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J Am Dent Assoc, Vol 139, No 10, 1389-1397.
© 2008 American Dental Association
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TRENDS

The Relationship of Periodontal Disease to Diseases and Disorders at Distant Sites

Communication to Health Care Professionals and Patients



Ira B. Lamster, DDS, MMSc, Dominick P. DePaola, DDS, PhD, Rui V. Oppermann, DDS, PhD, Panos N. Papapanou, DDS, PhD and Rebecca S. Wilder, BSDH, MS


   ABSTRACT
TOP
 ABSTRACT
BACKGROUND
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Background. The body of research defining relationships among periodontal disease and certain systemic diseases and disorders has been expanding, and questions have been raised regarding what information should be conveyed to health care professionals and patients.

Methods. Representatives from dentistry, medicine, the academic community and the insurance industry convened a two-day workshop July 23 and 24, 2007.

Results. The workshop participants achieved general consensus on a number of issues, including the need for greater cooperation between the health care professions. This cooperation should translate into improved clinical care as physicians refer patients for dental care, and dentists are proactive in regard to the general health of their patients.

Conclusion. Communication to health care professionals requires a multifaceted approach that includes publication of research findings in medical and dental journals, cooperation among professional organizations and initiatives at the local level such as presentations at medical grand rounds. Dental schools should play a role in their health science centers. Communication with patients may improve through the use of targeted informational brochures in the offices of medical specialists, appropriate media campaigns and efforts led by local dental organizations.

Practice Implications. It is too early to provide specific recommendations regarding the treatment of periodontal disease to improve specific health outcomes, but dentists can become advocates for a general health promotion and disease prevention message. The lifestyles approach includes an improved diet, smoking cessation, appropriate hygiene practices and stress reduction. These strategies can improve oral and general health outcomes.

Key Words: Periodontal diseases; health promotion; communication; oral health

Abbreviations: HPDP: Health promotion and disease prevention

In 2000, a report titled Oral Health in America by the U.S. surgeon general expressed a need for action that included plans to "change perceptions regarding oral health and disease so that oral health becomes an accepted component of general health" and to "accelerate the building of the science and evidence base and apply science effectively to improve oral health."1 During the last 20 years, extensive research has been published on the relationship of oral infection and inflammation to diseases and disorders of tissues and organs at distant sites; this is referred to as the relationship between oral and systemic health.

In 2006, the Global Oral and Systemic Health Summit was held to evaluate the state and future directions of such research. The consensus opinion that was attained at the summit was published in 2007.2 As a follow-up to the 2006 summit, a two-day oral care workshop titled "Oral and Systemic Diseases: From Bench to Chair—Putting Information Into Practice" was held July 23 and 24, 2007. Workshop participants from around the world, including representatives from the dental and medical professions, the academic community and the insurance industry, convened to develop consensus opinion on the topic of communication about the relationship between oral diseases and other disorders.


   BACKGROUND
TOP
 ABSTRACT
 BACKGROUND
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
In 1912, Billings3 formalized the concept of focal infection. Since then, interest has waxed and waned in regard to oral infection’s contributing to diseases and disorders of tissues and organs at distant sites. The modern study of oral infection—and, by extension, oral inflammation—as a risk factor for other diseases began in 1989 with an article from Finnish authors on the association of dental disease and tooth loss with cardiovascular disease.4 In less than 20 years, a large body of literature has been published that supports the concept that periodontal disease can have adverse effects on tissues and organs at distant sites. Specifically, periodontal disease has been studied as a risk factor for cardiovascular and cerebrovascular diseases,5,6 respiratory diseases,7,8 adverse pregnancy outcomes9,10 and poor metabolic control in patients with diabetes mellitus.11,12 Other associations have been proposed with diseases such as renal disease,13 pancreatic cancer14 and rheumatoid arthritis.15,16

Despite an expanding body of literature on the effect of periodontal infection and inflammation on other diseases, evidence from treatment studies has not been sufficient to allow for the establishment of specific treatment recommendations.

Bacteria initiate periodontal disease, but the tissue destruction in periodontitis is believed to be caused by the intensity of the resultant inflammatory response. Inflammation is important in the pathogenesis of many diseases that were not considered previously to have an inflammatory etiology. The literature relating oral inflammation and periodontal disease to cardiovascular and cerebrovascular diseases includes epidemiologic data,17,18 animal studies,19,20 clinical studies (including those that identified DNA from the microflora associated with periodontitis in atheromatous plaques21,22) and functional studies.23,24

The association of periodontal disease and diabetes mellitus has been recognized for more than 100 years, and periodontitis has been proposed as the sixth clinical complication of diabetes mellitus.25 Research results suggest that periodontal disease can have an adverse effect on metabolic control and, when periodontitis is present in a patient with diabetes mellitus, treatment of periodontal disease can improve glycemic control.26

The association of periodontitis and adverse pregnancy outcomes has been reported in clinical trials and observational studies.27,28 The potential pathways include the effect of specific periodontal pathogens, or the effect of inflammatory mediators produced as part of periodontal disease, on the placenta and uterus.29 A systematic review of periodontal disease as a risk factor for adverse pregnancy outcomes showed that of 44 studies in which this relationship was examined, 29 showed an association and 15 did not.30,31 The authors concluded that there may be an association between periodontal disease and adverse pregnancy outcomes, but additional studies with greater methodological rigor are needed.

The oral cavity is an active reservoir for microorganisms that may cause bacterial pneumonia and lung abscess if they transmitted by means of aspiration or via an endotracheal tube, which can be colonized by microbial biofilms.32 Investigators conducted a study of 417 patients in long-term care facilities in Japan to examine the effect of provision of oral health care (toothbrushing after meals, occasional use of povidone iodine and weekly professional care) on indicators of respiratory disease.33 When they compared residents who received this care with residents who did not receive care across two years, they found that the treatment group had a lower percentage of people with fever, with pneumonia and who died.

Despite an expanding body of literature on the effect of periodontal infection and inflammation on other diseases, evidence from treatment studies has not been sufficient to allow for the establishment of specific treatment recommendations due, in part, to difficulty in elucidating treatment study protocol methodologies to evaluate oral and systemic connections. For example, in a 2007 article, investigators observed that intensive periodontal therapy in patients with periodontitis was associated with improved endothelial cell function (flow-mediated dilatation) across six months.34 However, the effect of periodontal therapy on specific cardiovascular outcomes has been examined in only one pilot treatment trial.35 This trial evaluated the effect of periodontal therapy on secondary cardiovascular events. When the investigators compared people who received nonsurgical periodontal therapy (test group) with those who received community care (control group), they found no differences in the number of adverse events. Additional analysis revealed that a higher percentage of patients in the community care group experienced serious adverse events, but this percentage did not reach statistical significance (6.6 percent versus 3.3 percent; P = .19).

With the realization that infection and inflammation can affect metabolic control adversely, investigators have examined the effect of treatment of periodontitis on metabolic control in diabetes mellitus, specifically the effect of periodontal therapy on serum levels of glycosylated hemoglobin. Some data suggest that periodontal disease can affect metabolic control and that periodontal treatment can have a beneficial effect, especially in patients with poor metabolic control (that is, those with glycosylated hemoglobin levels higher than 9 or 10 percent).36,37

Results from a limited number of studies suggest that periodontal therapy decreases the rate of preterm low–birth-weight babies in populations of women with periodontal disease,27,38 and the results of a meta-analysis of treatment trials suggests that periodontal therapy can reduce the overall rate of preterm low–birth-weight babies but not the rate of preterm birth or the rate of low–birth-weight babies.31 These data were not sufficient, however, for the authors to recommend periodontal therapy during pregnancy to reduce adverse pregnancy outcome. The results of a multicenter randomized controlled treatment trial sponsored by the National Institute of Dental and Craniofacial Research failed to demonstrate a reduction in preterm births when periodontal care was delivered to women in the second trimester,39 although the results from this study also showed that delivery of nonsurgical periodontal services in the second trimester is safe.40 Trials have not yet been conducted to examine the effects of periodontal therapy on renal disease, pancreatic cancer or rheumatoid arthritis.

Although study results concerning the influence of periodontal disease on other nonoral disorders are not conclusive, when viewed in the context of how infection and low-grade inflammation have been associated with diseases not traditionally considered to have an infectious etiology, there is adequate reason to believe that these associations are biologically plausible and may affect patient morbidity. In light of this new understanding of periodontal disease as a possible risk factor for other diseases and conditions, emerging evidence of the systemic benefits of periodontal therapy and the safety of periodontal treatment even for pregnant women, it is important to communicate information about the relationship of oral inflammation and other diseases to health care professionals and to the public. Furthermore, the literature published on the link between oral health and diseases and disorders of tissues and organs at distant sites has caused considerable debate about larger issues such as the relationship between the dental and medical professions, the potential role of dentists in general health care and how these findings should modify what dental students are learning. The result is a healthy dialogue that will affect the future of the dental profession.

Using evidence-based knowledge about oral-systemic links to improve health care practices will require a collaboration between dental, medical and health insurance professionals, as well as innovative approaches in establishing true interdisciplinary patient care. Communicating information about these important relationships to health care providers both in and outside of the dental office, as well as to consumers, is essential. Although causality remains unclear and it is premature to suggest treatment protocols, it is necessary to determine how to disseminate this knowledge without causing confusion as to what conclusions should be drawn and what actions are required.


   METHODS
TOP
 ABSTRACT
 BACKGROUND
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Members of the academic dental community, dentists, dental hygienists, physicians, nurses and representatives from dental insurance carriers and professional dental societies convened a two-day workshop in July 2007. Participants were from the United States, Australia, Europe, South America and Japan.

After reviewing new research data on the relationship of oral infection and inflammation to nonoral diseases and disorders, participants discussed two questions—What are the key messages that health care professionals need to understand? What is the primary public health message that should be communicated to the general public?—at breakout sessions. In the first breakout session, participants were divided into groups according to specific systemic disorders: cardiovascular and cerebrovascular diseases, respiratory diseases, diabetes mellitus and adverse pregnancy outcomes. Then the participants were divided into groups according to profession (dentists and dental hygienists, physicians and nurses, and others, including representatives of professional dental societies and the health insurance industry) and were asked to discuss the same two questions. After these small group discussions, workshop participants reconvened to derive consensus opinions regarding the communication of the relationship of periodontal disease to other diseases and disorders.


   RESULTS
TOP
 ABSTRACT
 BACKGROUND
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
The participants in the workshop achieved consensus on a number of opinions regarding the communication of information about links between periodontal disease and other disorders (Box 1Go40). Workshop participants agreed that although most dental professionals are aware of the relationship between periodontal disease and other specific disorders, other health care professionals are not. This disparity likely is because of the volume of information they receive and the lack of defined paths that join dentistry and medicine. Workshop participants concluded that innovative methods of action and information transfers are needed to improve communication among health care professionals in different disciplines. Actions were suggested (Box 2Go).41,42 Likewise, workshop participants also suggested techniques for communicating these messages to the general public (Box 3Go, page 1394).


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  		BOX 1 Consensus opinions derived at the workshop.

 

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  		BOX 2 Suggestions for communicating to health care professionals.

 

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  		BOX 3 Suggestions for communicating to the general public.

 

   DISCUSSION
TOP
 ABSTRACT
 BACKGROUND
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
In 1998, the American Academy of Periodontology began a campaign to inform consumers about the connection between oral and general health. Information regarding this link and recommendations for maintaining good oral health are available online43–46 (TableGo, page 1395). Other organizations have expressed their stances about the relationships between oral and systemic health, some of which relate to specific disease states (TableGo).


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  		TABLE Statements about the relationship between oral diseases and systemic disorders.

 
Although evidence supporting an association between periodontal disease and other diseases and disorders is not sufficient to establish causality or warrant specific treatment recommendations, workshop participants concluded that current knowledge warrants broad communication of established links. Increased awareness can help health care professionals improve health care outcomes. Workshop participants provided suggestions for communicating to health care professionals and to the public to raise awareness of these relationships without causing confusion as to what actions should be taken.

Information transfer and translation of new knowledge into clinical practice A fundamental question that arises from the topic of this workshop is how new knowledge translates into changes in clinical care. Despite a growing body of literature on different methods for changing provider behavior, this process has not been outlined clearly. In a review of 41 systematic reviews of various interventions used for changing clinical practice, Grimshaw and colleagues47 concluded that active methods, as well as models that incorporate a variety of strategies to change behavior, are more effective, and passive approaches are ineffective. They also noted that no interventions were effective in all situations.

In another study, the authors concluded that continuing education events, including meetings and workshops, and outreach visits yielded changes in professional practice when active techniques are used.48 Audit and feedback, which allow providers to gauge how they provide care in relationship to their peers and accepted guidelines, also are moderately effective, but results are inconsistent.49 Results of a survey of different community-based health care facilities showed that public health professionals involved in decision making prefer to receive research information from Web sites, journals, e-mails, and conferences or workshops in the form of executive summaries, abstracts and original articles.50 The authors of this survey emphasized the need for researchers and policymakers to collaborate to develop a format that presents information that is easily adapted to evidenced-based health care.

Unlike the processes of synthesizing data and implementing changes in practice, which are prevalent in the literature, the process of translating evidence into recommendations for change has not been thoroughly addressed. The National Institute for Health and Clinical Excellence in the United Kingdom has implemented guideline development groups to study this process. That effort aims to illuminate the psychological theories and social influences underlying this process by observing a sample of guideline development groups over time.51 Furthermore, a report of a consensus meeting focused on implementation of best practices in medicine concluded that physicians do not always provide care that is in agreement with accepted recommendations and guidelines. Although this meeting was focused on improving the level of compliance, the conclusions can apply to the translation of findings related to the broader implications of oral infection and inflammation. The conference emphasized the importance of engaging leaders in the profession in this effort, participation by all parties, broad-based communication strategies and local meetings focusing on moving toward a consensus.52

Disseminating new knowledge about the implications of periodontal disease to health care professionals will require a broad effort that must occur on the national level of professional organizations, as well as at the regional and local levels, as dentists and scientists involved in this research speak to their colleagues in medicine at hospital grand rounds and other venues. It is the responsibility of organized dentistry and the dental schools, functioning as part of their medical centers, to promote communication of this information. The National Institutes of Health can play an important role by convening consensus conferences on this topic. For the individual practitioner, active versus passive learning appears to be important.

Targeting specific medical disciplines seems warranted, with a focus on obstetricians, cardiologists, pulmonary medicine specialists, endocrinologists and others involved in the care of patients (for example, diabetes educators and nurses). This targeting can and must occur at the level of national organizations, as well as at the regional and local levels. An example of this targeting is the workshop discussed in this article.53 There is preliminary evidence that groups of physicians for whom the relationship of periodontal disease and other disorders are particularly important have some degree of awareness that periodontal disease is a risk factor for systemic disease. A 2007 mail survey of obstetricians in North Carolina yielded 55 respondents, for a 40 percent return rate. When asked about risk factors for preterm low–birth-weight babies, 84 percent reported that they were aware of the possible contribution of periodontal disease to preterm low–birth-weight outcomes.54 However, only 22 percent of respondents reported that they performed an evaluation of the oral cavity during patients’ initial visits.

In 2008, North Carolina researchers surveyed 504 nurse practitioners, physician assistants and nurse midwives regarding their knowledge, behaviors and opinions about periodontal disease and adverse pregnancy outcomes.55 A total of 240 practitioners responded, for a 48 percent response rate. Of these, 63 percent reported that they performed an oral health examination only at patients’ initial visits. Only 20 percent agreed or strongly agreed that their knowledge about periodontal disease was current. All agreed that nurse practitioners, physician assistants and nurse midwives should be taught about periodontal disease, and 95 percent agreed they should collaborate with dental professionals to reduce patients’ risks of an adverse pregnancy outcome.

Health promotion and disease prevention. The translation of research and clinical findings that link oral infection and inflammation to diseases and disorders affecting tissues and organs at distant sites also can be considered in the context of health promotion and disease prevention (HPDP). Dental practice places an emphasis on disease prevention, because the most common oral diseases—caries and periodontal disease—and those oral diseases associated with substantial morbidity and mortality (for example, oral squamous cell cancer) are preventable. Nevertheless, the high rates of dental disease are a testament that patients do not follow the advice they receive, nor do they always practice the appropriate self-care that is an essential component of health. This outcome is a problem when oral health interventions are attempted in economically disadvantaged communities.56 It also is compounded since the increased prevalence of chronic diseases, including oral diseases, is linked to lower socioeconomic status.

Watt57 reviewed strategies for HPDP for oral diseases in the context of efforts made by the World Health Organization. Watt argued that the historical lifestyle approach, in which patients receive education about oral health care and then modify their behavior so that oral health improves, is naive and generally unsuccessful. Lifestyle changes require a change in human behavior, and knowledge alone is insufficient to change health behaviors. However, oral health care programs often are delivered without consideration of other public health initiatives, and incorporation of efforts to improve oral health into a general effort to improve approaches to chronic diseases, including obesity, diabetes mellitus, cardiovascular and cerebrovascular diseases, and cancer, may be a more effective strategy. This general health message involves a focus on improving diet, cessation of smoking, appropriate hygiene practices, reducing stress and avoiding unsafe behaviors. Incorporation of the oral health care message will be advantageous because there is one general theme delivered to patients and multiple, positive outcomes. Of even greater importance, "the common risk approach provides a rationale for partnership(s)."57 This HPDP strategy is an ideal way to deliver the message that oral health is fundamental to general health and that oral infection and inflammation are linked to diseases and disorders of tissues and organs at distant sites.

Clinical practice implications Dentists should consider incorporating into their dental practices primary health care activities such as smoking cessation programs, screening for undiagnosed or poorly managed diabetes mellitus or a more general health care screening for serum risk markers for cardiovascular or cerebrovascular diseases. The authors of a recent report described an algorithm that incorporates a periodontal examination into an approach to identify patients with undiagnosed diabetes mellitus.58 In a more general sense, it would be reasonable to test patients for undiagnosed diabetes mellitus if they have periodontitis and other related findings and health problems are reported.

Another example is health care professionals who care for critically ill patients and are increasingly concerned about patients’ avoiding respiratory infections that are associated with substantial morbidity, mortality and increased length of stay for hospitalized patients. Simple oral hygiene measures and disinfection of endotracheal tubes may be an effective way to control these nosocomial infections.

Gingival inflammation can develop during pregnancy, and occasionally this can cause clinically noticeable problems. Practicing good oral hygiene and appropriate professional care generally can prevent gingival inflammation from occurring. Dentists, dental hygienists, obstetricians, nurses, nurse practitioners and other health care providers involved in the care of pregnant women need to emphasize the importance of oral health care during pregnancy to their patients.


   CONCLUSIONS
TOP
 ABSTRACT
 BACKGROUND
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
It is important that educational programs be established to help health care professionals understand the link between oral infection and other diseases and disorders. In addition, patients need to be informed about the importance of oral health and the potential sequelae of longstanding, untreated periodontal infections. The result of these efforts will be improved oral health and general health outcomes.


   FOOTNOTES
 

Dr. Lamster is a professor and the dean, College of Dental Medicine, Columbia University, 630 W. 168th St., New York, N.Y. 10032, e-mail "ibl1{at}columbia.edu". Address reprint requests to Dr. Lamster.


Dr. DePaola is president emeritus, The Forsyth Institute, Boston; and a professor and special programs director, College of Dental Medicine, Nova Southeastern University, Fort Lauderdale, Fla.


Dr. Oppermann is the dean of the School of Dentistry and the chair of the Department of Periodontology, Federal University of Rio Grande do Sul, Porto Alegre, RS, Brazil.


Dr. Papapanou is a professor of Dental Medicine; the chair, Section of Oral and Diagnostic Sciences; and the director, Division of Periodontics, College of Dental Medicine, Columbia University, New York City.


Ms. Wilder is an associate professor and the director, Graduate Dental Hygiene Education, School of Dentistry, University of North Carolina, Chapel Hill.


Disclosures. None of the authors reported any disclosures.


The workshop discussed in this study was sponsored by Johnson & Johnson Consumer & Personal Products Worldwide, a Division of Johnson & Johnson Group of Consumer Companies, New Brunswick, N.J.


The authors thank C. Michael Fullem, BS, who was a clinical research assistant, Johnson & Johnson (Morris Plains, N.J.), for his help with the preparation of this manuscript.


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 BACKGROUND
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
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