Shared detection of Porphyromonas gingivalis in cohabiting family members: a systematic review and meta-analysis

Figures & data

Figure 1. Flowchart of the literature search and article selection

Table 1. Summary of the included studies assessing the simultaneous detection of Porphyromonas gingivalis (Pg) between adult couples of the same family

Author and year	Study design	Number of couples	Periodontal status of the proband	Periodontal status of the spouses	Bacteria sampling	Detection methods	Proportion of intra-familial transmission
Petit et al. 1993	Case series	4	Adult periodontitis	Adult periodontitis	4 periodontal pockets Mucous membrane Dorsum of the tongue	Culture DNA-REA	Culture: 3/4 DNA-REA: 0/4
Van Steenbergen et al. 1993a	Case series	18	Untreated adult severe periodontitis (at least 10 pockets of ≥5 mm and at least one pocket with ≥ 4 mm of attachment loss and sub-gingival presence of Pg)	5/18 spouses diagnosed as periodontitis patients	4 deepest pockets (by paper points) Buccal mucosal Dorsum of the tongue Tonsillar area Saliva	Culture DNA-REA	Culture: 8/18 DNA-REA: 6/18
Van Steenbergen et al. 1993	Case series	8	Severe adult periodontitis and subgingival presence of Pg		4 deepest pockets (by paper points) Buccal mucosa Dorsum of the tongue Tonsillar area Saliva	DNA-REA AP-PCR Ribotyping	DNA-REA: 6/8 AP-PCR: 6/8 Ribotyping: 6/8
Saarela et al. 1993	Case series	4	Advanced periodontitis and subgingival presence of Pg	Advanced periodontitis and subgingival presence of Pg	Deepest, the most inflamed periodontal pockets (by curette) Stimulated saliva	Serotyping Ribotyping	Ribotyping: 2/4 (married couples for at least 10 years)
Von Troil Lindén et al. 1995	Case-control	10 vs. 10	Advanced periodontitis probands vs. periodontally healty controls	Not specified	6 deepest and most inflamed periodontal pockets (by sterile curette) Stimulated saliva	Culture	Probands: 6/10 on subgingival samples 2/10 on salivary samples Controls: 1/10 on subgingival samples 0/10 on salivary samples
Asikainen et al. 1996	Case series	15	Adult periodontitis (AAP Classification 1989)	Adult periodontitis (85% of spouses)	4 to 6 deepest periodontal pockets (by curette) Dorsum of the tongue From healthy subjects: mesial subgingival sites of the first molars.	Culture AP-PCR	Culture: 9/15 AP-PCR: 2/15
Van der Velden et al. 1996	Longitudinal study Time frame: 1987–1994	22	No specific definition (based on clinical parameters: plaque index, calculus, probing depth, bleeding on probing, loss of attachment)	Not specified	4 periodontal pockets (paper points)	Culture	Culture: 9/22
Tuite-McDonnell et al. 1997	Cross-sectional	43	17% of individuals had at least one site with an attachment level or PPD ≥5.5 mm	Not specified	all teeth (paper point)	PCR	PCR: 32/43 Spouses were significantly more frequently colonized by Pg (RR: 4 [95%CI: 2.3–7]) than what would be expected if Pg was randomly distributed in the study population. No relationship was observed between the length of time a couple had been married and their concordance of colonization.
Von Troil Linden et al. 1997	Longitudinal experimental study Six month follow up study	8	Advanced periodontitis	3 spouses: moderate periodontitis undergone a mechanical treatment combined with metronidazole. 7 spouses: mild to moderate periodontitis were untreated	6 deepest and most inflamed pockets Paraffin-stimulated saliva	Culture	Culture: 4/8
Van Winkelhoff et al. 1999	Longitudinal study. Time frame: 1987 – 1994	19	No selection on the periodontal status	Not specified	4 sub-gingival samples using 1 paper point per pocket	Culture Serotyping	Culture: 15/19 Serotyping: 0/19
Asano et al. 2003	Cross-sectional	25	Periodontitis defined as at least 4 pockets with PPD > 4 mm and radiographs showing the presence of at least one intrabony defect > 4 mm.	Not specified	3 deepest pockets (by paper points), or gingival sulci	Culture PFGE FimA genotyping	Culture: 14/25 PFGE: 6/14 The frequency of FimA type II in isolates from the 6 couples with identical PFGE patterns was 83.3%, which was higher than for the periodontitis unrelated patients (46.8%) (positive for Pg).
Park et al. 2004	Case series	16	Chronic and aggressive periodontitis	Not specified	3 sterile paper points into the mesial sulcus of diseased sites of the probands and the deepest sites of their family members	PCR (Isi 1126 specific primer)	PCR (Isi 1126): 5/16
Rijnsburgurger et al. 2007	Case series	6	Untreated severe periodontitis	Not specified	Subgingival samples Dorsum of the tongue Buccal mucosa, Tonsils Saliva	REA AFLP-PCR	REA: 4/6 AFLP-PCR: 4/6 (showing a similarity >85%)
Van Winkelhoff 2007	Cross-sectional	13	Population without regular dental care	Not specified	Deepest bleeding sites with the greatest amount of attachment loss	AFLP-PCR	AFLP-PCR: 0/13
Van Winkelhof 2008	Longitudinal study. Time frame: 1994–2002	27	Population without regular dental care	Not specified	Deepest bleeding sites with the greatest amount of attachment loss	Culture AFLP-PCR	Culture: 1994: 13/27 2002: 18/27 AFLP-PCR: 1994: 0/27 2002: 3/27
Martelli et al. 2012	Case series	9	Untreated periodontitis	Untreated periodontitis	One pocket per quadrant (by paper point)	PCR FimA genotyping	PCR: 6/9 FimA type II: 6/9
Feng et al. 2015	Case series	10	Aggressive periodontitis	Not specified	Subgingival samples Saliva	PCR FimA genotyping	PCR: 7/10 FimA genotyping: 7/10

AP-PCR stands for arbitrarily primed polymerase chain reaction; BOP for bleeding on probing; PPD for probing pocket depth; PI for plaque index; Pg for Porphyromonas gingivalis. Aa for Agregatibacter actinomycetemcomitans. Pi for Prevotella intermedia. AFLP: Amplified fragment length polymorphism, DNA REA: Deoxyribo Nucleic Acid Restriction Endonuclease Analysis; Fim A: Fimbriae A.

Table 2. Summary of the included studies assessing the simultaneous detection of Porphyromonas gingivalis (Pg) between parents and children of the same family

Author and year	Study design	Number of children	Periodontal status of the parents	Periodontal status of the children	Bacteria sampling	Detection methods	Main findings (Number of positive/Total)
Petit et al. 1993	Case series	10	Adult periodontitis	Severe generalized juvenile periodontitis (GJP) with presence of Aa and Pg	4 periodontal pockets Mucous membrane Dorsum of the tongue First molar if no PPD	Culture DNA-REA	Culture: 7/10 DNA REA: 5/10
Petit et al. 1994	Case series	36	Untreated adult severe periodontitis (at least 10 pockets of ≥5 mm and at least one pocket with ≥ 4 mm of attachment loss and subgingival presence of Pg or Aa or Pi)	Not specified	4 periodontal pockets Mucous membrane Dorsum of the tongue Tonsilla area Saliva First molar if no PPD	Culture	Culture: 1/36
Asikainen et al. 1996	Case series	19	Adult periodontitis (AAP Classification 1989)	5% of children exhibited periodontal destruction	4 to 6 deepest periodontal pockets (by curette) Dorsum of the tongue First molar if no PPD	Culture AP PCR	Culture: 1/19 No AP PCR (not enough samples)
Tuite-McDonnell et al. 1997	Cross sectional	103 oldest children with their mothers 101 oldest children with their fathers 98 adult children with their mothers 69 adult children with their fathers	17% of individuals had ≥ 1 site with an attachment level or PPD ≥ 5.5 mm	Not specified	All teeth (Paper points)	PCR	PCR (Oldest child with the mother): 20/103 PCR (Oldest child with the father): 17/101 PCR (Adult child with the mother): 25/98 PCR (Adult child with the father): 14/69
Umeda et al. 2004	Cross sectional	56	Only 4 parents had PPD > 4 mm	Not specified	Saliva + supragingival plaque (Children) Saliva (Parents)	PCR	PCR (Parent): 54.8% PCR (Children): 7.1%
Okada et al. 2004	Cross sectional	28	1 healthy individual 4 gingivitis 7 periodotnitis	6 healthy individuals 6 gingivitis 6 periodontitis	Supra-gingival plaque collected with sterile tooth brushes (1 min)	PCR	PCR: 6/28 (21.4%)
Park et al. 2004	Case series	14	Chronic and aggressive periodontitis	Not specified	3 Sub-gingival samples (Paper points)	PCR with Isi 1126 specific primer	PCR Isi 1126: 11/14
Tamura et al. 2006	Cross sectional	106	Not specified. All patients were recruited from the Periodontics Clinic of Osaka University Hospital.	No children had periodontitis	Saliva samples	PCR	PCR (Mothers): 42.5% PCR (Children): 2.7%
Kobayachi et al. 2008	Cross sectional	78	Not specified	No children had moderate or severe gingivitis	Sub-gingival plaque (first molar for children; first and second molars for mothers)	PCR	PCR (Mothers):17.6% PCR (Children): 9%
Belcheva et al. 2012	Case control	11	Group of diseased parents and their children Group of healthy parents and their children	Not specified	Deepest pockets (First molars and lower incisors) Sulci between premolars and molars when healthy	Culture PCR	Culture (Children): No detection PCR (Children): 2/11 The study did not find statistically significant difference (p> 0.05) in the prevalence of Pg between children with healthy parents and children whose parents presenting with periodontal disease
Monteiro et al. 2014	Case control	15	Generalized aggressive periodontitis (GAP) vs healthy	Not specified	Stimulated saliva (without dental hygiene-no brushing 2 hours before sampling)	PCR	PCR (Periodontitis parent): 50% PCR (Infant): 30% Parents with GAP showed statistically higher Pg salivary concentration than periodontally healthy parents (p < 0.05). Children of GAP families, however, exhibited similar Pg concentration than healthy children (p > 0.05).
Monteiro et al. 2015	Case control	15	Generalized aggressive periodontitis vs healthy	Not specified	Stimulated saliva (without dental hygiene-no brushing 2 hours before sampling)	PCR	PCR (Periodontitis parent): 80% PCR (Infant): 60%
Feng et al. 2015	Case series	10	Aggressive periodontitis	Not specified	Saliva Sub-gingival samples (First molars)	PCR with Fim A genotype Specific primers	PCR (Fim A genotyping): 7/10
Al Yahyoufi. 2017	Case series	11	Chronic and Aggressive Periodontitis	Not specified	4 Sub-gingival samples (Paper point in each quadrant)	DNA probe	DNA probe: 7/11

AP-PCR stands for arbitrarily primed polymerase chain reaction; Pg for Porphyromonas gingivalis. Aa for Aggregatibacter actinomycetemcomitans. Pi for Prevotella intermedia. AFLP: Amplified fragment length polymorphism; Fim A for Fimbriae A; DNA REA for Deoxyribo Nucleic Acid Restriction Endonuclease Analysis.

Table 3. Summary of the included studies assessing the simultaneous detection of Porphyromonas gingivalis (Pg) between siblings

Author and Year	Study Design	Number of Subjects	Periodontal Status of the Probands	Periodontal Status of the Siblings	Bacteria Sampling	Detection Method	Main Findings
Van winkelhoff et al. 1999	Longitudinal study 1987–1994	29 sibships	No selection on the periodontal status	Not specified	4 sub-gingival samples using 1 paper point per pocket	Culture Serotyping	Culture: 26/29 Serotyping: 3/29
Van Winkelhoff. 2007	Cross sectional study	10 sibships 30 siblings	Population without regular dental care	Not specified	Deepest bleeding site with the greatest amount of attachment loss	AFLP typing	2/10 Sibships 13/30 Siblings
Van Winkelhoff. 2008	Longitudinal study 1994–2002	23 sibships 54 siblings	Population without regular dental care	Not specified	Deepest bleeding site with the greatest amount of attachment loss	Culture AFLPT typing	Culture (1994): 22/23 Culture (2002): 22/23 AFLP PCR (1994): 6/23 AFLP PCR (2002): 6/23

Pg stands for Porphyromonas gingivalis. AFLP for Amplified fragment length polymorphism.

Figure 2. The likelihood of co-occurrence of P. gingivalis once a family member harbors P. gingivalis assessed by culture

Figure 3. The likelihood of co-occurrence of P. gingivalis once a family member harbors P. gingivalis assessed by culture and PCR

Figure 4. The likelihood of co-occurrence of P. gingivalis once a family member harbors P. gingivalis assessed by genotyping