Periodontitis and osteoporosis: a systematic review

CLIMACTERIC 2010;13:523–529

Periodontitis and osteoporosis: a systematic review Ma A´. Martı´nez-Maestre, C. Gonza´lez-Cejudo, G. Machuca*, R. Torrejo´n and C. Castelo-Branco{ Gynecology Division, Hospitales Universitarios Virgen del Rocı´o, Seville; *Faculty of Odontology, University of Seville; {Clinic Institute Gynecology, Obstetrics and Neonatology, Hospital Clinic, University of Barcelona, IDIBAPS, Spain Key words: PERIODONTITIS, OSTEOPOROSIS, BONE MINERAL DENSITY, BONE FRACTURE, DENTAL LOSS

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ABSTRACT Background Osteoporosis and periodontitis are frequent disorders that affect aging populations. It has been hypothesized that both conditions may be related. Objective To determine whether dental osteoporosis is a local manifestation of systemic bone loss having similar etiology and risk factors, or whether it is an independent process depending primarily on factors that cause periodontitis. Methods A systematic review of clinical trials assessing the relationship between osteoporosis and periodontitis was carried out. An electronic search was made based on Internet search engines, MEDLINE (from 1966 to December 2009) and the Cochrane Controlled Clinical Trials Register. Results A total of 145 studies dealing with the relationship osteoporosis–periodontitis were identified. Of them, 35 were considered suitable for selection. Studies on maxillary and/or mandible radiological findings have a positive correlation in the majority of the cases (18 positive vs. three negative), whereas the findings on clinical periodontal examination are inconclusive (six positive vs. five negative). There were ten studies in which a diagnosis of osteoporosis was made, based on the existence of non-traumatic fracture, while there were nine studies using radiographs for diagnosis, of which six studies were found to have a positive correlation. There was only one study based on a clinical periodontal examination that found a positive correlation. Conclusions The majority of the studies suggested a relationship between osteoporosis and periodontitis. Further well-controlled studies are needed to better elucidate the inter-relationship between systemic and oral bone loss and to clarify whether dentists could usefully give an early warning for osteoporosis risk.

INTRODUCTION Osteoporosis and periodontitis are frequent conditions affecting middle-aged and elderly women1–3. Both diseases affect bone mass and share common risk factors4; for these reasons, it has been postulated that they may be related. No reports linking both conditions have been published up to 19605 and only in recent years has such a relationship been suggested6. Based on

the premise that bone resorption occurs at the same time in the mandible as in the rest of the skeleton, tooth loss7 and non-traumatic fracture8 may be manifestations of the same condition. Systemic imbalance in bone resorption might manifest in the alveolar bone earlier than in other bones; however, data from studies designed to support this hypothesis are controversial.

Correspondence: Dr C. Castelo-Branco, Institut Clı´nic de Ginecologia, Obstetrı´cia i Neonatologı´a, Hospital Clı´nic, Villarroel 170, 08036 Barcelona, Spain

REVIEW ª 2010 International Menopause Society DOI: 10.3109/13697137.2010.500749

Received 05-04-2010 Revised 29-05-2010 Accepted 05-06-2010

Periodontitis and osteoporosis

Martı´nez-Maestre et al.

Up to now, most of the studies on the relationship between periodontitis and osteoporosis have serious methodological drawbacks including small sample size, limited control of potential confounding factors, and inconsistent definitions of periodontitis and osteoporosis. The aim of this systematic review is to elucidate whether dental osteoporosis is a local manifestation of systemic bone loss having similar etiology and risk factors, or whether it is an independent process depending primarily on factors that cause periodontitis.

MATERIAL AND METHODS Climacteric Downloaded from informahealthcare.com by 84.76.84.112 on 12/01/10 For personal use only.

Studied conditions Osteoporosis is defined as a skeletal disorder characterized by low bone mass and microarchitectural deterioration of bone tissues, leading to enhanced bone fragility, with consequential increase in fracture risk9,10. The outcome of this condition is the appearance of nontraumatic fracture1,11. The detection of people at risk is based on risk factors (Table 1) and on measurement of bone mineral density (BMD)12. Periodontitis or periodontal disease is an inflammatory process characterized by loss of connective tissue and alveolar bone. It is generally accepted that the single, most important, etiological factor in periodontitis is subgingival dental plaque with its concurrent bacterial infection, leading to loss of epithelial attachment and loss of alveolar bone13,14. Like osteoporosis, it is a silent disease, being asymptomatic until late when mobile teeth, abscesses and tooth loss may occur. In addition, periodontitis and osteoporosis have several risk factors in common (Table 1).

The definition of periodontitis is based on two sets of criteria: radiological criteria, which evaluate systemic and mandible/maxilla bone loss (jaw BMD, thickness of the jaw cortex, jaw width), and clinical criteria based on periodontal charting, including exploration of gingival tissues and grades of inflammation and recession. The different studies use either only one15,16 or both of these sets of criteria17–23.

Search design To identify all of the articles that describe a relationship between osteoporosis and periodontitis, the following search strategy was designed: (Osteoporosis or Bone loss OR Bone fracture OR Bone mineral density) and periodontitis. This strategy was adapted and applied to different Internet search engines, to the MEDLINE database and to the Cochrane Controlled Trials Register. There was no language or date restriction. Controlled and randomized studies were included that evaluated the relationship between osteoporosis and periodontitis. One reviewer (A.M.M.) independently evaluated the eligibility of the trials. One reviewer (C.G.C.) extracted the data from the selected articles using a prefixed protocol (information was gathered on the characteristics of participants in the trial, the intervention and how the results were measured). Of the reviewed articles, those that did not establish a relationship between diseases, literature reviews or those whose purpose was to demonstrate a therapeutic impact were not considered. In the final selection of articles (Tables 2 and 3), only those using diagnostic techniques that are currently recognized to diagnose systemic osteoporosis were considered: double photon absorptiometry (DPA), tomography and dual-energy X-ray absorptiometry (DXA).

Statistical methods Table 1 Risk factors for osteoporosis and periodontitis Osteoporosis Female gender Caucasian or Asian Genetics Menopause Hypogonadism Hyperparathyroidism Hyperthyroidism High protein intake Low vitamin D or calcium intake Alcohol abuse Sedentarism Low peak bone mass Drugs: heparin Low weight

524

Common

Periodontitis

Tobacco Poor nutritional status Advanced age Glucocorticoid therapy Immunological diseases

Bacterial dental plaque Stress Diabetes Pregnancy

The correlations between periodontal disease and systemic osteoporosis were analyzed for each variable, accepting that, in the same study, these could have a positive correlation for certain variables and negative for others. The correlation between the different odontological variables was eliminated, analyzing only those directly related to periodontitis and systemic bone loss.

RESULTS From a total of 145 publications identified, 109 were not considered for further review (Figure 1). Among the 35 selected trials (Tables 2 and 3), ten used the presence of previous non-traumatic fractures as a diagnostic criterion for osteoporosis (see Figure 1 and Table 3). The relationship between osteoporosis and periodontitis was established using six non-discriminative

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Table 2 Studies assessing the relationship between osteoporosis and periodontitis Type of study*

Von Wowern Kribbs24

1988 1989

3 3

18 85

Kribbs17

1990

3

50

Elders18

1992

1, 4

286

Klemetti25 Krall38 Klemetti19 May39 Mohammad20 Hildebolt45 Mohammad21

1993 1994 1994 1995 1996 1997 1997

3 4 4 4 1 1 1, 4

74 329 227 874 52 155 44

Taguchi26 Weyant22

1999 1999

3, 4 1, 4

90 293

Tezal6 Lundstrom23

2000 2001

1, 3 1

70 36

Jonasson27

2001

3

80

Mohammad16 Yoshimoto46 White28 Taguchi50 Taguchi29 Ishii51 Brennan15 Brennan30

2003 2005 2005 2007 2007 2007 2007 2008

1 3 3 3 3 3 1 3

30 40 227 450 455 54 329 1256

44

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Diagnostic criteria

Year

Authors

n

Periodontitis

Osteoporosis

DPA mandible (þ) occlusal, periapical and panoramic radiographs (microdensitometry) (þ) occlusal, periapical and panoramic radiographs (microdensitometry) (þ), DP ABH (7), DP (7), bleeding (7), tooth loss (þ) RRR (þ) tooth loss (þ) tooth loss (þ), CPITN (7) tooth loss women (þ/7) men (þþ) CAL (þ), plaque, DP, gingival index (7) CAL (7) CAL (þ), gingival recession (þ), tooth loss (7) tooth loss (þ), RRR (þ) tooth loss (7), dental plaque (7), DP (7), bleeding (7) CAL(7), alveolar bone loss (þ) gingival bleeding (7), DP (7), gingival recession (7), marginal bone level (7) interdental alveolar thickness (þ), mandibular alveolar thickness (þ), trabeculation (þ) tooth loss (þ), CAL (þ) alveolar BMD (þ) MCW (þ) and shape (þ) MCW (þ) and shape (þ) ABH (7), MCW(þ) alveolar bone loss (7) CAL (þ) ACH (þ) 570 years old and (7) 4 70

DPA lumbar spine and forearm SPA radius, DPA and CT in lumbar spine radiograph of spine (no fracture), DPA and CT lumbar spine DPA L2–L4, metacarpal cortical thickness DXA spine and hip SPA forearm; DPA spine and hip DXA spine and hip DXA spine and hip DPA spine DXA spine and hip DXA spine CT spine DEXA spine and hip, SPA wrist, history of fracture DXA lumbar spine and femur DXA hip DXA forearm

DXA DXA DXA DXA DXA DXA DXA DXA

spine spine, calcaneus ultrasound spine and femoral neck spine spine and femoral neck femoral neck spine, hip and forearm spine, hip and forearm

DPA, dual photon absorptiometry; SPA, single photon absorptiometry; CT, computerized tomography; DP, probing depth; ABH, alveolar bone height; RRR, residual ridge resorption; DXA, dual-energy X-ray absorptiometry; CPITN, maximum value of community periodontal index of treatment needs; CAL, clinical attachment loss; BMD, bone mineral density; MCW, mandibular cortical width; ACH, alveolar crest height *, 1, systemic osteoporosis vs. periodontitis; 2, osteoporotic fracture vs. periodontitis; 3, systemic osteoporosis vs. mandibular osteoporosis; 4, systemic osteoporosis vs. tooth loss; 5, osteoporotic fracture vs. mandibular osteoporosis; 6, osteoporotic fracture vs. tooth loss

comparators (Table 4). Most of the studies focused on the relationship between mandible osteoporosis and systemic osteoporosis (12 out of 13) and demonstrated a positive association. In addition, the association between mandible osteoporosis and non-traumatic fractures was observed in six out of eight studies. Few studies have been designed to elucidate an association of dental loss with systemic osteoporosis and fractures. In most of them, a positive correlation was found (five out of seven and three out of three

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related dental loss to osteoporosis and to fractures, respectively) (Table 4). Data from studies utilizing clinical criteria to diagnose periodontitis (periodontal charting) are more controversial. Those considering periodontitis and bone mass in the lumbar spine and hip (nine studies), demonstrate, in four cases, positive and, in five cases, negative correlations. Additionally, only in one study based on fractures, a positive correlation was observed (Tables 2 and 3).

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Table 3 Diagnostic criteria for osteoporosis and periodontitis in the studies assessing fractures

Year

n

Periodontitis

Kribbs

1983

5

30

Astro¨m47 Kribbs17

1990 1990

6 2, 5

566 112

Von Wowern36 Von Wowern31 Taguchi7

1992 1994 1995

5 2, 5 5, 6

28 26 64

Hirai37 Xie41 Bollen8 White28

1993 1999 2000 2005

5 6 5 5

44 293 198 598

mandibular bone mass (microdensitometry) (mandibular second premolar and first molar) (þ) tooth loss (þ) occlusal, periapical and panoramic radiographs (þ); DP (7) DPA mandible and maxillar; RRR (7) DPA mandible (þ); plaque, gingival bleeding, CAL (þ) tooth loss (þ), MCW (7), mandible alveolar bone resorption (7) RRR (7) tooth loss (þ) cortical thickness (þ) trabecular pattern (þ)

Authors 33

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Diagnostic criteria

Type of study*

Osteoporosis vertebral fractures hip fracture vertebral fractures osteoporotic fracture osteoporotic fracture vertebral fracture osteoporotic fracture osteoporotic fracture osteoporotic fracture hip fracture

DPA, dual photon absorptiometry; DP, probing depth; RRR, residual ridge resorption; CAL, clinical attachment loss; MCW, mandibular cortical width *, 1, systemic osteoporosis vs. periodontitis; 2, osteoporotic fracture vs. periodontitis; 3, systemic osteoporosis vs. mandibular osteoporosis; 4, systemic osteoporosis vs. tooth loss; 5, osteoporotic fracture vs. mandibular osteoporosis; 6, osteoporotic fracture vs. tooth loss

Figure 1 Flow chart of trial selection process

In general, studies based on maxilla and/or mandible radiological findings demonstrated a higher positive correlation with osteoporosis (18 positive vs. three negative) than the studies based on

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periodontal examination (six positive vs. five negative) (Table 2). Among the studies using non-traumatic fractures as the diagnostic criterion for osteoporosis, a positive

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Periodontitis and osteoporosis

Martı´nez-Maestre et al.

Table 4 Different studies assessing the relationship between osteoporosis and periodontitis Type of study

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Systemic osteoporosis vs. periodontitis Systemic osteoporosis vs. mandibular osteoporosis Systemic osteoporosis vs. tooth loss Osteoporotic fracture vs. periodontitis Osteoporotic fracture vs. mandibular osteoporosis Osteoporotic fracture vs. tooth loss

Number of studies

Positive association

Negative association

9

4

5

13

12

1

7

5

2

1

1

0

8

6

2

3

3

0

correlation with periodontitis was found in six out of eight studies. On the other hand, the studies using periodontal examination as the diagnostic criterion for periodontitis showed a positive correlation with osteoporosis only in one case (Table 3).

DISCUSSION Risk factors (Table 1) and biological plausibility suggest that systemic bone loss could increase the risk of developing osteoporotic fractures and affect the mandible at the same time, and also increase the risk of developing periodontitis and, consequently, tooth loss. The pathogenesis of tooth loss involves both local and systemic factors. Infection is believed to be a necessary, but not a sufficient, component of periodontal disease progression. Although it has been considered to be a key local factor, several studies have failed to demonstrate a consistent relationship between periodontal disease and tooth loss. The unclear effect of local factors in the pathogenesis of tooth loss has led to consideration of the role of systemic factors. Demonstration of a relationship between osteoporosis and periodontitis is complex because both are multifactorial diseases and both share common mechanisms. Thus, a biological plausibility exists suggesting that at least part of the periodontal destruction is influenced by systemic bone loss. Most of the studies tend to demonstrate that periodontitis is an early warning sign of osteoporosis. Therefore, periodontitis could be used as a screening tool to identify individuals at high risk for osteoporosis who would benefit from preventive or therapeutic measures. In practice, this is a controversial topic probably due to the diverse criteria used to define osteoporosis and periodontitis in the literature. Cross-sectional designs have focused on BMD instead of bone fractures, small samples, different techniques

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for measuring BMD and different places in the skeleton to measure it and these are confounding factors that may make a comprehensive analysis more difficult. The correlation between periodontitis and systemic osteoporosis is generally positive when the definition of periodontitis is based on radiological criteria6,7,17,24–30; however, when clinical criteria for periodontitis are used, the results are controversial16,18–23,31. This is probably due to the fact that the radiological criteria for periodontitis are well defined and few in number, whereas there are at least 14 different definitions of periodontitis based on clinical criteria32. Radiological criteria also allow inclusion of edentulous women, which is a frequent condition in osteoporotic patients, usually of older age24,25,33–41. Current trends in osteoporosis are focused more on fracture prevention than on BMD. In this sense, it is noteworthy that most of the initial studies assessing the relationship between periodontitis and osteoporosis use, as diagnostic criteria, radiological examinations, DPA17,18,20,24,38,44 and DXA6,15,16,19–23,25,27–30,39,45,46 and only ten studies have been carried out in women having osteoporotic fractures7,8,17,28,31,33,36,37,41,47. Moreover, the majority of these were hindered by being non-prospective studies, of small sample size7,31,33,36,49,50 and with limited control of other potential confounding factors. Most of them were also based on mandible and/or maxilla examinations for periodontitis diagnosis7,8,17,28,36,49 and only one31 was based on a clinical examination. Von Wowern found a positive correlation between fracture and tooth loss, which links the final consequences of osteoporosis and periodontitis. The main drawback of this study was the small number of subjects included (12 women with fractures vs. 14 controls). To the best of our knowledge, there are only two prospective studies that assess the relationship between osteoporosis and periodontitis, with inconsistent results. Pilgram and colleagues48, after 3 years of women receiving postmenopausal hormone replacement therapy, did not find a correlation between periodontitis and femoral and lumbar spine BMD, assessed by DXA, whereas a positive correlation of calcaneous ultrasonography with dental loss and clinical attachment level was found by Yoshihara and colleagues49. In conclusion, after a comprehensive review, most of the questions related to this topic remain unresolved. Does the mandible experience similar bone loss to that observed in the spine after menopause? Does mandible bone density influence the rate of bone loss due to periodontitis or the loss of teeth? Could the periodontal examination be used to detect the population at higher risk for osteoporosis? Can strategies for prevention and treatment of osteoporosis and periodontitis be shared? Therefore, at present, the

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Periodontitis and osteoporosis

real relationship between periodontitis and osteoporosis remains unclear and further studies are warranted to clarify the exact role and effect of one condition on the other and the corresponding clinical implications.

Martı´nez-Maestre et al.

Conflict of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. Source of funding

Nil.

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