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The significance of mean osteon size in bone remodeling and its correlation with age, sex, and mechanical strain. various studies on human bones, including the rib, femur, humerus, and tibia, and their findings regarding age-related changes and sex differences in mean osteon size. The document also introduces the concept of woven bone formation and the role of bone cells, such as osteoblasts, osteocytes, bone lining cells, and osteoclasts, in bone growth and remodeling.
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by Bridget Jennifer Denny
A thesis submitted in partial fulfillment of the requirements for the degree of Master of Arts in Anthropology Boise State University
May 2010
of the thesis submitted by Bridget Jennifer Denny
Thesis Title: Does Mean Osteon Size Change with Age, Sex, or Handedness? Analysis of the Second Metacarpal in a 19th^ Century Sample from Belleville, Ontario, Canada Date of Final Oral Examination: 08 April 2010 The following individuals read and discussed the thesis submitted by student Bridget Jennifer Denny, and they evaluated her presentation and response to questions during thefinal oral examination. They found that the student passed the final oral examination.
Margaret Streeter, Ph.D. Chair, Supervisory Committee Chris Hill, Ph.D. Member, Supervisory Committee Mark Plew, Ph.D. Member, Supervisory Committee The final reading approval of the thesis was granted by Margaret Streeter, Ph.D., Chair of the Supervisory Committee.R. Pelton, Ph.D., Dean of the Graduate College. The thesis was approved for the Graduate College by John
ABSTRACT ............................................................................................................... iii LIST OF TABLES ...................................................................................................... vi
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Bone histomorphometry or quantitative bone histology has been used by bone biologists to estimate age at death, infer the health status of an individual, and study the effects of varying degrees of biomechanical stress on bones. This information is important to anthropologists because it can provide insight into how the human skeleton adapts to changing lifestyles in past and present populations.
Throughout life, human bones undergo remodeling, the renewal of discrete packets of bone called osteons. These osteons are known to vary in size between bones and even within the same bone (Evans and Bang, 1967). The size of osteons is thought to be determined by multiple factors, both intrinsic and extrinsic such as age, sex and biomechanical strain. Therefore, osteon size has the potential to provide information about the influence of these three factors. The purpose of this research is to investigate the association between these variables and mean osteon size in the second metacarpal in a 19th^ century Euro-Canadian sample.
This large sample of known age, sex, and ancestry offers a unique opportunity to study bone biology in a population that lived labor intensive lives. Most individuals were immigrants of European descent (Saunders, DeVito, Herring, Southern, and Hoppa, 1993; Lazenby, 1994; Jimenez, 1994; Saunders et al., 2002). In this population, men are believed to have experienced high levels of mechanical loading in their hands as a consequence of the manual manipulation required in occupations such as logging, factory
3 statistically significant difference in mean osteon size between males and females in the second metacarpal.
The organization of this research is as follows: Chapter Two discusses the functions of bone, gross and microanatomy of bones, metacarpals, growth, modeling, and remodeling and the factors that affect remodeling. The last two sections examine factors that influence mean osteon size and previous studies that have focused on it. Chapter Three discusses the sample being used for this study, including previous research this sample was included in, and the methods for this project. Chapter Four provides the results of the study. Chapter Five includes the discussion and conclusions.
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Bones are the support system for the body. As a result they must be extremely strong while at the same time sufficiently lightweight so that the individual can move without expending excessive energy (Marieb, 2004). Like all weight bearing materials damage can occur over time due to stress and fatigue. Unlike non-biological materials, bone has the capacity to self-repair microdamage and fatigue through remodeling (Parfitt, 2003; Taylor, Hazenberg, and Lee, 2007). Bones provide support and protection for organs like the brain, spinal cord and organs of the thorax. They also aid in movement of the body (Parfitt, 2003; Marieb, 2004). Other functions include mineral storage (two of the most important of which are calcium and phosphate) and blood cell formation (hematopoiesis) (Marieb, 2004). Wolff’s law, or the Law of Bone Transformation states that bone is laid down in areas where needed and is resorbed where it is not needed. This is because bone is metabolically expensive for the body to maintain in places it is not required (Wolff, 1869). The balance between strength and economy is achieved through the processes of modeling and remodeling.
Bone is comprised of two materials: collagen and hydroxyapatite. Collagen makes up a large portion of the organic content of bone. It is responsible for the elasticity, flexibility and tensile strength of bones, as well as their ability to withstand torsional
6 Bone can be categorized in many ways: trabecular and cortical, or primary and secondary. Trabecular (spongy) bone develops in the ends of long bones (epiphyses), and in the flared part of the bone shaft (metaphysis) (Fig. 2.1) and has a porosity of about 75- 95%. Trabecular bone is also found in vertebral bodies, beneath tendon attachment points, and within flat bones, such as the skull and pelvic bones (Marieb, 2004; Taylor et al., 2007). It is made up of thin plates or struts called trabeculae that form a lightweight but strong matrix (Martin, Burr, and Sharkey, 1998; Marieb, 2004). Cortical bone is much denser than trabecular bone and is found in the diaphysis, or shaft, of long bones and on all external bone surfaces. It is much less porous than trabecular bone with about 5-10% porosity (Martin et al., 1998; Taylor et al., 2007).
Bone can be also be categorized as primary and secondary bone. Primary bone is forms during growth and modeling on preexisting bone surfaces and can take the form of either circumferential lamellar bone or woven bone. Circumferential lamellar bone is laid down parallel to the bone surface, such as beneath the periosteum (Martin et al., 1998). It is well organized and deposited in layered sheets. Woven bone forms the primary spongiosa that is present when bones are initially forming. It forms at a faster rate, is poorly organized, and is weaker than lamellar bone. Woven bone formation is present during periods of rapid deposition, such as in tumor growth, and in trauma and pathological conditions (Martin et al., 1998). Secondary bone is produced through remodeling, the replacement of discrete packets of bone. The product of remodeling takes the form of secondary osteons, or Haversian systems (Martin et al., 1998).
The outer surfaces of bones are covered by a fibrous membrane called the periosteum. This thin two layered fibrous tissue helps nourish the bone (Fig. 2.2). The
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fibrous outer layer is comprised of dense, irregular connective tissue. The inner osteogenic layer consists primarily of bone lining cells. Under the periosteum is cortical bone, followed by a similar fibrous tissue layer called the endosteum. The endosteum lines the trabeculae of spongy bone and the medullary cavity (Marieb, 2004).
Figure 2.2 Cross Section of a Long Bone (White and Folkens, 2000) Metacarpals Metacarpals are cylindrical bones that support the palm of the hand (Fig. 2.3). Though small, their morphology resembles that of long bones. The diaphysis of the metacarpal is identical to the diaphysis of a long bone. It is covered by the periosteum on the outside. Underneath the periosteum is cortical bone. The central marrow cavity is lined by the endosteum. (Marieb, 2004; Bass, 2005). There are five metacarpals numbered I though V beginning on the lateral, or thumb side. The proximal end articulates with the carpals, or wrist bones, and the distal end attaches to the phalanges, or finger bones. The shaft, or middle section of the bone is cylindrical. There is a slight
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and disease related changes in bone mass (Lazenby, 1994, 1998; Sato, Asoh, and Oizumi, 1998a; Sato, Fujimatsu, Honda, Kunoh, Kikuyama, and Oizumi, 1998b; Nielsen, 2001; Lazenby, 2002a, 2002b; Lazenby, Cooper, Angus, and Hallgrimsson, 2008). They can indicate handedness of individuals and what side, if any, is undergoing increased mechanical loading. Metacarpals can provide further information about the roles of males and females in populations and the kinds of work they are doing.
Bone Cells There are four types of bone cells: osteoblasts, osteocytes, bone lining cells, and osteoclasts (Martin et al., 1998). Osteoblasts are mononuclear cells responsible for laying down new bone matrix, or osteoid, the non-mineralized organic component of bone. Osteocytes are mature osteoblasts that have become encased in the bone matrix in small spaces called osteocytic lacunae. Osteocytes serve to maintain bone tissue, detect mechanical stress, transport minerals in and out of bone, and communicate with other bone cells (Martin et al., 1998). Bone lining cells are osteoblasts that became flattened on bone surfaces. They initiate remodeling in response to chemicals and mechanical stimuli (Miller and Jee, 1992; Martin et al., 1998). Osteoclasts are multinuclear cells that resorb bone (Martin et al., 1998; Taylor et al., 2007).
Growth and Modeling Bones grow, are shaped and maintained through the processes of growth, modeling and remodeling, which take place throughout life. Skeletal development occurs through growth and modeling. Growth is the process by which the length and diameter of the bone is increased both internally and externally as determined by the genetic code
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(Martin et al., 1998). Modeling works with growth to shape bone (Frost, 1985) and is defined by either the activation of bone forming cells (A-F) resulting in the addition of new bone, or the activation of bone resorbing cells (A-R) which leads to the resorption of bone on selective bone surfaces (Frost, 1985; Parfitt, 2003).
Remodeling The focus of this study is the mean osteon size of secondary osteons which are the product of bone remodeling (Frost, 1985; Martin et al., 1998). This is the process by which discrete packets of bone are resorbed and replaced with new bone. Knowledge of remodeling provides information on how the skeleton repairs itself, how it adapts to changes in mechanical strain, and how bones respond to disease, aging, hormones and nutritional deficiencies (Hattner et al., 1965; Jowsey, 1966; Wu, Schubeck, Frost, and Villanueva, 1970; Lacroix, 1971; Parfitt, 1979; Thomson, 1979; Frost, 1987a, 1987b; Burr and Martin, 1989; Ericksen, 1991; Martin, 1991; Slemenda, Peacock, Hui, Zhou, and Johnston, 1997; Martin et al., 1998; Sato et al., 1998a; Sato et al., 1998b; Martin, 2003). These factors are discussed in the next section. Remodeling serves to repair old or damaged bone by replacing it with new bone (Frost, 1985; Parfitt, 2003). Remodeling always occurs in an activation, resorption, formation order (the A-R-F sequence) (Martin et al., 1998). In a longitudinal section remodeling can be depicted as a cutting cone with osteoclasts in the lead resorbing bone (Fig. 2.4). Located behind the osteoclasts are osteoblasts that lay down the unmineralized boney matrix. This group of cells is collectively called the Basic Multicellular Unit (BMU) and is estimated to move about 40 μm per day. Some of the osteoblasts are embedded in the new bone and become
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Osteons are the product of remodeling. There are many factors that can affect remodeling, especially the rate. Some these factors are age; sex; mechanical strain, including disuse and overuse; certain diseases; and nutritional deficiencies (Hattner et al., 1965; Jowsey, 1966; Wu et al., 1970; Lacroix, 1971; Parfitt, 1979; Thompson, 1979; Frost, 1987a, 1987b; Burr and Martin, 1989; Ericksen, 1991; Martin, 1991; Slemenda et al., 1997; Martin et al., 1998; Sato et al., 1998a; Sato et al., 1998b; Martin, 2003). During infancy remodeling rates are at their highest point then slowly decreases through childhood until adulthood is reached (Jowsey, 1960; Lacroix, 1971). At this point, a baseline rate of about 1 mm^2 per year is maintained, unless otherwise affected by activity or disease processes (Slemenda et al., 1997; Martin et al., 1998). Men have been shown to have higher remodeling rates than females (Thompson, 1979; Ericksen, 1991) while remodeling rates in menopausal women have been shown to increase (Parfitt, 1979).
Mechanical strain causes microdamage in bones that is repaired by remodeling (Frost, 1987a). Therefore with overuse and heavy mechanical loading remodeling rates increase (Martin, 2003). The same has also been found in cases of disuse, such as in individuals who are confined to bed (Frost, 1987b; Martin, 2003). There are also many pathogenic conditions that affect remodeling rates. For example, Osteogenesis Imperfecta (OI), hyperparathyroidism (HP), hemiplagia in stroke patients, Padget’s disease, Osteomalacia, and thyroxine can all increase the rate of remodeling, while adreanal coricoids, increased estrogen, osteopetrosis, diabetes, and postmenopausal osteoporosis can all decrease remodeling rates (Frost, 1963; Wu et al., 1970; Burr and Martin, 1989; Ericksen, 1991; Martin, 1991). Nutritional deficiencies, such as vitamin D, increase the
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amount of parathyroid hormone released, increasing remodeling. Vitamin D deficiency has also been linked to decreased bone mass density (Sato et al., 1998a). Although many studies have been done on the affects of disease and health on remodeling, no research has focused on their impact on mean osteon size.
The average size of an osteon, or the mean osteon size, includes bone formed within the reversal line of a whole, complete osteon. Mean osteon size has been determined for several human bones, such as the rib (Landeros and Frost, 1964; Hattner et al., 1965; Takahashi et al., 1965; Jowsey, 1966; Pfeiffer, 1998), the femur (Currey, 1964; Jowsey, 1966; Burr et al., 1990; Pfeiffer, 1998), the humerus (Yoshino et al., 1994), and the tibia (Black et al., 1974). It is important to remember that mean osteon size varies within a cross section of bone, as well as between bones of the body (Fig. 2.5) (Evans and Bang, 1967). In a number of studies mean osteon size has also been found to vary based on age, sex, and magnitude of mechanical strain (Currey, 1964; Jowsey, 1966; Burr et al., 1990; Yoshino et al., 1994).
