Tanning predicts bone mass but not structure in adolescent females living in Hawaii

Adult skeletal integrity is influenced by lifestyle throughout the growth period. Determinants of bone mass, however, remain poorly understood. It is clear measurable differences in bone quantity and structure exists between ethnic groups in adulthood and that these differences manifest early in life (Vidulich et al., 2007; Weaver et al., 2007). Bone strength tends to be highest in individuals who identify as African American and fracture rates are lowest (Finklestein et al., 2002). In general, Asians tend to have the lowest bone mass, but do not experience as many fractures as do whites. Individuals who identify as white and non-white Hispanic are intermediate in terms of bone strength, with whites suffering from the highest fracture rate (Finklestein et al., 2002; Weaver et al., 2007; Wu et al., 2003). Body size, and thus bone size, explains much of the discrepancy in bone strength between these groups (Lee et al., 2010). However, there is some evidence that Asians are less susceptible to fracture than are whites because the former maintain thicker trabecular bone (Wang et al., 2009). Although most researchers assume an underlying genetic basis to these differences, relatively few have studied actual genes in this pursuit. Lifestyle factors associated with contemporary Western society, such as dietary intake and physical activity level, may influence susceptibility to skeletal fragility. Many studies have found that Asians tend to be less physically active and consume less calcium than whites or Hispanics (Weaver et al., 2007). Interestingly, lack of calcium intake among adolescents appears to be due in part to perceived lactose intolerance. That is, many adolescents believe they are lactose intolerant when they are not (Matlik et al., 2007). This suggests persistence of a cultural belief that likely limits the amount of calcium consumed. Physical activity has a positive effect on bone mass so it is reasonable to assume that a more sedentary lifestyle would increase the likelihood of skeletal fragility. The cumulative effects of nutrition and activity across generations likely influences bone mass and structure as well. Another potential contributor to inadequate bone mass is lack of vitamin D3. When skin is penetrated by ultraviolet-B (UVB) radiation, 7-dehydrocholesterol is converted to previtamin D3 via temperature-dependent isomerization (Holick et al., 1980; Holick, 2007). Subsequently, previtamin D3 is converted to vitamin D3, which is ultimately metabolized in the liver to 25-hydroxycholecalciferol (25(OH)D3), and in the kidney to its biologically active form 1,25-dihydroxycholecalciferol (1,25(OH)2D3), or calcitriol. Although vitamin D3 can also be acquired through diet, dietary intake provides substantially less vitamin D3 than UVB exposure (Hollis, 2005). Vitamin D3 serves many regulatory purposes, including absorption of calcium and phosphorus in the intestine and reabsorption of calcium in the kidney. Vitamin D3 also promotes bone formation and mineralization (Harkness and Cromer, 2004). Insufficient vitamin D3 results in increased parathyroid hormone (PTH), in order to initiate bone resorption and to maintain calcium homeostasis. Individuals with more recent African ancestry (i.e., African Americans) achieve calcium homeostatis more efficiently than do whites (Weaver et al., 2008). Insufficient vitamin D3 may constrain bone mass (Cashman et al., 2008; Nieves et al., 2008; Tangpricha et al., 2004), but this relationship may be dependent on calcium intake (Weaver, 2007). Although vitamin D3 is fat soluble, and thus can be stored, stores can be exhausted with insufficient vitamin D synthesis over time. The capacity for vitamin D synthesis varies with season, latitude, pigmentation, age, and sex. Vitamin D3 synthesis did not occur between November and February in cities at 42.2 degrees north (e.g., Boston, MA), a seasonal effect related to the tilting of the earth’s axis during winter (Webb et al., 1988). In addition, winter weather complicates analyses, as the amount of surface area exposed to UV radiation typically decreases. Furthermore, UV intensity varies at a given location from year to year, so the assumption that UV intensity on a specific day will be similar one year to the next is not tenable (Jablonski and Chaplin, 2010). Skin pigmentation effectively filters UV radiation, so vitamin D3 synthesis is limited in individuals with greater amounts of pigmentation (Chen et al., 2007;; Jablonski and Chaplin, 2000; 2010; Rockell et al., 2008). Skin is pigmented by hemoglobin and carotene, but the predominant chemical responsible for pigmentation is melanin. Melanin is produced by cells in the stratum basale of the epidermis, termed melanocytes, when these cells are exposed to UVB radiation (Jablonski and Chaplin, 2000; 2010). Skin pigmentation is sexually dimorphic, with females being on average having less pigmentation than males, likely due to fluctuating hormone levels (Zouboulis et al., 2007). Further, skin loses its capacity for vitamin D3 synthesis with aging (Holick, 2007). Populations with long evolutionary histories at a particular region demonstrate a strong negative association between latitude and pigmentation. The evolution of depigmentation has been a matter of debate largely focused on the adaptive significance of UV induced vitamin D3 in homeostasis, particularly as it relates to skeletal integrity. For instance, some have suggested a negligible role for vitamin D in this process, suggesting that depigmentation has occurred through sexual selection (Aoki, 2002; Frost, 1988, 2007). Robins (1991; 2009) has also argued that the vitamin D hypothesis of depigmentation is not supported, suggesting that rickets is a disease of industrialization and age related bone loss occurs too late in life to be a strong selective pressure. However, Chaplin and Jablonski (2009) offer a strong rebuttal of Robins’ (1991,2009) critique of the vitamin D hypothesis providing not only support for its role in osteogenesis, but also pointing out the pivotal role Vitamin D3 plays in regulation of immune function, cellular differentiation, cancer prevention, normal functioning of several organs, and susceptibility to infectious disease. Convincing evidence in support of the vitamin D hypothesis continues to grow and illuminate the importance of the vitamin’s role in immune function (Baeke et al., 2008; Bilke, 2008; Cantorna and Mahon, 2005; Fernando de Abreu, 2009; Jablonski and Chaplin, 2000; 2010). In so far as bone is concerned, the mechanism is sound: with insufficient synthesis of vitamin D3, poor skeletal health will result. The amount of acceptable exposure to UV radiation varies across cultures and is often mediated by perceptions of beauty and, more recently, by concern over risk for skin cancer. Exposure to UV radiation may be limited by the type and timing of outdoor activities, the amount of concealing clothing worn, direct avoidance or through the use of sunscreens. Therefore, barriers to vitamin D synthesis are complex and may include aspects of culture and evolutionary history. Understanding how skin pigmentation, UVB, and vitamin D interact may provide insight into skeletal variation in contemporary populations, as well as in our evolutionary past. In this paper we examine the relationship between skin reflectance, as a proxy for melanin content of the skin, and BMC (the amount of mineral per square centimeter in a section of bone controlling for the width of the bone) and bone structural geometry, in a sample of Asian and white adolescent females living in Hawaii. We aim 1. to evaluate skin reflectance within and between ethnic groups and 2. to determine whether measures of skin reflectance predict, BMC at the lumbar spine, total hip, and total body, as well as cross sectional area of the proximal femur and section modulus at the proximal femur. We test the hypothesis that facultative (i.e., tanned) skin pigmentation is associated with greater BMC and structural geometry in these non-African populations, controlling for differences in body size, pubertal development, and lifestyle. Alternatively, darker non facultative skin pigmentation may be a barrier to greater BMC.