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Comparison of radiologic and gross examination for detection of cancer in defleshed skeletons.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 96:357-363 (1995)
Comparison of Radiologic and Gross Examination for Detection
of Cancer in Defleshed Skeletons
BRUCE M. ROTHSCHILD AND CHRISTINE ROTHSCHILD
Arthritis Center of Northeast Ohio, Youngstown, Ohio 44512; Department
of Medicine, Northeastern Ohio Uniuersities College of Medicine,
Rootstown, Ohio 44272; Department of Biomedical Engineering,
University of Akron, Akron, Ohio 44242; The Carnegie Museum,
Pittsburgh, Pennsylvania 15213; and Kansas Museum of Natural
History, Lawrence, Kansas 66045
KEY WORDS
X-ray, Skeletal pathology, Cancer, Metastasis
ABSTRACT
The reliability of visual examination of defleshed bones was
assessed for detection of postcranial metastatic disease in individuals known
to have had cancer. This was compared with standard clinical radiologic
techniques. The skeletons of 128 diagnosed cancer patients from an early 20th
century autopsied skeletal collection (Hamann-Todd Collection) were examined. Radiologic examination detected evidence of metastatic disease in 33
individuals, compared to 11 by visual examination of the postcranial skeletons. Four of these cases were detected by both techniques. Blastic lesions
were most commonly overlooked on visual examination, because they were
localized to trabecular (internal bone) structures. The ilium was the most
commonly affected bone, with lytic or blastic lesions detected in 30 of 33
individuals. While the proximal femur was affected in only nine individuals,
x-ray of the proximal femur and ilium detected all individuals with postcranial evidence of metastatic disease. Skeletal distribution of metastases provides no clue to the location of origin or histologic subtype of the cancer.
Survey of archeological human remains for metastatic cancer requires radiologic examination. Such skeletal surveys should x-ray at least the ilia and
femora. 0 1995 Wiley-Liss, Inc.
Because bone is secondary only to lung
and liver as a site of metastasis (Alvarez,
1948; Abrams et al., 1950; Wierman et al.,
19541, study of skeletal populations should
be a reasonable approach to determining the
presence of cancer in antiquity. The relationship of malignancy to environmental
conditions and occupations allows the anthropologist another tool with which to further characterize prehistoric living conditions. Presence and extent of cancer
provides insights to support networks (familial and community-based). Metastatic
cancer has, however, only sporadically been
recognized in archeologic human remains
(Allison et al., 1980; Grupe, 1988; Manchester, 1983). Such reports were premised on
initial visual recognition of pathology. Systematic archeologic human radiology does
0 1995 WILEY-LISS. INC
not appear to have been pursued. Given the
critical role of skeletal x-rays in clinical evaluation for presence of metastatic disease, it
seemed appropriate to radiologically assess
a well-defined skeletal population with cancer.
Metastatic cancer typically appears as
multiple holes (lytic areas) or areas of increased density (blastic areas) of quite variable size (Huvos, 1991; Kim and Barry,
1964; Resnick and Niwayama, 1988). Although metastatic disease has been reported in archeological human remains
Received February 21,1994; accepted October 19,1994.
Address reprint requests to Bruce M. Rothschild, Arthritis
Center of Northeast Ohio, 5701 Market Street, Youngstown,OH
44512.
358
B.M.ROTHSCHILD AND C. ROTHSCHILD
(Ortner and Putschar, 1985; Steinbock,
1976; Tkocz and Bierring, 1984), findings
have been predicated upon visual recognition (usually with subsequent radiologic
confirmation), The sensitivity of visual examination of defleshed bones for detection of
postcranial metastatic disease has not been
previously assessed.
The current study was initiated t o determine the relative sensitivity of visual and
radiologic examination for detection of metastatic cancer. Given the expense of radiologic evaluation, it was further desired to
identify which bones must be x-rayed (to assure that all individuals in the population
with metastatic disease would be identified).
The skeletons of diagnosed cancer patients from an early 20th century, autopsied
skeletal collection (Rothschild and Woods,
1991) were therefore examined for evidence
of visible and radiologic skeletal alterations.
METHODS
Defleshed, postcranial skeletal remains of
129 autopsied individuals with documented
cancer were examined. These were identified from the Hamann-Todd Collection
(Cleveland Museum of Natural History)
compiled by T. Wingate Todd between 1913
and 1933. The skeletons (484 women, 2422
men) were derived from cadavers of unclaimed status which, after autopsy (including histologic study), were subjected to defleshing (with sodium hydroxide to remove
soft tissues). The medical condition and
cause of death records attended most of the
individuals. The Hamann-Todd Collection is
the world's largest and best preserved collection of human skeletons for which a demographic background is known (Rothschild and Woods, 1991; Rothschild and
Martin, 1993). The representatives of this
collection has been documented in multiple
studies (Mensforth and Latimer, 1989;
Rothschild and Woods, 1991; Rothschild et
al., 1990; Shaibani et al., 1991).
Age and sex noted in the medical records
were confirmed, as described previously
(Rothschild et al., 1990). The skeletal remains were examined visually t o identify all
occurrences of osseous alterations, to specify
the types of bony alterations a t each occurrence, and to map the distribution of occur-
rences in each skeleton. Lesions were distinguished from artifact, as previously described (Rothschild et al., 1990). In the event
of disagreement as to whether a lesion represented erosion or artifact, for the purpose
of this study it was treated as artifact.
Radiographs and fluoroscopy of the entire
skeleton of each individual were obtained
with the bones arranged and oriented approximately as they would be in living patients. Fluoroscopy of all postcranial skeletons was performed using the Xi Scan 1000
fluoroscopy/digital storage system (X-Tech
Inc., Randolph, NJ). All radiologic evaluation was performed in a blinded manner,
without knowledge of the presence or absence of visible evidence of metastatic disease in any other portion of the skeleton.
One individual placedmanipulated the
bone(s), while the other solely viewed the
resulting image.
The Chi-square statistic was utilized to
assess if there was a significant difference in
recognition of metastatic osseous disease by
visual examination and radiologic techniques. The representativeness of the individuals evaluated was also investigated by
comparison of frequency and distribution
with that reported in the literature (Chi
square, P < 0.05).
RESULTS
Demographics
One hundred twenty-nine individuals
(4.3%)in the Hamann-Todd Collection had
diagnosed cancer. Ninety-eight men (4.0%of
the total Hamann-Todd Collection human
male component) and 30 women (6.2%of the
female component) had diagnosed cancer,
for a female predominance of 1.51. The ratio
was calculated on the basis of percentage of
women affected (from the 484 at risk [number of female skeletons represented]) versus
the percentage of men affected (from the
2,422 at risk). The average ages of affected
men and women were also indistinguishable
(61.0 and 60.3, respectively).
Radiologic-visualcomparisons
Radiologic examination revealed cancer in
33 individuals, compared to 11 individuals
by visual examination. The detection rate
of radiologic examination was three times
that of visual examination (Chi-square,
RADIOLOGIC DETECTION OF METASTATIC CANCER
Fig. 1. Lytic metastatic ilia and rib lesions. A Lytic iliac lesions with un-sharpborders (Hamann-Todd
Collection No. 2645). B Lytic iliac lesions with more sharply defined borders (Hamann-Todd Collection
No. 788). C: Lytic rib lesions (Hamann-Todd Collection No. 788).
359
B.M. ROTHSCHILD AND C. ROTHSCHILD
360
Fig. 2. Blastic metastatic ilia and rib lesions. A: Pure radiodense (increased blockage of x-ray beam,
producing dark image on x-ray), blastic rib lesion (Hamann-Todd Collection No. 1670). B: Radiodense,
blastic iliac metastases with associated lytic involvement (Hamann-ToddCollection No. 217).
TABLE I . Prevalence (number (percent7) of grossly visible and radiologically detected mefastatic disease in
Hamann-Todd Collection cancer individuals
Tumor
Clinically
diaenosed
Stomach
Lung
Colon
hostate
Breast
Esophagus
Pancreas
Urethrabladder
Uteruslcervix
Undetermined
I Not
32
8
7
3
8
5
5
6
10
35
All
1 (3)
3 (38)
0
1 (33)
1 (13)
0
0
1 (33)
1 (10)
3 (9)
Visual detection
Only'
Total
0
3
0
0
1
0
0
1
1
7
9 (28)
3 (38)
2 (29)
1 (33)
2 (25)
3 (60)
2 (40)
0
0
12 (34)
Radiologic detection
Blastic
Lvtic
4
5
0
1
3
0
0
1
2
2
1
2
0
1
0
0
4
-
Total
detection
1
0
8
recognized radiologically.
P < 0.001). Radiologically, the lesions in 23
individuals were lytic (Fig. 1)in nature, while
12 were blastic, occasionally with mixed patterns (Fig. 2). Lesions were irregular in outline (withoutdiscernable pattern). Metastatic
cancer was detected in four individuals by
both techniques (visible examination and
x-ray).The frequency, percentage of cancer occurrences by site of cancer origin, and type of
radiologic reaction are delineated in Table 1.
The site of origin or histologic subtype of the
cancer was not identified in 26% of individuals with metastatic bone disease in the Hamann-Todd Collection.
The distribution of skeletal involvement is
listed in Table 2. Vertebral lesions were less
frequently detected radiologicallythan visually. No relationship was noted between distribution of metastatic disease and the location of the initial cancer or its histologic
RADIOLOGIC DETECTION OF METASTATIC CANCER
TABLE 2. Distribution of visible and radiologic
skeletal metastases in the Humann-Todd Collection and
clinical literature
Site
Vertebrae
Pelvis
Ribs
Femur
Tibia
Scapula
Humerus
Radius
Clavicle
X-ray
Number
Percent
4
30
5
9
1
2
3
1
1
Visible
(%)
Literature'
12
91
15
27
3
45
64
21
69
6
9
18
18
3
3
0
0
36
9
41
25
25
3
6
10
0
0
361
nation, because most appear localized to
trabecular structures. Visual and radiologic
examination are complementary. We suggest, therefore, that study of cancer in the
skeletal record should use both approaches.
Because ilia or proximal femur were concommittently affected (radiologically) in all
individuals with any evidence of metastatic
disease (radiologically), it would seem that
at a minimum, any metastatic disease survey should include their x-rays.
Representatives of findings
Radiologic evidence of metastatic bone
disease in 26% of the Hamann-Todd Collecsubtype. Ninety-one percent of recognized tion falls well within the 7-27% range reradiologic metastases were identified on ported by Copeland (1964). The detection
x-ray of the ilia. Femoral metastases were frequencies by combined visible and radioradiologically detected in four individuals logic examination were also indistinguishwho had no evidence of metastatic disease able for the various tumors (Chi square,
on pelvic x-rays. All individuals with radio- P > 0.05) from those reported from clinical
logically detected metastases had involve- and autopsy studies (Clain, 1965; Tubianament of the ilia and/or femora.
Hulin, 1991). The pattern of distribution of
metastatic disease (Table 2) also proved inDISCUSSION
distinguishable from that reported in the litOnly 33 of 128 Hamann-Todd Collection erature (Clain, 1965). Thus, the representaindividuals with diagnosed cancer had ra- tiveness of the Hamann-Todd Collection
diologically recognizable skeletal alter- (Mensforth and Latimer, 1989; Rothschild
ations. The detection rate of radiologic ex- and Woods, 1991; Rothschild et al., 1990;
amination was three times that of visual Shaibani et al., 1991)is further documented.
Two apparent discrepancies between clinexamination (Chi square, P < 0.001). Although Ortner and Putschar (1985) sup- ical and radiologic detection of cancer in deported visual inspection for detection of fleshed bones must be addressed. Clinical
presence of cancer in osseous remains, their localization of vertebral metastases is freconjecture was not based on systematic skel- quently based on isotope bone scans, rather
etal radiology. Their radiologic evaluation than x-rays. Bone scans are more sensitive
was apparently limited to individuals (per- for detection of vertebral metastases (Resnick
haps even limited just t o visually affected and Niwayama, 1988). Increased radiologic
bones of individuals) with visual evidence of detection in the defleshed pelvis is probably
cancer. The current study confirms their no- related to lack of interference by soft tissues
tation that some visually detected lesions (as in the intact individual). Subtle changes
were not seen on x-ray. Because there must Seen on x-ray of defleshed bones are o h n not
be a 3050% increase or decrease of bone visualized in the intact specimen (Rothschild
density before it can be recognized radiolog- et al., 1990).
ically (Resnick and Niwayama, 1988; RothsRelationship of radiologic finding to
child and Martin, 1993), it is not surprising
variety of cancer
that all visually detected lesions cannot be
detected in this matter.
No relationship was noted between distriHowever, if visual inspection is the only bution of metastatic disease and the location
technique utilized, two thirds of metastatic of origin or histologic subtype of the cancer.
disease would have been missed in the Ha- This corroborated the observations of Wilmann-Todd Collection. Metastatic blastic le- son and Calhoun (1981) and Morgan et al.
sions especially are missed by visual exami- (1990) that the skeletal distribution of sites
'Chin. 1965.
362
B.M. ROTHSCHILD AND C. ROTHSCHILD
of metastasis was independent of tumor histologic type or tissue of origin. The skeletal
distribution of metastases provides no clue
to the site of origin or histologic subtype of
the cancer.
archeologic populations. As this can be accomplished using one 14 by 17-inch x-ray
plate to obtain a single anterior-posterior
view, this should meet the need for a costeffective approach.
Differential diagnosis
ACKNOWLEDGMENTS
We acknowledge the kindness of Drs.
Bruce Latimer and Lyman Jellema and the
Cleveland Museum of Natural History for
cogent comments and for logistical and technical support in examining The HamannTodd Collection, and David Vargo of %-Scan
for providing the fluoroscopy equipment.
Distinguishing the lytic lesions of cancer
from those of multiple myeloma (plasma cell
dyscrasia), lymphomas, and hematologic
malignancies is another subject for future
investigation. The lesions of multiple myeloma are typically considered to produce
sharply defined lytic or (rarely) blastic lesions, all comparable in size (Resnick and
Niwayama, 1988). The lesions of metastatic
cancer are generally thought to blend with
surrounding bone, with great variability of
size of individual metastases in a single individual (Resnick and Niwayama, 1988).
However, notation in diagnosed multiple
myeloma of lesions of variable size (unpublished observations) and of “punched out”
(sharply defined) lesions in diagnosed metastatic cancer preclude its use to distinguish
between the two phenomena.
Presence of lytic lesions in defleshed skeletons allows consideration of metastatic
cancer, but hematologic malignancies, multiple myeloma, lymphomatous disorders,
granulomatous infections (e.g., fungal, mycobacterial [such as tuberculosisl, brucellosis), and even treponemal disease must also
be considered (Resnick and Niwayama,
1988; Rothschild and Martin, 1993; Rothschild and Turnbull, 1987). The latter are
typically associated with characteristic patterns of periosteal reaction, which should allow easy discrimination (Rothschild and
Rothschild, 1994).
Implications
Radiologic examination must accompany
visual examination of skeletons if the epidemiology of metastatic disease is to be reliably determined in archeologic human remains. The expense of total skeleton
radiologic surveys must be overcome for routine radiologic examination of the entire
skeleton of archeologic human remains to
become practical. X-ray of ilia and femora
(Table 2) would seem the minimum required
to detect presence of metastatic disease in
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