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

^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.

	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.

View larger version (17K): [in this window] [in a new window]   FIGURE 1 Flowchart for identification of children with arthritis.

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).

View larger version (11K): [in this window] [in a new window]   FIGURE 2 Age distribution of children with arthritis according to diagnostic group.

View larger version (26K): [in this window] [in a new window]   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).

	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 numbers^20,21 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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