Increased prevalence of dental caries and poor oral hygiene in juvenile idiopathic arthritis

R. R. Welbury, J. M. Thomason1, J. L. Fitzgerald1, I. N. Steen3, N. J. Marshall2 and H. E. Foster2

Glasgow Dental Hospital and School, University of Glasgow and North Glasgow NHS Trust, Glasgow, 1School of Dental Sciences, Statistics and 2Child Health and Rheumatology, 3Department of Statistics, University of Newcastle upon Tyne and Newcastle upon Tyne Hospitals NHS Trust, Newcastle upon Tyne, UK

Correspondence to: R. Welbury, Department of Paediatric Dentistry, Glasgow Dental Hospital and School, 378 Sauchiehall Street, Glasgow G2 3JZ, UK. E-mail: r.welbury{at}dental.gla.ac.uk

Abstract

Objectives. Recent decades have seen a trend to treat juvenile idiopathic arthritis (JIA) with increasing immunosuppression to improve the long-term outcome. Poor oral hygiene and dental decay cause significant morbidity, and patients with chronic disease (who may be further immunocompromised by treatment) are at greater risk. This study investigated patients with JIA using standard measures of oral health.

Methods. One hundred and forty-nine patients with JIA were included. The children were attending a regional paediatric rheumatology service and the adults were attending an adult rheumatology clinic. Random age- and sex-matched healthy controls were recruited from a dental teaching hospital. The structured dental examination included standard epidemiological indices of oral hygiene (gingival index, plaque index, oral cleanliness index) and dental decay [DMFT (decayed, missing or filled teeth) index].

Results. JIA patients, at all ages, had increased levels of dental decay and poor oral hygiene. This increased level of decay was statistically significant in the patients aged 0–11 yr. Significant levels of untreated caries and increased levels of missing teeth were found in JIA, suggesting that patients with JIA had less restorative dental treatment, with tooth extraction often the chosen option for the treatment of dental decay.

Conclusions. This is the largest study of oral health in JIA and is cross-sectional with non-diseased controls. It shows significantly increased levels of poor oral hygiene and dental decay in patients with JIA. The high levels of untreated dental decay suggest barriers to dental care. These results emphasize the role of regular dental care in the multidisciplinary management of JIA.

KEY WORDS: Juvenile arthritis, Juvenile idiopathic arthritis, Dental decay, Caries, Oral cleanliness, Outcome, Complications.

Juvenile arthritis is a heterogeneous group of diseases of unknown aetiology, many of which are clinically and genetically distinct from chronic arthritis in adults. ‘Juvenile idiopathic arthritis’ (JIA) is the new term that replaces the previous terms ‘juvenile chronic arthritis’ and ‘juvenile rheumatoid arthritis’. This new classification, which is predominantly clinical, aims to facilitate research and further our knowledge and understanding of biologically significant and clinically homogeneous disease entities [1].

JIA is a clinically diverse spectrum of diseases and many children will have spontaneous remission. However, at least one-third have either ongoing active disease into adult years or will have significant morbidity from sequelae of previous inflammation, which includes joint damage that may require joint replacement surgery, visual loss from uveitis, osteoporosis or psychosocial morbidity, including unemployment despite good educational achievement. With increasing evidence that joint damage can occur early in the disease course, that early use of methotrexate reduces joint damage, and that the long-term outcome for some patients can be poor, there has been a trend towards earlier and more aggressive intervention [2] with intra-articular steroid injections, methotrexate, and for patients with refractory disease there are increasing options with biological therapies and autologous stem-cell rescue following T-cell immunosuppression [3, 4].

Theoretically, there is a significant risk to oral health in patients with JIA for several reasons. These include the involvement of the temporomandibular joint (TMJ), the effect of JIA on mandibular growth and masticatory function, upper limb functional disability affecting toothbrushing, sugar-containing oral medication and barriers to dental care [5]. Poor oral health is important because untreated dental disease and poor gingival health may combine to produce an oral infection which will be a significant risk factor for systemic infection, especially when the patient is immunosuppressed through the use of corticosteroids and disease-modifying anti-rheumatic drugs (DMARDs), such as methotrexate. TMJ involvement in JIA is well described [68], but there are very few reports of the effects of JIA or its treatment on the teeth and periodontal tissues. Dental caries in children with JIA is reported (Table 1) [912], but these few studies often included only small numbers of patients. Two studies did include controls, but different methods were used which do not reflect current dental epidemiological practice. The gingival health of children with JIA has been shown to be worse than that of controls in a study of 16 patients [11]. Periodontal health in children has not been addressed, but a study of 16 adults with rheumatoid arthritis showed no significant difference from controls [13].


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TABLE 1. Summary of published studies of dental caries in children with JIA

 
The aim of this study was to establish whether oral health is compromised in patients with JIA, using standardized and validated measures of oral health status.

Methods

Patients were recruited from the paediatric rheumatology clinics in Newcastle upon Tyne (UK) and neighbouring hospitals. Adult patients (aged >16 yr) with a previous diagnosis of JIA were recruited from adult rheumatology clinics. Healthy controls, matched for age (within 1 calendar year) and sex, were identified from the dental hospital database and were recruited when attending for routine care. Only control subjects with no medical or behaviour management problems were included in the study. Ethical approval was granted by the local ethics committee and written consent was obtained from each patient and control or their parent or guardian. The dental assessment included clinical examination of teeth for dental decay and the gingival tissues for oral hygiene. The dental examiner (JLF) underwent inter-examiner calibration training [British Association for the Study of Community Dentistry (BASCD)] for decay and oral hygiene indices ({kappa} score 0.92).

Most subjects were examined in a dental surgery under standard dental lighting using plain mouth mirrors and a ball-ended periodontal probe. When examining patients in a medical examination room, a portable Daray dental light was used. The surfaces of all erupted teeth were assessed using the dmft/DMFT (decayed, missing or filled teeth; lower-case letters for primary teeth, upper-case for permanent teeth) index and the BASCD standardized criteria [14] (Table 2). The teeth were not brushed prior to the examination but any obvious food debris was removed with a probe or cotton wool. No air was used to dry the teeth. The teeth were examined from the upper left to the upper right and from the lower left to the lower right. The surface status of each tooth was recorded. Diagnosis of a carious lesion was on a clinical (visual) basis and radiographs were not performed in any part of the study. For the analysis of the findings for dental decay, the subjects were considered to reflect the developmental stages of the dentition in five age bands: primary teeth (0–5 yr); the primary teeth, including the time in the mixed dentition (0–11 yr); the young permanent teeth in the mixed dentition (6–11 yr); the young permanent dentition (12–17 yr); and the mature permanent dentition (>=18 yr).


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TABLE 2. A summary of surface coding for the diagnosis of dental caries

 
Oral hygiene was assessed with three standard epidemiological indices. The gingival index [15] is scored as follows: 1 = normal gingiva, no inflammation discoloration or bleeding; 2 = mild inflammation, slight colour change, mild alteration of gingival surface, no bleeding on pressure; 3 = moderate inflammation, erythema and swelling, bleeding on pressure; 4 = severe inflammation, erythema and swelling, tendency to spontaneous bleeding, perhaps ulceration. The plaque index [16] is scored as follows: 0 = no plaque; 1 = tooth appears clean but plaque may be removed from its gingival third with a probe; 2 = moderate accumulation of plaque deposits visible to the naked eye; 3 = heavy accumulation of soft material filling the niche between the gingival margin and tooth surface. The oral cleanliness index [17] is scored as follows: 0 = more than two-thirds of the surface covered with plaque; 2 = between one-third and two-thirds of the surface covered with plaque; 4 = less than one-third of the surface covered with plaque; 6 = thin continuous band of plaque at the gingival margin; 8 = intermittent/sporadic areas of plaque at the gingival margin; 10 = no plaque. In order to facilitate compliance and avoid complication in the mixed dentition, six teeth were identified as index teeth in each patient. Separate recordings were made for the four smooth surfaces of these teeth and an average tooth score was then recorded. The oral hygiene indices of the study group were considered in three age bands: 0–11 yr, representing the full primary and the mixed dentition stage; 12–17 yr, representing the young permanent dentition; and >=18 yr, representing the mature permanent dentition.

Statistics
Individual patient data, including demographic and dmft/DMFT variables, were collected and transcribed onto a statistical database [18]. All data were carefully examined for the presence of obvious outliers caused by typing or transcription errors, and these were corrected. All statistical analysis was undertaken using a commercially available software package [18]. The continuous data sets were examined for normality using simple histogram plots. The mean and standard deviation were calculated as summary statistics for all variables (but when examining these statistics for non-normal data one should not assume that 95% of the data will fall within two standard deviations of the mean). Cases were compared with their matched controls, but as the correlation between paired observations was extremely low the comparisons were made using independent sample t-tests. The results are reported in the form of P-values and 95% confidence intervals. Significance was accepted at the 5% level.

Results

Patients
The study included 149 patients (107 females) with a median age of 17.9 yr (range 2–50 yr) and median disease duration of 10.8 yr (range 1–42 yr). A spectrum of JIA subtypes was seen, which included oligo-articular onset (n = 65, including 20 with extended course), polyarticular onset (n = 49, including 14 who were rheumatoid factor positive), systemic onset (n = 33), psoriatic arthritis (n = 13) and enthesitis-related arthritis (n = 11).

Decayed, missing and filled teeth
The results for decayed, missing or filled primary teeth (dmft) and permanent teeth (DMFT) for each of the age bands are shown as means and standard deviations in Table 3. Disease in the primary dentition was looked at in the 0–11 yr age group and in a 0–5 yr subset. In this latter subset the subject group would only have primary teeth, whereas in the 0–11 yr group the older subjects would also have some permanent teeth. The dmft for the patients aged 0–11 yr (1.46 ± 2.58) was significantly greater than that for the controls (0.56 ± 0.96) (P = 0.027). This difference comprised an increased frequency of both decayed (P = 0.008) and missing teeth (P = 0.004) and a trend towards a smaller number of filled teeth (0.23 ± 0.58) than in the control group (0.44 ± 0.87). No differences were seen between subjects and controls in the 0–5 yr subgroup but the group is probably too small (n = 12) to draw any meaningful conclusion. However, it is probable that as the majority of JIA is diagnosed either around or after the age of 5 yr the disease or its treatment is unlikely to result in any significant change in the amount of decay prior to this.


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TABLE 3. Components of dmft/DMFT

 
Permanent teeth were examined in three age groups: 6–11 yr, comprising patients with permanent teeth but who would also be expected to have some remaining primary teeth; 12–17 yr, the young permanent dentition; and >=18 yr, the mature permanent dentition. There was no difference between the study groups and controls for the DMFT when considered in this form. Nevertheless, in both the young permanent (12–17 yr) and the mature permanent group (>=18 yr), significantly more decay was found in the study groups (P = 0.03 and 0.002 respectively). In addition, there was a trend in both groups for there to be a greater number of missing teeth (reaching borderline significance) and a smaller number of filled teeth. We are therefore seeing more untreated decay, and this is perhaps associated with more missing teeth and fewer filled teeth in the study groups.

Periodontal parameters and hygiene
Assessment of gingival inflammation and oral hygiene, as measured by the gingival index, plaque index and the oral cleanliness index (Table 4), showed that the study groups had more gingival inflammation (P < 0.0001), more dental plaque (P < 0.0001) and poorer oral cleanliness (P < 0.0001) in each age band.


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TABLE 4. Periodontal indices (mean ± S.D.)

 

Discussion

This is the largest study of oral health in JIA to date, in a patient population with a spectrum of JIA subtypes such as may be expected in a regional paediatric rheumatology service [19]. This study shows a significant prevalence of poor oral health in patients with JIA compared with age- and sex-matched non-diseased controls.

An increased frequency of decayed teeth in the mouth was seen for all the major age bands (0–11, 12–17 and >=18 yr). In the 0–11 yr group this comprised an increased frequency of both decayed and missing teeth and a trend towards smaller numbers of filled teeth compared with the control group. This general pattern was maintained throughout the other age bands, although not always reaching significance. Study patients therefore have more untreated decay, and this is perhaps associated with more missing teeth and fewer filled teeth than in controls. These results suggest that study patients are more prone to dental decay (although this is not always shown in terms of the dmft or the DMFT) or that there may be barriers to dental care for JIA patients. Barriers to care could be categorized into patient and dentist factors. Patient factors could include a perceived lower priority for dental attendance in the study group compared with medical appointments, anxiety as a result of experience of painful procedures during their medical care, and reduced mouth opening due to TMJ disease making personal oral hygiene difficult. Unfortunately, the study did not allow an investigation into the dental attendance or registration for dental treatment of the JIA subjects, and therefore there is no firm evidence to support the suggestion that they may not be attending for dental care as frequently as controls. Dentist factors could include a delay of treatment intervention for carious lesions, either because of reduced intra-oral access due to TMJ disease or lack of knowledge of the disease process itself and the drugs used to treat it. Steroid and/or antibiotic cover may be needed for those at risk of adrenal crisis and infective endocarditis. However, it is clear that by the time a number of the study group are obtaining intervention for their dental decay the prognosis for the affected teeth is poorer and extraction is more common than in the control group.

The oral hygiene in the study groups at all ages was much poorer than that in the controls (Table 4) and may reflect either poorer access to the mouth due to restricted opening or poorer manual dexterity with the brush due to upper limb disability [10, 20, 28]. The latter will be more severe if it is the dominant hand that is predominantly affected. Alternatively, if chewing is painful due to TMJ disease, harder foods may be replaced by softer foods [21], and these may be more difficult to remove with the toothbrush.

The increased prevalence of dental caries in JIA is likely to be multifactorial [20], although the relative effects of different factors have not been elucidated. Risk factors relevant to dental caries include fluoride intake, diet, medicines and poor oral hygiene. Newcastle upon Tyne has had a fluoridated water supply for over 20 yr and is part of only 11% of the UK with this benefit. Fluoride incorporated into the developing and erupted tooth gives it significant resistance to decay. The study population of JIA patients was drawn from geographical areas of the northern region that were both within and without the fluoridated water area. Initially it was thought that this might create a bias, as the controls who were attending the dental hospital for routine care would be more likely to live within the fluoridated water area. However, this was not a practical concern because a similar number of controls came from without the fluoridated water area but travelled to Newcastle for their treatment. Full analysis of fluoride exposure during life would have required information such as lifetime areas of residency and lifetime information on toothpaste type and usage, and fluoride supplementation. Clearly this was impossible to obtain. There is some evidence that children with JIA often have small, frequent meals and hence their exposure to sugar is more frequent [21]. In addition, children with debilitating illness are often consoled with sweets [20]. The long-term use of sugar-containing liquid medicines may increase the caries rate [5, 2225], and the effect may be greater if they are taken at night or at bedtime when the protective buffering and cleansing effects of saliva are reduced as the salivary flow is less. The commonly used syrups (ibuprofen, naproxen, paracetamol) are often sugar-based [26] and contain a high percentage of sugar (10–80%) [27]. These medicines are given several times per day, and often at night, and may therefore increase the risk of dental caries.

The control group was drawn from medically fit and well patients attending for routine patient care at the dental hospital on the student teaching clinics. In other words, they were using the dental hospital as their general dental practice. The ideal would have been to recruit patients attending general dental practice, but this was impractical as it would have required electronic liaison between a significant number of practices and the dental hospital to recruit the requisite numbers. After recruitment, an investigator would have needed to travel to the practice or the patient would have needed to travel to the dental hospital. The question of having another medical group as controls was also considered but was logistically impractical, given the funding and time-scale of the project.

This research demonstrates that there is a detrimental effect of JIA on oral health. The effect is probably multifactorial and will include (apart from those factors already mentioned) biochemical abnormalities and the medications used to treat JIA. There has been no research into the relative importances of all the potential factors and the interplay between them; furthermore, barriers to dental care (e.g. knowledge, fear and access to dental care) have not been explored. Not all children with JIA will have oral health problems, and research is needed to identify children who are at risk in order to propose interventional strategies that may be both effective and cost-effective. Poor oral health is a risk factor for systemic infection, especially when the patient is immunosuppressed through the use of corticosteroids or DMARDs. Good oral health is therefore important in order to minimize complications of JIA and its treatment and to reduce the morbidity of caries and gingival disease.

Dental care and supervision is not routinely provided as part of the JIA multidisciplinary team. However, this research shows that there is a clear role for a paediatric dentist and hygienist. Advice to all patients, families and health professionals involved in the care of patients with JIA should include the following.

Regular dental examination, advice and early intervention where necessary.

Toothbrushing technique and plaque control. An electric toothbrush or a modified handle in a manual brush may be very helpful in patients with reduced manual dexterity.

Prescription of appropriate systemic and topical fluoride supplements.

Dietary intervention and prescription of sugar-free medicines.

Fissure sealant placement on occlusal surfaces of primary and permanent molars.

Early liaison with orthodontic colleagues if TMJ disease is clinically suspected. The use of regular daily exercises has been proposed to improve the range of movement of the TMJs and hence facilitate oral hygiene maintenance. The conventional treatment strategy for TMJ disease was to postpone any orthodontic therapy and any orthognathic surgical treatment until growth had ceased. However, current opinion favours early treatment, often with functional appliances during the pubertal growth spurt in an attempt to try to maintain occlusal stability and increase the function of the joint with the aim of allowing continuous uninhibited growth of the mandible [2830].

Good oral health is important in the reduction of the morbidity of caries and gingival disease. This study has shown that poor oral health is a significant problem in many patients with JIA. The outcome of JIA is varied, and there is considerable morbidity in many patients; to this list of complications can be added the risk of poor oral health. However, not all children with JIA have poor oral hygiene and increased caries. Research is needed to identify those children who are at particularly high risk, and to investigate the efficacy and cost-effectiveness of interventional strategies that are likely to be well received by patients and their families.

Acknowledgments

We acknowledge access to the patients of Dr F. Clarke (South Cleveland Hospital), Dr W. Hassan and Dr L. Kidd (Sunderland Royal Infirmary). We also acknowledge the considerable logistical help and advice of Sue Stephenson and Julie Wallis and the patience of our patients and their families. This work was supported by an Arthritis Research Campaign (ARC) project grant F0524.
Key messages:

Patients with JIA have more teeth extracted, more untreated caries and poorer oral hygiene.

There are barriers to dental care for for JIA patients which make prevention a priority

 

Conflict of interest

The authors have declared no conflicts of interest.

References

  1. Petty RE, Southwood TR, Baum J et al. Revision of the proposed classification criteria for juvenile idiopathic arthritis: Durban, 1997. J Rheumatol 1998;25:1991–4.[Medline]
  2. Wallace CA. The use of methotrexate in childhood rheumatic diseases. Arthritis Rheum 1998;41:381–9.[CrossRef][ISI][Medline]
  3. Lovell DJ, Giannini EH, Rieff A et al. Etanercept in children with polyarticular juvenile rheumatoid arthritis. N Engl J Med 2000;342:763–9.[Abstract/Free Full Text]
  4. Wulfraat N, van Royen A, Bierings M, Vossen J, Kuis W. Autologous haematopoietic stem cell transplantation in four patients with juvenile chronic arthritis. Lancet 1999;353:550–3.[CrossRef][ISI][Medline]
  5. Walton AG, Welbury RR, Thomason JM, Foster HE. Oral health and juvenile idiopathic arthritis: a review. Clin Rheumatol 2000;39:550–5.[CrossRef]
  6. Kjellberg H, Fasth A, Kiliaridis S, Wenneberg B, Thilander B. Craniofacial structure in children with juvenile rheumatoid arthritis (JCA) compared with healthy children with ideal or postnormal occlusion. Am J Orthod Dentofacial Orthop 1995;107:67–78.[ISI][Medline]
  7. Marini I, Vecchiet F, Spiazzi L, Capurso U. Stomatognathic function in juvenile rheumatoid arthritis and in developmental open bite subjects. ASDC J Dent Child 1999;66:30–4.[ISI][Medline]
  8. Stabrun AE, Larheim TA, Hoyeraal HM, Rosler M. Reduced mandibular dimensions and asymmetry in juvenile rheumatoid arthritis. Pathogenic factors. Arthritis Rheum 1988;31:602–11.[ISI][Medline]
  9. Storhaug K. Dental health problems in juvenile chronic arthritis. EULAR Bull 1977;3:88–92.
  10. Zifer SA, Sams DR, Potter BJ. Clinical and radiographical evaluation of juvenile rheumatoid arthritis: report of a case. Special Care Dent 1994;14:208–10.
  11. Siamopoulou A, Mavridis AK, Vasakos S, Benecos P, Tzioufas AG, Andronopoulos AP. Sialochemistry in juvenile chronic arthritis. Br J Rheumatol 1989;28:383–5.[ISI][Medline]
  12. Drecka-Kuzan K. Comparative survey on the incidence of dental caries in children with rheumatoid fever and rheumatoid arthritis. Rheumatologia 1971;9:125–33.
  13. Blair GS, Chalmers IM. The dental status of a chronically disabled section of the community: A study of 139 patients suffering from rheumatic diseases. SADJ 1976;31:329–36.
  14. Mitropoulos C, Pitts NB, Deery C. British Association for the Study of Community Dentistry criteria for the standardised assessment of dental health. Dundee: University of Dundee. BASCOD Trainers Pack for Caries Prevalence, 1992.
  15. Loe H, Silness J. Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol Scand 1963;21:533–51.
  16. Silness J, Loe H. Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand 1964;22:121–35.
  17. Turesky S, Gilmore ND, Glickman I. Reduced plaque formation by the chloromethyl analogue of vitamin C. J Periodontol 1970;41:41–3.[ISI][Medline]
  18. Minitab Statistical Software. Minitab Release 13.3. Minitab Inc., PA, USA, 1993.
  19. British Paediatric Association. Paediatric rheumatology. Report of a working party. British Paediatric Association, London, UK, 1994.
  20. Tanchyk AP. Dental considerations for the patient with juvenile rheumatoid arthritis. Gen Dent 1991;39:330–2.[Medline]
  21. Moynihan PJ, Welbury RR, Foster HE, Thomason JM, Kerber M. Is juvenile idiopathic arthritis associated with dietary practices which increase the risk of caries? EULAR Congress 1999. Ann Rheum Dis 1999;6:356.
  22. Roberts IF, Roberts GJ. Dental disease in chronically sick children. ASDC J Dent Child 1981;48:346–51.[ISI][Medline]
  23. Hobson P. Sugar based medicines and dental disease. Community Dent Health 1985;2:57–62.[Medline]
  24. Shaw L, Glenwright HD. The role of medications in dental caries formation: need for sugar free medications for children [review]. Paediatrician 1989;2:57–62.
  25. Walton AG, Foster HE, Welbury RR, Thomason JM. Juvenile idiopathic arthritis, dental caries, and long term liquid oral medicines. Int J Paediatr Dent 1999;9:55.
  26. Maguire A, Rugg-Gunn AJ. Consumption of prescribed and over the counter (OTC) liquid oral medicines (LOM’s) in Great Britain and the northern region of England with special regard to sugar content. Public Health 1994;108:121–30.[ISI][Medline]
  27. Newbrun E. The potential role of alternative sweeteners in caries prevention. Israeli J Dent Sci 1990;2:200–213.
  28. Pederson TK, Gronhoj J, Melsen B, Herlin T. Condylar condition and mandibular growth during early functional treatment of children with juvenile chronic arthritis. Eur J Orthod 1995;17:385–94.[ISI][Medline]
  29. Pearson MH, Ronning O. Lesions of the mandibular condyle in juvenile chronic arthritis. Br J Orthod 1996;23:49–56.[Abstract]
  30. Grosfield O. The orthodontist in the team treatment for children with rheumatoid arthritis. Eur J Orthod 1989;11:120–4.[ISI][Medline]
Submitted 17 January 2003; Accepted 31 March 2003