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Degenerative spondylolisthesis in ancient and historic skeletons from New Mexico Pueblo sites.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 116:285–295 (2001)
Degenerative Spondylolisthesis in Ancient and Historic
Skeletons From New Mexico Pueblo Sites
Charles F. Merbs*
Department of Anthropology, Arizona State University, Tempe, Arizona 85287-2402
KEY WORDS
olisthesis; osteoarthritis; lumbar; zygapophysial joints; disk degeneration;
vertebral shift; age; sex
ABSTRACT
The objective of this study was to identify
the presence of degenerative spondylolisthesis in adult
Native American skeletons recovered from prehistoric and
historic Pueblo sites in New Mexico. The vertebral columns of 491 individuals that were complete enough to
allow the necessary observations produced 64 cases, with
a total of 74 affected levels. The L5–S1 level was affected
most frequently (78%), in contrast to clinical and anatomical studies where the L4 –L5 level was usually affected
(80%). Age and sex were found to be important factors,
with the condition limited to middle and old adults, and
occurring in females over males at a ratio of approxi-
mately 5:1. Olisthesis was shown to occur only in association with severe osteoarthritis of the zygapophysial
joints, but severe osteoarthritis did not always result in
olisthesis, particularly in males. Parallel or convergent
inferior articular processes were found to increase in frequency in the presence of olisthesis, apparently resulting
from degenerative remodeling that produced the olisthesis. The data also suggest that individuals with cranial
border shifting in the column may be especially prone
to olisthesis. Degenerative olisthesis was also observed
in the cervical region. Am J Phys Anthropol 116:285–295,
2001. © 2001 Wiley-Liss, Inc.
Spondylolisthesis, derived from the Greek roots
spondylos (vertebra) and olisthesis (to slip), refers to
the anterior slippage of a vertebra relative to the
vertebra below (Merbs, 1996). Although known to
medicine since the early 19th century, the cause of
olisthesis was at first not determined. It was observed, however, that the superior surface of the
sacrum and the bodies of the lower lumbar vertebrae
were tilted forward and downward in humans when
the trunk is erect, allowing gravity to affect them.
Through careful dissection and removal of soft tissue, a Dr. Robert, working in Koblenz in the mid19th century, and known to history simply as Robert
zu Koblenz (Newell, 1995), demonstrated that under
normal circumstances it was impossible for a vertebra to slip forward as long as its neural arch was
intact (Robert, 1855). However, if the body became
separated from the arch, a condition now known as
spondylolysis, it was free to slip and could do so with
no greater force being applied than that equivalent
to the usual weight-bearing load of the affected vertebra. The potential for anterior slippage is particularly great in the lower lumbosacral region, where
the bodies are ventrally oriented downward and
gravity can work upon them. The degree of olisthesis
occurring varies greatly from one individual to another, ranging from none, or barely detectable, to
complete, the rare instance where the body of the
affected vertebra slips completely off that of the
vertebra below. In general, the slippage is not gradual but episodic in nature. In time, spondylolisthesis
as a sequel to complete bilateral spondylolysis be-
came easy to recognize and was observed to be a
relatively common phenomenon.
Cases were observed, however, where olisthesis
occurred in the absence of any arch defect. Junghanns (1931) referred to this as “pseudospondylolisthesis,” but the terms “spondylolisthesis with intact
neural arch” (Macnab, 1950) and “spondylolisthesis
without isthmus defect” (Potter and Norcross, 1954)
were also introduced. Subluxation or disarticulation
of the zygapophyses, or lengthening of the connection between the body and the inferior articular
processes through dysplasia or repeated fracturing
and healing, were seen as likely causes. A third,
more common cause, was anterior migration of the
zygapophyses due to severe osteoarthritic remodeling (Herron and Trippi, 1989). Newman (1955) referred to this as “degenerative spondylolisthesis,” a
term that was descriptive and specific enough to
gain wide popularity. Again it is the ventrally downward orientation of the vertebral bodies and the
force of gravity that generate the slippage, but as
opposed to olisthesis following lysis, the slippage
here is very gradual and much more limited in extent.
©
2001 WILEY-LISS, INC.
*Correspondence to: Charles F. Merbs, Department of Anthropology, Arizona State University, Tempe, AZ 85287-2402.
E-mail: Charles.Merbs@asu.edu
Received 24 January 2001; accepted 30 July 2001.
286
C.F. MERBS
Given its apparent cause, there is a temptation to
see degenerative spondylolisthesis as merely a severe form of osteoarthritis affecting the lower back,
particularly when considered entirely in its osteological context. Clinicians usually accord degenerative
olisthesis a separate status, however, because zygapophysial osteoarthritis, even when severe, does
not necessarily result in olisthesis, and because the
condition is associated with a specific cluster of
symptoms.
PREVIOUS STUDIES
Clinical studies demonstrated degenerative spondylolisthesis to be primarily a condition of older
adults. It is usually not observed before age 40
(Rosenberg, 1975; Bolesta and Bohlman, 1989; Herron and Trippi, 1989; Takahashi et al., 1990), with
most patients being in their sixties before they experience enough lower back pain to bring the condition to the attention of a physician (Rosenberg, 1975;
Epstein et al., 1983; Brown and Lockwood, 1983).
All studies agree that degenerative olisthesis occurs more frequently in women than in men (Rosenberg, 1975; Bolesta and Bohlman, 1989), but observed ratios vary from as low as 2:1 (Epstein et al.,
1983) or 3:1 (Potter and Norcross, 1954) to as high as
6:1 (Herron and Trippi, 1989). The higher frequency
in women suggests that pregnancy may play a role,
and this appears to be the case. Sanderson and
Fraser (1996) reviewed the records and radiographs
of 949 women and 120 men aged 50 years and over
who had received the attention of a spinal surgeon
for low back pain over a 5-year period, and found
that women who had borne children had a significantly higher incidence of degenerative olisthesis
than nulliparous women (28% to 16.7%). The men
they studied had a 7.5% incidence, significantly less
than for nulliparous women. These results suggest
that pregnancy is an important factor in the etiology
of degenerative spondylolisthesis, but that females
are still more prone to developing the condition,
even when the pregnancy factor is eliminated.
Because of the age factor, variable symptoms, and
complicating conditions, overall frequency values
are difficult to obtain. Potter and Norcross (1954)
found only 19 affected individuals in a review of
radiographs from 3,000 individuals, but their sample was skewed heavily in favor of the population
segment least likely to show the condition, i.e.,
young males. Racial comparisons are rare, with the
only agreement being that degenerative olisthesis is
more common in “Blacks” than in “Whites” (Rosenberg, 1975; Bolesta and Bohlman, 1989).
In a clinical study involving 200 patients, 80%
showed olisthesis at the L4 –5 level, 8% at L3– 4, and
11% at L5–S1 (Rosenberg, 1975), and other studies
confirmed that these frequencies are fairly typical
(Junghanns, 1931; Potter and Norcross, 1954; Epstein et al., 1983; Bolesta and Bohlman, 1989, Herron and Trippi, 1989; Takahashi et al., 1990; Postacchini and Perugia, 1991). Two levels were involved
in 5% of patients in two studies (Potter and
Norcross, 1954; Rosenberg, 1975), and 8% in another
(Takahashi et al., 1990).
A study of lumbosacral spines (L1 through S2)
collected at autopsy produced 19 cases of degenerative olisthesis: 18 at L4 –5, and 1 at L5–S1 (Farfan et
al., 1976). Degenerative olisthesis was also found in
20 skeletons of the Hamann-Todd Collection at Case
Western Reserve University, with L4 –5 being involved 18 times and L3– 4 twice (Rosenberg, 1975).
Stewart (1935) reported three archaeological cases
of olisthesis without lysis, one from Nunivak Island,
Alaska, involving L4 –5, and one each from Hooper
Bay, Alaska, and Hawikuh, New Mexico, involving
L5–S1. Although degenerative olisthesis is relatively easy to detect in archaeological skeletons, no
systematic studies of large series could be located.
Because the neural arch remains intact in degenerative olisthesis, the maximum amount of slippage
possible is considerably less than that following bilateral spondylolysis. Based on the percentage of
anteroposterior vertebral body diameter exposed by
the olisthesis (Laurent and Österman, 1976), a maximal slippage of approximately 30% is usually cited
(Rosenberg, 1975; Herron and Trippi, 1989), although a maximal slippage of 43% has been reported
(Postacchini and Perugia, 1991). At the minimum
end of the scale, olisthesis of less that 5% is often
excluded from studies because of the difficulty in
making such small measurements (2 mm) on radiographs (Rosenberg, 1975). One study found a mean
slippage of 14% among affected patients (Rosenberg,
1975).
The presence of similar degenerative changes in
the columns of monozygous twins suggests that
some inherited aspects of basic vertebral anatomy
may predispose an individual to eventual degenerative olisthesis. Although they do not comment on
degenerative olisthesis per se, Palmer et al. (1984)
found a close similarity in anatomy and general
degenerative changes when viewing radiographs of
the cervical vertebrae in 23 pairs of twins, particularly if the twins were monozygotic. All of their
subjects were 50 – 60-year-old males. The shapes of
vertebral bodies matched very well in twin pairs, but
spinous processes less so. Ten of the 23 pairs had
matching zygapophysial osteoarthritis, and 12 had
matching anterior osteophytes indicative of disk degeneration. The authors suggested that the shapes
of vertebrae are of considerable significance in the
development of the changes associated with aging,
and if this is true of the cervical region, it is likely
true of the lumbosacral region as well. Ryan (1994),
in fact, reported on twin brothers who were 73 years
old when lumbar degenerative olisthesis was observed. Both individuals showed involvement at L4 –
L5, along with symptomatic spinal canal stenosis.
Lumbar degenerative spondylolisthesis has been
associated with inferior articular processes that are
more likely to be parallel to the midsagittal line, or
even to converge caudally, rather than to diverge as
DEGENERATIVE SPONDYLOLISTHESIS
is usually the case (Sato et al., 1989). There is a
question, however, as to whether parallel or converging processes lead to degenerative olisthesis, or
whether they are a result of olisthesis.
Another aspect of degenerative olisthesis involves
long-standing cases of unilateral lumbar spondylolysis (Sherman et al., 1977; Aland et al., 1986; Gunzburg and Wagner, 1988; Waldron, 1992). Here the
apophysial stress is reduced or eliminated on the
side of the defect, but increased on the opposite side.
If long-standing, this condition can also result in
olisthesis due to the defect on one side and to degenerative changes of the zygapophysis on the opposite
side. This results in little if any osteoarthritis on the
side of the defect, but increasing osteoarthritis on
the other side, leading to the condition often referred
to clinically as “reactive sclerosis” (Albers and Yochum, 1980) and, potentially, the equivalent of degenerative olisthesis (Kornberg, 1988).
The most obvious pathological features of lumbar
degenerative olisthesis are the changes observable
in the zygapophysial joints of the vertebrae involved. Rosenberg (1975) described examples in the
Hamann-Todd Collection where “the articular processes had worn away, so that the articulation was
formed by the anterior surface of the inferior process
of the slipped vertebra and the entire posterior surface of the superior process of the subjacent vertebra. As the latter eroded posteriorly, hypertrophic
new bone formed anteriorly, so that the superior
process of the fifth lumbar vertebra encroached on
the spinal canal and its lateral recesses.” Farfan et
al. (1976) also observed at least moderately advanced osteoarthritis in the zygapophysial joints involved in degenerative olisthesis in the anatomical
specimens they studied, noting that in 14 of 19
cases, the cartilaginous surfaces were almost completely destroyed or nonexistent.
Other pathological conditions resulting from degenerative olisthesis have been identified, including
slight stenosis (narrowing) of the spinal canal without compression of neural structures and stenosis of
the nerve root canals (Postacchini and Perugia,
1991; Herkowitz and Kurz, 1991; Herkowitz, 1995).
Joint involvement may not be uniform in all patients, and a rotary component, although small, has
been reported (Bolesta and Bohlman, 1989). Intervertebral disk involvement was found with degenerative olisthesis to varying degrees (Elster and
Jensen, 1985; Bolesta and Bohlman, 1989). Diskspace narrowing, end-plate sclerosis, or osteophyte
formation, or a combination of these, were identified
on radiographs of 139 of 200 patients showing degenerative olisthesis with a total of 197 levels involved (Rosenberg, 1975). Although disk degeneration and herniation have sometimes been suggested
as factors contributing to degenerative olisthesis
(Rosenberg, 1975; Epstein et al., 1976), poor correspondence was observed between the level of olisthesis and that of disk degeneration, the latter occurring most often at L5–S1 (100 cases), followed by
287
L4 –5 (91 cases) and L3– 4 (6 cases). Also, changes at
L5–S1 were usually more profound, and occasionally
fusion had occurred. It thus seemed likely to the
clinicians involved that disk involvement was more
an effect of olisthesis than a cause.
In their study of 43 patients with degenerative
olisthesis, Fitzgerald and Newman (1976) noted the
virtual absence of congenital anomalies, but they did
report 4 cases of transitional lumbosacral vertebrae.
Epstein et al. (1973) also noted 3 examples of transitional lumbosacral vertebrae apparently associated with degenerative olisthesis. It is not clear in
either study, however, whether the transitional vertebrae represented a cranial or caudal shift. Herron
and Trippi (1989) reported that partial or complete
sacralization of L5 (cranial shift) occurred four times
more often in individuals with degenerative olisthesis than in the normal population. None of these
studies appears to have investigated the possibility
of shifting (as defined by Barnes, 1994) occurring at
any other border, particularly the thoracolumbar
border, in individuals with olisthesis. Although the
picture is unclear, the possibility that vertebral border shift, particularly cranial shift, may predispose
to degenerative olisthesis appears deserving of further investigation.
Potter and Norcross (1954) noted what appeared
to be a greater frequency of lumbar lordosis in individuals with degenerative olisthesis. More serious
effects, however, are generally attributed to lateral
stenosis that compromises the inferior nerve roots at
the level of the olisthesis, but even superior nerve
roots can be compressed in more advanced cases
(Bolesta and Bohlman, 1989). Symptoms in the
lower extremities had sometimes been present for 10
years, with varying degrees of back pain existing for
even longer periods, before individuals presented
themselves for treatment, according to Epstein et al.
(1983). Five different clinical pictures were noted by
Postacchini and Perugia (1991): no symptoms except
occasional low back pain; chronic low back pain with
no radicular symptoms; radicular symptoms and no
signs of nerve root compression, with or without low
back pain; radicular symptoms with neurologic deficit; and intermittent claudication. The marked disability caused by claudication contrasted sharply
with the lesser neurological changes (Epstein et al.,
1983). The extent of neural structure compression is
quite variable (Laus et al., 1992), and appears to
depend on three factors: the original size of the
spinal canal, the extent of degenerative changes in
the zygapophysial joints, and the extent of olisthesis
(Postacchini and Perugia, 1991). Given the complexity of the clinical picture, particularly with respect to
observable pathology, it seems unlikely that the
study of an archaeological skeletal collection would
be able to contribute much in relation to how individuals with lumbar degenerative olisthesis may
have felt or how the condition may have affected
their daily lives.
288
C.F. MERBS
Degenerative olisthesis also occurs in the cervical
region, but clinical reports are rare. Potter and
Norcross (1954) reported seeing occasional cases of
cervical involvement, most often between C7 and T1,
which were usually associated with “exaggerated
cervical lordosis in compensation for dorsal kyphos.”
Only 2 of the 21 cases of degenerative olisthesis they
found in an extensive radiographic study involved
the cervical region; all others involved the lumbar
region. Deburge et al. (1995) noted that cervical
degenerative olisthesis usually occurred at C3–C4 or
C4 –C5, immediately above a stiff lower cervical
spine. They found the condition to be associated with
two clinical patterns: neurological involvement
causing cervicobrachial pain or myelopathy, or neck
pain alone.
Relatively little is known about the occurrence of
spondylolisthesis in Native Americans. This study
sought to identify degenerative spondylolisthesis in
Native American adults, as shown in skeletons recovered from prehistoric and early historic Pueblo
sites in New Mexico.
MATERIALS AND METHODS
Approximately 1,000 Native American skeletons
from prehistoric or historic New Mexico Pueblo sites
were examined at the National Museum of Natural
History (Smithsonian Institution, Washington, DC),
the Maxwell Museum of Anthropology (University of
New Mexico, Albuquerque), the San Diego Museum
of Man (San Diego, CA), and the Department of
Anthropology at Arizona State University (Tempe).
Some of the skeletons in Tempe were being curated
at the time for the National Park Service. The minimal requirement of having the lower lumbosacral
region (L3–S1) sufficiently intact to be examined for
degenerative spondylolisthesis was met by 491 adult
skeletons. These came from the following prehistoric
and historic sites or areas in order of frequency:
Puye, 92; Hawikuh (Zuni), 72; Gran Quivira, 54;
Pottery Mound, 46; other Zuni sites (e.g., Heshatauthla, Helonawan), 43; Chaco Canyon (mostly Pueblo
Bonito), 28; Paako, 27; Kuaua, 20; Sapawe, 18; Pajarito Plateau (Ottowi and Sankawi), 18; Navajo
Reservoir, 15; Tijeras Canyon, 14; Giusewa, 12; Pecos Mission, 10; and Pindi, 9, with an additional 13
skeletons from nine different sites.
Areas of analysis included age at death, sex, identification of degenerative olisthesis, measures of actual slippage, evidence of lumbosacral zygapophysial osteoarthritis, lumbosacral disk degeneration,
and orientation of inferior articular processes. Also
noted were cases of unilateral and bilateral spondylolysis, and, in the case of complete columns, information on border shifting. Where questions came
up after initial analysis, it was possible, with one
exception (National Park Service), to go back for
restudy.
Sex and age determinations are based on standard criteria (Buikstra and Ubelaker, 1994), with
the condition of the vertebrae specifically eliminated
Fig. 1. Left lateral view of lumbosacral region, showing simulated degenerative spondylolisthesis at L4 –L5 and L5–S1 levels
(arrows). Dotted line indicates extension of anterior vertical plane
of vertebral body, indicating approximate amount of slippage.
as an age determinant. Sex in nearly all cases was
based on the shape of the pelvis. Skeletons were
placed in three approximate age categories: young
adult, 18 –30 years; middle adult, 30 – 45 years; and
old adult, over 45 years.
Adjacent vertebrae were articulated and examined for anterior slippage of a body relative to the
one below (Fig. 1). Measurements were taken using
adjacent dorsal margins, rather than ventral margins as on clinical radiographs, because they are
easier to take on bare bones (Fig. 2). The measure of
olisthesis was based on the amount of the lower body
exposed by the slippage when the affected vertebrae
were placed in articulated position. Although this
positioning does not take into account the cartilage
that would have been covering the zygapophysial
facets, measurements of slippage in columns lacking
moderate to severe degenerative changes in the apophyseal joints were essentially zero, indicating that
the contribution of cartilage is minimal. A millimeter scale was inserted in the midsagittal plane resting on the lower of the two bodies involved in the
olisthesis, with zero corresponding to the anterosuperior margin of the lower vertebra. A reading was
then taken corresponding to the length of the scale
exposed by the positioning of the vertebra above.
Extending a small rigid straightedge downward
289
DEGENERATIVE SPONDYLOLISTHESIS
Fig. 2. Superior view of L5 and S1, showing how the typical
olisthesis measurement (arrow) was taken in this study.
against the dorsal surface of the upper body to intersect with the scale usually allowed for more precise measurement.
All measurements were initially taken in the midsagittal plane, but additional right and left measurements were taken when the olisthesis was
clearly asymmetrical. The asymmetry was noted,
but the larger measurement was used in the final
analysis.
As in the clinical literature, the degree of olisthesis was interpreted as the amount of exposure divided by the anteroposterior diameter of the body of
the lower vertebra. Body diameters were obtained
using a standard sliding calliper, with osteophyte
development being avoided or subtracted from the
measurement. In actuality, osteophytes proved to be
less of a problem than anticipated, because in this
region of the column they tended to develop more to
the right and left of the midline than in the midline
itself. If the lower vertebra was too poorly preserved
or too pathological to provide an adequate measure,
the diameter of the upper vertebra was substituted.
Where both body diameters were available (most
cases), they were usually found to differ from each
other by 1 mm or less. Since the a-p diameters of the
vertebrae were relatively consistent, nearly all ranging between 30 –35 mm, the process was simplified
for presentation purposes in this article by using
actual measures of olisthesis rather than proportions.
Zygapophysial osteoarthritis was identified primarily from roughening (e.g., pitting, grooving) and
eburnation of articular surfaces, and enlargement of
these surfaces through osteophyte formation. Osteoarthritis was recorded on a scale of 0 – 4 as follows: 0,
none; 1, slight (usually limited to articular surface
irregularities); 2, moderate (more advanced surface
remodeling, slight marginal enlargement, and occasional traces of eburnation); 3, severe (larger areas
of eburnation and abrasion wear through the cortical surface, and more advanced marginal enlargement); and 4, very severe (surface eburnated and
deeply abraded into cancellous bone with parallel
vertical grooving, and pronounced marginal enlargement).
Osteophyte formation on body margins indicative
of disk degeneration was scored on a 0 – 4 scale similar to that used for osteoarthritis. Scoring was
based on how far osteophytes extended outward
from the vertebral margin based on the following
scale: 0, none; 1, 0.5–3.0 mm; 2, 3.0 – 6.5 mm; 3,
6.5–10.0 mm; and 4, more than 10.0 mm. Scoring
was based on approximations of this scale as determined by visual estimation, not actual measurement. Six scores were obtained for each disk space:
left, midline, and right on the ventral inferior margin of the body above, and the ventral superior margin of the body below. Marginal exostoses other than
osteophytes indicative of disk degeneration, such as
those associated with degenerative idiopathic skeletal hyperostosis (DISH), were rare and excluded
from the scoring when encountered.
Attempts to measure the angulation of the inferior
articular processes and facets in the manner described by Sato et al. (1989), using radiographs,
proved cumbersome and time-consuming when applied to bare bones. It was therefore abandoned in
favor of simple visual assessment into three categories: diverging caudally from the midsagittal line,
parallel to this line, or converging caudally toward
this line. In a number of cases the processes were
markedly asymmetrical, the two sides falling into
different categories, and they were recorded as such.
Evidence of cranial or caudal shift at vertebral
borders, including partial and unilateral shift, was
noted where columns were determined to be complete. Special attention was paid to lumbosacral
shift, the border at or closest to lumbar degenerative
olisthesis, and the one cited specifically in the clinical literature, but shift at any border was recorded.
The presence of classic spondylolysis, specifically
complete bilateral separation (separate neural
arch), was also noted. Bilateral separation frequently results in olisthesis, but the process is very
different from that producing degenerative olisthesis. A separate neural arch in fact appears to reduce
stress at the zygapophysial joints, thus decreasing
the likelihood of severe osteoarthritis or degenerative olisthesis at the affected level.
Unilateral separation presents a very different
situation. Complete separation on just one side appears to concentrate zygapophysial stress on the
opposite (intact) side, thus increasing the likelihood
of zygapophysial degeneration and degenerative
olisthesis on this side.
RESULTS
The study produced 10 examples of separate neural arch (complete bilateral spondylolysis), which
likely reduced stress in the area of potential degenerative olisthesis. These cases were thus eliminated
from further consideration. Also noted were 8 examples of spondylolysis in which the separation was
290
C.F. MERBS
Fig. 3. Cases of degenerative olisthesis in New Mexico Pueblo
skeletons by level of involvement and amount (in millimeters) of
slippage.
complete on one side, with the other side remaining
intact. In each case the affected unit was L5, and
separation was through interarticularis. In only 2
cases, however, was the vertebra involved in degenerative olisthesis. Five of those unaffected were
young adults (3 males and 2 females); the sixth was
a middle adult female. In 5 of these individuals, the
L5 laminae had not fused (spina bifida), making the
situation similar to separate neural arch (actually
hemiarch in this case). The 2 affected individuals
were a middle adult male with 3 mm (0.09) of olisthesis, and an old adult female with 8 mm (0.28) of
olisthesis. Although analogous to degenerative olisthesis without lysis, the primary subject of this report, these cases are not included in the analysis and
will be examined more carefully in a separate study.
The study identified 64 individuals with degenerative spondylolisthesis. A single level was involved
in 55 cases, two levels in 8 cases, and three levels in
1 case, for a total of 74 levels affected. The distribution by level is as follows: L3–L4 ⫽ 2, L4 –L5 ⫽ 14,
and L5–S1 ⫽ 58 (Fig. 3). Slippage ranged from the
defined minimum of 2 mm (6 –7%) to a maximum of
8 mm (24 –27%). In 6 cases, all at the L5–S1 level,
olisthesis was noticeably asymmetrical, with a difference of 2 mm or more between sides. The most
extreme example of asymmetry, 8 mm on one side
and 0 mm on the other, was observed in an old adult
female (Fig. 4). The asymmetrical cases were
equally divided with respect to side, 3 showing more
olisthesis on the left side, and 3 on the right side.
The degenerative olisthesis was well-distributed
across archaeological sites and site groups, with no
significant frequency differences observed.
Degenerative olisthesis was observed in 41% (31/
75) of old adults, 16% (33/271) of middle adults, and
in none of the 145 young adults (Fig. 5). More females were affected than males (53:11). In fact, 60%
(27/43) of all old females had the condition.
Zygapophysial osteoarthritis scores rarely varied
between superior and inferior articular facets, and
in those few instances where they did vary, the
maximum score was used (Fig. 6). The condition was
Fig. 4. Dorsal view of sacrum from Gran Quivira, showing
severe osteoarthritis in an individual with asymmetrical degenerative spondylolisthesis (8 mm right side, none on left side) at
L5–S1. Note that the osteophytic margin of the right zygapophysial facet (arrow) is nearly in contact with the body of the
sacrum, an example of severe degenerative remodeling. This
specimen received an osteoarthritis score of 3 on the left side and
4 on the right.
Fig. 5. Frequency of degenerative spondylolisthesis and separate neural arch in New Mexico Pueblo skeletons by age and sex.
found to be absent in young adults and rare in middle adults (less than 5% of joints affected), but then
to increase dramatically in old adults (23%). Frequencies were higher for males than females in both
middle adults (6% vs. 3%) and old adults (27% vs.
19%). However, old adult females showed higher
levels of involvement than males, with 11% of joints
in females scoring higher than 1 on the scale of 1– 4
compared with just 5.5% in males. Values increased
in frequency caudalward from the L3–L4 level, with
the degree of involvement increasing dramatically
at the L5–S1 level in old adult females. Especially
striking is a comparison of old adult females with
and without degenerative olisthesis: osteoarthritis
was present in 43% of joints (nearly all at the 3– 4
level of severity in individuals with olisthesis, compared to only 5.5% of joints (all at the 1–2 level) in
those without olisthesis). All individuals with degenerative olisthesis, regardless of sex, had level 3 or 4
DEGENERATIVE SPONDYLOLISTHESIS
291
Fig. 6. Distribution of zygapophysial osteoarthritis in vertebral columns of New Mexico Pueblo skeletons relative to age, sex, and
level of involvement.
osteoarthritis on at least one side at the affected
level.
In contrast to the osteoarthritis scores, those for
disk degeneration often varied considerably between
superior and inferior margins. The scores for inferior disk margins (superior vertebral margins) were
usually higher, and they were the ones ultimately
used in the analysis (Fig. 7). Observable changes
associated with disk degeneration were found in
young adults, with 6.3% of margins affected; this
increased to 56% in middle adults and 77% in old
adults. The amount of involvement by level proceeds
in the opposite direction as that of osteoarthritis,
with the highest frequencies and levels of intensity
occurring at L3– 4, and the lowest at L5–S1. The
amount of involvement by level proceeds in the opposite direction as that of osteoarthritis, with the
highest frequencies and levels of intensity occurring
at L3– 4 and the lowest at L5–S1 (Fig. 7). The vertebral level most likely to show degenerative olisthesis in this study, L5–S1, thus shows the least
amount of disk degeneration. The only difference in
pattern of disk degeneration between those with and
those without degenerative olisthesis is a greater
involvement (but with no greater intensity) at the
L5–S1 level in those with olisthesis.
Among young adults, more than 80% of L5 inferior
articular processes fell in the divergent category,
with the remainder being parallel (Fig. 8). One individual, a female, had processes that could be classified as convergent, but because they appear to
have resulted from a developmental error rather
than being a normal variant, they were eliminated
from the analysis. Among middle adults without
degenerative olisthesis, 25% of the processes were
parallel or convergent, and this figure increased to
58% in old adults. A comparison of old adult females
with olisthesis vs. those without produced a striking
difference (Fig. 8): 87% of the processes in those with
olisthesis were convergent or parallel, compared
with just 44% in those without olisthesis.
Border shifting was determined with reasonable
certainty for 87 columns, but 4 were eliminated because separate neural arch was present. The distribution of the remaining 83 columns is shown in
Table 1. This distribution produced a ␹2 value of 13.5
(df ⫽ 2, P ⬍ 0.01). Three of the 6 columns with
olisthesis and cranial shift have only 11 thoracic
vertebrae, and in one of these, the affected level
involved a sacralized lumbar vertebra. A second example of transitional lumbosacral vertebra involvement was observed, but in this case the column was
too incomplete to determine the direction of shift. All
3 cases of caudal shift associated with olisthesis
involved the sacrocaudal border, a marginal kind of
shift located well below the level of the olisthesis and
probably irrelevant to the condition.
Although the New Mexico collections were not
examined systematically for degenerative olisthesis
in the cervical region, the condition was observed in
5 individuals: 2 each from Tijeras Canyon and Navajo Reservoir, and 1 from Paako. Three of these
292
C.F. MERBS
Fig. 7. Distribution of vertebral disc degeneration in New Mexico Pueblo skeletons relative to age, sex, and level of involvement.
Fig. 8. Distribution of inferior articular process shape in New Mexico Pueblo vertebrae relative to degenerative spondylolisthesis.
were females: 1 middle adult and 2 old adults, and 2
were old adult males. The C4 –C5 level was affected
three times, and C5–C6 twice. All 5 cases were
markedly asymmetrical, with the left side more severely affected three times and the right side more
affected twice. In each case, olisthesis was accompa-
DEGENERATIVE SPONDYLOLISTHESIS
293
TABLE 1. Distribution of New Mexico Pueblo vertebral
columns, relative to border shift and
degenerative spondylolisthesis
With olisthesis
Without olisthesis
Totals
Cranial
shift
No
shift
Caudal
shift
Totals
6
8
14
2
41
43
3
23
26
11
72
83
nied by severe osteoarthritis at the same level, with
distinctly greater osteoarthritis on the side of
greater olisthesis, but these cases were greatly outnumbered by others with severe cervical osteoarthritis and no olisthesis. The maximum slippage in
the cases observed ranged from 2 mm (11%) to 4 mm
(22%), with the greater slippage occurring in older
individuals. The cervical olisthesis was accompanied
by lumbosacral involvement in 3 of these individuals, i.e., the 3 females. One of the columns, of a
female from Paako, also exhibited a retrolisthesis
(posterior slippage) of 3 mm (0.17) at C1–C2. C2 in
this individual presents an unusual anatomy, with
the odontoid tilting back and the spinous process
angling upward.
DISCUSSION AND CONCLUSIONS
New Mexico Pueblo skeletons closely resemble
modern patients in terms of the age and sex of
individuals most likely to develop degenerative olisthesis. They agree that this is a condition of older
individuals, absent in young adults, sometimes occurring in middle age, but most likely to be seen in
old adults, and females are more likely to be affected
than males. The approximate 5:1 ratio observed for
the New Mexico skeletons falls between the extremes of 2:1 and 6:1 reported in the clinical literature. Also, the maximum degree of slippage observed here (27%) is similar to that observed
clinically.
Little information on the overall frequency of degenerative olisthesis is provided by clinical studies.
The impression given, however, is that it is a relatively uncommon condition, certainly less frequent
than the 41% reported for old adults in this study.
Before much significance is read into this, however,
the nature of the two samples must be considered. In
this study, all skeletons that met the lumbosacral
completeness criterion were carefully examined,
with olisthesis as little as 2 mm recorded. The same
would be true, presumably, for an anatomical collection study or one of autopsy specimens. Subjects
ending up in the clinical studies, on the other hand,
usually present themselves for medical care with
pain threshold as a key factor. Small degrees of
olisthesis may not always be associated with pain
and thus may not come to the attention of a clinician. It is thus reasonable to assume that for degenerative olisthesis, clinical frequencies are underreported, but by how much it is difficult to say. It is
thus difficult to say if the high frequency observed in
Fig. 9. Percent of total degenerative spondylolisthesis according to level affected in New Mexico Pueblo skeletons and clinical
patients.
the New Mexico skeletons has any significance, especially since age and sex are key variables.
The results of this study are very different from
those obtained from clinical patients in one respect:
level of involvement (Fig. 9). Using the study of
Rosenberg (1975) as typical, 80% of the olisthesis is
expected to occur at level L4 –L5. This stands in
sharp contrast to our New Mexico study, where 79%
occurred at L5–S1. It should be noted, however, that
in both studies, “level” was identified by morphological appearance, and not by number of vertebrae
down from the cranium.
The relationship between degenerative olisthesis
and zygapophysial osteoarthritis appears fairly
straightforward: severe osteoarthritis must be
present for olisthesis to occur. The two conditions
follow the same pattern, increasing in frequency
from L3–L4 down to L5–S1 (Fig. 6). Even more
convincing is the fact that every case of degenerative
olisthesis observed was accompanied by severe zygapophysial osteoarthritis at the affected level, and
all examples of grade 4 zygapophyseal osteoarthritis
were associated with degenerative olisthesis. In addition, asymmetrical degenerative olisthesis was always accompanied by asymmetrical osteoarthritis,
with the side of greater involvement always in
agreement. However, the results also show that severe osteoarthritis need not result in degenerative
olisthesis, especially in males. Occasionally, males
showed high osteoarthritis scores in the L3–S1 level
range with no olisthesis; such cases were rare in
females.
In contrast, there appears to be little causal relationship between degenerative olisthesis and disk
degeneration in the lumbosacral region. It was common, for example, to encounter individuals with severe disk degeneration and no degenerative olisthesis. Also, the pattern of disk degeneration is the
opposite of that of osteoarthritis and degenerative
olisthesis, occurring with greatest frequency and intensity at L3–L4 and decreasing down to L5–S1
(Fig. 7). The one exception to this pattern can be
seen in old adult females with degenerative olisthe-
294
C.F. MERBS
sis, where the L5–S1 level shows more disk degeneration than expected. All results are consistent
with osteoarthritis predisposing to olisthesis,
whereas osteophyte formation is an adaptive response to instability in the vertebral column, with
olisthesis being one source of instability.
This study substantiated what has been observed
in the clinical context, that vertebrae involved in
degenerative olisthesis are more likely to have inferior articular processes that are parallel to the midline or actually converge toward it, rather than diverge from it, which is generally thought to be the
normal condition. The presence of parallel processes, even in young adults with no signs of osteoarthritis, degenerative olisthesis, or any other abnormal condition, suggests that they are part of the
normal range of variability of this feature. Although
it cannot be ruled out that parallel or convergent
processes may predispose an individual to degenerative olisthesis, their increase with age, and particularly their extremely high occurrence in old adult
females with degenerative olisthesis (Fig. 8), indicate that they most often develop as part of the
degenerative remodeling process that produces olisthesis.
Since identifying vertebral border shift requires
greater completeness of the column than identifying
degenerative olisthesis, and since data on shift were
collected only for individuals with olisthesis at the
beginning of the study, the sample size of individuals for which both olisthesis and shift is available is
relatively small (83). Nevertheless, the results are
quite interesting and may provide direction for future work, especially as border shift is thought to
have some genetic basis (Merbs, 1974). A ␹2 value
significant at a probability level of greater than 0.01
suggests that a relationship may indeed exist between degenerative olisthesis and cranial shift, but
the nature of this relationship is difficult to ascertain. However, if the affected vertebrae were identified based on their distance from the cranium (e.g.,
C1 ⫽ V1, T1 ⫽ V8, L1 ⫽ V20) rather than their
morphological appearance, the New Mexico results
would more closely resemble those of clinical studies. In 3 of the 6 cases for which this information is
available, the affected levels would be V23–V24 (ordinarily L4 –L5), and not L5–S1 as based on their
morphological appearance. Approached in this way,
the level of olisthesis in these 6 columns (one with
two levels affected) would change from L4/L5 ⫽ 3
and L5/S1 ⫽ 4, to L3/L4 ⫽ 1, L4/L5 ⫽ 5, and L5/S1 ⫽
1. Add to this the two columns showing no shift, and
the distribution becomes equivalent to L3/L4 ⫽ 1,
L4/5 ⫽ 7, and L5/S1 ⫽ 1. Even at that, however,
thoracolumbar cranial shift cannot account for all of
the difference in level of involvement seen in the two
kinds of studies.
One possible explanation for the difference in level
of involvement takes into consideration a contrast
between studies involving archaeological skeletons
and studies involving living patients. Since degen-
erative olisthesis produces stenosis of the neural
canal and impingement of the spinal nerves that
could result in enough pain to send the victim for
medical assistance, the pain factor must be taken
into consideration when evaluating clinical studies.
Generally, the higher the nerve impingement takes
place in the lumbar column, the greater the pain
produced. This might explain the higher level of
involvement in the column recorded in the clinical
literature (L4 –L5) than that observed in this archaeological study (L5–S1). It is possible that individuals with L4 –L5 involvement experienced
greater pain than those with L5–S1 involvement,
making them more likely to seek medical assistance
and thus to end up being cited in the clinical literature. Studies of archaeological specimens, on the
other hand, are based on pathological appearance;
pain cannot be a factor. Archaeological studies
would thus lack any bias for L4 –L5 involvement.
Although this suggestion makes some sense, it appears to be contradicted by the study by Farfan et al.
(1976) of lumbosacral spines collected at autopsy,
and by Rosenberg (1975) of anatomical skeletons.
Both studies presumably involved complete ascertainment based on pathological appearance with
pain not a factor, but both recorded degenerative
olisthesis primarily at the L4 –L5 level.
The difference in level of involvement might also
be attributed to differences between the Native
Americans who were the subjects of this study and
the Europeans or European-Americans who made
up the majority of subjects of the clinical and anatomical studies. Twin studies suggest that vertebral
anatomy, some of which may predispose to degenerative changes, may indeed be inherited. This suggests that the level differences might have some
genetic basis. Inherited morphological features may
produce subtle differences in the lumbar curve, for
example, that may have a significant effect on stress
patterns in the lower column which would be difficult if not impossible to determine from bare skeletons. Another possibility is that the differences are
essentially behavioral in nature, resulting from activity patterns that are specific to these prehistoric
and early historic Native Americans. Determining
what these might be, however, is beyond the scope of
the present study.
Although degenerative olisthesis in the cervical
region is represented by just 5 examples in this
study, some interesting observations can be made.
As with its lumbosacral equivalent, old adult females appear to be at greatest risk. The middle
cervical region, specifically C4, C5, and C6, appears
at greatest risk, and all the cases observed were
markedly asymmetrical, but with no consistency in
the side involved. As with its lumbosacral equivalent, the condition appears closely related to osteoarthritis, but not disk degeneration. Lumbosacral
olisthesis was also present in the 3 females affected,
but not in the 2 males. In one case, cervical olisthesis
was accompanied by posterior slippage at C1–C2.
DEGENERATIVE SPONDYLOLISTHESIS
ACKNOWLEDGMENTS
I acknowledge the valuable assistance provided by
my wife, Barbara Merbs, who served as my recorder
for the data collected in this study. I also thank the
people who provided valuable assistance at the various institutions that curated the New Mexico collections, particularly Diane Hawkey and Chelsea
Klein at Arizona State University, Rose Tyson at the
San Diego Museum of Man, Joseph Powell at the
Maxwell Museum of Anthropology, and Donald Ortner and David Hunt at the Smithsonian Institution.
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