ORAL Boutigny HEALTH et al
Oral Infections and Pregnancy: Knowledge of Gynecologists/Obstetricians, Midwives and Dentists Hervé Boutignya/Marie-Laure de Moegenb/Luc Egeac/Zahi Badrand/François Boschine/Elisabeth Delcourt-Debruynef/Assem Soueidang Purpose: To establish an inventory of knowledge, attitudes and daily pratice of dental and medical practitioners in France regarding oral health care and its relationship to pregnancy, particularly to preterm delivery and low birth-weight infants. Materials and Methods: A questionnaire was distributed to health-care professionals (n= 460), consisting of 100 prenatal care practitioners (obstetricians, midwives) and 360 dentists, about their knowledge of oral alterations during pregnancy, the possible association between periodontal disorders and preterm/low birth weight, and their conduct toward their patients. Results: Bleeding gums and pregnancy gingivitis were the oral manifestations most often cited by all the practitioners. In contrast, prenatal care practitioners were unaware of epulis and a greater percentage of them than dentists believed caries risk to increase during pregnancy. The most adverse pregnancy outcomes cited were risk of premature delivery and chorioamniotis. Only dentists had received initial training on pregnancy complications. Finally, all health professionals point out the lack of continuing education on this topic. Conclusion: The present results underline the need for a better initial professional education and continuing education regarding pregnancy and oral health conditions and emphasise the need to update the guidelines in health care practices for pregnant women for a more effective prevention of risk-related adverse pregnancy outcomes, such as pre-term birth or pre-eclampsia. Key words: clinical practice, oral infections, pregnancy, questionnaire Oral Health Prev Dent 2016;14:41-47 doi: 10.3290/j.ohpd.a34376
a
Professor, Department of Periodontology, UFR d’Odontologie, University of Lille, France. Idea, experimental design, performed the experiment, contributed substantially to discussion, wrote the manuscript. b Dentist and Postgraduate Student, UFR d’Odontologie, University of Lille, France. Performed the experiment. c Dentist and Postgraduate Student, UFR d’Odontologie, University of Nantes, France. Contributed substantially to discussion. d Professor, Department of Periodontology, UFR d’Odontologie, University of Nantes, France. Contributed substantially to discussion, proofread the manuscript. e Associate Professor, Department of Periodontology, UFR d’Odontologie, University of Lille, France. Critical proofreading, contributed to discussion. f Professor and Head, Department of Periodontology, UFR d’Odontologie, University of Lille, France. Contributed substantially to discussion. g Professor and Head, Department of Periodontology, UIC Odontologie, UFR d’Odontologie, University of Nantes, France. Idea, performed the experimental design, proofread the manuscript, contributed substantially to discussion. Correspondence: Prof. Assem Soueidan, UFR d’Odontologie 1, Place Alexis Ricordeau, 44042 Nantes, France. Tel: +33-6-19112579. Email: [email protected]
Vol 14, No 1, 2016
Submitted for publication: 14.12.13; accepted for publication: 19.03.14
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esearch into the associations between periodontal diseases and various chronic systemic diseases and conditions has burgeoned rapidly in the past few years.9,17,19,22 To date, associations have been found between periodontal diseases and diabetes,26 cardiovascular diseases,7 metabolic syndrome/obesity 22 and adverse pregnancy outcomes.15 Recently, data have been published on the potential associations between periodontal diseases and respiratory diseases, rheumatoid arthritis or cancer, but these require further investigation.21 Caused by pathogenic microflora in the dental biofilm, periodontal diseases (gingivitis and periodontitis) are common inflammatory disorders affecting the tissues surrounding and supporting the teeth (periodontium).27 A variety of such biofilm microorganisms adjacent to the gingival crevice can contribute to the pathogenesis of periodontitis, but some of
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them – such as Porphyromonas gingivalis, Tannerella forsythensis, Treponema denticola and Aggregatibacter actinomycetemcomitans – are more pathogenic than others. Colonisation and proliferation of these bacteria are accompanied by the release of bacterial proteases, e.g. leucotoxins, collagenases or fibrinolysins, which damage periodontal tissue.29 In addition to the predominant role of pathogenic microorganisms in the genesis of periodontitis, genetic and environmental factors and especially tobacco use6 modify the immunological-inflammatory host response and the nature and importance of periodontal tissue breakdown. By nature, the host response to infection is essentially protective. But in a host susceptible to periodontitis, dental biofilm accumulation and especially a sustained microbial challenge could trigger an immune-inflammatory hyper-response. This results in enhanced tissue destruction via the activation of cell-mediated immunological responses, cytokine and prostanoid cascades, leading to the overproduction and release of interleukin-1 (IL-1), IL-6, tumour necrosis factor α (TNF- α) and prostaglandin E2 (PGE2).23 During the normal progression of pregnancy, there is an increase in the secretion of female sex hormones, i.e. estrogen by 10 fold and progesterone by 30 fold. These significant hormonal modifications induce several systemic as well as local physiological and physical changes in the pregnant woman’s body. The main systemic changes occur in the respiratory, circulatory, hematological, renal, gastrointestinal, endocrine, genitourinary and musculoskeletal systems. The local physical changes occur in the different parts of the body, including the oral cavity.12 Pregnant women may be more susceptible than other women to infection: the increased total blood volume and vasodilatation increase the dissemination of bacteria throughout the body. Further, pregnancy may alter the cell-mediated immune function resulting in a delayed immune response to infection.4,8 The increased levels of estrogen and progesterone also lead to hypervascularisation of the periodontium and changes in collagen production, increasing the vascular permeability and making the gingival tissue more susceptible to dental biofilm. This may exacerbate pre-existing gingivitis or worsen pre-existing periodontitis.4 An adverse pregnancy outcome is defined as an event that reduces the chance of having a healthy baby. Spontaneous preterm birth and preterm preeclampsia are two of the adverse pregnancy outcomes described. Preterm deliveries are those that
42
occur at under 37 weeks of gestational age, which happens in about 5% to 13% of births in many developed countries and is the leading cause of perinatal morbidity and mortality in these countries.14 Pre-eclampsia is a hypertensive, multisystem disorder of pregnancy that significantly contributes to maternal and fetal/neonatal morbidity and mortality. It is characterised by high blood pressure and significant amounts of protein in the urine of the pregnant woman. It is the most common of the serious pregnancy complications and may affect both the mother and fetus.2 Offenbacher et al25 were the first to report a link between poor maternal periodontal heath and preterm labour or low birth-weight infants and concluded that periodontal infection could be a risk factor for preterm birth or low birth weight. Since this report, numerous epidemiological and prospective studies have confirmed or refuted these findings.15 The Consensus Report of the Sixth European Workshop on Periodontology in 200817 indicated a likely association between periodontal disease and an increased risk of adverse pregnancy outcomes. More recently, a systematic review15 confirmed a significant association between maternal periodontitis and low birth-weight infants, preterm birth and pre-eclampsia. The exact pathogenic mechanisms involved in these associations remain controversial, but two main mechanisms have been postulated to explain how maternal periodontal disease could affect pregnancy outcomes.8,24,33 First, the uterine cavity of women with periodontal disease may become exposed to or colonised by periodontal bacteria or their products (e.g. lipopolysaccharides of Gram-negative bacteria), which reach the maternal-fetal unit and release an inflammatory cascade leading to premature rupture of membranes or to preterm spontaneous labour. The second mechanism suggests that cytokines generated locally within the diseased periodontal tissues, mainly IL-1, IL-6, TNF- α and prostaglandins (e.g. PGE2), may enter the systemic circulation and precipitate a similar cascade, again leading to spontaneous preterm labor and birth. Our current understanding of the role of periodontal diseases in health and particularly in adverse pregnancy outcomes has changed dramatically and will thus be gaining the attention of both medical and dental professionals in their clinical practice. Few studies have evaluated the knowledge, attitudes and daily practice of dental and medical practitioners regarding oral health care and its relationship to pregnancy, particularly to preterm delivery
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Table 1 Professional demographic data Number of professionals (n=460)
%
Midwives
70
15.21
Gynecologists/obstetricians
30
6.52
360
78.26
Professional
Dentists
Graduation year
PP (n=100)
%
DP (n=360)
%
PP +DP
%
1970 to 1979
12
12
34
9
46
10
1980 to 1989
24
24
119
33
143
31
1990 to 1999
25
25
67
19
92
20
2000 to 2012
39
39
140
39
179
39
Abbreviations: PP: prenatal care practitioner; DP: dental professionals. Percentage may not total to 100% due to rounding.
and low birth-weight infants.11,33,34 Hence, the purpose of this study was to determine the knowledge of French dentists and French prenatal care practitioners (obstetricians/gynecologists and midwives) regarding associations between oral health and pregnancy associations, and how they incorporate that knowledge into daily clinical practice.
MATERIALS AND METHODS This study utilised two questionnaires, A and B, designed for pregnancy professionals (gynecologists/ obstetricians and midwives) and dentists, respectively. Each questionnaire contained a total of 10 questions grouped into four parts to elicit information about: • the personal characteristics of the health-care practitioners and the nature of their initial and continuing professional education • their knowledge of oral alterations during pregnancy • their knowledge of the possible association between periodontal disorders and preterm/low birth weight • their conduct toward/treatment of their patients. Questionnaire A was distributed to prenatal care practitioners from the regional maternity hospital of Lille (Hôpital ‘mère-enfant’ Jeanne de Flandre) and from six other maternity hospitals in northern France (maternity hospital Saint Vincent de Paul of Lille, and maternity hospitals of Grande-Synthe, Armentieres, Béthune, Saint-Omer and Tourcoing). Questionnaire B was distributed to private dental practitioners in northern France.
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RESULTS 883 questionnaires were administered, 725 to dentists and 158 to prenatal care practitioners. The total response rate was 52%. Of the questionnaires administered, 460 health professionals, consisting of 100 prenatal care practitioners and 360 dentists, responded. Of the prenatal care practitioners, 30 were gynecologists/obstetricians and 70 were midwives. The response rate to questionnaire A (distributed to prenatal care practitioners) was 63% and to questionnaire B (distributed to dentists) was 49.6%. Any survey that was incomplete or filled out incorrectly was not counted in the final sample of health-care professionals (N = 460). The incomplete response rate was 7%. Their period of professional practice ranged from 2 to 42 years, with 59% of the health professionals having been in practice an average of 19 years (Table 1). Figures 1 to 3 show the different health professionals’ knowledge concerning oral infections, periodontal diseases and adverse pregnancy outcomes. Gingival bleeding and pregnancy-associated gingivitis were the oral manifestations most often reported by both dentists and prenatal care practitioners. Fewer dentists than prenatal care practitioners considered pregnancy to increase the risk of caries. Pyogenic granuloma was known to less than 10% of the prenatal care practitioners (Fig 1). Oral infection was clearly identified as a risk factor for adverse pregnancy outcomes (Fig 2) by 99% of prenatal care practitioners vs 90% of dentists. The most frequent adverse pregnancy outcomes mentioned as a consequence of a periodontal disease (Fig 3) were preterm birth (80% of the prenatal practitioners vs 50% of dentists) followed by chorioamnionitis (59% of
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Boutigny et al
100
PP% DP%
80 percent
60 40 20 0
isk
h
t oo
r ay ec
d
g
al
h ut
ul
o
m
iv ng
gi
t
r giv
d
te
cia
gin
c
i en
ss
a
m
lo
u an
gr
ce
s ab
g
o
ss
s
iti
ce
in
ed
e bl
o py
-a cy
an
gn
e pr
Fig 1 Oral manifestations associated with pregnancy reported by health professionals (PP: Prenatal care practitioners; DP: dental professionals).
100
PP% DP%
80
the prenatal care practitioners vs 40% of dentists) and low birth-weight babies (41% of prenatal care practitioners vs 15% of dentists). Almost 70% of prenatal care practitioners did not perform a systematic oral examination, even briefly, on their pregnant patients. Only if the pregnant patient mentioned specific dental pain or discomfort did the prenatal care practitioners perform an oral examination. More than half (51%) of prenatal care practitioners referred their pregnant patients for dental care only when they had poor oral conditions. Only 20% of them routinely advised their pregnant patients to seek dental care during pregnancy regardless of oral status (Table 2). Fifty-eight percent of the dentists responded that they rarely see pregnant patients (Table 3). Among the 48% of the health professionals whose initial professional education included oral care for pregnant women, 60% of the dentists had received such education while 95% of the prenatal care professionals had not. However, 85% of all the healthcare professionals wished to receive continuing education relating to dental care during pregnancy (Table 4).
percent
60
DISCUSSION
40 20 0
yes
no
Fig 2 Oral infections as a risk factor for adverse pregnancy outcomes reported by health professionals (PP: Prenatal care practitioners; DP: dental professionals).
100
PP% DP%
80 percent
60 40
This study sought to assess the knowledge and clinical practice behaviours of health-care professionals – prenatal care practitioners and dentists – concerning oral manifestations during pregnancy and the possible relationship between periodontal disease and preterm birth/low birth weight. Despite comprehensive data showing an association between oral infection and adverse pregnancy outcomes, which demonstrates that periodontal disease could be a risk factor for preterm/ low birth weight, many studies found health-care practitioners to have limited knowledge of this or a mismatch between daily clinical behaviours and this important health issue.1,11,13,28,32,34 The two main oral factors that prenatal care practitioners
20 0
tis
m
m
o
a rio
ch
am
l
-ec
e pr
er
e-t
ag
bi
m
pr
rh or
h ry
e
w
b ht
g
ei -w r th
em
liv
de
y ab
e
r th
ia
ps
ni
o ni
rs
he
bi
lo
Fig 3 Adverse pregnancy outcomes as a consequence of periodontal disease reported by health professionals (PP: Prenatal care practitioners; DP: Dental professionals).
44
Table 3 Frequency of dentists’ care of pregnant women
ot
%
n = 360
0
0
Infrequently
58
209
Often
40
144
Always
2
7
Never
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believed to be associated with pregnancy were an increase in caries risk and gingival manifestations, such as pregnancy-associated gingivitis or gingival bleeding. During pregnancy, the frequency of tooth decay and the number of decayed teeth among pregnant women have been reported to be high.31 In the present study, 30% of the dentists vs 49% of the prenatal care practitioners effectively believed that caries risk increases during pregnancy. The dentists’ percentage may appear low and could be surprising when compared to the prenatal care
practitioners’ percentage. An explanation for this may be that dentists rightly believe that the caries incidence is not directly due to pregnancy but rather to less effective oral health care, changes in dietary habits with more sugary snacks,29 an increase in the number of certain salivary cariogenic microorganisms and salivary pH modification.18 In this study, gingival bleeding and pregnancyassociated gingivitis were the gingival problems most frequently mentioned by the health professionals. These results are similar to those of a
Table 4 Education of health professionals on oral care of pregnant woman PP+DP (n=460)
PP+DP %
PP (n=100)
PP %
DP %
DP (n=360)
During your initial professional education, did you receive any instruction on oral care of pregnant women? Yes
221
48
5
5
216
60
No
239
52
95
95
144
40
Have you participated in postgraduate or continuing education on pregnancy and dental care? Yes
75
16
11
11
64
18
No
385
84
89
89
296
82
Do you wish to attend continuing education courses about pregnancy and dental care? Yes
393
85
91
91
302
84
No
67
15
9
9
58
16
Abbreviations: PP: prenatal care practitioner; DP: dental professionals. Percentage may not total to 100% due to rounding.
Table 2 Prenatal care practitioners’ clinical attitude in relation to dental care (n = 100) % Oral examination by the prenatal care practitioners during medical consultation Always
1
Often
5
Infrequently
27
Never
68
If yes, at which moment of the pregnancy? At the compulsory declaration of the pregnancy
5
During the first encounter with the pregnant woman
30
For a specific painful dental reason or discomfort reported by the patient
60
Other
5
In your pregnancy care protocol, do you refer your pregnant patient to a dentist? Never
12
When the patient seems to have poor oral conditions
51
Upon patient request
12
Always
20
Not documented
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5
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study conducted with Jordanian physicians1 and those of another survey by Egéa et al.13 All of these results are consistent with results of epidemiological studies reporting that approximately 40% of pregnant women have some form of periodontal disease19,20 and that gingival bleeding is the most frequent oral sign associated with pregnancy4 and reported by pregnant women. Pyogenic granuloma, also named ‘pregnancy epulis tumour’ or ‘granuloma gravidarum,’3 seemed to be unknown to prenatal care practitioners in this study. This fibrous inflammatory hyperplasia is mainly found on the marginal gingiva of the anterior areas and develops in up to 5% of pregnancies.16 Paradoxically, abscesses associated with pregnancy were frequently mentioned by the prenatal care practitioners, although it does not occur more frequently in pregnancy than in other clinical situations. An overwhelming majority of the health-care professionals in the present study were aware of the association between oral infections and adverse pregnancy outcomes. Our results are consistent with those of other authors,1,11,28 but some significant differences in the nature of the outcomes cited were found between dentists and prenatal care professionals. Where preterm birth and low-birth weight babies were the two outcomes mentioned most often by the prenatal care practitioners as well as the dentists, chorioamnionitis was rarely mentioned by the dentists and pre-eclampsia was almost never cited. Pre-eclampsia is a maternal multi-organ disorder unique to pregnancy with the clinical appearance of hypertension and proteinuria. Chorioamnionitis refers to inflammation of the amniochorionic membrane. It is the result of a polymicrobial infection and is estimated to be present in approximately 40% to 70% of women who deliver prematurely. Pre-eclampsia and chorioamnionitis are two of the leading causes of maternal and neonatal morbidity and mortality in the Western world.5,10 The possible link between chorioamnionitis and oral infections has not yet been studied, even though prenatal care practitioners reported it when asked about it.13 This is likely because chorioamnionitis is a common obstetric problem well known among prenatal care practitioners, whose focus is on urinary/vaginal infections rather than oral infection. In contrast, few dentists in our study knew of these two pregnancy complications, despite the fact that the latest publications show an association between oral infections, pre-eclampsia and adverse pregnancy outcomes.15 Moreover, prenatal care practitioners underestimated the possi-
46
ble role of periodontal diseases in increasing the risk of developing pre-eclampsia. Our results were consistent with the results of other studies.13 The clinical behaviour of the prenatal care practitioners in this study did not always seem to be consistent with the large number of them who are aware of the role of oral infections and periodontal diseases in adverse pregnancy outcomes. Indeed, oral examination was never or infrequently performed by more than 90% of these prenatal care practitioners, and almost two-thirds of them only performed an oral exam for specific, painful dental reasons or discomfort reported by the patient. They referred pregnant women to a dentist only when poor oral conditions were found or upon patient request, thus overlooking other latent or less apparent oral conditions, such as gingivitis or periodontitis. These results are consistent with those found in other, similar studies.13,34 The content of the training received by the prenatal care professionals regarding oral health and oral care could explain why they did not routinely refer the pregnant patients to dental care or why they did not perform a systematic oral examination. Omitting oral examinations is not so surprising because prenatal care practitioners are not trained to perform them, but it is surprising that they seem to be reluctant to refer patients to a dentist. Indeed, only 5% of the prenatal care professionals in the present study had received any such training during their initial education and only 11% had participated in continuing education on oral health during pregnancy. These results could explain why, in our study, 58% of the dentists only infrequently treated pregnant women. A large majority (85%) of both the dental and the prenatal care professionals wish to have continuing education in dental care related to pregnancy.
CONCLUSIONS Although the results of this study cannot be extrapolated, they clearly demonstrate that discrepancies exist between current evidence from the literature and French health care professionals’ knowledge/ recognition of as well as their behaviour regarding oral manifestations in pregnancy. Their awareness of periodontal diseases as risk factors for preterm birth or pre-eclampsia is insufficient. Furthermore, these results underline the need for better initial professional education and continuing continuing education on pregnancy and oral health conditions. Finally, the present study emphasises the need to
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update the guidelines for health-care practices for pregnant women to more effectively prevent riskrelated adverse pregnancy outcomes, such as preterm birth or pre-eclampsia.
REFERENCES 1. Al-Habashneh R, Aljundi SH, Alweli HA. Survey of medical doctors attitudes and knowledge of the association between oral health and pregnancy outcomes. Int J Dent Hygiene 2008;6:214–220. 2. American College of Obstetricians and Gynecologists. ACOG practice bulletin No. 33, January 2002. Diagnosis and management of preeclampsia and eclampsia. Obstet Gynecol 2002;99:159–167. 3. Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol 1999;4:1–6. 4. Barak S, Oettinger-Barak O, Machtei EE, Peled M, Ohel G. Common oral manifestations during pregnancy: a review. Obstet Gynecol Surv 2003;58:624–628. 5. Boggess KA, Lieff S, Murtha AP, Moss K, Beck J, Offenbacher S. Maternal periodontal disease is associated with an increased risk for preeclampsia. Obstet Gynecol 2003;1001:227–231. 6. Boutigny H, Boschin, Delcourt-Debruyne E. Periodontal diseases, tobacco and pregnancy. J Gynecol Biol Reprod 2005;3:S74–S83. 7. Buhlin K, Mantyla P, Paju S, Peltola JS. Periodontitis is associated with angiographically verified coronary artery disease. J Clin Periodontol 2011;38:1007–1014. 8. Cetin I, Pileri P, Villa A, Calabrese S, Ottolenghi L, Abati S. Pathogenic mechanisms linking periodontal diseases with adverse pregnancy outcomes. Reprod Sci 2012;19:633– 641. 9. Cullinan MP, Seymour GJ. Periodontal disease and systemic illness: will the evidence ever be enough? Periodontology 2000 2013;62:271–286. 10. Czikk MJ, McCarthy FP, Murphy KE. Chorioamnionitis: from pathogenesis to treatment. Clin Microbiol Infect 2011;17:13041311. 11. Da Rocha JM, Chaves VR, Urbanetz AA, Baldissera RDS, Rösing CK. Obstetricians’ knowledge of periodontal disease as a potential risk factor for preterm delivery and low birth weight. Braz Oral Res 2011;25:248–254. 12. Dellinger TM, Livingston HM. Pregnancy: Physiologic changes and considerations for dental patients. Dent Clin N Am 2006;50:677–697. 13. Egéa L, Le Borgne H, Samson M, Boutigny H, Philippe HJ, Soueidan A. Infections buccodentaires et complications de la grossesse: connaissances et attitudes des professionnelles de santé. Gynecol Obst Fert 2013;41:635-640. 14. Goldenberg RL, Culhane JF, Iams JD, Romero R. Epidemiology and causes of preterm birth. Lancet 2008;371:75–84. 15. Ide M, Papanaou PN. Epidemiology of association between maternal periodontal diseases and adverse pregnancy outcomes. Systematic review. J Periodontol 2013;(4 suppl):S181–S194. 16. Jafarzadeh H, Snatkhani M, Mohtasham N. Oral pyogenic granuloma: a review. J Oral Sci 2006;48:167–175.
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17. Kinane D, Bouchard Ph. On behalf of group of the European Workshop on Periodontology. Periodontal disease and health: consensus report of the Sixth European Workshop on Periodontology. J Clin Periodontol 2008;35(suppl 8):333–337. 18. Laine MA. Effect of pregnancy on periodontal and dental health. Acta Odontol Scand 2002;60:257–264. 19. Le Borgne H, Soueidan A, Caroit-Cambazard Y, Boutigny H, Jean-Baptiste K, Nguyen JM, Philippe HJ. Maladies parodontales et accouchements prématurés: étude clinique pilote. Gynecol Obste Fert 2011;39:399–401. 20. Lieff S, Boggess KA, Murtha AP, Jared H, Madianos PN, Moss K, Beck J, Offenbacher S. The oral conditions and pregnancy study: periodontal status of a cohort of pregnant women. J Periodontol 2004;75:116–126. 21. Linden GJ, Herzberg MC, and on behalf of working groupe 4 of the joint EFP/AAP workshop. Periodontitis and systemic diseases: a record of discussions of working group 4 of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. J Periodontol 2013;84(4 suppl):S20–S23. 22. Linden GJ, Lyons A, Scannapieco FA. Periodontal systemic associations: review of the evidence. J Clin Periodontol 2013;40(suppl 14):S8–S19. 23. Liu YCG, Lerner UH, Teng YTA. Cytokine responses against periodontal infection: protective and destructive roles. Periodontol 2000 2010;52:165–206. 24. Michalowicz BS, Durand R. Maternal periodontal disease and spontaneous preterm birth. Periodontol 2000 2007;44:103–112. 25. Offenbacher S, Katz V, Fertik G, Collins J, Boyd D, Maynor G et al. Periodontal infection as a possible risk factor for preterm low birth weight. J Periodontol 1996;67:1103–1113. 26. Preshaw PM, Alba AL, Herrera D, Jepsen S, Konstantinidis A, Makkrilakis S, Taylor R. Periodontitis and diabetes: a two-way relationship. Diabetologia 2012;55:21–31. 27. Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet 2005;366:1809–1820. 28. Shenoy RP, Nayak DG, Sequeira PS. Periodontal disease as a risk factor in preterm low birth weight – An assessment of gynecologists’ knowledge: a pilot study. Indian J Dent Res 2009;20:13–16. 29. Silk H, Douglass AB, Douglass JM, Silk L. Oral health during pregnancy. Am Fam Physicians 2008;77:1139–1144. 30. Socransky SS, Haffajee AD. Periodontal microbial ecology. Periodontol 2000 2005;38:137–187. 31. Vergnes JN, Kminski M, Lelong N, Musset AM, Sixou M, Nabet C, for the EPIPA study. Frequency and risk indicators of tooth decay among pregnant women in France. A cross sectional analysis. PloS ONE 2012;7(5):e33296. doi:101371 32. Wilder R, Robinson C, Jared HL, Lieff S, Bogess K. Obstetricians’ knoweldge and practice behaviors concerning periodontal health and preterm delivery and low birth weight. J Dent Hyg 2007;81:81-96. 33. Winner G, Pihlstrom BL. A critical assessment of adverse pregnancy outcome and periodontal disease. J Clin Periodontol 2008;35(suppl 8):380–397. 34. Zanata RL, Fernandes KBP, Navarro PSL. Prenatal dental care: evaluation of professional knowledge of obstetricians and dentist in the cities of Londirna/Pr and Bauru/ Sp, Brazil, 2004. J Appl Oral Sci 2008;16:194–200.
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Oral Infections and Pregnancy: Knowledge of Gynecologists/Obstetricians, Midwives and Dentists Hervé Boutignya/Marie-Laure de Moegenb/Luc Egeac/Zahi Badrand/François Boschine/Elisabeth Delcourt-Debruynef/Assem Soueidang Purpose: To establish an inventory of knowledge, attitudes and daily pratice of dental and medical practitioners in France regarding oral health care and its relationship to pregnancy, particularly to preterm delivery and low birth-weight infants. Materials and Methods: A questionnaire was distributed to health-care professionals (n= 460), consisting of 100 prenatal care practitioners (obstetricians, midwives) and 360 dentists, about their knowledge of oral alterations during pregnancy, the possible association between periodontal disorders and preterm/low birth weight, and their conduct toward their patients. Results: Bleeding gums and pregnancy gingivitis were the oral manifestations most often cited by all the practitioners. In contrast, prenatal care practitioners were unaware of epulis and a greater percentage of them than dentists believed caries risk to increase during pregnancy. The most adverse pregnancy outcomes cited were risk of premature delivery and chorioamniotis. Only dentists had received initial training on pregnancy complications. Finally, all health professionals point out the lack of continuing education on this topic. Conclusion: The present results underline the need for a better initial professional education and continuing education regarding pregnancy and oral health conditions and emphasise the need to update the guidelines in health care practices for pregnant women for a more effective prevention of risk-related adverse pregnancy outcomes, such as pre-term birth or pre-eclampsia. Key words: clinical practice, oral infections, pregnancy, questionnaire Oral Health Prev Dent 2016;14:41-47 doi: 10.3290/j.ohpd.a34376
a
Professor, Department of Periodontology, UFR d’Odontologie, University of Lille, France. Idea, experimental design, performed the experiment, contributed substantially to discussion, wrote the manuscript. b Dentist and Postgraduate Student, UFR d’Odontologie, University of Lille, France. Performed the experiment. c Dentist and Postgraduate Student, UFR d’Odontologie, University of Nantes, France. Contributed substantially to discussion. d Professor, Department of Periodontology, UFR d’Odontologie, University of Nantes, France. Contributed substantially to discussion, proofread the manuscript. e Associate Professor, Department of Periodontology, UFR d’Odontologie, University of Lille, France. Critical proofreading, contributed to discussion. f Professor and Head, Department of Periodontology, UFR d’Odontologie, University of Lille, France. Contributed substantially to discussion. g Professor and Head, Department of Periodontology, UIC Odontologie, UFR d’Odontologie, University of Nantes, France. Idea, performed the experimental design, proofread the manuscript, contributed substantially to discussion. Correspondence: Prof. Assem Soueidan, UFR d’Odontologie 1, Place Alexis Ricordeau, 44042 Nantes, France. Tel: +33-6-19112579. Email: [email protected]
Vol 14, No 1, 2016
Submitted for publication: 14.12.13; accepted for publication: 19.03.14
R
esearch into the associations between periodontal diseases and various chronic systemic diseases and conditions has burgeoned rapidly in the past few years.9,17,19,22 To date, associations have been found between periodontal diseases and diabetes,26 cardiovascular diseases,7 metabolic syndrome/obesity 22 and adverse pregnancy outcomes.15 Recently, data have been published on the potential associations between periodontal diseases and respiratory diseases, rheumatoid arthritis or cancer, but these require further investigation.21 Caused by pathogenic microflora in the dental biofilm, periodontal diseases (gingivitis and periodontitis) are common inflammatory disorders affecting the tissues surrounding and supporting the teeth (periodontium).27 A variety of such biofilm microorganisms adjacent to the gingival crevice can contribute to the pathogenesis of periodontitis, but some of
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them – such as Porphyromonas gingivalis, Tannerella forsythensis, Treponema denticola and Aggregatibacter actinomycetemcomitans – are more pathogenic than others. Colonisation and proliferation of these bacteria are accompanied by the release of bacterial proteases, e.g. leucotoxins, collagenases or fibrinolysins, which damage periodontal tissue.29 In addition to the predominant role of pathogenic microorganisms in the genesis of periodontitis, genetic and environmental factors and especially tobacco use6 modify the immunological-inflammatory host response and the nature and importance of periodontal tissue breakdown. By nature, the host response to infection is essentially protective. But in a host susceptible to periodontitis, dental biofilm accumulation and especially a sustained microbial challenge could trigger an immune-inflammatory hyper-response. This results in enhanced tissue destruction via the activation of cell-mediated immunological responses, cytokine and prostanoid cascades, leading to the overproduction and release of interleukin-1 (IL-1), IL-6, tumour necrosis factor α (TNF- α) and prostaglandin E2 (PGE2).23 During the normal progression of pregnancy, there is an increase in the secretion of female sex hormones, i.e. estrogen by 10 fold and progesterone by 30 fold. These significant hormonal modifications induce several systemic as well as local physiological and physical changes in the pregnant woman’s body. The main systemic changes occur in the respiratory, circulatory, hematological, renal, gastrointestinal, endocrine, genitourinary and musculoskeletal systems. The local physical changes occur in the different parts of the body, including the oral cavity.12 Pregnant women may be more susceptible than other women to infection: the increased total blood volume and vasodilatation increase the dissemination of bacteria throughout the body. Further, pregnancy may alter the cell-mediated immune function resulting in a delayed immune response to infection.4,8 The increased levels of estrogen and progesterone also lead to hypervascularisation of the periodontium and changes in collagen production, increasing the vascular permeability and making the gingival tissue more susceptible to dental biofilm. This may exacerbate pre-existing gingivitis or worsen pre-existing periodontitis.4 An adverse pregnancy outcome is defined as an event that reduces the chance of having a healthy baby. Spontaneous preterm birth and preterm preeclampsia are two of the adverse pregnancy outcomes described. Preterm deliveries are those that
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occur at under 37 weeks of gestational age, which happens in about 5% to 13% of births in many developed countries and is the leading cause of perinatal morbidity and mortality in these countries.14 Pre-eclampsia is a hypertensive, multisystem disorder of pregnancy that significantly contributes to maternal and fetal/neonatal morbidity and mortality. It is characterised by high blood pressure and significant amounts of protein in the urine of the pregnant woman. It is the most common of the serious pregnancy complications and may affect both the mother and fetus.2 Offenbacher et al25 were the first to report a link between poor maternal periodontal heath and preterm labour or low birth-weight infants and concluded that periodontal infection could be a risk factor for preterm birth or low birth weight. Since this report, numerous epidemiological and prospective studies have confirmed or refuted these findings.15 The Consensus Report of the Sixth European Workshop on Periodontology in 200817 indicated a likely association between periodontal disease and an increased risk of adverse pregnancy outcomes. More recently, a systematic review15 confirmed a significant association between maternal periodontitis and low birth-weight infants, preterm birth and pre-eclampsia. The exact pathogenic mechanisms involved in these associations remain controversial, but two main mechanisms have been postulated to explain how maternal periodontal disease could affect pregnancy outcomes.8,24,33 First, the uterine cavity of women with periodontal disease may become exposed to or colonised by periodontal bacteria or their products (e.g. lipopolysaccharides of Gram-negative bacteria), which reach the maternal-fetal unit and release an inflammatory cascade leading to premature rupture of membranes or to preterm spontaneous labour. The second mechanism suggests that cytokines generated locally within the diseased periodontal tissues, mainly IL-1, IL-6, TNF- α and prostaglandins (e.g. PGE2), may enter the systemic circulation and precipitate a similar cascade, again leading to spontaneous preterm labor and birth. Our current understanding of the role of periodontal diseases in health and particularly in adverse pregnancy outcomes has changed dramatically and will thus be gaining the attention of both medical and dental professionals in their clinical practice. Few studies have evaluated the knowledge, attitudes and daily practice of dental and medical practitioners regarding oral health care and its relationship to pregnancy, particularly to preterm delivery
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Table 1 Professional demographic data Number of professionals (n=460)
%
Midwives
70
15.21
Gynecologists/obstetricians
30
6.52
360
78.26
Professional
Dentists
Graduation year
PP (n=100)
%
DP (n=360)
%
PP +DP
%
1970 to 1979
12
12
34
9
46
10
1980 to 1989
24
24
119
33
143
31
1990 to 1999
25
25
67
19
92
20
2000 to 2012
39
39
140
39
179
39
Abbreviations: PP: prenatal care practitioner; DP: dental professionals. Percentage may not total to 100% due to rounding.
and low birth-weight infants.11,33,34 Hence, the purpose of this study was to determine the knowledge of French dentists and French prenatal care practitioners (obstetricians/gynecologists and midwives) regarding associations between oral health and pregnancy associations, and how they incorporate that knowledge into daily clinical practice.
MATERIALS AND METHODS This study utilised two questionnaires, A and B, designed for pregnancy professionals (gynecologists/ obstetricians and midwives) and dentists, respectively. Each questionnaire contained a total of 10 questions grouped into four parts to elicit information about: • the personal characteristics of the health-care practitioners and the nature of their initial and continuing professional education • their knowledge of oral alterations during pregnancy • their knowledge of the possible association between periodontal disorders and preterm/low birth weight • their conduct toward/treatment of their patients. Questionnaire A was distributed to prenatal care practitioners from the regional maternity hospital of Lille (Hôpital ‘mère-enfant’ Jeanne de Flandre) and from six other maternity hospitals in northern France (maternity hospital Saint Vincent de Paul of Lille, and maternity hospitals of Grande-Synthe, Armentieres, Béthune, Saint-Omer and Tourcoing). Questionnaire B was distributed to private dental practitioners in northern France.
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RESULTS 883 questionnaires were administered, 725 to dentists and 158 to prenatal care practitioners. The total response rate was 52%. Of the questionnaires administered, 460 health professionals, consisting of 100 prenatal care practitioners and 360 dentists, responded. Of the prenatal care practitioners, 30 were gynecologists/obstetricians and 70 were midwives. The response rate to questionnaire A (distributed to prenatal care practitioners) was 63% and to questionnaire B (distributed to dentists) was 49.6%. Any survey that was incomplete or filled out incorrectly was not counted in the final sample of health-care professionals (N = 460). The incomplete response rate was 7%. Their period of professional practice ranged from 2 to 42 years, with 59% of the health professionals having been in practice an average of 19 years (Table 1). Figures 1 to 3 show the different health professionals’ knowledge concerning oral infections, periodontal diseases and adverse pregnancy outcomes. Gingival bleeding and pregnancy-associated gingivitis were the oral manifestations most often reported by both dentists and prenatal care practitioners. Fewer dentists than prenatal care practitioners considered pregnancy to increase the risk of caries. Pyogenic granuloma was known to less than 10% of the prenatal care practitioners (Fig 1). Oral infection was clearly identified as a risk factor for adverse pregnancy outcomes (Fig 2) by 99% of prenatal care practitioners vs 90% of dentists. The most frequent adverse pregnancy outcomes mentioned as a consequence of a periodontal disease (Fig 3) were preterm birth (80% of the prenatal practitioners vs 50% of dentists) followed by chorioamnionitis (59% of
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100
PP% DP%
80 percent
60 40 20 0
isk
h
t oo
r ay ec
d
g
al
h ut
ul
o
m
iv ng
gi
t
r giv
d
te
cia
gin
c
i en
ss
a
m
lo
u an
gr
ce
s ab
g
o
ss
s
iti
ce
in
ed
e bl
o py
-a cy
an
gn
e pr
Fig 1 Oral manifestations associated with pregnancy reported by health professionals (PP: Prenatal care practitioners; DP: dental professionals).
100
PP% DP%
80
the prenatal care practitioners vs 40% of dentists) and low birth-weight babies (41% of prenatal care practitioners vs 15% of dentists). Almost 70% of prenatal care practitioners did not perform a systematic oral examination, even briefly, on their pregnant patients. Only if the pregnant patient mentioned specific dental pain or discomfort did the prenatal care practitioners perform an oral examination. More than half (51%) of prenatal care practitioners referred their pregnant patients for dental care only when they had poor oral conditions. Only 20% of them routinely advised their pregnant patients to seek dental care during pregnancy regardless of oral status (Table 2). Fifty-eight percent of the dentists responded that they rarely see pregnant patients (Table 3). Among the 48% of the health professionals whose initial professional education included oral care for pregnant women, 60% of the dentists had received such education while 95% of the prenatal care professionals had not. However, 85% of all the healthcare professionals wished to receive continuing education relating to dental care during pregnancy (Table 4).
percent
60
DISCUSSION
40 20 0
yes
no
Fig 2 Oral infections as a risk factor for adverse pregnancy outcomes reported by health professionals (PP: Prenatal care practitioners; DP: dental professionals).
100
PP% DP%
80 percent
60 40
This study sought to assess the knowledge and clinical practice behaviours of health-care professionals – prenatal care practitioners and dentists – concerning oral manifestations during pregnancy and the possible relationship between periodontal disease and preterm birth/low birth weight. Despite comprehensive data showing an association between oral infection and adverse pregnancy outcomes, which demonstrates that periodontal disease could be a risk factor for preterm/ low birth weight, many studies found health-care practitioners to have limited knowledge of this or a mismatch between daily clinical behaviours and this important health issue.1,11,13,28,32,34 The two main oral factors that prenatal care practitioners
20 0
tis
m
m
o
a rio
ch
am
l
-ec
e pr
er
e-t
ag
bi
m
pr
rh or
h ry
e
w
b ht
g
ei -w r th
em
liv
de
y ab
e
r th
ia
ps
ni
o ni
rs
he
bi
lo
Fig 3 Adverse pregnancy outcomes as a consequence of periodontal disease reported by health professionals (PP: Prenatal care practitioners; DP: Dental professionals).
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Table 3 Frequency of dentists’ care of pregnant women
ot
%
n = 360
0
0
Infrequently
58
209
Often
40
144
Always
2
7
Never
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believed to be associated with pregnancy were an increase in caries risk and gingival manifestations, such as pregnancy-associated gingivitis or gingival bleeding. During pregnancy, the frequency of tooth decay and the number of decayed teeth among pregnant women have been reported to be high.31 In the present study, 30% of the dentists vs 49% of the prenatal care practitioners effectively believed that caries risk increases during pregnancy. The dentists’ percentage may appear low and could be surprising when compared to the prenatal care
practitioners’ percentage. An explanation for this may be that dentists rightly believe that the caries incidence is not directly due to pregnancy but rather to less effective oral health care, changes in dietary habits with more sugary snacks,29 an increase in the number of certain salivary cariogenic microorganisms and salivary pH modification.18 In this study, gingival bleeding and pregnancyassociated gingivitis were the gingival problems most frequently mentioned by the health professionals. These results are similar to those of a
Table 4 Education of health professionals on oral care of pregnant woman PP+DP (n=460)
PP+DP %
PP (n=100)
PP %
DP %
DP (n=360)
During your initial professional education, did you receive any instruction on oral care of pregnant women? Yes
221
48
5
5
216
60
No
239
52
95
95
144
40
Have you participated in postgraduate or continuing education on pregnancy and dental care? Yes
75
16
11
11
64
18
No
385
84
89
89
296
82
Do you wish to attend continuing education courses about pregnancy and dental care? Yes
393
85
91
91
302
84
No
67
15
9
9
58
16
Abbreviations: PP: prenatal care practitioner; DP: dental professionals. Percentage may not total to 100% due to rounding.
Table 2 Prenatal care practitioners’ clinical attitude in relation to dental care (n = 100) % Oral examination by the prenatal care practitioners during medical consultation Always
1
Often
5
Infrequently
27
Never
68
If yes, at which moment of the pregnancy? At the compulsory declaration of the pregnancy
5
During the first encounter with the pregnant woman
30
For a specific painful dental reason or discomfort reported by the patient
60
Other
5
In your pregnancy care protocol, do you refer your pregnant patient to a dentist? Never
12
When the patient seems to have poor oral conditions
51
Upon patient request
12
Always
20
Not documented
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study conducted with Jordanian physicians1 and those of another survey by Egéa et al.13 All of these results are consistent with results of epidemiological studies reporting that approximately 40% of pregnant women have some form of periodontal disease19,20 and that gingival bleeding is the most frequent oral sign associated with pregnancy4 and reported by pregnant women. Pyogenic granuloma, also named ‘pregnancy epulis tumour’ or ‘granuloma gravidarum,’3 seemed to be unknown to prenatal care practitioners in this study. This fibrous inflammatory hyperplasia is mainly found on the marginal gingiva of the anterior areas and develops in up to 5% of pregnancies.16 Paradoxically, abscesses associated with pregnancy were frequently mentioned by the prenatal care practitioners, although it does not occur more frequently in pregnancy than in other clinical situations. An overwhelming majority of the health-care professionals in the present study were aware of the association between oral infections and adverse pregnancy outcomes. Our results are consistent with those of other authors,1,11,28 but some significant differences in the nature of the outcomes cited were found between dentists and prenatal care professionals. Where preterm birth and low-birth weight babies were the two outcomes mentioned most often by the prenatal care practitioners as well as the dentists, chorioamnionitis was rarely mentioned by the dentists and pre-eclampsia was almost never cited. Pre-eclampsia is a maternal multi-organ disorder unique to pregnancy with the clinical appearance of hypertension and proteinuria. Chorioamnionitis refers to inflammation of the amniochorionic membrane. It is the result of a polymicrobial infection and is estimated to be present in approximately 40% to 70% of women who deliver prematurely. Pre-eclampsia and chorioamnionitis are two of the leading causes of maternal and neonatal morbidity and mortality in the Western world.5,10 The possible link between chorioamnionitis and oral infections has not yet been studied, even though prenatal care practitioners reported it when asked about it.13 This is likely because chorioamnionitis is a common obstetric problem well known among prenatal care practitioners, whose focus is on urinary/vaginal infections rather than oral infection. In contrast, few dentists in our study knew of these two pregnancy complications, despite the fact that the latest publications show an association between oral infections, pre-eclampsia and adverse pregnancy outcomes.15 Moreover, prenatal care practitioners underestimated the possi-
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ble role of periodontal diseases in increasing the risk of developing pre-eclampsia. Our results were consistent with the results of other studies.13 The clinical behaviour of the prenatal care practitioners in this study did not always seem to be consistent with the large number of them who are aware of the role of oral infections and periodontal diseases in adverse pregnancy outcomes. Indeed, oral examination was never or infrequently performed by more than 90% of these prenatal care practitioners, and almost two-thirds of them only performed an oral exam for specific, painful dental reasons or discomfort reported by the patient. They referred pregnant women to a dentist only when poor oral conditions were found or upon patient request, thus overlooking other latent or less apparent oral conditions, such as gingivitis or periodontitis. These results are consistent with those found in other, similar studies.13,34 The content of the training received by the prenatal care professionals regarding oral health and oral care could explain why they did not routinely refer the pregnant patients to dental care or why they did not perform a systematic oral examination. Omitting oral examinations is not so surprising because prenatal care practitioners are not trained to perform them, but it is surprising that they seem to be reluctant to refer patients to a dentist. Indeed, only 5% of the prenatal care professionals in the present study had received any such training during their initial education and only 11% had participated in continuing education on oral health during pregnancy. These results could explain why, in our study, 58% of the dentists only infrequently treated pregnant women. A large majority (85%) of both the dental and the prenatal care professionals wish to have continuing education in dental care related to pregnancy.
CONCLUSIONS Although the results of this study cannot be extrapolated, they clearly demonstrate that discrepancies exist between current evidence from the literature and French health care professionals’ knowledge/ recognition of as well as their behaviour regarding oral manifestations in pregnancy. Their awareness of periodontal diseases as risk factors for preterm birth or pre-eclampsia is insufficient. Furthermore, these results underline the need for better initial professional education and continuing continuing education on pregnancy and oral health conditions. Finally, the present study emphasises the need to
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update the guidelines for health-care practices for pregnant women to more effectively prevent riskrelated adverse pregnancy outcomes, such as preterm birth or pre-eclampsia.
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17. Kinane D, Bouchard Ph. On behalf of group of the European Workshop on Periodontology. Periodontal disease and health: consensus report of the Sixth European Workshop on Periodontology. J Clin Periodontol 2008;35(suppl 8):333–337. 18. Laine MA. Effect of pregnancy on periodontal and dental health. Acta Odontol Scand 2002;60:257–264. 19. Le Borgne H, Soueidan A, Caroit-Cambazard Y, Boutigny H, Jean-Baptiste K, Nguyen JM, Philippe HJ. Maladies parodontales et accouchements prématurés: étude clinique pilote. Gynecol Obste Fert 2011;39:399–401. 20. Lieff S, Boggess KA, Murtha AP, Jared H, Madianos PN, Moss K, Beck J, Offenbacher S. The oral conditions and pregnancy study: periodontal status of a cohort of pregnant women. J Periodontol 2004;75:116–126. 21. Linden GJ, Herzberg MC, and on behalf of working groupe 4 of the joint EFP/AAP workshop. Periodontitis and systemic diseases: a record of discussions of working group 4 of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. J Periodontol 2013;84(4 suppl):S20–S23. 22. Linden GJ, Lyons A, Scannapieco FA. Periodontal systemic associations: review of the evidence. J Clin Periodontol 2013;40(suppl 14):S8–S19. 23. Liu YCG, Lerner UH, Teng YTA. Cytokine responses against periodontal infection: protective and destructive roles. Periodontol 2000 2010;52:165–206. 24. Michalowicz BS, Durand R. Maternal periodontal disease and spontaneous preterm birth. Periodontol 2000 2007;44:103–112. 25. Offenbacher S, Katz V, Fertik G, Collins J, Boyd D, Maynor G et al. Periodontal infection as a possible risk factor for preterm low birth weight. J Periodontol 1996;67:1103–1113. 26. Preshaw PM, Alba AL, Herrera D, Jepsen S, Konstantinidis A, Makkrilakis S, Taylor R. Periodontitis and diabetes: a two-way relationship. Diabetologia 2012;55:21–31. 27. Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet 2005;366:1809–1820. 28. Shenoy RP, Nayak DG, Sequeira PS. Periodontal disease as a risk factor in preterm low birth weight – An assessment of gynecologists’ knowledge: a pilot study. Indian J Dent Res 2009;20:13–16. 29. Silk H, Douglass AB, Douglass JM, Silk L. Oral health during pregnancy. Am Fam Physicians 2008;77:1139–1144. 30. Socransky SS, Haffajee AD. Periodontal microbial ecology. Periodontol 2000 2005;38:137–187. 31. Vergnes JN, Kminski M, Lelong N, Musset AM, Sixou M, Nabet C, for the EPIPA study. Frequency and risk indicators of tooth decay among pregnant women in France. A cross sectional analysis. PloS ONE 2012;7(5):e33296. doi:101371 32. Wilder R, Robinson C, Jared HL, Lieff S, Bogess K. Obstetricians’ knoweldge and practice behaviors concerning periodontal health and preterm delivery and low birth weight. J Dent Hyg 2007;81:81-96. 33. Winner G, Pihlstrom BL. A critical assessment of adverse pregnancy outcome and periodontal disease. J Clin Periodontol 2008;35(suppl 8):380–397. 34. Zanata RL, Fernandes KBP, Navarro PSL. Prenatal dental care: evaluation of professional knowledge of obstetricians and dentist in the cities of Londirna/Pr and Bauru/ Sp, Brazil, 2004. J Appl Oral Sci 2008;16:194–200.
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