Journal of Clinical Periodontology: 1979: 6: 252-259 Key words: Bone loss - gingival in f him ma lion. Accepted for publicalion: December 13. 1978.
Gingival inflammation and bone loss in periodontal disease B. KARDACIHI, G . N . WOLFFE2 AND J. D . MANSON-
1 Royal Adelaide Hospital, Adelaide, Australia 5 Institute of Dental Surgery, Eastman Dental Hospital, London, England Abstract. Fifty subjects between 27 and 43 years of age were studied to determine the relationship between the severity of gingival inflammation, the amount of bone loss and the plaque score in interproximal sites. The results indicate moderately good correlations between Gingiva! Index or Plaque Index and percentage bone loss. However a low correlation was found between the amount of crevicular fluid and percentage bone loss. Gingival Index and Plaque Index were well correlated. It was also found that when patients were divided into two age groups, younger and older than 35 years, the older individuals studied had more bone loss interproximally compared with the younger despite comparable amounts of plaque or gingival inflammation. The data suggest that both severity and longevity of the inflammation may play a role in determining the rate of alveolar bone resorption.
It has been demonstrated that there is a direct cause and effect relationship between bacterial plaque deposits and gingival inflammation (Loe et ai. 1965). Lindbe et al. (1973) have shown that in an experimental model gingival inflammation can progress to loss of tooth attachment and resorption of alveolar bone. However, there is no evidence to suggest that there is a correlation between the severity of ginglva! inflammation and the degree of alveolar bone resorption as periodontal disease progresses. Several workers have approached this problem. Glass et al. (1973) evaluated six variables associated with periodontal disease and they found, as part of their results, a low correlation between gingivitis and bone loss. However, their subjects ranged from 25 to 74 years of age. No attempt was made to compare parameters in a more
homogeneous group with a similar age range. It has been suggested (Holm-Pederson et al. 1975) that, under equivalent experimental conditions, elderly subjects with loss of alveolar support produce a greater degree of gingival inflammation than young adults. However, Glass et al. (1973) found that the gingival scores decreased over the age range of 20-64 years rising only in the 67 to 75year-old group, despite a progressive loss of support, indicating an inverse correlation between gingival inflammation and bone loss. Since clinical observation does not suggest obvious association between the severity of gingivitis and the degree of bone loss, the present study was undertaken to define this relationship in a homogeneous group of patients with chronic periodontitis. These pa-
0303-6979/79/040252-08$02.50/0 © 1979 Munksgaard, Copenhagen
GINGIVAL INFLAMMATION AND BONE LOSS
253
tietits had an age range usually associated with the earlier stages of bone destruction and were uncomplicated by tooth loss and occlusal trauma.
(4) A minimum of 24 teeth had to be present. (5) Female patients should not he pregnant and must be a minimum of 3 months post-partum.
Material and Methods
Clinical Measurements Measurements were made on the mesial and distal surfaces of the following teeth: 16, 12, 24, 36, and 44 as it has been shown that the use of selected teeth provides a basis for accurate assessment of the total periodonta! status of the individual (Ramfjord 1959). Buccal and lingual/palatal measurements were not made since it Is not possible to assess bone levels radiographically on these surfaces. Substitutions of the distal premolar and mesial incisor were made in four subjects, in all six teeth were substituted. (1) Crevicidar fluid (CF). The amount of crevicular fluid was measured according to the technique of Loe & Holm-Pederson (1965). The strips were stained with 0.2 % ninhydrine and measured to the nearest 0.5 mm. (2) Gingival Inflammation (GJ). The state of the gingiva was assessed using the Gingival Index system (Loe & Silness 1963).
The study was performed on 50 subjects, 26 males and 34 females between the ages of 27 and 43 years. Of these, 42 were between 30 and 40 years of age. Subjects were patients referred for initial consultation to the periodontal departments of the Eastman Dental Hospital, London, and the Royal Adelaide Hospital, Adelaide, Australia. Criteria Subjects were selected as follows: (1) No periodontal treatment must have been carried out previous to the study. In addition subjects should not have received scaling and polishing for at least 6 months prior to the stndy. (2) No acute gingival or periodontal conditions should be present. (3) Subjects should be medically fit and must not have had any recent medication, such as antibiotics which would influence plaque and gingivitis scores.
Table 1. Values for Gingival Index (GI), Plaque Index (PI) Crevicular Fluid (CF) and Percentage Bone Loss (BL) ^'Mean values per subject, s.d. — standard deviation Werte fur den Gingivalindex (GI), den Plaqueindex (PI), die Krevikularfiiissigkeit (CF) und den prozentualen Knochenverlust (BL) "Mittelwerte pro Proband. s.d. = Standarddeviation Valeurs de I'Indice Gingival (GI), de I'Indice de Plague (PI), du Fluide Creviculaire (CF) et de la Perte Osseuse en pourcentage (BL) *Valeurs moyennes par sujet. s.d. — ecart-type Variahle
n
* Minimum
^•Maximum
Mean
s.d.
GI PI CF (mtn)
50 50 50 50
0.33 0.18 0.09 3.89
2.90 2.60 8.!5 37.73
1.3 LI2
0.60 0.52 1.44 7.88
BL
Mean (Mitlelwert, moyenne)
1.73 13.71
KARDACHI, WOLFFE AND MANSON
254
(3) Plaque (PI). The amount of plaque was assessed using the Plaque Index system (Silness & Loe 1964). AU clinical measurements were carried out by one examiner (B.K.). The percentage of bone loss (BL) on the mesial and distal surfaces of the selected teeth Vk-as assessed as follows; long cone radiographs were taken using a distance of 21 cm from the focal spot to the tip of the cone. The films were held in Rinn Holders (Rinn XCP instruments for extension cone paralleling technique) and a Phillips Oralix Dental X-ray unit was used. Radio-
graphs were taken by two examiners (G.W./ B.K.) and were developed using standard automatic processing. The percentage bone loss was measured by one examiner (G.W.) on the mesial and distal surfaces of the selected teeth using the technique of Schei et al. (1959). Although radiographs have their limitations, Ramfjord (1974) suggests that the above method provides an accurate and reproducible method of assessing bone loss. Reprodu cib ility Intra-examiner reliability was assessed on 10
zs
0 0-5 10 1-5 £0 Z5 3O
0 06
GI Fig 1
1-0 1-5 2 0 25 3O
•5 3-0 4^5 6 0 75 9-0
PI
CF
0
r
(4
21 2a 35
BL
Distribution of Subjects within each index studied A - Gingival index (GI) B - Plaque index (PI) C - Crevicuiar fluid-mm of stained filter strip (CF) D - Percentage bone loss (BL)
Verteilung der Probanden innerhalb der registrierten Indizes. A - Gingivulindex (GI). B - Plaqueindex (PI). C - KrevikularflUssigkeit - mm gejdrbtes Filterpapier (CF). D - Knochenverlust in Prozent (BL). Distribution des sujets pour chague indice etudie. A Indice Gingival (GI). B - Indice de Plague (PI). C - Fluide Creviculaire - mm de coloration sur les bandelettes de papier filtre (CF). D Perte Osseuse en pourcentage (BL).
GINGIVAL INFLAMMATION AND BONE LOSS
subjects for both the clinical and radiographic measurements. Gingival Index and Plaque Index measurements were repeated after approximately 2 hours, whilst radiographic measurements were repeated after a 24-h interval. The reproducibility for Gingival Index was 80.8 %, for Plaque Index 77.5 % and for percentage of bone loss 86.3 %.
Results
Not all radiographs were readable. A total of 63 out of 600 surfaces (10.5 %) were unreadable due to overlap or inability to locate the cemento-enamel junction. The majority of unreadable areas were on the left upper
25S
first premolar due to difficulty with film placement because of palatal anatomy. The GI and PI scores and crevicular fluid (CF) values associated with these unreadable radiographs were not used in the result analysis. Table 1 gives the mean values with standard deviation for all the indices used; the mean for GI was 1.30; PI, 1.12; CF, 1.73. Histograms showing the distribution of each index in the sample studied are shown in Fig. 1 with the interval widths indicated. Fig. 2 shows the relationship for GI to PI, PI to BL (bone loss) and GI to BL (bone loss). Using coefficient of correlation analysis,
8L - 3Z * 91(Pn , =062
SL = 3 55 + B(Gn r = 062
20
BL Fig 2
BL
The correlation between the measured variables A = Ginqival index (GI) with Plaque index (PI) 8 = Plaque index with percentage Bone loss (BL) C = Gingivol index with percentage Bone lass
Der Zusammenhang zwischen den registrierien Variablen. A - zwischen Giiigivalindex (GI) und Plaqueindex (PI). B - zwischen Plaqueindex (PI) und Knochenverlust in Prozent (BL). C - zwischen Gingivalindex und Knochenverlust in Prozent. Correlation entre les variables mesurees. A - Indice Gingival (GI) et Indice de Plaque (PI). B Indice de Plaque el Perte Osseuse en pourcentage (BL). C - Indice Gingival et Perte Osseuse en pourcentage.
256
KARDACHI, WOLFFE AND MANSON
Table 2. Results and statistical analysis comparing Gingival Index (Gl), Plaque Index (PI) and Percentage Bone Loss (BL) in subjects less than 34 years of age with those 35 years or older s.d. = Standard Deviation. NS = Not Significant Resultat und statistische Analyse des Vergleiches zwischen Gingivalindizes (Gl). Plaqueindizes (PI) und dem prozentualen Knochenverlust (BL) bei Probanden die jUnger als 34 Jahre und Probanden die 35 Jahre und alter sind s.d. = Standardabweichung. NS = Nlcht slatistisch abgesichert Resultats el analyse statistique de la comparaison entre I'Jndice Gingival (Gl), I'lndice de Plaque (PI) et la Perte Osseuse en pourcentage (BL) chez les sujels de moins de 34 ans el chez ies sujels ages de 35 ans ou plus Variable Gl BL
Mean s.d. < 34 years
Mean s.d. > 35 years
Test used
Significance
1.14 ± 0.59 0.97 ± 0.50 11.69 ± 6.90
1.48 ± 0.58 1.29 ± 0.50 16.20 ± 8.4
Mann-Whitney U Mann-Whitney U Student's t
NS NS
Gingival inflammation and bone loss in periodontal disease B. KARDACIHI, G . N . WOLFFE2 AND J. D . MANSON-
1 Royal Adelaide Hospital, Adelaide, Australia 5 Institute of Dental Surgery, Eastman Dental Hospital, London, England Abstract. Fifty subjects between 27 and 43 years of age were studied to determine the relationship between the severity of gingival inflammation, the amount of bone loss and the plaque score in interproximal sites. The results indicate moderately good correlations between Gingiva! Index or Plaque Index and percentage bone loss. However a low correlation was found between the amount of crevicular fluid and percentage bone loss. Gingival Index and Plaque Index were well correlated. It was also found that when patients were divided into two age groups, younger and older than 35 years, the older individuals studied had more bone loss interproximally compared with the younger despite comparable amounts of plaque or gingival inflammation. The data suggest that both severity and longevity of the inflammation may play a role in determining the rate of alveolar bone resorption.
It has been demonstrated that there is a direct cause and effect relationship between bacterial plaque deposits and gingival inflammation (Loe et ai. 1965). Lindbe et al. (1973) have shown that in an experimental model gingival inflammation can progress to loss of tooth attachment and resorption of alveolar bone. However, there is no evidence to suggest that there is a correlation between the severity of ginglva! inflammation and the degree of alveolar bone resorption as periodontal disease progresses. Several workers have approached this problem. Glass et al. (1973) evaluated six variables associated with periodontal disease and they found, as part of their results, a low correlation between gingivitis and bone loss. However, their subjects ranged from 25 to 74 years of age. No attempt was made to compare parameters in a more
homogeneous group with a similar age range. It has been suggested (Holm-Pederson et al. 1975) that, under equivalent experimental conditions, elderly subjects with loss of alveolar support produce a greater degree of gingival inflammation than young adults. However, Glass et al. (1973) found that the gingival scores decreased over the age range of 20-64 years rising only in the 67 to 75year-old group, despite a progressive loss of support, indicating an inverse correlation between gingival inflammation and bone loss. Since clinical observation does not suggest obvious association between the severity of gingivitis and the degree of bone loss, the present study was undertaken to define this relationship in a homogeneous group of patients with chronic periodontitis. These pa-
0303-6979/79/040252-08$02.50/0 © 1979 Munksgaard, Copenhagen
GINGIVAL INFLAMMATION AND BONE LOSS
253
tietits had an age range usually associated with the earlier stages of bone destruction and were uncomplicated by tooth loss and occlusal trauma.
(4) A minimum of 24 teeth had to be present. (5) Female patients should not he pregnant and must be a minimum of 3 months post-partum.
Material and Methods
Clinical Measurements Measurements were made on the mesial and distal surfaces of the following teeth: 16, 12, 24, 36, and 44 as it has been shown that the use of selected teeth provides a basis for accurate assessment of the total periodonta! status of the individual (Ramfjord 1959). Buccal and lingual/palatal measurements were not made since it Is not possible to assess bone levels radiographically on these surfaces. Substitutions of the distal premolar and mesial incisor were made in four subjects, in all six teeth were substituted. (1) Crevicidar fluid (CF). The amount of crevicular fluid was measured according to the technique of Loe & Holm-Pederson (1965). The strips were stained with 0.2 % ninhydrine and measured to the nearest 0.5 mm. (2) Gingival Inflammation (GJ). The state of the gingiva was assessed using the Gingival Index system (Loe & Silness 1963).
The study was performed on 50 subjects, 26 males and 34 females between the ages of 27 and 43 years. Of these, 42 were between 30 and 40 years of age. Subjects were patients referred for initial consultation to the periodontal departments of the Eastman Dental Hospital, London, and the Royal Adelaide Hospital, Adelaide, Australia. Criteria Subjects were selected as follows: (1) No periodontal treatment must have been carried out previous to the study. In addition subjects should not have received scaling and polishing for at least 6 months prior to the stndy. (2) No acute gingival or periodontal conditions should be present. (3) Subjects should be medically fit and must not have had any recent medication, such as antibiotics which would influence plaque and gingivitis scores.
Table 1. Values for Gingival Index (GI), Plaque Index (PI) Crevicular Fluid (CF) and Percentage Bone Loss (BL) ^'Mean values per subject, s.d. — standard deviation Werte fur den Gingivalindex (GI), den Plaqueindex (PI), die Krevikularfiiissigkeit (CF) und den prozentualen Knochenverlust (BL) "Mittelwerte pro Proband. s.d. = Standarddeviation Valeurs de I'Indice Gingival (GI), de I'Indice de Plague (PI), du Fluide Creviculaire (CF) et de la Perte Osseuse en pourcentage (BL) *Valeurs moyennes par sujet. s.d. — ecart-type Variahle
n
* Minimum
^•Maximum
Mean
s.d.
GI PI CF (mtn)
50 50 50 50
0.33 0.18 0.09 3.89
2.90 2.60 8.!5 37.73
1.3 LI2
0.60 0.52 1.44 7.88
BL
Mean (Mitlelwert, moyenne)
1.73 13.71
KARDACHI, WOLFFE AND MANSON
254
(3) Plaque (PI). The amount of plaque was assessed using the Plaque Index system (Silness & Loe 1964). AU clinical measurements were carried out by one examiner (B.K.). The percentage of bone loss (BL) on the mesial and distal surfaces of the selected teeth Vk-as assessed as follows; long cone radiographs were taken using a distance of 21 cm from the focal spot to the tip of the cone. The films were held in Rinn Holders (Rinn XCP instruments for extension cone paralleling technique) and a Phillips Oralix Dental X-ray unit was used. Radio-
graphs were taken by two examiners (G.W./ B.K.) and were developed using standard automatic processing. The percentage bone loss was measured by one examiner (G.W.) on the mesial and distal surfaces of the selected teeth using the technique of Schei et al. (1959). Although radiographs have their limitations, Ramfjord (1974) suggests that the above method provides an accurate and reproducible method of assessing bone loss. Reprodu cib ility Intra-examiner reliability was assessed on 10
zs
0 0-5 10 1-5 £0 Z5 3O
0 06
GI Fig 1
1-0 1-5 2 0 25 3O
•5 3-0 4^5 6 0 75 9-0
PI
CF
0
r
(4
21 2a 35
BL
Distribution of Subjects within each index studied A - Gingival index (GI) B - Plaque index (PI) C - Crevicuiar fluid-mm of stained filter strip (CF) D - Percentage bone loss (BL)
Verteilung der Probanden innerhalb der registrierten Indizes. A - Gingivulindex (GI). B - Plaqueindex (PI). C - KrevikularflUssigkeit - mm gejdrbtes Filterpapier (CF). D - Knochenverlust in Prozent (BL). Distribution des sujets pour chague indice etudie. A Indice Gingival (GI). B - Indice de Plague (PI). C - Fluide Creviculaire - mm de coloration sur les bandelettes de papier filtre (CF). D Perte Osseuse en pourcentage (BL).
GINGIVAL INFLAMMATION AND BONE LOSS
subjects for both the clinical and radiographic measurements. Gingival Index and Plaque Index measurements were repeated after approximately 2 hours, whilst radiographic measurements were repeated after a 24-h interval. The reproducibility for Gingival Index was 80.8 %, for Plaque Index 77.5 % and for percentage of bone loss 86.3 %.
Results
Not all radiographs were readable. A total of 63 out of 600 surfaces (10.5 %) were unreadable due to overlap or inability to locate the cemento-enamel junction. The majority of unreadable areas were on the left upper
25S
first premolar due to difficulty with film placement because of palatal anatomy. The GI and PI scores and crevicular fluid (CF) values associated with these unreadable radiographs were not used in the result analysis. Table 1 gives the mean values with standard deviation for all the indices used; the mean for GI was 1.30; PI, 1.12; CF, 1.73. Histograms showing the distribution of each index in the sample studied are shown in Fig. 1 with the interval widths indicated. Fig. 2 shows the relationship for GI to PI, PI to BL (bone loss) and GI to BL (bone loss). Using coefficient of correlation analysis,
8L - 3Z * 91(Pn , =062
SL = 3 55 + B(Gn r = 062
20
BL Fig 2
BL
The correlation between the measured variables A = Ginqival index (GI) with Plaque index (PI) 8 = Plaque index with percentage Bone loss (BL) C = Gingivol index with percentage Bone lass
Der Zusammenhang zwischen den registrierien Variablen. A - zwischen Giiigivalindex (GI) und Plaqueindex (PI). B - zwischen Plaqueindex (PI) und Knochenverlust in Prozent (BL). C - zwischen Gingivalindex und Knochenverlust in Prozent. Correlation entre les variables mesurees. A - Indice Gingival (GI) et Indice de Plaque (PI). B Indice de Plaque el Perte Osseuse en pourcentage (BL). C - Indice Gingival et Perte Osseuse en pourcentage.
256
KARDACHI, WOLFFE AND MANSON
Table 2. Results and statistical analysis comparing Gingival Index (Gl), Plaque Index (PI) and Percentage Bone Loss (BL) in subjects less than 34 years of age with those 35 years or older s.d. = Standard Deviation. NS = Not Significant Resultat und statistische Analyse des Vergleiches zwischen Gingivalindizes (Gl). Plaqueindizes (PI) und dem prozentualen Knochenverlust (BL) bei Probanden die jUnger als 34 Jahre und Probanden die 35 Jahre und alter sind s.d. = Standardabweichung. NS = Nlcht slatistisch abgesichert Resultats el analyse statistique de la comparaison entre I'Jndice Gingival (Gl), I'lndice de Plaque (PI) et la Perte Osseuse en pourcentage (BL) chez les sujels de moins de 34 ans el chez ies sujels ages de 35 ans ou plus Variable Gl BL
Mean s.d. < 34 years
Mean s.d. > 35 years
Test used
Significance
1.14 ± 0.59 0.97 ± 0.50 11.69 ± 6.90
1.48 ± 0.58 1.29 ± 0.50 16.20 ± 8.4
Mann-Whitney U Mann-Whitney U Student's t
NS NS
