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J Am Dent Assoc, Vol 132, No 7, 875-880. © 2001 American Dental Association

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COVER STORY
JADA Continuing Education

Results of a prospective study

	ABSTRACT

TOP ABSTRACT Early evidence of periodontal... Retrospective vs. prospective... METHODS RESULTS DISCUSSION CONCLUSION REFERENCES

 
Background. Previous studies have suggested that chronic periodontal infection may be associated with preterm births. The authors conducted a prospective study to test for this association.

Methods. A total of 1,313 pregnant women were recruited from the Perinatal Emphasis Research Center at the University of Alabama at Birmingham. Complete periodontal, medical and behavioral assessments were made between 21 and 24 weeks gestation. After delivery, medical records were consulted to determine each infant’s gestational age at birth. From these data, the authors calculated relationships between periodontal disease and preterm birth, while adjusting for smoking, parity (the state or fact of having born offspring), race and maternal age. Results were expressed as odds ratios and 95 percent confidence intervals, or CIs.

Results. Patients with severe or generalized periodontal disease had adjusted odds ratios (95 percent CI) of 4.45 (2.16–9.18) for preterm delivery (that is, before 37 weeks gestational age). The adjusted odds ratio increased with increasing prematurity to 5.28 (2.05–13.60) before 35 weeks’ gestational age and to 7.07 (1.70–27.4) before 32 weeks’ gestational age.

Conclusions. The authors’ data show an association between the presence of periodontitis at 21 to 24 weeks’ gestation and subsequent preterm birth. Further studies are needed to determine whether periodontitis is the cause.

Clinical Implications. While this large prospective study has shown a significant association between preterm birth and periodontitis at 21 to 24 weeks’ gestation, neither it nor other studies to date were designed to determine whether treatment of periodontitis will reduce the risk of preterm birth. Pending an answer to this important question, it remains appropriate to advise expectant mothers about the importance of good oral health.

Babies born prematurely are at a significant risk of developing serious and lasting health problems. Preterm delivery, or PTD, is the major cause of neonatal mortality and of nearly one-half of all serious long-term neurological morbidity.¹ In the United States, approximately 10 percent of women deliver before term (defined as 37 weeks’ gestational age), and PTDs at less than 32 weeks’ gestation constitute 1 to 2 percent of all births. PTD accounts for more than 60 percent of all neonatal mortality and for 50 percent of all perinatal health care costs in this country. While substantial strides have been made in the treatment of babies born prematurely, the incidence of prematurity continues to rise. Data from the National Center for Health Statistics and the March of Dimes show a 0.6 percent increase in preterm births between 1986 and 1990 and a 0.4 percent increase from 1990 to 1996 (Figure 1).²

View larger version (46K): [in this window] [in a new window]   Figure 1. Percentage change in preterm birth rate. Note the increase in the preterm birth rate. The National Center for Health Statistics/March of Dimes baseline percentage was 10 percent preterm births in 1986.

 

Pre-existing periodontal disease in the second trimester of pregnancy increases the risk of preterm birth.

Table 1 lists some of the major known risk factors for preterm births. Several characteristics are known to be associated with an elevated risk of experiencing PTD.³ Rural, poor and minority women have more preterm labor and deliveries than do middle-class women; those who have had a previous spontaneous PTD and those whose pre-pregnancy weight is less than 50 kilograms (110 pounds) are at the greatest risk. As often is the case with risk factors, however, the causal links between these observable characteristics and the PTD itself are not at all clear.

View this table: [in this window] [in a new window]   TABLE 1 RISK FACTORS FOR PRETERM BIRTH.

 
When using a risk factor to guide patient assessment and treatment planning, it is important to know whether the risk factor can be modified by either the patient or the clinician. Smoking, for example, is a known risk factor that clearly is modifiable (Table 1). A past history of preterm labor is just as clearly not modifiable, whereas a genetic tendency toward preterm labor (none has been identified yet) might be modifiable by appropriate therapy.

Characteristics that affect pregnancy outcomes, either directly or indirectly through health behaviors, are well-covered in an article by Kramer,⁴ in which he reviewed the determinants of low birthweight based on an extensive meta-analysis of more than 800 articles. Kramer classified the etiology of PTD into three major categories according to whether the causal factor is established, its contribution is of major importance and the characteristic is modifiable and, if so, over how long a period.

	Early evidence of periodontal disease as a potential risk factor for preterm birth.

TOP ABSTRACT Early evidence of periodontal... Retrospective vs. prospective... METHODS RESULTS DISCUSSION CONCLUSION REFERENCES

 
Chronic periodontitis has been proposed as a risk factor for preterm birth. Offenbacher and colleagues⁵ conducted a case-control study of 124 pregnant or postpartum women. Those with preterm or low-birthweight babies had significantly worse periodontal disease than did the control subjects who delivered babies at full term. Multivariate logistic regression models, controlling for other risk factors and covariates, indicated that periodontal disease is a significant risk factor, with impressively high odds ratios of 7.9 for mothers of preterm low-birthweight babies and 7.5 for mothers giving birth for the first time. The odds ratio is a customary way to express the risk of an undesirable outcome (such as PTD) in patients who have a condition (such as periodontitis) relative to patients who do not have the condition. An odds ratio of 1.0 means that the risk of an adverse outcome in a patient with periodontitis is the same as the risk for a subject without periodontitis. When the outcome may result from multiple causes, odds ratios need to be adjusted for other known risk factors, such as smoking, to the extent that data concerning these risks are available. Confidence intervals, or CIs, indicate the range of odds ratios that are explained by the data.

	Retrospective vs. prospective study designs.

TOP ABSTRACT Early evidence of periodontal... Retrospective vs. prospective... METHODS RESULTS DISCUSSION CONCLUSION REFERENCES

 
In a case-control study, patients who have experienced preterm labor (cases) are recruited after the births and are matched with patients (controls) whose deliveries were normal but who otherwise have similar personal and medical profiles. Periodontal examinations usually are performed after the birth, allowing for a clear comparison of the influence of this factor on outcome.

The major drawback of case-control and other cross-sectional studies is that they cannot show that the risk factor and the outcome occurred in a logical temporal order⁶; for example, that periodontitis was present before the preterm birth. Case-control studies can present another problem in that both a patient’s willingness to participate in a study and her postpartum health behaviors can be biased by the outcome being studied. A prospective study, in which all evaluations are conducted before delivery, overcomes these limitations.

Such a prospective study is under way at the University of Alabama at Birmingham, or UAB, and is being conducted jointly by clinical researchers from the department of periodontics and the department of obstetrics and gynecology. It draws its patient volunteers from a research program in perinatal health, from which we can efficiently abstract extensive medical information.

This article describes the design of this ongoing study and presents our results to date, linking periodontal disease to preterm birth. In addition, we offer some guidelines to practitioners on treating and advising their patients in the light of our current state of knowledge.

The best advice to give a woman contemplating pregnancy is to try to prevent periodontal disease from developing.

	METHODS

TOP ABSTRACT Early evidence of periodontal... Retrospective vs. prospective... METHODS RESULTS DISCUSSION CONCLUSION REFERENCES

 
Overall experimental design. We designed our study to correlate the presence of periodontitis in pregnant women assessed at 21 to 24 weeks’ gestation with the presence and severity of subsequent preterm births. Subjects were drawn from among subjects being studied by the Perinatal Emphasis Research Center, or PERC, at UAB. In this article, we report the results we obtained from the first 1,313 subjects to have delivered their babies.

Eligibility criteria. To be eligible for participation in this study, a pregnant woman must have attended one of the PERC study health clinics as an obstetric patient and have reached 21 to 24 weeks’ gestation. We obtained informed consent from each subject and, when possible, from the father. The study was reviewed and approved by UAB’s institutional review board, or IRB.

Exclusion criteria. We excluded subjects who required antibiotic prophylaxis—for example, for mitral valve prolapse with regurgitation. This exclusion was primarily in the interest of patient safety, but it also eliminated one potential source of confusion in the interpretation of study results. Since antibiotics could modify the risk factors being tested, patients taking antibiotics would complicate both this observational study and a future planned intervention study.

Medical data collection. After obtaining informed consent from the patient, a research nurse administered a study questionnaire covering the patient’s behavior and oral health history. We reviewed the patient’s prenatal medical record to obtain data not provided by the interview, including the patient’s age, race, parity (the state or fact of having born offspring), pre-pregnancy weight, height, medical diagnoses and blood pressure. After the baby’s birth, abstracted information concerning pregnancy complications and delivery information (including preterm labor, premature rupture of membranes and type of delivery) from the labor and delivery record and computerized it. Trained and standardized study nurses were responsible for collecting, recording and maintaining all medical data.

Oral examination. Each subject received an oral examination to check for dental caries and periodontal disease. We measured pocket depth and recession and calculated attachment loss. Full-mouth periodontal examinations also were performed, as partial recordings tend to underestimate the prevalence of disease and could have biased the results of the study.⁷ We did not take any radiographs, in the interest of patient safety.

Calibration of examiners. All dental examiners—a team of calibrated dental hygienists—received training using a series of standardized procedures, demonstrations and one-on-one tutorials. To assess intraexaminer and interexaminer error, we performed a calibration study in the periodontal research clinic after receiving full IRB approval and written informed consent from the subjects. Each examiner performed duplicate examinations of probing depth and attachment level in eight patients who had moderate periodontitis; none of the patients was pregnant. The examiners calculated error (defined as the mean of the absolute value of the difference between examinations) and the correlation between values at successive examinations. No examiner whose error exceeded 0.5 millimeter was allowed to participate further in the study.

Statistical analysis. We defined three levels of periodontal disease: periodontitis (three or more sites with attachment loss of 3 mm or more), generalized periodontal disease (90 or more sites with attachment loss of 3 mm or more) and no disease (less than three sites with 3 mm of attachment loss). We used descriptive statistics to characterize the population. We calculated odds ratios and 95 percent CIs for preterm birth and adjusted them for smoking, parity, race and maternal age. To explore the possibility of a "dose effect," we calculated separate adjusted odds ratios for preterm births before 37, 35 and 32 weeks.

	RESULTS

TOP ABSTRACT Early evidence of periodontal... Retrospective vs. prospective... METHODS RESULTS DISCUSSION CONCLUSION REFERENCES

 
The demographic characteristics and age distribution of the study population are shown in Table 2. We found significantly more periodontal disease among African-American subjects, who made up 82.68 percent of the population, than among Caucasians (² 22.59, P < .001).

View this table: [in this window] [in a new window]   TABLE 2 MATERNAL RACE (SELF-CLASSIFIED) AND AGE.

 
Figure 2 shows the unadjusted odds ratios for patients with generalized periodontal disease. Interestingly, we found that the odds ratios rise with increasing prematurity; that is, the association with periodontal disease is strongest when we focus on the most severe class of prematurity. It is important to note, however, that these unadjusted odds ratios do not account for other known risk factors.

View larger version (49K): [in this window] [in a new window]   Figure 2. Unadjusted odds ratios for preterm birth in patients with generalized periodontitis.

 
Figure 3 again presents results for patients with generalized periodontal disease, but in terms of odds ratios that have been adjusted for maternal smoking, parity, race and age. Among these first 1,313 subjects, the risk of preterm birth in subjects with generalized periodontitis was from 4.45 to 7.07 times higher than that in periodontally healthy patients. Again, the adjusted odds ratios rise with increasing prematurity. Specifically, subjects with severe or generalized periodontitis had adjusted odds ratios of 4.45 (95 percent CI, 2.16–9.18) for preterm delivery before 37 weeks’ gestational age. The odds ratio increased to 5.28 (95 percent CI, 2.05–13.60) for delivery before 35 weeks’ gestational age and increased again to 7.07 (95 percent CI, 1.70–27.40) for delivery before 32 weeks’ gestational age.

View larger version (49K): [in this window] [in a new window]   Figure 3. Adjusted odds ratios for preterm births in patients with generalized periodontitis. Note that the odds ratios rise with increasing prematurity. The odds ratios have been adjusted for smoking, parity, race and maternal age.

 

	DISCUSSION

TOP ABSTRACT Early evidence of periodontal... Retrospective vs. prospective... METHODS RESULTS DISCUSSION CONCLUSION REFERENCES

 
Two main points regarding periodontal disease and preterm birth may be drawn from our data. First, periodontal disease was present before the preterm births. While this does not prove a cause-and-effect relationship, it is a necessary condition. Second, in subjects with generalized or severe periodontitis, the odds of preterm births were greatest for women who gave birth to the most premature babies.

In other analyses,⁶ we have shown that the risk of experiencing preterm birth increases with increasing severity of periodontal disease.

This study also illustrates the importance of adjusting odds ratios for known risk factors. For example, smoking is a known risk factor for both preterm birth and periodontal disease; in the absence of adjusted odds ratios, the association between smoking and preterm birth and periodontitis could lead to a greatly exaggerated estimate of the importance of periodontal disease as a risk factor for preterm birth. Before applying risk data in a clinical context, one should always ask whether the odds ratios are adjusted and, if so, for what other factors.

While our data show that various patient subpopulations exhibit different patterns of both periodontal disease and preterm birth, it is not clear whether the causal linkages themselves vary among groups. We plan to study these effects in more detail in future analyses, so we can understand better the implications of such differences for diverse patient populations.

Explaining the biological mechanisms linking periodontal infection and preterm birth was beyond the scope of our study. One plausible mechanism begins with endotoxins resulting from gram-negative bacterial infections (such as periodontal disease). These endotoxins stimulate the production of cytokines and prostaglandins. It is known that prostaglandins and certain cytokines (interleukin-1ß, interleukin-6 and tumor necrosis factor-), in appropriate quantities, stimulate labor.^8–15 Our laboratory currently is studying these factors.

The weight of the evidence. Probably the central question for the dental practitioner is whether we have convincing evidence that treatment of periodontal disease will reduce the risk of preterm birth. The answer, on the basis of existing case-control studies and prospective and uncontrolled intervention studies, clearly is no.

Only a controlled intervention study is capable of unequivocally establishing a causal link between a treatment and an outcome. For this reason, randomized, placebo-controlled, double-blind studies are essential to test the efficacy, if any, of periodontal treatment in reducing the incidence of preterm birth. While opinions differ as to which treatments (for example, aggressive vs. minimal) should be tested, at least a test and a control group must be studied. A recent study by Mitchell-Lewis¹⁶ showed a prevalence of 19.9 percent preterm births without periodontal treatment and 13.5 percent with treatment. Its lack of randomization, however, makes interpretation difficult. As a next step, we are conducting a randomized, placebo-controlled, blinded intervention trial.

Advising the patient. For the present, in the absence of definitive intervention data, the best advice to give a woman contemplating pregnancy is to try to prevent periodontal disease from developing. Regardless of what may be discovered, this strategy has the sure and immediate benefit of minimizing treatment when mother and fetus are most vulnerable.

	CONCLUSION

TOP ABSTRACT Early evidence of periodontal... Retrospective vs. prospective... METHODS RESULTS DISCUSSION CONCLUSION REFERENCES

 
This study provides additional evidence that pre-existing periodontal disease in the second trimester of pregnancy increases the risk of preterm birth. The odds of increased prematurity were increased 4.5- to 7.0-fold.

Ongoing studies are addressing the question as to whether preterm births can be reduced by treating the periodontal disease.

	FOOTNOTES

Dr. Geurs is an assistant professor, Department of Periodontology, University of Alabama at Birmingham.

Dr. Reddy is a professor, Department of Periodontology, University of Alabama at Birmingham.

Ms. Cliver is a statistician, Department of Obstetrics and Gynecology, University of Alabama at Birmingham.

Dr. Goldenberg is a professor, Department of Obstetrics and Gynecology, University of Alabama at Birmingham.

Dr. Hauth is a professor, Department of Obstetrics and Gynecology, University of Alabama at Birmingham.

This study was supported by National Institutes of Health grant IH HDP50 1HD33927.

	REFERENCES

TOP ABSTRACT Early evidence of periodontal... Retrospective vs. prospective... METHODS RESULTS DISCUSSION CONCLUSION REFERENCES

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by JEFFCOAT, M. K. Articles by HAUTH, J. C. Search for Related Content PubMed PubMed Citation Articles by JEFFCOAT, M. K. Articles by HAUTH, J. C. Related Collections Periodontics