Letters to the Editor
J Periodontol • July 2014
the data of the control group at initial assessment, which occurred at 15 weeks of gestation; no data on the periodontal status of women in the control group are shown later in pregnancy. Thus, it is not possible to know whether the periodontal status of control women at the end of pregnancy was poorer or better than at the initial assessment, or whether it was similar to that of the treatment group. PT performed over two 1-hour sessions appears to be insufficient to assure the control of periodontal infection in pregnant women with chronic periodontitis, especially if maintenance treatment was not provided, as occurred in the Pirie study and in the Offenbacher et al. study.2 Early periodontal treatment during pregnancy does not preclude the periodontal condition from worsening later in gestation. As Armitage5 suggested, it is critically important that clinical trials designed to evaluate the effect of periodontal therapy on general health outcomes must include clinically acceptable targeted endpoints for successful periodontal therapy. Nestor J. Lo´pez, Department of Research and Postgraduate Studies, Faculty of Dentistry, University Andre´s Bello, Santiago, Chile. The author reports no conflicts of interest related to this letter. REFERENCES 1. Pirie M, Linden G, Irwin C. Intrapregnancy non-surgical periodontal treatment and pregnancy outcome: A randomized controlled trial. J Periodontol 2013;84: 1391-1400. 2. Offenbacher S, Beck JD, Jared HL, et al.; Maternal Oral Therapy to Reduce Obstetric Risk (MOTOR) Investigators. Effects of periodontal therapy on rate of preterm delivery: A randomized controlled trial. Obstet Gynecol 2009;114:551-559. 3. Macones GA, Parry S, Nelson DB, et al. Treatment of localized periodontal disease in pregnancy does not reduce the occurrence of preterm birth: Results from the Periodontal Infections and Prematurity Study (PIPS). Am J Obstet Gynecol 2010;202:147.e1-147e8. 4. Michalowicz BS, Hodges JS, DiAngelis AJ, et al. Treatment of periodontal disease and the risk of preterm birth. N Engl J Med 2006;355:1885-1894. 5. Armitage GC. Effect of periodontal therapy on general health — is there a missing component in the design of these clinical trials? J Clin Periodontol 2008;35:10111012. 6. Lo´pez NJ, Smith PC, Gutierrez J. Periodontal therapy may reduce the risk of preterm low birth weight in women with periodontal disease: A randomized controlled trial. J Periodontol 2002;73:911-924. 7. Lo´pez NJ, Da Silva I, Ipinza J, Gutierrez J. Periodontal therapy reduces the rate of preterm low birth weight in women with pregnancy-associated gingivitis. J Periodontol 2005;76:2144-2153. 8. Smulow JB, Turesky SS, Hill RG. The effect of supragingival plaque removal on anaerobic bacteria deep
periodontal pockets. J Am Dent Assoc 1983;107:737742. 9. Gomes SC, Nonnenmacher C, Susin C, Oppermann RV, Mutters R, Marcantonio RAC. The effect of a supragingival plaque-control regimen on the subgingival microbiota in smokers and never-smokers: Evaluation by real-time polymerase chain reaction. J Periodontol 2008;79:2297-2304. 10. Westfelt E, Rylander H, Dahlen G, Lindhe J. The effect of supragingival plaque control on the progression of advanced periodontal disease. J Clin Periodontol 1998; 25:536-541. 11. Gomes SC, Benetti F, Susin C, Oppermann R, Chierici RA. Effect of supragingival plaque control in smokers and never-smokers: 6-month evaluation of patients with periodontitis. J Periodontol 2007;78:1515-1521. Submitted October 22, 2013; accepted for publication October 22, 2013. doi: 10.1902/jop.2014.130626
Authors’ Response We thank Professor Lo´pez for his comments on our study of the effects of periodontal treatment provided during pregnancy.1 We recruited pregnant women with periodontitis, which was identified as the exposure. Periodontal treatment, which consisted of subgingival scaling and root planing (SRP) delivered over two visits by an experienced periodontist, resulted in significant improvements in clinical measures (probing depth and clinical attachment levels). The reduction in the percentage of sites that exhibited bleeding on probing (BOP) was in line with the changes identified in the Obstetrics and Periodontal Therapy (OPT) study,2 although less than those reported for other studies.3-5 There were differences between the various intervention studies in relation to the populations treated; whether the participants had gingivitis or periodontitis; and, importantly, in relation to the treatments provided as outlined in the comprehensive review by Michalowicz and colleagues.6 The concept of ‘‘eliminating the exposure’’ is raised in the letter, suggesting that this could be considered as an achievable endpoint of periodontal treatment. We are not aware of any intervention studies during pregnancy that have abolished periodontal inflammation. Therefore, the best that might be achieved is a reduction in risk if periodontal inflammation is reduced. The corollary is that residual high levels of periodontal inflammation as shown by the higher percentage of sites with BOP following treatment as reported in our study1 and in OPT2 are associated with little or no reduction in risk. To investigate this further, we completed a secondary analysis of our data to look for possible associations between the level of response to treatment (as 881
Letters to the Editor
measured by reduction in BOP) and birth outcome measures. Women in the test SRP group were divided into three subgroups in relation to the magnitude of the percent reduction in BOP, and we found no significant differences or trends in gestational age or birth weight standard deviation score across these subgroups. We designed this Belfast-based study some years ago based on the evidence that was available at that time and prior to the helpful analysis provided by Armitage,7 which suggested the need to consider endpoints. We did not specify periodontal treatment endpoints for the intervention we tested (SRP), nor are we aware of other studies investigating this relationship which did. It is difficult to envisage how a study could take place on this basis during pregnancy, as it would mean that some women would require numerous visits and significantly more treatment episodes than others, reflecting the variability in the response to periodontal treatment. On a more practical note, we are not aware that specific endpoints for such studies have been proposed. Observational studies provide little guidance about what threshold (in terms of residual probing depths, BOP, etc.) might be needed to achieve a reduction in risk of adverse pregnancy outcomes. Perhaps the periodontal research community should consider the concept of treatment to a predefined endpoint and reach consensus on how such an approach could be taken in relation to randomized controlled trials of the effects of interventions aimed at reducing risks associated with periodontal inflammation. Our study was planned with a focus on subject compliance and compared an intervention of SRP delivered over two sessions with supragingival cleaning. Both are treatment regimens that might reasonably be provided by dentists to their patients during pregnancy. From an ethical standpoint, we considered the delivery of basic oral hygiene information and simple supragingival cleaning to be essential in the control arm. We acknowledge that this supragingival treatment could have impacted the periodontal health of control subjects; however, any such effect would have been substantially less than the active treatment (SRP).8 We acknowledge that it would have been useful to have recorded periodontal data for the women in the control group later in pregnancy to demonstrate whether their periodontal status was better or worse than at initial assessment. However, this was not possible given manpower and time constraints and our focus on reducing pressures on the participants in the study. On the other hand, from a public health viewpoint if simple, more accessible, less risky periodontal treatment could reduce the risk of preterm low birth weight delivery, then surely this would be easier to implement and 882
Volume 85 • Number 7
provide than the time-consuming and often intensive periodontal therapy regimens currently being offered. However, we acknowledge that the solution is unlikely to be so simple. In conclusion, the precise relationship between maternal periodontal disease and adverse pregnancy outcomes such as low birth weight and preterm delivery continues to be the focus of much interest and debate. The consistent finding of recent systematic reviews and meta-analyses of randomized controlled trials is that non-surgical periodontal treatment delivered early in pregnancy does not alter the rates of low birth weight or preterm births and thus provision of periodontal treatment is not recommended as a method of improving pregnancy outcomes.9-11 We believe the results of this randomized controlled intervention trial1 carried out in Belfast, Northern Ireland add further weight to these findings. Martina Pirie and Chris Irwin, Center for Dental Education, School of Medicine, Dentistry, and Biomedical Sciences, Queen’s University Belfast, Belfast, Northern Ireland, UK; Gerry J. Linden, Center for Public Health, School of Medicine, Dentistry, and Biomedical Sciences, Queen’s University Belfast. The authors report no conflicts of interest related to this letter. REFERENCES 1. Pirie M, Linden G, Irwin C. Intrapregnancy non-surgical periodontal treatment and pregnancy outcome: A randomized controlled trial. J Periodontol 2013;84: 1391-1400. 2. Michalowicz BS, Hodges JS, DiAngelis AJ, et al. Treatment of periodontal disease and the risk of preterm birth. N Engl J Med 2006;355:1885-1894. 3. Lo´pez NJ, Smith PC, Gutie´rrez J. Periodontal therapy may reduce the risk of preterm low birth weight in women with periodontal disease: A randomized controlled trial. J Periodontol 2002;73:911-924. 4. Lo´pez NJ, Da Silva I, Ipinza J, Gutie´rrez J. Periodontal therapy reduces the rate of preterm low birth weight in women with pregnancy-associated gingivitis. J Periodontol 2005;76(11 Suppl.):2144-2153. 5. Offenbacher S, Lin D, Strauss R, et al. Effects of periodontal therapy during pregnancy on periodontal status, biologic parameters and pregnancy outcomes: A pilot study. J Periodontol 2006;77:2011-2024. 6. Michalowicz BS, Gustafsson A, Thumbigere-Math V, Buhlin K. The effects of periodontal treatment on pregnancy outcomes. J Periodontol 2013;84(Suppl. 4): S195-S208. 7. Armitage GC. Effect of periodontal therapy on general health — is there a missing component in the design of these clinical trials? J Clin Periodontol 2008;35:10111012. 8. Kaldahl WB, Kalkwarf KL, Patil KD, Dyer JK, Bates RE. Evaluation of 4 modalities of periodontal therapy.
Letters to the Editor
J Periodontol • July 2014
Mean probing depth, probing attachment level and recession changes. J Periodontol 1988;59:783-793. 9. Polyzos NP, Polyzos IP, Zavos A, et al. Obstetric outcomes after treatment of periodontal disease during pregnancy: Systematic review and meta-analysis. BMJ 2010;341:c7017. 10. Uppal A, Uppal S, Pinto A, et al. The effectiveness of periodontal disease treatment during pregnancy in reducing the risk of experiencing preterm birth and low birth weight: A meta-analysis. J Am Dent Assoc 2010;141:1423-1434.
11. Chambrone L, Pannuti CM, Guglielmetti M, Chambrone LA. Evidence grade associating periodontitis with preterm birth and/or low birth weight: II: A systematic review of randomized trials evaluating the effects of periodontal treatment. J Clin Periodontol 2011;38:902914. Submitted February 26, 2014; accepted for publication February 26, 2014. doi: 10.1902/jop.2014.140140
883
J Periodontol • July 2014
the data of the control group at initial assessment, which occurred at 15 weeks of gestation; no data on the periodontal status of women in the control group are shown later in pregnancy. Thus, it is not possible to know whether the periodontal status of control women at the end of pregnancy was poorer or better than at the initial assessment, or whether it was similar to that of the treatment group. PT performed over two 1-hour sessions appears to be insufficient to assure the control of periodontal infection in pregnant women with chronic periodontitis, especially if maintenance treatment was not provided, as occurred in the Pirie study and in the Offenbacher et al. study.2 Early periodontal treatment during pregnancy does not preclude the periodontal condition from worsening later in gestation. As Armitage5 suggested, it is critically important that clinical trials designed to evaluate the effect of periodontal therapy on general health outcomes must include clinically acceptable targeted endpoints for successful periodontal therapy. Nestor J. Lo´pez, Department of Research and Postgraduate Studies, Faculty of Dentistry, University Andre´s Bello, Santiago, Chile. The author reports no conflicts of interest related to this letter. REFERENCES 1. Pirie M, Linden G, Irwin C. Intrapregnancy non-surgical periodontal treatment and pregnancy outcome: A randomized controlled trial. J Periodontol 2013;84: 1391-1400. 2. Offenbacher S, Beck JD, Jared HL, et al.; Maternal Oral Therapy to Reduce Obstetric Risk (MOTOR) Investigators. Effects of periodontal therapy on rate of preterm delivery: A randomized controlled trial. Obstet Gynecol 2009;114:551-559. 3. Macones GA, Parry S, Nelson DB, et al. Treatment of localized periodontal disease in pregnancy does not reduce the occurrence of preterm birth: Results from the Periodontal Infections and Prematurity Study (PIPS). Am J Obstet Gynecol 2010;202:147.e1-147e8. 4. Michalowicz BS, Hodges JS, DiAngelis AJ, et al. Treatment of periodontal disease and the risk of preterm birth. N Engl J Med 2006;355:1885-1894. 5. Armitage GC. Effect of periodontal therapy on general health — is there a missing component in the design of these clinical trials? J Clin Periodontol 2008;35:10111012. 6. Lo´pez NJ, Smith PC, Gutierrez J. Periodontal therapy may reduce the risk of preterm low birth weight in women with periodontal disease: A randomized controlled trial. J Periodontol 2002;73:911-924. 7. Lo´pez NJ, Da Silva I, Ipinza J, Gutierrez J. Periodontal therapy reduces the rate of preterm low birth weight in women with pregnancy-associated gingivitis. J Periodontol 2005;76:2144-2153. 8. Smulow JB, Turesky SS, Hill RG. The effect of supragingival plaque removal on anaerobic bacteria deep
periodontal pockets. J Am Dent Assoc 1983;107:737742. 9. Gomes SC, Nonnenmacher C, Susin C, Oppermann RV, Mutters R, Marcantonio RAC. The effect of a supragingival plaque-control regimen on the subgingival microbiota in smokers and never-smokers: Evaluation by real-time polymerase chain reaction. J Periodontol 2008;79:2297-2304. 10. Westfelt E, Rylander H, Dahlen G, Lindhe J. The effect of supragingival plaque control on the progression of advanced periodontal disease. J Clin Periodontol 1998; 25:536-541. 11. Gomes SC, Benetti F, Susin C, Oppermann R, Chierici RA. Effect of supragingival plaque control in smokers and never-smokers: 6-month evaluation of patients with periodontitis. J Periodontol 2007;78:1515-1521. Submitted October 22, 2013; accepted for publication October 22, 2013. doi: 10.1902/jop.2014.130626
Authors’ Response We thank Professor Lo´pez for his comments on our study of the effects of periodontal treatment provided during pregnancy.1 We recruited pregnant women with periodontitis, which was identified as the exposure. Periodontal treatment, which consisted of subgingival scaling and root planing (SRP) delivered over two visits by an experienced periodontist, resulted in significant improvements in clinical measures (probing depth and clinical attachment levels). The reduction in the percentage of sites that exhibited bleeding on probing (BOP) was in line with the changes identified in the Obstetrics and Periodontal Therapy (OPT) study,2 although less than those reported for other studies.3-5 There were differences between the various intervention studies in relation to the populations treated; whether the participants had gingivitis or periodontitis; and, importantly, in relation to the treatments provided as outlined in the comprehensive review by Michalowicz and colleagues.6 The concept of ‘‘eliminating the exposure’’ is raised in the letter, suggesting that this could be considered as an achievable endpoint of periodontal treatment. We are not aware of any intervention studies during pregnancy that have abolished periodontal inflammation. Therefore, the best that might be achieved is a reduction in risk if periodontal inflammation is reduced. The corollary is that residual high levels of periodontal inflammation as shown by the higher percentage of sites with BOP following treatment as reported in our study1 and in OPT2 are associated with little or no reduction in risk. To investigate this further, we completed a secondary analysis of our data to look for possible associations between the level of response to treatment (as 881
Letters to the Editor
measured by reduction in BOP) and birth outcome measures. Women in the test SRP group were divided into three subgroups in relation to the magnitude of the percent reduction in BOP, and we found no significant differences or trends in gestational age or birth weight standard deviation score across these subgroups. We designed this Belfast-based study some years ago based on the evidence that was available at that time and prior to the helpful analysis provided by Armitage,7 which suggested the need to consider endpoints. We did not specify periodontal treatment endpoints for the intervention we tested (SRP), nor are we aware of other studies investigating this relationship which did. It is difficult to envisage how a study could take place on this basis during pregnancy, as it would mean that some women would require numerous visits and significantly more treatment episodes than others, reflecting the variability in the response to periodontal treatment. On a more practical note, we are not aware that specific endpoints for such studies have been proposed. Observational studies provide little guidance about what threshold (in terms of residual probing depths, BOP, etc.) might be needed to achieve a reduction in risk of adverse pregnancy outcomes. Perhaps the periodontal research community should consider the concept of treatment to a predefined endpoint and reach consensus on how such an approach could be taken in relation to randomized controlled trials of the effects of interventions aimed at reducing risks associated with periodontal inflammation. Our study was planned with a focus on subject compliance and compared an intervention of SRP delivered over two sessions with supragingival cleaning. Both are treatment regimens that might reasonably be provided by dentists to their patients during pregnancy. From an ethical standpoint, we considered the delivery of basic oral hygiene information and simple supragingival cleaning to be essential in the control arm. We acknowledge that this supragingival treatment could have impacted the periodontal health of control subjects; however, any such effect would have been substantially less than the active treatment (SRP).8 We acknowledge that it would have been useful to have recorded periodontal data for the women in the control group later in pregnancy to demonstrate whether their periodontal status was better or worse than at initial assessment. However, this was not possible given manpower and time constraints and our focus on reducing pressures on the participants in the study. On the other hand, from a public health viewpoint if simple, more accessible, less risky periodontal treatment could reduce the risk of preterm low birth weight delivery, then surely this would be easier to implement and 882
Volume 85 • Number 7
provide than the time-consuming and often intensive periodontal therapy regimens currently being offered. However, we acknowledge that the solution is unlikely to be so simple. In conclusion, the precise relationship between maternal periodontal disease and adverse pregnancy outcomes such as low birth weight and preterm delivery continues to be the focus of much interest and debate. The consistent finding of recent systematic reviews and meta-analyses of randomized controlled trials is that non-surgical periodontal treatment delivered early in pregnancy does not alter the rates of low birth weight or preterm births and thus provision of periodontal treatment is not recommended as a method of improving pregnancy outcomes.9-11 We believe the results of this randomized controlled intervention trial1 carried out in Belfast, Northern Ireland add further weight to these findings. Martina Pirie and Chris Irwin, Center for Dental Education, School of Medicine, Dentistry, and Biomedical Sciences, Queen’s University Belfast, Belfast, Northern Ireland, UK; Gerry J. Linden, Center for Public Health, School of Medicine, Dentistry, and Biomedical Sciences, Queen’s University Belfast. The authors report no conflicts of interest related to this letter. REFERENCES 1. Pirie M, Linden G, Irwin C. Intrapregnancy non-surgical periodontal treatment and pregnancy outcome: A randomized controlled trial. J Periodontol 2013;84: 1391-1400. 2. Michalowicz BS, Hodges JS, DiAngelis AJ, et al. Treatment of periodontal disease and the risk of preterm birth. N Engl J Med 2006;355:1885-1894. 3. Lo´pez NJ, Smith PC, Gutie´rrez J. Periodontal therapy may reduce the risk of preterm low birth weight in women with periodontal disease: A randomized controlled trial. J Periodontol 2002;73:911-924. 4. Lo´pez NJ, Da Silva I, Ipinza J, Gutie´rrez J. Periodontal therapy reduces the rate of preterm low birth weight in women with pregnancy-associated gingivitis. J Periodontol 2005;76(11 Suppl.):2144-2153. 5. Offenbacher S, Lin D, Strauss R, et al. Effects of periodontal therapy during pregnancy on periodontal status, biologic parameters and pregnancy outcomes: A pilot study. J Periodontol 2006;77:2011-2024. 6. Michalowicz BS, Gustafsson A, Thumbigere-Math V, Buhlin K. The effects of periodontal treatment on pregnancy outcomes. J Periodontol 2013;84(Suppl. 4): S195-S208. 7. Armitage GC. Effect of periodontal therapy on general health — is there a missing component in the design of these clinical trials? J Clin Periodontol 2008;35:10111012. 8. Kaldahl WB, Kalkwarf KL, Patil KD, Dyer JK, Bates RE. Evaluation of 4 modalities of periodontal therapy.
Letters to the Editor
J Periodontol • July 2014
Mean probing depth, probing attachment level and recession changes. J Periodontol 1988;59:783-793. 9. Polyzos NP, Polyzos IP, Zavos A, et al. Obstetric outcomes after treatment of periodontal disease during pregnancy: Systematic review and meta-analysis. BMJ 2010;341:c7017. 10. Uppal A, Uppal S, Pinto A, et al. The effectiveness of periodontal disease treatment during pregnancy in reducing the risk of experiencing preterm birth and low birth weight: A meta-analysis. J Am Dent Assoc 2010;141:1423-1434.
11. Chambrone L, Pannuti CM, Guglielmetti M, Chambrone LA. Evidence grade associating periodontitis with preterm birth and/or low birth weight: II: A systematic review of randomized trials evaluating the effects of periodontal treatment. J Clin Periodontol 2011;38:902914. Submitted February 26, 2014; accepted for publication February 26, 2014. doi: 10.1902/jop.2014.140140
883
