INTRODUCTION — Arthritis is a recognized extraintestinal manifestation of several illnesses and conditions, including inflammatory bowel disease (IBD), bacterial infections of the gut, gluten sensitive enteropathy (celiac disease), various parasitic infections, pseudomembranous colitis, and following intestinal bypass surgery. Other illnesses have a propensity for causing inflammation of joints and the gut. Examples discussed in this review include Behçet’s and Whipple's diseases.
The clinical features of arthritis associated with IBD are discussed in detail here, along with the treatment for synovitis in patients with Crohn's disease and ulcerative colitis. The pathogenesis of these manifestations and the treatment of IBD are discussed separately. (See "Mechanisms for the induction of rheumatic symptoms by gastrointestinal disease" and "Immunologic basis for extraintestinal manifestations in inflammatory bowel disease" and "Overview of the medical management of mild to moderate Crohn's disease in adults" and "Medical management of ulcerative colitis".)
Therapy for reactive arthritis (formerly called Reiter syndrome), Behçet’s and Whipple's diseases are also discussed separately. (See appropriate reviews).
PREVALENCE AND ASSOCIATED DISEASES — Arthritis occurs in 9 to 53 percent of patients with IBD [1-9]. Arthritis is somewhat more likely to occur in patients with large-bowel disease and in those patients with complications such as abscesses, pseudomembranous polyposis, perianal disease, massive hemorrhage, erythema nodosum, stomatitis, uveitis, and pyoderma gangrenosum. Among patients with Crohn's disease, those with colonic involvement are at higher risk of developing synovitis than those with isolated small bowel disease. Males and females are affected equally. Both children and adults are at risk for this complication of IBD. In addition subclinical gut inflammation, documented by endoscopy, has been described in up to two-thirds of patients with spondyloarthropathies [10].
ULCERATIVE COLITIS AND CROHN'S DISEASE — Ulcerative colitis and regional enteritis (Crohn's disease) are the most frequently encountered types of idiopathic IBD that are associated with arthritis or spondylitis and are discussed first. Other disorders associated with joint pain and/or inflammation are discussed later. (See 'Other diseases with bowel and joint involvement' below.)
Clinical manifestations — Arthritis may affect the spine, sacroiliac joints, appendicular joints, or a combination of these articulations. Peripheral arthritis may be acute and remitting (Type I), or be a more chronic problem or have frequent relapses (Type II) [11]. Complications of IBD may also cause joint pain and must be distinguished from sterile inflammation. Bacterial infection of the sacroiliac or peripheral joints may occur due to fistulization or bacteremia. Adverse effects of treatment of IBD may also affect joints. Osteonecrosis (avascular necrosis of bone) due to glucocorticoid use is one example. (See "Osteonecrosis (avascular necrosis of bone)".)
Spondylitis and sacroiliitis — Spondylitis occurs in 1 to 26 percent of patients with IBD [1-4,7,12]. Males are more frequently affected than females. Patients typically complain of prolonged stiffness in the back and/or buttocks in the morning or after rest. Stiffness and associated pain are often relieved by exercise. Back symptoms are unrelated to those of the gastrointestinal disease. Physical examination may reveal limited spinal flexion and reduced chest expansion. Spondylitis may be the only articular manifestation or it may occur in association with type I peripheral arthropathy [11], which is discussed below.
Asymptomatic sacroiliitis, detected by radiography, occurs in 4 to 18 percent of patients with IBD [12]. By contrast, 52 percent of patients with IBD have abnormal technetium pyrophosphate bone scans of the sacroiliac joints [4,12]. No increased frequency of HLA-B27 in the subset of patients with IBD and radiographic sacroiliitis was apparent in this study.
In contrast, sacroiliitis in patients with Crohn's disease is strongly associated with CARD15 gene polymorphisms [13]. In a study of 102 patients with Crohn's disease, 23 were found to have radiological evidence of sacroiliitis. Although only three of these patients were HLA-B27 positive, 78 percent of those with sacroiliitis had a CARD15 variant, compared with only 48 percent of those who did not have sacroiliitis (odds ratio 3.8).
The presence of an abnormal radiograph of the sacroiliac joints does not indicate a higher risk for the development of spondylitis. Magnetic resonance imaging can also reveal changes (picture 1).
Type I arthropathy — In type I arthropathy, the peripheral arthritis tends to be acute, is pauciarticular (affecting six or fewer joints), is often associated with flares of the bowel disease, occurs early in the course of the bowel disease, is self-limiting (90 percent under 6 months), and does not result in joint deformities [11,14]. The knee is most commonly affected. Five percent of IBD patients develop type I arthropathy. Joint symptoms may occur prior to the onset of symptoms suggestive of bowel disease.
Type II arthropathy — In Type II arthropathy, patients have polyarticular disease, with metacarpophalangeal (MCP) joints being particularly involved [11]. Other joints (knees, ankles, elbows, shoulders, wrists, proximal interphalangeal (PIP), and metatarsophalangeal (MTP) joints) are less often affected. Approximately one half of the patients with IBD have migratory arthritis. Active synovitis may persist for months, and may recur repeatedly. Episodes of exacerbations and remissions may continue for years.
Type II arthropathy affects 3 to 4 percent of patients with IBD. Articular involvement rarely precedes the diagnosis of IBD and joint symptoms typically do not parallel the activity of bowel disease [11].
Laboratory findings — The peripheral white blood cell count, hematocrit, erythrocyte sedimentation rate, and serum C-reactive protein concentration usually reflect the activity of the intestinal disease and are therefore of little help in assessing arthritis or spondylitis. Serum levels of rheumatoid factor are not elevated.
HLA-B27 is found in 50 to 75 percent of the patients with axial arthritis [4]. An increase in frequency in HLA-B27, B35, and DRB1*0103 has been described in those with a type I peripheral arthritis; type II arthropathy has been associated with HLA-B44 (and not B27) [11]. While the reported HLA associations are of interest, HLA typing has no role in management of individual patients.
Synovial fluids have yielded from 5000 to 12,000 white blood cells per microliter, predominantly polymorphonuclear leukocytes [4,12]. Synovial membrane biopsies reveal nonspecific abnormalities, including: proliferation of synovial lining cells, increased vascularity, and infiltration of mononuclear cells [4,12].
Radiographic findings — Radiographs of the spine and pelvis may show typical findings of ankylosing spondylitis and sacroiliitis. Plain film radiographs of the peripheral joints demonstrate soft-tissue swelling, juxtaarticular osteoporosis, mild periostitis, and effusions, usually without erosions or destruction. Radiographs frequently have abnormal findings even in asymptomatic patients with IBD. In one study, for example, plain film and computer aided tomography (CT) were used to evaluate the sacroiliac joints of 65 patients with IBD, none of whom had symptoms of sacroiliitis; 18 percent had finding of sacroiliitis by plain film and 32 percent had had abnormal sacroiliac joints noted by CT scanning [15].
Diagnosis — There is no pathognomonic finding to confirm the clinical suspicion of arthritis due to IBD. While the diagnosis may be suspected in the proper clinical setting, it remains largely one of exclusion. (See "Evaluation of the adult with polyarticular pain".) If the arthritis affects a single joint (monoarthritis), or a few joints (oligoarthritis), it is particularly important to perform a joint aspiration to exclude septic arthritis, the presentation of which may be atypical in patients with IBD who are receiving antiinflammatory or immunosuppressive treatment. (See "Evaluation of the adult with monoarticular pain".)
Differential diagnosis — The differential diagnosis of joint pain in a patient with IBD is broad. Disorders causing joint pain that may occur with increased frequency in this setting include, but are not limited to:
In addition to the disorders listed above, there are other diseases and states that have prominent intestinal manifestations and are associated with arthritis. These include reactive arthritis (formerly Reiter syndrome), Whipple's disease, Behçet’s syndrome, intestinal bypass, gluten sensitive enteropathy, and parasitic infestations. Each of these conditions is discussed following the section on treatment of arthritis in IBD. (See 'Other diseases with bowel and joint involvement' below.)
Treatment — Effective treatment of the underlying IBD is often helpful in controlling the peripheral arthritis. Spinal involvement is more problematic and no therapy has been definitively shown to slow the radiographic progression of spondylitis. (See "Assessment and treatment of ankylosing spondylitis in adults".)
Peripheral arthritis — Some agents, notably sulfasalazine, azathioprine, 6-mercaptopurine, methotrexate, glucocorticoids, and tumor necrosis factor (TNF) inhibitors may be helpful for both bowel and joint inflammation [17-22]. NSAIDs may relieve the arthritic symptoms, but may have an adverse effect on the IBD. There is only limited information from randomized trials to guide treatment decisions for arthritis associated with inflammatory bowel disease; most of the available information is from small case series. Our recommendations are based upon the available evidence, inferences from studies of other forms of arthritis, including spondyloarthritis and reactive arthritis, and our clinical experience.
Recommendations — Since the peripheral arthritis associated with IBD is generally nondestructive, therapy is primarily directed at symptomatic relief.
Spondylitis and sacroiliitis — The axial disease associated with IBD is treated as is any spondyloarthropathy. The treatment for spinal and sacroiliac involvement is symptomatic, as it is for the peripheral arthritis. (See "Assessment and treatment of ankylosing spondylitis in adults".) However, even if back pain and stiffness are controlled, radiographic progression to bony ankylosis may occur. NSAIDs or COX-2 selective agents are used to treat spinal pain and stiffness. The same concerns and cautions that were noted above for peripheral arthritis apply to their use for spondylitis and sacroiliitis.
As noted earlier, experience with infliximab is limited to small case series in which it has been associated with improvement in symptoms of spondylitis as well as peripheral arthritis during treatment with infliximab [30]. Whether anti-TNF therapy has any long term effect upon the progression of spondylitis remains to be determined.
In selecting among the available anti-TNF therapies, it should be noted that while etanercept may be used safely, and is reported to be effective for arthritis and spinal involvement in Crohn's disease, it is of no benefit for the intestinal manifestations of that disorder, unlike infliximab, which is often used for Crohn's disease and complications such as fistula formation [32,33]. (See "Infliximab in Crohn's disease".)
Recommendations — Nonpharmacologic and pharmacologic treatment are complementary for patients with spinal involvement.
Although data are limited, it can be expected that sacroiliac and spinal inflammation associated with IBD will respond to anti-TNF therapy as it does in ankylosing spondylitis.
OTHER DISEASES WITH BOWEL AND JOINT INVOLVEMENT — In addition to ulcerative colitis and Crohn's disease, several other illnesses and conditions have intestinal involvement and arthritis as prominent clinical features. These include, but are not limited to: reactive arthritis (Reiter syndrome), Whipple's disease, Behçet’s disease, celiac disease, parasitic infestation, pseudomembranous colitis, and as a result of intestinal bypass surgery. These disorders are also considerations in the differential diagnosis of patients with suspected IBD and arthritis.
Reactive arthritis — Reactive arthritis may occur after enteric infection due to Salmonella, Shigella, Yersinia, or Campylobacter species [17,34]. The incidence of reactive arthritis following bacterial dysentery has been reported to range from 2 to 33 percent [2]. An increased risk of arthritis is associated with Yersinia infection and presence of HLA-B27 genotype [1]. HLA-B27 has been found in over ninety percent of such cases.
Joint pain following diarrheal illness due to pathogenic E. coli infection has been noted. This group of E. coli includes enterotoxigenic E. coli (ETEC), attaching and effacing E. coli (A/EEC), enteropathogenic E. coli (EPEC), and verocytotoxin (shigatoxin)-producing E. coli (VTEC). (See "Pathogenic Escherichia coli".) Unlike reactive joint pain following Salmonella, Shigella, and Yersinia infection, the risk for developing arthralgia following E. coli infection is not affected by HLA-B27 status [35].
Joint symptoms develop within two to three weeks of developing diarrhea. The knee, ankle, wrist, and sacroiliac joints are commonly involved. Demonstration of a pathogenic organism by stool culture and/or finding a rise in antibody titers to the putative organism is helpful in confirming the clinical suspicion of reactive arthritis. Antibiotic treatment may be effective if begun during the diarrheal phase, but is not effective once arthritis is present. (See "Reactive arthritis (formerly Reiter syndrome)".)
Whipple's disease — Whipple's disease is due to infection with Tropheryma whippelii. Infection can be wide spread and may cause diarrhea, malabsorption, and weight loss. Systemic infection is often associated with joint manifestations. The knee, ankle, and wrist are frequently affected. Some patients may develop spondylitis and or sacroiliac joint involvement. In some patients the articular symptoms develop prior to symptomatic enteric involvement. Small bowel biopsy is usually diagnostic. Whipple's disease requires long-term antibiotic therapy. (See "Whipple's disease".)
Behcet's disease — Behçet’s disease is characterized by oral and genital ulceration, iritis, and occasionally by central nervous system involvement. In addition, oligoarticular, asymmetric arthralgia and/or arthritis may develop in approximately 50 percent of patients. The knee, ankle, wrist, and elbow are common sites of involvement. Mucosal ulceration of the small bowel is a frequent manifestation and may cause nausea, diarrhea, abdominal pain, and distension. Behçet’s disease may be particularly difficult to distinguish from IBD. The presence of pathergy, sterile neutrophilic infiltration of sites of injury, may be one helpful diagnostic clue. (See "Clinical manifestations and diagnosis of Behçet’s disease" and "Treatment of Behçet’s disease".)
Celiac disease — Diet sensitive enteropathy/arthropathy (gluten sensitive enteropathy or celiac disease) may be associated with arthritis in some patients [3]. Articular involvement was peripheral in 10 percent, axial in 8 percent, and combined in 9 percent. The arthritis is typically nonerosive and can be either oligo-or polyarticular. Joint symptoms may precede gastrointestinal manifestations of the disease. Joint symptoms respond to a gluten free diet. (See "Pathogenesis, epidemiology, and clinical manifestations of celiac disease in adults" and "Management of celiac disease in adults".)
A patient has been described who developed arthritis due to milk allergy [36]. The arthritis could be provoked by challenge with milk and alleviated by milk withdrawal. Occasional patients with lactose deficiency have been reported to have arthritis [37].
Intestinal bypass arthritis — Intestinal bypass surgery was developed for the treatment of obesity in 1952; 11 years later arthritis was recognized as a postoperative complication [1,2]. Polyarthralgia and sometimes arthritis has been reported to occur weeks or years following surgery in 8 to 36 percent of patients [1,2]. Because of an unacceptably high incidence of adverse effects, including arthritis, the jejunocolic and jejunoileal bypass operations have been abandoned. (See "Surgical management of severe obesity".)
Joint pain and tenderness exceed objective findings in most cases of intestinal bypass associated arthropathy, but episodes with abrupt onset of pain and inflammation may also develop. Tenosynovitis is common, with episodes possibly lasting for days and even months affecting the knee, wrist, ankle, shoulder, and finger joints. It may also be responsible for pain in the neck and back. This risk of developing this syndrome is higher after jejunocolic than after jejunoileal surgery and higher in females than males. There is often an associated urticarial, vesicular, pustular, macular, or nodular skin eruption. (See "Neutrophilic dermatoses", section on 'Bowel-associated dermatosis-arthritis syndrome'.) The Raynaud phenomenon has been reported in one-third of patients.
Plain radiographs generally show no joint damage, although marginal erosions may develop in patients with persistent arthritis. Synovial fluids generally have white blood cell counts of 500 to 27,000 per microliter with predominantly polymorphonuclear leukocytes. Synovial biopsies show chronic synovitis with lymphocytes but without lymphoid follicles. Tests for rheumatoid factor, antinuclear antibodies, and HLA-B27 are usually negative, while immune complexes (and cryoglobulins) are often present. These complexes contain bacterial antigens (eg, E. coli, B. fragilis), their antibodies, IgA secretory component, and various complement components (eg, C3, C4, C5) [2].
NSAIDs and glucocorticoids are effective in controlling joint symptoms but more lasting results can be achieved by use of tetracycline therapy to decrease bacteria overgrowth. Severe and refractory arthritis may require reanastomosis of the bowel.
Parasitic rheumatism — Parasitic infections of the gut have been associated with arthritis and other rheumatic disease syndromes [2,38-40]. These include Strongyloides stercoralis, Taenia saginata, Endolimax nana, and Dracunculus medinensis. As the parasites are not isolated from the joints it has been postulated that the joint symptoms represent a form of reactive arthritis. (See "Reactive arthritis (formerly Reiter syndrome)".)
Pseudomembranous colitis — Arthritis associated with pseudomembranous colitis has been described following antibiotic therapy in case series. In a report of four patients, arthritis developed 9 to 35 days after the onset of diarrhea [2]. The large joints of the lower extremity are most often affected. Clostridium difficile was isolated from two patients. (See "Clinical manifestations and diagnosis of Clostridium difficile infection in adults".)
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SUMMARY AND RECOMMENDATIONS — Arthritis may occur as an extraintestinal manifestation of several conditions, including inflammatory bowel disease (IBD) and a number of other disorders. Other illnesses, such as Behçet's disease, may cause inflammation of both the joints and the gut. (See 'Introduction' above.)
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