Published online January 28, 2008
PEDIATRICS Vol. 121 No. 2 February 2008, pp. e299-e306 (doi:10.1542/10.1542/peds.2007-0291)
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ARTICLE

Incidence and Characteristics of Arthritis in Norwegian Children: A Population-Based Study

Øystein Rolandsen Riise, MD, MPHa,b, Kai Samson Handeland, MDa, Milada Cvancarova, MScc, Karl-Olaf Wathne, MD, PhDb, Britt Nakstad, MD, PhDd,e, Tore Gunnar Abrahamsen, MD, PhDf, Eva Kirkhus, MDg and Berit Flatø, MD, PhDa

a Departments of Rheumatology
c Biostatistics
g Radiology, Rikshospitalet Medical Centre, Oslo, Norway
b Department of Pediatrics, Ullevål University Hospital, Oslo, Norway
d Department of Pediatrics, Akershus University Hospital, Nordbyhagen, Norway
e Akershus Faculty Division, University of Oslo, Nordbyhagen, Norway
f Department of Pediatrics, Rikshospitalet Medical Centre and Faculty Division Rikshospitalet, University of Oslo, Oslo, Norway


   ABSTRACT
TOP
 ABSTRACT
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
OBJECTIVE. The purpose of this work was to assess the annual incidence of arthritis in children and describe early disease and patient characteristics, microbiologic features, and immunogenetic factors in children with different subgroups of childhood arthritis.

PATIENTS AND METHODS. A population-based multicenter study was performed in southeastern Norway between June 1, 2004, and May 31, 2005. The total population of children under 16 years of age was 255303. Physicians were asked to refer their patients with suspected arthritis to the local department of pediatrics or rheumatology. The children were assessed on the basis of clinical, radiologic, and laboratory examinations at inclusion and followed up at 6 weeks, 6 months, and thereafter as long as clinically indicated. A chart review was performed to identify patients with arthritis who had not been included prospectively.

RESULTS. The total annual incidence of arthritis was 71 per 100000 children. Transient arthritis, juvenile idiopathic arthritis, postinfectious arthritis, and infectious arthritis were found in 43, 14, 9, and 5 of 100000 children, respectively. The incidence was higher in children under the age of 8 years than in older children (107 vs 34 per 100000). Arthritis occurred more frequently in boys than in girls before the age of 8 years but not thereafter. The median age of onset was lower in children with infectious arthritis than in those with other types of arthritis. Monarthritis was less frequent in patients with juvenile idiopathic arthritis than in the other subgroups (64% vs 83%–100%). Ten percent of the patients had poststreptococcal reactive arthritis, and only 1 had enteropathic arthritis. Autoantibodies and the presence of HLA-B27 were associated with juvenile idiopathic arthritis.

CONCLUSIONS. The annual incidence of childhood arthritis was 71 per 100000 children. We found several factors that may help in differentiating between subgroups of arthritis.

Key Words: incidence • arthritis • children

Abbreviations: PRSA—poststreptococcal reactive arthritis • WBC, white blood cell • JIA—juvenile idiopathic arthritis • IgM—immunoglobulin M • ANA—antinuclear antibody • anti-CCP—anti–cyclic citrullinated peptide antibody • RF—rheumatoid factor • CI—confidence interval • OR—odds ratio

Arthritis is an inflammation of the synovia of the joints.1 It may be directly or indirectly caused by infectious agents, transient or chronic idiopathic, or associated with other diseases.2 A delay in diagnosis, treatment, or follow-up may result in heart disease in streptococcal-associated arthritis, visual impairment in chronic arthritis, and joint damage and bone destruction in septic and chronic arthritis.3–7 Only 1 single study has been performed that dealt with immunologic and microbiologic tests for identifying the different diagnostic groups, which would contribute to early recognition of the disease.2

Only 2 studies of the incidence of childhood arthritis have been performed, and the results have varied. In a study of Finnish children in 1986, Kunnamo et al8 found an incidence of 109 per 100000 children, and in 2001, von Koskull et al9 reported an incidence of 83 per 100000 children in a German study. However, subgroups of childhood arthritis were not described in detail in the German study, and the inclusion of patients was mainly based on questionnaires distributed to primary care physicians. There are few reports on the incidence of subgroups of childhood arthritis, such as enteropathic, Lyme, and poststreptococcal reactive arthritis (PSRA).8,10,11

The aim of this prospective, population-based study was to estimate the annual incidence of arthritis in children and to describe the role of patient characteristics, auto-antibodies, HLA-B27, and microbiologic variables in early recognition of distinct subgroups of childhood arthritis.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Background Population
We conducted a population-based, multicenter study in 3 counties in southeastern Norway between June 1, 2004, and May 31, 2005. Twenty-seven percent of the Norwegian population live in this region, and the total population is 1252835. The total number of children under the age of 16 years was 255303 on January 1, 2004,12 93688 in the city of Oslo, 112129 in the mainly suburban county of Akershus, and 49486 in the small-town and rural county of Buskerud. In Scandinavia the majority of patients receive care within their county of residence, and the homogeneous health care and social security system, with its equality of access, facilitates recruitment to epidemiologic studies.13

Recruitment
We recruited children under the age of 16 years with possible or evident arthritis and/or osteomyelitis, determined on the basis of ≥1 of the following characteristics: (1) joint swelling; (2) limited range of motion in ≥1 joint and walking with a limp or other functional limitations affecting arms and/or legs; and (3) pain in ≥1 joint or extremity together with C-reactive protein level of >20 mg/L and/or an erythrocyte sedimentation rate of >20 mm/hour and/or white blood cell (WBC) count of >12 x 109/L. These signs should have lasted for <6 weeks and should not have been caused by trauma.

All of the general practitioners, pediatricians, orthopedic surgeons, and rheumatologists in the 3 counties (n = 1300) were contacted. They received 4 letters, 1 at the beginning and then every 3 months during the study period. They were asked to refer children who satisfied the criteria to a local hospital on the day the patient was first seen. Within 1 to 3 days, the patient was examined at 1 of the pediatric departments in the region or at the regional department of pediatric rheumatology, (ie, Akershus University Hospital, Buskerud Hospital, Ullevål University Hospital, or the Rikshospitalet Medical Centre). We searched the hospitals' computerized records for 181 relevant diagnoses based on the International Classification of Diseases, 10th Revision,14 at the end of the study, to identify any patients with arthritis who had not been included.

Inclusion Criteria
Only patients with permanent residence in the counties of Oslo, Buskerud, or Akershus were included, and the arthritic disease had to include 1 of the following 3 signs: (1) swelling of a joint; (2) restricted mobility of a joint with warmth and/or tenderness and/or pain1; or (3) arthritis demonstrated by ultrasound or MRI.

Exclusion Criteria
Patients who had been diagnosed with juvenile idiopathic arthritis (JIA) before June 1, 2004, or who had inflamed synovia related to trauma or malignant disease were excluded.

Classification Procedure
All of the follow-up data from the medical charts relevant to the final diagnosis were included up to March 2006 (range: 9–21 months). Two researchers recorded the clinical information independently on a standardized form. In case of disagreement, the classification was established in consultation with specialists in pediatric infectious diseases and pediatric rheumatology. Written informed consent was obtained from the parents of the children included in the study. The regional ethics committee for medical research and the ombudsman for privacy in research at the Norwegian Social Science Data Services approved the study.

Assessments
The number of swollen, tender, and mobility-restricted joints1 was registered on admission, after 6 weeks, and after 6 months. In addition, the children were reexamined within a few days if they had not improved significantly. An ultrasound of affected joints was performed on admission. In addition, an ultrasound of the hips was performed on all of the children <5 years of age with symptoms from the legs. Joint aspiration and MRI were recommended within 3 days if monoarthritis or oligoarthritis of <2 weeks' duration occurred in combination with 1 of the following: (1) fever of >38.5°C; (2) C-reactive protein level of >30 mg/L, erythrocyte sedimentation rate of >30 mm/hour, or WBC count of >12 x 109/L; (3) excessively painful joint or bone; or (4) other suspicious factors for septic arthritis or osteomyelitis. In addition, we recommended that joint aspiration and MRI be performed within 14 days if arthritis in 1 to 3 joints persisted for >1 week.

Classification Criteria
The classification criterion for septic arthritis was that either the synovial fluid tested positive for bacteria by culture or microscopy or the synovial fluid WBC count was >50 x 109/L. Acute rheumatic fever was classified according to the modified Jones criteria.4 PSRA was classified on the basis of the criteria proposed by Ayoub.15 The criterion for enteropathic arthritis was arthritis together with positive bacterial stool culture (Yersinia, Salmonella, Shigella, or Campylobacter species) or serologic evidence of Yersinia infection. Patients with no other obvious cause of arthritis and Borrelia infection confirmed by serology were diagnosed with Lyme arthritis. Arthritis that had lasted <6 weeks, with no established association to infection, was classified as transient arthritis. Arthritis with transient erythematous raised skin lesions was classified as urticaria arthritis. Henoch-Schönlein purpura was classified according to the American College of Rheumatology criteria.16 JIA was classified according to the International League of Associations for Rheumatology criteria, that is, arthritis of unknown etiology that persisted for ≥6 weeks with onset before the age of 16 years.17

Microbiologic, immunologic, radiologic, and HLA-B27 tests were performed at each of the hospitals as part of the routine diagnostic procedure (Table 1). The evidence of antecedent group A streptococcal infection was defined as the presence of 1 of the following: (1) group A streptococci in throat culture or rapid antigen testing at inclusion or during the previous 4 weeks; (2) increasing antistreptolysin-O and/or anti-deoxyribonuclease B titer of ≥2 dilution steps between the acute and convalescent phases; or (3) antistreptolysin-O and/or anti-deoxyribonuclease B titer of ≥600 during the first 6 weeks after inclusion. For other infections, positive immunoglobulin M (IgM) antibody or a significant change in immunoglobulin G antibodies or titers determined on the basis of the laboratory findings was considered positive. One antinuclear antibody (ANA) titer of ≥40 or a ratio of >1.4 was considered positive. In addition, anti–cyclic citrullinated peptide antibody (anti-CCP) level of ≥25 U, >5 IU/mL, or IgM rheumatoid factor (RF) of ≥24.0 IU/mL was considered positive.


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  		TABLE 1 Tests Performed on 182 Patients With Arthritis

 
Statistics
Relations between categorical variables were studied using the {chi}2 test or Fisher's exact test, for groups composed of <5 case subjects. The only 2 continuous variables in our study were age and duration of symptoms. Because these were not normally distributed, nonparametric tests were used: the Mann-Whitney-Wilcoxon test for comparison between 2 groups and the Kruskal-Wallis test for comparison between multiple groups. The continuous variables were described in terms of range, median, and quartiles. We constructed 95% confidence intervals (CIs) for incidence using the normal distribution approximation. A P value of <.05 was considered significant. All of the analyses were performed by using SPSS 13 for Microsoft Windows (SPSS Inc, Chicago, IL).


   RESULTS
TOP
 ABSTRACT
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
A total of 427 children fulfilled the recruitment criteria for possible arthritis, of whom 281 (66%) were part of the prospective study and 146 (34%) were identified through chart reviews (Fig 1). A total of 182 patients had arthritis, of whom 154 (85%) were included prospectively and 28 (15%) were identified through chart reviews. The age and gender composition was comparable in both groups (data not shown). Twenty-two arthritis patients (28%) in Akershus were included on the basis of chart reviews, compared with 6 patients (7%) in Oslo and 0 patients (0%) in Buskerud (Oslo versus Akershus: P < .01). A total of 146 arthritis patients (80%) were reexamined after 6 weeks and 111 patients (61%) at the 6-month follow-up. The prospectively enrolled patients who did not attend the planned follow-up visit reported (on their previous visit or by telephone) that they no longer had symptoms of arthritis. Additional data on the numbers of children with arthritis were collected from chart reviews from 9 to 21 months after the start of the study. Of the 245 patients without arthritis, 42 had an orthopedic disease, 32 had arthralgia, 28 had osteomyelitis, 27 had vasculitis without arthritis, 6 had a malignant disease, and 110 had various other conditions.


Figure 1
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  		FIGURE 1 Flowchart for identification of children with arthritis.

 
Incidence
A total of 182 patients with arthritis corresponds with an annual incidence of 71 per 100000 children <16 years of age (Table 2). The annual incidence per 100000 children was 43 for transient arthritis, 14 for JIA, 9 for postinfectious arthritis, and 5 for infectious arthritis (septic arthritis or arthritis with acute osteomyelitis). The overall incidence of arthritis was higher in boys than in girls (odds ratio [OR]: 1.6; 95% CI: 1.2–2.1). Transient arthritis was more frequent in boys than girls (OR: 2.1; 95% CI: 1.4–3.2), whereas the proportion of JIA was higher among girls than boys (OR: 2.9; 95% CI: 1.4–6.0).


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  		TABLE 2 Annual Incidence of Recent-Onset Arthritis in Children <16 Years of Age According to Diagnostic Group and Gender

 
In the urban population of Oslo, the overall incidence of childhood arthritis was 88 per 100000 (95% CI: 68–105) compared with 70 per 100000 (95% CI: 55–86) in the suburban population of Akershus and 44 per 100000 (95% CI: 26–63) in the small-town and rural population of Buskerud. The incidence of JIA was similar in all 3 of the counties (range: 12–15 per 100 000). In 2 counties we compared the incidence of arthritis in areas with a high versus those with a low average income, and there was no statistical difference (data not shown).

The overall incidence of arthritis was higher in children under the age of 8 years than in older children (107 vs 34 per 100000; P < .0001). There was a higher occurrence of arthritis among boys than among girls in the age group 1 to 7 years (OR: 1.7; 95% CI: 1.3–2.2), but no gender difference was found in older children.

Patient and Disease Characteristics in Subgroups of Arthritis
Transient arthritis was most frequent in the age group from 2 to 5 years (Fig 2). The peak age of onset in postinfectious arthritis was 6 to 7 years. In JIA, the age distribution tended to be bimodal, with a slightly higher incidence in the age groups 1 to 3 and 8 to 9 years. Infectious arthritis occurred before the age of 3 years in 10 of 12 patients. The median age at study entry for patients with infectious arthritis was 1.9 years, which was lower than that for patients with all of the other subgroups of arthritis (P < .05; Table 3). The median age at onset was 7.1 years for patients with postinfectious arthritis compared with 4.7 years for transient arthritis (P < .05). The median age at onset for patients with PSRA was 7.6 years (range: 1.7–13.1 years). The median duration of symptoms before inclusion was 31 days (1 and 3 quartiles; range: 6–114 days) in patients with JIA compared with 2 days (1 and 3 quartiles; range: 1–6 days) in the other subgroups (P < .001). Monarthritis was significantly less frequent in subjects with JIA than in the other groups (P < .05). At 6 weeks after inclusion, 169 patients (93%) had had lower limb disease, 28 patients (15%) upper limb disease, and 16 patients (9%) upper and lower limb disease. Knee joints were found to be the most frequently affected joints at 6 weeks (n = 72; 40%), followed by hip joints (n = 69; 38%) and ankles (n = 35; 19%; P < .05 for knees or hips versus ankles; Fig 3).


Figure 2
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  		FIGURE 2 Age distribution of children with arthritis according to diagnostic group.

 

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  		TABLE 3 Patient and Disease Characteristics in Children With Recent-Onset Arthritis

 

Figure 3
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  		FIGURE 3 Joint involvement within the first 6 weeks of follow-up in patients with arthritis. Thirty-four patients had affection of >1 joint. a P < .05 versus ankles or other joints; b finger joints (n = 12), wrist (n = 6), elbow (n = 4), foot (n = 3), shoulder (n = 4), sacroiliac (n = 2).

 
Microbiologic and Immunologic Factors
Positive bacterial culture in a joint was found in 5 of 8 patients with septic arthritis. One patient with septic arthritis had Gram-positive cocci on microscopy. In the remaining 2 patients, the diagnosis of septic arthritis was based on WBC counts of >100 x 109/L of synovial fluid. Signs of current or recent infection were found in 50 patients (27%) with arthritis: 24 patients (100%) with postinfectious arthritis, 8 patients with infectious arthritis (75%), 7 patients with JIA (19%) and 11 patients with transient arthritis (10%; Table 4).


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  		TABLE 4 Microbiologic Findings in Patients With Arthritis by Diagnostic Group

 
Twenty one (58%) of the 36 patients with JIA had oligoarthritis, 7 (19%) had IgM RF-negative polyarthritis, 4 (8%) had enthesitis-related arthritis, 2 (6%) had psoriatic arthritis, and 2 (6%) had undifferentiated arthritis. Of the patients tested for HLA-B27, the test results were positive in 11 of 30 patients with JIA (37%) compared with 4 of 54 patients (7%) in other subgroups (P < .001). ANA was positive within the first 6 weeks in 8 patients with JIA (22%) and in 1 patient with Henoch-Schönlein purpura. IgM RF was positive in 3 patients with JIA within the first 6 weeks (2 of the patients tested positive on ≥2 occasions 3 months apart within the first 6 months). Anti-CCP was positive in 3 patients with JIA. IgM RF or anti-CCP was not positive in any of the children with other subgroups of arthritis.


   DISCUSSION
TOP
 ABSTRACT
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
This is the third large prospective study of the total annual incidence of arthritis in children. We found a total annual incidence of 71 per 100000 children. Arthritis was more common in the youngest age groups and was more prevalent in boys. Transient arthritis was by far the most frequent subgroup, followed by JIA, postinfectious arthritis, and infectious arthritis. Children with septic arthritis were younger than those in the other groups, and patients with postinfectious arthritis had the highest age of onset. Number and type of joint involvement and association with ANA, anti-CCP, IgM RF, and HLA-B27 differed between the diagnostic groups. PSRA was frequent, whereas arthritis associated with enteropathic bacteria was rare.

Although all of the physicians were repeatedly informed of the recruitment criteria, our incidence figures must be considered minimum estimates. Because arthritis can be of short duration and/or migratory, some patients may not have been referred. The fact that the incidence was higher in the urban county (Oslo), where the distance to primary health care centers and hospitals is short, could be because of underrecruitment of patients outside of Oslo. Some children in our study had suffered persisting symptoms for weeks and months before inclusion, which supports our assumption that not all of the patients with mild cases were recruited. Children with disease duration of >6 weeks would also not have been referred to our study, because recent onset was 1 of the recruitment criteria. Incomplete data, differences between laboratory methods in the different hospitals, and significantly different disease duration between patients with JIA and the other diagnostic groups before inclusion mean that our data must be interpreted with caution. Because of multiple testing, a P value of >.01 should be interpreted cautiously.

Our total incidence of 71 per 100000 children is similar to the study performed in a small city in Finland, where the incidence was 64 per 100000,18 and the prospective urban study from Germany, with an incidence of 83 per 100000.9 However, septic arthritis was not included in the German study, and most of the patients were recruited on the basis of a questionnaire returned by primary care physicians. Interobserver disagreement in the assessment of arthritis is high among rheumatologists19 and is probably even higher in primary health care.

The total annual incidence of 109 per 100000 subjects in the study by Kunnamo et al8 was higher than in our study. This is mainly because of the incidence of transient synovitis of the hip that they found in 52 per 100000 subjects, whereas we only found 18 per 100000 subjects. On the other hand, we classified several children with hip affection as having postinfectious arthritis. Other studies from Germany (urban), Sweden (urban), and the Netherlands (urban and nonurban) have found incidences of transient synovitis of the hip ranging from 39 to 200 per 100000 subjects using different classification criteria.9,20,21 In contrast to Kunnamo et al,8 we used signs of inflammation as 1 of the criteria and did not ask for referral of children with hip pain as the only symptom. We also included nonurban children and found a lower incidence in the nonurban counties. On the basis of these previous studies, this may indicate that our Oslo data are the most representative. However, it cannot be ruled out that there may be true differences between Finland and eastern Norway or urban and nonurban districts or that the incidence has declined over the last 2 decades.

The lower incidence of septic arthritis in our study versus in the Finnish study could be because of the effect of the Haemophilus influenzae type B vaccination, which was introduced in Norway in 1992, and this is in line with other studies.22 Three of our patients had arthritis and a positive bacterial blood culture without meeting the criteria for septic arthritis. A positive blood culture has been used as a criterion for the diagnosis of septic arthritis in a few previous studies,23,24 and this would have increased our incidence for septic arthritis.

Enteropathic arthritis was rare in our study: 0.4 per 100000, as suggested previously by Rudwaleit et al.25 In Finland and Italy, Yersinia infections seem to be frequent in children, and geographical differences may exist.8,26,27 The incidence of PSRA was higher in our study than the estimates from Florida and Finland.8,11 However, the heterogenous use of the term and difficulties in diagnosing recent streptococcal infection may explain the variations in the results.3,15 The 14 per 100000 annual incidence of JIA presented here is lower than the incidence of juvenile rheumatoid arthritis reported by Kunnamo et al,8 but our results are in accordance with those of other Nordic studies.28,29

In line with previous studies, arthritis was found in our study to be more frequent in boys than in girls and more common in the youngest age groups.8,9 On the other hand, we found that the gender difference was only present in children under the age of 8 years. Septic arthritis was most frequent in children younger than 3 years in our study, which is in accordance with results reported previously.8,30,31 Our finding of a late age at onset of postinfectious arthritis is also similar to that of others.3,10,32,33 We found the knee, hip, and ankle to be the most frequently affected joints. Hip involvement in transient arthritis has been reported in very high numbers20,21 and may have been underestimated in our study. Five of 6 patients with polyarthritis had JIA, and knee and ankle involvement were frequent in JIA, as found previously by others.34–36 ANA, anti-CCP, or IgM RF was positive in 31% of the patients with JIA but in only 1 patient in the other subgroups, showing that these test have high specificity and low sensitivity for the classification of JIA.

Signs of possible previous or concomitant infection were demonstrated microbiologically in 27% of our children, and there were microbiologic findings in all of our diagnostic groups. In a Swedish population-based cohort of patients with adult undifferentiated arthritis, 45% had signs of previous infection based on patient histories or microbiologic findings.37 Most cases of childhood arthritis are of unknown origin, and testing for other agents could increase our knowledge of environmental triggers. The infections for which we tested may vary from one year to another, and inclusion of patients for >1 year might have provided a better estimate of the annual incidence of postinfectious and parainfectious arthritis. The effect of microbes in childhood arthritis patients requires additional study.


   CONCLUSIONS
TOP
 ABSTRACT
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Childhood arthritis is common, particularly transient arthritis that is 3 times as frequent as JIA. Young age at onset was most frequent in infectious arthritis. Hip involvement was associated with transient arthritis, whereas female gender, extended joint involvement, and immunologic factors correlated with JIA. Signs of current or recent infection were associated with the onset of arthritis in 27% of the children. Our results suggest that the incidence of childhood arthritis may differ between geographic areas or might have declined over the last 2 decades.


   ACKNOWLEDGMENTS
 
This study was supported by a grant from the Norwegian Foundation for Health and Rehabilitation via the Norwegian Rheumatism Association.

We are indebted to the patients, guardians, and primary care physicians who made this work possible. We thank Dr V. Halvorsen (Orthopedic Centre, Ulleval University Hospital) and Dr K. Mreihil (Department of Pediatrics, Akershus University Hospital) for assistance in planning the study and recruiting patients. We are grateful to Professor P. Gaustad, Department of Microbiology, Rikshospitalet Medical Centre, for assistance in planning the study and performing microbiologic tests. We also thank the staff in the Departments of Clinical Chemistry, Microbiology, Immunology, and Radiology at Akershus University Hospital, Sykehuset Buskerud, Ulleval University Hospital, and Rikshospitalet Medical Centre.


   FOOTNOTES
 
Accepted Jun 21, 2007.

Address correspondence to Øystein Rolandsen Riise, MD, MPH, Department of Rheumatology, Rikshospitalet Medical Centre, N-0027 Oslo, Norway. E-mail: oystein.riise{at}rikshospitalet.no

The authors have indicated they have no financial relationships relevant to this article to disclose.


   REFERENCES
TOP
 ABSTRACT
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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PEDIATRICS (ISSN 1098-4275). ©2008 by the American Academy of Pediatrics

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