The Relationship Between Oral Health
and Hemodialysis Treatment Among
Adults with Chronic Kidney Disease:
A Systematic Review
Kimberly Wallace
Saima Shafique
Ubolrat Piamjariyakul
urrently, there are over
C
760,000 Americans who have
been diagnosed with end stage
renal disease (ESRD) (United
States Renal Data System [USRDS],
2018). Of the 726,331 prevalent
patients with ESRD as of December
31, 2016 (the most recent full year data
available), approximately 468,000
(63%) were using hemodialysis as
their renal replacement therapy
(RRT) (USRDS, 2018). Chen,
Chiang, Chan, Hung, and Huang,
(2006) found that 59% of patients on
hemodialysis had moderate to severe
periodontitis. In the past, there was
limited evidence of the association
between periodontal health and
ESRD; however, more recent studies
have found a strong relationship, with
many reporting a bidirectional rela-
tionship between the two (Akar, Akar,
Carrero, Stenvinkel, & Lindholm,
2011; Ariyamuthu, Nolph, & Ring-
dahl, B., 2013; Hou et al., 2017).
Kimberly Wallace, MSN, RN, FNP-C, is a
Nephrology Nurse Practitioner, West Virginia
University Medicine, and PhD candidate, West
Virginia University School of Nursing,
Morgantown, WV.
Saima Shafique, MPH, is a PhD student in
Department of Epidemiology, West Virginia
University School of Public Health, Morgantown,
WV.
Ubolrat Piamjariyakul, PhD, RN, is the
Associate Dean for Research, West Virginia
University School of Nursing, Morgantown, WV.
Statement of Disclosure: The authors reported
no actual or potential conflict of interest in rela-
tion to this continuing nursing education activity.
Note: The Learning Outcome, additional state-
ments of disclosure, and instructions for CNE
evaluation can be found on page 395.
Nephrology Nursing Journal July-August 2019
Continuing Nursing
Education
Copyright 2019 American Nephrology Nurses Association.
Wallace, K., Shafique, S., & Piamjariyakul, U. (2019). The relationship between oral
health and hemodialysis treatment among adults with chronic kidney disease: A sys-
tematic review. Nephrology Nursing Journal, 46(4), 375-394.
Adult patients on hemodialysis experience a high prevalence of poor oral health and
periodontitis. The chronic inflammation associated with poor periodontal health can
increase the risk of cardiovascular disease and mortality among patients on hemodialy-
sis. A systematic review of research articles published from 2012-2018 was conducted to
synthesize current literature on the subject. Forty-three articles were identified. Findings
were summarized into two categories: clinical measurements and lifestyle/quality of life.
We suggest the development, implementation, and evaluation of oral health nursing
interventions and periodontal treatments among patients on hemodialysis.
Key Words: Hemodialysis, chronic kidney disease, end stage renal disease, oral
health, periodontal disease.
Periodontal disease is characterized hemodialysis has grown in the past
by chronic inflammation (Alpert, 2017), decade, including past reviews
which can increase the risk of cardio- (Ariyamuthu et al., 2013; Bossola &
vascular disease and mortality among Tazza, 2012; Craig, 2008; Ruospo et
patients undergoing hemodialysis al., 2014; Wahid, Chaudhry, Ehsan,
(Kshirsagar et al., 2007; Said & Butt, & Khan, 2013). Recent reviews
Hernandez, 2014). Poor oral health also summarized the bidirectional relation-
has a significant impact on quality of life ship between CKD and periodontal
because it can affect a person’s self-con- disease, noting a higher prevalence of
fidence; ability to eat, taste, swallow, periodontal disease in patients with
and speak (Hebling & Pereira, 2007; CKD, and identified that nonsurgical
Rodakowska, Wilczy ska-Borawska, periodontal treatment decreased over-
Fryc, Baginska, & Naumnik, 2018); and all systemic inflammatory burden in
can lead to dry mouth, gingivitis, dental patients with CKD, especially individ-
caries, alteration in salivary composi- uals undergoing hemodialysis therapy.
tion, altered taste, and pain (Gavalda et An abundance of studies completed in
al., 1999; Marinho et al., 2007; Nasci- the last six years indicates a need for
mento, Soares, Chimenos-Küstner, additional review. The purpose of this
Dutra, & Cavalcanti, 2018; Proctor, systematic literature review was to
Kumar, Stein, Moles, & Porter, 2005). identify the relationship between oral
The body of knowledge regarding health and hemodialysis treatment
oral health among patients with chron- among adults with ESRD.
ic kidney disease (CKD) who are on
Vol. 46, No. 4 375
The Relationship Between Oral Health and Hemodialysis Treatment Among Adults with Chronic Kidney Disease: A Systematic Review

Figure 1.
Selection Flow Chart According to PRISMA Statement

Records identified through

database searching
(n = 467)

Records after duplicate removal (n = 383)

Title and abstract screened Records excluded

(n = 383) (n = 340)

Full-text articles assessed for eligibility

(n = 43)
Full-text articles
excluded, with
reason; not
research study
Papers identified through (n =2); unable to
hand-searching, obtain (n = 1);
snowballing (n=6) patients not on HD
(n =1); population
without periodontal
disease (n =1);
study protocol
Studies included in synthesis (n =1)
(n = 43)

Note: HD = hemodialysis.

Literature Search
Search Strategy
This systematic review was con-
ducted using the Preferred Reporting
Items for Systematic Review and Meta-
Analyses (PRISMA) statement. The
PRISMA guidelines provide an evi-
dence-based framework on which to
report systematic review (Moher,
Liberati, Tetzlaff, & Altman, 2010).
Seven electronic databases were uti-
lized for the search: PubMed,
Academic Search Complete, CINAHL
with full text, HAPI, Health Source:
Nursing/Academic Edition, Psyc
Articles, and PsycInfo. Search terms
included ‘oral health OR oral hygiene
OR dental health OR periodontal’
and ‘hemodialysis OR haemodialysis
OR dialysis.’
The search was limited to scholar-
ly, peer-reviewed, full-text articles of
both quantitative and qualitative stud-
ies published between 2012-2018 that
were available in the English lan-
guage. The search was limited to stud-
ies including patients on hemodialysis
aged 18 years and older, and exclud-
ing articles focused on peritoneal dial-
ysis or renal transplant recipients. The
second reviewer used the same search
strategy and inclusion/exclusion crite-
ria. After completion of independent
article selection, articles were
reviewed and added to the study by
mutual agreement.
A total of 467 articles were
returned in the database search. After
removal of duplicate articles, the
abstracts of 383 articles were reviewed
per inclusion and exclusion criteria.
During the abstract review, 340 arti-
cles were excluded because they did
not meet inclusion criteria. Through
snowballing, six additional articles
were identified. This strategy was
completed to minimize the risk that
relevant papers were accidentally
omitted from the search. A total of 43

376 Nephrology Nursing Journal July-August 2019 Vol. 46, No. 4

studies, all of which were quantitative
in methodology, met inclusion criteria
and were included for this systematic
review (see Figure 1).
Included articles were read in their
entirety before abstraction and syn-
thesis. Data regarding study design,
sample, and findings were extracted
using an extraction form designed by
the authors. Data were abstracted on
the following subjects: country of ori-
gin, sample size, purpose, participant
characteristics including age and gen-
der, study design, and findings (see
Table 1).
Results
Forty-three studies were reviewed,
including a total of 17,135 adult partic-
ipants. The majority of the studies uti-
lized cross-sectional and observational
methods. Three were randomized
controlled trials (RCTs), and one was
interventional without randomization.
In addition, three case-control and six
cohort studies were also included.
Findings were summarized into two
categories: 1) clinical measurements
and 2) lifestyle/quality of life. Clinical
measurements were characterized by
periodontal measurements and symp-
toms, inflammatory and nutritional
markers, salivary flow rate, and the
decayed, missing, and filled teeth
index. Lifestyle and quality of life
were characterized by lifestyle choices
and interventions, and oral and gener-
al health-related quality of life
(HRQoL).
Clinical Measurements
Periodontal measurements and
symptoms. In patients undergoing
hemodialysis, the following periodon-
tal measurements and symptoms
increased:
• Clinical attachment level (Brito et
al., 2012; Jain et al., 2014; Limeres
et al., 2016).
• Dental caries (Pakpour, Kumar,
Fridlund, & Zimmer, 2015).
• Visual plaque index (Pakpour et
al., 2015).
• Gingival index (Kim et al., 2017;
Limeres et al., 2016; Pakpour et al.,
2015).
• Bleeding on probing (Tiwari et al.,
2013).
• Dental calculus (Limeres et al.,
2016; Tiwari et al., 2013).
• Probing pocket depth (Limeres et
al., 2016; Pakpour et al., 2015).
• Community periodontal index
(Gautam et al., 2014; Nascimento
et al., 2018, Zhao et al., 2014).
• Periodontal disease index (Veisa et
al., 2017).
• Tongue biofilm and oral mucosa
alterations (Silva et al., 2017).
Longer hemodialysis duration was
also found to be associated with high-
er clinical attachment level (Andrade
et al., 2017; Jenabian, Mirsaeed,
Ehsani, & Kiakojori, 2013; Sekiguchi,
Pannuti, Silva, Medina-Pestana, &
Romito, 2012), and worse values of
probing depth, plaque index, and gin-
gival index (Sekiguchi et al., 2012).
Jenabian and colleagues (2013) identi-
fied that the plaque index and probing
pocket depth increased with age.
However, this study also identified
that the gingival index and clinical
attachment level were not significantly
increased with age.
Zhao and colleagues (2014) report-
ed severe periodontitis and periodon-
tal bone loss for patients on hemodial-
ysis when compared to general popu-
lation control. Individuals with peri-
odontitis showed worse values of peri-
odontal disease, clinical attachment
level, bleeding on probing, visual
plaque index, and gingival index
(Rodrigues et al., 2014). In an inter-
ventional study, periodontal treatment
improved mean probing depth, the
extent of probing depth, and extent of
the gingival index at three months,
but the difference between treatment
and no treatment was no longer pres-
ent at six months (Wehmeyer et al.,
2013).
Patients with diabetes mellitus had
a significantly higher prevalence of
dysgeusia (altered taste), dry mouth,
and increased pocket depth as com-
pared to patients without diabetes
who had high levels of mucosal
petechiae (Nascimento et al., 2018;
Swapna et al., 2013). Patients with
increased fasting blood glucose levels
were more likely to develop periodon-
tal disease (Hou et al., 2017). Patients
with diabetic nephropathy who were
undergoing hemodialysis had fewer
teeth and worse symptoms of peri-
odontal health and xerostomia com-
pared with those with chronic
glomerulonephritis (Teratani et al.,
2013). Intensive periodontal disease
treatment was found to be associated
with a reduction in overall infectious
diseases and infection-related hospital-
ization among patients on hemodialy-
sis (Huang, Lin, Yu, Wu, & Koo, 2015).
Inflammatory and nutritional
markers. One study found that high-
sensitivity C-reactive protein (hs-
CRP) levels were independently asso-
ciated with regular tooth brushing in
patients on hemodialysis (Afsar, 2013).
Hou and colleagues (2017) found that
hs-CRP was associated with periodon-
tal disease, while no significant differ-
ence in serum calcium and phospho-
rus levels was found between patients
with and without periodontal disease
who were undergoing hemodialysis
treatment. Higher serum calcium had
a protective effect against periodontal
disease; thus, a higher calcium intake
might help decrease periodontal dis-
ease prevalence in patients on mainte-
nance hemodialysis. Phosphorus levels
were higher among patients undergo-
ing hemodialysis treatment (Cholewa,
Madziarska, & Radwan-Oczko, 2018;
Rodrigues et al., 2014). In individuals
with periodontitis, albumin levels
were lower (Palmer et al., 2016), and a
strong negative correlation between
the number of teeth and serum CRP
was also observed (Cholewa et al.,
2018).
Fang and colleagues (2015) found
that inflammatory and nutritional
markers were improved after non-sur-
gical periodontal therapy. Wehmeyer
and colleagues (2013) found that treat-
ment of periodontitis in patients
receiving hemodialysis improved clin-
ical measurements of periodontitis
severity but did not produce an
observable impact on serum markers
of inflammation. Yazdi, Karimi,
Rasouli, and Roozbeh (2013) identi-
fied that eight weeks after non-surgical
periodontal treatment, CRP levels
were significantly lower. However,

Nephrology Nursing Journal July-August 2019 Vol. 46, No. 4 377

 Table 1

378
Literature Matrix of Included Studies

Author/
Year/
Country Design Purpose (N) Gender/Age/Mean Findings
Afsar (2013) Cross-sectional Determine regular tongue Male, n=73 HRQoL better in patients with regular tongue biofilm compared to
Turkey (N=135) biofilm frequency in patients on Female, n=62 patients without regular tongue biofilm.
HD and determine factors Mean age=52.4 years Depressive behavior, cognitive function, educational status, and
related with regular tongue high sensitivity CRP levels were independently associated with
biofilm in patients on HD. regular tongue biofilm in patients on HD.

Andrade et al. Cross-sectional Evaluate and compare the Group 1: Poor oral health indicators may be a reflection of unsatisfactory
(2017) (N=60 in Group quality of life and oral health Male, n=30 overall quality of life in patients undergoing HD for a prolonged
Brazil 1, <4 years HD, indicators in patients Female, n=30 period of time.
N=40 in group undergoing HD considering the Mean age=39.75 years
2, >4 years HD) influence treatment duration.
Group 2:
Male, n=19
Female, n=21
Mean age=41.58
Belazelkovska Cross-sectional Find the association between Male, n=38 Lowest SFR among individuals undergoing HD compared to
et al. (2014) (N=30 patients salivary flow rate and oral Female, n=52 healthy individuals and renal transplant patients.
Macedonia on HD) clinical findings in patients with Mean age = 46 years Negative correlation between thirst, xerostomia, and burning
CKD. tongue, and unstimulated salivary flow and patients on HD.
Negative correlation between uremic fetor, dry fissured lips,
petechiae, and ecchymoses among patients who are pre-dialysis,
on HD, and with renal transplant.
Brito et al. Cross-sectional Determine the extent and Male, n=21 Patients who are pre-dialysis and patients on HD had more sites
(2012) (N=40 patients severity of periodontitis in Female, n=19 with CAL than healthy individuals.
Brazil on HD) patients with CKD undergoing Mean age=50 years More cases of severe chronic periodontitis in patients who are
pre-dialysis, CAPD, or HD, and predialysis or on HD as compared to healthy individuals and those
to compare findings with those with CAPD.

Nephrology Nursing Journal

from systemically healthy
subjects.
Chhokra, Cross-sectional Evaluate the clinical periodontal Male, n=13 Supports link between patients with ESRD receiving HD and poor
Manocha, (N=40) status of ESRD patients Female, n=27 plaque, gingival, and periodontal status.
Dodwad, undergoing HD for exploring the Mean age=38 years
Gupta, &  underlying association between
Vaish (2013) renal failure and periodontal

July-August 2019
India disease.

continued on next page

The Relationship Between Oral Health and Hemodialysis Treatment Among Adults with Chronic Kidney Disease: A Systematic Review

Vol. 46, No. 4

 Table 1 (continued)
Literature Matrix of Included Studies

Author/
Year/
Country Design Purpose (N) Gender/Age/Mean Findings
Cholewa et al. Cross-sectional Analyze the association Dentate: High prevalence and severity of periodontal disease are observed
(2018) (Dentate, between periodontal conditions Male, n=60 in patients on HD.
Poland N=103; and inflammation, nutritional Female, n=43
Edentulous, status, and calcium-phosphate Mean age=63 years

Nephrology Nursing Journal

N=25) metabolism disorders in patients
on HD. Edentulous:
Male, n=7
Female, n=18
Mean age=74
de Souza et Prospective Assess the prevalence and Male, n=79 Poor oral health was prevalent among patients on HD.
al. (2014) cohort (N=122) impact of oral health parameters, Female, n=43

July-August 2019
Low frequency of dental visits, lack of dental floss use, elevated
Brazil periodontitis, and its treatment Mean age=50 years DFMT index, and the presence of chronic periodontitis were
on survival in a group of patients significantly associated with high mortality.
undergoing HD.
Identified possible increase in survival among patients treated for
chronic periodontitis. However, did not maintain significance after
adjusting for confounders.

Vol. 46, No. 4

Fang et al. Randomized Determine the impact of non- Male, n=28 Non-surgical periodontal therapy of periodontitis in patients with
(2015) parallel control surgical periodontal therapy on Female, n=20 ESRD improved clinical measures of periodontitis severity.
China study (N= 48 in clinical measures of Mean age=53.71 years Inflammatory and nutritional markers were significantly improved
intervention periodontitis severity. after non-surgical periodontal therapy.
group) Determine the impact of non- Patients with ESRD receiving periodontal therapy had a reduction
surgical periodontal therapy on in inflammation as compared to control group.
systemic inflammatory,
nutritional, and lipid profiles. Lipids did not differ between intervention and control group.

Gautam et al. Cross-sectional Evaluate the effect of chronic Male, n=167 There is greater deterioration of periodontal health among patients
(2014) (N=206) renal failure on oral health in Female, n=39 with CKD on dialysis.
India patients on HD. Mean age=46.79 years
Assess and improve awareness
of staff regarding oral health
care of the patients in HD unit.

continued on next page

379
 Table 1 (continued)

380
Literature Matrix of Included Studies

Author/
Year/
Country Design Purpose (N) Gender/Age/Mean Findings
Hajian-Tilaki, Cross-sectional Determine the dental and Male, n=77 As age increases, DMFT index scores get higher, and oral health
Oliae, (N=145) periodontal health status, the Female, n=68 and periodontal status declines.
Jenabian, self-perceived oral health, Mean age=58.17 years No significant differences between periodontal indexes, DMFT, and
Hajian-Tilaki, & attitude toward oral health, and OHI-S with the HD duration.
Motallebnejad the effect of oral health on
(2014) quality of life in patients on HD Mean DMFT score was significantly higher among patients with
Iran in Babol. diabetes.
HRQoL not significantly impacted by poor oral health.
Hou et al. Retrospective Explore characteristics and Male, n=79 Diabetes, total cholesterol, high sensitivity CRPs, and peripheral
(2017) cohort (N=136) relevant risk factors of Female, n=57 WBC were independent risk factors, whereas tooth brushing twice
China periodontal disease among Mean age=50.8 years a day and serum calcium were protective factors against
patients on HD. periodontal disease for patients on HD.

Huang et al. Retrospective Investigate the relationship Male, n=2016 Intensive periodontal treatment is associated with a significant risk
(2015) cohort (N=4,451) between intensive PD therapy Female, n=2435 reduction in major infectious complications in patients on HD with
Taiwan and clinical infectious outcomes Mean age=58.3 years periodontal disease.
in patients on HD.
Iwasaki et al. Retrospective Evaluate the potential Male, n=131 Participants with periodontal disease had a significantly higher risk
(2018) cohort (N=211) association of periodontal Female, n=80 of pneumonia mortality than those without periodontal disease.
Japan disease with pneumonia Mean age=52.2 years
mortality in patients on HD.

Jain et al. Cross-sectional Assess the effect of duration of Male, n=268 Loss of attachment scores were significantly higher among
(2014) (N=400 in inter- HD therapy and the underlying Female, n=132 patients on HD as compared to control group.
India vention group) kidney disease on dental health Mean age=51.33 years Dental caries prevalence was significantly higher among patients
status of patients undergoing on HD as compared to healthy controls.
HD at various dialysis centers of
multispecialty hospitals in Delhi, Oral hygiene index scores were higher among patients on HD, but

Nephrology Nursing Journal

and to make appropriate not statistically significant.
recommendations and Prosthetic needs were significantly higher among patients on HD,
suggestions for improving their and prosthetic needs increased significantly with duration of
oral health. dialysis
Jenabian et Cross-sectional Investigate the duration of HD Male, n=63 PI and PPD increased significantly with age, but in the increase in
al. (2013) (N=115) on the periodontal status of Female, n=52 GI and CAL was not significant.
Iran patients in Babol, north of Iran. Mean age=47.9 years Silness-Loe plaque index, Loe and Silness gingival index, GI, CAL,

July-August 2019
and PPD were all significantly increased with longer dialysis
duration.

continued on next page

The Relationship Between Oral Health and Hemodialysis Treatment Among Adults with Chronic Kidney Disease: A Systematic Review

Vol. 46, No. 4

 Table 1 (continued)
Literature Matrix of Included Studies

Author/
Year/
Country Design Purpose (N) Gender/Age/Mean Findings
Kaushik et al. Cross-sectional Assess the oral and salivary Male, n=61 Mean salivary flow rate of unstimulated and stimulated whole
(2013) (N=100) changes (flow rate, pH, and Female, n=39 saliva was significantly lower in patients with ESRD compared to
India buffer capacity) in patients with controls.
ESRD on HD. pH and buffer capacity of the unstimulated whole saliva in patients

Nephrology Nursing Journal

with ESRD were significantly higher than in controls.
pH and buffer capacity of the stimulated whole saliva of patients
with ESRD did not show significant differences compared to
controls.
Kim et al. Cross-sectional Establish a profile of periodontal Male, n=71 Most patients with CKD presented with periodontal disease,
(2017) (N=107) conditions in patients with CKD Female, n=44 indicating the presence of chronic inflammatory and infection

July-August 2019
Brazil on HD and their periodontal Mean age=47.3 years process that may influence in systemic conditions.
risk.

Książek, Cross-sectional Determine the relationship Male, n=59 Lower concentrations of phosphate marked before HD and higher
Żołnierz, & (N=124) between Application Female, n=65 iron levels contributing to maintaining optimal interdental hygiene in
Sak (2016) Programming Interface and the Mean age = 65.4 years patients treated with RRT.

Vol. 46, No. 4

Poland quality of life and biochemical Normalization of biochemical parameters of calcium-phosphate
parameters of the calcium, and iron metabolism promotes a sense of better quality of life
phosphate, and iron among patients on chronic HD.
metabolism.
Higher calcium levels both before and after HD promote a better
sense of quality of life in terms of physical health.
Higher concentrations of iron and transferrin favor a better sense
of the quality of life both in terms of physical health and in general.
The level of interdental hygiene does not distinguish between
general indicators of the sense of quality of life.

continued on next page

381
 Table 1 (continued)

382
Literature Matrix of Included Studies

Author/
Year/
Country Design Purpose (N) Gender/Age/Mean Findings
Limeres et al. Cross-sectional Evaluate the prevalence and Male, n=18 Total number of decayed teeth was lower in patients with ESRD.
(2016) (N=44) aetiopathogenesis of edentulism Female, n=26 Higher levels of supragingival bacterial plaque, dental calculus
Portugal in patients on HD. Mean age=69.8 years deposits, gingival inflammation, saliva concentrations of creatinine,
urea, sodium, potassium, chloride, and calcium concentrations
were detected in the study group.
Depth of periodontal pockets and CAL measurements were higher
in patients with ESRD.
Saliva volume was lower in patients with ESRD.
Level of amylase is higher in patients with ESRD.
Statistically significant relationship between number of missing teeth
and supragingival plaque, gingival inflammation, PPD, and CAL.
Statistically significant positive correlations between number of lost
teeth and saliva concentrations of potassium and calcium.
Marques, Cross-sectional Identify HD-related factors Male, n=66 Serum urea, ca x Pi product, and use of sevelamer were
Libōrio, & (N=128) associated with reduced SFR. Female, n=62 independently associated with low SFR.
Lima Saintrain Mean age=56.2 years Diabetes and age greater than 65 years were associated with
(2014) reduced SFR.
Brazil
Men had higher SFR than women.
No difference in SFR according to smoking status or between
patients undergoing HD session in the morning or the afternoon.

Nascimento et Cross-sectional Determine oral health conditions Male, n=48 Patients with CKD undergoing HD may present a high amount of
al. (2018) (N=74) and oral symptoms of patients Female, n=26 dental calculus, even when low amount of dental biofilm is
Brazil with CKD undergoing HD. Mean age=50.7 years observed, as well as high percentage of symptoms of oral
discomfort.

Nephrology Nursing Journal

Pakpour et al. Case control Assess the influence of oral Male, n=322 Patients on HD had higher caries, VPI, and GI values as
(2015) (N=512) health status and socio- Female, n=190 compared to controls.
Iran behavioral variables on Mean age=57.7 years Patients on HD had poor OHRQoL and GHRQoL compared to
OHRQoL in a sample of Iranian healthy subjects.
patients on HD.
Regular tooth brushing, non-smoking, and dental visits in previous

July-August 2019
6 months were predictors for better OHRQoL among patients on
HD.
Pockets deeper than 4 mm were more frequent among patients on
HD.
The Relationship Between Oral Health and Hemodialysis Treatment Among Adults with Chronic Kidney Disease: A Systematic Review

Vol. 46, No. 4

continued on next page
 Table 1 (continued)
Literature Matrix of Included Studies

Author/
Year/
Country Design Purpose (N) Gender/Age/Mean Findings
Palmer et al. Prospective Assess all cause and Male, n=2,426 Edentulism and extensive dental disease were associated with
(2015) multinational cardiovascular mortality at 12 Female, n=1,779 increased mortality.
France, cohort (N=4,205) months after dental Mean age=61.6 years Dental flossing, using mouthwash, brushing teeth daily, spending
Hungary, Italy, assessment. 2 minutes or more on oral hygiene, changing a toothbrush every

Nephrology Nursing Journal

Poland, 3 months, and visiting a dentist within the past 6 months were
Portugal, associated with longer survival.
Spain,
Argentina Age at which patient first consulted a dental practitioner is not
associated with either all-cause of cardiovascular mortality.
DMFT index showed a dose-response relationship with all-cause
and cardiovascular mortality.

July-August 2019
Association of edentulism and DMFT index with all-cause and
cardiovascular mortality was stronger in adults greater than 60
years of age.
Palmer et al. Cross-sectional Assess the prevalence and Male, n=2426 Women had more extensive dental disease, while men more
(2016) (N=4,205) severity of oral diseases among Female, n=1779 frequently had moderate to severe periodontitis.

Vol. 46, No. 4

France, adults treated with HD. Mean age=61.6 years Adults with higher income had more filled teeth than those with
Hungary, Italy, lower income.
Poland,
Portugal, Extent and severity of dental and periodontal disease increased
Spain, with age, although enamel hypoplasia was more frequent in
Argentina younger adults.
Less frequent teeth brushing was associated with a higher number
of DMFT.
Male sex and lower albumin were independently associated with
moderate to severe periodontitis, whereas social and clinical
characteristics were not.
Parkar & Cross-sectional Assess the periodontal status Male, n=114 Periodontal status was poor among patients receiving HD as
Ajithkrishnan (N=152) among group of patients Female, n=32 compared to healthy control group.
(2012) receiving HD. Mean age=37.22 years Higher prevalence of periodontal diseases in patients with CKD
India due to failure of oral hygiene rather than chronic uremia in this
population.

continued on next page

383
 Table 1 (continued)

384
Literature Matrix of Included Studies

Author/
Year/
Country Design Purpose (N) Gender/Age/Mean Findings
Rodakowska Cross-sectional Determine OHRQoL in patients Mean age=63.2 years Patients on HD had an unsatisfactory oral status, but using only
et al. (2018) (N=72) on HD and estimate which the OHRQoL scale was insufficient to capture all their oral health
Poland scale describing OHRQoL, Oral problems. In this study, more variables were significantly related to
Health Impact Profile (OHIP-14) the OHIP-14 scale than to the GOHAI scale. Thus, the OHIP-14
or Geriatric/General Oral Health scale may be more useful in assessing OHRQoL in patients on HD.
Assessment Index (GOHAI),
was more useful in this
particular group.
Rodrigues et Cross-sectional Investigate the association Male, n=45 Individuals with periodontitis showed worse values of periodontal
al. (2014) (N=96) between periodontal status and Female, n=51 disease, CAL, bleeding on probing, visible plaque, and GI.
Brazil serum biomarkers levels in Mean age=39.8 years In the group with periodontitis, serum albumin was significantly
patients on HD. lower, and serum phosphorus was significantly higher.
Ruospo et al. Prospective Determine whether oral disease Male, n=2426 In contrast to the general population, periodontitis does not appear
(2017) cohort study was associated with all-cause Female, n=1779 to be associated with an increased risk of early death in adults
France, (N=4,205) and cardiovascular mortality in Mean age=61.6 years treated with HD.
Hungary, Italy, adults treated with HD.
Poland,
Portugal,
Spain,
Argentina

Schmalz et al. Cross-sectional Examine the OHRQoL, dental Male, n=54 DMFT higher in patients on HD compared to healthy controls and
(2016) (N=87) and periodontal health, as well Female, n=33 renal transplant recipients.
Germany as their impact on OHRQoL in Mean age=60.98 years No significant difference among DMFT index between transplant
patients on HD or with kidney and healthy controls.
transplant in comparison with
healthy controls. F-T scores were higher in healthy controls compared to HD and
renal transplant. No significant difference between HD and renal

Nephrology Nursing Journal

transplant in F-T.
OHIP scores between HD, renal transplant, and health controls
were not statistically significant.
In the HD group, only patients with DM had higher OHIP scores.

continued on next page

July-August 2019
The Relationship Between Oral Health and Hemodialysis Treatment Among Adults with Chronic Kidney Disease: A Systematic Review

Vol. 46, No. 4

 Table 1 (continued)
Literature Matrix of Included Studies

Author/
Year/
Country Design Purpose (N) Gender/Age/Mean Findings
Sekiguchi et Cross-sectional Evaluate how oral health is Male, n=51 Probing depth and CAL were statistically significant greater in
al. (2012) (N=94) affected by the length of time a Female, n=43 patients on HD longer than 3 years.
Brazil patient has been receiving HD No significance between groups in regard to tooth brushing
treatment. frequency, dental floss use, and time since last dental visit.

Nephrology Nursing Journal

Individuals on HD longer than 3 years had higher prevalence of
decayed teeth and larger DFMT index.
Length of time subjects were on HD was significantly correlated
with CAL and decayed teeth.
Silva et al. Cross-sectional Evaluate OHRQoL of Brazilians Male, n=134 Old age, living in rural areas, and tooth pain in last 6 months may
(2017) (N=226) undergoing HD and to identified Female, n=92 influence the OHRQoL of patients undergoing HD.

July-August 2019
Brazil associated factors. Mean age=55.52 years

Soroye & Cross-sectional Evaluate the periodontal status Male, n=42 Periodontal disease is common, prevalent, and unrecognized
Ayanbadejo (N=65) of those with kidney disease Female, n=23 among patients with CKD and patients on HD.
(2016) and assess their treatment Mean age=45.14 years

Vol. 46, No. 4

Nigeria need.

Swapna et al. Cross-sectional Assess oral and dental health Male, Nondiabetic Dysgeusia, dry mouth was significantly more prevalent in patients
(2013) (N=97) status of diabetic uremic n=30, Diabetic n=32 without diabetes mellitus.
India patients who undergo HD. Female, Nondiabetic Mucosal petechiae was higher among patients without diabetes
n=20, Diabetic n=15 mellitus
Mean age=55.34
nondiabetic, 53.78 DMFT significantly higher among patients with diabetes mellitus.
diabetic Increased pocket depth in patients with diabetes mellitus.

Teratani et al. Cross-sectional Clarify differences in oral health Male, n=135 Patients on HD with diabetic nephropathy were found to have
(2013) (N=98) status between patients who Female, n=84 fewer teeth ad worse symptoms of periodontal health and
Japan need HD owing to diabetic Mean age=65.2 years xerostomia compared with those with chronic GN and with the
nephropathy and chronic control subjects not undergoing HD.
glomerulonephritis. Oral health of patients on HD with chronic GN was similar to that
of control subjects for symptoms related to xerostomia.
Tiwari et al. Matched case Compare prevalence of caries Male, n=28 Bleeding on probing and calculus were higher among HD group.
(2013) control (N=30 and periodontal status among Female, n=2 DMFT was greater among individuals on HD.
India patients on HD) patients on renal dialysis with
healthy individuals.

continued on next page

385
 Table 1 (continued)

386
Literature Matrix of Included Studies

Author/
Year/
Country Design Purpose (N) Gender/Age/Mean Findings
Veisa et al. Cross-sectional Explore the link between Male, n=44 The study showed a high prevalence and severity of periodontal
(2017) (N=101) periodontal disease and quality Female, n=57 disease. The gingival and periodontal index was associated with
Romania of life, assessed with the Short Mean age=52.5 years low QoL on both physical and mental components.
Form 36-Item Health Survey in
patients on HD.

Wehmeyer et Randomized Examine the effect of Control group At 3 months, statistically significant improvement for treatment
al. (2013) controlled trial periodontal treatment in patients Male, n=18 group compared to control group in mean probing depth, extent of
United States (N=51) receiving outpatient HD. Female, n=8 probing depth, and extent of gingival index.
Mean age=52.7 years At 6 months, difference between groups was no longer present for
any variable except for extent of probing depth.
Treatment group
Male, n=15 No difference in serum albumin or high sensitivity IL-6 level at any
Female, n=10 time.
Mean age=54.1 years Treatment of periodontitis in patients on HD improved clinical
measurements of periodontitis severity but did not produce an
observable impact on serum markers of inflammation.

Wilczyńska- Cross-sectional Evaluate and compare HGF Male, n=19 Higher HGF level in saliva of patients on HD compared with
Borawaska et (N=26 patients level in unstimulated mixed Female, n=7 healthy controls.
al. (2012) on HD) saliva of three groups of Mean age=57 years GI and PBI values were higher in patients on HD as compared to
Poland patients with CRF (patients on patients on CAPD.
HD or CAPD, and patients with
CKD undergoing conservative HGF is probable cause of considerable intensity of periodontal
treatment. disease in patients on HD.
Compare HGF level in saliva of
the above-mentioned patients in
relation to patients with
periodontal disease without

Nephrology Nursing Journal

CRF and other coexisting
diseases and to healthy
subjects without periodontal
disease.
Determine the correlation
between HGF level in saliva and
the progression of periodontal

July-August 2019
disease in the above-mentioned
groups of patients with renal
failure, as well as in the general
population of subjects with
periodontal disease.
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Vol. 46, No. 4

continued on next page
 Table 1 (continued)
Literature Matrix of Included Studies

Author/
Year/
Country Design Purpose (N) Gender/Age/Mean Findings
Xie et al. Cross-sectional Evaluate the oral health status Male, n=165 14% of patients thought kidney disease was more important than
(2014) (N=306) of Chinese patients on HD. Female, n=141 oral health.
China Mean age=58.09 years 19.5% of patients could not obtain proper dental service due to
rejection of the dentist.

Nephrology Nursing Journal

2% hid their history of kidney disease in order to see dentist.

Yazdi et al. Interventional Evaluate the impact of Male, n=52 CRP level did not show significant relation to severity of
(2013) (N=77) nonsurgical periodontal Female, n=25 periodontitis not to the BI.
Iran treatment on the serum levels of Mean age=44.35 years Eight weeks after treatment, mean CRP was significantly lower;
CRP in patients with CKD who however, there was no significant difference in the severity of
are on HD.

July-August 2019
periodontitis.

Yu et al. Single blind Investigate using a mouthwash Male, n=61 Pure water and licorice mouthwash improved unstimulated whole
(2016) randomized as a means to reduce Female, n=61 SFR.
Taiwan (N=122) xerostomia and improve saliva Mean age=60.8 years Licorice mouthwash reduced xerostomia while pure water did not.
flow rates in patients on HD.

Vol. 46, No. 4

Zhao et al. Case control Investigate the periodontal Male, n=59 Compared with the generally healthy population, periodontitis and
(2014) (N=102) status in Chinese patients on Female, n=43 periodontal bone loss were significantly more severe in Chinese
China HD and assess periodontal Mean age=58.4 years patients undergoing HD.
bone loss using cone-beam
computerized tomography.
Ziebolz, Cross-sectional Determine oral hygiene Male, n=31 Patients with a high proportion of missing teeth investigated had a
Fischer, (N=54) behavior and the oral health Female, n=23 good level of caries restoration. Visually evaluated, the gingiva
Hornecker, & condition of patients on HD who Mean age=63.9 years showed only a low level of inflammatory changes.
Mavsberg. were being treated at two
(2012) dialysis centers in Germany.
Germany

Notes: TB = tongue biofilm, HD = hemodialysis, CKD = chronic kidney disease, CAPD = continuous ambulatory peritoneal dialysis, ESRD = end stage renal disease,
PD = peritoneal dialysis, CRP = C-reactive protein, SFR = salivary flow rate, OHRQoL = oral health-related quality of life, HGF = hepatocyte growth factor, CRF = chronic
renal failure, CAL = clinical attachment level, DFMT = decayed/missing/filled teeth, OSH-I = Simplified Oral Hygiene Index, HRQoL = health-related quality of life,
GHRQoL = general health-related quality of life, WBC = white blood count, PPD = probing pocket depth, PI = plaque index, GI = gingival index, BI = bleeding index,
RRT = renal replacement therapy, VPI = visible plaque index, FT = filled teeth, OHIP = oral health impact profile, PBI = papillary bleeding index.

387
 Table 2

388
Results of Critical Appraisal of Cross-Sectional Studies

Selection Outcome
Comparability
Representativeness Sample Non- Ascertainment Based on Design and Assessment Statistical
Study (First Author) Study Design of the Sample Size Respondents of Exposure Analysis of Outcome Test
Afsar et al. (2013) Cross-sectional * * ** ** ** *
Andrade et al. (2017) Cross-sectional * * ** * ** *
Belazelkovska et al. (2014) Cross-sectional * * ** * ** *
Brito et al. (2012) Cross-sectional * * ** ** *
Chhokra et al. (2013) Cross-sectional * * ** * ** *
Cholewa et al. (2018) Cross-sectional * * ** * ** *
Gautam et al. (2014) Cross-sectional * * ** * ** *
Haijan et al. (2014) Cross-sectional * * * ** * ** *
Jain et al. (2014) Cross-sectional ** * ** ** *
Jenabian et al. (2013) Cross-sectional * * * *
Kaushik et al. (2013) Cross-sectional ** * ** *
Kim et al. (2017) Cross-sectional * * ** ** *
Ksiązek et al. (2016) Cross-sectional * *
Limeres et al. (2016) Cross-sectional * * * ** *
Marques et al. (2014) Cross-sectional * * ** * *
Nascimento et al. (2018) Cross-sectional * * ** ** *
Palmer et al. (2016) Cross-sectional * * ** ** *
Parkar et al. (2012) Cross-sectional * ** ** *
Rodakowska et al.(2018) Cross-sectional * * * ** ** *
Rodrigues et al. (2014) Cross-sectional * ** * ** *
Schmalz et al. (2016) Cross-sectional * * ** * *
Sekiguchi et al. (2012) Cross-sectional * ** * * *

Nephrology Nursing Journal

Silva et al. (2017) Cross-sectional * * * ** * ** *
Soroye et al. (2016) Cross-sectional * * * * *
Swapna et al. (2013) Cross-sectional * * * **
Teratani et al. (2013) Cross-sectional ** * ** *
Veisa et al. (2017) Cross-sectional * * * ** ** *

July-August 2019
Wilczyńska-Borawaska et al. (2012) Cross-sectional * * ** *
Xie et al. (2014) Cross-sectional * * ** *
Ziebolz et al. (2012) Cross-sectional * * ** ** *
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Vol. 46, No. 4

 Table 3
Results of Critical Appraisal of Cohort Studies

Selection Outcome

Was Follow-Up
Selection of Demonstration that Outcome Comparability Long Enough for
Representativeness Non-Exposed Ascertainment of Interest Was Not Present Based on Design Assessment Outcomes to Adequacy of
Study (First Author) Study Design of Exposed Cohort Cohort of Exposure at Start of Study and Analysis of Outcome Occur? Follow Up
de Souza et al. (2014) Prospective * * * * ** * * *
Hou et al. (2017) Retrospective * * * ** ** *

Nephrology Nursing Journal

Huang et al. (2015) Retrospective * * * * ** * * *
Iwasaki et al. (2018) Prospective * * * * * * * *
Palmer et al. (2015) Prospective * * * * ** * * *
Ruospo et al. (2017) Prospective * * * * ** * * *

July-August 2019
Table 4
Results of Critical Appraisal of Case Control Studies

Selection Exposure

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Adequacy of Comparability Same Method of
Case Representativeness Selection of Definition of Based on Design Ascertainment Ascertainment for Cases Non-Response
Study (First Author) Study Design Definition of Cases Controls Controls and Analysis of Dxposure and Controls Rate
Pakpour et al. (2015) Case control * * * * ** *
Tiwari et al. (2013) Case control * * ** *
Zhao et al. (2014) Case control * * * ** * * *

Table 5
Results of Critical Appraisal of Experimental Studies

Selection Bias Performance Bias Detection Bias Attrition Bias Reporting Bias

Blinding of
Random Sequence Allocation Participants and Blinding of Incomplete Selective
Study (First Author) Study Design Generation Concealment Personnel Outcome Outcome Data Reporting Other
Fang et al. (2015) RCT Low Low Low Unclear Low Unclear Low
Wehmeyer et al. (2013) RCT Low Low Low Low Low Low Low
Yazdi et al. (2013) Interventional High High High High High Low Unclear
Yu et al. (2016) RCT Low High Unclear Low Unclear Low Unclear

389
The Relationship Between Oral Health and Hemodialysis Treatment Among Adults with Chronic Kidney Disease: A Systematic Review
there was no significant impact on the
severity of periodontitis.
Salivary flow rate. Xerostomia
(dry mouth) is a common symptom
among patients on hemodialysis
(Curtin, Bultman, Thomas-Hawkins,
Walters, & Schatell, 2002) and can be
measured by assessing salivary flow
rate. Low salivary flow rate con-
tributes to xerostomia, which can lead
to oral lesions, dysphagia, and ill-fit-
ting dental prosthetics. These compli-
cations can hinder the quality of life.
Four studies in the literature review
found that salivary flow rate was low
among patients on hemodialysis
(Belazelkovska et al., 2014; Kaushik et
al., 2013; Limeres et al., 2016;
Nascimento et al., 2018). Specifically,
Belazelkovska and colleagues (2014)
identified a negative correlation
between thirst, xerostomia, and burn-
ing tongue and unstimulated salivary
flow rate among patients on
hemodialysis. According to
Nascimento and colleagues (2018),
xerostomia had a statistically signifi-
cant association with the number of
drugs consumed, and dysgeusia was
associated with a higher oral hygiene
index (OHI-S). Buffer capacity and
pH of the unstimulated whole saliva in
patients with ESRD were significantly
higher than in controls, whereas stim-
ulated whole saliva did not show sig-
nificant differences (Kaushik et al.,
2013).
One interventional study found
that while both pure water and
licorice mouthwash improved unstim-
ulated whole salivary flow rate,
licorice mouthwash reduced xerosto-
mia while pure water did not (Yu et
al., 2016). Patients with diabetes
undergoing hemodialysis treatment,
individuals older than 65 years, and
men were more likely to have
reduced salivary flow rate. There was
also no significant difference in sali-
vary flow rate related to smoking sta-
tus or the morning vs. afternoon
hemodialysis sessions (Marques,
Liborio, & Lima Saintrain, 2013).
The decayed, missing, and
filled teeth (DMFT) index. The
DMFT index is a well-established tool
that uses the number of decayed, miss-
390
ing, and filled teeth as a measurement
of oral health. Elevated DMFT was
higher among patients on hemodialy-
sis ( Jain et al., 2014; Schmalz et al.,
2016; Tiwari et al., 2013; Ziebolz,
Fischer, Hornecker, & Mausberg,
2012), older age (Hajian-Tilaki, Oliae,
Jenabian, Hajian-Tilaki, & Motal-
lebnejad, 2014; Silva et al., 2017), and
individuals with diabetes (Hajian-
Tilaki et al., 2014; Hou et al., 2017;
Swapna et al., 2013). In contrast,
Limeres and colleagues (2016) report-
ed that the total number of decayed
teeth was lower in patients with
ESRD. Individuals with higher
incomes had a higher number of fill-
ings and less frequent tooth brushing
was associated with higher DMFT
(Palmer et al., 2016). Two studies
found that years spent on hemodialy-
sis was associated with a higher
DMFT index, while one study
(Hajian-Tilaki et al., 2014) did not.
Individuals on hemodialysis for a
duration longer than three (or four)
years had higher levels of decayed
teeth and DMFT index (Andrade et
al., 2017; Sekiguchi et al., 2012).
Palmer and colleagues (2015) reported
an association of edentulism and
DMFT with all-cause and cardiovas-
cular mortality in adults greater than
60 years of age.
Lifestyle and Quality of Life
Lifestyle choices and interven-
tions. Two studies identified that low
frequency of dental visits, lack of den-
tal flossing, elevated DMFT, and
chronic periodontitis had a significant
association with high mortality
(Andrade et al., 2017; de Souza et al.,
2014). Dental flossing, using mouth-
wash, brushing teeth daily, spending
two minutes or more on oral hygiene,
changing a toothbrush every three
months, and visiting a dentist within
the past six months were associated
with longer survival in patients on
hemodialysis (Palmer et al., 2015).
Parkar and Ajithkrishnan (2012)
observed a higher prevalence of peri-
odontal diseases in patients with CKD
due to the negligence of oral hygiene
rather than due to the chronic uremia
in this population. Physiological sus-
Nephrology Nursing Journal
ceptibility and hygiene behaviors (less
tooth brushing) among elderly
patients (70 to 79 years) were associat-
ed with a higher incidence of peri-
odontal disease when compared with
younger (30 to 39 years) patients on
hemodialysis (Hou et al., 2017).
Sekiguchi and colleagues (2012) found
no significant difference between
groups by years on hemodialysis with
regard to tooth brushing frequency,
dental floss use, and time since last
dental visit. Gautam and colleagues
(2014), using a survey, found a lack of
knowledge related to oral health
among patients on hemodialysis in
India.
Oral and general health-relat-
ed quality of life. HRQoL is an indi-
vidual’s perceived physical, mental,
emotional, and social health over time
(Centers for Disease Control and
Prevention, 2016). Oral HRQoL is a
multidimensional measurement of
HRQoL that includes a subjective
measurement of the individual’s oral
health, functional well-being, emo-
tional well-being, expectations, satis-
faction with care, and sense of self
(Sischo & Broder, 2011). One study
(Veisa et al., 2017) used the Short Form
36-Item Health Survey (SF-36) to
study the impact of periodontal dis-
ease on physical and physiological
domains of patients on long-term
hemodialysis. They examined the
relationship between periodontal dis-
ease index (PDI) (assessed by three
components: gingival and periodontal
index, bacterial plaque index, and cal-
culus index) and quality of life (physi-
cal and mental component), and found
that PDI was negatively associated
with QoL scores. Oral HRQoL evalu-
ates comfort while eating, engaging in
social activities and self-esteem, and
satisfaction regarding oral health
(Scully, 2000). HRQoL has a strong
association with regular tooth brushing
as opposed to individuals on hemo-
dialysis who did not have regular tooth
brushing (Afsar, 2013). Regular tooth
brushing was also a better predictor of
oral HRQoL among patients on
hemodialysis, as was non-smoking sta-
tus and dental visits in the previous six
months (Pakpour et al., 2015).
July-August 2019 Vol. 46, No. 4
 The Oral Health Impact Profile
(OHIP) is a reliable and valid instru-
ment for measuring the impact of oral
disorders on quality of life (Slade &
Spencer, 1994). To assess oral health-
related quality of life, Rodakowska
and colleagues (2018) compared
OHIP-14 with the Geriatric/General
Oral Health Assessment Index
(GOHAI) and found more variables
were significantly related to OHIP-14
scale than GOHAI and patients on
chronic hemodialysis. Two studies
reported that, in general, patients on
hemodialysis have poorer Oral
HRQoL and general HRQoL com-
pared to healthy subjects (Andrade et
al., 2017; Pakpour et al., 2015), while
another study found that OHIP scores
were not significantly different be-
tween patients on hemodialysis or
who received a renal transplant, and
healthy controls (Schmalz et al., 2016).
In the hemodialysis group, only
patients with diabetes mellitus had
higher OHIP scores (or poorer oral
health) (Schmalz et al., 2016). In addi-
tion, Hajian-Tilaki and colleagues
(2014) reported that oral HRQoL was
not significantly impacted by poor
oral health. However, older age, resi-
dence in rural areas, and tooth pain in
the last six months affected oral
HRQoL among patients on hemo-
dialysis (Silva et al., 2017). Nor-
malization of biochemical parameters
of calcium-phosphate and iron meta-
bolism promotes the sense of a better
quality of life among patients on chron-
ic hemodialysis (Ksiąkek, Zolnierz, &
Sak, 2016). Higher calcium levels
before and after hemodialysis are asso-
ciated with a better sense of quality of
life in terms of physical health. The
level of interdental hygiene does not
distinguish between general indicators
of the sense of the quality of life.
Risk of Bias Assessment
Risk of bias assessment is used to
interpret findings and assess quality of
included studies to reduce the risk of a
biased synthesis (Institute of Medicine,
2011). Studies with lower scores, or a
higher risk of bias, can be excluded. In
this systematic review, 43 studies were
reviewed, including 30 cross-sectional
Nephrology Nursing Journal July-August 2019
studies, six cohort (both prospective
and retrospective), three case-control,
and four experimental studies (see
Tables 2 to 5). The risk of bias was eval-
uated using the Newcastle/Ottawa
Quality Assessment Scale (Wells et al.,
n.d) for cohort and case-control studies,
an adapted form of Newcastle/Ottawa
cohort scale for cross-sectional studies,
and the Cochrane Collaboration tool
for experimental studies (Higgins &
Green, 2018). The majority of cross-
sectional studies were awarded scores
ranging from 6 to 8, indicating medium
to low risk of bias. Only four studies
compared the responders and non-
responders, indicating risk of selection
bias. However, outcome assessment
was rated high among most studies due
to clinical oral assessment and use of
medical records. Out of six, four were
prospective cohort studies, and two
were retrospective. Seven to eight stars
were awarded, showing a low risk of
bias among cohort studies. Case-con-
trol studies raged from five to eight
stars due to the risk of selection bias,
poor ascertainment of exposure, and
high non-response rate. Two out of four
experimental studies were deemed at
low risk for selection, performance,
and attrition bias. One study was con-
sidered at high risk of bias for most
items and unclear at other biases. No
studies in this systematic review were
rated less than five stars; therefore,
none were excluded from review.
Discussion
A bidirectional association exists
between CKD and periodontal dis-
ease. Individuals with advanced peri-
odontal disease are more likely to
have CKD. Comparably, individuals
with CKD are more likely to have
periodontal disease and periodontitis.
Review of recent studies classify the
current state of knowledge on peri-
odontal health among patients receiv-
ing hemodialysis into two categories:
clinical measurements), and lifestyle
and quality of life.
Clinical Measurements
The impact of periodontal therapy
on inflammation among patients
Vol. 46, No. 4
undergoing hemodialysis has been
evaluated in hopes of decreasing the
frequency of cardiovascular events,
mortality, increased inflammatory
markers, and negative patient symp-
toms. Findings continue to conflict
regarding whether or not non-surgical
periodontal therapy is beneficial in
reducing periodontal disease severity
and inflammatory markers. Addi-
tional evaluations of periodontal ther-
apies and their impact on patient out-
comes would be beneficial.
Edentulous individuals were often
omitted from the study samples includ-
ed in this review. While most studies
did not state a reason for this exclusion,
it is likely due to the difficulty in evalu-
ating clinical measurements, as well as
the perceived severity of periodontal
disease that led to an edentulous state.
Exclusion of edentulous patients may
skew study findings. This exclusion
may also prevent the assessment of the
most severe cases of periodontal dis-
ease over time and the most vulnerable
patients regarding nutritional status.
Although usual measures of periodon-
tal health may need to be modified for
this population, we recommend eden-
tulous patients be included in future
studies when possible.
Most studies included in this
review did not differentiate between
etiologies or underlying causes of
CKD (such as diabetes, hypertension).
Recent studies found that patients
with diabetes undergoing hemodialy-
sis had a significantly higher preva-
lence of dysgeusia, dry mouth, and
increased pocket depth as compared
to patients without diabetes. There-
fore, studies that investigate underly-
ing CKD etiology are needed. Lack of
known etiology prevents differentia-
tion between disease processes and
their impact on outcomes. This
reduces the opportunity to create eti-
ology-specific nursing interventions
for patients on hemodialysis.
Poorer oral health is associated with
higher inflammatory markers and
higher mortality from cardiovascular
and other causes. Therefore, it is likely
that the poor oral health associated
with patients on hemodialysis is posi-
tively correlated with increased mortal-
391
The Relationship Between Oral Health and Hemodialysis Treatment Among Adults with Chronic Kidney Disease: A Systematic Review
ity. Studies regarding non-surgical peri-
odontal treatment reveal discrepancies
regarding the benefit of inflammatory
burden and severity of periodontal dis-
ease. Thus, interventional studies are
needed to better understand the rela-
tionship between ESRD and periodon-
tal disease, but specifically, the impact
of periodontal treatment on patient
outcomes and HRQoL.
Lifestyle and Quality of Life
Patients receiving hemodialysis are
less likely to attend regular dental visits,
use dental floss, or complete regular
tooth brushing. The cause is consid-
ered multifactorial, including lack of
financial resources and the prioritiza-
tion of renal health above oral health.
Individuals with positive dental care
practices frequently reported higher
HRQoL. However, study findings
identify some discrepancies regarding
whether poor oral health negatively
impacts oral HRQoL. This supports
that patients may not perceive a prob-
lem with their state of poor oral health
and would, therefore, be unlikely to
change their oral self-care practices.
Identifying factors associated with poor
oral health among hemodialysis
patients would help design interven-
tions to improve quality of life.
We also recommend further inter-
ventional study regarding possible
benefits of proper oral hygiene prac-
tices. If oral health negligence is a
higher or equal prognostic factor com-
pared to the inflammatory and uremic
state, intervention and improvement
of patient outcomes will be more
widely available and more cost-effec-
tive at all levels.
Methodological Limitations
There are a few limitations in this
systematic review. The majority of
included studies were observational.
Only four studies completed during
the timeframe of this review were ran-
domized controlled trials, and one
was interventional without random-
ization. While some studies had large
sample sizes, most were conducted
with smaller samples, limiting the gen-
eralizability of the study. Search strate-
gies excluded articles not written in
392
English. In addition, one article was
excluded because the author was
unable to obtain the full-text article.
There is potential to have unintention-
ally omitted studies that evaluated oral
health among multiple co-morbidities,
including CKD and/or ESRD. This
would have been missed in the search.
Conclusion
The review shows a bidirectional
relationship between CKD and peri-
odontal disease. We recommend more
extensive evaluation of the impact of
periodontal treatment and nursing edu-
cation outcomes on periodontal health,
patient quality of life, nutritional and
inflammatory markers, and mortality.
Continued inclusion of serum albumin,
CRP, calcium, phosphorus, and iron as
baseline evaluation for inflammatory
and nutritional markers is recommend-
ed. Implications for future nursing
research include recommended differ-
entiation of underlying CKD etiology
and the impact of poor oral health on
patient outcomes and HRQoL.
Nursing practice implications include
the creation of targeted interventions
for patients with diabetes undergoing
hemodialysis treatment, development
of educational opportunities to im-
prove oral health status and behaviors,
and incorporation of oral health nurs-
ing screenings and education into stan-
dard of care in outpatient hemodialysis
centers.
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