Bone Mineral Density and Microarchitecture Change During Skeletal Growth in Harbor Seals (Phoca Vitulina) from the German Coast

Overview

Journal Sci Rep

Specialty Science

Date 2023 May 3

PMID 37137898

Authors

Julian Delsmann

Britta Schmidt

Ralf Oheim

Michael Amling

Tim Rolvien

Ursula Siebert

Affiliations

Soon will be listed here.

Abstract

Across species, the skeletal system shares mutual functions, including the protection of inner organs, structural basis for locomotion, and acting as an endocrine organ, thus being of pivotal importance for survival. However, insights into skeletal characteristics of marine mammals are limited, especially in the growing skeleton. Harbor seals (Phoca vitulina) are common marine mammals in the North and Baltic Seas and are suitable indicators of the condition of their ecosystem. Here, we analyzed whole-body areal bone mineral density (aBMD) by dual-energy X-ray absorptiometry (DXA) and lumbar vertebrae by high-resolution peripheral quantitative computed tomography (HR-pQCT) in neonate, juvenile, and adult harbor seals. Along skeletal growth, an increase in two-dimensional aBMD by DXA was paralleled by three-dimensional volumetric BMD by HR-pQCT, which could be attributed to an increasing trabecular thickness while trabecular number remained constant. Strong associations were observed between body dimensions (weight and length) and aBMD and trabecular microarchitecture (R = 0.71-0.92, all p < 0.001). To validate the results of the DXA measurement (i.e., the standard method used worldwide to diagnose osteoporosis in humans), we performed linear regression analyses with the three-dimensional measurements from the HR-pQCT method, which revealed strong associations between the two imaging techniques (e.g., aBMD and Tb.Th: R = 0.96, p < 0.0001). Taken together, our findings highlight the importance of systematic skeletal investigations in marine mammals during growth, illustrating the high accuracy of DXA in this context. Regardless of the limited sample size, the observed trabecular thickening is likely to represent a distinct pattern of vertebral bone maturation. As differences in nutritional status, among other factors, are likely to affect skeletal health, it appears essential to routinely perform skeletal assessments in marine mammals. Placing the results in the context of environmental exposures may allow effective measures to protect their populations.

References

Shaw S, Brenner D, Bourakovsky A, Mahaffey C, Perkins C . Polychlorinated biphenyls and chlorinated pesticides in harbor seals (Phoca vitulina concolor) from the northwestern Atlantic coast. Mar Pollut Bull. 2005; 50(10):1069-84. DOI: 10.1016/j.marpolbul.2005.04.010. View

Weijs L, Das K, Siebert U, van Elk N, Jauniaux T, Neels H . Concentrations of chlorinated and brominated contaminants and their metabolites in serum of harbour seals and harbour porpoises. Environ Int. 2009; 35(6):842-50. DOI: 10.1016/j.envint.2009.02.001. View

Hall A, Law R, Wells D, Harwood J, Ross H, Kennedy S . Organochlorine levels in common seals (Phoca vitulina) which were victims and survivors of the 1988 phocine distemper epizootic. Sci Total Environ. 1992; 115(1-2):145-62. DOI: 10.1016/0048-9697(92)90039-u. View

Kahle P, Rolvien T, Kierdorf H, Roos A, Siebert U, Kierdorf U . Age-related changes in size, bone microarchitecture and volumetric bone mineral density of the mandible in the harbor seal (Phoca vitulina). PLoS One. 2019; 14(10):e0224480. PMC: 6812799. DOI: 10.1371/journal.pone.0224480. View

Delsmann M, Seist R, Sturznickel J, Schmidt F, Mansour A, Kobelski M . Conductive Hearing Loss in the Hyp Mouse Model of X-Linked Hypophosphatemia Is Accompanied by Hypomineralization of the Auditory Ossicles. J Bone Miner Res. 2021; 36(12):2317-2328. PMC: 8688200. DOI: 10.1002/jbmr.4443. View

Karsenty G, Khosla S . The crosstalk between bone remodeling and energy metabolism: A translational perspective. Cell Metab. 2022; 34(6):805-817. PMC: 9535690. DOI: 10.1016/j.cmet.2022.04.010. View

Karsenty G, Wagner E . Reaching a genetic and molecular understanding of skeletal development. Dev Cell. 2002; 2(4):389-406. DOI: 10.1016/s1534-5807(02)00157-0. View

Bonewald L . Osteocytes as dynamic multifunctional cells. Ann N Y Acad Sci. 2007; 1116:281-90. DOI: 10.1196/annals.1402.018. View

Bonewald L, Johnson M . Osteocytes, mechanosensing and Wnt signaling. Bone. 2008; 42(4):606-15. PMC: 2349095. DOI: 10.1016/j.bone.2007.12.224. View

10.

Rolvien T, Hahn M, Siebert U, Puschel K, Wilke H, Busse B . Vertebral bone microarchitecture and osteocyte characteristics of three toothed whale species with varying diving behaviour. Sci Rep. 2017; 7(1):1604. PMC: 5431672. DOI: 10.1038/s41598-017-01926-7. View

11.

Schmidt B, Sonne C, Nachtsheim D, Dietz R, Oheim R, Rolvien T . Variation in skull bone mineral density of ringed seals (Phoca hispida) from the Gulf of Bothnia and West Greenland between 1829 and 2019. Environ Int. 2020; 143:105968. DOI: 10.1016/j.envint.2020.105968. View

12.

Sonne C, Lakemeyer J, Desforges J, Eulaers I, Persson S, Stokholm I . A review of pathogens in selected Baltic Sea indicator species. Environ Int. 2020; 137:105565. DOI: 10.1016/j.envint.2020.105565. View

13.

Sonne C, Siebert U, Gonnsen K, Desforges J, Eulaers I, Persson S . Health effects from contaminant exposure in Baltic Sea birds and marine mammals: A review. Environ Int. 2020; 139:105725. DOI: 10.1016/j.envint.2020.105725. View

14.

Anderson P, Morgan S, Krueger D, Zapalowski C, Tanner B, Jeray K . Use of Bone Health Evaluation in Orthopedic Surgery: 2019 ISCD Official Position. J Clin Densitom. 2019; 22(4):517-543. DOI: 10.1016/j.jocd.2019.07.013. View

15.

Siris E, Miller P, Barrett-Connor E, Faulkner K, Wehren L, Abbott T . Identification and fracture outcomes of undiagnosed low bone mineral density in postmenopausal women: results from the National Osteoporosis Risk Assessment. JAMA. 2001; 286(22):2815-22. DOI: 10.1001/jama.286.22.2815. View

16.

Sornay-Rendu E, Boutroy S, Munoz F, Delmas P . Alterations of cortical and trabecular architecture are associated with fractures in postmenopausal women, partially independent of decreased BMD measured by DXA: the OFELY study. J Bone Miner Res. 2006; 22(3):425-33. DOI: 10.1359/jbmr.061206. View

17.

Muller R, Hildebrand T, Ruegsegger P . Non-invasive bone biopsy: a new method to analyse and display the three-dimensional structure of trabecular bone. Phys Med Biol. 1994; 39(1):145-64. DOI: 10.1088/0031-9155/39/1/009. View

18.

Whittier D, Boyd S, Burghardt A, Paccou J, Ghasem-Zadeh A, Chapurlat R . Guidelines for the assessment of bone density and microarchitecture in vivo using high-resolution peripheral quantitative computed tomography. Osteoporos Int. 2020; 31(9):1607-1627. PMC: 7429313. DOI: 10.1007/s00198-020-05438-5. View

19.

Zotti A, Poggi R, Cozzi B . Exceptional bone density DXA values of the rostrum of a deep-diving marine mammal: a new technical insight in the adaptation of bone to aquatic life. Skeletal Radiol. 2009; 38(12):1123-5. DOI: 10.1007/s00256-009-0647-4. View

20.

Sonne C, Dietz R, Born E, Riget F, Kirkegaard M, Hyldstrup L . Is bone mineral composition disrupted by organochlorines in east Greenland polar bears (Ursus maritimus)?. Environ Health Perspect. 2004; 112(17):1711-6. PMC: 1253664. DOI: 10.1289/ehp.7293. View