Low Calcium Intake and Hypovitaminosis D Negatively Affect Oral Health in Young Men

  

    
 
    
Calcium Intake (mg/day)
    
25 OHD (ng/mL)
  
  

    
 
    
=800
    
800-600
    
< 600
    
= 30
    
21-29
    
= 20
  
  

    
 
    
-28%
    
-24%
    
-48%
    
-29%
    
-49%
    
-22%
  
  

    
D (DMFT)
    
3.8±1.0 
    
2.0±0.8 
    
6.4±0.9*,** 
    
4.2±0.8 
    
4.7±1.3 
    
4.8±0.7 
  
  

    
M (DMFT) 
    
0.3±0.2 
    
0.2±0.1 
    
1.8±0.5* 
    
0.8±0.6 
    
1.3±0.5 
    
1.5±0.9 
  
  

    
F (DMFT) 
    
6.3±1.2 
    
6.2±1.1 
    
5.3±1.0 
    
5.7±1.8 
    
5.8±1.2 
    
6.1±2.0 
  
  

    
PI RV: =1
    
1.5±0.2 
    
1.5±0.1 
    
2.2±0.2*,** 
    
1.8±0.5 
    
1.8±0.4 
    
1.6±0.2 
  
  

    
SI� RV: <4 
    
5.3±0.2 
    
5.4±0.1 
    
5.7±0.1 
    
5.2±0.3 
    
5.4±0.2 
    
5.5±0.2 
  
  

    
Total Teeth
    
29.2±0.4 
    
29.0±1.1 
    
28.9±0.3 
    
28.6±0.9 
    
29.3±0.6 
    
29.1±0.8 
  
  

    
D/Total
    
7.10% 
    
6.90% 
    
18.8%*,** 
    
19.10% 
    
17.80% 
    
16.20% 
  
  

    
IC95:1.9-13.7 
    
IC95:2.4-13.5 
    
IC95:13.9-32.8 
    
IC95:10.9-28.7 
    
IC95:4.8-23.9 
    
IC95:3.1-23.2 
  
  

    
M/Total
    
1% 
    
2% 
    
11%*,** 
    
0% 
    
1% 
    
3.8%#,� 
  
  

    
IC95:0.0-3.9 
    
IC95:0.0-6.0 
    
IC95:4.1-14.5 
    
IC95:0.0-3.5 
    
IC95:0.0-6.6 
    
IC95:1.0-11.2 
  
  

    
F/Total
    
9.50% 
    
15.80% 
    
18.2%* 
    
16.10% 
    
19.30% 
    
19.90% 
  
  

    
IC95:3.2-9.5 
    
IC95:7.8-29.1 
    
IC95:13.1-30.8 
    
IC65:7.1-34.9 
    
IC95:8.0-24.7 
    
IC95:7.6-34.1 
  
  

    
D/DMF and M/DMF, PI, SI and total teeth are    expressed as mean±SD. Data were analyzed by ANOVA two factors and Multiple    Comparison test as a post hoc test. D/total and M/total are expressed as    percentage and they were analyzed by Chi-square test and Multiple comparison    test as a post hoc test *p < 0.05 compared to CaI intake>    800 mg/day; **p < 0.05 compared to Ca intake 800-600 mg/day; #    p<0.05 compared to levels of 25OHD>30 ng/mL;
      
�� p<0.05 compared to levels of 25OHD 21-29 ng/mL. 
  

Table 4: Mean values the decayed (D), Missing (M) and Filling (F) index (DMFT) and, D and M component as percentage of total teeth, Plaque Index Löe Silness (PI
), Sugar Intake (SI) and total teeth according to Ca intake and 25OHD levels in the studied men (n=241).

Dental status parameters corresponding to each of the studied 25 OHD levels are shown in Table 4. Only M/T was higher in the group with 25OHD levels <20 ng/mL as compared to the other studied groups (p<0.05). No significant differences in the remaining dental studied parameters were observed among the three 25 OHD groups.

When the group with the highest caries score was compared to the rest of the men several differences in the study variables were observed. In this regard, comparison of the one third of the studied group with the highest DMFT scores (DMFT33%: 17.4±0.5) with the remaining 67% (DMFT67% 8.1±0.6) showed that those with highest prevalence of dental caries (HPC) had significantly lower CaI (657±49 vs. 481±72 mg/d, p=0.023) and Ca/protein intake (10.9±1.2 vs. 7.1±1.0 p<0.05) than those with low prevalence of caries (LPC); however no significant differences were observed in protein intake (1.11±0.39 vs. 0.98±0.51 g/kg/d) or in 25OHD levels (26.2±4.3 vs. 22.9±3.1 ng/mL). HPC men as compared to LPC subjects also showed significantly higher mean PI (1.8±0.1 vs. 2.1±0.1; p<0.05) and daily consumption of soft drinks (55% vs. 79%; p<0.05) while SI almost reached significance (5.1±0.2 vs. 5.5±0.1; p=0.06).

Discussion

The group of young men studied here showed high cariogenic activity and severity of oral disease. The poor Ca and vitamin D nutritional status, the high CaI/protein intake ratio, the frequent intake of extrinsic sugar, and the high consumption of soft drinks might have contributed to the high dental caries activity observed in the studied men. The negative impact of the dietary factors became evident when comparing the 33% of men exhibiting significantly higher cariogenic activity and the remaining 67%. Indeed, the group of men exhibiting the worst oral health had lower CaI and Ca/protein intake ratio, higher daily consumption of soft drinks, and higher plaque index.

The severity and prevalence of caries was established with the DMFT score, commonly used in the dental practice. This score has continuously been used by the National Health and Nutrition Examination Survey (NHANES) to assess caries prevalence [29]. The overall mean DMFT score in the studied men was 11.4, with filled teeth accounting for around 50% of the dental caries experience. This value is almost two-fold the 6.6 DMFT score estimated for the Argentine population aged 20 to 30 years. This estimate arises from extrapolating the DMFT scores of 12-year-old children and 35-44- year old adults published by the WHO oral health surveillance in 2003 [25]. Mean DMFT score increased to 17.4 in the 33% of men corresponding to the group with higher cariogenic activity; the contribution of the F component was similar (50%) to that observed in the whole population.

Several dietary habits may account for the high cariogenic activity observed in the studied men. Mean CaI was 619.4 mg/d [432.5-809.1], showing that a very high percentage did not meet dietary recommendation. In this regard, 72% of men had estimated average requirements (EAR) lower than 800 mg/d, and 91% did not meet the recommended dietary allowance (RDA) of 1000 mg/d. The percentage of men with poor Ca nutritional status rose to 78% and to 100%, respectively, when analysing the third of the studied population with worse dental health. The low CaI observed here is certainly the result of low consumption of milk and dairy products, since these products provide the largest amounts of dietary Ca. This was not an unexpected finding: although there are no epidemiological studies conducted exclusively in young men, several national and international reports have shown inadequate CaI in adolescents and young adults. A review of several studies conducted between 1998 and 2006 showed insufficient CaI (approximately 500 mg/d) in the Argentinean population associated with low consumption of milk and dairy products, independently of age and socioeconomic status [20]. The aforementioned review included the results of the National Survey on Nutrition and Health (ENNyS), which showed inadequate Ca intake in a high percentage of participants whose age was within the age range studied here [12]. A more recent study, the éDairy consumption patterns in Argentina Population” conducted in 2009 in 1137 Argentinean adult subjects of both sexes (19-30 years of age) revealed that 65% of subjects did not meet the recommended dietary portion of milk or dairy products per day [30].

Over the last two decades, several researchers have reported a decrease in milk intake together with an increase in the consumption of soft drinks, suggesting that consumption of the latter has displaced consumption of milk [1]. The results of the present report evidenced such displacement, showing an inverse correlation between daily consumption of soft drinks and CaI. An important finding herein, was that the young men who covered RDA of Ca did not consume this kind of beverage daily. It is well known that an optimal CaI prevents alveolar bone loss, benefiting tooth retention [2,8]. Milk provides Ca and other components such as P, lactose, and caseinphosphopeptides which enhance not only Ca absorption but also tooth health [15,31]. The concentrations of Ca and P in dental plaque are critical in terms of caries development, given the inverse relation between the concentrations of these ions in the plaque matrix and caries experience [32]. The increase in these components in plaque or saliva inhibits bacterial adhesion to enamel and bacterial biofilm formation [31], and enhances and decreases enamel remineralization and demineralization, respectively [33]. Two deleterious effects on tooth health may result from replacing milk with soft drinks: a change in the type of ingested sugar and an increase in the frequency of sugar intake. A high consumption of soft drinks increases the intake of free sugars or énon-milk extrinsic sugars” as opposed to the intake of lactose or émilk sugars”. This change is potentially damaging to dental health because extrinsic sugars are potentially more cariogenic, whereas milk sugars have low cariogenicity and are cariostatic [6]. Fermentable sugars (glucose, sucrose, and fructose) induce major changes during the process of biofilm formation. Following intake of these sugars, the anaerobic metabolism of oral bacteria lowers the pH in the dental plaque and triggers a shift in the balance of resident plaque microflora to a more cariogenic one that reduces the Ca, P and fluoride in the matrix of dental plaque, increasing susceptibility to caries development [28,32]. Whereas sucrose is the most cariogenic sugar, excessive exposure to fructose may also produce dental caries. However, according to reports, fresh fruit appears to be of low cariogenicity and citrus fruits have not been associated with dental caries. Moreover, it has been posited that increasing consumption of fresh fruit in order to replace ‘non-milk extrinsic sugars’ (free sugars) in the diet is likely to decrease the level of dental caries in a population [28].

The frequency of sugar consumption is also directly related to the prevalence of dental caries [28,34]. An increase in the frequency of exposure to carbohydrates results in the plaque being subjected to a prolonged period below the critical pH for enamel demineralization. This effect favors growth and selection of cariogenic bacteria, thereby enhancing demineralization. The very high SI and low consumption of fruit observed in the men studied here strongly suggest that sweeteners from soft drinks were eaten frequently during the day, increasing the overall length of time of exposure of teeth to sugars. Furthermore, although 60.1% of the studied men had a normal BMI, 18.7% had degree I obesity and 11.2% were overweight. A high BMI in healthy individuals may account for a high consumption of sugars, specially sucrose, and other carbohydrates. Moreover, a high BMI has been associated with poor oral health [7].

Dietary sugar changes the bacterial profile increasing the number of aciduric-bacteria. This type of microorganism can largely synthetize insoluble extracellular polysaccharides (EPS), which not only increase biofilm acidogenicity but also promote adherence of oral bacteria providing the biofilm with structural integrity and bulk. Dental plaque accumulation and poor oral hygiene are the two main overriding factors in the etiology of periodontal disease. Time must be a most important factor in considering plaque as an etiological risk-factor for caries and periodontitis [6]. In the present study, the men exhibiting deficient CaI had high plaque index values at the time of inspection. Plaque accumulation is an additional factor that would account for the high cariogenic status observed in the studied men who lived in a region where drinking-water is fluoridated.

Vitamin D is essential to Ca absorption and mineralization. The nutritional status of vitamin D is determined by the levels of 25OHD, which in the present report were 25.3±1.9 ng/mL. However, 71% of the studied men had an insufficient/deficient vitamin status D. This percentage is like the percentage of men who showed Ca inadequacy. It is well documented that chronically low CaI together with low 25OHD levels have a deleterious effect on bone health, which would become manifest in adulthood. Ca and vitamin D are required to achieve optimal peak bone mass, which is not attained until the age of 25-30 years, the age range of the men studied here [1]. Both nutrients are also required in adulthood to reduce age-related bone loss. A low Ca and/or vitamin D nutritional status stimulates parathyroid hormone (PTH) release, the main factor causing the increase in bone resorption. In the present report, mean PTH and CTX concentrations were within reference values; however, the group of men with the lowest CaI and/or 25OHD levels presented the highest serum levels of both parameters suggesting a slight increase in bone remodeling. Systemic bone resorption would not only lead to bone loss overtime, increasing the risk of fragility fractures, but would also decrease alveolar bone mineral density (BMD), affecting tooth retention in the long term [6,35].

Low serum levels of 25OHD have been reported to be a risk factor for periodontal disease [24]. Vitamin D may potentially influence periodontal risk by reducing oral inflammation and by promoting antimicrobial peptide production. Several researchers have suggested that to ensure these extra-skeletal effects, 25OHD levels should be higher than 30-32 ng/ml [11]. The results of the present report showed that 73% of the young men had 25OHD levels below 32ng/ ml, suggesting that the immunomodulatory action of vitamin D was impaired. This high prevalence of vitamin D insufficiency was not unexpected, since it has been classified as an éepidemic” affecting different age groups, including young adults [11]. In the present report 100% of the studied men had gingivitis, suggesting a certain degree of inflammation. Although pocket probing depth was not assessed, the high level of both gingivitis and plaque accumulation suggests that onset of periodontitis was imminent.

The results of the present report showed that protein intake recommendation was met. Nevertheless, it must be kept in mind that protein protects bone health when CaI requirements are met [36,37]. The low CaI, observed in the present report decreased the CaI/protein intake ratio below the 20 mg/g required to protect mineralized tissues [32], adding yet another risk factor potentially affecting the subjects’ oral health. In addition, the Ca/protein intakes ratio was even lower in the men exhibiting higher cariogenic activity.

It is well documented that smoking affects oral health [17]. The present study had too few smokers (25%) to investigate the changes according to smoking status. However, 71% of smokers did not meet CaI recommendations, and 53% had a deficient CaI. The latter men had more teeth affected by caries and 37% were missing at least one tooth.

Limitations

The limitations to the present report are the relatively small population of healthy men and the lack of information regarding many potentially confounding variables related to oral hygiene that may affect oral health. However, the number of missing teeth and high plaque index clearly evidence that the young men studied here had poor oral health. The strength of the present report is that all participants had a similar socioeconomic status, since a low socioeconomic status is a predisposing factor in the development of dental caries in adults.

Conclusion

The results of this cross-sectional report evidenced a low consumption of milk that along with a high daily consumption of soft drinks may account for the great severity of oral disease observed in the studied group of young men. Inadequate nutritional status of vitamin D together with certain dietary factors may contribute, at least in part, to the high cariogenic activity, one of the main risk factors of tooth loss. The findings of the present report underscore the necessity for several nutritional strategies to prevent caries development, and consequently tooth loss. Nevertheless, other additional factors must be considered in the prevention of dental diseases. In this regard, improving dental hygiene by encouraging tooth-brushing with fluoride-containing toothpaste is also an important tool to ensure caries prevention. These strategies would improve the quality of life by preserving the natural dentition and by preventing the development of bone pathologies

Acknowledgment

This paper was part of Olga Antonenko´s Doctoral thesis presented at the School of Dentistry, Buenos Aires University, in partial fulfillment of the PhD, degree requirements. The authors thank ISALUD University for allowing them to carry out this investigation, and Miss Julia Somoza for her technical assistance. This study was performed with the support of the Buenos Aires University grant UBACYT CO21 N° 20020100100320 and the CONICET.

References

1. Abrams SA. Normal acquisition and loss of bone mass. Horm Res. 2003; 60: 71-76.
2. Adegboye AR, Christensen LB, Holm-Pedersen P, Avlund K, Boucher BJ, Heitmann BL. Intakes of calcium, vitamin D, and dairy servings and dental plaque in older Danish adults. Nutr J. 2013; 12: 61.
3. Adegboye AR, Fiehn NE, Twetman S, Christensen LB, Heitmann BL. Low calcium intake is related to increased risk of tooth loss in men. J Nutr. 2010; 140: 1864-1868.
4. Ritchie CS, Joshipura K, Hung HC, Douglass CW. Nutrition as a mediator in the relation between oral and systemic disease: associations between specific measures of adult oral health and nutrition outcomes. Critical reviews in oral biology and medicine. Crit Rev Oral Biol Med. 2002; 13: 291-300.
5. Touger-Decker R, Mobley C. Position of the Academy of Nutrition and Dietetics: oral health and nutrition. J Acad Nutr Diet. 2013; 113: 693-701.
6. Adegboye AR, Twetman S, Christensen LB, Heitmann BL. Intake of dairy calcium and tooth loss among adult Danish men and women. Nutrition. 2012; 28: 779-784.
7. Benguigui C, Bongard V, Ruidavets JB, Sixou M, Chamontin B, Ferrieres J, et al. Evaluation of oral health related to body mass index. Oral Dis. 2012; 18: 748-755.
8. Kashket S, DePaola DP. Cheese consumption and the development and progression of dental caries. Nutri Rev. 2002; 60: 97-103.
9. Krall EA, Wehler C, Garcia RI, Harris SS, Dawson-Hughes B. Calcium and vitamin D supplements reduce tooth loss in the elderly. Am J Med. 2001; 111: 452-456.
10. Zanetti M, Harris SS, Dawson-Hughes B. Ability of vitamin D to reduce inflammation in adults without acute illness. Nutr Rev. 2014; 72: 95-98.
11. Holick MF. Vitamin D and bone health. J Nutr. 1996; 126: 1159S-64S.
12. Argentina MdSdlN. Encuesta Nacional de Nutrición y Salud –ENNyS–2005. Documento de resultados. Ministerio de Salud de la Nación. 2007.
13. Pellegrini GG, Gonzales Chaves MM, Fajardo MA, Ponce GM, Toyos GI, Lifshitz F, et al. Salivary bone turnover markers in healthy pre- and postmenopausal women: daily and seasonal rhythm. Clin Oral Investig. 2012; 16: 651-657.
14. Forshee RA, Storey ML. Total beverage consumption and beverage choices among children and adolescents. Int J Food Sci Nutr. 2003; 54: 297-307.
15. Ha EJ, Caine-Bish N, Holloman C, Lowry-Gordon K. Evaluation of effectiveness of class-based nutrition intervention on changes in soft drink and milk consumption among young adults. J Nutr. 2009; 8: 50.
16. Moynihan PJ. The role of diet and nutrition in the etiology and prevention of oral diseases. Bulletin of the World Health Organization. 2005; 83: 694-699.
17. Hanioka T, Ojima M, Tanaka K, Matsuo K, Sato F, Tanaka H. Causal assessment of smoking and tooth loss: a systematic review of observational studies. BMC Public Health. 2011; 11: 221.
18. Christensen LB, Petersen PE, Krustrup U, Kjoller M. Self-reported oral hygiene practices among adults in Denmark. Community Dent Health. 2003; 20: 229-235.
19. World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. The Journal of the American College of Dentists. 2014; 81: 14-18.
20. Ware J, Snoww K, Ma K, Bg G. SF36 Health Survey: Manual and Interpretation Guide. 1993.
21. Ware J. SF-36 Health Survey update. 2001. 3130-3139.
22. World, Health, Organization. Global Database on Body Mass Index. 2004.
23. Ross AC, Taylor CL, Yaktine AL, Del Valle HB. Dietary Reference Intakes for Calcium and Vitamin D. Washington DC: National Academy of Sciences. 2011.
24. Grant WB, B.J. B. Low vitamin D status likely contributes to the link between periodontal disease and breast cancer. Breast Cancer Res Treat. 2011; 128: 907.
25. PE P. Continuous improvement of oral health in the 21st century – the approach of the WHO Global Oral Health Programme. Geneva, Switzerland. The World Oral Health Report. 2003.
26. Bratthall D. Introducing the Significant Caries Index together with a proposal for a new global oral health goal for 12-year-olds. Int Dent J. 2000; 50: 378- 384.
27. Silness J, Loe H. Periodontal disease in pregnancy II. Correlation between oral hygiene and periodontal condition. Acta odontologica Scandinavica. 1964; 22: 121-135.
28. Moynihan P, Petersen PE. Diet, nutrition and the prevention of dental diseases. Public Health Nutrition. 2004; 7: 201-226.
29. Dye BA, Tan S, Smith V, Lewis BG, Barker LK, Thornton-Evans G, et al. Trends in oral health status: United States, 1988-1994 and 1999-2004. National Center for Health Statistics Vital Health Stat. 2007; 11.
30. Carmuega E, Rovirosa A, ME Z. La población argentina necesita consumir más calcio. El calcio de los lácteos se aprovecha mejor. Sitio Argentino de Producción Animal: Centro de Estudios sobre Nutrición Infantil (CESNI). 2013.
31. Danielsson Niemi L, Hernell O, Johansson I. Human milk compounds inhibiting adhesion of mutans streptococci to host ligand-coated hydroxyapatite in vitro. Caries Research. 2009; 43: 171-178.
32. Paes Leme AF, Koo H, Bellato CM, Bedi G, Cury JA. The role of sucrose in cariogenic dental biofilm formation--new insight. J Dent Research. 2006; 85: 878-887.
33. Ferrazzano GF, Cantile T, Quarto M, Ingenito A, Chianese L, Addeo F. Protective effect of yogurt extract on dental enamel demineralization in vitro. Australian Dental J. 2008; 53: 314-319.
34. Moynihan PJ. Dietary advice in dental practice. Br Dent J. 2002; 193: 563- 568.
35. Stewart S, Hanning R. Building osteoporosis prevention into dental practice. J Can Dent Assoc. 2012; 78: c29.
36. Rodrigues HL Jr., Scelza MF, Boaventura GT, Custodio SM, Moreira EA, Oliveira Dde L. Relation between oral health and nutritional condition in the elderly. J Appl Oral Sci. 2012; 20: 38-44.
37. Rodriguez-Rodriguez E, Navia Lomban B, Lopez-Sobaler AM, Ortega Anta RM. Review and future perspectives on recommended calcium intake. Nutricion Hospitalaria. 2010; 25: 366-374.