Effect of periodontal treatment on the glomerular filtration rate, reduction of inflammatory markers and mortality in patients with chronic kidney disease: A systematic review

Théo Delbove; François Gueyffier; Laurent Juillard; Emilie Kalbacher; Delphine Maucort-Boulch; Patrice Nony; Brigitte Grosgogeat; Kerstin Gritsch

doi:10.1371/journal.pone.0245619

Abstract

Aim

To assess the effect of periodontal treatment (PT) on glomerular filtration rate (GFR), systemic inflammation, or mortality in patients with chronic kidney disease (CKD).

Methods

A literature search was performed on PubMed and Web of Science databases on articles published until December 2019. The PRISMA guidelines were used throughout the manuscript.

Results

Of the total studies found, only 18 met the inclusion criteria; four retrospective and 14 prospective studies (including 3 randomized controlled trials–RCT). After PT, 3 studies investigated GFR, 2 found significant improvement; 11 (including 2 RCTs) investigated C-reactive protein levels, 9 found a significant improvement (including the 2 RCTs); 5 (including 3 RCTs) investigated Interleukine-6 level, 4 found a significant improvement (including 2 RCTs) and 2 studies evaluated mortality, one (retrospective study) found a significant difference.

Conclusions

Within the limitations of the present study, PT seems to improve CKD status, especially by reducing the systemic inflammation. Further RCTs are needed to confirm the results and specifically assess the influence of different types of PT in CKD patients. Taking into consideration the ability of PT to prevent further tooth loss and denutrition, early management of periodontitis is extremely important in patients with impaired renal function.

Citation: Delbove T, Gueyffier F, Juillard L, Kalbacher E, Maucort-Boulch D, Nony P, et al. (2021) Effect of periodontal treatment on the glomerular filtration rate, reduction of inflammatory markers and mortality in patients with chronic kidney disease: A systematic review. PLoS ONE 16(1): e0245619. https://doi.org/10.1371/journal.pone.0245619

Editor: Bhagwan Dass, University of Florida, UNITED STATES

Received: July 7, 2020; Accepted: January 4, 2021; Published: January 22, 2021

Copyright: © 2021 Delbove et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the manuscript and its Supporting Information files.

Funding: The author(s) received no specific funding for this work.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Periodontitis is an immune-mediated inflammatory disease that is due to bacterial infection (periodontal flora), leading to the destruction of the tissues surrounding the tooth (periodontium). The global prevalence of its severe forms has been estimated to 10.8%, affecting 743 million people worldwide [1]. Both innate and adaptive immune responses are stimulated by the periodontal bacteria [2] and the release of bacterial products and inflammatory mediators from periodontal pockets result in low-grade systemic inflammation [3, 4]. Periodontitis has been most strongly associated with an increase of pro-inflammatory cytokines levels [5] and serum C-reactive protein (CRP) levels [6]. Moreover, the relationship between periodontitis and some systemic diseases has been well documented (for example periodontitis and diabetes [7, 8], periodontitis and cardiovascular diseases [9, 10]). There is also strong evidence supporting a positive association between periodontitis and chronic kidney disease (CKD) [11–13], and some studies suggest a more severe periodontal breakdown with the progression of kidney disease [14, 15], and the duration of dialysis therapy [16]. Furthermore, the risk of death is higher in haemodialysis (end-stage renal disease) patients with periodontitis than those without periodontitis [17, 18]. If relationship between these two diseases is often described, recent meta-analysis concluded that there is a need to determine whether prevention of periodontal disease or periodontal treatment can reduce the severity of CKD [11, 19]. CKD is related to many specifics markers: diagnostic of CKD is based on the glomerular filtration rate (GFR) levels, also CKD have an influence in inflammatory markers, and is related to death due to cardio-vascular disease. We aimed to systematically review all prospective and retrospective studies assessing the effect of periodontal treatment in CKD using clinical parameters, in patients suffering of periodontitis.

Materials and methods

The preferred reporting items for systematic reviews and meta-analyses (PRISMA) [20] were used as a guideline throughout the manuscript and the protocol was registered in the international prospective register of systematic reviews (PROSPERO; registration number CRD42017075376).

Study selection

The inclusion criteria were: at least one group of patients with periodontitis and CKD at any stage, including end-stage-renal disease (ESRD); any kind of PT, including oral hygiene instruction, nonsurgical or surgical treatment; and at least one of the following–renal function evaluation (i.e. GFR), inflammatory marker, or mortality.

Search strategy

A literature search was performed using two electronic databases (PubMed & Web of Science) on articles published until December 2019. Language restrictions were not applied. The keywords used in the electronic search (in “Title/Abstract” for MEDLINE database and “Topic” for Web of Science database) were as follows: periodont* AND (oral hygiene OR root planing OR treatment OR therapy) AND (end-stage renal disease OR renal failure OR chronic kidney disease OR hemodialysis OR dialysis)

Authors (TD, KG) independently reviewed and screened the title and abstract of potentially relevant records and determined final eligibility through examination of full texts. Citations were screened for additional publications that were missed by the electronic search. Review articles and short communications were excluded. Disagreements were resolved through discussion.

Data collection

Our analysis focused for each study on the protocol parameters, the assessment criteria, the comparison groups, and the biological and clinical results. To determine the bias of studies, the Cochrane risk of bias tool was used for RCTs [21]; two reviewers (TD, PN) assigned a judgment of high, low, or unclear risk of material bias for each item independently. Discrepancies about risk of each risk of bias have been resolved by discussion in the first instance; where consensus could not be reached, a third reviewer was consulted. The quality of each non-randomized study (including at least one control group) was evaluated using the Newcastle-Ottawa Scale [22]. This scale includes 3 categorical criteria with a maximum score of 9 points: the selection of the study groups; the comparability of the groups; and the ascertainment of the outcome of interest. The quality of each study was rated using the following scoring algorithms: ≥7 points was considered as “high”, 4 to 6 points was considered as “moderate”, and ≤3 point was considered as “poor” quality study.

Results

Study selection

The search identified 369 records. After removal of duplicates 277 records remained and the title and abstract of these records were assessed. A total of 257 records were rejected because they did not meet the inclusion criteria. The remaining 20 underwent full text examination: one article did not meet the inclusion criteria (publication of a future study protocol) [23] and one article was a short communication [24]; 18 studies were finally included (Fig 1) [25–42].

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Fig 1. Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram.

https://doi.org/10.1371/journal.pone.0245619.g001

Study characteristics

Type of studies.

Among the 18 included studies, 4 were retrospective [39–42], and 14 were prospective studies [25–38] including 3 RCTs (Table 1) [27, 29, 34].

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Table 1. Characteristics of the 18 included studies.

https://doi.org/10.1371/journal.pone.0245619.t001

Study design.

There were 17 studies that had an experimental group mixing renal disease, periodontitis and periodontal treatment [25–41], and one had a treatment cohort combining periodontitis and periodontal treatment and assessed the incidence and risk of ESRD in this group [42].

In prospective studies, seven did not include control groups [25, 28, 31–33, 35, 38], while the remaining 7 had at least one control group [26, 27, 29, 30, 34, 36, 37] with 3 studies including two control groups [26, 27, 30]. In these 7 studies including control groups, the experimental groups consisted of patients with renal disease (different stages), periodontitis and periodontal treatment [27, 29, 30, 34, 36, 37] or of patients with diabetes, dialysis, periodontitis and periodontal treatment [26]. In those studies, the control groups consisted of patients with periodontitis and periodontal treatment without renal disease in 4 studies [26, 27, 36, 37], patients with renal disease and periodontitis in 3 studies [29, 30, 34], patients with renal disease, periodontitis and periodontal treatment limited to oral hygiene instructions in 1 study [27], patients with diabetes, periodontal disease and periodontal treatment in one study [26] or patients with renal disease in the last study [30].

In the retrospective studies, three estimated the risk of complications of patients with end-stage renal disease, periodontitis and periodontal treatment (experimental group) versus end-stage renal disease (control group) [39–41] and the other estimated the incidence and risk of ESRD in patients with periodontitis and periodontal treatment (experimental group) versus patients with periodontal disease only (without periodontal treatment) (Table 1) [42].

Primary endpoint.

The primary endpoint of 9 studies was systemic inflammation: eight studies evaluated this using CRP or high-sensitivity CRP (hs-CRP) levels [27, 29, 31–33, 35, 36, 38] and 1 study evaluated this using interleukin-6 [34]. Five studies [30, 39–42] focused on clinical outcomes; ESRD incidence [42], the risk of hospitalization for an infectious disease [41] or cardiovascular diseases [39, 40], and mortality [30, 39, 40]. For 2 studies [28, 37], the main assessment criterion was the GFR estimated from the Modification of Diet in Renal Disease (MDRD) [28] or the Cockcroft and Gault equation [37]. Two studies did not define primary endpoint (Table 2) [25, 26].

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Table 2. Assessment criteria and improvement after PT compared to baseline in prospective studies.

https://doi.org/10.1371/journal.pone.0245619.t002

Assessment of renal disease and systemic inflammation.

To evaluate the impact of periodontal treatment on CKD, the included prospective studies evaluated 22 different criteria related to renal dysfunction and/or systemic inflammation (Table 2); the most frequently evaluated was CRP (11 studies), followed by albumin (10 studies), cholesterol (high/low-density lipoprotein, HDL/LDL) (7 studies), transferrin (6 studies), haemoglobin (6 studies), phosphate (6 studies), calcium (6 studies), parathyroid hormone (5 studies), ferritin (5 studies), IL-6 (5 studies), triglycerides (4 studies), blood urea nitrogen (4 studies), creatinine (4 studies), eGFR (3 studies), normalized protein catabolism (3 studies), tumour necrosis factor alpha (3 studies), pentraxin-3 (1 study), haematocrit (1 study), absolute lymphocyte counts level (1 study), asymmetric dimethylarginine (1 study), and mortality (1 study). The number of criteria assessed per study ranged from 1 [33] to 15 [26] (Table 2).

Periodontal assessment criteria and periodontal treatment efficacy evaluation.

For 9 of the 14 prospective studies [27–31, 33, 34, 36, 37], diagnosis of periodontitis was conducted by consensus with general chronic periodontitis defined as a CAL >4mm on 30% of affected sites [43]. Three studies [32, 35, 38], including two from the same team, used another system for diagnosis that was based on periodontal disease index (PDI) [44]. For one study [26], the clinical diagnosis of chronic periodontitis was based on the following criteria [45]; the presence of ≥ 5 teeth with ≥ 1 sites with probing depth ≥ 5 mm, clinical attachment level ≥ 2 mm, and the presence of bleeding on probing. For the last study [25], the diagnosis of periodontitis was performed according to the criteria of the American Academy of Periodontology (2017). Among the 14 prospective studies, 11 also evaluated the efficacy of the purposed periodontal treatment, measuring plaque index (PI) [25, 26, 28, 29, 31, 32, 34–37], gingival index (GI) [26, 31, 34, 36, 37], probing pocket depth (PPD) [25–29, 31, 34, 36, 37], bleeding on probing (BOP) [25–29, 31, 34, 36, 37], clinical attachment level (CAL) [25–29, 31, 34, 36, 37], or periodontal disease index (PDI) [32, 35]. Among these 11 studies, 4 showed a significant improvement of 2 criteria or less [31, 32, 34, 35], and 7 of 3 or more criteria (Table 3) [25–29, 36, 37].

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Table 3. Periodontal criteria and periodontal treatment evaluation after PT in experimental group compared to baseline in prospective studies.

https://doi.org/10.1371/journal.pone.0245619.t003

For the 4 retrospectives studies [39–42], the authors included patients who underwent for periodontal treatment. No evaluation of the periodontal treatment effectiveness was mentioned.

Clinical outcomes

Among the 11 studies evaluating CRP levels, 9 showed a significant improvement after periodontal treatment either with respect to baseline [26, 27, 29, 31–33, 35, 36, 38] or to a control group [29]. For IL-6 level, 4 studies (on 5 studies) showed a significant decrease after periodontal treatment compared to baseline [26, 27, 29, 36]. RCT studies comparing experimental groups (ESRD and periodontitis and PT) to control groups (ESRD and PT) were Fang et al. [29] and Wehmeyer et al. [34]. At 3 and 6 months after completion of periodontal treatment, a significant decrease of IL-6 level was demonstrated in the first study [29] whereas no significant differences were observed in the second one (Table 1) [34].

The two studies investigating GFR as primary endpoint found a significant increase after periodontal treatment as compared to baseline [28, 37] without significant differences between the experimental group (CKD and periodontitis and PT) and the control group (PD and PT) (Table 1) [37].

Among the 4 retrospective studies, one found that the incidence of ESRD was 37% lower in the treatment group (PD and PT) than in the non-treatment group (PD without PT) with an adjusted HR of 0.59 (95% CI = 0.46 to 0.75) [42], and the three other found that patients with ESRD and periodontitis receiving periodontal treatment had a significantly lower risk of acute and subacute infective endocarditis, pneumonia, and osteomyelitis [41], and of cardiovascular diseases and mortality [39, 40] than patients with ESRD only (Table 1).

In the prospective study investigating the effect of treatment on fatal events, no significant difference was found between the groups after adjustments for confounders (Table 1) [30].

Risk of bias

Among the 14 prospective studies, 3 were RCTs [27, 29, 34], 4 included at least one control group [26, 30, 36, 37] and 7 had no control group [25, 28, 31–33, 35, 38].

The 3 RCTs could be used for the Cochrane collaboration’s tool for assessing risk of bias in randomized trials. Two studies showed high risk of bias concerned blinding conditions (Table 4) [27, 34].

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Table 4. Cochrane risk of bias tool's table (RCT studies).

https://doi.org/10.1371/journal.pone.0245619.t004

According to the Newcastle-Ottawa Scale, the quality of the 4 prospective studies including at least one control group and of the 4 retrospective studies were considered as moderate quality [26, 30, 37] and the others as high quality [36, 39–42] (Table 5).

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Table 5. Newcastle-Ottawa quality assessment scale (studies including control groups).

https://doi.org/10.1371/journal.pone.0245619.t005

The 7 prospective studies having no control group were considered at high risk of bias.

Discussion

To the best of our knowledge, this is the first systematic review to have investigated the effect of periodontal treatment in CKD and periodontitis patients in terms of GFR, systemic inflammation, and morbidity and mortality. Some recent systematic review and meta-analysis have demonstrated an association between renal impairment and periodontitis [11, 12, 19], and pointed out the need of RCTs investigating the effect of prevention or periodontal treatment on the severity of renal dysfunction.

Among the 14 prospective studies, only 3 were RCTs and 11 were non-randomized. The objective of the 3 randomized studies was to evaluate the effect of periodontal treatment on systemic inflammation. However, the periodontal treatment differed between each study: oral hygiene instructions and non-surgical periodontal treatment or oral hygiene instructions alone [27], oral hygiene instructions and non-surgical treatment and teeth extractions if necessary [29], or oral hygiene instructions and non-surgical treatment with adjunctive local-delivery antimicrobial therapy and teeth extraction if necessary [34]. Systemic inflammation as assessed by hs-CRP [27, 29] or IL-6 [34] was the primary endpoint. Two were restricted to ESRD patients [29, 34], whereas the third study included all patients with a GFR<60 mL/min:1.73 m² [27]. Two concluded to a significant effect of the purposed treatment (even oral hygiene instructions only) after treatment compared to baseline [27, 29] or compared to the control group [29] while the third did not [34]. Despite the heterogeneity in the design of the RCTs included in this study, results supported improvement of systemic inflammation (hs-CRP) after periodontal treatment.

Furthermore, RCTs were single centre [27, 29] or single centre pilot studies [34]. Although single centre studies provide the flexibility of approach necessary for clinicians and scientists and an important source for new therapeutic ideas, they may be limited by difficulties in recruiting large numbers of participants. Another problem of such studies is the restrictive selection of studied patients that may hamper the generalization of findings.

About the 11 non-randomized prospective studies, only 4 of these included a control group [26, 30, 36, 37]. The objectives of the latter was to evaluate the effect of periodontal treatment on fatal events in ESRD patients [30], and on systemic inflammation [26, 36] or glomerular filtration rate [37] in patients with different stages of CKD undergoing conservative treatment. Despite the heterogeneity in the design of non-randomized prospective studies and therefore the difficulties to conclude on the influence of periodontal treatment on CKD, results are promising about impact of periodontal treatment on systemic inflammation and GFR.

The primary endpoint differed between studies; inflammation markers were the most frequently used. Measurement of CRP is obviously interesting owing to its association with cardiovascular disease and mortality [46], but periodontitis is an infectious disease that creates overall inflammation in active periods, including increase of CRP levels [6], and therefore improvement of inflammatory markers may not be sufficiently specific to CKD improvement. Furthermore, GFR is used to diagnose CKD and eGFR <60 ml/min/1.73 m² is associated with subsequent risk of all-cause and cardiovascular mortality, kidney failure, acute kidney injury, and CKD progression in the general population and in populations with increased risk for CVD [47]. However, this was the primary endpoint in only 2 studies. This endpoint should be measured in future studies.

In most studies, the efficacy of the purposed periodontal treatment was evaluated by measuring periodontal indices; this is a prerequisite to conclude on the influence of periodontal treatment on CKD status. However, in the included studies, the number of teeth or the capacity of chewing were not taken in account in the design of studies whereas the decrease of chewing ability will influence the diet of patients [48]. Moreover, periodontal treatment is able to prevent further tooth loss [49]. Not taking in account the number of teeth could be a bias regarding the fact that a liquid alimentation is a negative predictive risk in CKD or ESRD patients. A matching on this confounding factor can be implemented with the simple use of a questionnaire.

About the retrospectives studies, three [39–41] showed that ESRD patients receiving intensive periodontal treatment had a significantly lower risk of infections, of cardiovascular diseases and of mortality compared to those without periodontal disease. However, this could also lead to the conclusion that having a treated periodontal disease is better than no disease at all. This highlights a problem with retrospective studies for which it is practically impossible to identify and include patients who are underdiagnosed for periodontal disease.

The heterogeneity of design and protocols between studies does not allow for clear conclusions about the benefit of periodontal treatment in CKD and periodontitis patients in terms of systemic inflammation, GFR, or mortality; further methodologically robust RCTs are needed to demonstrate with a high level of evidence such potential benefit. It is of note that although there are studies that specifically investigated ESRD patients, the others did not distinguish patients on renal disease severity. Future RCTs should separate ESRD patients from those at other stages of CKD as the former are more fragile, often with haemodialysis, and are less likely to follow PTs and regular follow-up; studies including ESRD patients should assess specifically adapted therapies, e.g. prevention or oral hygiene instructions, which can be provided in haemodialysis centres. In addition, basic methodological aspects must be taken into account in order to minimize confounding bias, i.e. selection, attrition, performance, and detection bias. Randomization should include an adequate generation of allocation sequence associated with a clear concealment of allocation. When double-blinding cannot be obtained, a blinded assessment of the endpoints must be performed by a specific adjudication committee. The number of lost to follow-up must be minimized and handling of dropouts and missing data should be specified a priori in the study protocol. In order to avoid Type I Error Rate Inflation, dealing with multiplicity has to be also considered in the first versions of the protocol. Coordinated work and dialogue between nephrologist and periodontist seems obviously extremely important to set up for these future studies.

Periodontal treatment seems to improve CKD status, and results are encouraging especially for the reduction of systemic inflammation. However, further RCTs are needed to confirm these results and to specifically assess the influence of different types of periodontal treatment in CKD patients as well-documented for other systemic diseases such as diabetes [50, 51].

Supporting information

S1 Checklist. PRISMA 2009 checklist.

https://doi.org/10.1371/journal.pone.0245619.s001

(TIF)

Acknowledgments

The authors thank Philip Robinson for his careful language review.

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Figures

Abstract

Aim

Methods

Results

Conclusions

Introduction

Materials and methods

Study selection

Search strategy

Data collection

Results

Study selection

Study characteristics

Type of studies.

Study design.

Primary endpoint.

Assessment of renal disease and systemic inflammation.

Periodontal assessment criteria and periodontal treatment efficacy evaluation.

Clinical outcomes

Risk of bias

Discussion

Supporting information

S1 Checklist. PRISMA 2009 checklist.

Acknowledgments

References