Received: 14 February 2018 Revised: 20 July 2018 Accepted: 24 July 2018

DOI: 10.1111/scd.12319

ARTICLE

Systemic medical conditions and periodontal status

in older individuals
Georgios S. Chatzopoulos DDS, MS Alejandro Cisneros BA Miguel Sanchez DDS
Larry F. Wolff DDS, MS, PhD

Division of Periodontology, Department

of Developmental and Surgical Sciences,
School of Dentistry, University of Minnesota,
Minneapolis, MN, USA
Correspondence
Dr. Georgios S. Chatzopoulos, Department of
Developmental and Surgical Sciences, Divi-
sion of Periodontology, School of Dentistry,
University of Minnesota, 515 Delaware Str. SE,
Minneapolis, 55455, USA.
Email: chatz005@umn.edu
Funding information
UMSOD Summer Fellowship Program; Den-
tistry Student Research Campaign
Abstract
Aims: The purposes of this study are to: (1) assess the prevalence of systemic and
periodontal disease in older individuals, (2) compare periodontal conditions between
four age cohorts, and (3) investigate the relationship between periodontal disease and
systemic medical conditions.
Methods: Electronic records from a total of 5,000 adults were randomly selected
from the University of Minnesota School of Dentistry database. Individuals ≥60 years
of age, with at least six remaining teeth in their dentition with a complete medical
history and full-mouth series of radiographs were included in the study to determine
the severity of periodontal disease based on the percentage of radiographic bone loss.
Results: A total of 2,163 patients were included in the final analysis. The multivari-
able regression analysis showed that patients self-reported tobacco use and diabetes
were significantly associated with moderate and severe bone loss than none to mild,
whereas the opposite was found for those with joint replacement, past use of steroids
and acid reflux/GERD.
Conclusion: A number of systemic medical conditions and tobacco use are associ-
ated with periodontitis. This reflects the importance of an interdisciplinary interaction
between dental and medical professionals.

KEYWORDS
alveolar bone loss, health status, risk indicators, tobacco use

1 I N T RO D U C T I O N dysbiosis and may influence the progression and severity of

Periodontal disease is defined as a multifactorial inflamma-
tory disease, which results from the interactions between
periodontal pathogens and the host immune response. The vir-
ulence factors of the subgingival microbes disrupt the immune
surveillance and elevates the virulence of the microbial com-
munity leading to a dysbiotic community and disruptive tissue
homeostasis including the periodontal ligament, cementum,
and alveolar bone.1 Presence of systemic conditions, obe-
sity, smoking, stress, and aging characterize a susceptible
host that can shift the polymicrobial synergy towards
periodontal disease.2 A number of studies have shown that
oral health is significantly associated with general health
among elderly individuals.3–6 The overall prevalence of
periodontitis in adults ≥65 years of age range from 62.1%
to 74.2% across the United States with an average of 66.2%
revealing the need for preventive measures.7
The number of older adults in the United States is expected
to double as a result of the aging of the population.8 Cur-
rently, the number of individuals ≥65 years of age is greater
than the number of children <5 years of age (World Health
Organization) showing the dramatic demographic change of

© 2018 Special Care Dentistry Association and Wiley Periodicals, Inc.

Spec Care Dentist. 2018;1–9. wileyonlinelibrary.com/journal/scd 1

2 CHATZOPOULOS ET AL.
the population worldwide.9 It is expected that noncommuni-
cable chronic diseases will lead to death of 70% of the pop-
ulation for high-, middle-, and low-income countries (World
Health Organization),9 a number which has also been shown
to be associated with periodontal disease. However, only lim-
ited data are available on the association between periodon-
tal diseases and systemic medical conditions in the geriatric
population. Large-scale studies are needed to allow for further
investigation of the association between systemic diseases and
tobacco use with periodontal disease in the aging population.
Several theories supporting the association between oral
health and systemic health have been proposed. First of all,
bacteria, bacteria products and toxins may spread from the
oral cavity to distant sites adversely impacting an individual's
general health.10,11 Secondly, periodontal disease may trig-
ger a chronic inflammatory cascade of events through inflam-
mation and inflammatory mediators that may cause systemic
inflammation.11,12 Finally, expression of virulence factors by
periodontal pathogens and the presence of oral pathogens
in nonoral tissues may support the biological link between
chronic oral diseases including periodontitis with systemic
diseases.11
Although life expectancy in most western societies is
increasing, both systemic and oral health deteriorates with
aging which affects the quality of life.13,14 The economic bur-
den resulting from the management of periodontitis and other
systemic health conditions underscores the need for imple-
menting strategies to prevent their onset and development.
Therefore, it is important to gain knowledge on the associa-
tions between systemic diseases and oral health. Large patient
samples from electronic health records may provide valu-
able information surrounding the role of chronic diseases and
tobacco use in periodontal disease enabling clinicians to take
preventive measures in patients with a high risk of bone loss
and tooth loss based on their medical health condition, but
also a holistic approach to patient care management. Due to
increasing human longevity, there is a need for studies focused
on this older population.
Susceptibility to oral diseases such as periodontal disease is
influenced by the underlying health of older adults. To under-
line the fundamental concept of prevention in dental practice,
the purposes of the present study are to: (1) assess the preva-
lence of systemic and periodontal disease in older individuals,
(2) compare periodontal conditions between four age cohorts,
and (3) investigate the relationship between periodontal dis-
ease and systemic medical conditions.
2 M AT E R I A L A N D M E T H O D S
Electronic health records of 5,000 adults were randomly
selected by a computer-generated program from a total of
10,201 dental records from the electronic database at the Uni-
versity of Minnesota School of Dentistry. Individuals ≥60
years of age, with at least six remaining teeth in the denti-
tion, with a complete medical history and full-mouth series
of radiographs who received any type of dental treatment
at the University of Minnesota dental clinics between 2012
and 2016 were included in the analysis. Patients’ demo-
graphic characteristics including age and gender, systemic
medical history, alcohol consumption, and smoking status
were recorded and analyzed. Sixty medical conditions were
examined in the study including communicable diseases, car-
diovascular diseases, respiratory diseases, neurological disor-
ders, mental and substance use disorders, diabetes, blood and
endocrine diseases, musculoskeletal disorders, gastrointesti-
nal disorders, common infectious diseases, neoplasms, skin
and sense organ diseases, and others.
A full-mouth series of radiographs were utilized to deter-
mine the number of missing teeth and the severity of peri-
odontal disease based on the percentage of bone loss: none
to mild (0–25% bone loss), moderate (26–50% of bone loss),
severe (>50% of bone loss or presence of at least four poste-
rior teeth with >50% bone loss). Three independent calibrated
examiners (GC, AC, MS) reviewed the available radiographs
for the number of missing teeth (kappa index of agreement
ranged from 0.88 to 0.97) and the severity of bone loss (kappa
index of agreement ranged from 0.93 to 0.95). The radio-
graphic examination for the severity of bone loss included the
following measurements: (1) distance between the Cemento–
Enamel junction (CEJ) and the root tip, and (2) distance from
the CEJ to the alveolar crest. After taking into considera-
tion the 2-mm distance from the alveolar bone to the CEJ
in health,15,16 the percentage of bone loss was expressed as
a ratio of the amount of bone loss to the overall root length
for the entire dentition. Third molars were excluded from the
analysis.
The ethical approval for the study was received from the
Institutional Review Board (IRB) of the University of Min-
nesota and the study was conducted in accordance with the
Declaration of Helsinki of 1975, as revised in 2013.
2.1 Statistical analysis
Electronic health records including demographic character-
istics, medical history, and tobacco use were recorded in a
computer database file. The severity of bone loss and the
number of missing teeth from the eligible patients were also
included in the dataset and analyzed using a statistical soft-
ware (SPSS v.19.0, IBM, Armonk, NY, USA). Periodontal
status reported by the severity of bone loss was selected as
dependent variable. Descriptive statistics including frequen-
cies, percentages, means and standard deviations were cal-
culated. Fisher's exact test (univariate analysis) was used to
assess the association between the percentage of bone loss
CHATZOPOULOS ET AL. 3

TABLE 1 Population characteristics compared between the radiographic bone loss groups
Bone loss
Total population None to mild Moderate Severe
Parameters (N = 2,163) (n = 1,537 – 71.1%) (n = 462 – 21.4%) (n = 164 – 7.6%) p-value*
Age (mean ± SD) in years 70.31±7.42 69.84±7.22 72.01±7.77 69.91±7.55 <0.001†
Age groups <0.001
60–63 years (%) 437 (20.2) 340 (22.1) 64 (13.9) 33 (20.1)
64–68 years (%) 577 (26.7) 413 (26.9) 114 (24.7) 50 (30.5)
69–74 years (%) 565 (26.1) 395 (25.7) 124 (26.8) 46 (28.0)
75–94 years (%) 584 (27.0) 389 (25.3) 160 (34.6) 35 (21.3)
Gender 0.001‡
Males (%) 1,150 (53.2) 778 (50.6) 269 (58.2) 103 (62.8)
Females (%) 1,013 (46.8) 759 (49.4) 193 (41.8) 61 (37.2)
Missing teeth (mean ± SD) 4.83±4.25 4.02±3.83 6.51±4.52 7.74±4.56 <0.001†
Tobacco use (%) 185 (8.6) 90 (5.9) 54 (11.7) 41 (25.0) <0.001‡
Alcohol use (%) 490 (22.7) 341 (22.2) 104 (22.5) 45 (27.4) 0.310
*
Statistical significance between study groups with p-value ≤0.001.
†
For mean age and number of missing teeth, ANOVA was used. Bold values represent statistically significant difference.
‡ For age groups, gender, tobacco and alcohol use, chi-square test was used. Bold values represent statistically significant differences.

groups and the medical conditions as well as to compare age
groups, gender and tobacco use with the bone loss groups.
ANOVA was also utilized to compare the mean age and the
mean number of missing teeth between the groups. Multivari-
able logistic regression analysis was also employed for the
parameters that reached statistical significance with the uni-
variate analysis and confidence intervals (CI) were reported.
None to mild group was selected as a reference category for
the comparisons with severe and moderate groups. All tests
of significance were evaluated at the 0.05 error level.
Because of multiple hypothesis testing, there is a higher
risk of type I error which may result in accepting an alterna-
tive hypothesis where the results may be attributed to chances
because of multiple testing. A priori sample size calculation
for multiple regression that takes into consideration the antici-
pated effect size (f2 = 0.15), the desired statistical power level
(𝛽 = 0.90), the number of predictors (n = 60) and the probabil-
ity level (𝛼 = 0.05) showed that the minimum required sam-
ple size in this study was 309 patients. The final size, 2,163,
of the study population individuals could reveal any potential
association between the investigated medical conditions and
periodontal disease.
3 RESULTS
Five thousand adults were randomly selected from a total of
10,201 dental records. When eligibility to this study was eval-
uated based on the inclusion criteria, it was determined that a
total of 2,163 electronic health records of patients with an age
of ≥60 years and a full-mouth series of radiographs met the
inclusion criteria and were included in the final analysis. The
remaining 2,837 records were excluded to age limitation (age
between 18 and 59 years), incomplete medical history, or an
incomplete full-mouth series of radiographs. The final anal-
ysis to investigate the association between periodontal dis-
ease/bone loss and systemic conditions and tobacco use was
based on records of 2,163 patients.
Population characteristics compared between the radio-
graphic bone loss groups are shown in Table 1. None to mild
bone loss was found in 71.1% of the population, moderate
in 21.4%, and severe in 7.6%. The mean age of the included
individuals was 70.31 years (range from 60 to 94 years) and
patients with moderate bone loss showed statistically signifi-
cant higher mean age than those with none to mild and severe
(p < 0.001). The population was divided into four groups (60–
63 years, 64–68 years, 69–74 years, 75–94 years) based on
the percentiles of the included individuals. Similarly with the
previous finding, older patients were significantly more likely
to diagnosed with moderate bone loss (p < 0.001) than none
to mild and severe. In regards to gender, moderate and severe
bone loss were statistically significant more prevalent in males
than in females (p = 0.001). The worse the periodontal status,
the higher mean number of missing teeth with severe bone
loss group having the highest number. This difference was
statistically significant (p < 0.001). Tobacco users were also
diagnosed with severe bone loss significantly more frequently
than tobacco nonusers (p < 0.001). No significant associa-
tions were observed between alcohol use and periodontal sta-
tus (p = 0.310).
The prevalence of systemic conditions for the total popula-
tion and compared between the bone loss groups are shown
in Table 2. High blood pressure (47.9%), high cholesterol
4 CHATZOPOULOS ET AL.

TABLE 2 Prevalence of systemic conditions for the total population and compared between the bone loss groups
Bone loss
Total population None to mild Moderate Severe
Systemic condition (n = 2,163) (n = 1,537 – 71.1%) (n = 462 – 21.4%) (n = 164 – 7.6%) p-value*
Communicable diseases
HIV positive/AIDS 3 (0.1) 2 (0.1) 1 (0.2) 0 (0.0) 0.803
HPV 22 (1.0) 13 (0.8) 7 (1.5) 2 (1.2) 0.438
Sexually transmitted disease 28 (1.3) 19 (1.2) 8 (1.7) 1 (0.6) 0.513
Hepatitis 43 (2.0) 29 (1.9) 10 (2.2) 4 (2.4) 0.850
Cardiovascular diseases
Angina 79 (3.7) 49 (3.2) 22 (4.8) 8 (4.9) 0.196
Damaged heart valve 72 (3.3) 58 (3.8) 11 (2.4) 3 (1.8) 0.184
Heart attack 122 (5.6) 80 (5.2) 28 (6.1) 14 (8.5) 0.193
Heart failure 42 (1.9) 28 (1.8) 8 (1.7) 6 (3.7) 0.251
Heart infection 12 (0.6) 8 (0.5) 3 (0.6) 1 (0.6) 0.943
Heart surgery 216 (10.0) 148 (9.6) 48 (10.4) 20 (12.2) 0.551
High blood pressure 1,037 (47.9) 721 (46.9) 228 (49.4) 88 (53.7) 0.205
High cholesterol 819 (37.9) 578 (37.6) 172 (37.2) 69 (42.1) 0.507
Irregular heart beat 244 (11.3) 168 (10.9) 54 (11.7) 22 (13.4) 0.603
Stroke 103 (4.8) 68 (4.4) 28 (6.1) 7 (4.3) 0.334
Respiratory diseases
Asthma 176 (8.1) 136 (8.8) 29 (6.3) 11 (6.7) 0.163
Difficulty breathing 107 (4.9) 68 (4.4) 30 (6.5) 9 (5.5) 0.188
Emphysema/bronchitis 78 (3.6) 56 (3.6) 17 (3.7) 5 (3.0) 0.923
Sleep apnea 249 (11.5) 184 (12.0) 43 (9.3) 22 (13.4) 0.212
Neurological disorders
Dementia 23 (1.1) 13 (0.8) 7 (1.5) 3 (1.8) 0.286
Epilepsy/seizures 25 (1.2) 15 (1.0) 7 (1.5) 3 (1.8) 0.447
Headaches 194 (9.0) 140 (9.1) 41 (8.9) 13 (7.9) 0.878
Multiple sclerosis 14 (0.6) 12 (0.8) 2 (0.4) 0 (0.0) 0.402
Parkinson's disease 13 (0.6) 8 (0.5) 5 (1.1) 0 (0.0) 0.229
Mental and substance use disorder
Anxiety 233 (10.8) 164 (10.7) 56 (12.1) 13 (7.9) 0.321
Bipolar disorder 39 (1.8) 28 (1.8) 8 (1.7) 3 (1.8) 0.992
Chemical dependency 28 (1.3) 20 (1.3) 8 (1.7) 0 (0.0) 0.241
Depression 326 (15.1) 240 (15.6) 67 (14.5) 19 (11.6) 0.363
Eating disorders 19 (0.9) 12 (0.8) 7 (1.5) 0 (0.0) 0.152
Learning disorder 31 (1.4) 24 (1.6) 6 (1.3) 1 (0.6) 0.599
Sleep disorder 167 (7.7) 123 (8.0) 36 (7.8) 8 (4.9) 0.362
Street/recreational or illicit drug use 1 (0.0) 1 (0.1) 0 (0.0) 0 (0.0) 0.816
Diabetes, blood, and endocrine diseases
Abnormal bleeding 33 (1.5) 22 (1.4) 6 (1.3) 5 (3.0) 0.249
Anemia 61 (2.8) 48 (3.1) 10 (2.2) 3 (1.8) 0.401
Diabetes 351 (16.2) 228 (14.8) 87 (18.8) 36 (22.0) 0.015
Dialysis 4 (0.2) 3 (0.2) 1 (0.2) 0 (0.0) 0.845
Jaundice 15 (0.7) 10 (0.7) 4 (0.9) 1 (0.6) 0.879
Kidney disorder 73 (3.4) 46 (3.0) 23 (5.0) 4 (2.4) 0.092
Sickle cell disorders 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) -
Thyroid disorder 336 (15.5) 241 (15.7) 72 (15.6) 23 (14.0) 0.856
a
(Continues)
CHATZOPOULOS ET AL. 5

TABLE 2 (Continued)
Bone loss
Total population None to mild Moderate Severe
Systemic condition (n = 2,163) (n = 1,537 – 71.1%) (n = 462 – 21.4%) (n = 164 – 7.6%) p-value*
Musculoskeletal disorders
Arthritis 813 (37.6) 595 (38.7) 171 (37.0) 47 (28.7) 0.039
Artificial joint 290 (13.4) 236 (15.4) 42 (9.1) 12 (7.3) <0.001
Fibromyalgia 68 (3.1) 59 (3.8) 8 (1.7) 1 (0.6) 0.012
Lupus 13 (0.6) 7 (0.5) 2 (0.4) 4 (2.4) 0.007
Osteoporosis 206 (9.5) 137 (8.9) 54 (11.7) 15 (9.1) 0.202
Sjogren's syndrome 19 (0.9) 16 (1.0) 2 (0.4) 1 (0.6) 0.437
Gastrointestinal disorders
Acid reflux/GERD 484 (22.4) 375 (24.4) 80 (17.3) 29 (17.7) 0.002
Irritable bowel syndrome 96 (4.4) 73 (4.7) 19 (4.1) 4 (2.4) 0.366
Stomach ulcer 59 (2.7) 40 (2.6) 10 (2.2) 9 (5.5) 0.069
Common infectious diseases
Influenza 104 (4.8) 72 (4.7) 28 (6.1) 4 (2.4) 0.162
Pneumococcal 85 (3.9) 55 (3.6) 26 (5.6) 4 (2.4) 0.082
Varicella 76 (3.5) 52 (3.4) 21 (4.5) 3 (1.8) 0.235
Neoplasms
Cancer 358 (16.6) 268 (17.4) 70 (15.2) 20 (12.2) 0.151
Cancer treatment 274 (12.7) 200 (13.0) 59 (12.8) 15 (9.1) 0.366
Skin and sense organ diseases
Glaucoma 125 (5.8) 82 (5.3) 32 (6.9) 11 (6.7) 0.380
Hives or skin rash 133 (6.1) 100 (6.5) 24 (5.2) 9 (5.5) 0.551
Other
Delayed healing 30 (1.4) 21 (1.4) 6 (1.3) 3 (1.8) 0.876
Liver disease 22 (1.0) 16 (1.0) 3 (0.6) 3 (1.8) 0.427
Past use of steroids 204 (9.4) 158 (10.3) 39 (8.4) 7 (4.3) 0.031
* Fisher
exact test was used to compare the bone loss groups in regards to the prevalence of systemic conditions and tobacco use. Bold values represent statistically
significant differences with p-value <0.05.

(37.9%), depression (15.1%), diabetes (16.2%), thyroid dis-
order (15.5%), arthritis (37.6%), acid reflux/GERD (22.4%),
and cancer (16.6%) were found to be the most prevalent sys-
temic diseases. Tobacco use was also self-reported by 8.6% of
the included population. However, HIV positive/AIDS (0.1%)
and dialysis (0.2%) were rarely reported. Street/recreational or
illicit drug use was reported by one individual, whereas none
of the included individuals had sickle cell disorder. Based
on the univariate analysis, tobacco use (p < 0.001), diabetes
mellitus (p = 0.015), arthritis (p = 0.039), artificial joint
(p < 0.001), fibromyalgia (p = 0.012), lupus (p = 0.007),
acid reflux/GERD (p = 0.002), and past use of steroids
(p = 0.031) were significantly different among the bone loss
groups.
The summary of the multivariable logistic regression
model of bone loss and systemic medical conditions/tobacco
use is presented in Table 3. Self-reported tobacco use and dia-
betes were significantly associated with both moderate and
severe bone loss when compared to none to mild (p < 0.05).
Individuals who reported tobacco use had 5.4 (95% CI, 3.5–
8.2) times higher prevalence of severe bone loss (p < 0.001)
and 2.1 (95% CI, 1.5–3.0) times of moderate bone loss
(p < 0.001) compared to none to mild. Similarly, diabetics
showed 1.8 (95% CI, 1.2–2.7) higher prevalence of severe
(p = 0.006) and 1.4 (95% CI, 1.1–1.9) of moderate (p = 0.014)
bone loss rather than none to mild. Severe bone loss was also
significantly more frequently diagnosed in patients with lupus
(PR: 7.1; 95% CI, 1.8–27.5; p = 0.005). Severe (p = 0.048)
and moderate (p = 0.002) bone loss were significantly less
prevalent than none to mild in individuals with artificial joint.
Similarly, the prevalence of severe and moderate bone loss
was significantly less than none to mild in the included older
individuals who reported past use of steroids (p = 0.028) and
acid reflux/GERD (p = 0.004), respectively. To test the cor-
relation between the independent variables in the regression
model, a multicollinearity test was performed. The obtained
6 CHATZOPOULOS ET AL.

TABLE 3 Summary of multivariable model of bone loss and the on the percentage of bone loss. Radiographs must show 30–
systemic medical conditions/tobacco use 50% demineralization before bone loss can be detected, when
Bone Systemic condition/ Adjusted PR radiographs are examined directly by eye. This may under-
loss tobacco use (95% CI)* p-value* estimate the amount of bone loss.19 To minimize the risk of
Severe Tobacco use 5.4 (3.5–8.2) <0.001 underestimation as a result of the demineralization as well as
Diabetes 1.8 (1.2–2.7) 0.006 because we were not able to standardize the radiographs due
Arthritis 0.8 (0.5–1.1) 0.177 to the retrospective study design, patients exhibiting bone loss
Artificial joint 0.5 (0.3–0.9) 0.048 0–25% were included in the “none to mild bone loss” group.
Fibromyalgia 0.2 (0.1–1.5) 0.111
In this study of individuals ≥60 years of age, the prevalence of
severe bone loss was 7.6%, moderate bone loss was 21.4% and
Lupus 7.1 (1.8–27.5) 0.005
71.1% for none to mild. The prevalence of severe periodontitis
Acid reflux/GERD 0.8 (0.5–1.2) 0.193
in the United States among individuals ≥65 years of age varies
Past use of steroids 0.4 (0.2–0.9) 0.028
from 9.5% to 16.3% with a mean prevalence of 12% regard-
Moderate Tobacco use 2.1 (1.5–3.0) <0.001
less of the administrative or geographical unit.7 Our finding is
Diabetes 1.4 (1.1–1.9) 0.014 close to the reported range of the National Health and Nutri-
Arthritis 1.1 (0.9–1.4) 0.433 tion Examination Survey (NHANES) but the small difference
Artificial joint 0.6 (0.4–0.8) 0.002 may be attributed to the inclusion of adults ≥60 years and not
Fibromyalgia 0.5 (0.2–1.1) 0.077 limited to over 65 years.7
Lupus 1.1 (0.2–5.1) 0.961 Age and periodontal disease were significantly associated
Acid reflux/GERD 0.7 (0.5–0.9) 0.004 when age was expressed as a mean value and as a cate-
Past use of steroids 0.9 (0.6–1.2) 0.395 gorical variable. More specifically, the higher the mean age
*
and the age group, the higher the prevalence of moderate
Prevalence ratio, 95% confidence interval and p-values are from a multivariable
generalized model. “None to mild” group was selected as a reference category for bone loss. Similar results were also reported by Eke et al.7
the comparisons with “severe” and “moderate” groups. All independent variables who found that nonsevere periodontitis was more prevalent
are dichotomous. in the older subgroup (≥75 years) when compared to a sub-
group of 65–74 years of age. This may be explained by the
generalized variance inflation factor (GVIF) was 1.177, which mean number of missing teeth that was, on average, higher in
reveals no multicollinearity. the older individuals. Severely diseased teeth may have been
extracted in the older group of patients. Furthermore, individ-
uals with severe periodontal disease were also prone to exhibit
4 DISCUSSI O N more missing teeth than those with none to mild bone loss,
which was expected due to the extent of the disease severity
Studies assessing the association between medical and peri- (p < 0.001). Males showed also significantly higher preva-
odontal health of older adults are inconsistent. In this retro- lence of severe bone loss than females which is in agreement
spective investigation, a large group of 2,163 patients ≥60 with the NHANES data.7 A systematic review of the litera-
years of age who attended the University of Minnesota School ture that aimed to assess gender-specific data on prevalence
of Dentistry seeking dental therapy was included to assess and severity of periodontitis from large epidemiologic stud-
the prevalence of systemic medical conditions and periodontal ies demonstrated that United States national surveys have pro-
disease. In addition, an evaluation of the association between vided strong evidence that males exhibit a greater prevalence
age and systemic conditions and tobacco use with periodon- and severity of destructive periodontal disease than females
tal disease as expressed by the severity of radiographic bone of comparable age, while smoking history does not seem to
loss was determined. The retrospective cross-sectional design affect these differences.20
of this study may only identify risk indicators for periodontal Tobacco users were significantly associated with the sever-
disease and if a significant association exist. However, inter- ity of bone loss (p < 0.001). More specifically, severe bone
ventional studies would be needed to recognize risk factors.17 loss was significantly more prevalent than moderate (11.7%)
Radiographic evaluation is commonly used in confirming and none to mild (5.9%) bone loss in individuals who reported
and supporting a periodontal diagnosis and provide additional tobacco use (25.0%). In this investigation, the multivariable
information essential in treatment planning. Radiographs are regression analysis revealed that tobacco users showed 5.4
of paramount importance in determining the extent and sever- (95% CI, 3.5–8.2) times higher (p < 0.001) prevalence of
ity of alveolar bone loss and detecting osseous lesions.18 In severe bone loss than none to mild and 2.1 (95% CI, 1.5–
this study, a full-mouth series of periapical radiographs in 3.0) of moderate (p < 0.001) when compared to none to mild.
combination with horizontal or vertical bitewings was utilized Smoking is considered an environmental factor that has been
to categorized the included population into three groups based related to a dysbiotic subgingival microbial communities that
CHATZOPOULOS ET AL.
increases the risk for periodontal disease onset.21 Our findings
agree with previous studies that showed the negative impact
of smoking on the periodontium. Tobacco users exhibit a two-
to eight-fold increased risk for periodontal attachment loss
and bone loss with heavy smokers showing an odds ratio of
5.6 and light smokers an odds ratio of 2.8.22–25 Because of
the retrospective design of the present study, dose-dependent
effect could not be examined as no information about the
pack-years was available as in other studies that have shown a
positive correlation between smoking and periodontal disease
severity.25
Diabetes mellitus was also statistically significantly asso-
ciated with radiographic severity of bone loss (p < 0.05).
In this study of adults ≥60 years, diabetics exhibited 1.8
(95% CI, 1.2–2.7) times higher prevalence of severe bone loss
(p = 0.006) and 1.4 (95% CI, 1.1–1.9) greater prevalence of
moderate bone loss (p = 0.014) than none to mild. This is in
agreement with previous studies that have been included in a
meta-analysis which reported a statistically significant higher
mean attachment loss of 1 mm and a greater mean pocket
depth of 0.46 mm compared to nondiabetics.26 This associa-
tion may be explained by the elevated levels of systemic mark-
ers of inflammation and the increased inflammatory reac-
tion to bacteria that may significantly affect the periodon-
tal destruction.27,28 Individuals self-reported systemic lupus
were also significantly associated with presence of severe
bone loss (p = 0.005). In particular, it is shown that there
is a 7.1 (95% CI, 1.8–27.5) increased prevalence of severe
bone loss than none to mild. This may be attributed to the
common biologic mechanisms of both diseases. Periodontal
disease and systemic lupus affect the immune response by
leading to tissue damage and destruction of periodontal tis-
sues in periodontal disease and destruction of connective tis-
sues in systemic lupus.29 Patients with systemic lupus have
shown a greater rate of tooth loss, more severe periodontal
disease and greater gingival inflammation than those without
lupus.30 Lupus also results in an increased local inflammation
and a dysbiotic subgingival microbiota which is character-
ized by greater proportions of periodontopathogens, a reduced
microbial diversity and higher subgingival bacterial load.31
However, in this investigation, the low prevalence of systemic
lupus in the included population (n = 13–0.6%) as well as the
wide confidence interval (1.8–27.5) may suggest the presence
of a random finding that needs further research.
Patients with artificial joint (p = 0.048) and past use of
steroids (p = 0.028) showed a statistically significant nega-
tive association with severe bone loss. Artificial joint was also
significantly negatively associated with moderate bone loss
when compared to none to mild bone loss (p = 0.002). Joint
replacement is primarily caused by osteoarthritis and rheuma-
toid arthritis. In this study, based on the univariate analysis,
arthritis showed a significant negative association with the
severity of bone loss (p = 0.039). None to mild bone loss was
7
significantly more prevalent than severe bone loss in indi-
viduals with arthritis which is in agreement with the find-
ing about the joint replacement. These results reasonably lead
to the question why arthritis and artificial joint would have
a negative association with severe bone loss than with none
to mild. A potential explanation may be due to the gener-
ally good dental hygiene that characterize these patients.32
In addition, these patients may follow a frequent mainte-
nance protocol because of the greater incidence and magni-
tude of bacteremia in periodontal disease which may impact
the long-term prognosis of the joint replacement.33–35 Lim-
ited studies have assessed the association between steroid
therapy and periodontal disease. In a study that included
multiple sclerosis patients with and without corticosteroid
therapy for 1–4 years, no differences were found in regards
to probing depth, gingival recession and the height of the
alveolar bone.36 Similarly, no effect on the severity of peri-
odontal status, especially when compared to the standard
of oral hygiene, was reported by Krohn.37 Studies have
also evaluated the effect of gastroesophageal acid reflux on
periodontal disease but are limited and inconclusive.38,39
In the present investigation, self-reported acid reflux/GERD
was significantly negatively associated with moderate bone
loss (p = 0.004) when compared to none to mild bone
loss.
This study exhibits the limitations inherent in retrospective
cross-sectional studies such as the inability to demonstrate
causality between risk factors and periodontal disease. It can
provide evidence for potential risk indicators and prevalence
of systemic conditions as well as periodontal disease severity
but no evidence for risk factors can be established. Another
limitation of this investigation is the lack of information about
the race and socioeconomic status of the included population.
The retrospective design of the study enabled us to use self-
reported measures for the examined systemic conditions, but
laboratory or physical examinations were not possible. The
most important strengths of this study are the large number of
available dental records that minimizes the risk of selection
bias as well as the bone loss examination protocol that was
based on a full-mouth series of radiographs. The final analy-
sis was based on the records of 2,163 patients and included 60
self-reported medical conditions and tobacco use.
5 CONC LU SI ON S
Within the limitations of this large-scale retrospective study,
tobacco users, patients with diabetes, and patients with sys-
temic lupus were significantly positively associated with mod-
erate and severe bone loss when compared with none to mild
bone loss. However, the opposite was found for those patients
with artificial joint, past use of steroids and acid reflux/GERD.
8 CHATZOPOULOS ET AL.
These findings reflect the importance of an interdisciplinary
interaction between dental and medical professionals.
FUNDING SUPP O RT
This study was supported by the UMSOD Summer Fellow-
ship Program and the Dentistry Student Research Campaign.
CONFLICTS O F INTEREST
The authors declare that they have no conflict of interest for
this study.
ETHICS STATE ME N T
The ethical approval for the study was received from the Insti-
tutional Review Board (IRB) of the University of Minnesota.
ORC ID
Georgios S. Chatzopoulos DDS, MS
http://orcid.org/0000-0002-6951-8794
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How to cite this article: Chatzopoulos GS, Cis-
neros A, Sanchez M, Wolff LF. Systemic medical
conditions and periodontal status in older individuals.
Spec Care Dentist. 2018;1–9. https://doi.org/10.1111/
scd.12319