Age-related changes in size, bone microarchitecture and volumetric bone mineral density of the mandible in the harbor seal (Phoca vitulina)

English version

Autoři: Patricia Kahle ^aff001; Tim Rolvien ^aff002; Horst Kierdorf ^aff001; Anna Roos ^aff004; Ursula Siebert ^aff005; Uwe Kierdorf ^aff001
Působiště autorů: Department of Biology, University of Hildesheim, Hildesheim, Germany ^aff001; Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, Hamburg, Germany ^aff002; Department of Orthopedics, University Medical Center Hamburg-Eppendorf, Hamburg, Germany ^aff003; Department of Contaminant Research, Swedish Museum of Natural History, Stockholm, Sweden ^aff004; Institute of Terrestrial and Aquatic Wildlife Research, University of Veterinary Medicine Hannover, Hannover, Germany ^aff005
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0224480

Souhrn

Detailed knowledge of age-related changes in the structure and mineralization of bones is important for interpreting osseous changes in wild mammals caused by exposure to environmental contaminants. This study analyzed mandibular size, microarchitecture and volumetric bone mineral density (vBMD) in harbor seals (n = 93, age range 0.5 months to 25 years) from the German North Sea. Bone microarchitecture and vBMD were assessed using high-resolution peripheral quantitative computed tomography (HR-pQCT). Significant differences were observed between the analyzed age classes (i) young juveniles (0.5–10 months), (ii) yearlings (12–23 months), and (iii) adults (12–25 years) for several of the variables, indicating an overall increase in cortical and trabecular area, cortical thickness and total and cortical vBMD with age. Furthermore, for juvenile animals (≤ 23 months), significant positive correlations with age were observed for mandible length and perimeter, cortical area, cortical thickness, trabecular separation, and total and cortical vBMD. The findings demonstrate a rapid increase in overall size, cortical dimensions and the degree of mineralization of the harbor seal mandible during the first two years after birth. Negative correlations with age existed for trabecular number and thickness as well as for trabecular bone volume fraction in the juveniles. The findings suggest a reduction in trabecular bone volume fraction with age, due to the bone trabeculae becoming thinner, less numerous and more widely spaced. Given the strong age dependence of most analyzed parameters, it is recommended to standardize samples with respect to age in future studies comparing microarchitecture and mineralization of harbor seal mandibles from different populations or different collection periods.

Klíčová slova:

Mandible – Bears – Contaminants – Marine mammals – Pollutants – Seals

Zdroje

1. Drescher HE, Harms U, Huschenbeth E. Organochlorines and heavy metals in the harbor seal Phoca vitulina from the German North Sea Coast. Marine Biol. 1977; 41:99–106.

2. Olsson M, Karlsson B, Ahnland E. Diseases and environmental contaminants in seals from the Baltic and the Swedish west coast. Sci Total Environ. 1994; 154:217–227. doi: 10.1016/0048-9697(94)90089-2 7973608

3. Weijs L, Dirtu AC, Das K, Gheorghe A, Reijnders PJH, Neels H, et al. Inter-species differences for polychlorinated biphenyls and polybrominated diphenyl ethers in marine top predators from the southern North Sea: Part 1. Accumulation patterns in harbour seals and harbour porpoises. Environ Pollut. 2009; 157:437–444. doi: 10.1016/j.envpol.2008.09.024 18954926

4. Weijs L, van Elk C, Das K, Blust R, Covaci A. Persistent organic pollutants and methoxylated PBDEs in harbor porpoises from the North Sea from 1990 until 2008: Young wildlife at risk? Sci Total Environ. 2010; 409:228–237. doi: 10.1016/j.scitotenv.2010.09.035 20937522

5. HELCOM. Hazardous substances in the Baltic Sea–An integrated thematic assessment of hazardous substance in the Baltic Sea. Baltic Sea Environ Proc. 2010; 120B:1–116.

6. Kakuschke A, Griesel S. Essential and toxic elements in blood samples of harbor seals (Phoca vitulina) from the islands Helgoland (North Sea) and Anholt (Baltic Sea): A comparison study with urbanized areas. Arch Environ Contam Toxicol. 2016; 70:67–74. doi: 10.1007/s00244-015-0205-0 26253942

7. Lehnert K, Desforges JP, Das K, Siebert U. Ecotoxicological biomarkers and accumulation of contaminants in pinnipeds. In: Fossi MC, Panti C (Eds) Marine Mammal Ecotoxicology. Impacts of Multiple Stressors on Population Health. London; Academic Press; 2018. pp. 261–289.

8. Marsili L, Jiménez B, Borrell B. Persistent organic pollutants in cetaceans living in a hotspot area: The Mediterranean Sea. In: Fossi MC, Panti C (Eds) Marine Mammal Ecotoxicology. Impacts of Multiple Stressors on Population Health. London; Elsevier-Academic Press; 2018. pp. 185–212.

9. Routti H, Jenssen BM, Tartu S. Ecotoxicological stress in Arctic marine mammals, with particular focus on polar bears. In: Fossi MC, Panti C (Eds.) Marine Mammal Ecotoxicology. Impacts of Multiple Stressors on Population Health. London; Elsevier-Academic Press; 2018. pp. 345–380.

10. Helle E.; Olsson M.; Jensen S. PCB levels correlated with pathological changes in seal uteri. Ambio. 1976; 5:261–262.

11. Bergman A, Olsson M. Pathology of Baltic grey seal and ringed seal females with special reference to adrenocortical hyperplasia: Is environmental pollution the cause of a widely distributed disease syndrome? Finnish Game Res. 1985; 44:47–62.

12. De Swart RL, Ross PS, Vos JG, Osterhaus AD. Impaired immunity in harbour seals (Phoca vitulina) exposed to bioaccumulated environmental contaminants: review of a long-term feeding study. Environ Health Perspect. 1996; 104 Suppl 4:823–828.

13. Brown TM, Ross PS, Reimer KJ. Transplacental transfer of polychlorinated biphenyls, polybrominated diphenylethers, and organochlorine pesticides in ringed seals (Pusa hispida). Arch Environ Contam Toxicol. 2016; 70:20–27. doi: 10.1007/s00244-015-0191-2 26142122

14. Desforges JPW, Sonne C, Levin M, Siebert U, de Guise S, Dietz R. Immunotoxic effects of environmental pollutants in marine mammals. Environ Int. 2016; 86:126–139. doi: 10.1016/j.envint.2015.10.007 26590481

15. Lind PM, Bergman A, Olsson M, Orberg J (2003). Bone mineral density in male Baltic grey seal (Halichoerus grypus). Ambio. 2003; 32:385–388. doi: 10.1579/0044-7447-32.6.385 14627366

16. Sonne C, Dietz R, Born EW, Rigét FF, Kirkegaard M, Hyldstrup L, et al. Is bone mineral composition disrupted by organochlorines in East Greenland polar bears (Ursus maritimus)? Environ Health Perspect. 2004; 112:1711–1716. doi: 10.1289/ehp.7293 15579418

17. Sonne C. Bechshøft TØ, Rigét FF, Baggøe HJ, Hedayat A, Andersen M, et al. Size and density of East Greenland polar bear (Ursus maritimus) skulls: Valuable bio-indicators of environmental change? Ecol Indic. 2013; 34:290–295.

18. Sonne C, Dyck M, Rigét FF, Beck Jensen JE, Hyldstrup L, Letcher RJ, et al. Penile density and globally used chemicals in Canadian and Greenland polar bears. Environ Res. 2015; 137:287–291. doi: 10.1016/j.envres.2014.12.026 25601730

19. Roos A, Rigét F, Orberg J. Bone mineral density in Swedish otters (Lutra lutra) in relation to PCB and DDE concentrations. Exotoxicol Environ Safety. 2010; 73:1063–1070.

20. Daugaard-Petersen T, Langebæk R, Rigét FF, Dyck M, Letcher RJ, Hyldstrup L, et al. Persistent organic pollutants and penile bone mineral density in East Greenland and Canadian polar bears (Ursus maritimus) during 1996–2015. Environ Int. 2018a; 114:212–218.

21. Daugaard-Petersen T, Langebæk R, Rigét FF, Letcher RJ, Hyldstrup L, Bech Jensen JE, et al. Persistent organic pollutants, skull size and bone density of polar bears (Ursus maritimus) from East Greenland 1892–2015 and Svalbard 1964–2004. Environ Res. 2018b; 162:74–80.

22. Pertoldi C, Jensen LF, Alstrup AKO, Munk OL, Pedersen TB, Sonne C. et al. Prevalence of skull pathologies in European harbor seals (Phoca vitulina) during 1981–2014. Mamm Res. 2018; 63:55–63.

23. Bergman A, Olsson M, Reiland S. Skull-bone lesions in the Baltic grey seal (Halichoerus grypus). Ambio. 1992; 21:517–519.

24. Mortensen P, Bergman A, Bignert A, Hansen HJ, Härkönen T, Olsson M. Prevalence of skull lesions in harbor seals (Phoca vitulina) in Swedish and Danish museum collections: 1835–1988. Ambio. 1992; 21: 520–524.

25. Schandorff S. Developmental stability and skull lesions in the harbour seal (Phoca vitulina) in the 19th and 20th Centuries. Ann Zool Fennici. 1997; 34:151–166.

26. Österblom H, Hansson S, Larsson U, Hjerne O, Wulff F, Elmgren R, et al. Human-induced trophic cascades and ecological regime shifts in the Baltic Sea. Ecosystems. 2007; 10:877–889.

27. Aarts G, Brasseur S, Poos JJ, Schop J, Kirkwood R, van Kooten T, et al. Top-down pressure on a coastal ecosystem by harbor seals. Ecosphere. 2019; 10:e02538.

28. Galatius A, Brasseur S, Cremer J, Czeck R, Jeß A, Körber P, et al. Aerial surveys of harbor seals in the Wadden Sea in 2018. Common Wadden Sea Secretariat, Wilhelmshaven, Germany, 2018. https://www.waddensea-secretariat.org/sites/default/files/downloads/TMAP_downloads/Seals/2018_harbour_seal_report.pdf. Last accessed 13 August 2019.

29. Burns JJ. Harbor seal and spotted seal—Phoca vitulina and P. largha. In: Perrin WF, Würsig BG, Thewissen JGM (Eds) Encyclopedia of Marine Mammals. Second edition. Amsterdam; Elsevier-Academic Press; 2009 pp. 533–542.

30. Aerrsens J, Boonen S, Lowet G, Dequeker J. Interspecies differences in bone composition, density, and quality: Potential implications for in vivo bone research. Endocrinology. 1998; 139:663–670. doi: 10.1210/endo.139.2.5751 9449639

31. Mulder L, Koolstra JH, de Jonge HW, van Eijden TMGJ. Architecture and mineralization of developing cortical and trabecular bone of the mandible. Anat Embryol. 2006; 211:71–78. doi: 10.1007/s00429-005-0054-0 16374611

32. Willems NMBK, Mulder L, Langenbach GEJ, Grünheid T, Zentner A, van Eijden TMGJ. Age-related changes in microarchitecture and mineralization of cancellous bone in the porcine mandibular condyle. J Struct Biol. 2007; 158:421–427. doi: 10.1016/j.jsb.2006.12.011 17300959

33. Storå J. Skeletal development in the grey seal Halichoerus grypus, the ringed seal Phoca hispida botnica, the harbour seal Phoca vitulina vitulina and the harp seal Phoca groenlandica. Epiphyseal fusion and life history. Archaeozoologia 2000; 11:199–222.

34. Kahle P, Ludolphy C, Kierdorf H, Kierdorf U. Dental anomalies and lesions in Eastern Atlantic harbor seals, Phoca vitulina vitulina (Carnivora, Phocidae), from the German North Sea. PLoS ONE. 2018;13:e0204079. doi: 10.1371/journal.pone.0204079 30281623

35. Ludolphy C, Kahle P, Kierdorf H, Kierdorf U. Osteoarthritis of the temporomandibular joint in the Eastern Atlantic harbour seal (Phoca vitulina vitulina) from the German North Sea: a study of the lesions seen in dry bone. BMC Vet Res. 2018; 14:150. doi: 10.1186/s12917-018-1473-5 29716601

36. Abt KF. Phänologie und Populationsdynamik des Seehundes (Phoca vitulina) im Wattenmeer: Grundlagen zur Messung von Statusparametern. Doctoral thesis. Christian-Albrechts-Universität, Kiel. 2002.

37. Härkönen T, Heide-Jørgensen MP. Comparative life histories of East Atlantic and other harbour seal populations. Ophelia. 1990; 32:211–235.

38. Chu TMG, Liu SSY, Babler WJ. Craniofacial biology, orthodontics, and implants. In: Burr DB, Allen MR (Eds): Basic and Applied Bone Biology. Amsterdam; Elsevier-Academic Press; 2014. pp. 225–242.

39. Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Müller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res. 2010; 25:1468–1486. doi: 10.1002/jbmr.141 20533309

40. Siegel S, Castellan NJ. Nonparametric Statistics for the Behavioral Sciences. Second edition. New York; McGraw-Hill; 1988.

41. Bala Y, Farlay D, Delmas PD, Meunier PJ, Boivin G. Time sequence of secondary mineralization and microhardness in cortical and cancellous bone from ewes. Bone. 2010; 46:1204–1212. doi: 10.1016/j.bone.2009.11.032 19969115

42. Bala Y, Farlay D, Boivin G. Bone mineralization. From tissue to crystal in normal and pathological contexts. Osteoporos Int. 2013; 24:2153–2166. doi: 10.1007/s00198-012-2228-y 23229470

43. Cao T, Shirota T, Yamazaki M, Ohno K, Michi K. Bone mineral density in mandibles of ovariectomized rabbits. Clin Oral Impl Res. 2001; 12:604–608.

44. Glorieux FH, Travers R, Taylor A, Bowen JR, Rauch F, Norman M, et al. Normative data for iliac bone histomorphometry in growing children. Bone. 2000; 26:103–109. doi: 10.1016/s8756-3282(99)00257-4 10678403

45. Gosman JH. 2012. Growth and Development: Morphology, Mechanisms, and Abnormalities. In: Crowder C, Stout S (Eds) Bone histology: An anthropological perspective. Boca Raton; CRC Press. pp. 23–44.

46. Rolvien T, Hahn M, Siebert U, Püschel K, Wilke H-J, Busse B, et al. Vertebral bone microarchitecture and osteocyte characteristics of three toothed whale species with varying diving behaviour. Sci Rep. 2017; 7:1604. doi: 10.1038/s41598-017-01926-7 28487524

47. Schmidt FN, Delsmann MM, Mletzko K, Yorgan TA, Hahn M, Siebert U, et al. Ultra-high mineralization of sperm whale auditory ossicles facilitates high sound pressure and high-frequency underwater hearing. Proc R Soc B. 2018; 285:20181820. doi: 10.1098/rspb.2018.1820 30963901

48. Blake GN; Fogelman I. Methods and clinical issues in bone densitometry. In: Bilezikian JP, Raisz LG, Martin TJ (Eds) Principles of Bone Biology. Third edition. Amsterdam; Elsevier-Academic Press; 2008. pp. 1883–1894.

49. Sekhon K, Kazakia GJ, Burghardt AJ, Hermannson B, Majumdar S. Accuracy of volumetric bone mineral density measurement in high resolution peripheral quantitative computed tomography. Bone. 2009; 45:473–479. doi: 10.1016/j.bone.2009.05.023 19501201

50. Zhou B, Wang J, Yu YE, Zhang Z, Nawathe S, Nishiyama KK, et al. High-resolution peripheral quantitative computed tomography (HR-pQCT) can assess microstructural and biomechanical properties of both human distal radius and tibia: Ex vivo computational and experimental validations. Bone. 2016; 86:58–67. doi: 10.1016/j.bone.2016.02.016 26924718

Age-related changes in size, bone microarchitecture and volumetric bone mineral density of the mandible in the harbor seal (Phoca vitulina)

Souhrn

Klíčová slova:

Zdroje

PLOS One

Aktuální možnosti diagnostiky a léčby litiáz