' ' ' ' ' ' ' ' ' ' ' ' s p s U M OSTEOPOROSIS: PATHOPHYSIOLOGY AND BONE REMODELLING
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1 ' s p s U M ' OSTEOPOROSIS: PATHOPHYSIOLOGY AND BONE REMODELLING Louis~Georges Ste~Marie, MD, CSPQ, Associate Professor of Medicine, Department of Medicine, Faculty of Medicine, Universite de Montreal, Director, Laboratory of Metabolic Bone Diseases, Centre de Recherche Clinique Andre Viallet, Hopi tal Saint~Luc, Montreal, Quebec ABSTRACT RESUME Osteoporosis is a skeletal disease characterized by low bone mass and deterioration of bone micro-architecture resulting in bone fragility. Normal bone remodelling in the adult follows a precise sequence of cellular events: activation, bone resorption, reversal phase and then, bone formation. This sequence of cellular activities occurring at a given site on trabecular bone surfaces or in cortical bone is called the bone remodelling unit (BRU). Bone mass results from the sum of focal bone balance at each BRU. After the age of 35, there is a physiological bone loss due to focal imbalance between the resorption and the formation phases at the BRU level. In Type I osteoporosis, observed in postmenopausal women, there is a predominant trabecular bone loss due to an increased number of new BRUs and a more pronounced unbalanced coupling between resorption and formation. This results in thinning of trabeculae but also in irreversible trabecular perforations with subsequent deterioration of the trabecular bone micro-architecture. In Type II osteoporosis, observed in older people, cortical bone loss is mainly due to secondary hyperparathyroidism due to vitamin D and/or calcium deficiency. L' osteoporose est une maladie du squelette caracterisee par une faible masse osseme et une deterioration de Ia micro-architecture des os qui conduit a leur fragilisation. Le remplacement des tissus osseux chez l'adulte s'effectue sewn une sequence precise d'evenements au niveau cellulaire : activation, resorption, phase de reversion et formation. Cette sequence d' activites cellulaires qui s' observe en des lieux precis de Ia surface osseuse trabeculaire ou dans l' os cortical porte le nom d' «unite de remade/age osseux" (bone remodelling unit ou BRU). La masse osseme depend de Ia somme des bilans osseux focaux a chaque BRU. Apres l' age de 35 ans, on observe une perte physiowgique de tissm osseux due a un desequilibre focal entre les phases de resorption et de formation au niveau des BRU. Dans l'osteoporose de type I, observee chez les femmes menopausees, on observe surtout une perte d'os trabeculaire due a une augmentation du nombre de nouveaux BRU eta un desequilibre plm prononce entre les phenomenes de resorption et de formation. Ceci entraine un amincissement de Ia surface osseme trabeculaire ainsi que des perforations irreversibles de l' os trabeculaire conduisant a une deterioration de Ia micro-architecture osseuse. Dans l' osteoporose de type II, observee chez les personnes plus iigees, Ia perte d' os cortical est principalement due a l'hyperparathyroidisme secondaire came par une carence en vitamine D ou en calcium. KEY WORDS Osteoporosis, pathophysiowgy, bone remodeling, histomorphometry. J SOGC 1995;17: JOURNAL SOGC 1205 DECEMBER 1995
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3 DEFINITION The currently accepted definition of osteoporosis is: "A systemic skeletal disease characterized by low bone mass and microarchitectural deterioration of bone tissue, with a consequent increase in bone fragility and susceptibility to fracture risk." 1 A major component of the bone fragility in osteoporosis is the low bone mass which results from either: 1 ) a small peak bone mass achieved at young adulthood, 2) an increased bone loss occurring at menopause or at later ages or 3) a combination of both mechanisms. Many factors will influence the achievement of peak bone mass and subsequent bone loss including physical activity, genetic factors (mainly for peak bone mass), nutritional, and hormonal factors. A classification of osteoporosis has been proposed distinguishing the disease into Type I and Type II on the basis of age of onset, type of fractures, and hormonal changes. 2 It is hypothesized that their underlying pathophysiology is different. Type I osteoporosis (or postmenopausal osteoporosis) occurs mainly in women after menopause and will result in vertebral crush fractures due to the fact that the bone loss induced by estrogen deficiency affects predominantly trabecular bone. Type II osteoporosis (or senile osteoporosis) is observed in both sexes after the age of 70. It causes mainly hip fractures resulting from a predominant loss of cortical bone, possibly due to secondary hyperparathyroidism which is frequently observed in the elderly. NORMAL BONE REMODELLING Throughout adult life, bone is continuously being turned over. This leads to the renewal of bone tissue, maintaining the biomechanical properties of the skeleton. The major bone cells involved in bone remodelling are the osteoclasts which are responsible for bone resorption and the osteoblasts which synthesize bone matrix and lead to its mineralization. The process of bone remodelling is a precise sequence of cellular activities occurring at a given site on trabecular bone surfaces or in cortical bone.' First, there is a phase of activation leading to the retraction of lining cells from the bone surface. In the bone marrow, osteoclast precursors proliferate and differentiate themselves into mature osteoclasts. These active osteoclasts are attracted to this specific locus of bone surface. The second step is the phase of bone resorption by the team of osteoclasts which will excavate an erosion cavity (Howship's lacuna). This lasts for seven to 20 days and then the osteoclasts disappear. The reversal phase follows, during which mononuclear cells prepare the bony lacuna for the next step. It is at this stage that the factors involved in the coupling of bone formation to bone resorption (possibly insulin growth factor II, transforming growth factor B, collagen fragments... ) play their roles. They stimulate the proliferation and the differentiation of the osteoblasts. During the phase of bone formation, the osteoblasts synthesize layers of osteoid matrix which are mineralized subsequently. The result of this bone forming activity is the bone structural unit (BSU) which is delineated on one side by the bottom of the "ex"-lacuna and on the other by the trabecular border. The thickness of the BSU can be measured by histomorphometry and it is globally a good parameter of bone formation. This temporal and spatial sequence of cellular activities is called the bone remodelling unit (BRU). This constitutes an intermediary level of organization between the cellular level and the organ level. Therefore, bone mass will be affected by the focal bone balance (resulting from the difference between the bone resorption and the bone formation) at each BRU and by the number of BRUs. AGE DEPENDENT BONE LOSS After the age of 35, bone mass decreases with age. This bone loss results from a focal imbalance between the resorption and the formation phases at the BRU level, the quantity of deposited bone being smaller than that resorbed. 4 The bone loss is, thus, the sum of the focal bone deficits of all of the BRUs. This imbalance is mainly due to a decrease in the formation period which results in thinner BSUs. Consequently, the bony trabeculae become thinner. Although bone resorption does not seem to be increased (the depth of the resorption cavities is not increased), i osteoclasts can perforate these thin trabeculae. When trabecular perforations do occur, bone loss then becomes irreversible.' In addition, the perforations will lead to a loss of trabecular elements resulting in discontinuity of the trabecular network. This deterioration of the trabecular bone micro-architecture will contribute, independently of the low bone mass, to the decreased mechanical resistance of bone.' JOURNAL SOGC 1207 DECEMBER 1995
4 PosT-MENOPAUSAL BoNE Loss AND TYPE I OSTEOPOROSIS At the time of the menopause, the negative balance between bone formation and bone resorption is more pronounced. The decrease of estrogen secretion leads to the activation of bone remodelling with an increased number of new BRUs. In addition, there is possibly a stimulation of bone resorption either due to more active osteoclasts or a greater number of osteoclasts at each resorption site.' Adding to the age dependent decrease in bone formation, these two mechanisms will cause the accelerated bone loss observed in the first years after menopause." Moreover, the trabecular perforation phenomenon is more marked due to increased resorption activity on thinned trabeculae. This increased bone remodelling at menopause translates into rises in serum and urinary concentrations of biochemical markers of bone formation (total and bone isoenzyme of serum alkaline phosphatase, serum osteocalcin) and of bone resorption (urinary excretion of calcium, hydroxyproline and pyridinolines).10 TYPE II OSTEOPOROSIS With advancing age, the cortical thickness decreases whereas the cortical porosity increases. The bone remodelling is accelerated in cortical bone and at the cortico-endosteal envelope leading to an expansion of the medullary cavity at the expense of the cortex. 11 Histomorphometric analyses of bone biopsies taken from subjects with recent femoral neck fractures showed that the trabecular bone volume was normal but the cortical thickness was decreased with increased parameters of bone resorption. 1 ' Secondary hyperparathyroidism due to vitamin D and/or calcium deficiency is not rare in the elderly population.11 This hyperparathyroidism might play an important role in the increased fragility of the femoral neck by increasing cortical bone remodelling. In addition, it was shown recently that there was a significant increase in the serum level of undercarboxylated osteocalcin (ucoc) in an elderly institutionalized population.h This increased ucoc was found to be a marker of the risk of hip fracture. The mechanism by which ucoc is linked to bone fragility is yet unclear. SECONDARY OSTEOPOROSIS Osteoporosis can be induced by various diseases, drugs, and immobilization. In these cases, the bone disease is called "secondary osteoporosis." The mechanism(s) underlying the bone loss in secondary osteoporosis will vary according to the cause. In hyperthyroidism, there is an increase in bone remodelling with an increased birthrate ofbrus which will lead to an increased number of focal bone deficits. The sum of the latter will result in an accelerated bone loss. Excess of glucocorticoids (iatrogenic or endogenous Cushing's syndrome) is mainly due to a marked depression of the osteoblastic activity resulting in reduced thickness of the BSU. When glucocorticoids are administered at high doses, secondary hyperparathyroidism might develop as a result. This will increase the birthrate of the BRUs and thus, bone loss will be more marked. Osteoporosis due to immobilization is usually also quite severe because there is the same combination of increased birthrate of the BRUs with decreased bone formation. In conclusion, the underlying mechanisms of osteoporosis are multiple. Recent advances in bone histomorphometry and biochemical markers of bone remodelling have increased our understanding of the pathophysiology of the disease. This knowledge is important for the proper use of currently available preventive measures and treatments. However, the precise mechanisms of the control of bone remodelling are not well known. Their elucidation will help in designing new therapeutic approaches. REFERENCES 1. Anonymous. Consensus development conference: diagnosis, prophylaxis and treatment of osteoporosis. Am J Med 1993;94: Riggs BL, Melton Ill U. Evidence for two distinct syndromes of involutional osteoporosis. Am J Med 1983;75: Eriksen EF. Normal and pathological remodelling of human trabecular bone: three-dimensional reconstruction of the remodelling sequence in normals and in metabolic bone disease. Endocrine Rev 1986;7: Lips P, Courpron P, Meunier PJ. Mean wall thickness of trabecular bone packets in the human iliac crest biopsies. Bone Miner 1989;6: JOURNAL SOGC 1208 DECEMBER 1995
5 5. Cohen-Solal ME, Shih MS, Lundy MW, Parfitt AM. A new method for measuring cancellous bone erosion depth: application to the cellular mechanisms of bone loss in postmenopausal osteoporosis. J Bone Miner Res 1991;6: Parfitt AM, Matthews CHE, Villanueva AR, Kleerekoper M, Frame B, Rao DS. Relationships between surface volume and thickness of iliac trabecular bone in aging and in osteoporosis. Implications for the microanatomic and cellular mechanisms of bone loss. J Clin Invest 1983; 72: Steiniche T, Christiansen P, Vesterby A et al. Marked changes in iliac crest bone structure in postmenopausal osteoporotic patients without any signs of disturbed bone remodelling or balance. Bone 1994;15: Eriksen EF, Hodgson SF, Eastell R, Cedel SL, O'Fallon WM, Riggs BL. Cancellous bone remodeling in type I (postmenopausal) osteoporosis: quantitative assessment of rates of formation, resorption, and bone loss at tissue and cellular levels. J Bone Miner Res 1990;5: Dempster DW, Lindsay R. Pathogenesis of osteoporosis. Lancet 1993;341: Delmas PD. Biochemical markers of bone turnover. J Bone Miner Res 1993:8(suppl 2):S549-S Reeve J. Osteoporosis. In: Cohen RD, Lewis B, Alberti KGMM, Denman AM (Eds). The metabolic and molecular basis of acquired diseases. London, Balliere Tindall 1990: Lips P, Netelenbos JC, Jongen HKM et al. Histomorphometric profile and vitamin D status in patients with femoral neck fracture. Metab Bone Dis Rei Res 1982; 4: Compston JE, Silver AC, Croucher PI, Brown RC, Woodhead JS. Elevated serum intact parathyroid hormone levels in elderly patients with hip fracture. Clin Endocrinol 1989;31 : Szulc P, Chapuy MC, Meunier PJ, Delmas PD. Serum undercarboxylated osteocalcin is a marker of the risk of hip fracture in elderly women. J Clin Invest 1993; 91: JOURNAL SOGC 1209 DECEMBER 1995
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