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South African Dental Journal

On-line version ISSN 0375-1562
Print version ISSN 0011-8516

S. Afr. dent. j. vol.77 n.1 Johannesburg Feb. 2022

http://dx.doi.org/10.17159/2519-0105/2022/v77no1a1 

RESEARCH

 

Association between dental and periodontal conditions with chronic kidney disease: A cross-sectional analysis of urban South Africans

 

 

C GeorgeI; T E MatshaII; S F G DavidsIII; G M HonIV; U ChikteV; R T ErasmusVI; A P KengneVII

INon-Communicable Disease Research Unit, South African Medical Research Council, Cape Town, South Africa, http://oricid.org/0000-0002-4561-0529
IISAMRC/Cardiometabolic Health Research Unit, Department of Biomedical Sciences, Faculty of Health & Wellness Sciences, Cape Peninsula University of Technology, Cape Town, South Africa, https://orcid.org/0000-0001-5251-030X
IIISAMRC/Cardiometabolic Health Research Unit, Department of Biomedical Sciences, Faculty of Health & Wellness Sciences, Cape Peninsula University of Technology, Cape Town, South Africa, https://orcid.org/0000-0003-2960-7327
IVSAMRC/Cardiometabolic Health Research Unit, Department of Biomedical Sciences, Faculty of Health & Wellness Sciences, Cape Peninsula University of Technology, Cape Town, South Africa, https://orcid.org/0000-0001-8551-1798
VDivision of Health Systems and Public Health, Department of Global Health, Stellenbosch University, Cape Town, South Africa, https://orcid.org/0000-0002-7985-2278
VIDivision of Chemical Pathology, Faculty of Medicine and Health Sciences, National Health Laboratory Service (NHLS) and University of Stellenbosch, Cape Town, South Africa, https://orcid.org/0000-0001-6831-4215
VIINon-Communicable Disease Research Unit, South African Medical Research Council, Cape Town, South Africa and Department of Medicine, University of Cape Town, Cape Town, South Africa, https://orcid.org/0000-0002-5183-131X

Correspondence

 

 


ABSTRACT

INTRODUCTION: Oral diseases are preventable causes of poor health outcomes in people with chronic kidney disease (CKD).
AIMS AND OBJECTIVES: Investigate the association between dental and periodontal conditions with kidney function and determine whether inflammation mediate the association between periodontitis and CKD.
DESIGN: Cross-sectional analysis of 1551 South African adults of mixed ancestry.
METHODS: CKD was classified as estimated glomerular filtration rate (eGFR) <60mL/min/1.73m2. Oral profile was captured by decayed, missing, filled teeth index (DMFTi), bleeding on probing (BOP), pocket depth (PD), clinical attachment loss (CAL), and periodontitis classified as PD >4 mm.
RESULTS: Overall, 6% had CKD, with 93% and 66% of participants with and without CKD, respectively having a high DMFTi (p<0.0001). Further, 84% (CKD) and 43% (without CKD) were edentulous (p<0.0001). A great proportion of the dentate sub-sample (n=846) had periodontitis, however, BOP, PD >4mm and CAL >4mm were similar between the groups. DMFTi was associated with eGFR and prevalent CKD (p<0.023), with this association driven by the Missing component. Periodontitis was not associated with eGFR nor CKD (p>0.282
CONCLUSION: In routine care of people with CKD, attention should be given to oral health.

Key words: chronic kidney disease; oral disease; periodontitis; dental; tooth loss; Africa


 

 

INTRODUCTION AND BACKGROUND

Chronic kidney disease (CKD) is a major public health problem,1 estimated to affect at least 10% of the global adult population.2 Given that African populations are at even higher risk of developing CKD,3 it is essential to identify and manage the modifiable risk factors for CKD and progression to end-stage renal disease (ESRD), to reduce the significant burden on an already ailing health system.

Oral diseases are estimated to affect nearly half the global population.4,5 Of these oral diseases, periodontitis and dental caries have been implicated as a potential and preventable cause of poor health outcomes in people with CKD.6-9 Periodontitis, which affects the tissue surrounding the teeth, is thought to contribute to renal deficiency via inflammatory pathways.10-13 Indeed, several cross-sectional studies have reported that adults with periodontitis generally have elevated acute-phase systemic markers, like serum C-reactive protein (CRP) and oxidative stress responses,14,15 and are up to twice as likely to have CKD as their counterparts without periodontitis.9,16,17 On the contrary, dental caries, characterized by the localized destruction of the teeth due to the accumulation of acidic by-products,10 is much less explored in the context of CKD. In fact, there is no consensus in the literature on dental caries prevalence and the association with CKD. Certainly, some studies have shown that patients with CKD presents with lower dental caries,18,19 where others show that CKD is associated with a worse dental status20 compared to those without CKD, with a few studies showing no association between dental complications and CKD.21,22

Despite the advances made in the aetiology governing the development and progression of CKD, including the potential link with the oral cavity, population-based data on the overall oral status of people with CKD, particularly in Africa are lacking. We therefore aimed to, 1) characterise the dental and periodontal profile of those with and without CKD, 2) investigate the association between dental and periodontal conditions with kidney function and prevalent CKD, and further 3) evaluate whether systemic inflammation, as measured by hsCRP, mediates the association between periodontitis and kidney function and prevalent CKD in a community-based sample of urban South Africans of mixed-ancestry.

 

MATERIALS AND METHODS

Study setting and population

The data utilized in this analysis is from adult South Africans of mixed-ancestry (in South Africa referred to as the Coloured population).23 The study was approved by the Research Ethics Committees of the Cape Peninsula University of Technology and Stellenbosch University (NHREC: REC-230 408-014 and N14/01/003) respectively and conducted in accordance with the Declaration of Helsinki. As such, voluntarily signed written informed consent was received from all participants after the explanation of all procedures.

Questionnaires and physical examination

All anthropometric measurements were taken three time and the average presented in this paper. An Omron body fat meter HBF-511 digital bathroom scale was used to determine body weight, with the individual in light clothing and without shoes. Waist circumference (WC) was measured with a non-elastic tape measure by standard procedure, thus at the level of the narrowest part of the torso, as seen from the anterior view. Body mass index (BMI) was calculated by means of the conventional calculation as weight divided by the square of height (kg/m2). Systolic and diastolic blood pressure (SBP and DBP, respectively), taken in a seated position after 10 minutes of seated rest, were recorded three times on the right arm using a semi-automated digital blood pressure monitor (Omron M6 Comfort (Omron Healthcare Co., Ltd.). With the first measurement discarded, the average of the last two measures were used as the blood pressure measurement. A standardized oral examination, based on the World Health Organization (WHO) guidelines,24 was performed on all participants by a trained dental practitioner and has been published earlier.25 Briefly, bleeding on probing (BOP) was classified if bleeding was observed after a gentle periodontal probing around the tooth circumference. Each tooth was also examined for the presence of dental pockets by probing around the whole circumference and recording the highest score. Pocket depth (PD) categories included 0-3mm and >4mm. Finally, clinical attachment loss (CAL) was recorded with a periodontal probe as the highest score obtained for each sextant. Periodontitis was classified as the presence of PD >4 mm of one site. Decayed, missing and filled teeth (DMFT) index, which is a key measure of caries experience in dental epidemiology, was recorded for every participant, according to WHO guidelines.24 In short, the DMFT index is applied to all permanent dentition and is expressed as the total number of teeth or surfaces that are decayed (D), missing (M), or filled (F). Based on the DMFT score, DMFT severity was categorized based on the WHO criteria,24 as very low (<5.0), low (5.0-8.9), moderate (9.0-13.9) and high (>14). All participants were also asked about their perceived health of their mouth and to rate it as excellent, good, fair, poor or bad.

Biochemical analysis and classifications

The biochemical analyses were all conducted at an ISO 15189 accredited pathology practice (Path-Care, Reference Laboratory, Cape Town, South Africa) according to set protocols. Serum samples were processed for the measurement of creatinine, hsCRP and cotinine by the modified Jaffe-Kinetic method (Beckman AU, Beckman Coulter, South Africa), and chemiluminescent assays (Immun Diagnostik AG, Bensheim, Germany and Immulite 1000, Siemens) respectively.

Kidney function was estimated by means of the serum creatinine-based 4-variable Modification of Diet in Renal Disease (MDRD) equation,26 without the ethnicity correction factor. Findings were mostly similar in secondary analyses based on CKD Epidemiology Collaboration (CKD-EPI) equation27 estimated GFR (data not shown). As per the National Kidney Foundation Disease Outcomes Quality Initiative (NKF-KDOQI) guidelines,28 CKD was classified as an estimated glomerular filtration rate (eGFR) <60 ml/min/1.73 m2. Smoking and nonsmoking were categorized as cotinine levels >15 ng/ml and <15 ng/ml, respectively. Hypertension was classified as SBP >140 mmHg and/or DBP >90 mmHg,29 or a previous diagnoses of hypertension. Diabetes was classified as a history of previously diagnosed type 2 diabetes (T2D) or fasting glucose >7.0 mmol/l and/or 2-h glucose >11.1 mmol/l. Additional glucose tolerance categories were also classified based on the oral glucose tolerance test (OGTT)30 as: (1) normal glucose tolerance [FG <6.1 mmol/l and 2-h glucose <7.8 mmol/l], (2) impaired fasting glucose (IFG, 6.1<FG< 7.0 mmol/l), and (3) impaired glucose tolerance (IGT, 7.8<2-h glucose<11.1 mmol/l). A BMI>25kg/m2 and BMI>30kg/m2 were classified as overweight and obese, respectively.

Statistical analysis

Due to the skewed distribution of most variables, participant characteristics were summarised as median (25th-75th percentiles) or count and percentages. However, the DMFT index and total number of teeth were also presented as mean and standard deviation (SD), to comply with the standard presentation of data obtained from the WHO and mean comparisons with other studies. Group comparisons were done with chi-square tests (categorical variables) and Student-t test or Wilcoxon rank-sum test (continuous variables). Multivariable robust linear regression models were used to assess the independent association between eGFR and the DMFT index. Whereas multivariable logistic regression models were used to determine whether the DMFT index predicted prevalent CKD, independent of confounding variables (listed in the models below). Since individuals with edentulism are unable to experience periodontitis, a sub-analysis on dentate participants (n=846) were conducted. Thus, multivariable linear regression and logistic regression models were employed to assess the independent association of eGFR and prevalent CKD with periodontitis. The models used were as follows: Model 1: DMFT or periodontitis; Model 2: Model 1 + Age >60years; Model 3: Model 2 + smoking status + obesity; Model 4: Model 3 + hypertension; Model 5: Model 4 + diabetes; Model 6 (DMFT): Model 5 + edentulism; Model 6 (periodontitis): Model 5 + hsCRP. All statistical analyses were performed using STATA version 15 (Statcorp, College Station, TX) and statistical significance was based on a p-value <0.05.

 

RESULTS

General characteristics of study population

The general characteristics of the study population are summarised in Table I. The original study sample comprised 1,979 participants. Of those, 428 participants were excluded from this analysis due to missing data on serum creatinine or variables required to estimate kidney function, including age and gender, as well as those participants who did not receive an oral examination. The final sample included 1,551 participants, of which 25.2% were male, with ages ranging from 20 to 91 years (median age of 51 years), and 6% having an eGFR <60 ml/min/1.73m2. Of those with CKD, 79.2%, 15.6% and 5.2% wherein stages 3, 4 and 5 CKD, respectively. Compared to the participants with normal kidney function, those with CKD were on average older (68 vs. 49 years; p<0.0001), had a greater weight (75.0 vs. 71.7 kg; p=0.049), with a higher WC (100.2 vs. 91.0 cm; p<0.0001) and BMI (30.8 vs. 28.2 kg/m2; p=0.001). Further, 81.8% had a BMI in the overweight/obese range, compared to 65.0% in the group with normal kidney function. Of the participants with CKD, 11.8% and 44.7% had IFG/IGT and T2D, respectively, compared to 14.7% and 17.5%, respectively, in the group with normal kidney function. Also, those with CKD had a higher prevalence of hypertension compared to those without CKD (54.6% vs 35.1%, p<0.0001). Compared to those with normal kidney function, those with CKD also had higher hsCRP levels (4.7 vs. 3.9 pg/ml; p=0.044), with similar prevalence of smokers (p=0.765).

Dental and periodontal profile of study population

The dental profile of the study population is summarised in Table II and Figure 1. In the total sample, edentulism was found in 84.1% of those with CKD, compared to 43.1% of individuals with normal kidney function. On average those with reduced kidney function had significantly less teeth compared to those participants with normal kidney function (3.2 vs. 13 teeth; p<0.0001). Furthermore, CKD was characterized by a higher mean DMFT index compared to those without CKD (29.2 vs. 20.6; p<0.0001). Despite 93.2% and 66.0% of people with CKD and without CKD, respectively having a DMFT index greater than 14, 50% and 38.5% of those with and without CKD, respectively rated their overall oral health as either good or excellent. Based on the components of the DMFT index, for both groups the "missing" component had the highest contribution to the score with a greater contribution in those with CKD compared to those without CKD (87% vs. 69%; p<0.0001). On the contrary, compared to those without CKD, participants with CKD had a lower prevalence of decayed (8% vs. 25%; p<0.0001) and similar prevalence of filled teeth (5% vs. 6%; p=0.053) (Figure 1). Of the participants with CKD, 76.1% were fitted with dentures, compared to 45.8% of individuals with normal kidney function.

The periodontal profile of the dentate sub-sample (n=846) is presented in Table III and Figure 2. Compared to the participants with edentulism, those in the dentate sub-sample were on average younger (40.4 vs. 59.5 years; p<0.0001), had a higher eGFR (112.7 vs. 91.7 ml/ min/1.73m2; p<0.0001) and lower prevalence of CKD (2% vs. 11%; p<0.0001). The periodontal profile of those with CKD were not different to those with normal kidney function. On average, people with CKD had similar total number of teeth compared to those without CKD (19.9 vs. 23.3 teeth; p=0.075). Despite the high prevalence of periodontitis, no differences were observed between those with and without CKD (67.1% vs. 57.1%; p=0.301) (Figure 2). Likewise, similar prevalence of BOP, PD >4mm and CAL >4mm was observed for participants with and without CKD (p>0.276 for all). Furthermore, the average number of teeth with BOP and PD >4mm was similar for individuals with CKD and those without CKD (p>0.391 for all). Also, similar prevalence levels of bleeding teeth and teeth with dental pockets greater than 4mm were observed between the two groups (12.2% vs. 10.9%; p=0.656 and 14.9% vs. 7.7%; p=0.246, respectively).

Relationship between dental caries and periodontitis with kidney function and prevalent chronic kidney disease

The unadjusted and adjusted associations for eGFR and prevalent CKD by DMFT index and periodontitis are presented in Tables IV and V, respectively. In robust linear regression analysis, higher DMFT scores were associated with lower eGFR (p<0.0001 for all), independent of older age (>60 years), smoking status, obesity, hypertension, and diabetes status (Table IV, Models 1-5). However, this association was not independent of edentulism (p=0.261) (Table IV, Model 6). Similarly, higher DMFT scores predicted prevalent CKD (p<0.023 for all) (Table V, Models 1-5), however not independent of edentulism (p=0.645) (Table V, Model 6). Periodontitis on the other hand was not associated with eGFR (p>0.558 for all) nor prevalent CKD (p>0.258 for all) (Tables IV and V, respectively; Model 1-5), before and after adjustment for relevant confounding variables.

Effect modification by hsCRP on the relationship between periodontitis and kidney function and prevalent CKD

There was no evidence of effect modification by hsCRP on the relationship between periodontitis and eGFR (p=0.792) (Table IV, Model 6), nor did hsCRP mediate the association between periodontitis and prevalent CKD (p=0.390) (Table V, Model 6), as the addition of hsCRP to the models had no effect on the association.

 

DISCUSSION

To the best of our knowledge, this is the first study to evaluate the periodontal and dental status of people of mixed ancestry with CKD. This study shows that adults of mixed ancestry, with and without CKD, have a severely impaired periodontal and dental status, with the clear majority experiencing periodontitis, dental caries and/or edentulism. Yet, despite the high prevalence of periodontitis in this population, this inflammatory condition seemingly had no effect on renal function nor could it predict CKD in this sample. However, given the small sub-sample of dentate individuals with CKD, this result should be viewed cautiously. We further showed that even though CKD is associated with a higher level of dental caries experienced, given the high DMFT index, this association is driven by the "missing" component and particularly the high level of edentulism in this group. Indeed, evaluating the components of the DMFT score, we found that CKD is associated with less decayed and filled teeth, but more missing teeth.

Though there is support for an association between periodontitis and CKD6 and periodontitis has been identified as a potential source of inflammation in CKD patients,31,32 the current evidence is insufficient to link periodontitis with CKD, through an inflammatory pathway. Contrary to our study, previous studies evaluating the link between periodontitis and CKD are either in patients undergoing haemodialyis or peritoneal dialysis or in the instance where the studies are conducted in predialysis patients, these patients have severe CKD, thus close to initiating dialysis.6,16,33 Also, the association between periodontitis and CKD is dependent on the severity of periodontitis. As such, the strength of the link between periodontitis and CKD increases with increasing severity of periodontitis.6,34 Even though we found no association between periodontitis and reduced kidney function in this study, we cannot exclude the possibility of such an association. Thus, it is not possible to determine, based on the existing evidence, if the relationship is truly absent in this group, or whether our study was not sufficiently powered to detect the difference, given the reduced sample of dentulous individuals. This hypothesis therefore needs further investigation.

With more than two thirds of the population presenting with a DMFT score greater than 14, the severity of caries experienced in this under-studied South African population is more comparable to higher income countries, such as the USA, Australia and Canada as opposed to other African countries,35 or even other population groups in South Africa.36 Furthermore, and perhaps of greater concern, is that CKD is associated with even higher DMFT scores. Indeed, in people with CKD nearly all teeth are somehow affected, with the M (missing) component making the largest contribution to the DMFT score. Given that untreated dental caries is one of the main causes of tooth loss,37,38 with the prevalence increasing with age,39 it could be assumed that higher dental caries and thus higher tooth loss associates with CKD. However, because the DMFT index quantifies the life-long caries experience and do not account for teeth lost for reasons other than decay, it is difficult to say whether the prevalence of the missing component in this population is solely because of untreated caries. In fact, there is no consensus in the literature on caries prevalence in people with CKD.19,21 Thus, based on the cross-sectional design of this study it might be more appropriate to evaluate the contribution of each component making up the score, as opposed to the overall score.

In this study, compared to the F (filled) and M (missing) component, we found that the D (decayed) component contributed less to the DMFT index in those with CKD, compared to the contribution of this component to those with normal kidney function. This lower prevalence of decayed teeth in people with CKD has been reported in other studies,19,33 and this finding has previously been ascribed to the high salivary urea and phosphate levels in people with CKD.18,33,40 Even though those end-points were not measured in the current study, the lower prevalence of decayed teeth in those with CKD could be explained by the higher pH environment originating from urea hydrolysis in the saliva, resulting in the neutralization of the end products of bacterial plaque and consequent reduced tooth decay.18,33,40 People with CKD also presented with a significantly smaller proportion of filled teeth and higher proportion of missing teeth, reflecting the low utilization of curative dental care in the CKD population. Certainly, in resource-poor public healthcare settings, recommended regular preventive dental care may not be readily accessible.35,41,42 Also, the perceived importance of oral health in this older population with CKD is of importance. Indeed, there is a perception that the loss of teeth, as the result of dental caries, are an inevitable consequence of ageing43 and therefore preventative measures are not generally perceived as priority. Consequently, tooth extraction is often the socially acceptable solution to the pain or discomfort due to caries, in exchange for fitted dentures, rather than restoring the natural teeth.35,43 Also, there is a lack of awareness regarding the importance of oral health and disease.44 Previous research indicates that a significant positive predictor of the utilisation of dental care is the "perceived need" for it.45 This is indirectly shown through our findings, where despite the very high DMFT scores in 93% of people with CKD, all rated their overall oral health as either, fair, good or excellent. This perception of adequate oral health can be explained by the fact that people often rate their oral health status based on undesirable oral symptoms displayed46 and since those with high DMFT had dentures the perception of good oral health are very likely.

Edentulism, which is the condition of being completely toothless, is also a major concern in this subpopulation with CKD, as 84% of the group had no teeth; an estimate substantially higher than most other countries.47 Indeed, according to the latest systematic review, the global prevalence of edentulism in people with CKD is estimated at around 20% for adults aged 65 years and above.37 This disparity from global estimates could be explained by the main factors associated with tooth loss and edentulism. According to the findings of a recent multi-country study, factors including older age, lower education, non-communicable diseases, obesity, tobacco use, and inadequate fruit and vegetable consumption are some of the risk factors predicting edentulism.47 Indeed, more than half of the population with CKD in the current study were obese, 39% had diabetes and 64% had hypertension. Further, those with CKD were older, with 83% being older than 60 years, compared to those without CKD. Thus, the high exposure to risk factors and high prevalence of edentulism (because of age) are likely to explain the higher missing component and thus higher DMFT scores reported in the CKD population compared to the group with normal kidney function.

This study has some limitations, which includes the high female to male participation, however this is a common trend in South African population studies. The association across CKD categories could not be evaluated as there were very few participants in the advanced stages of CKD (stage >4). Our study also used a single serum creatinine measure to determine the grade of kidney function and did not include estimates of albuminuria. It is however a common practice in community-based studies to diagnose CKD using a single measurement of serum creatinine. Also, because such a large proportion of people with CKD were edentulous, removing those with no teeth rendered the group with CKD very small. Also, we never gained information centred around the reason for tooth loss, and we are therefore unable to confirm whether tooth loss was due to caries, periodontitis or due to any other reasons. However, despite these limitations, we are not aware of other studies that have assessed the association between oral disease and CKD and the potential mediatory effect of systemic inflammation on this association in this previously understudied South African population group.

 

CONCLUSION

It is crucial that decision makers implement health strategies that focus on promoting good oral health and preventing oral disease, such as periodontitis and dental caries, also shifting away from the current predominantly emergency service of dental extractions. Due to the complex nature of the determinants of oral disease, both for people with and without CKD, exploring CKD patient preferences and priorities for dental care could guide additional research and practice interventions.

 

Acknowledgements

We are grateful to the Cape Town VMH study investigation team and population of Bellville-South (Cape Town, South Africa) for their participation.

The author contributions are as follows: Conceived and/or designed the work that led to the submission (TEM, UC, RTE, APK, CG), acquired data (TEM, SFGD, GMH, UC), and/or played an important role in interpreting the results (UC, APK, CG), drafted (CG) or revised the manuscript (all authors), and approved the final version (all authors). The authors have no conflict of interest to disclose.

Funding declaration: This study was funded by the South African Medical Research Council (SAMRC) with funds from National Treasury under its Economic Competitiveness and Support Package (MRC-RFA-UFSP-01-2013/VMH Study) and strategic funds from the SAMRC received from the South African National Department of Health.

 

References

1. Eckardt KU, Coresh J, Devuyst O, Johnson RJ, Kottgen A, Levey AS, Levin A. Evolving importance of kidney disease: from subspecialty to global health burden. Lancet. 2013;382(9887):158-69. doi: 10.1016/S0140- 6736(13)60439-0.         [ Links ]

2. George C, Mogueo A, Okpechi I, Echouffo-Tcheugui JB, Kengne AP. Chronic kidney disease in low-income to middle-income countries: the case for increased screening. BMJ Glob Health. 2017;2(2):e000256. doi: 10.1136/bmjgh-2016-000256.         [ Links ]

3. Kaze AD, Ilori T, Jaar BG, Echouffo-Tcheugui JB. Burden of chronic kidney disease on the African continent: a systematic review and meta-analysis. BMC Nephrol. 2018;19(1):125. doi: 10.1186/s12882-018-0930-5        [ Links ]

4. Petersen PE, Bourgeois D, Ogawa H, Estupinan-Day S, Ndiaye C. The global burden of oral diseases and risks to oral health. Bulletin of the World Health Organization. 2005;83(9):661-9.         [ Links ]

5. Global Burden of Disease 2016 Disease and Injury Incidence and Prevalence Collaborators. Global, regional, and national incidence, prevalence, and years lived with disability for 328 diseases and injuries for 195 countries, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet (London, England). 2017;390(10100):1211-59. doi: 10.1016/S0140-6736(17)32154-2.         [ Links ]

6. Deschamps-Lenhardt S, Martin-Cabezas R, Hannedouche T, Huck O. Association between periodontitis and chronic kidney disease: Systematic review and meta-analysis. Oral diseases. 2019;25(2):385-402. doi: 10.1111/odi.12834.         [ Links ]

7. Ioannidou E, Swede H, Dongari-Bagtzoglou A. Periodontitis predicts elevated C-reactive protein levels in chronic kidney disease. Journal of dental research. 2011;90(12):1411-5. doi: 10.1177/0022034511423394.         [ Links ]

8. Sharma P, Dietrich T, Ferro CJ, Cockwell P, Chapple IL. Association between periodontitis and mortality in stages 3-5 chronic kidney disease: NHANES III and linked mortality study. Journal of clinical periodontology. 2016;43(2):104-13. doi: 10.1111/jcpe.12502.         [ Links ]

9. Fisher MA, Taylor GW. A prediction model for chronic kidney disease includes periodontal disease. Journal of periodontology. 2009;80(1):16-23. doi: 10.1902/ jop.2009.080226.         [ Links ]

10. Peres MA, Macpherson LMD, Weyant RJ, Daly B, Venturelli R, Mathur MR, Listl S, Celeste RK, Guarnizo-Herreho CC, Kearns C, Benzian H, Allison P, Watt RG. Oral diseases: a global public health challenge. Lancet. 2019;394(10194):249-60. doi: 10.1016/S0140-6736(19)31146-8.         [ Links ]

11. Zhao D, Khawaja AT, Jin L, Li KY, Tonetti M, Pelekos G. The directional and non-directional associations of periodontitis with chronic kidney disease: A systematic review and meta-analysis of observational studies. Journal of periodontal research. 2018;53(5):682-704. doi: 10.1111/jre.12565.         [ Links ]

12. Petersen PE, Ogawa H. The global burden of periodontal disease: towards integration with chronic disease prevention and control. Periodontology 2000. 2012;60(1):15-39. doi: 10.1111/J.1600-0757.2011.00425.x.         [ Links ]

13. Hajishengallis G, Lambris JD. Complement and dysbiosis in periodontal disease. Immunobiology. 2012;217(11):1111-6. doi: 10.1016/j. imbio.2012.07.007.         [ Links ]

14. D'Aiuto F, Parkar M, Andreou G, Suvan J, Brett PM, Ready D, Tonetti MS. Periodontitis and systemic inflammation: control of the local infection is associated with a reduction in serum inflammatory markers. Journal of dental research. 2004;83(2):156-60. doi: 10.1177/154405910408300214.         [ Links ]

15. Paraskevas S, Huizinga JD, Loos BG. A systematic review and meta-analyses on C-reactive protein in relation to periodontitis. Journal of clinical periodontology. 2008;35(4):277-90. doi:10.1111/j.1600-051X.2007.01173.x.         [ Links ]

16. Borawski J, Wilczynska-Borawska M, Stokowska W, Mysliwiec M. The periodontal status of pre-dialysis chronic kidney disease and maintenance dialysis patients. Nephrol Dial Transplant. 2007;22(2):457-64. doi: 10.1093/ndt/gfl676.         [ Links ]

17. Ioannidou E, Hall Y, Swede H, Himmelfarb J. Periodontitis associated with chronic kidney disease among Mexican Americans. Journal of public health dentistry. 2013;73(2):112-9. doi: 10.1111/j.1752-7325.2012.00350.x.         [ Links ]

18. Andrade MR, Salazar SL, de Sá LF, Portela M, Ferreira-Pereira A, Soares RM, Leão AT, Primo LG. Role of saliva in the caries experience and calculus formation of young patients undergoing hemodialysis. Clinical oral investigations. 2015;19(8):1973-80. doi: 10.1007/s00784-015-1441-4.         [ Links ]

19. Menezes CR, Pereira AL, Ribeiro CC, Chaves CO, Guerra RN, Thomaz É B, Monteiro-Neto V, Alves CM. Is there association between chronic kidney disease and dental caries? A case-controlled study. Medicina oral, patologia oral y cirugia bucal. 2019;24(2):e211-e6. doi: 10.4317/medoral.22737.         [ Links ]

20. Thorman R, Neovius M, Hylander B. Clinical findings in oral health during progression of chronic kidney disease to end-stage renal disease in a Swedish population. Scandinavian journal of urology and nephrology. 2009;43(2):154-9. doi: 10.1080/00365590802464817.         [ Links ]

21. Andrade MR, Antunes LA, Soares RM, Leao AT, Maia LC, Primo LG. Lower dental caries prevalence associated to chronic kidney disease: a systematic review. Pediatric nephrology (Berlin, Germany). 2014;29(5):771-8. doi: 10.1007/s00467-013-2437-4.         [ Links ]

22. Garcez J, Limeres Posse J, Carmona IT, Feijoo JF, Diz Dios P. Oral health status of patients with a mild decrease in glomerular filtration rate. Oral surgery, oral medicine, oral pathology, oral radiology, and endodontics. 2009;107(2):224-8. doi: 10.1016/j.tripleo.2008.09.018.         [ Links ]

23. Kengne AP, Erasmus RT, Levitt NS, Matsha TE. Alternative indices of glucose homeostasis as biochemical diagnostic tests for abnormal glucose tolerance in an African setting. Primary care diabetes. 2017;11(2):119-31        [ Links ]

24. World Health Organization. Oral health surveys: basic methods. 5th ed. Geneva: WHO; 2013.         [ Links ]

25. Chikte U, Pontes CC, Karangwa I, Kimmie-Dhansay F, Erasmus R, Kengne AP, et al. Dental caries in a South African adult population: findings from the Cape Town Vascular and Metabolic Health Study. Int Dent J. 2019:10.1111/idj.12538.         [ Links ]

26. Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D. A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Modification of Diet in Renal Disease Study Group. Annals of internal medicine. 1999;130(6):461-70. doi: 10.7326/0003-4819-130-6199903160-00002.         [ Links ]

27. Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF, 3rd, Feldman HI, Kusek JW, Eggers P, Van Lente F, Greene T, Coresh J, Chronic Kidney Disease Epidemiology Collaboration. A new equation to estimate glomerular filtration rate. Annals of internal medicine. 2009;150(9):604-12. doi: 10.7326/00034819-150-9-200905050-00006.         [ Links ]

28. Levey AS, Coresh J, Balk E, Kausz AT, Levin A, Steffes MW, Hogg RJ, Perrone RD, Lau J, Eknoyan G, National Kidney Foundation. National Kidney Foundation practice guidelines for chronic kidney disease: evaluation, classification, and stratification. Annals of internal medicine. 2003;139(2):137-47. doi: 10.7326/0003-4819-139-2-200307150-00013.         [ Links ]

29. World Health Organization. A global brief on Hypertension: Silent killer, global public health crisis. 2013.         [ Links ]

30. World Health Organization, International Diabetes Federation. Definition and diagnosis of diabetes mellitus and intermediate hyperglycaemia: report of a WHO/IDF consultation. Geneva: World Health Organization; 2006.         [ Links ]

31. Tonelli M, Sacks F, Pfeffer M, Jhangri GS, Curhan G, Cholesterol Recurrent Events Trial Investigators. Biomarkers of inflammation and progression of chronic kidney disease. Kidney Int. 2005;68(1):237-45. doi: 10.1111/j.1523-1755.2005.00398.x.         [ Links ]

32. Menon V, Greene T, Wang X, Pereira AA, Marcovina SM, Beck GJ, Kusek JW, Collins AJ, Levey AS, Sarnak MJ. C-reactive protein and albumin as predictors of all-cause and cardiovascular mortality in chronic kidney disease. Kidney Int. 2005;68(2):766-72. doi:10.1111/j.1523-1755.2005.00455.x.         [ Links ]

33. Akar H, Akar GC, Carrero JJ, Stenvinkel P, Lindholm B. Systemic consequences of poor oral health in chronic kidney disease patients. Clin J Am Soc Nephrol. 2011;6(1):218-26. doi: 10.2215/CJN.05470610.         [ Links ]

34. Grubbs V, Vittinghoff E, Taylor G, Kritz-Silverstein D, Powe N, Bibbins-Domingo K, Ishani A, Cummings SR, Osteoporotic Fractures in Men Study Research Group. The association of periodontal disease with kidney function decline: a longitudinal retrospective analysis of the MrOS dental study. Nephrol Dial Transplant. 2016;31(3):466-72. doi: 10.1093/ndt/gfv312.         [ Links ]

35. Petersen P, World Health Organization Oral Health Programme. The world oral health report 2003: continuous improvement of oral health in the 21st century - the approach of the WHO Global Oral Health Programme. Geneva: World Health Organization; 2003.         [ Links ]

36. South African Department of Health. National Oral Health Survey: South Africa 1988/89. In: Health Do, editor. Pretoria1994.         [ Links ]

37. Ruospo M, Palmer SC, Craig JC, Gentile G, Johnson DW, Ford PJ, Tonelli M, Petruzzi M, De Benedittis M, Strippoli GF. Prevalence and severity of oral disease in adults with chronic kidney disease: a systematic review of observational studies. Nephrol Dial Transplant. 2014;29(2):364-75. doi: 10.1093/ndt/gft401.         [ Links ]

38. Jepsen S, Blanco J, Buchalla W, Carvalho JC, Dietrich T, Dörfer C, Eaton KA, Figuero E, Frencken JE, Graziani F, Higham SM, Kocher T, Maltz M, Ortiz-Vigon A, Schmoeckel J, Sculean A, Tenuta LM, van der Veen MH, Machiulskiene V. Prevention and control of dental caries and periodontal diseases at individual and population level: consensus report of group 3 of joint EFP/ORCA workshop on the boundaries between caries and periodontal diseases. Journal of clinical periodontology. 2017;44 Suppl 18:S85-s93. doi: 10.1111/jcpe.12687.         [ Links ]

39. Kassebaum NJ, Bernabé E, Dahiya M, Bhandari B, Murray CJL, Marcenes W. Global Burden of Severe Tooth Loss: A Systematic Review and Meta-analysis. Journal of dental research. 2014;93(7 Suppl):20S-8S. doi: 10.1177/0022034514537828.         [ Links ]

40. Pham TAV, Le DD. Dental condition and salivary characteristics in Vietnamese patients with chronic kidney disease. International journal of dental hygiene. 2019;17(3):253-60. doi: 10.1111/idh.12380.         [ Links ]

41. Grubbs V, Plantinga LC, Tuot DS, Powe NR. Chronic kidney disease and use of dental services in a United States public healthcare system: a retrospective cohort study. BMC Nephrol. 2012;13(1):16. doi:10.1186/1471-2369-13-16.         [ Links ]

42. WHO Regional Office for Africa. Promoting Oral Health in Africa: Prevention and control of oral diseases and noma as part of essential noncommunicable disease interventions. 2016.         [ Links ]

43. Kailembo A, Preet R, Stewart Williams J. Common risk factors and edentulism in adults, aged 50 years and over, in China, Ghana, India and South Africa: results from the WHO Study on global AGEing and adult health (SAGE). BMC oral health. 2016;17(1):29. doi: 10.1186/s12903-016-0256-2.         [ Links ]

44. van Wyk PJ, van Wyk C. Oral health in South Africa. Int Dent J. 2004;54(6 Suppl 1):373-7. doi: 10.1111/J.1875-595x.2004.tb00014.x.         [ Links ]

45. Molete MP, Yengopal V, Moorman J. Oral health needs and barriers to accessing care among the elderly in Johannesburg. SADJ: journal of the South African Dental Association = tydskrif van die Suid-Afrikaanse Tandheelkundige Vereniging. 2014;69(8):352, 4-7.         [ Links ]

46. Olutola BG, Ayo-Yusuf OA. Socio-environmental factors associated with self-rated oral health in South Africa: a multilevel effects model. International journal of environmental research and public health. 2012;9(10):3465-83. doi: 10.3390/ijerph9103465.         [ Links ]

47. Peltzer K, Hewlett S, Yawson AE, Moynihan P, Preet R, Wu F, Guo G, Arokiasamy P, Snodgrass JJ, Chatterji S, Engelstad ME, Kowal P. Prevalence of loss of all teeth (edentulism) and associated factors in older adults in China, Ghana, India, Mexico, Russia and South Africa. International journal of environmental research and public health. 2014;11(11):11308-24. doi: 10.3390/ijerph111111308.         [ Links ]

 

 

Correspondence:
Cindy George
South African Medical Research Council
Tel: +27 21 938 0482
Email: cindy.george@mrc.ac.za

 

 

Author contributions:
1 . Cindy George: 20% Contribution
2 . Tandi E Matsha: 15% Contribution
3 . Saarah FG Davids: 10% Contribution
4 . Gloudina M Hon: 10% Contribution
5 . U Chikte: 15% Contribution
6 . Rajiv T Erasmus: 15% Contribution
7 . Andre P Kengne: 15% Contribution

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