The normal process of remodeling of compact bone in the long bones of the lower extremity provides histological information that can prove useful in estimating age at death, especially in adults (125-128). Bone remodeling involves the conversion of primary bone (i.e., that formed during the initial ossification of the bone) to secondary bone. Bone turnover is accomplished through the action of osteoclasts to create resorption spaces, which are subsequently filled in to form secondary osteons. This process begins early in life and continues until death. With increasing age, the original components of diaphyseal compact bone are gradually replaced by the new structures. Preexisting structures, such as lines of increased density, may be altered or removed (129). With advancing age, resorption spaces are created not only at the expense of the original circumferential lamellar bone and primary osteons but pre-existing secondary osteons as well, thereby forming secondary osteon fragments.
In 1965, Kerley introduced a histological technique based on the examination of thin cross-sections of undecalcified ground tissue removed from the mid shaft of the femur, tibia, and fibula. This technique calls for the examination of four circular fields, each measuring approximately 1.62 mm in diameter and located adjacent to the periosteal edge of the bone on its anterior, posterior, medial, and lateral surfaces (130-132). Within each of these fields, the numbers of primary osteons, secondary osteons, and osteon fragments must be counted, as well as the percentage remaining of the original circumferential lamellar bone. The technique recognizes that circumferential lamellar bone and primary osteons were formed during the original formation process. Secondary osteons and osteon fragments are created during the remodeling process. Thus with increasing age, the percentage of circumferential lamellar bone and the number of primary osteons decrease while the number of secondary osteons and osteon fragments increases. The Kerley system allows the age at death to be estimated through the use of a "profile chart" or regression equations. The profile chart is created by plotting age distribution data for each variable and then observing the age at which they overlap. The regression equations allow direct estimation of age for each variable.
The Kerley method is useful if complete cross-sections are available, but is limited if the external (periosteal) surface is damaged or otherwise missing. Error is introduced if visual fields are used other than those defined, because the histology of the bone cortex varies (133).
Several modified or alternative methods have been introduced since Kerley introduced this technique. Ahlqvist and Damsten (134) offered a modification of this technique in which the combined frequencies of secondary osteons and osteon fragments within fields located between those used by Kerley are examined. These field locations were chosen because they avoid Kerley's posterior field on the linea aspera, a site of muscle attachment and potential activity-induced change unrelated to age. However, their sample was more restricted than Kerley's, in terms of size and composition, and by combining two of Kerley's variables, they sacrificed some useful sources of information (135).
Another modification, suggested by Singh and Gunberg (136), examines the number of secondary osteons, the average number of lamellae per osteon, and the average shortest diameter between Haversian canals in two randomly selected fields within the periosteal third of the cortex. Regression equations are available from their study of 59 individuals aged 40 to 88 yr. These equations include those applicable to the femur and tibia.
In 1979, Thompson (137) published a technique that utilizes only a small core of bone (4 mm in diameter) removed from the anterior mid shaft of the femur and the medial mid shaft of the tibia, as well as other bones. His complex method employing 19 variables was based on a sample of 116 adults. Although the method examines only one area of the bone cortex, it has the advantage of not requiring a cross section.
Watanabe et al. (138) studied stained ground thin sections taken from the mid-shaft of the femur in 72 Japanese males aged 43 to 92 yr and 26 females aged 2 and 88 yr. They examined the area, maximum diameter, minimum diameter, and perimeter of intact osteons and Haversian canals, as well as type II osteons, fragments, and the triangular area of associated osteons. The osteon dimensions displayed a higher correlation with age than the Haversian canals.
Walker et al. (139) reported that in individuals aged more than 50 yr, the density of osteons and osteon fragments correlated with cortical mass but not with age.
These researchers urged caution in the use of these attributes to estimate histological age in individuals in this age bracket.
Of course, all of the histological methods are by nature destructive and require the necessary equipment. Experience with these techniques is also important to ensure correct identification of the structures involved (140). For general reviews of histological approaches, see Robling and Stout (125) and Ubelaker (127,128).
A 1953 study by Hansen (141) revealed that among adults, the medullary cavity increases in size with age. At the proximal end of the femur, the cavity advances (at the expense of trabecular bone) to the level of the surgical neck during the fourth decade and reaches the epiphyseal line between 61 and 74 yr. The medullary cavity also increases in width with aging, creating a loss of cortical bone and thickness in advanced years.
Walker and Lovejoy (142) present radiographic data on age progression in the proximal femur and calcaneus in 130 individuals from the Hamann-Todd collection. For the femur, they present radiographic standards comprised of eight phases. Radiographic images of each phase are accompanied by descriptive narrative. The first of the eight phases has a suggested age range of 18 to 24 yr, and the final one is listed at 60 yr or more.
Ruff and Jones (143) add that adult remodeling can alter asymmetry in cortical bone. With aging, patterns of adult cortical remodeling correlate with activity levels. Their study of mature tibiae indicates that the loss of cortical bone with remodelling likely produces shifts in asymmetry.
In older adults, bone density decreases with age. Note, however, that Atkinson and Weatherell found that within the femoral diaphysis, bone density varied at several locations in the diaphysis but was greatest at mid shaft (144). Density also varied at sites around the circumference of the diaphysis. The reader is encouraged to review the chapter entitled Radiology of the Lower Extremity for a comprehensive treatise on evaluating ossification centers from radiographs.
General changes associated with arthritis provide an additional source of age information from bones in the lower extremity (131). Obviously, as adults age, the frequency and probability of arthritis-associated changes in the joints increases. Generalized changes provide clues to advancing age, but pathological conditions can produce such evidence prematurely or with varied expressions in different anatomical areas.
Ohtani et al. (145) report that aspartic acid racemization ratios in the human femur may provide some information that is useful in age determination procedures. The normal L form of amino acids change to the D form with aging. Their study of femoral compact bone revealed that sex differences were apparent, with males demonstrating the greater increase in the D/L ratio with aging. They recommend using the total amino-acid fractions instead of the acid-insoluble collagen fraction.
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