Prevalence and severity of periodontal disease in patients with inflammatory bowel disease

Thomas R Fergus Shanahan^ and Kenneth T. Miyasaki^ UCLA School of Dentistry, Sections of ^Orai Biology and ^Periodontics; ^UCLA School of Medicine, Section of Gastroenterology, Los Angeles, California 90024, USA

Flemmig TF, Shanahan F and Miyasaki KT: Prevalence and severity of periodontal disease in patients with inflammatory bowel disease. J Clin Periodontol 1991; 18: 690-697. Abstract. Previous reports have demonstrated that oral mucosa and periodontal lesions occur in patients suffering from inflammatory bowel disease (Crohn's disease [CD] and ulcerative colitis [UC]). It is unknown whether periodontal disease is an occasional or regular finding in these patients. The purpose of this study was to assess the prevalence and severity of periodontal disease in patients with inflammatory bowel disease (IBD). The periodontal status of 107 consecutive patients seeking treatment for inflammatory bowel disease was assessed. Examination of the mid- and mesiobuccal aspects of one quadrant on one jaw and the contralateral quadrant of the opposite jaw revealed that 93,5% of the CD patients and 95,1% of UC patients had at least one site with probing attachment loss of 2 mm or greater, and a mean probing attachment loss of 1,4 + 0.9 mm and 1.5+1,0 mm, respectively. We found that 28.3% of CD patients and 29.5% of UC patients possessed at least 1 site with a pocket probing depth of 4 mm or greater; the mean pocket probing depth in these patients was 2.4 + 0,2 mm and 2.3 + 0.2 mm, respectively. Compared with the assessment of Oral Health of United States Adults, IBD patients revealed a 11.9% higher prevalence (P1

Mean CI

+ SD

n

% Su w/ CI>1

Mean CI

+ SD

n

% Su w/ CI>1

Mean CI

+ SD

15-29 30-39 40-49 50-82

12 12 13 9

16,7 41,7 46,2 33,3

0,12 0,48 0,31 0,5

0,15 0,46 0,27 0,44

17 18 9 17

17,6 38,9 44,4 52,9

0,18 0.34 0,24 0,36

0,24 0,36 0,23 0,44

29 30 22 26

17,2 40 45,5 46.2

0,16 0,39 0.28 0,41

0,2 0,4 0,25 0,43

Total IBD

46

34,8

0,32

0,35

61

37,7

0,31

0,35

107

36,5

0,31

0.35

Table 3. Age and gingival index (GI) in IBD subjects; % of subjects with at least 1 site with G I > 2 and mean GI per subject Crohn's disease Age group (years)

n

Total IBD

% Su w/ GI>2

Mean GI

±SD

n

% Su w/ GI>2

Mean GI

±SD

0,31 0,39 0,47 0,56

0,18 0,37 0,21 0,3

17 18 9 17

29,4 33.3 0 17.7

0,3 0,32 0.27 0.53

0,43

0,26

61

23

0.37

15-29 30-39 40-49 50-82

12 9

25, 50 38.5 55.6

Total IBD

46

41.3

n'

Ulcerative colitis n

% Su w/ GI>2

Mean GI

+ SD

0.22 0,19 0,25 0,17

29 30 22 26

11.6 40 22,7 30,8

0,31 0,34 0,39 0,54

0.2 0.27 0,24 0.22

0,24

107

30.8

0,39

0.25

692

Flemmig et al.

. • "- '

Table 4. Age and bleeding on probing (BOP) in IBD subjects; % of subjects with at least 1 site with BOP and mean % of sites per subject with BOP Total IBD Ulcerative colitis Crohn 's disease Mean % Sites w/ Mean % Sites w/ Mean % Sites w/ % Su w/ % Su w/ % Su w/ Age group ±SD BOP BOP n ±SD BOP BOP n + SD BOP n BOP (years) 34.5 2,51 5,62 29 7.02 3.43 41.2 17 2.35 1.21 25 12 15-29 30 3.76 9.65 30 4.01 2.23 27.8 18 14.53 6.07 33.3 12 30-39 27,3 2.35 4.51 22 5,2 2.51 22.2 9 4.19 2.24 30.8 13 40-49 .?....:. 53.9 5.85 8,24 26 6.64 4.87 58.8 17 10.87 1.1 44,4 9 50-82 • 36.5 3.64 7.47 107 5.85 3.32 39.3 61 9.25 4.04 34.1 46 Total IBD

Table 5. Age and probing attachment loss (PAL) in IBD subjects; mean % of sites per subject available for examination and % of subjects with at least 1 site with PAL > 2 mm Total IBD Ulcerative colitis Crohn 's disease Mean % Sites Mean % Sites Mean % Sites % Su w/ % Su w/ % Su w/ Age group PAL>2 examined + SD n PAL>2 examined + SD n PAL>2 examined + SD n (years) 97.54 5.15 86.2 29 3.78 98.74 88.2 17 6.43 95.83 83.3 12 15-29 6.68 95.95 93.3 30 4.9 97.62 94.4 18 8.32 93,45 91.7 12 30-39 17.66 100 87.66 22 7.99 95.24 100 9 20.75 82.42 100 13 40^9 21.68 100 81.59 26 22.41 80.67 100 17 21,43 83.33 100 9 50-82 15.31 91.19 94.4 107 14.46 92.86 95.1 61 16.13 88.98 93,5 46 Total IBD

per patient with PAL greater or equal to 2 mm. For all assessments the patient was used as the statistical unit. For comparison, the data of the latest assessment of the Oral Health of United States Adults (U.S. DHHS 1987) were age adjusted to the age groups of this study. Statistical analysis was performed using a two tailed one sample ttest for averages and a two tailed one sample z-test for proportions.

creased from 44.8% to 73.1% and the mean plaque index from 0.4 + 0.5 to 0.6 + 0.4 (Table 1). Supragingival calculus of at least 1

mm width was found in 34,8% of the CD patients and 37.7% of the UC patients with a mean calculus index of 0.3 + 0.4 and 0.3 + 0.4 respectively. Both

Results Demographics

A total of 107 patients with a mean age of 40.5 + 14.2 years were examined (Table 1). Among these were 58 males and 49 females. 46 of the patients suffered from Crohn's disease and 61 from ulcerative colitis. The sex distribution of CD patients was 56.5% male and 43.5% female and of UC patients 52.5% and 47.5%, respectively. The consecutive sampling resulted in a relatively even sex and IBD distribution.

I

Oral hygiene

63% of CD patients and 59.0% of UC patients had visible supragingival plaque in at least 1 site and a mean plaque index of 0.5 + 0.5 and 0.4±0.4, respectively. With increasing age the prevalence of plaque of all patients in-

Fig. 1. % of IBD subjects with at least 1 site with probing attachment loss (PAL) equal to or greater than indicated PAL (mm).

Periodontal disease and IBD

693

Table 6. Age and probing attachment loss (PAL) in IBD subjects; mean % of sites per subject with PAL>2 mm and mean PAL (mm) per subject ^ Crohn's disease

Ulcerative colitis

Age group (years)

n

Mean % Sites w/ Mean PAL>2 + SD PAL + SD

15-29 30-39 40-49 50-82

12 12 13 9

18,2 22,7 0,98 28,04 29,4 31,73 18,73 62,65 33,12

Total IBD

46

33,29

29,44

n

Total IBD

Mean % Sites w/ Mean PAL>2 + SD PAL + SD

n

Mean % Sites w/ Mean PAL>2 + SD PAL

+ SD

0,55 1,19 1,33 2,24

17 0,88 0,48 1,04

19,75 18 9 17

14,61 31,61 48,69 55,3

1 26,06 22,79 25,51

0,38 1,23 1,75 2,24

29 0,73 0,79 1,19

19,11 30 22 26

18,03 30,18 38,67 57,84

0,99 27 21,7 27,78

0,45 1,21 1,5 2,24

0,78 0,65 1,12

1,38

0,85

61

37,43

26,4

1,52

0,95

107

35,65

27,69

1,46

0,91

Table 7. Age and probing attachment loss (PAL) in IBD subjects with at least 1 site with PAL>2 mm; mean % of sites per subject with PAL > 2 mm and mean PAL (mm) per subject Crohn's disease

Ulcerative cohtis

Mean % Sites w/ Mean PAL>2 + SD PAL + SD

Total IBD

Age group (years)

n

15-29 30-39 40-49 50-82

12 12 13 9

21,85 30,58 31,76 62,65

23,27 29,41 18,73 33,12

1,09 1,25 1,33 2,24

0,53 0,89 0,48 1,04

17 18 9 17

22,39 33,47 48,69 55,3

13,45 25,6 22,79 25,25

1,08 1,27 1,75 2,24

0,34 0,73 0,79 1,19

29 30 22 26

22,17 33 38,67 57,84

17,57 26,93 21,7 27,78

1,08 1,28 1,5 2,24

0,42 0,79 0,65 1,12

Total IBD

46

35,61

29,05

1,45

0,84

61

39,36

25,61

1,58

0,95

107

37,77

27,05

1,52

0,9

the prevalence of calculus and the mean calculus index increased with increasing patient age (Table 2), Gingivitis

n

Mean % Sites w/ Mean PAL>2 + SD PAL + SD

88,9+16,1% for CD patients and 92,9 ±14,5% for UC patients. There was a negative correlation between age and available sites in all groups (Table 5), The mean probing attachment loss was 1,4 + 0,9 mm for CD patients and

n

Mean % Sites w/ Mean PAL>2 + SD PAL

+ SD

1,5+1,0 mm for UC patients, with an average of 1,5 + 0,9 mm for all groups combined (Table 6), Both mean probing attachment loss and mean percent of sites affected was shghtly higher in patients with at least on sites of attach-

Marginal gingival bleeding (gingival index > 2) in at least one site occurred in 41,3% of the CD patients and 23,0% of the UC patients. The incidence of marginal gingival bleeding and the mean gingival index was greater in CD patients over 30 years compared to UC patients of the same age group. No constant relationship was found between marginal gingival bleeding and age nor between mean gingival index and age (Tabib 3), Bleeding on probing occurred in 37,0% of CD patients and in 36,1% of UC patients. The highest incidence of bleeding on probing was found in the 50-82 year old population (Table 4),

Periodontitis

Most of the subjects examined, including 93,5% of the CD patients and 95.1% of the UC patients, had at least one site where the probing attachment loss was 2 mm or greater (Table 5), A smaller proportion of all patients, 13,1 %, had at least one site with attachment loss of 6 mm or greater (Fig, 1), The mean % of sites available for measurement of probing attachment loss was

Fig. 2. Mean % of sites per IBD subject with indicated probing attachment loss (PAL) (mm).

694

Flemmig et al.

Table 8. Age and pocket probing depth (PPD) in IBD subjects; % of subjects with at least 1 site with PPD> mm and mean % of sites per subject with PPD > 4 mm Crohn 's disease Age group (years)

n

% Su w/ PPD>4

15-29 30-39 40-49 50-82

12 12 13 9

25 41,7 0 55,6

1,89 3,91 0 5,15

Total IBD

46

28,3

2,52

Ulcerative colitis

Mean % Sites w/ PPD>4 + SD

ment loss than the whole sample population (Table 7), The prevalence of probing attachment loss of 2 mm or greater, mean probing attachment loss and mean percentage of affected sites increased with age in all groups (Tables 6, 7), Most of the attachment loss was found to be in the 1 to 3 mm range (Fig. 2). • At least I site with a pocket probing depth of 4 mm or greater was observed in 28.3% of CD patients and 29.5% of UC patients,, 3.7% of all patients had pocket depths of 6 mm, and none had pockets deeper than this (Table 8, Fig. 3). An average of 2.5 ±4.6% of the sites in CD patients and 2.5 + 4.8 in UC patients were affected (Table 8). The mean pocket probing depth was 2.4 + 0.2 mm

n

% Su w/ PPD>4

3,42 5,42 0 6,47

17 18 9 17

29,4 22,2 44,4 29,4

2,12 1,69 4.46 2,82

4.62

61

29,5

2.53

Total IBD

Mean % Sites w/ PPD>4 + SD

n

% Su w/ PPD>4

4,21 3,8 6,5 5,21

29 30 22 26

27,6 30 18,2 38,5

2,02 2.58 1.83 3,63

3.84 4.56 4,6 5,66

4,75

107

29

2.53

4.67

and 2.3 ±0.2 mm for CD and UC patients, respectively. Sites with recession of at least 1 mm occurred in 54,4% of CD patients and 49.2% of UC patients with an average of 14.3 ±20.8% and 10.4±17.9% of the sites affected, respectively. There was a positive correlation between the prevalence of sites exhibiting recession with increasing age (Table 9). Soft tissue

The soft tissue alterations found in all patients are listed in Table 10. Most remarkable were two cases, one with localized, atypical gingivitis (Fig. 4) and another with localized gingival hyperplasia (Fig. 5).

Mean % Sites w/ PPD>4 + SD

Oral health of IBD subjects versus oral health of US adults

Bleeding on probing was found in 6.6% less IBD subjects compared to the Oral Health of US Adults (US DHHS 1987). On the average, IBD subjects had 2.2% less sites that bled on probing (P < 0.01). The proportion of IBD subjects who had at least one site with pocket probing depth of 4 mm or more, was significantly (P4 GR>1 GR>1 27.6** 30* 18.2 38.5*

24.1 43.3 54.6 88,5

3.39 8.02 10.85* 27.4

Mean % % Su w/ Sites w/ BOP BOP 46.76 42.75 41.7 40.7

5.88 5.57 5.73 6,18

% Su w/ % Su w/ Sites w/ GR>1 PPD>4 GR>1 8.61 15.24 18.65 19.37

27,78 51.42 64.62 81.97 55,15

2.5 6.82 14.37 25.59 11,76

15,15 5.84 43.12 12,06 51,4 29** 3.64** 36.5 107 Total IBD Standard deviations of IBD subject data are depicted in Tables 4, 8 and 9. * Statistically significant different to US adults at P2 mm US Total IBD Mean % % Su w/ Sites w/ PAL>2 PAL>2

Age group (years) 15-29 30-39 40-49 50-82 Total IBD

Mean PAL

Mean % Sites w/ PAL>2

Mean PAL

Su with PAL>2

All Su

Su with PAL>2

All Su

Mean % % Su w/ Sites w/ PAL>2 PAL>2

Mean PAL

Mean % Sites w/ PAL>2

29 30 22 26

86.2** 93,3* 100* 100

19.11* 30,18* 38.67* 57,84**

0,99** 1,21** 1.5** 2,24**

22.17 33 38.67 57.84*

1,08** 1.28** 1 5** 2.24**

63.12 78.24 84,3 93

11.11 18.9 27.74 39,97

1.39 1.91 2.21 2.71

17.41 24.13 32.83 42.99

107

94,4**

35.65**

1,46**

37.77**

1,52**

78.97

23.72

2,03

28.68

Standard deviations of IBD subject data are depicted in Tables 5, 6 and 7. ** Statistically highly significant different to US adults at /'

Prevalence and severity of periodontal disease in patients with inflammatory bowel disease.

Previous reports have demonstrated that oral mucosa and periodontal lesions occur in patients suffering from inflammatory bowel disease (Crohn's disea...
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