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: firstname.lastname@example.org 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. 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