text:
Subchondral bone in osteoarthritis: insight into risk factors and microstructural changes
- Guangyi Li1, 2,
- Jimin Yin1,
- Junjie Gao2,
- Tak S Cheng2,
- Nathan J Pavlos2,
- Changqing Zhang1Email author and
- Ming H Zheng2Email author
DOI: 10.1186/ar4405
© BioMed Central Ltd. 2013
Received: 1 August 2013
Accepted: 2 December 2013
Published: 9 December 2013
Osteoarthritis (OA) is a major cause of disability in the adult population. As a progressive degenerative joint disorder, OA is characterized by cartilage damage, changes in the subchondral bone, osteophyte formation, muscle weakness, and inflammation of the synovium tissue and tendon. Although OA has long been viewed as a primary disorder of articular cartilage, subchondral bone is attracting increasing attention. It is commonly reported to play a vital role in the pathogenesis of OA. Subchondral bone sclerosis, together with progressive cartilage degradation, is widely considered as a hallmark of OA. Despite the increase in bone volume fraction, subchondral bone is hypomineralized, due to abnormal bone remodeling. Some histopathological changes in the subchondral bone have also been detected, including microdamage, bone marrow edema-like lesions and bone cysts. This review summarizes basic features of the osteochondral junction, which comprises subchondral bone and articular cartilage. Importantly, we discuss risk factors influencing subchondral bone integrity. We also focus on the microarchitectural and histopathological changes of subchondral bone in OA, and provide an overview of their potential contribution to the progression of OA. A hypothetical model for the pathogenesis of OA is proposed.
Osteoarthritis (OA) is a common leading cause of pain and disability in the aging population. As a slowly progressive degenerative joint disorder, OA is characterized by cartilage damage, changes in the subchondral bone, osteophyte formation, muscle weakness, and inflammation of the synovium tissue and tendon [1].
Although OA has long been considered as a primary disorder of articular cartilage, the contribution of subchondral bone to the physiopathology of OA is arousing interest [2]. Subchondral bone deterioration is commonly associated with articular cartilage defects [3], and subchondral bone sclerosis, together with progressive cartilage degradation, is widely considered as a hallmark of OA [4, 5]. Despite the increase in the number of trabeculae and bone volume, subchondral bone is hypomineralized and of inferior quality, as a consequence of abnormal local high bone turnover [6]. Some histopathological changes in the subchondral bone have also been detected, including microdamage, bone marrow edema-like lesions and bone cysts [7–9].
In this review, we summarize basic features of a functional joint unit comprised of subchondral bone and articular cartilage. We also discuss factors that influence the integrity of subchondral bone. Importantly, we focus on the microarchitectural and histopathological changes of subchondral bone in OA, and provide an overview of their potential contribution to the progression of OA.
The structure and function of subchondral bone
Subchondral bone plate is a thin cortical lamella, lying immediately beneath the calcified cartilage [12]. This cortical endplate is not an impenetrable structure, but possesses a marked porosity. It is invaded by channels that provide a direct link between articular cartilage and subchondral trabecular bone. A surprisingly high number of arterial and venous vessels, as well as nerves, penetrate through the channels and send tiny branches into calcified cartilage [3, 13]. The distribution and intensity of the channels depend not only on aging, but also on the magnitude of the compressive forces transmitting through cartilage and subchondral bone within and between joints [12]. These channels are preferentially concentrated in the heavily stressed areas of the joint. Channel shape and diameter also differs with the thickness of the cortical plate. Channels are narrower and form a tree-like mesh in regions where the subchondral plate is thicker, while they tend to be wider and resemble ampullae where the plate is thinner [12].
Arising from subchondral bone plate is the supporting trabeculae, which comprises subchondral trabecular bone, together with deeper bone structure [3]. Subchondral trabecular bone exerts important shock-absorbing and supportive functions in normal joints, and may also be important for cartilage nutrient supply and metabolism [10]. Relative to the subchondral bone plate, subchondral trabecular bone is more porous and metabolically active, containing blood vessels, sensory nerves, and bone marrow [2]. Subchondral trabecular bone has an inhomogeneous structure that varies with the distance from the articular surface. It exhibits significant structural and mechanical anisotropy; that is, the bone trabeculae shows preferential spatial orientation and parallelism [14].
Subchondral bone is a very dynamic structure and is uniquely adapted to the mechanical forces imposed across the joint. In addition to bone density patterns and mechanical properties, subchondral bone also dynamically adjusts trabecular orientation and scale parameters in a precise relationship with principal stress [15]. Mechanical stress also modifies the contour and shape of subchondral bone by means of bone modeling and remodeling [16].
The interaction between subchondral bone and articular cartilage
Articular cartilage overlies subchondral bone, and provides a vital function of maintaining homeostasis of the joint environment. It encompasses superficial non-calcified cartilage and deeper calcified cartilage. Calcified cartilage is permeable to small molecule transport, and plays an important role in the biochemical interaction between non-calcified cartilage and subchondral bone [17]. It is separated from non-calcified cartilage by a boundary called the 'tidemark', a dynamic structure that appears as a basophilic line in histological sections. The tidemark represents the mineralization front of calcified cartilage, and provides a gradual transition between the two dissimilar cartilage regions [18]. Continuous collagen fibrils cross the tidemark, indicating the strong link between non-calcified and calcified cartilage [3]. There is also a sharp borderline between calcified cartilage and subchondral bone, called the 'cement line' [19]. Unlike the tidemark, however, no continuous collagen fibrils cross the cement line.
Given the intimate contact between articular cartilage and subchondral bone, they form a closely composited functional unit called the 'osteochondral junction' [2] (Figure 1). The osteochondral junction is peculiarly complex, and consists of a deeper layer of non-calcified cartilage, the tidemark, calcified cartilage, the cement line and subchondral bone [18]. Alterations of either tissue will modulate the properties and functions of other parts of the osteochondral junction [20]. There is intensive biomechanical and biochemical cross-talk across this region that may play a role in maintenance and degeneration of the joint.
Subchondral bone and cartilage are dynamic stress-bearing structures that play complementary roles in load-bearing of joints [17]. Subchondral bone supports overlying articular cartilage and distributes mechanical loads across joint surfaces with a gradual transition in stress and strain. Stiffened and less pliable subchondral bone could transmit increased loads to overlying cartilage, leading to secondary cartilage damage and degeneration [11]. The load transmitted to underlying bone will also be substantially increased after articular cartilage damage or loss [21].
Although biomechanical coupling between subchondral bone and cartilage is well established, the biochemical interaction remains comparatively undefined. The permeability of calcified cartilage and subchondral bone plates allows crossover communication, and provides connecting channels between subchondral bone and cartilage [17]. In vivo studies showed that prostaglandins, leukotrienes and various growth factors released by osteoblasts during subchondral bone remodeling could reach overlying articular cartilage [22]. Accordingly, inflammatory and osteoclast stimulation factors released by articular cartilage may also lead to subchondral bone deterioration through increased bone remodeling in OA [5, 23].
Factors affecting subchondral bone integrity
OA is a progressive degenerative joint disease with different etiologies, and multifaceted risk factors have been suggested for the onset of OA, which include genetic predisposition, gender, aging, obesity, physical activity, previous joint injury, joint malalignment and abnormal joint shape [24]. These factors are reported to specifically influence subchondral bone.
Genetic predisposition
OA has been widely considered to be a polygenic disease, having an important hereditary component [25]. Inheritance studies involving family groups and twin pairs have revealed a considerable genetic contribution to the development of OA, with heritability estimates ranging from 39% to 78% at different joints [26–28].
Most of the candidate OA-associated genes reported to date relate to joint development and structural components of the joint [29]. Malformations in joint structure (for example, developmental dysplasia of the hip (DDH) and femoroacetabular impingement) caused by relative genetic mutations could lead to abnormal subchondral bone and contribute substantially to the susceptibility to OA by altering joint biomechanics [30–32].
In a transgenic Del1 mouse harboring a mutated Col2a1 gene (the type II collagen gene), augmentation of matrix metalloproteinase-13, cysts and sclerosis were detected in the subchondral bone of the knee joint at an early age [33, 34]. Mice with Col9a1 gene inactivation (the type IX collagen gene) were also reported to prematurely develop OA, with fibrillation or cartilage erosion extending to subchondral bone [35]. However, the impact of genetic predisposition on the integrity of subchondral bone in humans has not been extensively investigated.
Men are reported to have a higher prevalence of OA than women before the age of 50 years, but after this age the prevalence is higher in women, which coincides with menopause [36–38]. Accordingly, estrogen deficiency occurring with menopause has been associated with an increased incidence and severity of OA in women [39]. Postmenopausal women taking estrogen replacement therapy exhibit a reduced risk of hip and knee OA, compared with those not taking it [40, 41].
In animal experiments, estrogen depletion by ovariectomy has been related to high bone remodeling, structure deterioration and weakened biomechanical properties in subchondral trabecular bone of joints [42, 43]. Estrogen depletion could also enhance subchondral bone plate thinning, especially when an additional OA trigger is applied [44]. In a cynomolgus macaque model, estrogen replacement therapy was reported to decrease bone remodeling and preserve bone mass in subchondral bone [45]. A cross-sectional study has also shown that elderly women receiving estrogen had a significantly decreased prevalence of knee OA- related subchondral bone attrition and bone marrow edema-like abnormalities [46].
Aging is considered as a primary risk factor for OA, due to loss of normal bone structure and accumulation of bone microdamage [47]. The microarchitecture of subchondral trabecular bone in joints has a significant dependence on aging, which is characterized by a decrease in trabecular thickness and bone volume fraction, loss of connectivity, increased trabecular separation and bone marrow space volume, transformation of trabeculae from plate-like into rod-like, and an increase in anisotropy degree [48].
However, opinions differ and Crane and colleagues [49] suggested that OA changed the close relationship between age and trabecular bone structure. To illustrate, bone volume fraction of trabecular bone in the proximal femur in those with OA did not depend on age. Further, Perilli and colleagues [50] recently demonstrated that neither structural parameters nor mechanical properties of trabecular bone in the osteoarthritic femoral head depend on age. This phenomenon may be due to altered mechanical factors in the joints with OA, which inhibit age-related bone loss when mechanical stresses are relatively higher [51].
Obesity is a significant risk factor for OA, especially in the knee [52]. However, the relationship between obesity and OA in the hand and hip remains controversial [53, 54]. Traditionally, increased compressive stresses on weight-bearing joints due to increased body weight and fat mass is thought to influence obesity-associated OA progression [55]. Recently, attention has shifted to the potential influence of metabolic dysfunction on the progression of obesity-associated OA [56]. It has been suggested that the early stage of obesity-associated OA is more strongly influenced by body weight and fat mass, while metabolic dysfunction is more important in the late stage of OA in which cartilage degeneration becomes more severe [57].
A matched case-control cohort study evaluated the relationship between obesity and bone strength and microarchitecture in postmenopausal women. The increase of absolute values of all bone parameters was not in proportion to excess weight, leading to relative bone fragility [58]. The negative effect of obesity on bone health may be attributed to inflammatory cytokines, increased abnormal fat acid and adipokines [59]. Specifically, Dequeker and colleagues [60] speculated that subchondral bone stiffness was greater due to increased biomechanical loads in obese individuals and this rendered bone less able to cope with higher impact loads. However, the precise impact of obesity on the microarchitecture and pathology of subchondral bone requires further investigation.
Physical activity
Numerous studies have investigated the relationship between physical activity and OA. However, whether physical exercise alone induces OA remains highly controversial. In general, moderate bearing loading exercise protects against OA [61], while non-physiological loading or joint abuse is detrimental and increases the risk of developing OA [62].
In one cross-sectional study of runners, tibia diaphyseal volumetric bone mineral content, cortical area and polar moment of resistance were highest in sprinters, followed in descending order by middle and long distance runners, race-walkers and controls. This was considered to be due to an adaption to 'exercise specific peak forces' experienced during running [63]. In a canine experiment, running enhanced bone remodeling in subchondral bone regions, resulting in thicker subchondral bone plate and higher trabecular volume [64]. Subchondral bone responds to the stress of exercise by increasing bone formation and density in an attempt to increase strength [65]. Exercise during the critical years of growth and development may be instrumental for subchondral bone modeling, and might assist in reducing the risk of OA later in life [66].
However, exercise may have varying effects on joints, depending on the mode, rate, intensity and duration of the activity [14]. Abnormal impulsive loading was reported to induce high bone remodeling, microdamage and vascular invasion in subchondral bone, which eventually reduced its elasticity and led to subchondral bone sclerosis [9, 67, 68]. Racehorses running long distances at high speeds exhibited tremendous changes within the subchondral bone in the carpal and metacarpophalangeal joints, including osteochondral fragmentation and fracture, subchondral bone necrosis and sclerosis [69, 70].
Joint injury
Joint injuries, including intra-articular fractures, meniscal tears, ligamentous damages, and traumatic cartilage injuries, all increase the risk of progressive joint degeneration that causes post-traumatic OA [71].
Joint injuries not only lead to cartilage degeneration, but also have negative effects on subchondral bone. In a mouse model, intra-articular fractures caused subchondral bone thickening and sclerosis in the knee [72]. In a canine model, transarticular impact below the joint fracture threshold led to subchondral bone bruises [73]. Based on clinical experience and epidemiologic studies, many OA animal models have been developed through cruciate ligament transection and meniscus destabilization, in which abnormal changes of subchondral bone are detected [74, 75].
In humans, meniscal damages may lead to subchondral bone pathological changes, including increased bone mineral density, bone cysts and bone marrow lesions [76, 77]. Traumatic ligament injuries also jeopardized subchondral bone integrity, causing microdamage [78]. Radiological evidence also supports that traumatic cartilage injuries have a close relationship with subchondral bone damage (for example, subchondral edema) [79].
Joint malalignment
OA is a quantitative or qualitative abnormality in intra-articular stress that may be caused by a host of factors, such as joint malalignment. The mechanical abnormality overwhelms innate physiologic mechanisms for repairing damaged joint tissues [24].
In a population study of 2,644 knees, both valgus and varus alignment, resulting from genetic, developmental, and traumatic factors, were found to be highly associated with the development of OA [80]. It is not the malalignment per se that is detrimental to the joint, but the excessive concentration of stress on the articular cartilage and underlying bone. Malalignment seems to be associated with subchondral bone attrition [81]. Increased mechanical stress by malalignment would give rise to microcracks of subchondral bone, leading to abnormal bone remodeling [82]. In a longitudinal study of the knee, intra-osseous lesions were widely detected in subchondral bone adjacent to abnormal, malaligned joints [83].
Abnormal joint shape
Joint shape has been considered as a key predictor of OA for five decades, and joint shape is in turn altered by the disease, leading to an intricate interplay between joint shape and OA [84]. Joint shape is under tight genetic control, including genes such as those encoding bone morphogenetic proteins or members of the Wnt signaling family [85]. A cross-sectional survey across a wide age range (22 to 93 years), reported that hip dysplasia-associated malformations (for example, DDH, acetabular dysplasia, pistol-grip deformity) constituted significant risk factors for the progression of hip OA [86].
Subchondral bone is widely believed to be able to adapt its structure to acting loads as well as to joint shape [87]. During the development of hip dysplasia observed in a canine model, abnormal weight bearing forces caused subcondral bone fractures and subsequent sclerosis in both femoral head and acetabulum [31]. In a study of human femoral heads with late-phase DDH, synchrotron radiation micro-computed tomography identified many large and small cysts in sclerotic subchondral bone [88].
Microarchitectural changes of subchondral bone in osteoarthritis
Despite the focus on the contribution of subchondral bone to the pathogenesis of OA for over four decades, there remains a controversy over its role: is it a trigger factor or a secondary consequence of cartilage degeneration [3]? Irrespective of the precise mechanism, subchondral bone is believed to play a vital role in OA pathogenesis. Subchondral sclerosis is commonly considered an indisputable sign of OA [77]. However, some studies suggest that different microarchitectural alterations of subchondral bone occur during different stages of OA; subchondral sclerosis may be observed only during more advanced stages of OA [89].
In early stages of OA in humans, elevated bone remodeling and subchondral bone loss was observed, and was considered as a determinant of OA progression [6]. In a rabbit model with preceding osteoporosis, subchondral bone microstructural damage by increased remodeling aggravated experimental OA [23]. Temporal subchondral bone loss in early OA was also documented in a number of different animal models [78, 89, 90]. Specifically, thinning and increased porosity of the subchondral bone plate were detected, which are testified to be strongly associated with cartilage damage [89]. However, the subchondral bone plate remained thin in the feline OA knee joint [78], while other animals showed a subsequent thickening of the cortical plate with OA progression [77, 90]. In the underlying subchondral trabecular bone, increased trabecular separation, decreased bone volume fraction and trabecular thickness in subchondral trabecular bone were detected in these animal models, in contrast with previous concepts [77, 78, 89, 90]. A high incidence of microdamage (highly associated with subchondral bone stiffening and cartilage degeneration) was also reported in the subchondral bone of patients with early OA [91].
Although the underlying mechanism for the increased bone turnover and structural deterioration in the early phase of OA is not fully understood, several factors have been implicated, including microdamage repair [92], increased vascularity stimulated by angiogenic factors [93] and enhanced bone-cartilage crosstalk via increased subchondral plate pores [17, 18]. Further, it has been suggested that elevated bone remodeling and its associated stimulated vascularity are indispensable for the progression of OA, rather than subchondal sclerosis [4].
Despite increased bone volume density in the so-called 'sclerotic' subchondral bone, its mineralization is reduced and lower than that in normal or even osteoporotic joints [95]. Although collagen synthesis is elevated in subchondral bone, the deposited collagen is hypomineralized and has a markedly reduced calcium-to-collagen ratio [96]. When tested mechanically, subchondral bone stiffness is also low, based on its higher volume fraction [95]. One theory is that bone volume density increases as a mechanoregulatory bone adaptation/compensation in response to decreased mineralization and reduced bone stiffness [97]. Decreased mineralization and reduced bone stiffness result from accelerated bone turnover in OA joints. The lowered subchondral bone modulus may contribute to cartilage degeneration [98], challenging the previous concept that increased subchondral stiffness drives the process of cartilage damage in OA [91].
Bone marrow edema-like lesions of subchondral bone in osteoarthritis
Bone marrow edema-like lesions (BMELs), which are strongly associated with pain among patients with OA, are frequently identified by magnetic resonance imaging (MRI) in patients with progressive OA [99]. BMELs are also observed in the healthy, asymptomatic population, and predict an increased risk of OA [100]. The exact pathogenesis of BMELs is unclear. However, damaged cartilage, an inflammatory reaction to cartilage breakdown products or other factors in intruded synovial fluid, and microtraumatic changes associated with altered biomechanics, may contribute to the formation of BMELs [101].
Histological changes of bone marrow edema-like lesions in osteoarthritic subchondral bone
Bergman et al.[105]
1.Thickening trabeculae
2. Bone marrow fibrosis
Zanetti et al.[106]
1. Normal tissue: fatty marrow (53%), intact trabeculae (16%), blood vessels (2%)
2. Abnormal tissue: bone marrow necrosis (11%), necrotic or remodeled trabeculae (8%), bone marrow fibrosis (4%), bone marrow edema (4%), bone marrow bleeding (2%)
Hunter et al.[104]
1. Sclerotic trabeculae
2. Abnormal marrow infiltration: granulation, edema, diffuse necrosis, fibrosis, hyperplasia of blood vessel walls
Kazakia et al.[107]
1. Sclerotic trabeculae
2. Abnormal marrow infiltration: fibrous collagen, woven bone
Nolte-Ernsting et al.[108]
1. Osteosclerosis
2. Intra-osseous cysts
3. Abnormal marrow infiltration: fibrosis, new bone formation
Baird et al.[109]
1. Remodeled trabeculae
2. Myxomatous fibro-reactive marrow, increased hemato/myelopoietic elements and vascular congestion
Martig et al.[110]
Hematopoiesis and myxomatous transformation of the bone marrow, fibrosis
BMELs are consistently and fundamentally involved in development of OA, and are considered as an important risk factor for structural deterioration [8, 107]. Focal cartilage lesions are preferentially located in proximity to BMELs, and the level of cartilage degradation is proportional to BMEL signal intensity [111]. BMELs also have a profound relationship with subchondral bone cysts (SBCs), which could develop in pre-existing regions of BMELs [112].
Subchondral bone cysts in osteoarthritis
Plewes first identified SBCs in subchondral bone adjacent to osteoarthritic joint surfaces in 1940 [114]. Despite the continuous focus on SBCs in OA over seven decades, the exact etiology and pathogenesis of these lesions are still unclear. There are two main conflicting hypotheses that explain the origin of SBCs in OA. The 'synovial fluid intrusion' theory proposes that synovial fluid intrudes into subchondral bone and leads to formation of SBCs, which is due to the breach of the osteochondral junction [115]. The 'bone contusion' theory suggests that SBCs originate from the necrotic lesions in subchondral bone, which are induced by abnormal mechanical stress and subsequent microcracks, edema and focal bone resorption [116].
However, the term 'subchondral bone cysts' is not accurate, as the cavitary lesions in subchondral bone do not have an epithelial lining and are not uniformly fluid filled [117]. As such, they are also described as 'intra-osseous lesions', 'pseudo-cysts' or 'geodes' [117, 118]. SBCs are composed of fibroconnective tissue that may initially contain fluid but ossify in later stages [7]. SBCs appear as well-defined areas of fluid signal on MRI, which correspond to well-defined lucent areas with sclerotic rims on radiographic images [112]. They appear at sites of greatest cartilage loss, in both human [113] and animal models [7]. SBCs are also shown to be associated with high bone mineralization and bone turnover [88]. Osteoclastic bone resorption, activated osteoblasts and new bone formation were detected to be present surrounding SBCs in OA [119, 120] (Figure 3C, D).
Microdamage of calcified cartilage and subchondral bone in osteoarthritis
Linear microcracks, defined as short interstitial cracks, play a vital role in the initiation and progression of OA [9]. In general, microcracks have two main functions: first, they act as a nidus for the initiation of bone remodeling [92]; and second, they provide a conduit for the physiological communication between cartilage and subchondral bone, with more catabolic agents crossing the osteochondral junction, which may be accelerated by accompanying vascular invasion and cutting cones into cartilage [4]. The mechanism for the promotion of bone remodeling by microcracks may involve damage to osteocyte canalicular processes and subsequent osteocyte apoptosis, which may induce osteoclastic resorption and microcrack repair [92]. The high bone turnover induced by microcracks leads to the thickening of subchodral plates and calcified cartilage with tidemark advancement, which eventually causes thinning of cartilage [123].
Diffuse microdamage, present in the form of a range of submicron-sized cracks, is also detected in subchondral trabecular bone in osteoarthritic joints [124]. It is primarily located in tensile regions and contributes to the deterioration of bone mechanical properties [125]. However, diffuse damage has a different biomechanical response, compared with linear microcracks. Diffuse microdamage does not lead to osteocyte apoptosis, nor does it activate focal bone remodeling activities to remove and replace the damaged area [122].
Subchondral bone is an intricate structure consisting of a dome-like subchondral plate and underlying trabeculae, which enjoys a close biomechanical and biochemical relationship with overlying cartilage. Subchondral bone plays a vital role in the pathogenesis of OA. Strong evidence associates subchondral bone alterations with cartilage damage and loss in OA. At the microstructure level, subchondral bone changes are not consistent between the initiation and progression periods of OA. Subchondral sclerosis is widely considered as a main feature of late-stage OA, while early-stage OA is characterized by a thinning subchondral plate with increased porosity and deteriorated subchondral trabeculae with decreased bone density. Histopathological alterations in the subchondral bone, including BMELs, SBCs and microdamage, are also highly associated with the progression of OA.
As an important pathological lesion, SBCs have been underestimated in the pathogenesis of OA and should be closely considered more seriously in future research. SBCs may expand upwards, and damage subchondral plate and calcified cartilage, facilitating more biochemical catabolic molecule transportation between subchondral bone and cartilage. This would contribute to structural change across the whole joint. In addition, the inhomogeneity of the subchondral plate and calcified cartilage, which is caused by intruding SBCs, microdamage and penetrating pores, could lead to high tensile and shear stresses at the bone-cartilage interface. The abnormal stress distribution of the bone-cartilage interface will degrade the overlying cartilage and cartilage damage could, in turn, influence subchondral bone deterioration. This vicious circle leads to the progression of OA. Collectively, the optimal strategy may therefore be to promote the maintenance of subchondral bone integrity.
Given that the importance of subchondral bone in OA has been recognized for over four decades, the progression in this area is far from satisfying. The fundamental science and pathophysiology of subchondral bone in OA warrants further investigation. It is only through a better understanding and appreciation of the role of this often overlooked structure in the development and progression of OA that we will be able to effectively prevent, diagnose and treat this disease.
Bone marrow edema-like lesion
Developmental dysplasia of the hip
Magnetic resonance imaging
Subchondral bone cyst.
The authors thank Prof. Heather A McKay from the Department of Orthopedics, Centre for Hip Health and Mobility, University of British Columbia for critical comments of important intellectual content and Dr Julia S Kuliwaba from Discipline of Anatomy and Pathology, School of Medical Sciences, The University of Adelaide for provision of microdamage images.
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Black & Graham, LLC
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Christian A. Schwaner, P.C.
Colorado Springs, Colorado Criminal Defense Attorney(719) 577-9700
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Hebets & McCallin
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Fort Collins Criminal Defense Lawyer(970) 279-1968
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Edward Levy, PC
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Fife Luneau, P.C.
Colorado Criminal and DUI Defense Lawyers(303) 945-3050
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Flesch Law
Colorado Criminal Defense Lawyer(720) 689-0322
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Gerash Steiner, P.C.
Denver Personal Injury, Medical Malpractice, & Criminal Defense Trial Attorneys(303) 732-5048
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James L. Finegan, PC
Lakewood, Colorado Personal Injury Attorney(303) 980-5511 or (877) 834-4609
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subset: commoncrawl


text:
Yellow Page contacts
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LinkedIn: Alan Geldard | LinkedIn
View Alan Geldard's (Australia) professional profile on LinkedIn. LinkedIn is the world's largest business network, helping professionals like Alan Geldard ...
All-Time Olympic Results - USA Cycling
Points - Individual
British Cycling
Alan Geldard Bio, Stats, and Results | Olympics at...
Medals: 1 Bronze (1 Total); Sport: Cycling; Country: Great Britain; Years: 1948; See page for full bio and event results.
Business Profiles
Alan Geldard | Forkwest | ZoomInfo.com
View Alan Geldard's business profile at David Evans Group and see work history, affiliations and more.
Overview for Alan Geldard
Get biography information about Alan Geldard on tcm.com
Filmography for Alan Geldard
Cold Sweat (1993) as Boom Operator A former political soldier turned professional hitman reluctantly takes a contract for one last hit, but what seemed like a ...
Private Homepages
Olympische Spiele - Radsport - 4000m…
Alan Geldard/Thomas Godwin/David Ricketts/Wilfred Waters: 4:55.8 : Berlin 1936 : Gold: France: Robert Charpentier/Jean Goujon/Guy Lapebie/Roger Le Nizerhy
Lowthers Contact
Lowthers IT offer expert technical support for all IT related products and services for home users and small businesses across the North West.
WM - Radsport - 4000m…
Alan Geldard/Thomas Godwin/David Ricketts/Wilfred Waters : 1936 OS: Gold: France: Robert Charpentier/Jean Goujon/Guy Lapebie/Roger Le Nizerhy: Silver
Contact Schaffer Loaders - Front End Loaders - Wheel Loaders
Schaffer Loaders Australia is based in Perth, Western Australia with dealers across the country. Please contact us with your enquiries. Schaffer Loaders is...
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(1 - 2 from 3
Wikipedia: Alan Geldard
Robert Alan Geldard (born 1927) is a British cyclist. He was born in Manchester. He won a bronze medal in the team pursuit at the 1948 Summer Olympics in London, together with David Ricketts, Tommy Godvin and Wilfred Waters.
Alan Geldard | Biography and Filmography - Hollywood.com
Biography. Filmography. Sound (1). Cold Sweat 1993 (Movie). (Boom Operator) ...
Family Tree for Alan Esdale Geldard - WikiTree
www.wikitree.com/genealogy/Geldard-Family-Tree-4 Cached Genealogy of Alan Geldard born 1911 in Colne, Lancashire England.
Helen Geldard - 1901 England Census - Ancestry.co.uk
Walter Alan Geldard, Emily, abt 1875, city, Yorkshire, England, info, city, Yorkshire. View Record. Allen Geldard, Allen, Ann, abt 1882, city, Lancashire, England ...
Alan Alfred Gellert - Australia, Electoral Rolls, 1903-1980 -...
Alan Alfred Gellert - Australia, Electoral Rolls, 1903-1980
Books & Literature
Rules of the Hunt (book) by Hugh T McCracken on AuthorsDen
Rules of the Hunt, A group of modern-day schoolboys is thrown back through a time portal to thirteenth century Scotland where they become the quarry in the...
Olímpicos: Historias asombrosas y divertidas anécdotas sobre...
Historias asombrosas y divertidas anécdotas de héroes de carne y hueso sobre medallistas olímpicos Hace cerca de tres mil años una antorcha se encendió en...
The Palgrave Handbook of Olympic Studies - Google Books
A comprehensive, state-of-the-art reference collection, bringing together an authoritative and international line-up of scholars to examine key social and...
The Austerity Olympics: When the Games Came to London in 1948 - Janie...
DIV'An enthralling account' Independent 'A fascinating book… researched with an awesome thoroughness' Daily Telegraph 'Hampton's excellent book should be...
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The Polishers Rag 2011 04 web - darling downs veteran ...
Maree & Clyde Baker, Alan Geldard, Merv & Denise Klein and. Brad McKeiver at Rotary Park, Oakey. Neil & Maree Hamilton and one of their ...
The Polishers Rag 2012 04 print.indd - darling downs ...
Keith & Shane Hoffmann,. (FC Holden). 3rd. Pat & Lynne Murphy. (XP Falcon). 4th. Bill & Del Fischer. (FJ Holden). 5th. Alan Geldard. (29 Chev) ...
Harvest rally - December 2011 Page 1 Dedicated to the life-long ...
Dating officer: Des dated a 1929 Chevrolet for Alan Geldard. Swap: Budget for the swap suggested including pre booking monies, float, sponsorship, etc to be transferred to
Alan Geldard - WikiVisually
Rochdale, Lancashire. He won a bronze medal in the team pursuit at the 1948 ...
Davies does it again. - Free Online Library
Davies, who had to make do with the bronze medal in the Pursuit at the World Masters last September but won the Alan Geldard Trophy 20km at the same event, once again had to ...
Alan Geldard - Wikidata
Alan Geldard (Q325534)[edit]. No description defined yet [edit] ... norsk bokmål, nowiki, Alan Geldard, [edit]. polski, plwiki, Alan Geldard, [edit] ...
Video & Audio
Alan Geldard was part of the bronze medal wining team in the 1948...
Alan Geldard was part of the bronze medal wining team in the 1948 Olympics Watch more videos like this at http://www.kyte.tv/ch/video/alan-geldard-was-part-o...
(1 - 4 from 21
Alan Geldard: We could have won gold, I feel it in my bones | The ...
London, but missing out on gold still hurts.
Alan-Geldard: Latest News, Videos and Alan-Geldard Photos ...
Alan-Geldard profile at Times of India.
Guardian: Tommy Godwin obituary | Sport | The Guardian
raced with Dave Ricketts, Alan Geldard and Wilf Waters.
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Twitter Posts: PCSO 8196 Beckett (ManorArbourPCSO)
26.06.2012 Been an amazing experience working #olympictorch. As a cyclist & cycling fan the highlight was seeing Alan Geldard, bronze winning cyclist.
Twitter Posts: World Track Masters (masterstrack)
25.06.2012 Just been watching the live feed from Sheffield of Alan Geldard carrying the Olympic Torch.
Twitter Posts: cheryl moulton (cherylmoulton1)
20.06.2012 @Trafford_2012 Alan Geldard
Wikipedia: Alan Geldard – Wikipedia, wolna encyklopedia
wspólnie z Thomasem Godwinem, Davidem Rickettsem i Wilfem Watersem zdobył ...
(1 - 20 from 54
Alan Geldard Meaning - Name Alan Origin
path of the name Alan. Read about the name Alan Geldard meaning.
Baanwielrennen - Alan Geldard (Groot-Brittannië) - Sportuitslagen.org
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Alan Geldard's original opening ceremony ticket ... - Panos Pictures
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was born in Rochdale, Lancashire.
Alan Geldard - TuttoSu - Virgilio
August 2016.Il vincitore del.....Rio 2016, Froome: "Le...
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https://udgie.com/982098/alan-geldard Cached Offerings made to for words and actions in the public eye - udgie.com.
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life path number this name has. Learn what the first name Alan means.
Alan Geldard | Wiki | Everipedia, the encyclopedia of everything
cyclist. He was born in Rochdale, Lancashire. He won a bronze ...
Cyclisme sur piste - Alan Geldard (Grande Bretagne) - Les-Sports.info
les données présentes sur Les-Sports.info qui peuvent être incomplètes.
Gregory Alan Geldard - Australian Sole Traders
Centenary Heights Charlton Clifford Gardens Cotswold Hills
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Building 120 Wood St, Mackay, QLD 4740.
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wooster's review of Avene Cold cream ultra-rich cleansing gel
77 reviews
71% would repurchase
Package Quality: 4.1
Price: $$
Package Quality: 4.1
Price: $$
INGREDIENTSAvene thermal spring water, disodium cocamphodiacetate, myristic acid, peg-7 glyceryl cocoate, coco-glucoside, glycerin, sodium cocoyl isethionate, isohexadecane, cocamidopropyl dimethylaminohydroxypropyl hydrogenated collagen, sodium lauryl sarcosinate, ceteareth-60 myristyl glycol, beeswax, cetyl alcohol, orange oil, glyceryl stearate, propylparaben, rosemary leaf oil, salt, styrene/acrylates copolymer, triclosan, xanthan gum
Age: 30-35
Skin: Combination, Fair, Not Sure
Hair: Blond, Other, Other
Eyes: Blue
This made me look like I had been burnt!! It's a shame as so many reviewer rave about it so I was hoping it would be perfect for my sensitive skin. I came up in lots of red lumps & face stung so bad that I had to take an antihistamine. I gave it to my sister and the same thing happened to her.
Read all 77 reviews of Cold cream ultra-rich cleansing gel
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text:
Shrimp in Green Cheese Sauce
|Cooked medium shrimp
|1 Pound, shelled and chilled
|Ripe avocado
|1 Small, peeled and mashed
|Cream cheese
|3 Ounce, softened (1 Package)
|Lime juice
|1 Teaspoon
|1 Dash
|Ground pepper
|To Taste
|Minced cilantro/Parsley
|1 Tablespoon
|To Taste
Arrange shrimp on serving platter.
Combine avocado, cream cheese, lime juice, tequila, salt and pepper and blend thoroughly.
Serve sauce over shrimp or on the side, garnished with cilantro or parsley.
Recipe Summary
Rate It
Nutrition Rank
Nutrition Facts
Serving size: Complete recipe
Calories 918 Calories from Fat 431
% Daily Value*
Total Fat 50 g76.5%
Saturated Fat 20 g100%
Trans Fat 0 g
Cholesterol 978.1 mg326%
Sodium 1691.6 mg70.5%
Total Carbohydrates 14 g4.7%
Dietary Fiber 7.8 g31.3%
Sugars 3.7 g
Protein 102 g204.9%
Vitamin A 65.4% Vitamin C 44.1%
Calcium 28.8% Iron 86%
*Based on a 2000 Calorie diet


text:
Society for Economic Dynamics
2005 Meeting Papers
Postal: Society for Economic Dynamics Marina Azzimonti Department of Economics Stonybrook University 10 Nicolls Road Stonybrook NY 11790 USA
Web page: http://www.EconomicDynamics.org/
More information through EDIRC
Web page: http://www.EconomicDynamics.org/
More information through EDIRC
For corrections or technical questions regarding this series, please contact (Christian Zimmermann)
Series handle: repec:red:sed005
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- 242 Housing and the Macroeconomy: The Role of Implicit Guarantees for Government Sponsored Enterprises
by Dirk Krueger & Karsten Jeske
- 241 Job Mobility and Wage Dynamics
by Luigi Pistaferri
- 240 Capital Flows to Developing Countries: the Allocation Puzzle
by Olivier Jeanne & Pierre-Olivier Gourinchas
- 24 Land Inequality and the Origin of Divergence and Overtaking in the Growth Process: Theory and Evidence
by Oded Galor & Omer Moav
- 238 The Local Dynamics of Culture
by Onur Ozgur & Alberto Bisin
- 235 U.S. Inequality: Debt Constraints or Incomplete Markets?
by Juan Carlos Cordoba
- 234 Cultural Biases in Economic Exchange
by Luigi Guiso & Paola Sapienza & Luigi Zingales
- 233 A Theory of Stability in Many-to-Many Matching Markets
by Jorge Oviedo & Federico Echenique
- 232 Semiparametric Estimation of Two-Sided Matching Models with Endogenous Prices
by Jeremy T. Fox
- 231 Accounting for the Changing Life-Cycle Profile of Earnings
by Iourii Manovskii & Gueorgui Kambourov
- 230 Firm Volatility and Wage Inequality
by Thomas Philippon & Fatih Guvenen
- 23 Dual Inflation and the Real Exchange Rate in New Open Economy Macroeconomics
by Balazs Vilagi
- 229 Fiscal Policy Amplified Shocks in Emerging Markets
by Gita Gopinath & Mark Aguiar & Manuel Amador
- 228 The Value of Information in Credit Markets
by Jose Wynne
- 227 Search Frictions and Asset Price Volatility
by B. Ravikumar & Enchuan Shao
- 226 Copyrights, Price Discrimination and Hidden Trading: Lessons from a Ricardian Theory of Innovation
by V. V. Chari & Mike Golosov
- 225 Experimentation and Observational Learning in a Market with Exit
by Juuso Valimaki & Pauli Murto
- 222 Reputation and Price Dynamics in Financial Markets
by Andrea Prat & Amil Dasgupta
- 220 Understanding Consumption Inequality and Income Inequality: A Human Capital Approach
by Burhanettin Kuruscu & Fatih Guvenen
- 22 No-Arbitrage Taylor Rules
by Andrew Ang & Sen Dong
- 219 Firm Entry and Finance: Distinguishing Information Regimes
by Robert Townsend & Alexander Karaivanov
- 218 Assortative Matching with Explicit Search Costs
by Alp Atakan
- 214 Measuring and Mismeasuring Industry Productivity Growth Using Plant-Level Data
by Amil Petrin & James Levinsohn
- 211 Rising Earnings Instability and Prices of Housing and Financial Assets
by Makoto Nakajima
- 21 Sovereign Defaults: Information, Investment and Credit
by Guido M. Sandleris
- 209 Inefficiency in Legislative Policy-Making: A Dynamic Analysis
by Stephen Coate & Marco Battaglini
- 208 Credible Group Stability in Multi-Partner Matching Problems
by Utku Unver & Hideo Konishi
- 207 What Makes You Click? An Empirical Analysis of Online Dating
by Guenter Hitsch & Ali Hortacsu
- 206 Amplification of Labor Market Fluctuations: Why Vacancies Don't Like to Hire the Unemployed?
by Eva Nagypal
- 205 Social Preferences, Skill Segregation, and Wage Dynamics
by Antonio Cabrales & Antoni Calvo-Armengol & Nicola Pavoni
- 204 Optimal Taxation with Persistent Shocks
by Marek Kapicka
- 203 Dynamic Optimal Taxation of Productive Assets
by Stefania Albanesi & Christopher Sleet
- 202 Optimal Taxation with Limited Memory
by Christopher Sleet & Stefania Albanesi
- 201 Trade Costs, Pricing to Market, and International Relative Prices
by Ariel Burstein & Andrew Atkeson
- 199 The Product Cycle and Inequality
by Boyan Jovanovic
- 198 Lobbying and Technology Diffusion
by Bart Hobijn & Diego Comin
- 197 An Anatomy of International Trade: Evidence from French Firms
by Francis Kramarz & Jonathan Eaton & Samuel Kortum
- 196 Offshoring in a Knowledge Economy
by Esteban Rossi-Hansberg & Pol Antras & Luis Garicano
- 195 A Life-Cycle Theory of Household Size: United States 1850-2000
by Michele Tertilt & Todd Schoellman
- 192 Reflections on Economic Growth
by Robert Lucas
- 190 Varieties, Terms of Trade and Growth
by David Weinstein & Christian Broda
- 19 Colonies
by Andrea Eisfeldt & Matthias Doepke
- 189 Living Arrangements in Western Europe: Does Cultural Origin Matter?
by Paola Giuliano
- 188 Job Displacement Risk and the Cost of Business Cycles
by Tom Krebs
- 187 The Surprising Dynamism of the Malthusian Economy: England, 1200-1800
by Gregory Clark
- 186 Private Debt and Idiosyncratic Volatility: A Business Cycle Analysis
by Matteo Iacoviello
- 184 International Asset Portfolios: A Dynamic General Equilibrium Perspective
by Robert Kollmann
- 182 Modeling Inventories Over the Business Cycle
by Julia K. Thomas & Aubhik Khan
- 18 Haircuts
by Jeromin Zettelmeyer & Federico Sturzenegger
- 179 The Great Synergy: The European Enlightenment as a Factor in Modern Economic Growth
by Joel Mokyr
- 178 Borrowing Constraints, Durables, and the Business Cycle
by Dirk Krueger & Jesus Fernandez-Villaverde
- 175 How Large are Search Frictions
by Pieter Gautier & Coen Teulings
- 174 Market Expectations and Currency Crises: Theory and Empirics
by Bernardo Guimaraes
- 173 Approximate Generalizations in Applied Equilibrium Analysis
by Felix Kubler
- 172 Financial Crises and Interest Rates
by Christian Hellwig & Arijit Mukherji
- 170 Inflation and Interest Rates with Endogenous Market Segmentation
by Julia K. Thomas & Aubhik Khan
- 17 Estimating the Response of Bequests to Early and Late Income Shocks
by Ernesto Villanueva & Joseph G. Altonji
- 169 International Financial Adjustment
by Helene Rey & Pierre Olivier Gourinchas
- 162 Spousal Matching, Marriage Contracts and Divorce: A Collective Household Approach
by Pierre-Andre Chiappori & Murat Iyigun
- 161 Competition, Innovation and Growth with Limited Enforcement
by Vincenzo Quadrini & Ramon Marimon
- 158 Unemployment Insurance under Moral Hazard and Limited Commitment:Public versus Private Provision
by Tim Worall & Jonathan P Thomas
- 156 Informal Insurance in Social Networks
by Francis Bloch & Garance Genicot
- 152 Globalization and Emerging Markets: With or Without Crash?
by Helene Rey & Philippe Martin
- 148 Two-Fund Separation in Dynamic General Equilibrium
by Karl Schmedders
- 146 An Assignment Theory of Foreign Direct Investment
by Stephen Yeaple & Volker Nocke
- 144 Estate taxes, entrepreneuship, and wealth
by Mariacristina De Nardi & Marco Cagetti
- 143 Asset Prices and Liquidity in an Exchange Economy
by Ricardo Lagos
- 141 Career Progression and Formal versus On the Job Training
by J. Adda & C. Dustmann
- 138 Sovereign Default and Debt Renegotiation
by Vivian Z. Yue
- 135 Search, Money, and Inflation under Private Information
by Huberto M. Ennis
- 132 A Tale of Two States
by Amartya Lahiri & Kei-Mu Yi
- 131 Why are Some Cities So Crowded?
by Jordan Rappaport
- 129 Income Redistribution and Disability Insurance
by Juan Carlos Hatchondo & Hugo Hopenhayn
- 127 Time Consistent Fiscal Policy and Heterogeneous Agents
by Roc Armenter
- 124 Three Equations Generating an Industrial Revolution
by Aubhik Khan & Michele Boldrin & Larry E. Jones
- 123 Human Capital Risk, Stockholder Consumption, and Asset Returns
by Christopher Malloy & Tobias Moskowitz
- 122 Consumption Commitments: Neoclassical Foundations for Habit Formation
by Adam Szeidl & Raj Chetty
- 121 Optimal Policy Under Sticky Prices: How to Get Accurate Solutions
by Michael Reiter
- 120 The Role of Collateralized Household Debt in Macroeconomic Stabilization
by Zvi Hercowitz & Jeffrey C. Campbell
- 118 Inflation Differentials and Labor and Product Market Differences in the EMU
by Ester Faia & Alessia Campolmi
- 117 Sticky Demand or Sticky Prices?
by Chris Edmond
- 116 A Likelihood-Based Evaluation of the Segmented Markets Friction in Equilibrium Monetary Models
by Filippo Occhino & John Landon-Lane
- 115 Current Account Fact and Fiction
by David Backus & Espen Henriksen & Frederic Lambert & Chris Telmer
- 113 Heterogeneity within Communities: A Stochastic Model with Tenure Choice
by Sven Rady & Francois Ortalo-Magne
- 112 Globalization and Democracy, 1870-2000
by Christopher M. Meissner & Jose Ernesto Lopez Cordova
- 110 Wage-Tenure Contracts, Experience and Employment Status
by Carlos Carrillo-Tudela
- 11 Mechanism Design and Payments
by Thorsten Koeppl & Cyril Monnet & Ted Temzelides
- 108 Endogenously Segmented Asset Market in an Inventory Theoretic Model of Money Demand
by Jonathan Chiu
- 107 Insurance and Opportunities: The Welfare Implications of Rising Wage Dispersion
by Jonathan Heathcote & Kjetil Storesletten
- 105 The Returns on Human Wealth: Good News on Wall Street is Bad News on Main Street
by Stijn Van Nieuwerburgh & Hanno Lustig


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