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J Clin Periodontol 2012; 39: 213–228 doi: 10.1111/j.1600-051X.2011.01784.x

Periodontal health status and bacteraemia from daily oral activities: systematic review/ metaanalysis

Toma´ s I, Diz P, Tobı´as A, Scully C, Donos N. Periodontal health status and bacteraemia from daily oral activities: systematic review/meta-analysis. J Clin Periodontol 2012; 39: 213228. doi: 10.1111/j.1600-051X.2011.01784.x.

Abstract Aim: The aim of this study was to investigate the robustness of the observations on the influence of oral hygiene, gingival and periodontal status on the develop- ment of bacteraemia from everyday oral activities (B-EOA), analysing its preva- lence, duration, magnitude and bacterial diversity. Material and Methods: This systematic review/meta-analysis complies with PRIS- MA reporting guidelines. MEDLINE-PubMed, the Cochrane Library and Em- base were explored for detecting studies on B-EOA. Results: There were 290 potentially eligible articles, of which 12 article on B-EOA fulfilled the inclusion criteria and were processed for data extraction (seven on toothbrushing, one on dental flossing and four on chewing). Evaluating the influence of plaque and gingival indices on the prevalence of bacteraemia following toothbrushing, the pooled odds ratios were 2.61 [95% confidence inter- val (CI) = 1.454.69] and 2.77 (95% CI = 1.505.11), respectively. None of five studies on bacteraemia following dental flossing and chewing revealed a statisti- cally significant association between oral hygiene, gingival or periodontal status and the development of bacteraemia. Conclusions: Meta-analysis showed that plaque accumulation and gingival inflam- mation scores significantly increased the prevalence of bacteraemia following toothbrushing. However, systematic review showed no relationship between oral hygiene, gingival and periodontal status and the development of B-chewing, and there is no evidence that gingival and periodontal health status affects B-flossing.

gingival and periodontal health status affects B-flossing. Review Article Inmaculada Toma´ s 1 , Pedro Diz

Review Article

Inmaculada Toma´ s 1 , Pedro Diz 1 , Aurelio Tobı´as 2 , Crispian Scully 3 and Nikolaos Donos 4

1 Special Needs Unit, School of Medicine and Dentistry, Santiago de Compostela University, Santiago de Compostela; 2 Institute of Environmental Assesssment and Water Research, Spanish Council for Scientific Research, Barcelona, Spain; 3 Oral Medicine and Special Needs Unit; 4 Periodontology Unit, UCL Eastman Dental Institute, London, UK

Key words: bacteraemia; everyday oral activity; gingivitis; meta-analysis; oral hygiene; periodontitis; systemic review

Accepted for publication 23 July 2011

Bacteraemia of oral origin is defined as presence of viable oral bacteria in

Conflict of interest and source of funding statement

The authors declare that they have no conflict of interests. This work was supported by Xunta de Galicia (Grant PGIDT 08CSA010208PR), Spain.

© 2011 John Wiley & Sons A/S

the bloodstream following dental procedures or everyday oral activi- ties (Carmona et al. 2002). A feature that is unique to the oral bacterial biofilm, particularly the subgingival plaque biofilm, is its close proximity to highly vascularized tissues. Any disruption of the natural integrity of the subgingival epithelium, which is at most about 10 cell layers thick, could lead to bacteraemia (Parahitiy-

awa et al. 2009). This can lead to seeding of microorganisms in differ- ent target organs, resulting in focal infections such as infective endocar- ditis (IE) (Carmona et al. 2002). In the latest guidelines published by the British Society for Antimicro- bial Chemotherapy (Gould et al. 2006), the American Heart Associa- tion (AHA) (Wilson et al. 2007), the National Institute for Health and

213

214 Toma´ s et al.

Clinical Excellence (NICE) of the United Kingdom (National Institute for Health and Clinical Excellence 2008), and the European Society of Cardiology et al. 2009, the emphasis for the cause of IE has shifted from procedure-related bacteraemia to cumulative bacteraemia due to every- day oral activities (B-EOA). NICE (National Institute for Health and Clinical Excellence 2008) considered that it was “biologically implausible” that a dental procedure would lead to a greater risk of IE than regular toothbrushing. B-EOA, such as toothbrushing and chewing, can also play an important role in the development of cardiovascular disease by promoting the formation of atherosclerotic pla- ques in blood vessel (Drangsholt 1998, Olsen 2008). Evidence from epidemiological and interventional studies suggests that periodontal infections are independently associ- ated with atherosclerotic vascular disease and that periodontal treat- ment generally results in favourable effects on subclinical markers of this disease (Kebschull et al. 2010). Oral bacteria have been detected in ath- erosclerotic plaques, heart valves and aortic aneurysms (Pucar et al. 2007, Gaetti-Jardim et al. 2009, Nakano et al. 2009), particularly including periodontopathogens such as Aggre- gatibacter actinomycetemcomitans , Treponema denticola and Porphyro- monas gingivalis (Pucar et al. 2007, Gaetti-Jardim et al. 2009, Nakano et al. 2009). Experimental mechanis- tic in vitro and in vivo studies have established the plausibility of a link between periodontal infections and atherogenesis and have identified biological pathways through which these effects may be mediated (Kebschull et al. 2010). Everyday oral activities can pro- voke bacteraemia possibly because these activities produce small move- ments of the tooth within the socket, causing intermittent positive and neg- ative pressures that cause microor- ganisms to gain access to the bloodstream (Roberts 1999). Studies on B-EOA in both children and adults have focused principally on bacteraemia after toothbrushing (Parahitiyawa et al. 2009, Diz Dios et al. 2011). It has been estimated that the prevalence of bacteraemia from toothbrushing is 062% (Bhanji

et al. 2002, Hartzell et al. 2005), from

dental flossing is 041% (Carroll & Sebor 1980, Crasta et al. 2009), the

risk occurs with the use of supragingi-

val irrigation devices is 050% (Felix

et al. 1971, Romans & App 1971,

Berger et al. 1974) and the lowest risk

with chewing (range: 017%) (Cobe 1954, Murphy et al. 2006). The maxi- mum duration of B-EOA does not usually exceed 15 min. and the bacte-

ria most frequently isolated in posi-

tive post-toothbrushing blood

cultures are Streptococcus spp. (45%), followed by obligate anaer- obes (19%) and Staphylococcus spp. (15%) (Diz Dios et al. 2011). In gen- eral, B-EOA is of low intensity: the median level in the majority of studies published to date is 0.97 CFU/ml (range: 0.0132 CFU/ml), although this intensity is considerably higher than that of the baseline bacteraemia reported in those same studies (med- ian baseline bacteraemia in the majority of studies published to date,

0.02

CFU/ml; range: 0.01

0.05

CFU/ml) (Diz Dios et al. 2011).

At the present time, the clinical importance of B-EOA is based on the concept of cumulative exposure to bacteraemia (Gutheroth 1984, Rob- erts 1999). Gutheroth (1984) esti- mated a collective exposure of 5370 min. of bacteraemia in a 1- month period in dentate patients as a

result of everyday oral activities com- pared with only 6 min. of bactera- emia associated with a single-tooth extraction. Other authors have esti- mated that the risk of cumulative bacteraemia with toothbrushing twice

a day was 154,219 times greater than

with tooth extraction (Roberts 1999). In common inflammatory condi- tions such as gingivitis and chronic periodontitis, the periodontal vascu- lature proliferates and dilates, pro-

ducing an even greater surface area and facilitating the entry of microor- ganisms into the bloodstream (Para- hitiyawa et al. 2009). Consequently,

health may reduce the incidence of B-EOA and is more important than prophylactic antibiotics for a dental procedure to reduce the risk of IE” (Wilson et al. 2007, National Insti- tute for Health and Clinical Excel- lence 2008). However, there is limited information regarding the impact of oral hygiene, gingival or periodontal status on B-EOA and findings are inconsistent (Madsen 1974, Silver et al. 1977, Schlein et al. 1991, Lockhart et al. 2009). In an age of evidence-based medi- cine and dentistry, a systematic review/meta-analysis of the situation is required. The purpose of the pres- ent systematic review/meta-analysis was to investigate the robustness of the observations on the influence of oral hygiene, gingival or peri- odontal status on the development of B-EOA, analysing its prevalence, duration, magnitude and bacterial diversity. One hypothesis was formu- lated: oral hygiene, gingival or peri- odontal status represent risk factors for the development of B-EOA.

Material and Methods

This systematic review/meta-analysis complies with PRISMA reporting guidelines (Liberati et al. 2009) (Appendix 1).

Literature search

Three internet databases were selected to search for suitable article:

the National Library of Medicine, Washington DC, USA (MEDLINE, PubMed), the Cochrane Library and Embase. No date or publication sta- tus restrictions were imposed. Only English-language articles were con- sidered (Moher et al. 2000). All databases were researched up to 31 July, 2010. Studies that satisfied the follow- ing inclusion criteria were selected:

it

has been assumed that the patients

(a)

Studies on B-EOA.

with periodontal disease may have

(b)

Studies analysing the influence

a

much higher risk of developing

of oral hygiene, gingival or peri-

B-EOA and, hence, systemic diseases

 

odontal status on the develop-

of

oral origin (Gendron et al. 2000,

ment of B-EOA.

Li

et al. 2000, Carmona et al. 2002;

(c)

Study group(s) formed of sub-

Study group(s) having a mini-

Sakamoto et al. 2007, Olsen 2008, Bolger 2009). Even some Expert Committee guidelines concurred with

(d)

jects aged 15 years or older.

mum of 11 subjects.

the premise: “Maintenance of opti- mal oral hygiene and periodontal

(e)

Determination of baseline bacter- aemia.

© 2011 John Wiley & Sons A/S

When the title and the abstract of a article failed to provide suffi- cient information to assess its eligi- bility, the full report was obtained. Article with no abstract but whose title suggested that they were related to the objectives of this review were also selected so that the full text could be screened. Data that were published twice or more were selected only once. Unpublished data described in the full text of published article were included in the analysis. Reviews containing comments on B-EOA were excluded after screening for additional studies or unpublished data. The search was supplemented by reference checking.

Search strategy

The electronic search was performed in accordance with the most recent recommendations published by the Centre for Reviews and Dissemina- tion, University of York (Centre for Reviews and Dissemination, Univer- sity of York 2008). The primary out- come variable was the development of B-EOA. The databases were searched using the following strategy and keywords:

Everyday oral activities : Toothbrush- ing [MeSH Terms] OR toothbrush- ing [All Fields]; mastication [MeSH Terms] OR mastication [All Fields] OR chewing [All Fields]; mouth [MeSH Terms] OR mouth [All Fields] OR oral [All Fields]; irriga- tion [MeSH Terms] OR irrigation [All Fields]; equipment and supplies [MeSH Terms] OR equipment [All Fields] AND supplies [All Fields] OR equipment and supplies [All Fields] OR device [All Fields]; dental devices, home care [MeSH Terms] OR dental [All Fields] AND devices [All Fields] AND home [All Fields] AND care [All Fields] OR home care dental devices [All Fields] OR dental [All Fields] AND floss [All Fields] OR dental floss [All Fields]; toothpick [All Fields]; daily [All Fields] AND activities [All Fields]; oral hygiene [MeSH Terms] OR oral [All Fields] AND hygiene [All Fields] OR oral hygiene [All Fields] AND methods [Subheading] OR methods [All Fields] OR procedures [All Fields] OR methods [MeSH Terms] OR procedures [All Fields]

© 2011 John Wiley & Sons A/S

Periodontal status and oral bacteraemia

215

AND nursing [Subheading] OR nursing [All Fields] OR home [All Fields] AND care [All Fields] OR home care [All Fields] OR home care services [MeSH Terms] OR home [All Fields] AND care [All Fields] AND services [All Fields]) OR home care services [All Fields] OR home [All Fields] AND care [All Fields] AND methods [Subheading] OR methods [All Fields] OR proce- dures [All Fields] OR methods [MeSH Terms] OR procedures [All Fields].

AND

Outcome : bacteremia [All Fields] OR bacteremia [MeSH Terms] OR bac- teraemia [All Fields] OR bacteraemia [MeSH Terms] AND spontaneous [All Fields] AND mouth [MeSH Terms] OR mouth [All Fields] OR oral [All Fields] AND random allo- cation [MeSH Terms] OR random [All Fields] AND allocation [All Fields] OR random allocation [All Fields] OR random [All Fields].

Screening and selection of article

Two reviewers (IT and PD) indepen- dently inspected each reference iden- tified by the search, scanned the full texts of relevant studies, applied the inclusion criteria and extracted the data. Any disagreement between the reviewers was resolved after additional discussion. The following factors were evalu- ated to investigate the heterogeneity of the studies:

(a) Study design. (b) Methodological study quality assessment.

Study design

Two different types of study design were found:

(a) Studies based on an analysis of the influence of oral hygiene, gingival or periodontal status on the development of B-EOA in control subjects (with good gin- gival and periodontal health) and/or patients with a diagnosis of gingivitis and/or periodontitis (comparing at least two groups). (b) Studies based on an analysis of the influence of oral hygiene, gingival or periodontal status on the development of B-EOA in

patients with different oral hygiene, gingival and periodontal index values, with an initially known or unknown periodontal diagnosis.

Methodological quality assessment of the studies

The quality assessment of studies was performed in accordance with the most recent recommendations pub- lished by the Centre for Reviews and Dissemination, University of York (Centre for Reviews and Dissemina- tion, University of York 2008), evalu- ating the following parameters:

(a)

Description of possible selection bias (inclusion and exclusion cri- teria).

(b)

Description of the specific char- acteristics associated with per- forming each activity.

(c)

Definition of control subjects and patients with gingivitis or periodontitis.

(d)

Description of the clinical parameters recorded to evaluate oral hygiene, gingival and peri- odontal status.

(e)

Microbiological methods used to determine exposure to B-EOA.

(f)

Statistical methods used to ana- lyse exposure to B-EOA.

(g)

Reference to the calculation of sample size.

Quantitative outcome analysis

The principal results obtained on the influence of oral hygiene and gingi- val or periodontal status on the development of B-EOA were analy- sed in terms of prevalence and/or duration and/or intensity and/or bacterial diversity of the bactera- emia. In the different studies, the post-activity blood samples (exclud- ing the first blood sample drawn after the activity) were considered for the analysis of the duration of the bacteraemia.

Data extraction and statistical analysis

Cohen’s Kappa coefficient was used to measure the agreement between the two readers at each stage. First, the eligibility criteria were applied and the factors evaluating heterogeneity

216 Toma´ s et al.

of the primary outcome studies were then analysed. Initially, extracted data were expressed in the same way that they were presented in the different stud- ies. However, in studies that had the same design but varied in their pre- sentation of results, the results were processed for data extraction.

Meta-analysis

Meta-analysis could be only per- formed on article on bacteraemia fol- lowing toothbrushing: four article on the influence of the plaque index (PI) (Madsen 1974, Silver et al. 1977, Schlein et al. 1991, Lockhart et al. 2009) and four article on the influ- ence of the gingival index (GI) (Mad- sen 1974, Silver et al. 1977, Schlein et al. 1991, Lockhart et al. 2009). In those studies, the influence of plaque and gingival indices was analysed through a comparison of different cut-off values (Madsen et al. com- pared 00.50, 0.511.00, 1.011.50, 1.512.00 and 2.012.50; Silver et al. 00.75, 0.761.50, 1.512.25 and 2.263.00; Schlein et al. 01.50 and 1.513.00; and Lockhart et al. 01.99 and 2.00) (Madsen 1974, Silver et al. 1977, Schlein et al. 1991, Lockhart et al. 2009). To compare those studies in the present meta- analysis, the influence of the plaque and gingival indices was analysed comparing values 01.50 versus 1.51, except for the paper by Lockhart et al. where the values used were 01.99 versus 2.00 (Lockhart et al. 2009). The odds ratios (OR) and 95% confidence intervals (CI) were calculated for the data extracted from each study to estimate the asso- ciation between these clinical param- eters and the prevalence of bacteraemia following toothbrushing, excepting the paper by Lockhart et al. (2009), in which the OR and 95% CI were already reported. In consequence, we used the OR as the summary statistic. We used the DerSimonian and Laird Q statistic to test for signifi- cance and homogeneity. To quantify the heterogeneity, the proportion of total variance caused by between- study variance (the I 2 statistic) was calculated (Takkouche et al. 1999). The study-specific adjusted log ORs were weighted by the inverse of their variance to compute a pooled OR

and its 95% CI. On the basis of the results on homogeneity, we calculated and used fixed-effects (F-effects) pooled estimates. The fixed-effects model assumes that there is no between-study variance (i.e. that the results of the studies used in the meta- analysis are homogeneous and their variation is purely a result of sam- pling). Due to the small number of studies included in the meta-analysis, the evaluation of publication bias was not considered relevant. All analyses were performed using the Stata 10.0 software (Stata Corporation, College Station, TX, USA). The forest plots for each meta- analysis show the following data:

(a)

The raw data (OR and 95% CI) for each arm of each study included.

(b)

(c)

Point estimates and 95% CI for the selected effect measure, as blocks and lines, respectively.

Heterogeneity statistics ( I 2 ).

(d)

The total number of participants per group.

(e)

The overall average effect in the F-effect model; and

(f)

Percent weight given to each study.

Results

The combined MEDLINE PubMed, EMBASE and Cochrane CENTRAL searches resulted in 290 potentially eligible articles (Fig. 1).These articles were screened by title and abstract for eligibility. The screening resulted in 34 articles that qualified for full-text reading (inter-reader agree- ment, k = 0.90 ± 0.05). Screening of reviews (n = 35) for additional studies and unpublished data gave additional information (Appendix 2). After full-text reading, 22 article were considered to be unsuitable and were therefore excluded (inter-reader agreement, k = 1), leaving 12 articles for analysis. The studies that were excluded are listed in Appendix 3, together with the reason for exclu- sion. Thus, 12 articles on B-EOA fulfilled the inclusion criteria and were processed for data extraction:

seven articles on bacteraemia from toothbrushing (B-toothbrushing) (Sconyers et al. 1973, Madsen 1974, Silver et al. 1977, Schlein et al. 1991, Hartzell et al. 2005, Kinane et al. 2005, Lockhart et al. 2009), one on bacteraemia from dental flossing (B-dental flossing) (Crasta et al.

Article retrieved from MEDLINE PubMed research (n = 242) Article retrieved from Cochrane Library research
Article retrieved from
MEDLINE PubMed
research (n = 242)
Article retrieved from
Cochrane Library
research (n = 28)
Article retrieved from
EMBASE research (n = 20)
Article retrieved from combined research (n = 290)
Excluded during title/abstract
screening (n = 241)
Article retrieved for further evaluation after title/abstract screening (n = 69)*
Article excluded during full-text
reading (n = 22) (Appendix 3)
Reviews excluded after
screening for additional studies
and unpublished data (n = 35)
(Appendix 2)
Article appropriate for full reading and data extraction (n = 12) (Tables 1–4)
Article included in the meta-analysis (n = 4) (Figure 2)

* Additional reviews (n = 20) were added after reference checking of previously selected reviews.

Fig. 1. Flow-chart outlining the search strategy and results at the different stages

© 2011 John Wiley & Sons A/S

2009) and the remaining four on bacteraemia from chewing (B-chew- ing) (Robinson et al. 1950, Forner et al. 2006, Murphy et al. 2006, Fine et al. 2010).

Study designs

In four (34%) of the 12 selected stud- ies, study groups of subjects with a specific gingival or periodontal diag- nosis were compared (one paper on

B-toothbrushing: patients with gingi- vitis versus patients with periodonti- tis; one paper on B-dental flossing:

patients with gingivitis versus patients with periodontitis; two article on B-chewing: one paper including con- trol subjects versus patients with gingivitis versus patients with peri- odontitis and one paper including patients with gingivitis versus patients with periodontitis) (Madsen 1974,

2006, Murphy et al.

2006, Crasta et al. 2009). In the remaining eight article (66%), the study groups comprised subjects with different oral hygiene, gingival and periodontal index values, with known or unknown periodontal diagnosis (six article on B-toothbrushing and two article on B-chewing) (Robinson et al. 1950, Sconyers et al. 1973, Sil- ver et al. 1977, Schlein et al. 1991, Hartzell et al. 2005, Kinane et al. 2005, Lockhart et al. 2009, Fine et al.

Forner et al.

2010).

Quality assessment

The different aspects of the quality assessment of the selected studies are described in Tables 14.

Description of possible selection bias (inclusion and exclusion criteria) (Table 1)

These criteria were expressed as exclusion criteria, which were grouped into four categories:

(a) Systemic infections and other systemic diseases or conditions (principally haematological dis- orders, cardiovascular diseases, congenital or acquired heart defects, diabetes and pregnancy) were considered exclusion criteria in 10 article (Sconyers et al. 1973, Madsen 1974, Silver et al. 1977, Schlein et al. 1991, Kinane et al. 2005, Forner et al. 2006, Murphy et al. 2006, Crasta et al.

© 2011 John Wiley & Sons A/S

Periodontal status and oral bacteraemia

217

2009, Lockhart et al. 2009, Fine et al. 2010). (b) Previous pharmacological treat- ment (mainly antibiotic and/or immunosuppressive medication, although the period of use con- sidered was heterogeneous, rang- ing from 2 weeks to 6 months) was applied as an exclusion cri- terion in 10 article (Madsen 1974, Silver et al. 1977, Schlein et al. 1991, Hartzell et al. 2005, Kinane et al. 2005, Forner et al. 2006, Murphy et al. 2006, Crasta et al. 2009, Lockhart et al. 2009, Fine et al. 2010). (c) Certain oral or dental factors (mainly the presence of at least 10 teeth and/or teeth with caries or pulpal/periapical infections) were considered as exclusion fac- tors in nine article (Sconyers et al. 1973, Madsen 1974, Hartz- ell et al. 2005, Kinane et al. 2005, Forner et al. 2006, Murphy et al. 2006, Crasta et al. 2009, Lock- hart et al. 2009, Fine et al. 2010). (d) Other factors, such as previous problems with venepuncture, were considered in three article (Kinane et al. 2005, Murphy et al. 2006, Fine et al. 2010).

Description of the specific characteris- tics associated with the performance of each activity

With respect to toothbrushing, the time of brushing varied from 1 to 4 min. (Sconyers et al. 1973, Madsen

1974, Silver et al. 1977, Schlein et al. 1991, Hartzell et al. 2005, Kinane et al. 2005, Lockhart et al. 2009). Manual brushing was used in five studies (Madsen 1974, Schlein et al. 1991, Hartzell et al. 2005, Kinane et al. 2005, Lockhart et al. 2009), while powered brushing was used in the other two (Sconyers et al. 1973, Silver et al. 1977). The activity was performed by the study subjects in six studies (Sconyers et al. 1973, Madsen 1974, Schlein et al. 1991,

2005, Kinane et al.

Hartzell et al.

2005, Lockhart et al. 2009) and in one was performed by the investiga- tor (Silver et al. 1977). In the only article selected that considered dental

flossing (Crasta et al. 2009), the flossing was performed by the inves- tigator on all teeth in accordance with the 2008 recommendations of the American Dental Association

(2008). With respect to chewing, the duration of the activity varied between 2 and 10 min. and the prod- ucts chewed were of different consis- tency in each study (apple, paraffin and chewing gum) (Robinson et al. 1950, Forner et al. 2006, Murphy et al. 2006, Fine et al. 2010).

Definition of control, gingivitis and periodontitis

Varying diagnostic criteria were used to define gingival and periodontal health and to establish the diagnoses of gingivitis and periodontitis in the studies in which the patient groups comprised individuals with a speci- fied initial diagnosis of gingival or periodontal disease (Madsen 1974, Kinane et al. 2005, Forner et al. 2006, Murphy et al. 2006, Crasta et al. 2009, Fine et al. 2010). There was only one paper in which no details were given of the clinical and radiographic criteria for the diagno- sis of periodontitis (Sconyers et al.

1973).

Description of the clinical parameters recorded to evaluate the oral hygiene, gingival and periodontal status

Parameters related to oral hygiene, gingival or periodontal status were recorded in all studies included in the meta-analysis. The parameters most frequently evaluated were degree of gingival inflammation (10 article) (Robinson et al. 1950, Mad- sen 1974, Silver et al. 1977, Schlein et al. 1991, Hartzell et al. 2005,

Forner et al. 2006, Murphy et al. 2006, Crasta et al. 2009, Lockhart et al. 2009, Fine et al. 2010), levels of plaque (nine article) (Sconyers et al. 1973, Madsen 1974, Silver et al. 1977, Schlein et al. 1991, Forner et al. 2006, Murphy et al. 2006, Crasta et al. 2009, Lockhart et al. 2009, Fine et al. 2010), pocket depth (six article) (Sconyers et al. 1973, Kinane et al. 2005, Forner

et al.

Crasta et al. 2009, Lockhart et al. 2009) and degree of tooth mobility (six article) (Robinson et al. 1950, Sconyers et al. 1973, Kinane et al. 2005, Murphy et al. 2006, Crasta et al. 2009, Lockhart et al. 2009). Some of the selected article included an evaluation of other clinical parameters, such as the degree of gingival recession and loss of clini- cal attachment, presence of bleeding

2006, Murphy et al. 2006,

No palpable vein in the antecubital fossa (Murphy et al. 2006) Eating or toothbrushing within 1 h before the study (Lockhart et al.

Adverse events resulting from the use of oral

(Fine

Previous problems with venepuncture (Kinane et al. 2005, Fine et al.

Other factors

products

)

§

al. 2010

et hygiene

2009)

2010)

General No dental factors that might have influenced the incidence of bacteraemia (Sconyers et al. 1973) Specified Less than 20 teeth (Kinane et al. 2005, Fine et al. 2010) Less than 10 teeth (Crasta et al. 2009, Lockhart et al. 2009) Less than 9 teeth per arch (Sconyers et al.

crowned surfaces, parcial dentures or teeth

scaling)

Incompatible dentition (orthodontic bands,

(Madsen 1974, Forner et al. 2006, Crasta

History of periodontal treatment in the preceding 12 months (Crasta et al. 2009 ,

Less than four pairs of opposing posterior

2010 § ) gum on a regular

Murphy et al. 2006) History of dental work within 30 days (Hartzell et al. 2005) Allergy to dental products (Kinane et al.

Desquamative oral lesions (Kinane et al.

the eect of an essential oil antiseptic mouthwash on the reduction of bacteraemia after chewing was analysed.

)

et al. 2009) or retained root fragments

Teeth with pulpitis, apical periodontitis

2005) or oral ulceration (Crasta et al.

et al. 2005

disease (Fine et al. 2010 § )

al. 2010 study §

Facial cellulitis (Lockhart et al. 2009)

, Kinane ultrasonic

Teeth with caries (Fine et al. 2010)

)

Oral or dental factors

Use of antimicrobial toothpaste,

et plaque

teeth (Murphy et al. 2006)

2010 extensive §

dental

(Fine et or al. chewing

in a (Fine

Table 1. Inclusion and exclusion criteria applied in the selected studies expressed as exclusion criteria, in reversed chronological order

(Madsen 1974)

within 30 days

et al. for

Participation

mouthwash

Periodontal

unsuitable

)

2009)

2005)

(Fine

basis

1973

General medication Taking any medication at the time of the study (Madsen 1974, Kinane et al.

Immunosuppressants History of administration (Murphy et al. 2006, Fine et al. 2010) In the previous month (Hartzell et al.

In the previous month (Silver et al. 1977, Schlein et al. 1991, Hartzell et al.

Any pharmacological treatment other than oral contraceptives (Forner et al.

Antibiotic prophylaxis needed (Crasta et al. 2009, Lockhart et al. 2009, Fine et al. 2010) Penicillin allergy (Lockhart et al. 2009*) Anticoagulants History of administration (Fine et al.

In the previous 2 weeks (Lockhart et al.

In the previous 3 months (Murphy et al. 2006, Crasta et al. 2009) In the previous 6 months (Forner et al.

Previous pharmacological treatment

Drug abuse (Kinane et al. 2005) Taking medication for treatment of chronic conditions unstable in the previous 3 months (Fine et al. 2010)

Antibiotics History of administration (Fine et al.

extraction with antibiotic prophylaxis.

In the paper published by Robinson et al. (1950), there were no inclusion or exclusion criteria.

2006)

2005)

2005)

2006)

2010)

2010)

2009)

2005)

General No good general health (Madsen 1974, Silver et al. 1977, Schlein et al. 1991, Fine et al. 2010) No medical factors that might have influenced the incidence of bacteraemia (Sconyers et al. 1973) Significant medical problems (Crasta et al. 2009) Systemic diseases and chronic infections other than periodontitis (Forner et al. 2006) Poorly controlled systemic disease (Lockhart et al. 2009) Specified History of rheumatic fever (Schlein et al. 1991, Fine et al.

Rheumatic heart disease (Schlein et al. 1991) At risk of endocarditis (Kinane et al. 2005, Crasta et al. 2009) Previous endocarditis (Forner et al. 2006) Heart defects (Schlein et al. 1991, Murphy et al. 2006, Crasta et al. 2009, Fine et al. 2010) Heart murmur (Fine et al. 2010) Prosthetic heart valves (Schlein et al. 1991, Forner et al. 2006) Sickle cell disease (Schlein et al. 1991) Arteriosclerotic heart disease (Schlein et al. 1991) Immunocompromised due to disease or medication (Murphy et al. 2006, Crasta et al. 2009, Lockhart et al. 2009, Fine et al.

Haematological disorders (Fine et al. 2010, Crasta et al. 2009, Murphy et al. 2006, Kinane et al. 2005, Schlein et al. 1991) Diabetes (Kinane et al. 2005, Murphy et al. 2006, Crasta et al.

Upper respiratory tract infections (Murphy et al. 2006, Crasta et al. 2009) Active viral infection (Lockhart et al. 2009) History of infectious disease (Kinane et al. 2005) Malignancy (Kinane et al. 2005) Trasplants (Forner et al. 2006) Renal disease (Fine et al. 2010) Orthopaedic implants (Fine et al. 2010) Fever over 100.5°F (Lockhart et al. 2009) Pregnant (Forner et al. 2006, Murphy et al. 2006, Crasta et al. 2009) and/or breast-feeding women (Forner et al. 2006)

maxillary arch.

in the single-tooth

group; scaling.

Systemic infections and/or diseases or conditions

underwent

ultrasonic

group.

ve teeth

a gingivitis

a periodontitis

patients

underwent

who of had

included

a group

patients

included

one patient

only

In this study,

study,

In this study study

* Except

2009)

2010)

2010)

This

¶ § This

218 Toma´ s et al.

© 2011 John Wiley & Sons A/S

Yes, with oral hygiene status and type of bleeding (on prevalence and duration)

Conclusions

prevalence)

prevalence)

prevalence)

No (on

No (on

No (on

PI 1.51

On prevalence (at 3 min after toothbrushing) Basal = 0%; Total G = 25%

Basal = 0%; Total G = 0% On duration (at 20 min after toothbrushing) Basal = 0%; Total G = 0%

(23%); (subjects

On prevalence (at 30 s after toothbrushing)

(28%); GI 01.50 (29%); GI 1.51 (0%)

On prevalence (during toothbrushing) and on duration (immediately, 20, 40 and 60 min after toothbrushing) Basal = 1%**; Total G (cumulative bacteraemia) = 22% Range values of clinical parameters and incidence of B-toothbrushing (OR, 95%

CAI 2 (4.43, 1.6012.25); generalized

(subjects with pos-BC) = PPD < 4 mm

No significant association with GI 2,

BOP<50% (50%); BOP >50% (50%)

Basal = 6% (culture) and 9% (PCR);

PG = 3% (culture) and 13% (PCR)

Table 2. Characteristics, results and conclusions of the selected studies on the development of bacteraemia from toothbrushing, in reverse chronological order

bleeding after toothbrushing, PPD

Range values of clinical parameters

parameters

(7%) ; PPD 4 mm (19%) ;

On prevalence (immediately after

= PI 2 (3.78, 1.4110.16);

= PI 01.50

Results

bleeding (7.96, 1.4942.56)

range of clinical

and tooth mobility

toothbrushing)

with pos-BC)

Values

CI)

Blood sample of 20 ml collected at 3 min Aerobic (TS broth) and anaerobic (Columbia broth) culture bottles Incubation at 37°C for 7 days Subculture: TS agar (aero- and anaero- incubation at 37° C for 48 h) Phenotypic identification Sample size not calculated

Blood sample of 28 ml collected immediately Aerobic and anaerobic BACTEC bottles BACTEC automated system (for 14 days) Subculture: CB agar (5% CO 2 incubation at 37 °C for 14 days), FA agar (anaero- incubation at 37 C for 14 days) Phenotypic identification Bacterial detection by PCR (16S rRNA) Sample size not calculated

Blood sample of 20 ml collected during, immediately, at 20 min, 40 min and 60 min Aerobic and anaerobic BACTEC bottles

AB agar,

Blood sample of 20 ml collected at 30 s and 20 min Aerobic and anaerobic culture bottles Automated system (for 5 days) Subculture and bacterial identification not specified Sample size calculated

incubation) Genotypic identification (16S rRNA) Bacterial quantification by real-time PCR

Blood agar § (anaero-

Choco agar,

Microbiological processing Statistical analysis

(aero-incubation);

Blood agar, system

Sample size calculated

BACTEC : automated

agar and

MacC II agar

Subculture

C-CNA

Type of subjects (n) Diagnostic criteria Register of parameters related to OHS, GS and/or PS* Examiner

Untreated moderate-severe chronic PG (30) At least 1 site with PPD > 6 mm in all quadrants PPD at 6 s/t BOP inter-proximally Recession at 6 s/t CAL at 6 s/t tooth mobility No reference about examiner Subjects without previous OHS, GS and/or PS diagnosis (96) Non-available GI using PSR (Nasi 1994) No reference about examiner

Subject without previous OHS, GS and/or PS diagnosis (98) Non-available PI at 4 s/t (Silness & Loe 1964)¨ CAI at 4 s/t (Ramfjord 1959) GI at 4 s/t (Loe & Silness 1963)¨ PPD at 6 s/t tooth mobility (Armitage 1990) GB after toothbrushing (yes, no) and type (generalized, localized) No reference about examiner

Subjects without previous OHS, GS and/or PS diagnosis (20) Non-available PI (Loe 1967)¨ GI (Loe 1967)¨ No reference about examiner

Characteristics of

toohbrushing

dentifrice plus

rinse, brushed

New manual

New manual

brushed by

brushed by

brushed by

toothbrush

toothbrush

toothbrush

by subject

dentifrice,

dentifrice,

Soft-bristle

Supervised

manual,

without

without

manual

(2 min)

(2 min)

(1 min)

(2 min)

subject

subject

subject

with

References

Lockhart

Hartzell

(2009)

(1991)

(2005)

(2005)

Kinane

Schlein

et al.

et al.

et al.

et al.

© 2011 John Wiley & Sons A/S

Periodontal status and oral bacteraemia

219

gingival or periodontal status and bacteraemia development; No means that

there was no a statistically significant association between oral hygiene, gingival or periodontal status and bacteraemia development. OHS = oral hygiene status; GS = gingival status; PS = periodontal status; PG = periodontitis group; PPD = probing pocket depth; GG = gingivitis group; PI = Plaque Index; s/t = sites per

tooth; CAI = Calculus Index; GI = Gingival Index; GB = gingival bleeding; BOP = bleeding on probing; CAL = clinical attachment loss; PSR = periodontal screening and recording; Choco = chocolate; MacC = MacConkey; aero-incubation = plates that were incubated aerobically; AB = anaerobic blood; C-CNA = Columbia CNA; anaero-incubation = plates that were incubated anaerobically; 5% CO 2 -incubation = plates that were incubated at 5% CO 2 ; CB = columbia blood; FA = fastidious anaerobe; TS = trypticase soy; PRAS = prereduced anaerobi- cally sterile; BHI = brain heart infusion; SPS = sodium polyanethol sulfonate; NS = nutrient serum; SN = semisolid nutrient; Total G = total group; B-toothbrushing = bacteraemia from toothbrushing; OR = odds ratio; CI = confidence interval; pos-BC = positive blood cultures; neg-BC = negative blood cultures.

prevalence and

Conclusions

gingivitis (on

prevalence)

oral hygiene

status and

prevalence)

aetiology)

Yes, with

No (on

No (on

On prevalence (at 1 min after toothbrushing) Basal = 0%; PG = 17% Clinical parameters (mean values of subjects with pos-BC versus subjects with neg-BC) = PI (1.91 versus 1.85); PPD (3.71 versus 3.63); tooth mobility (1.25 versus 1.17); Number of teeth (24.80 versus 25.24)

1.51

On prevalence (at 3060 s after toothbrushing) Basal = 2%; Total G = 43%

PI 1.51

On prevalence (at 1 min after toothbrushing) Basal = 0%; GG = 19%; PG = 54%

(36%); GI 01.50 (50%); GI 1.51 (50%)

(35%); (subjects

(33%); (subjects

(60%); GI 01.50 (25%); GI 1.51 (62%) On bacterial diversity (pos-bc with 3

PI

parameters

parameters

bacteria) GI 01.50 (2%); GI 1.51 (28%)

= PI 01.50

= PI 01.50

Results

and malt agar) was attached to the trypticase soy culture bottle.

range of clinical

range of clinical

with pos-BC)

with pos-BC)

Values

Values

Blood sample collected at 3060 s Aerobic (TS broth) and anaerobic (PRAS “E” broth, BHI broth) culture bottles Incubation at 37° C for 5 days (aerobes) and 21 days (anaerobes) Subculture: Blood agar (aero- and anaero- incubation) Phenotypic identification not specified Sample size not calculated Blood sample of 20 ml collected at 1 min Transport tubes containing serum broth and 1% SPS Culture: NS broth, SN agar, semisolid thioglycollate and Blood agar (aero- and anaero-incubation at 35° C for 7 days) Subculture on solid media Phenotypic identification of streptococci Sample size not calculated Blood sample of 10 ml collected at 1 min Aerobic and anaerobic incubation at 37°C (PRAS “E” agar, “E” medium, TS broth) Subculture: Aerobic pour plate (TS agar) Phenotypic identification Sample size not calculated

al. (2008).

Microbiological processing Statistical analysis

oral et hygiene,

was established.

Lockhart

between

paper by

association

(2008).

clinical diagnosis

et al. agar

sulcus.

in a previous

paper.

MacConkey

in the signicant

the gingival

original

by Lockhart

kanamycin/vancomycin.

Loe 1964)¨ 1963)¨

described

Type of subjects (n) Diagnostic criteria Register of parameters related to OHS, GS and/or PS* Examiner

GG (16); PG (13) Presence of gingivitis with PPD 3 mm; Presence of periodontitis with PPD >3 mm and at least 1 interdental ulceration PI (Silness & Loe 1964)¨ GI (Loe & Silness 1963)¨ No reference about examiner PG (30) Clinical and radiographic diagnostic criteria non-described PI (Silness & Loe 1964)¨ PPD Bone loss Tooth mobility Number of teeth present No reference about examiner

after the

Subjects without previous OHS, GS and/or PS diagnosis (96) Non-available

statistically

paper agar,

PS were recorded within

No reference about examiner

(Loe & & Silness

(chocolate

was described

a was

of instrumentation

PI (Silness

previous

that on there conditions

those

agar in and media a

Modified GI

Modified

basal

GS and/or

alcohol

detailed

based

to OHS, omission

was three

in

Yes means

bacteraemia

were of re-calculated

phenylethyl

Characteristics of

s) and use of

containing

toohbrushing

related involved

description

investigador

toothbrush,

Roll method manual toothbrush (2 min and

brushed by

(2 min and

toothbrush

toothpicks

dentifrice

medium

without

Powered

Powered

results section:

(2 min)

(4 min)

with

media slide

s)

Table 2. (continued)

The modication

prevalence

30

30

¶ § A Supplemented Culture

Septi-Chek

Conclusions

*Parameters

References

Sconyers

Madsen

These ‡‡ †† **This

(1977)

(1973)

(1974)

et al.

et al.

Silver

220 Toma´ s et al.

© 2011 John Wiley & Sons A/S

and aetiology)

OHS = oral hygiene status; GS = gingival status; PS = periodontal status; CG = control group; PG = periodontitis group; BOP = bleeding on probing; PPD = probing pocket depth; CAL = clinical attachment loss; PI = Plaque Index; MGI = Marginal Gingival Index; GI = Gingival Index; s/t = sites per tooth; CA = calibration; RE = reproducibility; MacC = MacCon- key; aero-incubation = plates that were incubated aerobically; HB = horse blood; Choco = chocolate; 5% CO 2 -incubation = plates that were incubated at 5% CO 2 ; BHI = brain heart infu-

Conclusions §

prevalence,

duration

No (on

association between oral hygiene, gingival or periodontal status and bacteraemia development.

Basal = 2%; CG = 41%; PG = 40% On duration (at 10 min after dental flossing):

Basal = 2%; CG = 14%; PG = 27% No significant association with PI, GI, Bleeding on flossing, PPD, BOP, CAL On bacterial diversity (Streptococcus

CG = 33% and 13%; PG = 43%

periodontopathogenic

Table 3. Characteristics, results and conclusions of the selected studies on the development of bacteraemia from dental flossing, in reverse chronological order

Results

On prevalence (at 30 s after dental flossing):

spp. and pos-BC):

and 25%

bacteria

sion; anaero-incubation = plates that were incubated anaerobically; BOP = bleeding on probing; pos-BC = positive blood cultures.

Blood sample of 20 ml collected at 30 s and 10 min BACTEC Aerobic and anaerobic culture bottles BACTEC automated system (for 14 days) Staff at laboratory were blinded Subculture: MacC agar (aero- incubation at 35°C), HB agar and Choco agar (5% CO 2 -incubation at 35° C), BHI agar (anaero- incubation at 35°C) Phenotypic identification Sample size calculated

Microbiological processing Statistical analysis

tooth. recorded after the clinical diagnosis was established.

CG (30); Untreated chronic PG (30) 20% BOP and 10% sites with PPD 4 mm; at least two inter-proximal sites with CAL 6 mm with at least 1 of these sites with PPD 5 mm PI at 4 s/t (Silness & Loe 1964)¨ MGI at all gingival papillae (Lobene et al. 1986) Papillary bleeding on flossing (Carter & Barnes 1974) PPD at 6 s/t (mm) BOP at 6 s/t CAL Recession at 6 s/t Tooth mobility (Miller 1938) One examiner (CA and RE)

Type of subjects (n) Diagnostic criteria Register of parameters related to OHS, GS and/or PS* Examiner

original paper.

in the signicant

no statistically

was described

PS were

those

there

the same

Recommended flossing action (American Dental Association 2008) Calibrated force of 50 g Action repeated three times on each tooth surface (all teeth), performed by investigator

that on

GS on and/or

Characteristics of

No means based

dental flossing

were re-calculated

and not

to OHS,

related teeth

These results section:

On non-adjacent

§ Conclusions

*Parameters

Crasta et al. (2009)

References

© 2011 John Wiley & Sons A/S

Periodontal status and oral bacteraemia

221

on probing and after performing a specific activity, and the levels of calculus (Kinane et al. 2005, Forner et al. 2006, Murphy et al. 2006, Crasta et al. 2009, Lockhart et al.

2009).

In nine of the 12 studies selected, the authors did not comment on the examiner characteristics (Robinson

et al. 1973,

Madsen 1974, Silver et al. 1977, Schlein et al. 1991, Hartzell et al. 2005, Kinane et al. 2005, Lockhart et al. 2009, Fine et al. 2010). In one study, the clinical parameters were recorded by a single general dentist (Forner et al. 2006) and in the remaining two studies the examiners were calibrated to establish repro- ducibility (Murphy et al. 2006, Crasta et al. 2009).

Microbiological methods used to measure exposure to B-EOA

When studying the influence of oral hygiene, gingival or periodontal sta- tus on the prevalence of B-EOA, blood samples were drawn at differ- ent times, ranging from during the activity (Lockhart et al. 2009) to 3 min. after the activity (Schlein et al. 1991); for the analysis of the duration of bacteraemia, samples were drawn between 10 (Crasta et al. 2009) and 60 min. (Lockhart et al. 2009) after the activity. In all studies included, the detec- tion of bacteria in the bloodstream was performed using conventional microbiological techniques, although we found marked differences in the types of transport and culture media used, incubation atmospheres and incubation times (Robinson et al. 1950, Sconyers et al. 1973, Madsen 1974, Silver et al. 1977, Schlein et al. 1991, Hartzell et al. 2005, Kinane et al. 2005, Forner

et al.

2006, Murphy et al. 2006,

Crasta et al. 2009, Lockhart et al. 2009, Fine et al. 2010). There were three article in which bacterial quantification was performed using pour-plate (Sconyers et al. 1973, Fine et al. 2010) or lysis-filtration (Forner et al. 2006) techniques. Only Kinane et al. (2005) made simultaneous use of conventional

microbiological techniques and poly- merase chain reaction (PCR) analy- sis. Phenotypic identification of the bacterial isolates was performed in 10 article (Robinson et al. 1950,

et al. 1950, Sconyers

§§

Conclusions

magnitude)

prevalence)

prevalence,

prevalence

duration)

duration

No (on

(on

No (on

and

and

No

Basal = 0 CG = 0; GG = 0; PG = 0.19 (0.110.22) CG = 0; GG = 0; PG = 0 CG = 0; GG = 0; PG = 0.11

On prevalence (at 30 seg after chewing):

Basal = 0%; CG = 0%; GG = 0%; PG = 0% Basal = 0%; CG = 0%; GG = 0%; PG = 5% On magnitude in CFU/ml (at 30 s and 10 and 30 min after chewing):

On prevalence (at 2 min ± 30 s after chewing): Basal = 50%; GG = 35%** Clinical parameters (mean values of subjects with pos-BC versus subjects with neg-BC) = PI (2.00 versus 1.88); GI (1.75 versus 1.72) On magnitude in CFU/ml (at 23 min after chewing):

Basal = 7%; GG = 0%; PG = 0% On duration (at 5 min after chewing):

Basal = 0%; CG = 0%; GG = 0%; PG = 20% On duration (at 10 and 30 min after chewing):

Basal = 7%; GG = 0%; PG = 0%

Basal = 12; GG = 19.5025.70** On prevalence (at 23 min after chewing):

Table 4. Characteristics, results and conclusions of the selected studies on the development of bacteraemia from chewing, in reverse chronological order

Results

Blood sample of 20 ml collected at 23 min and 5 min BACTEC aerobic and anaerobic culture bottles BACTEC automated system Subculture: MacC agar (aero-incubation

at 35 °C), at 35°C)

Blood sample of 2 ml collected at 2 min ± 30 s Transport tubes containing 1% SPS Direct plating method: TS agar (aero-incubation at 35 ± 2° C for 12 days), SB agar (anaero-incubation at 35 ± 2°C for 57 days) Staff at laboratory were blinded

Blood sample of 9 ml collected at 30 s, 10 min and 30 min Transport tubes containing 0.35% SPS lysis-filtration method: TS agar (anaero-incubation at 37° C for 10 days) Subculture: TS agar and R-SL agar Phenotypic identification Genotypic identification (gdh gene, 16S rRNA) Sample size not calculated

not specified

Microbiological processing Statistical analysis

at 35°C), HB agar and Choc agar

(anaero-incubation

Phenotypic identification

size identification

calculated

Sample size calculated

agar 2 -incubation §

Phenotypic

(5% CO

Sample

BHI

Plaque-induced GG (20); untreated chronic PG (21) Previously described by Mariotti (1999); at least four sites with PPD and CAL 5 mm and radiographic bone loss PI at 2 s/t (Silness & Loe 1964)¨ GI at 2 s/t (Loe & Silness 1963)¨ PPD at 6 s/t BOP at 6 s/t Recession at 6 s/t Tooth mobility (Miller 1938) One examiner (CA and RE) CG (20); GG (20); PG (20) Distance between CEJ and alveolar bone < 2 mm, PPD < 4 mm, GI < 1.5; distance between CEJ and alveolar bone <2 mm, PPD < 4 mm, GI > 1.5; At least 10 sites with PPD > 5 mm PI (Silness & Loe 1966)¨ GI (Loe & Silness 1963)¨ PPD and PSS BOP CAL One general dental practitioner

PI (Turesky modification of the Quigley

Mild to moderate GG (62) Presence of a PI 1.5 and modified

Type of subjects (n) Diagnostic criteria Register of parameters related to OHS, GS and/or PS* Examiner

Hein Index) (Turesky et al. 1970) Modified GI (Lobene et al. 1986) No description of examiner

1.5

GI

Three pieces of chewing gum (10 min)

A standardized

Characteristics

Three bites of an apple (2 min)

of chewing

paraffin

(4 min)

References

Fine et al.

Murphy

(2006)

(2010)

(2006)

Forner

et al.

et al.

222 Toma´ s et al.

© 2011 John Wiley & Sons A/S

OHS = oral hygiene status; GS = gingival status; PS = periodontal status; CG = control group; GG = gingivitis group; PG = periodontitis group; s/t = sites per tooth; PPD = probing pocket depth; CAL = clinical attachment loss; CEJ = cemento-enamel junction; GI = Gingival Index; PI = Plaque Index; BOP = bleeding on probing; PSS = Pocket Sum Score; CA = cali- bration; RE = reproducibility; MacC = MacConkey; BHI = brain heart infusion; HB = horse blood; Choc = chocolate; aero-incubation = plates that were incubated aerobically; 5% CO 2 - incubation = plates that were incubated at 5% CO 2 ; anaero-incubation = plates that were incubated anaerobically; SPS = sodium polyanethol sulfonate; SB = Schaedler blood; TS = trypti-

was calculated to provide at least 90% power to detect a 5 CFU/ml treatment dierence on bacteraemia after chewing between the essential oil-containing

Conclusions

prevalence)

No (on

**In this study, bacteraemia was defined as a minimum increase after the apple challenge of 10 CFU/ml above the magnitude of bacteraemia detected under basal conditions.

of bacteraemia and oral hygiene, gingival or periodontal status.

On prevalence (immediately after chewing):

= 8% ; Total G = 0%

Results

Basal

case soy; R-SL = Rogosa SL; pos-BC = positive blood cultures; neg-BC = negative blood cultures; Total G = overall group.

Blood sample of 10 ml collected immediately Transport tubes containing tryptic digest broth with dextrose (aero-incubation at 37°C for 7 days) Subculture: blood agar Phenotypic identification of streptococci Sample size not calculated

analysis.

Microbiological processing Statistical analysis

development

a statistical

*Parameters related to OHS, GS and/or PS were recorded after the clinical diagnosis was established.

between

not perform

association

did

paper.

authors

signicant

original

Subjects with no previous diagnosis of OHS, GS and/or PS (21) Non-available Gingival inflammation Tooth mobility No description of examiner

Type of subjects (n) Diagnostic criteria Register of parameters related to OHS, GS and/or PS* Examiner

as the

in the

no the statistically

paper

was described in

reported

those

there

that on

K. rst bite.

the results

based

size blood.

mouthwash and control mouthwash.

on means

re-calculated

after the

5% sheep

Characteristics

34 “inch cube of tough” (510 min)

No

vitamin

of chewing

with sample

were is based

drawn

results section:

blood was with

Table 4. (continued)

this study, the

conclusion

Supplemented

Supplemented

Conclusions

References

Robinson

These

(1950)

et al.

§§ ‡‡ †† This

¶ § The

‡ † In

© 2011 John Wiley & Sons A/S

Periodontal status and oral bacteraemia

223

Sconyers et al. 1973, Madsen 1974, Silver et al. 1977, Schlein et al. 1991, Hartzell et al. 2005, Kinane

et al. 2005, Forner et al. 2006, Mur-

phy et al. 2006, Crasta et al. 2009),

while Forner et al. (2006) and Lockhart et al. (2009) performed genotypic identification of the bacte- ria isolated in positive blood cul- tures.

Statistical methods used to measure exposure to B-EOA

In the article on B-EOA evaluating the influence of oral hygiene, gingi- val or periodontal status in subjects with a previous diagnosis of a gingi-

val and/or periodontal condition, the analysis of the results was based on

a comparison of the percentages of

positive and negative post-activity blood cultures between the different groups (Madsen 1974, Forner et al.

2006, Murphy et al. 2006, Crasta

et al. 2009). In studies evaluating the

influence of more than one clinical parameters, the data were analysed in several ways: comparison of the mean values of the different clinical parameters between subjects with positive and negative blood cultures (Sconyers et al. 1973, Fine et al. 2010), comparison of the percentage of subjects with and without bactera-

emia in a given value range of a clin- ical parameter (Madsen 1974, Silver

et al. 1977, Schlein et al. 1991,

Kinane et al. 2005), calculation of the risk statistics (e.g. OR and 95% CI) (Lockhart et al. 2009), or the

use of statistics of association between the clinical parameters and the development of B-EOA (Crasta

et al. 2009).

Reference to the sample size calculation

Only five of the 12 selected article (42%) performed a calculation of the sample size (Hartzell et al. 2005, Murphy et al. 2006, Crasta et al. 2009, Lockhart et al. 2009, Fine

et al. 2010).

Quantitative outcomes analysis

The results of the selected studies are described in Tables 24.

Studies on B-toothbrushing (seven article)

All the studies on B-toothbrushing included in the systematic review evaluated the influence of the oral

224 Toma´ s et al.

hygiene, gingival or periodontal sta-

tus on the prevalence of bacteraemia

(Sconyers et al. 1973, Madsen 1974, Silver et al. 1977, Schlein et al. 1991, Hartzell et al. 2005, Kinane et al. 2005, Lockhart et al. 2009), two arti- cle analysed the duration (Hartzell

et al. 2005, Lockhart et al. 2009) and one paper determined the bacte- rial diversity (Silver et al. 1977). In five of the seven selected article,

the authors found no statistically sig-

nificant association between the state of oral hygiene, gingival or periodon- tal status and the development of B-toothbrushing (Sconyers et al. 1973, Madsen 1974, Schlein et al.

1991, Hartzell et al. 2005, Kinane et al. 2005). In patients with PI and GI scores greater than 1.50, Silver et al. (1977) detected B-toothbrush- ing percentages of 60% and 62%, respectively, compared to 35% and 25%, respectively, in patients with PI and GI scores between 0 and 1.50; those authors also demonstrated that positive post-toothbrushing blood cultures with isolation of three or more different bacterial species were significantly more common in patients with GI scores greater than 1.50 than in those with GI scores between 0 and 1.50 (28% versus 2%). Lockhart et al. (2009), analysing the influence of a number of clinical parameters, found a significant effect

of the following parameters on the

prevalence and duration of B-tooth- brushing: PI 2.00 (OR = 3.78, 95% CI = 1.4110.16), calculus index

2.00 (OR = 4.43, 95% CI = 1.6012.25) and the type of bleeding (gen- eralized versus localized bleeding) after the activity (OR = 7.96, 95%

CI = 1.4942.56).

Studies on B-dental flossing (one paper)

Crasta et al. (2009) evaluated the influence of oral hygiene, gingival and periodontal status on the preva- lence (at 30 s), duration (at 10 min.) and bacterial diversity of B-dental flossing. They detected no statisti- cally significant association between oral hygiene, gingival or periodontal status and the development of B- dental flossing.

Studies on B-chewing (four article)

All four studies on B-chewing included in the systematic review evaluated the influence of oral hygiene, gingival or periodontal sta- tus on the prevalence of B-chewing (Robinson et al. 1950, Forner et al. 2006, Murphy et al. 2006, Fine et al. 2010), two article analysed the dura- tion (Forner et al. 2006, Murphy et al. 2006) and one paper deter- mined the magnitude (Forner et al. 2006). None of the four studies revealed a statistically significant association between oral hygiene, gingival or periodontal status and the development of B-chewing.

Meta-analysis

Individual and pooled OR and 95% CI, the weight (%) of each study and I 2 -statistic values are shown in Fig- ure 2. The studies by Silver et al. (1977) and Lockhart et al. (2009) pre- sented the highest weight in the analysis of PI (F-effects = 43.50% and 35.39%, respectively) and of GI (F-effects = 48.59% and 39.91%, respectively). Evaluating the influence of the PI (01.50 versus 1.51) on the preva-

lence of bacteraemia following toothbrushing, the F-effects pooled OR was 2.61 (95% CI = 1.454.69) with statistically non-significant het- erogeneity ( I 2 = 0%, p = 0.576). Evaluating the influence of the GI (01.50 versus 1.51) on the preva- lence of bacteraemia following toothbrushing, the F-effects pooled OR was 2.77 (95% CI = 1.505.11), with statistically non-significant het- erogeneity (I 2 = 17.6%; p = 0.303).

Discussion

Eligibility criteria

The prevalence of bacteraemia after everyday oral activities (mainly toothbrushing) detected in children appears to differ from that of adults (Bhanji et al. 2002, Kinane et al. 2005); it would therefore be inappro- priate to perform a direct compari- son of the findings obtained in subjects aged 15 years or older. Baseline blood sample collection (prior to performing any everyday oral activity) is a standard methodo- logical characteristic in studies of B-EOA (Robinson et al. 1950, Scon- yers et al. 1973, Madsen 1974, Silver et al. 1977, Schlein et al. 1991, Hartzell et al. 2005, Kinane et al. 2005, Forner et al. 2006, Murphy et al. 2006, Crasta et al. 2009, Lock- hart et al. 2009, Fine et al. 2010). In 2004, in a paper published jointly with the Bristish Cardiac Society Clinical Practice Committee & Royal College of Physicians (2004) stated that to obtain results on significant oral bacteraemia, it is necessary to exclude those reports in which the investigators did not take a

those reports in which the investigators did not take a Fig. 2. Meta-analysis (Forrest Plots, fixed-effects

Fig. 2. Meta-analysis (Forrest Plots, fixed-effects model) of the influence of plaque and gingival indices on the prevalence of bactera- emia following toothbrushing (four article): individual and pooled OR and 95% CI, the weight (%) of each study and the I 2 statis- tic value. The I 2 statistic defines the proportion of the total variance caused by between-study variance: high values ( > 75 %) indicate marked heterogeneity between studies and low values ( < 40% ) indicate a low level of heterogeneity (Takkouche et al. 1999).

© 2011 John Wiley & Sons A/S

pre-activity blood sample. We there- fore only selected those studies on B-EOA that included a determina- tion of basal bacteraemia. Some authors investigated the development of B-EOA in a single group of subjects with healthy gin- giva and periodontium, in patients with gingivitis or in patients with periodontitis, but they did not ana- lyse the influence of different oral hygiene, gingival and periodontal index values (Diener et al. 1964, Romans & App 1971, Berger et al. 1974; Ramadan et al. 1975). We decided to select only the studies on B-EOA that, using the same method- ology, simultaneously analysed the influence of oral hygiene, gingival or periodontal status on the develop- ment of bacteraemia in subjects with different gingival and/or periodontal diagnosis or those with different oral hygiene, gingival and periodontal index values, as described in Mate- rial and Methods section (“Screening and selection of article”). We recognize the risk of publica- tion bias as the literature search was limited to English-language articles.

Methodological study quality assessment

Almost all article reported informa- tion on the different variables used to assess the methodological quality, although there was marked heteroge- neity. With regard to possible selection bias, the parameters most frequently considered were the presence of sys- temic infections and/or other sys- temic diseases and previous drug treatment (Madsen 1974, Silver et al. 1977, Schlein et al. 1991, Kinane et al. 2005, Forner et al. 2006, Mur- phy et al. 2006, Crasta et al. 2009, Lockhart et al. 2009, Fine et al. 2010), followed by certain oral or dental factors (Sconyers et al. 1973, Madsen 1974, Hartzell et al. 2005, Kinane et al. 2005, Forner et al. 2006, Murphy et al. 2006, Crasta et al. 2009, Lockhart et al. 2009, Fine et al. 2010). Parahitiyawa et al. (2009) stated that the effect of routine personal oral hygiene measures and chewing on the development of bacteraemia is difficult to evaluate, mainly due to the different characteristics associ- ated with the performance of each activity. The studies on B-tooth-

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225

brushing included differences in brushing time (14 min.), the type of brush used (manual or powered), the use of toothpaste or mouthwashes and whether the subject or investiga- tor performed the activity (Sconyers et al. 1973, Madsen 1974, Silver et al. 1977, Schlein et al. 1991, Hartzell et al. 2005, Kinane et al. 2005, Lockhart et al. 2009). Further- more, in one paper the toothbrush- ing was complemented by the use of toothpicks (Madsen 1974). With respect to the type of brush used, Bhanji et al. (2002) and Misra et al. (2007) demonstrated that powered toothbrushing produced a signifi- cantly higher rate of bacteraemia than did manual toothbrushing. In the studies on B-chewing, differences were detected in the chewing time (210 min.) and in the consistency of the material chewed (Robinson et al.

1950, Forner et al. 2006, Murphy et al. 2006, Fine et al. 2010). On this subject, a series published by Cobe (1954) showed that chewing hard candy provoked a higher incidence of bacteraemia than chewing gum (17.4% versus 0%). Murphy et al. (2006) stated more recently that the different consistencies of the various chewing mediums could contribute to the differences in bacteraemia rates reported. Differences were detected in the diagnostic criteria used for the defi- nition of subjects with good gingival and periodontal health, patients with gingivitis and patients with peri- odontitis (Madsen 1974, Kinane et al. 2005, Forner et al. 2006, Mur- phy et al. 2006, Crasta et al. 2009, Fine et al. 2010). These discrepancies could be justified by the fact that, to date, there is no generally accepted epidemiological definition for peri- odontitis (Page & Eke 2007, Savage et al. 2009). The most frequently used param- eters for the evaluation of oral hygiene, gingival and periodontal status were the plaque levels and the degrees of gingival inflammation (Robinson et al. 1950, Sconyers et al. 1973, Madsen 1974, Silver et al. 1977, Schlein et al. 1991, Hartzell et al. 2005, Forner et al. 2006, Murphy et al. 2006, Crasta

2009, Lockhart et al. 2009,

et al.

Fine et al. 2010) and, less frequently, the depth of periodontal pockets and degree of tooth mobility (Robinson

et al. 1950, Sconyers et al. 1973, Kinane et al. 2005, Forner et al. 2006, Murphy et al. 2006, Crasta et al. 2009, Lockhart et al. 2009). However, Lockhart et al. (2009) rec- ognized that there is no consensus on which clinical measures of oral hygiene, gingival or periodontal sta- tus are most appropriate to study with regard to risk of developing bacteraemia. Roberts et al. (1992) studied the prevalence of post-extraction bacter- aemia at different times after com- pleting the operative procedure (at 10, 30, 60, 90, 120, 180 and 600 s). They found that the highest preva- lence of bacteraemia occurred at 30 s after tooth extraction. However, we have found no studies in the liter- ature that have evaluated the opti- mum time for analysing the prevalence in B-EOA. In the present review, the moment at which the blood sample was taken after per- forming the activity of daily living was variable, being during the activ- ity (Lockhart et al. 2009) or up to 3 min. later (Schlein et al. 1991). Most studies have applied con- ventional qualitative microbiological techniques for the detection and identification of bacterial isolates, and differences were detected in the techniques used (broth culture, pour- plate and lysis-filtration), transport and culture media, atmosphere, incu- bation times and in the characteris- tics of the phenotypic identification (Robinson et al. 1950, Sconyers et al. 1973, Madsen 1974, Silver et al. 1977, Schlein et al. 1991, Hartzell et al. 2005, Kinane et al. 2005, Forner et al. 2006, Murphy et al. 2006, Crasta et al. 2009, Lock- hart et al. 2009, Fine et al. 2010). These differences in microbiological methodology were particularly noticeable when we compared stud- ies reported in the period 19501977 (Robinson et al. 1950, Sconyers et al. 1973, Madsen 1974, Silver et al. 1977) with those reported in 20052010 (Kinane et al. 2005, Forner et al. 2006, Lockhart et al. 2009), detecting greater precision in the detection and identification of bacterial isolates in the article pub- lished more recently. However, some authors have therefore stated that “it is likely that oral bacteria recovered from blood by culture are probably only part of those present there”

226 Toma´ s et al.

(Olsen 2008). It should be noted that molecular sequence-based methods have higher sensivities than do cul- ture-based methods (Parahitiyawa et al. 2009). In particular, 16S RNA- based methods have brought renewed interest to this field for the specific detection and identification of oral microorganisms, as shown by the studies performed by Kinane et al. (2005) and Lockhart et al. (2009). Recently it has been demon- strated that real-time PCR and pyrosequencing can identify microor- ganisms directly from positive blood culture bottles as accurately as cul- ture-based methods (the two tech- niques were concordant for 97.8% of the bacteria) (Jordan et al. 2009). Hence, it is imperative that these molecular sequence-based methods be validated and used in prospective trials of oral bacteraemia, including B-EOA. In the studies on B-EOA in which different clinical gingival and periodontal parameters were recorded, varying statistical methods were used to measure the exposure to B-EOA. The most widely used was the comparison of the percent- age of subjects with and without post-activity bacteraemia for a given value range of a clinical parameter (Madsen 1974, Silver et al. 1977, Schlein et al. 1991, Kinane et al. 2005). Based on the design of studies of B-EOA, it is particularly useful to calculate the risk indices (Rutledge & Loh 2004); however, the only study in which the OR and 95% CI were calculated was the one pub- lished by Lockhart et al. (2009). In the present review, only five of the 12 selected article, all of them pub- lished recently, performed a calcula- tion of the sample size (Hartzell et al. 2005, Murphy et al. 2006, Crasta et al. 2009, Lockhart et al. 2009, Fine et al. 2010). In agreement with some authors (Rutledge & Loh 2004), we recognize that a suitable sample size is an important statistical consideration. It is well known that an apparent lack of statistical signifi- cance can often be attributed to design in a study based on a sample that is too small to detect a given level of difference (Rutledge & Loh 2004). However, this dogma has been challenged by authors who con- sider that some information is better than none and that even a small

amount of inconclusive information may contribute to a later systematic review (Guyatt et al. 2008). Never- theless, in our opinion, the results obtained in six of the remaining seven studies (in which no calcula- tion of the sample size was per- formed) reporting “no statistically significant association between the state of oral hygiene, gingival or periodontal status and the develop- ment of B-EOA” should be inter- preted with caution (Robinson et al. 1950, Sconyers et al. 1973, Madsen 1974, Schlein et al. 1991, Kinane et al. 2005, Forner et al. 2006).

Influence of oral hygiene, gingival and periodontal status on the prevalence of bacteraemia from everyday oral activities

Most studies included in this review reported very low percentages of bacteraemia under basal conditions (02%) (Sconyers et al. 1973, Mad- sen 1974, Silver et al. 1977, Schlein et al. 1991, Hartzell et al. 2005, Forner et al. 2006, Crasta et al. 2009, Lockhart et al. 2009), although some authors have reported figures of 68% of positive blood cultures (Robinson et al. 1950, Kinane et al. 2005, Murphy et al. 2006). Toothbrushing is the activity of daily living for which there is greatest evidence of an influence on the preva- lence of bacteraemia depending on the state of oral hygiene, gingival or periodontal status (Sconyers et al. 1973, Madsen 1974, Silver et al. 1977, Schlein et al. 1991, Hartzell et al. 2005, Kinane et al. 2005, Lockhart et al. 2009). In most article (five of seven; 71%), the authors found no statistically significant association between the state of oral hygiene, gingival or periodontal status and the prevalence of B-toothbrushing (Sconyers et al. 1973, Madsen 1974, Schlein et al. 1991, Hartzell et al. 2005, Kinane et al. 2005). The results obtained in the present meta-analysis showed a significant influence of the plaque and gingival indices (01.50 versus 1.51) on the prevalence of bacteraemia following toothbrushing (OR = 2.61, 95% CI = 1.454.69 and OR = 2.77, 95% CI = 1.505.11, respectively). There are few studies published on the influence of oral hygiene, gin- gival or periodontal status on the prevalence of bacteraemia after per-

forming other activities of daily living (one paper on B-dental flossing and four article on B-chewing) (Robin- son et al. 1950; Forner et al. 2006, Murphy et al. 2006, Castra et al. 2009; Fine et al. 2010). In those five studies, there was no statistically sig- nificant association between the state of oral hygiene, gingival or peri- odontal status and the prevalence of B-dental flossing (Crasta et al. 2009) or B-chewing (Robinson et al. 1950, Forner et al. 2006, Murphy et al. 2006, Fine et al. 2010).

Influence of oral hygiene, gingival and periodontal status on the duration, magnitude and bacterial diversity of bacteraemia from everyday oral activities

To date, there are no data indicating that a greater duration or magnitude of bacteraemia is more likely to cause a focal infection of oral origin (Lock- hart & Durack 1999, Wilson et al. 2007). However, the bacterial inocu- lum size in individuals with healthy versus diseased gingival tissues needs to be explored (Roberts 1999), as a higher magnitude of bacteraemia would take longer to clear from the bloodstream (Crasta et al. 2009). On the other hand, several studies have demonstrated the presence of period- ontopathogens in atherosclerotic pla- ques and aortic aneurysms (Pucar et al. 2007, Gaetti-Jardim et al. 2009, Nakano et al. 2009), which indicates previous episodes of bacteraemia. However, only four studies evaluated the influence of the oral health status on the duration of the B-EOA (Forn- er et al. 2006, Murphy et al. 2006, Crasta et al. 2009, Lockhart et al. 2009). Of these studies, only the one published by Lockhart et al. (2009) detected a significant association between PI, the type of bleeding after toothbrushing and the duration of B-toothbrushing. With respect to the magnitude of the B-EOA, only one paper (Forner et al. 2006) analysed the influence of oral hygiene, gingival and periodon- tal status on the magnitude of B-chewing, finding no relationship. The influence of oral hygiene, gingi- val and periodontal status on the bacterial diversity of B-EOA was evaluated in only two article, one on B-toothbrushing (Silver et al. 1977) and one on B-dental flossing (Crasta et al. 2009), with conflicting results.

© 2011 John Wiley & Sons A/S

Conclusions

Meta-analysis showed that plaque accumulation and gingival inflam- mation significantly increase the prevalence of B-toothbrushing. Sys- tematic review showed no relation- ship between oral hygiene, gingival and periodontal status and the devel- opment of B-chewing, and there is no evidence that gingival and periodon- tal health status affects B-flossing. Further studies are needed to investigate the correlation between gingival and periodontal status and the development of B-EOA, and the analysis of other important parame- ters such as duration, magnitude and bacterial diversity of B-EOA should be considered.

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Supporting Information

Additional Supporting Information may be found in the online version of this article:

Appendix 1. Prisma checklist. Appendix 2. Reviews used for screen- ing of unpublished data and reference checking, in reverse chronological

order (n = 35). Appendix 3. Studies on bacteraemia from everyday oral activities which were excluded from the systematic review/meta-analysis and main rea- sons for rejection, in reverse chrono- logical order (n = 22).

Please note: Wiley-Blackwell is not responsible for the content or functionality of any supporting materials supplied by the authors.

Any queries (other than missing material) should be directed to the corresponding author for the article.

Address:

I. Toma´ s School of Medicine and Dentistry Santiago de Compostela University C./Entrerrios s/n 15872 Santiago de Compostela Spain E-mail: inmaculada.tomas@usc.es

Clinical Relevance

Scientific rationale for the study:

Everyday oral activities (EOA) can provoke bacteraemia. The clinical relevance of these bacte- raemias remains unknown, but EOA may represent a greater risk than dental procedures because of cumulative exposure. The purpose of this study was to investigate

the influence of oral hygiene, gin- gival and periodontal status on the development of bacteraemia due to EAO. Principal findings: Plaque accumu- lation and gingival inflammation significantly increase the preva- lence of bacteraemia from tooth- brushing. Oral hygiene, gingival and periodontal status did not

favour the development of bacter- aemia from chewing, and there is no enough evidence that they affect bacteraemia from flossing. Practical implications: Mainte- nance of optimal oral hygiene may reduce the risk of bactera- emia from toothbrushing.

© 2011 John Wiley & Sons A/S