| |
|
|
| Year : 2013 | Volume
: 24
| Issue : 4 | Page : 468-473 |
|
| Evaluation of micronutrient (zinc, copper and iron) levels in periodontitis patients with and without diabetes mellitus type 2: A biochemical study |
|
|
Biju Thomas1, Anshuman Gautam1, B Rajendra Prasad2, Suchetha Kumari3
1 Department of Periodontics, A.B. Shetty Memorial Institute of Dental Sciences, Mangalore, India
2 Department of Oral and Maxillofacial Surgery, A.B. Shetty Memorial Institute of Dental Sciences, Mangalore, India
3 Department of Biochemistry, K.S. Hegde Medical Academy, Karnataka, India
Click here for correspondence address and email
| Date of Submission | 23-Nov-2012 |
| Date of Decision | 31-Mar-2013 |
| Date of Acceptance | 25-Mar-2013 |
| Date of Web Publication | 19-Sep-2013 |
|
|
 |
|
 Abstract | | |
Context: Periodontal tissue destruction is caused by an inappropriate host response to microorganisms. Diabetes is a metabolic disease and most of its complications are due to hyperglycemia. Periodontitis is considered as its sixth complication. Micronutrients such as zinc, copper and iron are essential for human health. There is accumulating evidence that the metabolism of several trace elements is altered in diabetes mellitus and that these nutrients might have specific roles in the pathogenesis and progress of this disease and its complication. An association between micronutrients and periodontitis has also been suggested by preliminary studies. However, till date there is a lack of relevant clinical data.
Aim: This study was designed to estimate and compare the serum levels of zinc, copper and iron in diabetes mellitus type 2 patients and healthy individuals with and without periodontitis.
Setting and Design: Single centre case-control study.
Subjects and Materials: This study included 150 subjects, 50 in each group. Group 1 comprised of 50 subject with diabetes mellitus type 2 and periodontitis. Group 2 comprised of 50 subjects with chronic periodontitis and Group 3 comprised of 50 control subjects. Atomic absorption spectrophotometry method was used to measure clinical level of zinc and copper in serum. Estimation of serum iron levels was done by bathophenanthroline method.
Statistical analysis: The results obtained were tabulated and subjected to statistical analysis by analysis of variance and Tukey multiple comparison tests using statistical software SPSS version 17.
Results: The results showed that the serum levels of zinc decreased and serum levels of iron and copper increased in diabetes patients with periodontitis compared to healthy individuals with and without periodontitis.
Conclusion: Imbalance of Zinc, copper and iron levels in the serum can predispose an individual to the risk of developing periodontitis. Keywords: Copper, diabetes mellitus type 2, iron, periodontitis, zinc
How to cite this article:
Thomas B, Gautam A, Prasad B R, Kumari S. Evaluation of micronutrient (zinc, copper and iron) levels in periodontitis patients with and without diabetes mellitus type 2: A biochemical study. Indian J Dent Res 2013;24:468-73 |
How to cite this URL:
Thomas B, Gautam A, Prasad B R, Kumari S. Evaluation of micronutrient (zinc, copper and iron) levels in periodontitis patients with and without diabetes mellitus type 2: A biochemical study. Indian J Dent Res [serial online] 2013 [cited 2023 Jun 1];24:468-73. Available from: https://www.ijdr.in/text.asp?2013/24/4/468/118400 |
Periodontitis is an immuno-inflammatory disease of the periodontal tissue characterized by destruction of bone and connective tissue attachment. It is a multifactorial disease modified by numerous risk factors, which include diabetes, smoking, host response, diet. [1] It is now accepted that though periodontitis is initiated by microbes, most of the periodontal tissue destruction is caused by an inappropriate host response (inflammatory and immune response) to those microorganisms. Loss of homeostasis between protective and destructive factors determines the host response and thus, eventually the extent of periodontal damage. [2]
Diabetes mellitus is a clinically and genetically heterogeneous group of metabolic disorders manifested by abnormally high levels of glucose in the blood. The hyperglycemia is the result of a deficiency of insulin secretion caused by pancreatic β-cell dysfunction or of resistance to the action of insulin in the liver and muscle, or a combination of these. [3]
The more prevalent form of diabetes is diabetes mellitus type-2 also referred to as non-insulin dependent diabetes mellitus, a condition which often develops over a period of time, involves reduced responsiveness of tissues to circulating insulin, and is often controlled by diet or oral hypoglycemic drugs. This condition is characterized by hyperglycemia, hyperlipidemia, and associated complications. [4],[5] The American Dental Association has recognised periodontitis as its sixth complication. [6]
Nutrition has significant effects on the inflammatory processes as well as the cellular and humoral immune mechanism. The interaction between nutritional status and the immune response to the bacterial challenge can be an underlying factor in the progression of periodontal disease. [7] Nutrition also plays an important role in wound healing. [8] A periodontal lesion is essentially a wound, and adequate nutrition must be available for optimal healing to take place. [9]
The daily diet consists of both macronutrients and micronutrients. The micronutrients are required in milligram (mg) to microgram (μg) quantity and include vitamins and minerals. Recommended daily allowance of micronutrient such as iron, copper, and zinc is less than 100 μg. These micronutrients have diverse metabolic characteristics and functions and are essential for human health. They are also necessary for functioning of many enzyme systems like deoxyribonucleic acid (DNA) polymerase, ribonucleic acid (RNA) polymerase, superoxide dismutase, catalases, alkaline phosphatase. [10] However, the exact mechanism by which micronutrients modify periodontal destruction has not been precisely understood.
Several studies suggest that diabetes mellitus can disrupt the homeostasis of several trace elements. Conversely, research also suggests that imbalances of specific elements may play an important role in the pathogenesis of diabetes and its various complications. [11]
However, there are only a few studies that have evaluated the possible relationship between micronutrients and periodontitis. Hence this study was designed to estimate and compare the serum levels of zinc, copper and iron in diabetes mellitus type 2 patients and healthy individuals with and without periodontitis.
| Subjects and Methods | |  |
The study was a case control study comprising of 150 subjects, 50 in each group.
- Group 1: 50 subjects with type 2 diabetes mellitus and chronic periodontitis
- Group 2: 50 subjects who were systemically healthy with chronic periodontitis
- Group 3: 50 subjects who were systemically healthy and without chronic periodontitis.
The subjects were selected from the Department of Periodontics, A.B. Shetty Memorial Institute of Dental Sciences and Department of Medicine, K.S. Hegde Medical Academy, Mangalore. A written informed consent was taken from each subject. The ethical clearance was obtained from ethical board of NITTE University. The study was conducted from December 2010 to June 2012.
Subjects aged from 35 years to 60 years of both sexes were included in the study.
Criteria for subject selection are as follows:
Inclusion criteria
- Patients categorized as type 2 diabetes mellitus who are under treatment for atleast 6 months and are on oral hypoglycaemic drugs, in the age group of 35-60 years
- Patients with clinical attachment loss ≥ 4 mm in more than 30% of the sites for Group 1 and 2
- Subjects who have a gingival index score of less than 2 in Group 3
- Subjects with minimum complement of 20 teeth
Exclusion criteria
- History of any antibiotic/anti-inflammatory therapy for 3 months prior to study
- History of any systemic diseases for Group 2 and 3
- History of any systemic disease other than diabetes mellitus type 2 for the Group 1
- Pregnancy/lactation
- Subjects with a history of smoking and any form of tobacco consumption
- Subjects with a history of use of mouth wash within 3 months prior to study
- Subjects with a history of vitamins/minerals or antioxidant supplements intake during the last 3 months
- Subjects who had undergone any periodontal treatment for at least 3 months prior to study.
Screening examination
- Medical history and dental history
- Probing depth and loss of attachment using William's periodontal probe [Figure 1]
- Gingival index (Loe and Silness)
- History of use of vitamins/minerals or antioxidants.
All measurements and readings were taken before the collection of the blood sample. The samples were coded before being sent for laboratory investigations.
Evaluation of zinc, copper and iron:
5 ml of venous blood sample was drawn from the subject through a disposable syringe and transferred to a centrifuge tube [Figure 2]. The sample was centrifuged at 3000 rpm for 15 min and the supernatant serum was collected [Figure 3]. Then digestion of the serum was done. Atomic abosorption spectrophotometry method was used to measure clinical levels of zinc and copper in serum [Figure 4]. Estimation of serum iron levels was done by bathophenanthroline method.
Statistical analysis
The results obtained were tabulated and subjected to statistical analysis by one way analysis of variance (ANOVA) using statistical software SPSS version 17. The data were expressed as mean and standard deviation. Inter group comparison was done using Tukey test for multiple comparison. P values were considered to be statistically significant (P < 0.0005).
| Results | | |
The study was designed as a case control study.
- Group 1: 50 subjects with type 2 diabetes mellitus and chronic periodontitis
- Group 2: 50 subjects who were systemically healthy with chronic periodontitis
- Group 3: 50 subjects who were systemically healthy and without chronic periodontitis
[Table 1] and [Figure 5] shows and compares the mean and standard deviation of serum zinc levels in the three groups. The serum levels of zinc in Group 1 Shows a mean and standard deviation of 38.75 ± 8.482 when compared to Group 2 and 3, which shows a mean and standard deviation of 68.96 ± 7.267 and 74.71 ± 8.280 respectively. The result of one way ANOVA showed high statistical significance (P < 0.0005) between Group 1 and Group 2, between Group 2 and Group 3 and between Group 1 and Group 3. | Figure 5: Zinc -Group 1: Diabetic patients with chronic periodontitis. Group 2: Systemically healthy individuals with chronic periodontitis. Group 3: Systemically healthy individuals without chronic periodontitis
Click here to view |
 | Table 1: Mean and standard deviation of serum zinc levels in the three groups
Click here to view |
The Tukey test of significance showed highly statistically significant difference (P < 0.0005) between Group 1 and Group 3, between Group 1 and Group 2 and statistically significant difference (P < 0.018) between Group 2 and Group 3 as depicted by [Table 2].
[Table 3] and [Figure 6] shows and compares the mean and standard deviation of serum Copper levels in the three group. The serum levels of Copper in Group 1 shows a mean and standard deviation of 128.94 ± 6.458 when compared to Group 2 and 3 which shows a mean and standard deviation of 88.64 ± 18.408 and 76.68 ± 4.893 respectively. The result of one way ANOVA showed high statistical significance (P < 0.0005) between Group 1 and Group 2, between Group 2 and Group 3 and between Group 1 and Group 3. | Figure 6: Copper -Group 1: Diabetic patients with chronic periodontitis. Group 2: Systemically healthy individuals with chronic periodontitis. Group 3: Systemically healthy individuals without chronic periodontitis
Click here to view |
 | Table 3: Mean and standard deviation of serum copper levels in the three groups
Click here to view |
Tukey test of significance showed highly statistically significant difference (P < 0.0005) between Group 1 and Group 3, between Group 1 and Group 2 and between Group 2 and Group 3 as depicted in [Table 4].
[Table 5] and [Figure 7] shows and compares the mean and standard deviation of serum Iron levels. The serum levels of Iron in Group 1 shows a mean of 165.45 ± 14.612 when compared to Group 2 and 3 which shows a mean of 141.69 ± 24.412 and 130.67 ± 21.863 respectively. The result of one way ANOVA showed high statistical significance (P < 0.0005) between Group 1 and Group 2, between Group 2 and Group 3 and between Group 1 and Group 3. | Figure 7: Iron -Group 1: Diabetic patients with chronic periodontitis. Group 2: Systemically healthy individuals with chronic periodontitis. Group 3: Systemically healthy individuals without chronic periodontitis
Click here to view |
 | Table 5: Mean and standard deviation of serum iron levels in the three groups
Click here to view |
Tukey test of significance showed highly statistically significant difference (P < 0.0005) between Group 1 and Group 2 and between Group 1 and Group 3. The difference between Group 2 and Group 3 was not significant as depicted in [Table 6].
| Discussion | | |
Micronutrients like zinc, copper and iron play an essential role in regeneration, for coping with oxidative stress and for an adequate immune response. Hence, these elements are essential for maintaining health throughout life. Micronutrients can cause diseases through deficiency, imbalance, or toxicity. Studies have shown that elevated copper and iron levels and decreased zinc levels may be a contributing factor in many inflammatory conditions. [12]
The results of the study demonstrated lower levels of zinc and higher levels of copper and iron in the serum of individuals with periodontitis compared to the control group without periodontitis. The difference is found to be statistically significant for serum zinc and copper levels.
Frithiof et al. and Tulin et al. in separate studies found decreased serum zinc levels in individuals with periodontitis when compared to healthy controls. [13],[14] In contrast, Freeland et al. found no difference. [15] Frinthof et al. also showed an inverse relation between serum zinc levels and alveolar bone loss. This could be explained on the basis that zinc is an essential cofactor in enzymes like DNA polymerase and RNA polymerase and thus essential for DNA synthesis, protein synthesis, and cellular proliferation. Zinc deficiency has been shown to reduce osteoblastic activity, collagen and proteoglycan synthesis as well as alkaline phosphatase activity. [16] Hence, deficiency in zinc could impair regenerative capacity. Along with this, zinc deficiency also impairs both innate and acquired immunity (e.g., downregulation of phagocytosis by macrophages and neutrophils, natural killer cell activity, generation of oxidative burst, antibody responses, and the numbers of cytotoxic T cells). [17] Zinc deficiency also leads to altered metabolism of androgens, oestrogens and progesterone which impairs immunity indirectly. [18]
Zinc has antioxidant properties as it stabilizes the cell membrane structure, contributing, to the structure of the superoxide dismutase and maintaining the metallothionein tissue concentrations. Hence long term deficiency of zinc can promote tissue injury due to oxidative stress. [18]
Thus, it can be suggested that inadequate intake of zinc may lead to suppressed immunity along with increased oxidative stress and poor regenerative capacity in an individual, which can predispose to periodontitis.
The present study showed an increase in serum copper levels in individuals with periodontitis when compared with healthy individuals. A study by Freeland et al. also showed increased serum copper levels in individuals with periodontitis. [15] Turnlund and associates reported that increased serum Copper can modulate immune function and antioxidant status. Studies on animal models have shown that increased serum copper levels reduce several aspects of immune response, including neutrophil numbers, lymphocyte proliferation, and antigen-specific antibody production. [19] It has also been reported that elevated serum copper levels alter collagen metabolism and hence can promote periodontitis. [20]
On the other hand, inflammation is also believed to increase the copper levels. Pekarek et al. have suggested that hepatic copper primarily as ceruloplasmin can get mobilized as a feedback signal by leukocyte endogenous mediators. [21] However, it is beyond the scope of the present study to suggest whether, elevated levels of copper can be a risk factor for periodontitis or that the elevated levels of copper is caused by inflammatory conditions like periodontitis.
The results of the present study showed an increase in iron levels in an individual with periodontitis compared to control group without periodontitis, but the difference is not statistically significant. A recent study by Prakash et al. also found no significant difference between periodontitis patients and healthy controls. [22]
The other objective of the present study was to evaluate the serum zinc, copper and iron levels in diabetes mellitus type 2 patients with periodontitis. The result of the study demonstrated lower levels of zinc and increased levels of copper and iron in diabetes mellitus type 2 patients with periodontitis when compared to healthy individuals with and without periodontitis and the difference is statistically significant. The result correlates with a recent study by Thomas et al. [23]
Both animal and human studies have suggested a possible role of altered micronutrient status in the pathogenesis of diabetes mellitus type 2 and its complication.
Chung et al. in their study have suggested that diabetes mellitus is associated with increased urinary excretion of zinc leading to its lower levels in serum. Intestinal absorption of zinc is also decreased in this condition. [24] Lowered serum levels in turn can depress immune response and promote free-radical activity.
Excessive copper and iron in serum may promote development and progression of oxidative stress, altered immunity and altered insulin secretion or its action. [11]
An abundance of information accumulated from studies on the complication of diabetes and periodontal disease have revealed that altered immune response may be antecedent of both diseases, which may have a synergistic effect when they coexist in the host. Zinc deficiencies and elevated levels of copper and iron are associated with an increased oxidative stress along with an altered immune response which could lead to various diabetes complications including periodontitis.
The present study may have important therapeutic implications in terms of the use of micronutrient supplements in periodontal therapy to prevent tissue destruction. An interventional study on rat has shown that a topical administration of zinc ion containing compound either as a mouthwash or toothpaste can reduce loss of alveolar bone. [25] However, interventional trials done on humans are required to determine the exact therapeutic success.
This study is limited primarily by its cross sectional design, which prevents the establishment of a temporal relationship between micronutrients and periodontitis. Another limitation is that serum concentrations are perhaps not the best index of micronutrient levels in periodontal tissues.
More longitudinal studies with a larger sample size should be carried out to have a better understanding of the inter-relationship between micronutrient imbalance and chronic disease processes like periodontitis and diabetes. Further studies should also be carried out to evaluate the serum levels of micronutrients before and after periodontal therapy to arrive to a more conclusive result.
| Conclusion | | |
In the last decades, the impact of micronutrients on human physiology has begun to be elucidated. Imbalance of zinc, copper and iron levels in the serum can predispose an individual to the risk of developing periodontitis due to decreased regenerative capacity and impaired immune function along with development of excessive oxidative stress.
| References | | |
| 1. | Van Dyke TE, Sheilesh D. Risk factors for periodontitis. J Int Acad Periodontol 2005;7:3-7. 
[PUBMED] |
| 2. | Van Dyke TE, Lester MA, Shapira L. The role of the host response in periodontal disease progression: Implications for future treatment strategies. J Periodontol 1993;64:792-806.
[PUBMED] |
| 3. | Mealey BL, Oates TW, American Academy of Periodontology. Diabetes mellitus and periodontal diseases. J Periodontol 2006;77:1289-303.
|
| 4. | Bjelland S, Bray P, Gupta N, Hirscht R. Dentists, diabetes and periodontitis. Aust Dent J 2002;47:202-7.
[PUBMED] |
| 5. | Cowie CC, Eberhardt MS. American diabetes associatation vital statistics. Am Diabetes Assoc 1996;42:13-20.
|
| 6. | Löe H. Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care 1993;16:329-34.
|
| 7. | Nishida M, Grossi SG, Dunford RG, Ho AW, Trevisan M, Genco RJ. Dietary vitamin C and the risk for periodontal disease. J Periodontol 2000;71:1215-23.
[PUBMED] |
| 8. | DePaola DP, Faine MP, Palmer C. Nutrition in relation to dental medicine. In: Modern Nutrition in Health and Disease. 9 th ed. Philadelphia: Williams & Wilkins; 1999.
|
| 9. | Schifferle RE. Periodontal disease and nutrition: Separating the evidence from current fads. Periodontol 2000 2009;50:78-89.
|
| 10. | Nizel AE, Papas AS. Nutrition in Clinical Dentistry. 3 rd ed. Philadelphia: Saunders; 1989.
|
| 11. | Kazi TG, Afridi HI, Kazi N, Jamali MK, Arain MB, Jalbani N, et al. Copper, chromium, manganese, iron, nickel, and zinc levels in biological samples of diabetes mellitus patients. Biol Trace Elem Res 2008;122:1-18.
|
| 12. | Mujico JR, Pérez-de-Heredia F, Gómez-Martínez S, Marcos A. Malnutrition and Inflammation, Inflammation, Chronic Diseases and Cancer - Cell and Molecular Biology, Immunology and Clinical Bases. InTech; 2012.
|
| 13. | Frithiof L, Lavstedt S, Eklund G, Söderberg U, Skårberg KO, Blomqvist J, et al. The relationship between marginal bone loss and serum zinc levels. Acta Med Scand 1980;207:67-70.
|
| 14. | Kuraner T, Beksac MS, Kayakirilmaz K, Caðlayan F, Onderoðlu LS, Ozgünes H. Serum and parotid saliva testosterone, calcium, magnesium, and zinc levels in males, with and without periodontitis. Biol Trace Elem Res 1991;31:43-9.
|
| 15. | Freeland JH, Cousins RJ, Schwartz R. Relationship of mineral status and intake to periodontal disease. Am J Clin Nutr 1976;29:745-9.
|
| 16. | Starcher BC, Hill CH, Madaras JG. Effect of zinc deficiency on bone collagenase and collagen turnover. J Nutr 1980;110:2095-102.
|
| 17. | Prasad AS, Beck FW, Snell DC, Kucuk O. Zinc in cancer prevention. Nutr Cancer 2009;61:879-87.
|
| 18. | Tapiero H, Tew KD. Trace elements in human physiology and pathology: Zinc and metallothioneins. Biomed Pharmacother 2003;57:399-411.
|
| 19. | Turnlund JR. Human whole-body copper metabolism. Am J Clin Nutr 1998;67:960-4.
|
| 20. | Burch RE, Hahn HK, Sullivan JF. Newer aspects of the roles of zinc, manganese, and copper in human nutrition. Clin Chem 1975;21:501-20.
|
| 21. | Pekarek RS, Wannemacher RW Jr, Beisel WR. The effect of leukocytic endogenous mediator (LEM) on the tissue distribution of zinc and iron. Proc Soc Exp Biol Med 1972;140:685-8.
|
| 22. | Prakash S, Dhingra K, Priya S. Similar hematological and biochemical parameters among periodontitis and control group subjects. Eur J Dent 2012;6:287-94.
|
| 23. | Thomas B, Kumari S, Ramitha K, Ashwini Kumari MB. Comparative evaluation of micronutrient status in the serum of diabetes mellitus patients and healthy individuals with periodontitis. J Indian Soc Periodontol 2010;14:46-9.
[PUBMED]  |
| 24. | Chung JS, Franco RJ, Curi PR. Renal excretion of zinc in normal individuals during zinc tolerance test and glucose tolerance test. Trace Elem Electrolytes 1995;12:62-7.
|
| 25. | Hughes BD. Use of zinc ion in the treatment of periodontitis. European Patent 1992. (EP no. 0508524)
|
Correspondence Address:
Anshuman Gautam
Department of Periodontics, A.B. Shetty Memorial Institute of Dental Sciences, Mangalore
India
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/0970-9290.118400
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6] |
|
| This article has been cited by | | 1 |
Advances of nanoparticles employment in dental implant applications |
|
| Nayem Hossain, Mohammad Aminul Islam, Mohammad Asaduzzaman Chowdhury, Ashraful Alam | | Applied Surface Science Advances. 2022; 12: 100341 | | [Pubmed] | [DOI] | | | 2 |
Application of Copper Nanoparticles in Dentistry |
|
| Veena Wenqing Xu, Mohammed Zahedul Islam Nizami, Iris Xiaoxue Yin, Ollie Yiru Yu, Christie Ying Kei Lung, Chun Hung Chu | | Nanomaterials. 2022; 12(5): 805 | | [Pubmed] | [DOI] | | | 3 |
ROLE OF ZINC IN PERIODONTAL HEALTH AND DISEASE |
|
| Vishakha Gupta, Pavitra Rastogi, Sadhna Ajay, Rameshwari Singhal | | INTERNATIONAL JOURNAL OF SCIENTIFIC RESEARCH. 2022; : 51 | | [Pubmed] | [DOI] | | | 4 |
Periodontitis and circulating blood cell profiles: a systematic review and meta-analysis |
|
| João Botelho, Vanessa Machado, Syed Basit Hussain, Syeda Ambreen Zehra, Luís Proença, Marco Orlandi, José João Mendes, Francesco D'Aiuto | | Experimental Hematology. 2021; 93: 1 | | [Pubmed] | [DOI] | | | 5 |
Efficacy of Curcumin Gel on Zinc, Magnesium, Copper, IL-1ß, and TNF-a in Chronic Periodontitis Patients |
|
| Chenar Anwar Mohammad, Vincenzo Iorio Siciliano | | BioMed Research International. 2020; 2020: 1 | | [Pubmed] | [DOI] | | | 6 |
Decreased Hemoglobin Concentration and Iron Metabolism Disorder in Periodontitis: Systematic Review and Meta-Analysis |
|
| Donglei Wu, Zhengshen Lin, Shiwei Zhang, Fengdi Cao, Defeng Liang, Xincai Zhou | | Frontiers in Physiology. 2020; 10 | | [Pubmed] | [DOI] | | | 7 |
ICP-Mass-Spectrometry Ionic Profile of Whole Saliva in Patients with Untreated and Treated Periodontitis |
|
| Federica Romano, Alexandra Castiblanco, Francesca Spadotto, Federica Di Scipio, Mery Malandrino, Giovanni Nicolao Berta, Mario Aimetti | | Biomedicines. 2020; 8(9): 354 | | [Pubmed] | [DOI] | | | 8 |
Improved General and Oral Health in Diabetic Patients by an Okinawan-Based Nordic Diet: A Pilot Study |
|
| Helene Holmer,Cecilia Widén,Viveca Wallin Bengtsson,Michael Coleman,Björn Wohlfart,Stig Steen,Rutger Persson,Klas Sjöberg | | International Journal of Molecular Sciences. 2018; 19(7): 1949 | | [Pubmed] | [DOI] | | | 9 |
Improved General and Oral Health in Diabetic Patients by an Okinawan-Based Nordic Diet: A Pilot Study |
|
| Helene Holmer,Cecilia Widén,Viveca Wallin Bengtsson,Michael Coleman,Björn Wohlfart,Stig Steen,Rutger Persson,Klas Sjöberg | | International Journal of Molecular Sciences. 2018; 19(7): 1949 | | [Pubmed] | [DOI] | | | 10 |
Effect of micronutrient malnutrition on periodontal disease and periodontal therapy |
|
| Henrik Dommisch,Denica Kuzmanova,Daniel Jönsson,Melissa Grant,Iain Chapple | | Periodontology 2000. 2018; 78(1): 129 | | [Pubmed] | [DOI] | | | 11 |
Effect of micronutrient malnutrition on periodontal disease and periodontal therapy |
|
| Henrik Dommisch,Denica Kuzmanova,Daniel Jönsson,Melissa Grant,Iain Chapple | | Periodontology 2000. 2018; 78(1): 129 | | [Pubmed] | [DOI] | | | 12 |
Trace Mineral Micronutrients and Chronic Periodontitis—a Review |
|
| Sumit Gaur,Rupali Agnihotri | | Biological Trace Element Research. 2017; 176(2): 225 | | [Pubmed] | [DOI] | | | 13 |
Trace Mineral Micronutrients and Chronic Periodontitis—a Review |
|
| Sumit Gaur,Rupali Agnihotri | | Biological Trace Element Research. 2017; 176(2): 225 | | [Pubmed] | [DOI] | | | 14 |
Copper in Diabetes Mellitus: a Meta-Analysis and Systematic Review of Plasma and Serum Studies |
|
| Qihong Qiu,Fuping Zhang,Wenjun Zhu,Juan Wu,Min Liang | | Biological Trace Element Research. 2017; 177(1): 53 | | [Pubmed] | [DOI] | | | 15 |
Copper in Diabetes Mellitus: a Meta-Analysis and Systematic Review of Plasma and Serum Studies |
|
| Qihong Qiu,Fuping Zhang,Wenjun Zhu,Juan Wu,Min Liang | | Biological Trace Element Research. 2017; 177(1): 53 | | [Pubmed] | [DOI] | | | 16 |
Associating Serum Iron and Magnesium Levels in Hypertensive and Chronic Periodontitis Patients: Do They have a Link? |
|
| Arati C Koregol, TJ Jerin Mary, Shivaraj Warad, Tejaswini Annam, Nitesh Kataria, Nagaraj B Kalburgi | | Journal of Health Sciences & Research. 2017; 8(2): 61 | | [Pubmed] | [DOI] | | | 17 |
Rapid assessment of iron in blood plasma and serum by spectrophotometry with cloud-point extraction |
|
| Tatyana Samarina,Mikhail Proskurnin | | F1000Research. 2015; 4: 623 | | [Pubmed] | [DOI] | | | 18 |
Rapid assessment of iron in blood plasma and serum by spectrophotometry with cloud-point extraction |
|
| Tatyana Samarina,Mikhail Proskurnin | | F1000Research. 2015; 4: 623 | | [Pubmed] | [DOI] | |
|
|
|
|
|
|
|
|
|
|
|
|
| Article Access Statistics | | | Viewed | 10931 | | | Printed | 516 | | | Emailed | 4 | | | PDF Downloaded | 405 | | | Comments | [Add] | | | Cited by others | 18 | | |
|
|
Users online:
