To the editorPeriodontal disease is a common, multifactorial chronic inflammatory disease of the gums and tooth-supporting apparatus, associated with loss of teeth, systemic inflammation and increased mortality.1Kinane D.F. Stathopoulou P.G. Papapanou P.N. Various factors may contribute to the development of periodontal disease in patients with chronic kidney disease (CKD), including altered immune system function, CKD mineral and bone disease, oral dysbiosis, poor oral hygiene and the presence of co-morbidities such as diabetes; some have suggested that periodontal disease may itself be a risk factor for progression of CKD. Patients with CKD who also have periodontal disease have been shown to have increased mortality compared to those who do not.2Sharma P. Dietrich T. Ferro C.J. Cockwell P. Chapple I.L. Association between periodontitis and mortality in stages 3-5 chronic kidney disease: NHANES III and linked mortality study. Despite the established benefits of regular preventative dental care, this may not be readily accessible, particularly for patients attending hemodialysis sessions three times a week.We evaluated a program of on-dialysis dental screening to determine objectively the prevalence of periodontal disease in our hemodialysis patients. Patients attending for daytime sessions at seven in-center hemodialysis units across four separate hospital sites were invited to participate; those giving consent completed an oral health questionnaire and underwent a focused periodontal examination carried out during the dialysis session by three qualified dentists who had previously calibrated examination techniques, using an adjustable overhead lights and disposable dental kits. An adaptation of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions 3Caton J.G. Armitage G. Berglundh T. et al.A new classification scheme for periodontal and peri-implant diseases and conditions - Introduction and key changes from the 1999 classification. was created, to allow a confident periodontal diagnosis to be made on the basis of examination findings alone, in the absence of radiographic data.A total of 127 patients consented to be included in the study, and a periodontal diagnosis was reached in 118 of these (seven were entirely edentulous and two did not tolerate the full examination). Only 15 patients (12.7%) had an entirely healthy periodontium; a further 21 (17.8%) had evidence only of gingivitis. All the rest (69.5%) had periodontitis, with 59 (50%) having moderate or severe disease (figure 1a, supplementary table S2). Almost half (49.6%) of all patients reported active dental symptoms at the time of examination; this did not associate closely with periodontal diagnosis and 54% of those with periodontal disease were asymptomatic.

Figure 1Prevalence of periodontal disease in patients receiving hemodialysis. a, periodontal status in the whole study population. b, periodontal status according to ethnicity, eligibility for free dental care and employment status.

Multivariate ordinal regression identified three patient factors associated with increased disease severity: age (odds ratio (OR) 0.456 on a five-point disease severity score, 95% confidence interval 0.118-0.734, p=0.007), non-white ethnicity (OR 1.51, 0.319-2.701, p=0.013) and smoking status (OR for never having smoked -1.093, -1.885 - -0.3, p=0.007). Patients with gingivitis or healthy gums had a mean age of 54 years vs 63 years in those with periodontitis (p=0.004). There was a trend toward higher disease scores in those with a greater duration of renal replacement therapy (OR 0.04, 0.0-0.09, p=0.068), and in those living in more deprived areas based on the index of multiple deprivation (OR 0.15, 0.043 – 0.342, p=0.127). Compared to patients with gingival health or gingivitis, there was a trend for those with severe periodontitis to weigh less (mean body weight 69.1kg vs 76.6kg, p=0.087), have lower body mass index (25.2 vs 27.3, p=0.192) and have higher rates of diabetes (60% vs 41.6%, p=0.093). Diabetic patients with periodontitis had higher HbA1c than those without (mean 43.9mmol/mol in healthy patients vs 55.6 in those with periodontitis, p=0.007).

We did not demonstrate associations between periodontal disease and a range of biochemical parameters including serum albumin, C-reactive protein and parathyroid protein.

Almost all patients (97.5%) reported brushing their teeth at least once daily, with two thirds (65%) brushing twice daily. Although 69.9% of patients were registered with a dentist, only 38.6% attended for regular review (table 1). Of the 78 patients not attending for regular dental review, 41% could not identify a particular reason for this. Among those identifying a reason, lack of time to attend appointments was the leading barrier to accessing care (37.8%), followed by fear of dentists (17.9%), access problems caused by the COVID-19 pandemic (13.3%) and mobility issues (8.9%). Only 6.7% identified financial problems as a barrier to care. 82.7% of patients indicated that they would welcome a dental service set up specifically for dialysis patients.

Table 1Access to dental care in the study population.

Although not statistically significant, we found that only 36.3% of patients living in more deprived areas (index of multiple deprivation 1-4) attended the dentist regularly compared with 44.4% of patients living in less deprived areas. Non-significant ethnic differences also emerged with 42.5% of white patients attending the dentist regularly compared with 40.7% of Asians, 35.1% of black patients and 34.8% of those from other ethnicities.

As far as we are aware, this is the first study to evaluate a dental screening program comprising dental examinations performed whilst patients are receiving hemodialysis. The system we devised for classifying periodontal disease, whilst not previously validated, allows a confident (although limited) severity assessment based on international guidelines (as set out fully in the supporting documents) during a bedside dental examination, limiting the number of visits patients need to make to healthcare facilities.

We have demonstrated a very high prevalence of periodontal disease among patients receiving hemodialysis, similar to those reported previously, and highest in patients who were older, current or former smokers, non-white and diabetic.3Caton J.G. Armitage G. Berglundh T. et al.A new classification scheme for periodontal and peri-implant diseases and conditions - Introduction and key changes from the 1999 classification., 4Chen L.P. Chiang C.K. Chan C.P. Hung K.Y. Huang C.S. Does periodontitis reflect inflammation and malnutrition status in hemodialysis patients?., 5Camacho-Alonso F. Canovas-Garcia C. Martinez-Ortiz C. et al.Oral status, quality of life, and anxiety and depression in hemodialysis patients and the effect of the duration of treatment by dialysis on these variables., 6Tai Y.H. Chen J.T. Kuo H.C. et al.Periodontal disease and risk of mortality and kidney function decline in advanced chronic kidney disease: a nationwide population-based cohort study., 7Borrell L.N. Crawford N.D. Socioeconomic position indicators and periodontitis: examining the evidence.There is good evidence in the general population that non-surgical periodontal therapy, involving scaling and root planing, reduces the severity of periodontal disease.8Cugini M.A. Haffajee A.D. Smith C. Kent Jr., R.L. Socransky S.S. The effect of scaling and root planing on the clinical and microbiological parameters of periodontal diseases: 12-month results. In the CKD population, randomised controlled trials have highlighted similar benefits including an improvement in disease scores and a reduction in systemic inflammation.9Yue H. Xu X. Liu Q. Li X. Xiao Y. Hu B. Effects of non-surgical periodontal therapy on systemic inflammation and metabolic markers in patients undergoing hemodialysis and/or peritoneal dialysis: a systematic review and meta-analysis. Our results suggest that patients receiving hemodialysis may be denied this treatment because so few, especially in disadvantaged groups, attend the dentist regularly. The requirement for three-times weekly hospital attendance, along with travel and recovery times, represents a considerable burden for many patients receiving hemodialysis, meaning that it is unsurprising that lack of time is the most commonly-cited reason why patients do not undergo regular dental review. The inability of many patients to give a reason for their lack of engagement with dental care may imply that they are unaware of its relevance to their clinical condition, highlighting the need for clinicians to take a proactive approach in addressing their oral health.

This was a cross-sectional observational study carried out in a single dialysis program in the east of London which contains a diverse population and includes areas of considerable socioeconomic deprivation. It was carried out during the COVID-19 pandemic at a time when many routine healthcare services were severely disrupted. We surveyed only patients attending for day-time dialysis slots as opposed to those in evening slots; therefore, our results may preferentially represent the frailer parts of our total patient population. Furthermore, we are based in the UK where free dental treatment is available via the National Health Service for many on low incomes. Each of these factors may limit the generalizability of our findings in other contexts, and suggest the need for further, larger, multi-center trials.

Notwithstanding this, there is accumulating evidence that CKD itself is a risk factor for periodontal disease, meaning that regardless of demographics, a high prevalence may be expected in any patients receiving hemodialysis. We suggest that periodontal disease may be an overlooked healthcare need in these patients, and that as clinical services are being re-built after the pandemic, a dedicated dialysis dental service might be a way to address healthcare inequalities and reduce barriers to care.

ReferencesKinane D.F. Stathopoulou P.G. Papapanou P.N. Periodontal diseases. Nat Rev Dis Primers. 317038https://doi.org/10.1038/nrdp.2017.38Sharma P. Dietrich T. Ferro C.J. Cockwell P. Chapple I.L.

Association between periodontitis and mortality in stages 3-5 chronic kidney disease: NHANES III and linked mortality study.

J Clin Periodontol. Feb. 43: 104-113https://doi.org/10.1111/jcpe.12502Caton J.G. Armitage G. Berglundh T. et al.

A new classification scheme for periodontal and peri-implant diseases and conditions - Introduction and key changes from the 1999 classification.

J Clin Periodontol. Jun. 45: S1-s8https://doi.org/10.1111/jcpe.12935Chen L.P. Chiang C.K. Chan C.P. Hung K.Y. Huang C.S.

Does periodontitis reflect inflammation and malnutrition status in hemodialysis patients?.

Am J Kidney Dis. May. 47: 815-822https://doi.org/10.1053/j.ajkd.2006.01.018Camacho-Alonso F. Canovas-Garcia C. Martinez-Ortiz C. et al.

Oral status, quality of life, and anxiety and depression in hemodialysis patients and the effect of the duration of treatment by dialysis on these variables.

Odontology. 106: 194-201https://doi.org/10.1007/s10266-017-0313-6Tai Y.H. Chen J.T. Kuo H.C. et al.

Periodontal disease and risk of mortality and kidney function decline in advanced chronic kidney disease: a nationwide population-based cohort study.

Clin Oral Investig. https://doi.org/10.1007/s00784-021-03924-6Borrell L.N. Crawford N.D.

Socioeconomic position indicators and periodontitis: examining the evidence.

Periodontol 2000. 58: 69-83https://doi.org/10.1111/j.1600-0757.2011.00416.xCugini M.A. Haffajee A.D. Smith C. Kent Jr., R.L. Socransky S.S.

The effect of scaling and root planing on the clinical and microbiological parameters of periodontal diseases: 12-month results.

J Clin Periodontol. Jan. 27: 30-36Yue H. Xu X. Liu Q. Li X. Xiao Y. Hu B.

Effects of non-surgical periodontal therapy on systemic inflammation and metabolic markers in patients undergoing hemodialysis and/or peritoneal dialysis: a systematic review and meta-analysis.

BMC Oral Health. 20: 18https://doi.org/10.1186/s12903-020-1004-1Article InfoPublication History

Accepted: June 20, 2022

Received in revised form: June 10, 2022

Received: February 23, 2022

Publication stageIn Press Journal Pre-ProofFootnotes

Conflict of interests statement

None of the authors declare any competing interests.

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DOI: https://doi.org/10.1016/j.ekir.2022.06.016

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© 2022 Published by Elsevier Inc. on behalf of the International Society of Nephrology.

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