Osteoporosis and Paleopathology: a Review
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doi 10.4436/JASS.92003 JASs Invited Reviews Journal of Anthropological Sciences Vol. 92 (2014), pp. 119-146 Osteoporosis and paleopathology: a review Francisco Curate Research Centre for Anthropology and Health, University of Coimbra, Rua Arco da Traição, 7, 3000 Coimbra, Portugal e-mail: [email protected] Summary - Osteoporosis is a complex and heterogeneous disorder, of multi-factor aetiology. It is the most frequent metabolic bone disorder, affecting an increasing number of post-menopausal women and aging individuals from both sexes. Although first recognized more than 250 years ago, the clinical and epidemiological knowledge about osteoporosis is largely limited to the last 70 years. Within the conceptual frames of paleopathology, disease is necessarily perceived in a space without depth (the skeleton) and of coincidence without development (the crucial moment of death) – but is also interpreted in a time interval which adds an historical gaze to its “biography”. The study of osteoporosis in past populations (which faced sociocultural conditions utterly different from the genus vitae experienced by modern communities) supplements diachronic depth to the knowledge about bone modifications related to age, menopausal status or lifestyle. This article aims to provide a comprehensive record on the history of osteoporosis and fragility fractures as perceived by the biomedical, historical and, particularly, paleopathological sciences. As such, the main focus of this review is to present an exhaustive and historical-framed exposition of the studies of osteoporosis, bone loss and associated fractures within the field of paleopathology and, to a lesser extent, in the history of medicine. A biomedical-oriented synopsis of the main operational definitions, etiological agents and epidemiological features of osteoporosis and osteoporotic fractures is also provided Keywords - Osteoporosis, Bone loss, Fractures, History of medicine, Paleopathology. Introduction of France), first described osteoporosis (without christening it) more than 250 years ago in his post- Osteoporosis (OP) – the «silent thief» – humous «Traité des Maladies des Os» (Duverney, is a metabolic disorder characterized by the 1751). In the beginning of the 18th century, reduction in bone mass, impaired bone quality Jean-Louis Petit (1674-1750) already had docu- and subsequent increase in the risk of fracture mented the inherent fragility of bones (Petit, (Consensus Development Conference, 1993; 1705). A century later – and after – the readily NIH Consensus Development Panel, 2001). apparent and recognizable propensity of bones to The loss of mineral content per unit of volume, break due to «fragility» was well acknowledged in alongside trabecular deterioration, concurs to the medical literature (e.g., Paiva, 1804; Cooper, bone fragility and increased propensity to frac- 1822). The term «osteoporosis» (from the Greek ture (Strømsøe, 2004). The classical hip, distal ostéon-oûn: bone, and póros: porous) was coined radius and vertebral compression fractures are by the French pathologist Johann Lobstein, the main clinical complications associated with the Younger (1777-1835), in a text entitled De osteoporosis (Johnell & Kanis, 2006). l’osteoporose (Lobstein, 1820). Lobstein charac- Joseph Guichard Duverney (1648-1730), terized it as a disease that causes an increase in the professor of anatomy and surgery at the Jardin size of bones and a rarefication of their internal du Roi (medical school established by Louis XIV tissue. Notwithstanding, the disease described by the JASs is published by the Istituto Italiano di Antropologia www.isita-org.com 120 Osteoporosis and paleopathology Johann Lobstein was probably osteogenesis imper- noticing that vertebral fractures occurred more fecta (Schapira & Schapira, 1992). A few years often in women who were subjected to an early later, OP was histologically distinguished from oophorectomy. The relevance of sex steroids in osteomalacia (Pommer, 1885). the etiopathogeny of the disease has been com- Unlike other medical concepts, OP defini- prehensively established by subsequent studies tion has changed substantively, reflecting the (Almeida, 2010; Lindsay, 2010). However, OP is state of knowledge about the disease (Schapira & a complex pathological condition with multiple Schapira, 1992; Wylie, 2010). With the incep- etiological drives, including senescence, genetics, tion of clinical radiology, OP was defined as a physical activity, reproductive history, and die- noticeable loss of bone mass, or as a condition tary status (Burnham & Leonard, 2008; Curate in which bone resorption exceeds bone forma- et al., 2012; Heaney, 2008; Livshits et al., 2004; tion (Nordin, 1987). However, generalized loss Møller et al., 2012; Recker et al., 2004; Zhang of bone should be termed osteopenia (Agarwal, et al., 2009). 2008; Frost, 2003). The American endocri- The demographic profile of the world pop- nologist Fuller Albright (1900-1969) described ulation changed dramatically in the past few osteoporosis as a vertebral fracture syndrome in years, with a remarkable increase in the total and postmenopausal women, defining it as “too lit- relative numbers of elderly individuals. As OP tle calcified bone” (Albright et al., 1941). Later, affects a large proportion of the aged population, Albright & Riefenstein (1948) proposed two resulting in fractures that have costly human and primary categories of osteoporosis: postmeno- economic consequences, it is now recognized as pausal osteoporosis and senile osteoporosis. one of the major public health concerns affecting Riggs & Melton III (1986) refined this scheme the geriatric community (Becker et al., 2010). with the analogous designations, Types I and II. Although typically acknowledged as a “mod- Although heuristically valuable, the model does ern disease”, OP has a vast diachronic depth not account for the intricate etiopathogenesis of (Agarwal, 2008; Brickley, 2002; Turner-Walker the disease (Marcus & Bouxsein, 2008). et al., 2001). The prevalence of the disease has Until the 1990’s, different definitions of oscillated with the historical changes in its etio- osteoporosis emerged in the medical literature logical agents, like longevity or nutrition. The (Bijlsma et al., 2012). The introduction of dual- study of osteoporosis epidemiology in the past energy X-ray absorciometry (DXA) scanners in is, therefore, crucial to the scientific perception the late 1980’s inspired a raging discussion about of the disease. Paleopathology – the study of dis- the definition of osteoporosis (e.g., Mazess, eases, human or nonhuman, in the past using a 1987; Melton III & Wahner, 1989; Nordin, plethora of different sources (Ortner, 2003) – has 1987) until the consensus conference promoted been focused in age-related bone loss since the by the WHO. In 1992, an experts study group, late 1960’s, with the pivotal papers by Dewey et led by the English clinician and researcher John al. (1969) and Armelagos et al. (1972), on three Kanis, met in Rome and proposed a densito- Sudanese Nubia samples, and the studies of van metric definition of osteoporosis: a reduction of Gerven et al. (1969) or Perzigian (1973) with pre- bone mineral density (BMD) by 2.5 standard historic Native-American materials. The body of deviations or more from the peak bone mass in knowledge in the paleopathology of osteoporosis early adulthood, taking into account gender and has developed since, recounting the long history ethnicity (WHO, 1994). of bone involution and fragility fractures in past Though it has been suggested since the 19th communities all over the world (e.g., Agarwal & century that OP is a disease that typically affects Grynpas, 2009; Agnew & Stout, 2012; Curate et older women (Bruns, 1882), it was Albright et al., 2009; Curate et al., 2013b; Lees et al., 1993; al. (1941) who first highlighted the role of estro- Mafart et al., 2008; Mays et al., 1998; Mays et gen depletion in postmenopausal osteoporosis, al., 2006; Cho & Stout, 2011; Zaki et al., 2009). F. Curate 121 Etiopathogenesis of osteoporosis resorption. As such, any imbalance in the pro- cess favoring bone resorption results in bone loss Bone tissue constitutes the fundamental (Nolla & Rozadilla, 2004). template of the skeleton, a complex multifunc- Almost none of the most common diseases tional system comprising three key functions: of mankind can be attributed to only one cause; mechanical / structural, protection, and meta- the majority stems from multiple causes, better bolical. Bone is a mineralized connective tissue, described as risk factors. In the case of osteopo- composed by an extracellular matrix (organic rosis, the risk factors arise at different levels but and inorganic) and a distinctive group of cells they are not mutually exclusive (Nordin, 2008). (Nolla & Rozadilla, 2004). The organic matrix, OP is a gargantuan landscape difficult to classify which constitutes approximately 25% of the dry by its pathogenesis: the question remains whether bone weight, is largely composed of collagen it should be viewed as a unique disease or a group (Boyd, 2009; Fleisch, 2000; Nolla & Rozadilla, of syndromes of skeletal fragility resulting from 2004). The inorganic bone phase is formed by a stochastic process (Heaney, 2008; Marcus & hydroxyapatite. Bone cells occur in four funda- Bouxsein, 2008). mental types: osteoblasts, osteoclasts, osteocytes and bone lining cells (Boyd, 2009). Mature bone Peak bone mass is macroscopically dissociated in two compart- Peak bone mass (PBM) is defined as