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Brief communication Developmental dysplasia of the hip in medieval London.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 144:479–484 (2011)
Brief Communication: Developmental Dysplasia
of the Hip in Medieval London
Piers D. Mitchell1* and Rebecca C. Redfern2
1
2
Leverhulme Centre for Human Evolutionary Studies, University of Cambridge, UK
Centre for Human Bioarchaeology, Museum of London, UK
KEY WORDS
DDH; disability; St Mary Spital (Spitalfields); medieval; joint pathology
ABSTRACT
Developmental dysplasia of the hip
(DDH) is a spectrum of disease starting in childhood and
in many cases persisting into adulthood. The spectrum
ranges from acetabular dysplasia, through hip subluxation to dislocation. The aim of this research was to determine the prevalence and pathoanatomy of acetabular
dysplasia and subluxation in excavated human skeletal
remains, to complement past research on dislocation in
DDH. The material under study was the medieval cemetery of St. Mary Spital in London, in use from c.1100 to
1539 AD. A series of 572 adults with both hips preserved
were analyzed. Acetabular dysplasia was indicated by a
shallow acetabulum with upward sloping roof. Subluxation was suggested by degenerative change along the
margin of the acetabulum suggestive of labral tears, and
degenerative change in the outer part of the acetabular
roof suggestive of osteoarthritis. The prevalence of DDH
(acetabular dysplasia, subluxation, or dislocation) was
1.7%. Because this a congenital musculoskeletal disorder
of relatively high frequency, with significant variation in
prevalence between populations around the world, it is a
topic that warrants targeted research from physical
anthropologists studying past populations. Am J Phys
Anthropol 144:479–484, 2011. V 2010 Wiley-Liss, Inc.
Most children are born with hips that are in joint, stable, and formed with normal acetabular and femoral
anatomy. However, a proportion of children suffer with a
spectrum of disease known as developmental dysplasia of
the hip (DDH). Some are born with complete dislocation
of the joint, known in the past as congenital dislocation
of the hip. However, a larger number are born with
hips that are in joint but nevertheless abnormal. This
spectrum of abnormality has become known over the last
decade as DDH (Herring, 2002; Weinstein, 2006).
The mildest end of the spectrum is acetabular dysplasia, a shallow acetabulum with increased obliquity and
reduced concavity of the acetabulum. However, the femoral head continues to articulate normally within the hip
joint. Subluxation represents the intermediate stage in
the DDH continuum, where the femoral head is laterally
displaced, and only articulates with the lateral margin of
the dysplastic acetabulum. Dislocation represents the
most severe end of the DDH spectrum, with complete
loss of continuity between the articular surfaces of the
femoral head and acetabulum. The femoral head therefore articulates with a false acetabulum on the lateral
aspect of the iliac wing of the pelvis (Fig. 1). The following soft-tissue and skeletal changes in DDH have also
been reported in the clinical literature: acetabular labral
tears (Fujii et al., 2009; Noguchi et al., 1999; Tanzer and
Noiseux, 2004; Cashin et al., 2008; Tschauner and
Hofman, 1998), degenerative changes to the acetabular
rim (Ganz and Leunig, 2007; McCarthy and Lee, 2002;
Fujii et al., 2009), abnormal femoral head and neck morphology and differences in limb length (Storer and Skaggs,
2006), valgus angulation at the knee (Kandemir et al.,
2002), and osteoarthritis (OA) (Jacobsen et al., 2005;
McCarthy and Lee, 2002; Haene et al., 2007; Jessel et al.,
2009). Even if dysplasia and subluxation present as a
unilateral condition, the contralateral hip joint will also be
abnormal compared with a normal healthy hip, in terms of
femoral neck anteversion, femoral neck-shaft angle, and
increased acetabular anteversion (Jacobsen et al., 2006).
These changes have been summarized in Table 1.
Previous research has demonstrated that in archaeologically derived samples of human remains, hip dislocation
can be clearly differentiated from other pathological
lesions of the hip (Blondiaux and Millot, 1991; Stirland,
1997; Mafart et al., 2007). The morphology of both the
localized hip pathology and the generalized skeletal
consequences of DDH with dislocation have been defined
(Mitchell and Redfern, 2008). Acetabular labral tears have
also been studied in medieval skeletal remains from the
cystic change along the supra-acetabular margin (Mays,
2005). The aim of this article is to clarify the diagnostic
criteria for acetabular dysplasia and subluxation with
labral tears in human skeletal remains and determine the
prevalence in a population from medieval London.
C 2010
V
WILEY-LISS, INC.
C
MATERIALS
The sample examined for evidence of DDH was recovered from the site of St. Mary Spital, located in Spitalfields
Market, London, in the United Kingdom. The excavations
were undertaken by the Museum of London Archaeology
Service between 1996 and 2001 (Thomas, 2004). This sample does not include the individuals previously published
by Thomas et al. (1997). The remains were originally
*Correspondence to: Dr. Piers Mitchell, Leverhulme Centre for
Human Evolutionary Studies, University of Cambridge, The Henry
Wellcome Building, Fitzwilliam Street, Cambridge CB2 1QH, UK.
E-mail: pdm39@cam.ac.uk
Received 8 July 2010; accepted 13 October 2010
DOI 10.1002/ajpa.21448
Published online 29 December 2010 in Wiley Online Library
(wileyonlinelibrary.com).
480
P.D. MITCHELL AND R.C. REDFERN
Fig. 1. Representation of acetabular dysplasia, subluxation, and dislocation in DDH.
TABLE 1. Summary table of pathological changes helpful in the diagnosis of acetabular dysplasia and subluxation in DDH
Anatomical structure
Acetabular roof or sourcil
Acetabular margin
Femoral head
Femoral neck
Knee
Leg length
Pathological change
1) Shallow acetabulum with superolateral slope to roof (sourcil), indicates acetabular dysplasia.
A normal roof curves down beyond horizontal to slope inferiorly at the lateral margin.
2) Degenerative change (cysts, eburnation, hard sclerotic bone) at lateral part of acetabular roof and
not medial part, indicates osteoarthritis due to subluxation
Osteophytes and cysts along acetabular rim, indicates labral tears. If acetabular dysplasia is also
present but acetabular roof is smooth, this combination suggests subluxation without osteoarthritis.
Eburnation, subchondral cysts and osteophytes on medial part of superior surface suggests
subluxation if acetabular degenerative change is positioned laterally.
Femoral neck anteversion and valgus neck shaft angle may be present.
Valgus angulation at the knee (knock knees) when femur and tibia orientated in anatomical position.
The leg on the side with the abnormal hip may be shorter than the contralateral leg.
The first three criteria are key to diagnosis.
buried in the cemetery that belonged to the medieval hospital and priory of St Mary Spital, between c.1100 and
1539 AD and are believed to be comprised of individuals
from the population of the city and suburbs of London. A
total of 5,387 individuals, who were considered to be [35%
complete were recorded using the Wellcome Osteological
Research Database (WORD) by a team of four osteologists
between 2003 and 2006 (Connell and Rauxloh, 2003; Connell et al., in press). The methods used have previously
been published by the Museum of London (Powers, 2008)
and are based on the widely accepted standards of Buikstra
and Ubelaker (1994) and Brickley and McKinley (2004).
This study was performed on a consecutive series of 572
adult individuals that had originally been studied by the second author during the Spitalfields Market project (Museum
of London Archaeology). All had both acetabula and femoral
heads preserved. Of these 572 burials, 323 were males, 213
females, 36 undeterminable sexes. Adults were studied,
because the angle of the acetabular roof may be difficult to
determine in immature individuals in whom the acetabular
roof will be made of cartilage that gradually ossifies with
increasing age. Only those with a fully ossified pelvis,
including the iliac crest apophyses (growth plates), were
included in the study
METHODS
Sex determination was undertaken using seven pelvic
features and seven skull characters (Buikstra and
Ubelaker, 1994; Ferembach et al., 1980). Determination
American Journal of Physical Anthropology
of age in these adult individuals was estimated using degenerative changes of the pubic symphysis, auricular surface, and sternal rib end morphology (Brooks and Suchey,
_
_
1990; Lovejoy et al., 1985; Isçan
et al., 1984; Isçan
et al.,
1985). The molar wear age group stages generated by
Brothwell (1991) were also used. However, as the prevalence of this congenital disorder does not change during
adulthood, estimated age at death is only given for those
cases included in the illustrations.
In each case, the pelvis was orientated in three dimensions to the anatomical position by comparison with an
articulated skeleton, and then examined for the points
summarized in Table 1. The first three items in Table 1
(acetabular roof, acetabular margin, and femoral head)
were of particular use in identifying the diagnosis of DDH
and also where on the spectrum each case lay. The last
three items on Table 1 (femoral neck, knee, and leg length)
help to confirm the diagnosis of DDH but do not differentiate which form of DDH is present.
Individuals with skeletal evidence for other diseases
that might cause hip instability in childhood were
excluded from the study. These include spina bifida and
other congenital spinal pathology, cerebral palsy, arthrogryposis and related congenital musculoskeletal syndromes.
Similarly, those with other hip diseases such as fractures,
septic arthritis, and tuberculosis were also excluded.
RESULTS
A total of 10 adult individuals from the study series of
572 were identified as having DDH of some kind, giving
481
DDH IN MEDIEVAL LONDON
Fig. 3. Left hip subluxation in middle aged adult male,
with cystic change (thin arrow), and osteophytes (broad arrow)
indicative of degenerative change. The lesions are located on the
superolateral part of acetabulum, adjacent to the acetabular rim.
Fig. 2. Left hip acetabular dysplasia in middle-aged adult
female, seen easily due to post mortem damage to anterior part
of acetabulum. There is no evidence for osteoarthritis.
an overall prevalence of 1.7% for this disease spectrum.
Sixteen hips out of the 1,144 hips analyzed (572 3 2)
had DDH of some kind. Six individuals had bilateral
DDH and four unilateral disease. Disease in the bilateral cases was not necessarily symmetric in its type,
as it is possible to have acetabular dysplasia on one
side and subluxation on the other. One male had bilateral acetabular dysplasia (Fig. 2) without evidence for
subluxation or dislocation. Three females had at least
one hip with acetabular dysplasia without evidence for
subluxation or dislocation, one of these being bilateral.
Two individuals of unknown sex had at least one hip
with acetabular dysplasia without evidence for subluxation or dislocation, one of these being bilateral. In
consequence, the prevalence of simple acetabular dysplasia in the population was 0.3% in males and 1.4% in
females, and 1.0% overall. Two males had bilateral
acetabular dysplasia with bilateral subluxated hips
(Figs. 3–4), and a further one had unilateral subluxation. One female had unilateral subluxation, giving a
prevalence of subluxation of 0.7% overall. One female
had DDH with unilateral dislocation, while no males
had dislocation in this series, giving a prevalence of
dislocation of 0.2% overall. The data are given in detail
in Table 2.
OA within the hip joint (indicated by eburnation,
osteophytes, and subchondral cysts) was present in one
of the 16 hips (6%), a case of DDH with subluxation.
Fig. 4. Left hip subluxation in middle aged adult male, with
degenerative change on the superomedial aspect of the femoral
head (arrow). When viewed in the context of the superolateral
acetabular degenerative change, this suggests hip subluxation
during life.
DISCUSSION
Here, we have applied clinical knowledge to identify
the skeletal changes of acetabular dysplasia and subluxation in human skeletal remains, complementing past
research on DDH with dislocation (Mitchell and Redfern,
2008). Evidence from modern clinical research suggests
the primary cause of hip joint instability and DDH
seems to be mechanical: an intrauterine posture in full
hip flexion and adduction combined with abnormal presAmerican Journal of Physical Anthropology
482
P.D. MITCHELL AND R.C. REDFERN
TABLE 2. Data for the number of acetabula that show evidence for dysplasia, subluxation, and dislocation due to DDH in the series
of 572 individuals under study
Sex
Side
Number of
acetabula
Number with simple
dysplasia (%)
Number with dysplasia
and subluxation (%)
Number with dysplasia
and dislocation (%)
Male
Right
Left
Right
Left
Right
Left
Right
Left
323
323
213
213
36
36
572
572
1 (0.3)
1 (0.3)
1 (0.5)
3 (1.4)
2 (5.6)
1 (2.8)
4 (0.7)
5 (0.9
6/572 (1.0)
2 (0.6)
3 (0.9)
1 (0.5)
0
0
0
3 (0.5)
3 (0.5)
4/572 (0.7)
0
0
1 (0.5)
0
0
0
1 (0.2)
0
1/572 (0.2)
Female
Unsexed
Total
Prevalence
Key: Percentages rounded up or down to nearest tenth of a percent, to reflect the degree of accuracy possible from a sample size of
572 individuals. The data in the upper part of the table refer to the number of hips involved, as a percentage of right or left hips in
the male, female, or unsexed group. The prevalence data and percentages at the foot of the table refer to the number of individuals
involved. Because each individual has two hips, an individual can have just unilateral disease, or bilateral disease that may be
symmetric or of different types in each hip.
sure on the greater trochanter that shifts the femoral
head in a superoposterior direction relative to the acetabulum (Koureas et al., 2007). This is why the incidence
is higher in babies born with breech presentation (more
mechanical force on the hips), being first born (less
compliant uterus) or one of a multiple birth (less space
in the uterus), premature birth with a low birth weight
(immature hips) and being female (Sionek et al., 2008;
Stein-Zamir et al., 2008; Czubak et al., 2003). DDH is
thought to have an autosomal dominant heritage that
can be either polygenic or rarely monogenic, and therefore, the genes possessed by an individual can predispose
them to developing DDH when exposed to such mechanical forces in the uterus (Abu Hassan and Shannak,
2007; Mabuchi et al., 2006). The risk of developing DDH
is also higher if the mother has the endocrine disorder
hyperthyroidism, where too much thyroid hormone is
produced (Ishikawa, 2008). Cultural influences have also
been shown to significantly affect the development of
these conditions, for example in Japan, where an initiative in 1975 to reduce the use of swaddling resulted in a
rapid decrease in incidence. However, if an infant only
has its arms swaddled and the legs are left free to flex
and abduct at the hips, then the risk of hip dysplasia is
very much reduced (Yamamuro and Ishida, 1984; Akman
et al., 2007; Mahan and Kasser, 2008; van Sleuwen et
al., 2007). These various clinical research studies must
be borne in mind when we interpret evidence for DDH
in past populations. As the cause is multifactorial, we
must be careful before claiming that genetics, or swaddling, or any other specific cause must be responsible for
any differences in prevalence between past populations
where so many of these factors remain unknown.
The prevalence of the DDH spectrum in this medieval
population was 1.7%. Previous research in this population (Mitchell and Redfern, 2007) based on a different
series of 6,580 hips that were assessed for DDH with dislocation (but not acetabular dysplasia or subluxation)
found a prevalence of 0.27%. The new data presented
here shows that the entire spectrum of DDH (acetabular
dysplasia, subluxation, and dislocation) was over six
times more common than DDH with dislocation alone.
Modern clinical studies have not been able to determine
the true prevalence of acetabular dysplasia in untreated
Caucasian populations. That is because so many countries screen their population in some way shortly after
birth in an attempt to identify this disease. Prevalence
American Journal of Physical Anthropology
data for DDH with acetabular dysplasia based on ultrasound testing in babies will greatly overestimate the
prevalence that might persist into adulthood even if no
treatment was ever given, as many children with acetabular dysplasia as a baby will grow to develop a normal
acetabulum by the time they reach adulthood. For this
reason we cannot say whether acetabular dysplasia is
more or less common the medieval London that it is
today. However, the prevalence of DDH with dislocation
(which does not get better with growth) has previously
been shown to be the same in medieval London as it was
in the twentieth century, (Mitchell and Redfern, 2008) so
we might speculate that the prevalence of DDH with
acetabular dysplasia or subluxation might also be similar.
Individuals with a dysplastic joint may be asymptomatic until late adolescence or early adulthood when they
may begin to experience pain and develop degenerative
change (Herring, 2002: 523). In those with subluxated
hips, OA and pain manifest themselves between the ages
of 20 to 60 years, depending on the degree of subluxation
(Herring, 2002: 524; Weinstein, 2006: 1006). Clinical data
show that individuals with subluxation will be most
affected by symptoms such as pain as they have the most
wear-and-tear on their hip joint. This is because of
the abnormal point loading of the femoral head on the
margin of acetabulum. Those with simple acetabular dysplasia and complete dislocation are less likely to develop
pain than those with subluxation (Shapiro, 2001: 198).
Clinical studies of untreated dysplastic and subluxated
hip joints show that not all DDH leads to OA. A recent
meta-analysis of the natural history of these conditions
suggests that if the hip joint is well centered and stable,
then early onset OA is unlikely to be observed (Ziegler
et al., 2008). These results are also supported by an
analysis of a middle-aged Sámi population (Norway),
where no statistically significant relationship was found
between hip dysplasia and OA (Johnsen et al., 2009).
However, decentered hips are prone to degenerative
change. It can be a challenge to determine whether a
hip was well centered or not in life after the soft tissue
has decomposed and the skeletal remains are excavated.
If there is acetabular dysplasia and degenerative change
on the acetabular margin then hip subluxation is likely
to have been present in life. However, subluxation in a
young adult may be missed in archaeological specimens
if bony change to the margin has not developed by the
time of death. In consequence we may underestimate the
DDH IN MEDIEVAL LONDON
proportion of those with subluxation due to DDH in past
populations, and overestimate the proportion that
had simple acetabular dysplasia. In light of this, future
studies of OA of the hip in past populations should state
the prevalence of DDH in their sample to interpret the
meaning of their OA prevalence and demonstrate the
proportion of those with OA that were actually secondary to DDH. In populations where DDH is common
(such as some North American indigenous peoples), OA
of the hip will most likely also be more common.
DDH is one of the most common congenital abnormalities that affects the musculoskeletal system in a way
that can be clearly identified in excavated human skeletal remains. It is also a condition that varies in prevalence quite dramatically around the world in modern
populations. We might also expect a wide variation in
prevalence in past populations too. Such variation might
help us to identify populations that were genetically
distinct from those near them due to inbreeding or recent
migration, identify those practicing childcare methods
that altered the prevalence of the disease due to the position of babies hips, and improve our understanding of
disability in the past. The lack of publications on the
spectrum of DDH in archaeological contexts has resulted
in its relative absence from standard texts on physical
anthropology and paleopathology. It is hoped that now
diagnostic criteria in human skeletal remains have been
proposed, and a base-line prevalence has been presented
for one population, that further research can improve our
understanding of the way this condition affected past
populations across time and geographical space.
ACKNOWLEDGMENTS
We thank Chris Thomas (MoLA) for allowing this
research to be undertaken and Natasha Powers for her
help with obtaining the data. We also thank Brian Connell, Don Walker, and Amy Gray Jones for their work on
the Spitalfields Market Project. The Spitalfields Market
Project was funded by MoLA, the Corporation of London,
Hammerson, and the Spitalfields Development Group.
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