Periodontal disease and fluoride bone levels in two separate Iberian red deer populations
C. Azorit A B , M. J. Rodrigo A , S. Tellado A and M. C. Sánchez-Ariza A
+ Author Affiliations
- Author Affiliations
A Department of Animal and Vegetal Biology and Ecology, Faculty of Experimental Sciences, University of Jaén, 23071, Spain.
B Corresponding author. Email: cazorit@ujaen.es
Animal Production Science 52(8) 774-780 https://doi.org/10.1071/AN12014
Submitted: 13 January 2012 Accepted: 27 April 2012 Published: 12 June 2012
Abstract
The mandibles of 209 red deer (Cervus elaphus hispanicus) from 6 months to 15 years old, shot between 2001 and 2002 in the Sierra de Andújar Natural Park (n = 173) and National Park of Doñana (n = 36) in southern Spain, were studied in order to assess spatial variations in the occurrence of periodontal disease and bone fluoride levels in two separate populations. Similarities were found in periodontal disease prevalence between the study areas (20.8% in Sierra de Andújar Natural Park and 33.3% in National Park of Doñana), and enamel defects or abnormal abrasion (7–10%, respectively). There were also variations in fluoride levels according to the area and the occurrence of periodontal disease, irrespective of age. Fluoride content was significantly lower in deer in Sierra de Andújar (250.5 ± 158.9 mg F/kg ash) than in Doñana (752.4 ± 451.0 mg F/kg ash), and the higher levels of bone fluoride occurred in mandibles showing periodontal disease in both areas (358.6 ± 201.7 and 1224.9 ± 422.34 mg F/kg, respectively). The fluoride levels were lower than expected, typical of non-polluted areas, and there was no significant influence of the occurrence of enamel defects on the bone fluoride concentration. In these areas pathologically increased attrition, enamel discolouration or enamel surface lesions seem not to be caused by fluorosis, so that special care must also be taken in using macroscopic lesions instead of fluoride determination as an indicator for monitoring the magnitude of environmental contamination. Research into the global mineral content and possible deficiencies in certain minerals such as selenium, phosphorus and calcium interacting with fluoride is necessary in order to understand the high prevalence of periodontal disease in younger animals and the higher concentrations of fluoride in mandibles with periodontal disease.
References
Alexander TL (1983) ‘Management and diseases of deer.’ (Veterinary Deer Society: London)Azorit C, Analla M, Carrasco R, Calvo JA, Muñoz-Cobo J (2002a) Teeth eruption pattern in red deer (Cervus elaphus hispanicus) from southern Spain. Annals of Biology 24, 193–200.
Azorit C, Muñoz-Cobo J, Analla M (2002b) Seasonal deposition of cementum in first lower molars from Cervus elaphus hispanicus. Mammalian Biology 67, 243–245.
| Seasonal deposition of cementum in first lower molars from Cervus elaphus hispanicus.Crossref | GoogleScholarGoogle Scholar |
Azorit C, Analla M, Hervas J, Carrasco R, Muñoz-Cobo J (2002c) Growth marks observation: preferential techniques and teeth for ageing of Spanish Red Deer (Cervus elaphus hispanicus). Anatomia, Histologia, Embryologia 31, 303–307.
| Growth marks observation: preferential techniques and teeth for ageing of Spanish Red Deer (Cervus elaphus hispanicus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38jitFOmuw%3D%3D&md5=dbe416c67a2f0d62febafad05f8ae6f1CAS |
Azorit C, Analla M, Carrasco R, Muñoz-Cobo J (2003) Effect of sex, density and year of death upon the tooth wear in red deer populations (Cervus elaphus hispanicus Erxleben, 1777) (Mammalia, Cervidae) in Sierra Morena. Boletin de la Real Sociedad Espanola de Historia Natural. Seccion Biologica 98, 115–122.
Azorit C, Analla M, Hervás J, Muñoz-Cobo J (2004) Aging through growth marks in teeth of Spanish red deer (Cervus elaphus hispanicus). Wildlife Society Bulletin 32, 702–710.
| Aging through growth marks in teeth of Spanish red deer (Cervus elaphus hispanicus).Crossref | GoogleScholarGoogle Scholar |
Azorit C, Muñoz-Cobo J, Tellado S, Cara-Ortega C, López-Pulido P, López-Izquierdo O, Moro J (2011) Assessing mineral content in teeth and bones of red (Cervus elaphus hispanicus) and fallow deer (Dama dama) using scanning electron microscope analysis. In ‘Abstracts book of the XXXth International Union of Game Biologists Congress and Perdix XIII, Barcelona, Spain, 5th–9th September 2011’. (Eds M Puigcerver, JDR Teijeiro, F Buner) p. 235.
Azorit C, Oya A, Tellado S, Carrasco R, Moro J (2012) Mandibular osteomyelitis in red deer (Cervus elaphus hispanicus) and fallow deer (Dama dama): occurrence and associated factors in free-living populations in southern Spain. Journal of Wildlife Diseases 48, 77–86.
Browne D, Whelton H, O’Mullane D (2005) Fluoride metabolism and fluorosis. Journal of Dentistry 33, 177–186.
| Fluoride metabolism and fluorosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhslCisbc%3D&md5=bfb25fa049b7019489aab63baea37bdbCAS |
Fagan DA (1980) Diet consistency and periodontal disease in exotic carnivores. In ‘Proceeding of the annual meeting of the American Association of Zoo Veterinarians, Washington, DC’. pp. 34–37.
Federation Dentaire Internationale (1982) An epidemiological index of developmental defects of enamel (DDE Index). International Dental Journal 42, 411–426.
Flueck W, Smith-Flueck JA (2008) Age-independent osteopathology in skeletons of a South American cervid, the Patagonian huemul (Hippocamelus bisulcus). Journal of Wildlife Diseases 44, 636–648.
Flueck WT, Smith-Flueck JAM (2011) Recent advances in the nutritional ecology of the Patagonian huemul: implications for recovery. Animal Production Science 51, 311–326.
Geiger G, Thome H, Kuehl A (1992) Parodontal bedingte Veränderungen am Processus alveolaris beim Rotwild. Zeitschrift fur Jagdwissenschaft 38, 107–115.
| Parodontal bedingte Veränderungen am Processus alveolaris beim Rotwild.Crossref | GoogleScholarGoogle Scholar |
Glickman I (1979) Bone loss and patterns of bone destruction in periodontal disease. In ‘Clinical periodontology’. (Ed. I Glickman) pp. 248–258. (WB Saunders: Philadelphia, PA)
González I, Aparicio P, Galán E, Fabbri B (2002) A proposal for reducing F and Cl emission in the brick industry using new formulations. Applied Clay Science 22, 1–7.
| A proposal for reducing F and Cl emission in the brick industry using new formulations.Crossref | GoogleScholarGoogle Scholar |
Gual F, Suárez de Gual MC (1996) Enfermedad periodontal en mamíferos silvestres; ¿un problema asociado al cautiverio? Veterinaria (México) 27, 165–173.
Hidalgo C, Rey J, Benavente J, Martínez J (2010) Hydrogeochemistry of abandoned Pb sulphide mines: the mining district of La Carolina (southern Spain). Environmental Earth Science 61, 37–46.
| Hydrogeochemistry of abandoned Pb sulphide mines: the mining district of La Carolina (southern Spain).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXos1CitLg%3D&md5=a3408b14c78aeb3e50274c4f5277474dCAS |
Hudson-Edwards KA, Schellb C, Macklinb MG (1999) Mineralogy and geochemistry of alluvium contaminated by metal mining in the Rio Tinto area, southwest Spain. Applied Geochemistry 14, 1015–1030.
| Mineralogy and geochemistry of alluvium contaminated by metal mining in the Rio Tinto area, southwest Spain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtVOksbc%3D&md5=6953872f7aaac040475ac5b9dab1b9c5CAS |
Jelenko I, Pokorny B (2010) Historical biomonitoring of fluoride pollution by determining fluoride contents in roe deer (Capreolus capreolus L.) antlers and mandibles in the vicinity of the largest Slovene thermal power plant. The Science of the Total Environment 409, 430–438.
| Historical biomonitoring of fluoride pollution by determining fluoride contents in roe deer (Capreolus capreolus L.) antlers and mandibles in the vicinity of the largest Slovene thermal power plant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFaktrrN&md5=201fd67d2e5bced0a3fbc1aecd1adeb0CAS |
Kierdorf H, Kierdorf U (1999) Dental fluorosis in wild deer: its use as a biomarker of increased fluoride exposure. Environmental Monitoring and Assessment 57, 265–275.
| Dental fluorosis in wild deer: its use as a biomarker of increased fluoride exposure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkslelurc%3D&md5=4c4b1597897df6797a2f8fbc37dafbf2CAS |
Kierdorf U, Kierdorf H (2000) The fluoride content of antlers as an indicator of fluoride exposure in red deer (Cervus elaphus): a historical biomonitoring study. Environmental Contamination and Toxicology 38, 121–127.
| The fluoride content of antlers as an indicator of fluoride exposure in red deer (Cervus elaphus): a historical biomonitoring study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXks1yj&md5=3b2879b403b026fae9c5fa187071a47cCAS |
Kierdorf U, Kierdorf H, Erdelen M, Korsch JP (1989) Mandibular fluoride concentration and its relation to age in roe deer (Capreulus capreolus L.) Comparative Biochemistry and Physiology 94A, 783–785.
Kierdorf U, Kierdorf H, Erdelen M, Machoy Z (1995) Mandibular bone fluoride accumulation in wild red deer (Cervus elaphus L.) of known age. Comparative Biochemistry and Physiology. Part A, Physiology 110, 299–302.
| Mandibular bone fluoride accumulation in wild red deer (Cervus elaphus L.) of known age.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M3ltlyqsQ%3D%3D&md5=aa8f1da9d642fc581120daefd225fe93CAS |
Kierdorf H, Kierdorf U, Sedlacek F, Erdelend M (1996) Mandibular bone fluoride levels and occurrence of fluoride induced dental lesions in populations of wild red deer (Cervus elaphus) from central Europe. Environmental Pollution 93, 75–81.
| Mandibular bone fluoride levels and occurrence of fluoride induced dental lesions in populations of wild red deer (Cervus elaphus) from central Europe.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlvVCnt7s%3D&md5=7f6fcdfb2fa3b4d1a2306f34f2365f53CAS |
Kierdorf U, Richards A, Sedlacek F, Kierdorf H (1997) Fluoride content and mineralization of red deer (Cervus elaphus) antlers and pedicles from fluoride polluted and uncontaminated regions. Archives of Environmental Contamination and Toxicology 32, 222–227.
| Fluoride content and mineralization of red deer (Cervus elaphus) antlers and pedicles from fluoride polluted and uncontaminated regions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXisFejtr4%3D&md5=ecba2aba09a2d58a4dcb2a5500b18098CAS |
Kierdorf U, Kierdof H, Boyde A (2000) Structure and mineralisation density of antler and pedicle bone in red deer (Cervus elephus L.) exposed to different levels of environmental fluoride: a quantitative backscattered electron imaging study. Journal of Anatomy 196, 71–83.
| Structure and mineralisation density of antler and pedicle bone in red deer (Cervus elephus L.) exposed to different levels of environmental fluoride: a quantitative backscattered electron imaging study.Crossref | GoogleScholarGoogle Scholar |
Kierdorf U, Bahelková P, Sedláček F, Kierdorf H (2012) Pronounced reduction of fluoride exposure in free-ranging deer in North Bohemia (Czech Republic) as indicated by the biomarkers skeletal fluoride content and dental fluorosis. The Science of the Total Environment 414, 686–695.
| Pronounced reduction of fluoride exposure in free-ranging deer in North Bohemia (Czech Republic) as indicated by the biomarkers skeletal fluoride content and dental fluorosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XotVansQ%3D%3D&md5=6c110745640dd80950beec90b7b1cae3CAS |
Machoy Z, Dabkowska E, Nowicka W (1991) Increased fluoride content in mandibular bones of deer living in industrialised regions of Poland. Environmental Geochemistry and Health 13, 161–163.
| Increased fluoride content in mandibular bones of deer living in industrialised regions of Poland.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XhtlGns7s%3D&md5=08cc7a35a11ebabe04dd905ad6ed84b3CAS |
Miles AEW, Grigson C (1990) ‘Colyer’s variation and diseases of the teeth of animals.’ (Cambridge University Press: Cambridge, UK)
Ozsvath DL (2009) Fluoride and environmental health: a review. Reviews in Environmental Science and Biotechnology 8, 59–79.
| Fluoride and environmental health: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitVOrtbo%3D&md5=9d045d2c0309ca0504c149b744d5b829CAS |
Palmer N (1993) Metabolic diseases of bone. In ‘Pathology of domestic animals’. (Eds KVF Jubb, PC Kennedy, N Palmer) pp. 55–93. (Academic Press: Orlando, FL)
Richter H, Kierdorf U, Richards A, Kierdorf H (2010) Dentin abnormalities in cheek teeth of wild red deer and roe deer from a fluoride-polluted area in Central Europe. Annals of Anatomy 192, 86–95.
| Dentin abnormalities in cheek teeth of wild red deer and roe deer from a fluoride-polluted area in Central Europe.Crossref | GoogleScholarGoogle Scholar |
Samuel JL, Woodall PF (1988) Periodontal disease in feral pigs (Sus scrofa) from Queensland, Australia. Journal of Wildlife Diseases 24, 201–206.
Schultz M, Kierdorf U, Sedlacek F, Kierdorf H (1998) Pathological bone changes in the mandibles of wild red deer (Cervus elaphus L.) exposed to high environmental levels of fluoride. Journal of Anatomy 193, 431–442.
| Pathological bone changes in the mandibles of wild red deer (Cervus elaphus L.) exposed to high environmental levels of fluoride.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjsVWnsw%3D%3D&md5=67d809de9d9800f4e857f9c37a021b95CAS |
Wactawski-Wende J (2001) Periodontal diseases and osteoporosis: association and mechanisms. Annals of Periodontology 6, 197–208.
| Periodontal diseases and osteoporosis: association and mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD387lsFKrtQ%3D%3D&md5=003a24b32c09db14d25545a79e616a8cCAS |
Whalen JP, Krook L (1996) Periodontal disease as the early manifestation of osteoporosis. Nutrition 12, 53–54.
| Periodontal disease as the early manifestation of osteoporosis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK28vjsF2msA%3D%3D&md5=fa73a399a7d3aecb32d12b519c05cdbbCAS |
Wiebe CB, Putnins EE (2000) The periodontal disease classification system of the American Academy of Periodontology: an update. Journal of the Canadian Dental Association 66, 594–597.
Wiebe CB, Adkins CA, Putnins EE, Hakkinen L, Larjava HS (2001) Naturally occurring periodontal bone loss in the wild deer mouse Genus Peromyscus. Journal of Periodontology 72, 620–625.
| Naturally occurring periodontal bone loss in the wild deer mouse Genus Peromyscus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3Mzis1KltA%3D%3D&md5=fb0abce744a78325b21603649d042a2eCAS |
Woodall PF (1989) Periodontal disease in southern African bushpigs (Potamochoerus porcus) and warthogs (Phacochoerus aethiopicus). Journal of Wildlife Diseases 25, 66–69.
Zipkin I, Likins RC, McClure FJ (1958) Deposition of fluoride, calcium and phosphorus in experimental low-phosphorus rickets. The Journal of Nutrition 67, 59–68.
