradwo B 1 and Mailliard, 1987). Compared to other types of fractures, avulsion of the lesser trochanter is rare in orthopedic medicine. The majority of cases relate to extreme muscular exertion associated with sports activity when the apophysis pulls away from the growth plate

tons I ; rom the site. While this sample is small

434 V. FORMICOLA ET AL

(Resnick and Niwa ama, 1988). For exam- le, cases of these P ractures in the medical

Piterature involve a male tennis professional (Birnbaum, 19801, a “woman articipating actively in sports” (Elwart an B Urbanczyk, 1986), but most often boys playing running games (Dimion, 1972; Green and Gay, 1956; Lewin, 1928; Magistroni and Viscontini, 1964; Parisel, 1966; Poston, 1921; Sweet- man, 1972). Other causes, such as falling, pushing a wheelbarrow, doing cheerleading splits, and car accidents, have been associated much less frequently with lesser tro- chaatsrk dVu!Si9n (Dhhn, 1972). These h cidents were all limited to a single side, but Binazzi et al. (1986) report a case ofbilateral avulsion of the lesser trochanter (separated by an 8 month period) in a 16 year-old male related to running during a soccer match.

Avulsion fractures generally occur before the complete fusion of the secondary ossification center, which begins at about 17 years (Pugh, 1965). Muscular contractions or trauma detach the lesser trochanter epiphysis from the upper shaft by a few centimeters (Fernbach and Wilkinson, 19811, severing the insertion of the psoas major muscle on the lesser trochanter and affecting the insertion of the iliacus portion just inferior to the lesser trochanter. The traumatic injury involves severe pain in the hip, eventually leading to immobilization due to limited hip flexion, loss of medial rotation, and reduced weight-bearing on the fractured side (Dimion, 1972; Green and Gay, 1956). Treat- ment generally does not require surgery nor a cast; rather bed rest with the hip flexed at 90” for a couple of weeks followed by the use of crutches is the standard orthopedic prac- tice (Dimion, 1972; Green and Gay, 1956; Milch and Milch, 1959). In most of the reported cases, after recovery the lesser trochanter and iliopsoas muscle re-attach in their normal positions, but Birnbaum (1980:124) states that “nonunion of a small fragment” sometimes occurs. In general, the prognosis for recovery is excellent with the resumDtion of “normal activities. . . within 12 wkeks after the injury” (Dimion, 1972:248). ~~. . _ _ ~ _ , .

The main difficulty for accepting trauma as the cause for this bilateral condition is the complete lack of evidence for any re-attachment of the avulsed apophyses. However, certain features of the Arene Candide 2 femurs seem to accord with this diagnosis, if we accept the presumption that the detached

tendon re-inserted in the approximate position of the lesser trochanters. On both sides, evidence exists for muscular insertions near the region where the lesser trochanter should be located. These low ridges are slightly lateral and inferior to the normal insertions of the psoas major and iliacus muscles, but it is unlikely they represent bony landmarks for any other muscular ori- gin or insertion. If trauma was the cause of this anomaly, absence of periostitis suggests the injuries occurred long before death, and lack of osteoarthritic changes in the hip, knee, and foot indicate no long-term diszbil- ity. There is also no indication that more serious trauma (such as an inter-trochanteric fracture) was associated with the bilateral lesser trochanter injury. In addition, radiographs of the proximal femur (Fig. 3) show no evidence for impaired gait, even though the iliopsoas muscle re-attachment appears to have occurred in a more distal, lateral position. Compression and tension trabecular concentrations are present and are normal in their orientation and density. As discussed above, the femoral head, greater trochanter, and diaphyseal cortices appear well-developed, so Arene Candide 2 completely recovered from these bilateral fractures. High negative torsion angles may relate to some bony and muscular adjust- ments consequent to the bilateral avulsion, since Morscher argues that “[tlhere is no doubt that mechanical forces are responsible for the alterations of the anteversion angle” (1967:lll; his italics). Moreover, Kate (1976:463! reports that retroversion occurs “without exception in cases of united fractures of either the shaft or of the neck,” yet none of the femurs in his study included avulsion of the lesser trochanter. Given the high amount of retroversion, Arene Candide 2 likely had a “toe-out” gait pattern, and the extreme reduction in pilaster development coupled with tibiayfibular robusticity may be consequences of some minor locomotor abnormalities or biomechanical adjust- ments. Finally, given the young age of death for Arene Candide 2, complete healing of the fractures and absence of other pathological lesions suggest the bilateral avulsion is related to extreme muscular exertion and not to the onset of metastatic carcinoma.

CONCLUSIONS Paleopathological conditions occur with

some frequency in late Pleistocene skeletons


(e.g., Dastugue and delumley, 1976; Klima, 1987) and healed long bone fractures are not uncommon in Up er Paleolithic skeletal ma-

Barma del Caviglione has a healed, but malaligned fracture of the left distal radius (Verneau, 1906: plate 11, a male from Veyrier (#1) shows a healed, severely distorted fracture of the left tibia and fibula which certainly resulted in a pronounced limp (Pittard and Sauter, 1945; D.W.F., pers. observ.), the Oberkassel 1 male has a poorly aligned fracture of the right distal ulna (Bonnet, 1919; D.W.F., pers. observ.), and a young maie from Vado all’Arancio shows fractures of the left tibia1 and fibular malleolus (Minellono et al., 1980). These cases exemplify the vig- orous lifestyle of Upper Paleolithic individuals and their ability to survive traumatic injuries.

As for the precise etiology of the missing lesser trochanters in Arene Candide 2, it is difficult to completely eliminate either ge- netics or trauma. If the condition represents a congenital anomaly, it will be interesting to see if future workers can document a similar occurrence in other skeletal samples. For now, this explanation lacks other reported cases in the literature, but it could be an extremely rare anomaly, like the presum- ably genetic condition of bilateral aplasia of the humeral trochlea reported only once in the literature (McKusick, 1986) or uncommon cases of congenital absence of limb seg- ments (Ortner and Putschar, 1981).

If a diagnosis of bilateral avulsive fractures of both lesser trochanters is correct, the individual is another exampie of healed trauma in the Upper Paleolithic. Our most serious reservation concerning the “traumatic” diagnosis is the fact that the lesser trochanters are not re-attached as is the common outcome in medically treated cases. However, since the cases reported in the medical literature only concern treated inci- dents, it is difficult to predict from this literature what the condition would be if an individual did not undergo modern medical intervention. Given the anomalous insertion and the absence of evidence for an epiphyseal platform for the lesser trochanter, it seems very likely the bilateral trauma occurred sometime before the full ossification of the epiphyseal centers. According to Pugh (19651, ossification of the lesser trochanter begins at 11 years and remains incompletely fused until about 17. If trauma to the region

terial. For examp P e, the male specimen from

occurred before the full ossification of the lesser trochanter apophyses (whether simultaneously or separately over time) and modern medical procedures were not applied, it seems possible that the observed morphology could have been produced. For example, if the individual somehow was able to walk before the lesser trochanters could re- attach, the tendons for the iliacus and psoas major muscles may have re-attached in a broad band. Subsequent muscle pull could have remodelled the region, resulting in the morphology we describe. If this diagnosis is correct, the inctividuzf. .r?rou!d have heen mod- erately to seriously debilitated for about 3 months (according to modern recovery rates) and during this period would have required assistance from his local group during recu- peration. Arene Candide 2 completely recovered from the traumatic injury which would have had to occur some years before his death given the amount of remodelling. While it seems possible some of the idiosyn- cratic femoralkibial metric and non-metric variation of Arene Candide 2 (com ared to the two Late Upper Paleolithic samp 1; es) may be a secondary consequence of this trauma, this provides no evidence that the individual suffered any long-lasting disability.

AC~OWLEDGMENTS

We thank Dr. A. Gallina Zevi (Soprinten- denza Archeologica di Genova) for permis- sion to study this material and G. Vicino and 0. Giuggiola (Museo Civic0 di Finale Ligure, Savona) for their assistance in our examina- tion of the skeleton in Finale Ligure. We also appreciate information and critical input provided by S. Borgognini Tar-li, R. Caspari, J. Drennan, M. Finnegan, D. Hiebert, J. Long, T.E. Keats, B. Latimer, 0. Lovejoy, R. Mensforth, G. Paoli, E. Rustighi, 0. Serrato, K.E. Stoner, D.G. Steele, R. Tague, E. Trinkaus, and M.H. Wolpoff. Research support to V.F. from the Minister0 della Pub- blica Istruzione and to D.W.F. from the Na- tional Science Foundation (BNS 8419057) and the University Kansas General Re- search Fund is gratefully acknowledged.

LITERATURE CITED Adler C-P (1984) Case report 255. Skeletal Radiol.

Alessio M, Bella F, Bachechi F, and Cortesi C (1966) University of Rome carbon-14 dates IV. Radiocarbon 8:401-403.

Rernabo Brea L (1946) Gli Scavi Nella Caverna Delle Arene Candide. Bordighera: Istituto di Studi Liguri.

11 :65-68.


Bernabo Brea L (1956) Gli Scavi Nella Caverna Della Arene Candide. Campagne di Scavo 1948-50. Bordigh- era: Istituto di Studi Liguri.

Bertin KC, Horstman J , and Coleman SS (1984) Isolated fracture of the lesser trochanter in adults: An initial manifestation of metastatic malignant disease. J. Bone Joint Surg. [Am.] 66:770-773.

Bietti A (1987) Some remarks on the new radiocarbon dates from the Arene Candide cave (Savona, Italy). Hum. Evol. 2:185-190.

Binazzi R, DElia L, Vaccari V, and Cantagalli S. (1986) Su un caso di distacco bilaterale traumatic0 del piccolo trocantere. Ital. J . Sports Traum. 8:53-56.

Birnbaum DA (1980) Missed avulsion fracture of the lesser trochanter in a tennis professional. Med. Trial Tech. Q. 26:121-125.

bonnet R (i9i9; Die Skeiea. in Ti4 Verwni , B Buiiiiei, and G. Steinmann (eds.): Der Diluviale Menschen- funden van Oberkassel bein Bonn. Weisbaden: JF Bergmann Verlag, pp. 11-185.

Brouwer K J (1981) Torsional deformities after fractures of the femoral shaft in childhood. Acta Orthop. Scand

Cardini L (1946) Gli strati mesolitici e paleolitici della caverna delle Arene Candide. Riv. Studi Liguri 12:29- 37.

Cardini L (1980) La necropoli mesolitica delle Arene Candide (Liguria). Mem. 1st. Ital. Paleont. Umana (n.s.)3:9-31.

Cartmill M, Hylander WL, and Shafland J (1987) Hu- man Structure. Cambridge (MA): Harvard University Press.

Cassoli PF (1980) L'avifauna del Pleistocene superiore delle Arene Candide (Liguria). Mem. 1st. Ital. Paleon- tol. Umana 3:155-234.

Dastugue J , and deLumley M-A (1976) Les maladies des hommes prehistoriques du Paleolithique et du Mes- olithique. In H deLumley (ed.): La Prehistoire Fransaise. Paris: CNRS, pp. 611-622.

Dimion JH (1972) Isolated fractures of the lesser trochanter of the femur. Clin. Orthop. 82:144-148.

Elwart A, and Urbanczyk (1986) Czqsciowe oderwanie krqtarza mniejszego kosci udowej podczas porodu u kobiety czynnie uprawiajacej sport. Wiad. Lek. 39:1266-1269.

Fernbach SK; and Wilkinson RH i19811 Adsion inin-

[Suppl.] 195.

ries of the pelvis and proximal femur. Am. J . Radiol. 7.77.581 -584 - . . . - - . - -.

Finnegan M (1978) Non-metric variation of the infracra- nial skeleton. J . Anat. 125:23-37.

Finnegan M, and Faust MA (1974) Bibliography of Hu- man and Nonhuman Non-Metric Variation. Research Reports No. 14. Amherst: University of Massachu- setts.

Formicola V (1983) Stature in Italian prehistoric samples, with particular reference to methodological prob- lems. Homo 34:33-47.

Formicola V (1986a) Una mandibola umana dal deposit0 dell'Epigravettiano finale delle Arene Candide (Scavi 1970). Riv. Antropol. 64:271-278.

Formicola V (198613) Anthropologie dentaire des restes de l'lhieravettien final retrouves dans la Grotte des AreneClndide (Ligurie). Bull. Mein. SOC. d'hthropol. Paris (Serie XIV) 3:37-46.

Formicola V. and Scarsini C (1987) Contribution to the knowledge of the late Epigravettian human remains from Arene Candide cave (Liguria, Italy): a peculiar- shaped skull. Homo 38:160-170.

Frayer DW (1978) Evolution of the Dentition in Upper

Paleolithic and Mesolithic Europe. University of Kan- sas Publications in Anthropology, No. 10. Lawrence: University of Kansas.

Frayer DW (1981) Body size, weapon use and natural selection in the European Upper Paleolithic and Meso- lithic. Am. Anthropol. 83:57-73.

Frayer DW (1984) Biological and cultural change in the Euro ean Late Pleistocene and early Holocene. In FH Smiti and F Spencer (eds.): The Origins of Modern Humans: A World Survey of the Fossil Evidence. New York: Alan R. Liss, Inc., pp. 211-250.

Gradwohl JR, and Mailliard JA (1987) Cough induced avulsion of the lesser trochanter. Nebr. Med. J. 72: 280-281.

Gray H, and Goss CM (1968) Anatomy of the Human Body. Philadelphia: Lea & Febiger.

Grccr, JT, and G3y FE (19%) -4m!sior? of the lesser trochanter. South. Med. J. 49:1308-1310.

Howe WW, Lacey T, and Schwartz RP (1950) A study of the gross anatomy of the arteries sup lying the proximal portion of the femur and acetaiulum. J. Bone Joint Surg. [Am.] 32:856-866.

Kate BR(1976)Anteversionversus torsion ofthe femoral neck. Acta Anat. (Basel) 94r457-463.

Keagy RD, Brumlik J , and Bergan JJ (1966) Direct electromyography of the psoas major muscle in man. J . Bone Joint Surg. [Am.] 48:1377-1382.

Klima B (1987) Une triple sepulture du Pavlovien a Dolni Vestonice, Tchecoslovaquie. L'Anthropologie (Paris) 91:329-334.

Kumar V (1973) The syndrome of the fracture of the lesser trochanter in adults: a neglected aspect of the trochanteric fracture. Injury 4:327-334.

Lewin P (1928) Avulsion fracture of the lesser femoral trochanter. J. Bone Joint Surg. [Am.] 10:339-343.

Lower RF, McNiesh LM, and Callaghan JJ (1988) Ipsi- lateral lesser and greater trochanter fractures of the hip without intertrochanteric extension: a case report. Milit. Med. 153:421-423.

Magistroni A, and Viscontini GR (1964) Sul distacco isolata del piccolo trocantere. Minerva Ortop. 18:217- 219.

McKusick V (1986) Mendelian Inheritance in Man. Bal- timore: Johns Hopkins Press.

Mensforth RP, and Latimer BM i1989i Hamann-Todd collection aging studies: ostgoporo ture y y n - drome. Am. J. Phys. Anthropoi. 8U:4

Milch H, and Milch RA (1959) Fracture Surgery. New York: Hoeber-Harper.

Minellono F, Pardini E, and Fornaciari G (1980) Le se olture epigravettiane di Vado all'Arancio (2 rosseto). Riv. Sci. Preist. 35:3-44.

Morscher E (1967) Developmental and clinical signifi- cance of the anteversion ofthe femoral neck. Reconstr. Surg. Traumatol. 9:107-125.

Mussi M (1986) Italian Paleolithic and Mesolithic buri- als. Hum. Evol. 1:545-556.

Mussi M, Frayer DW, and Macchiarelli R (1989) Les vivants et le morts. Les sepultures Paleolithique su- perieur en Italie et leur interpretation. In I Hershko- vitz (ed.): People and Culture in Change. Oxford: BAR International Series (508i), pp. 435-458.

Norcross KN, and Pearson JR (1966) Movement of the lesser trochanter in pertrochanteric fracture. Post- grad. Med. J. 42:16-19.

Oakley KP, Cam bell BG, and Molleson TI (1971) Cata- logue of Fossf Hominids. Part 11: Europe. London: British Museum (Natural History).

Ortner DJ, and Putschar WJG (1981) Identification of


Pathological Conditions in Human Skeletal Remains. Washington, DC: Smithsonian Contributions to An- thropology 28.

Paoli G, Parenti R, and Sergi 5 (1980) Gli scheletri mesolitici della caverna delle Arene Candide (Liguria). Mem. 1st. Ital. Paleont. Umana 3:l-154.

Parenti R (1946a) Osservazioni sulle ossa lun he degli arti degli uomini mesolitici delle Arene Canfide. Riv. Studi Liguri 12:3&41.

Parenti R(1946b) Gli angoli di torsione e deviazione delle ossa dell'arto inferiore dell'uomo e loro rapporti reci- proci. Arch. Antropol. Etnol. 76:5-61.

Parisel F (1966) Fracture du petit trochanter chez le grand enfant. Acta Orthop. Belg. 32:423,424.

Phillips CD. Pope TL, Jones JE, Keats TE, and Mac- Millan RH (1988) Nontraumalii- wu!sion ef the lesser trochanter: a pathognomonic sign of metastatic disease? Skeletal Radiol. 17:106-110.

Pittard E, and Sauter M-R (1945) Un squelette magdale-

nien prouvent de la station des Grenouilles (Veyrier, Haute-Savoie). Arch. Suisses d'hthropol. Genet.

Poston H (1921) Traction fracture of the lesser trochanter of the femur. Br. J. Surg. 9:256-258.

Pugh DG (1965) Roentgenologic Diagnosis of Disease in Bone. Baltimore: Williams & Wilkins.

Resnick D, and Niwayama G (1988) Diagnosis of Bone and Joint Disorders. Philadelphia: WB Saunders.

Steele DG, and Bramblett CA (1988) The Anatomy and Biology of the Human Skeleton. College Station, TX: Texas A&M Press.

Sweetman R J (1972) Avulsion fracture of the lesser trochanter. Nurs. Times 68(41:122, 123.

Verneau R (1906) Les Grottes de Grimaldi (Baousse- Rousse). Tome 11, Fasc. I. Monaco: Imprimerie de Monaco,

Wilkinson RH (1979) Case Report 90. Skeletal Radiol.

11 :149-197.

4:99-101.

bilateral absence of the lesser trochanter in a late epigravettian skeleton from arene candide...

Documents