JCDR - Register at Journal of Clinical and Diagnostic Research
Journal of Clinical and Diagnostic Research, ISSN - 0973 - 709X
Dentistry Section DOI : 10.7860/JCDR/2016/16310.7351
Year : 2016 | Month : Mar | Volume : 10 | Issue : 03 Full Version Page : ZC12 - ZC14

Correlation of Salivary pH, Incidence of Dental Caries and Periodontal Status in Diabetes Mellitus Patients: A Cross-sectional Study

C. Seethalakshmi1, R.C. Jagat Reddy2, Nisha Asifa3, S. Prabhu4

1 Senior Lecturer, Department of Oral Medicine and Radiology, Chettinad Dental College and Research Institute, Kelambakkam, Chennai, India.
2 Professor and Head, Department of Oral Medicine and Radiology, Chettinad Dental College and Research Institute, Kelambakkam, Chennai, India.
3 CRRI, Chettinad Dental College and Research Institute, Kelambakkam, Chennai, India.
4 Senior Lecturer, Department of Public Health Dentistry, Chettinad Dental College and Research Institute, Kelambakkam, Chennai, India.


NAME, ADDRESS, E-MAIL ID OF THE CORRESPONDING AUTHOR: Dr. C. Seethalakshmi, 7F2-Amber Block, Olympia Opaline, Navallur, OMR, Chennai-603103, India.
E-mail: seethamds@gmail.com
Abstract

Introduction

Diabetes mellitus is a chronic disease affecting many parts of the body. A number of oral diseases have been associated with diabetes mellitus with an increased risk of dental caries and periodontal disease.

Aim

The aim of the study was to evaluate the salivary pH and incidence of dental caries and periodontal status in diabetes mellitus compared to that of the normal subjects.

Materials and Methods

The study population consisted of 40 patients divided into 2 groups with group I comprising of 20 known diabetes mellitus patients and group II comprising of 20 non diabetic subjects as control group. The pH of the saliva was determined using a digital pH meter. Dental caries and periodontal status were assessed by DMFT and PDI indices respectively.

Results

There was a decrease in the mean salivary pH of 6.51 in the study group, compared to the normal mean salivary pH of 7.88 in the control group. The mean DMFT index was higher in the study group (8.10) when compared to that of control group (1.15). The mean PDI score was also higher in the study group (4.0) as compared to that of the control group (0.45).

Conclusion

The results of the present study concluded that there was a significant relationship between the diabetes mellitus and increased incidence of dental caries and periodontitis and there was also a significant reduction in the salivary pH in diabetes mellitus patients, compared to that of non diabetic subjects.

Keywords

Introduction

Diabetes mellitus is a global health challenge faced by the world today. India ranks second with 66.8 million people with diabetes in 2014 following China which ranks first with 96.2 million diabetics. International Diabetes Federation estimates that currently, more than 387 million people worldwide have diabetes and it is estimated to increase to 592 million by 2035 [1]. It is a common chronic metabolic disease with various oral consequences. Diabetes mellitus manifests in altering the salivary composition and its functions. Change in oral environment initiates pathogenic bacteria, damaging hard and soft tissues of the oral cavity leading to an increased cariogenic activity and periodontal lesions. Since, saliva provides a protective effect; there can be development of dental caries when there is clinically significant decrease in salivary functions [2].

Alterations in pH of saliva are often reported in diabetes mellitus patients. There is often a correlation between pH changes in plaque and sugar clearance from saliva [3]. The low salivary pH provides an acidogenic environment for the growth of aciduric bacteria leading to dental caries which again further lowers the salivary pH leading to a vicious cycle. Diabetes promotes periodontitis through an exaggerated inflammatory response to the periodontal microflora [4].

Aim

The aim of this study was to evaluate pH of saliva in diabetes mellitus patients and to compare with that of normal subjects and also to evaluate the caries incidence and periodontal status of the diabetes mellitus patients and compare it with normal subjects.

Materials and Methods

A cross-sectional study was conducted in the Department of Oral Medicine and Radiology, Chettinad Dental College and Research Institute where a total of 40 subjects were included after taking the institutional ethical clearance and informed consent from the subjects. The subjects were divided into two groups. Group I (study group) comprised of 20 known diabetic patients (6 males and 14 females), with a fasting blood glucose more than 121mg/dl, with minimum of two years of disease duration. Both the Type 1 and Type two diabetic patients were included in this group. Group II (control group) comprised of 20 non diabetic patients (4 males and 16 females), who were age and gender matched as that of the previous group. The exclusion criteria included subjects who did not give written informed consent, gestational diabetic patients and patients with the habit of smoking. A detailed history of the patient was taken including personal history, drug history, allergies. The patients were clinically examined and assessed for dental caries and periodontal status using the Decay, Missing, Filled, Treatment (DMFT) index and Periodontal Disease Index (PDI) respectively. The blood samples were collected to estimate the fasting and postprandial blood glucose levels. The unstimulated whole salivary samples were collected from subjects in both the groups using spitting method, after a waiting period of 10 minutes, so as to avoid sample dilution before collecting the subjects were asked to bend the head forward and accumulate the saliva in the floor of the mouth and expectorate it in a sterile container, every five minutes for15 minutes. The pH of the samples was immediately analysed using a digital pH meter “pH Tester 10, 20, 30, 10 BNC, Spear”.

Results

In the present study, 20 diabetic (study group) and 20 non-diabetic (control group) subjects participated. [Table/Fig-1] depicts the comparison of mean salivary pH, DMFT and PDI among diabetic patients and non-diabetic patients, the salivary pH was low (6.5) among the study group compared to the control group (7.89) and the mean DMFT (8.1) and PDI (4) score were high in diabetic patients than non-diabetic patients whose DMFT and PDI score were 1.15 and 0.45 respectively. Independent sample t-test showed that there was a highly significant difference in the mean score between the study group and the control group, with a p-valve of <0.05, which was statistically significant.

Comparison of mean salivary pH, DMFT and PDI between Diabetic and Non- Diabetic Patients.

ParameterGroupNMeanStd. Deviationt- valuep-value
SALIVA pH*DM*206.50.716927.950.00
NDM*207.890.279117
DMFT*DM*208.15.8755.130.00
NDM*201.151.461
PDI*DM*2041.5899.330.00
NDM*200.450.605

*Independent Samples t-test, (p<0.05 – Statistically Significant)


[Table/Fig-2] depicts the correlation between the salivary pH, DMFT and PDI among the study group, a significant negative correlation (r = -0.52) was observed between the salivary pH and DMFT among diabetic patients.

Correlation between Salivary pH with DMFT and PDI among Diabetic Patients.

Diabetic PatientsDMFT*PDI
Saliva pH*-0.52*-0.09

*Pearsons correlation (p<0.05)


[Table/Fig-3] depicts the correlation between the salivary pH, DMFT and PDI among the control group, no significant correlation observed between the salivary pH, DMFT and PDI among non-diabetic patients.

Correlation between Salivary pH with DMFT and PDI among Non-Diabetic Patients.

Non -Diabetic PatientsDMFT*PDI*
Saliva pH*-0.065-0.35

* Pearsons correlation


Discussion

Diabetes mellitus is a common chronic metabolic disease with numerous oral and systemic manifestations. Oral manifestations of diabetes mellitus includes dental caries, salivary dysfunction, oral mucosal and other oral infections, taste and neurosensory disorders, gingivitis, periodontitis etc., [5]. This study evaluates the salivary pH, incidence of dental caries and periodontal status of diabetes mellitus patients and compares them with normal subjects. Saliva has a normal pH range of 6.2-7.6 with an average of 6.7 [3]. In the oral cavity, the pH is maintained near neutrality (6.7-7.3) by saliva. The saliva maintains the pH by two mechanisms. First the flow of saliva eliminates the carbohydrates which could be metabolized by the bacteria hence the acid produced by the bacteria is removed. Second, the buffering activity of saliva neutralizes the acidity formed from food and drinks, as well as from the microbial activity [3]. In the present study un-stimulated saliva samples were collected from diabetes and non-diabetes patients as the composition and pH may alter in stimulated salivary samples for determining the salivary pH [6].

The mean salivary pH was compared among the diabetic and non-diabetic. Diabetes mellitus subjects had decreased salivary pH when compared to that of control group [Table/Fig-1]. This may be attributed to the metabolic changes in diabetes mellitus patients resulting in acidic pH. In diabetes, there is reduction in the level of bicarbonates in all body fluids which leads to metabolic acidosis of all body fluids. This explains the acidic nature of the saliva in patients with diabetes mellitus [7]. Patients with diabetes mellitus had increased DMFT score when compared to the control group [Table/Fig-1]. This is due to loss of protective mechanism of the saliva in diabetics. The cleansing and buffering action of saliva is also impaired. Low salivary pH promotes the growth of aciduric bacteria which then allows the acidogenic bacteria to proliferate creating an inhospitable environment for the protective oral bacteria. This allows for a shift in the oral environmental balance to favour cariogenic bacteria, which further lowers the salivary pH and the cycle continues [8]. Cariogenic bacteria are likely to thrive in acidic environment. Other risk factors such as increased blood glucose levels, reduced salivary flow rate, buffering capacity, poor dietary control also increases the risk of dental caries in diabetes mellitus patients.

The present study is in accordance with studies done by Deepak Goyal et al., Ciglar et al., Rai K et al., Elkafri et al., who have reported decreased salivary pH and increased dental caries among diabetes mellitus patients [811]. Studies by Sadia Iqbal et al., Jawed et al., Akapata et al., have reported increased incidence of dental caries among diabetes mellitus patients [1214]. In contrast, studies by Collin HL et al., and Alves C et al., reported that no differences were found in the DMFT score among diabetics and non-diabetics [15,16].

When the periodontal status was compared, patients with diabetes mellitus had increased occurrence of gingivitis and periodontitis than the non-diabetic control group [Table/Fig-1]. Diabetes increases the risk of gingivitis and periodontitis. One of the major complications of diabetes is change in the microvascular integrity. In diabetes mellitus, chronic and prolonged hyperglycaemia leads to high levels of accumulation of irreversibly glycated proteins called Advanced Glycation End Products (AGEs) in the tissues including periodontium. Changes in the collagen stature, altered immune function have been reported. The changes in collagen stature, altered immune function and accumulation of AGEs in the periodontium causes impaired polymorphonuclear leukocyte function which may facilitate bacterial persistence in the tissues. Interactions between AGEs and inflammatory cells lead to increased production of proinflammatory cytokines such as IL-1β and TNF-α, which leads to an increase in collagenase activity and reduction in collagen synthesis which affects the collagen metabolism [1720]. This results in compromised wound healing and increased periodontal tissue destruction in diabetes mellitus patients. This study is in accordance with study done by Poplawaska-Kita A et al., who reported that there was an increased risk of periodontitis in patients with diabetes mellitus [21]. Also, the reduction in salivary pH which was evident in our study may increase the growth of periodontal-pathogens which is in accordance with that of Takahashi et al., Fujikawa et al., and Galgut [2225].

Negative correlation was found between salivary pH & DMFT and between salivary pH & PDI, [Table/Fig-2] which suggests that when the pH of the saliva is decreased (acidic), there is increased incidence of dental caries. This result is in accordance with the study done by Michelle Hurlbutt et al., who reported that low salivary pH promotes cariogenic lesions in the oral cavity [26]. Similarly, pH of saliva in patients with periodontitis is more acidic than control group [Table/Fig-2], which is similar to the study done by Sharmila Baliga et al., who reported that pH of saliva in patients with chronic generalized periodontitis was more acidic than pH of saliva of the control group [3]. This can be explained in accordance with the study conducted by Takahashi et al., that the microorganism which are responsible for periodontitis have a favourable environment for growth in an acidic pH such as P. gingivalis grows at a pH of 6.5-7.0, P. intermedia grows at a pH of 5.0-7.0 and F. nucleatum grows at a pH of 5.5-7.0 [22,23].

Limitation

In this study the blood glucose values were taken without any alteration in the medications which may influence the values of the results. This could be a limitation to our study but this was not taken into consideration as the disease is a chronic condition.

Conclusion

The present study concludes that patients with diabetes mellitus have reduced salivary pH, increased incidence of caries and periodontitis when compared to the control group. The pH of the saliva in patients with an increased DMFT and PDI score was more acidic than the patients with low DMFT and PDI score.

Diabetes mellitus has been consistently documented to be associated with altered salivary composition and function which disrupts the homeostasis of the oral cavity. This predisposes them to various oral ailments including dental caries and periodontitis. As salivary diagnostics is an emerging field, pH of saliva can be used to evaluate the severity of dental caries and periodontitis in diabetes mellitus patients. Saliva can be used as an indicator of prognosis during periodontal treatment. Prevention and management of oral complications in patients with diabetes and promotion of oral health is important due to their possible adverse effects on glycaemic control.

*Independent Samples t-test, (p<0.05 – Statistically Significant)*Pearsons correlation (p<0.05)* Pearsons correlation

References

[1]International Diabetes Federation. IDF diabetes atlas update poster, 6th edn. brussels, belgium: international diabetes federation, 2014. Available from www.idf.org/diabetesatlas  [Google Scholar]

[2]Devi TJ, Saliva-A Potential Diagnostic Tool IOSR Journal of Dental and Medical Sciences 2014 13(2):52-57.  [Google Scholar]

[3]Baliga S, Mugilkar S, Kale R, Salivary pH: A diagnostic biomarker J Indian Soc Periodontol 2013 17(4):461-65.  [Google Scholar]

[4]Lamster IB, Lalla E, Borgnakke WS, Taylor GW, The relationship between oral health and diabetes mellitus J Am Dent Assoc 2008 139(10 suppl):19S-24S.  [Google Scholar]

[5]Bangash RY, Khan AU, Tariq KM, Yousaf A, Oral aspects and complications in type 2 diabetes mellitus – a study Pakistan Oral & Dental Journal 2012 32(2):296-99.  [Google Scholar]

[6]Schipper R, Loof A, de Groot J, Harthoorn L, van Heerde W, Dransfield E, Salivary protein/peptide profiling with SELDI-TOF-MS Ann N Y Acad Sci 2007 1098:498-503.  [Google Scholar]

[7]Prathibha KM, Evaluation of salivary profile among adult type 2 diabetes mellitus patients in South India Journal of Clinical and Diagnostic Research 2013 7(8):1592-95.  [Google Scholar]

[8]Goyal D, Kaur H, Jawanda MK, Salivary pH and dental caries in diabetes mellitus International Journal of Oral & Maxillofacial Pathology 2012 3(4):13-16.  [Google Scholar]

[9]Ciglar I, Sutalo J, Sjaljac-Staudt G, Bozikov J, Saliva as a risk factor for caries in diabetic patients Acta Stomatol Croat 1991 25(3):143-49.  [Google Scholar]

[10]Rai K, Hegde AM, Kamath A, Shetty S, Dental Caries and salivary alterations I Type 1 Diabetes J Clin Pediatr Dent 2011 36(2):18-24.  [Google Scholar]

[11]Elkafri IH, Mashlah A, Shaqifa A, Relationship between blood glucose levels and salivary pH and buffering capacity in type II diabetes patients East Mediterr Health J 2014 20(2):139-45.  [Google Scholar]

[12]Iqbal S, Kazmi F, Asad S, Mumtaz M, Khan AA, Dental Caries & Diabetes mellitus Pakistan Oral & Dental Journal 2011 31(1)  [Google Scholar]

[13]Jawed M, Shahid SM, Qader SA, Azhar A, Dental caries in diabetes mellitus: role of salivary flow rate and minerals J Diabetes Complications 2011 25(3):183-86.  [Google Scholar]

[14]Akpata ES, Alomari Q, Mojiminiyi OA, Al-Sanae H, Caries experience among children with type 1 diabetes in Kuwait Pediatr Dent 2012 34(7):468-72.  [Google Scholar]

[15]Collin HL, Uusitupa M, Niskanen L, Koivisto AM, Markkanen H, Meurman JH, Caries in patients with non-insulin- dependent diabetes mellitus Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998 85(6):680-85.  [Google Scholar]

[16]Alves C, Menezes R, Brandão M, Salivary flow and dental caries in Brazilian youth with type 1 diabetes mellitus Indian J Dent Res 2012 23(6):758-62.  [Google Scholar]

[17]Duarte PM, Bezerra JP, Miranda TS, Feres M, Chambrone L, Shaddox LM, Local levels of inflammatory mediators in uncontrolled type 2 diabetic subjects with chronic periodontitis J Clin Periodontol 2014 41:11-18.  [Google Scholar]

[18]Pietropaoli D, Tatone C, D’Alessandro AM, Monaco A, Possible involvement of advanced glycation end products in periodontal diseases Int J Immunopathol Pharmacol 2010 23(3):683-91.  [Google Scholar]

[19]Kim J, Amar S, Periodontal disease and systemic conditions: a bidirectional relationship Odontology 2006 94(1):10-21.  [Google Scholar]

[20]Al-Maskari AY, Al-Maskari MY, Al-Sudairy S, Oral Manifestations and complications of diabetes mellitus A review SQU Med J 2011 11(2):179-86.  [Google Scholar]

[21]Popławska-Kita A, Siewko K, Szpak P, Król B, Telejko B, Klimiuk PA, Association between type 1 diabetes and periodontal health Adv Med Sci 2014 59(1):126-31.  [Google Scholar]

[22]Takahashi N, Schachtele CF, Effect of pH on the growth and proteolytic activity of Porphyromonas gingivalis and Bacteroides intermedius J Dent Res 1990 69:1266-69.  [Google Scholar]

[23]Takahashi N, Saito K, Schachtele CF, Yamada T, Acid tolerance and acid-neutralizing activity of Porphyromonas gingivalis, Prevotella intermedia and Fusobacterium nucleatum Oral Microbiol Immunol 1997 12:323-28.  [Google Scholar]

[24]Fujikawa K, Numasaki H, Kobayashi M, Sugano N, Tomura S, Murai S, pH determination in human crevicular fluids. Examination of the pH meter and evaluation of the correlation between pH level and clinical findings or the microflora in each periodontal pocket Nihon Shishubyo Gakkai Kaishi 1989 31:241-48.  [Google Scholar]

[25]Galgut PN, The relevance of pH to gingivitis and periodontitis J Int Acad Periodontol 2001 3:61-67.  [Google Scholar]

[26]Hurlbutt M, Novy B, Young D, Dental Caries: A pH-mediated disease Canadian Dental Hygienists’ Association Winter 2010   [Google Scholar]