Content uploaded by Raheela Khalid
Author content
All content in this area was uploaded by Raheela Khalid on Sep 21, 2019
Content may be subject to copyright.
Available via license: CC BY
Content may be subject to copyright.
Received 07/07/2019
Review began 08/27/2019
Review ended 08/30/2019
Published 09/18/2019
© Copyright 2019
Attalla et al. This is an open access
article distributed under the terms of
the Creative Commons Attribution
License CC-BY 3.0., which permits
unrestricted use, distribution, and
reproduction in any medium, provided
the original author and source are
credited.
Relationship between Ulcerative Colitis and
Rheumatoid Arthritis: A Review
Mark G. Attalla , Sangeeta B. Singh , Raheela Khalid , Musab Umair , Epenge Djonga
Emmanuel
1. Research, California Institute of Behavioral Neurosciences and Psychology, Fairfield, USA 2. Urology,
California Institute of Behavioral Neurosciences and Psychology, Fairfield, USA 3. Neurology, California
Institute of Behavioral Neurosciences and Psychology, Fairfield, USA
Corresponding author: Mark G. Attalla, mark_george.2029@yahoo.com
Disclosures can be found in Additional Information at the end of the article
Abstract
Ulcerative colitis (UC) is a colonic disease characterized by chronic inflammation. Rheumatoid
arthritis (RA) is a rheumatological chronic inflammatory disease characterized by joint swelling
and tenderness. It is also considered an autoimmune disorder. We want to discover if a link
exists between UC and RA and if so, how UC affects the progress of arthritis.
We used PRISMA guidelines. In this study, we used PubMed, PubMed Central (PMC), and
Google Scholar to collect data. Studies conducted more than 50 years ago, non-English articles,
and animal studies were excluded. All types of studies were included. We used keywords like
"ulcerative colitis", "rheumatoid arthritis", or "colitic arthritis" in the search.
We identified the following sets of results: 187,611 PubMed studies, 197,610 PMC studies, and
2,282,000 Google scholar studies. After applying inclusion and exclusion criteria, the number of
appropriate studies was narrowed down to 50.
Arthritis is the most common complication of ulcerative UC. The radiological changes are
similar to those seen in RA. There are common genes and antigens found in both diseases, such
as human leukocyte antigen (HLA-B27), interleukin 15, IgA. Certain drugs used for the
treatment of both disorders, including omega-3. Many studies revealed that a large number of
patients with UC developed RA within a few years.
All the findings prove that there is a relation between ulcerative colitis and rheumatoid
arthritis. This study is useful for doctors, scientists, and patients.
Categories: Gastroenterology, General Surgery, Rheumatology
Keywords: rheumatoid arthritis, ulcerative colitis, colitic arthritis
Introduction And Background
“As with many life-altering events, an autoimmune illness is almost guaranteed to cause you to
re-evaluate your priorities.” -Joan Friedlander
Ulcerative colitis (UC) is an immune disorder of the colon characterized by chronic
inflammation. The cause of the immune response is unclear, but genetic, dietary, and
environmental risk factors all play a role [1].
1 1 1 2
3
Open Access Review
Article DOI: 10.7759/cureus.5695
How to cite this article
Attalla M G, Singh B, Khalid R, et al. (September 18, 2019) Relationship between Ulcerative Colitis and
Rheumatoid Arthritis: A Review. Cureus 11(9): e5695. DOI 10.7759/cureus.5695
In contrast with that of Crohn's disease (CD), the inflammation of ulcerative colitis is limited to
the mucosa of the colon. The annual incidence of UC in the United States (US) is between nine
and twelve cases per 100,000 persons [1]. Inflammatory bowel diseases are more common in
industrialized countries and Western nations. The incidence levels also increased in persons
who live at higher latitudes. Smokers and patients who have had an appendectomy are less
likely to develop ulcerative colitis. The incidence of UC is equal between women and men, in
contrast to CD, which has a higher incidence in women. UC often presents with abdominal pain,
hematochezia, and diarrhea [1]. The onset of these symptoms may occur suddenly or gradually.
About one-third of patients with UC have extraintestinal manifestations, with the most
common one being arthritis (21% )[1].
Rheumatoid arthritis (RA) is a rheumatological chronic inflammatory disease characterized by
joint swelling, joint tenderness, and the destruction of these synovial joints, leading to severe
disability [2]. It is considered an autoimmune disease. RA is regarded as the most commonly
diagnosed form of arthritis: inflammatory arthritis. The etiology of RA is multifactorial.
Genetic susceptibility is evident in monozygotic twin and familial clustering studies, with a 50
percent risk of RA attributable to genetic factors. A study in the UK found that the population
minimum prevalence of RA is 0.44% in men and 1.16% in women [2]. Patients with RA typically
present with stiffness and pain in multiple joints. Respectively the wrists, proximal
interphalangeal joints, and metacarpophalangeal joints are most commonly involved, and if the
morning stiffness lasts more than one hour, it suggests an inflammatory etiology. It may
present with boggy swelling due to synovitis [2]. Patients may also present with more indolent
arthralgia before the onset of clinically apparent joint swelling. Systemic symptoms of weight
loss, fatigue, and low-grade fever may occur with active disease [2].
Both UC and RA involve an immune response that is inappropriate or excessive. These
autoimmune diseases can be caused or accompanied by a systemic disruption that may result in
acute or chronic injury, sometimes severe, in any organ system. They have common
inflammatory pathways; patients with one condition have a higher risk of having another of
these diseases relative to the rest of the population. Individually, these autoimmune diseases
are rare.
However, is there a relation or link between UC and RA? How can a patient with UC
subsequently develop RA? How does ulcerative colitis affect the progress, prevalence,
symptoms, and signs of RA? The answer to all these questions will create a clearer and fuller
picture of UC and RA. It will improve the treatment of these cases, limit the appearance of
arthritis in the colitic patient, and prevent the complications associated with these diseases.
This study aims to discover the link between these two diseases and how ulcerative colitis
affects the progress of RA. We used the US National Library of Medicine (PubMed), PubMed
Central (PMC), and Google Scholar to access appropriate data. This review presents the
assimilated information from several articles, reviews, case reports, case studies, cohort
studies, and clinical trials.
Review
Methods
Literature Search
We followed the PRISMA guidelines for data collection and presentation in this study.
Search Strategy and Study Selection
2019 Attalla et al. Cureus 11(9): e5695. DOI 10.7759/cureus.5695 2 of 9
The search strategy was designed and executed using data obtained from PubMed, PMC, and
Google Scholar to identify the link between UC and RA. The search query employed both a list
of keywords and index terminology including: "ulcerative colitis", “rheumatoid arthritis” and
“colitic arthritis." We excluded animal studies and articles published more than 50 years
ago. We included all types of studies published in English, including systemic reviews, clinical
trials, case reports, and traditional reviews. In the study, we did not specify a particular country
but included all countries worldwide. We included all full-text studies and abstracts with
information about the link between UC and RA.
Role of the Funding Source
The funder of the search had no role in the study design, data collection, data interpretation,
data analysis, or writing any of the reports. All the studies and the data of the search were
collected legally. The author had full access to all data in the study; the corresponding author
had the final responsibilities for the decision to submit for publication.
Results
The results for our methods and the inclusion and exclusion criteria are shown in Figure 1.
FIGURE 1: Flowchart describing the search strategy with the
inclusion and exclusion criteria
2019 Attalla et al. Cureus 11(9): e5695. DOI 10.7759/cureus.5695 3 of 9
Discussion
UC and RA involve an immune response. These autoimmune diseases can be caused, presented,
or accompanied by the systemic disruption that may result in acute or chronic inflammatory
injury. However, is there a relation or link between UC and RA? How does RA develop in a
patient with UC? We will discuss how UC affects the progress, the prevalence, the symptoms,
and signs of RA.
The Characteristics of Arthritis in Ulcerative Colitis
Arthritis is the most common complication of UC [3,4]. The rheumatologic complications of UC
may produce higher morbidity than the underlying intestinal disease [5]. Three studies describe
the characteristics of arthritis [6-8]. Two studies characterized it as recurrent, earlier onset, and
with acute asymmetrical involvement; usually monoarticular, the attacks were of short
duration and accompanied with little residual deformity or disability [6,7]. The study by Wright
and Watkinson is better as it contains several patients and has more references [6]. The third
study suggested that peripheral arthritis might change from acute and nondestructive to
chronic and destructive in some cases [8]. Sometimes there is an effusion in the affected joints,
but the aspiration is sterile [3]. However, the serological test for the rheumatoid factor, which is
always positive in RA, is negative [4,9].
Gravallese and Kantrowitz divided the rheumatological conditions associated with
inflammatory bowel disease into four categories [10]. First, a unique form of peripheral arthritis
which occurs in 15-20% of patients and is the self-limited, nondeforming, and seronegative
type that waxes and wanes with bowel flares. Second, spondylitis which occurs in 3-6% of
patients and is clinically and radiographically similar to idiopathic ankylosing spondylitis.
Third, a bilateral, symmetrical sacroiliitis which occurs in 4-18% of patients. Fourth, a category
that includes the rheumatologic complications of inflammatory bowel disease like clubbing,
vasculitis, osteoporosis, and septic arthritis [10].
Also, the radiological changes are similar to those seen in RA [4]. One study reported that 18
patients of 22 patients with UC have specific radiological osseous abnormalities [11]. The
computed tomography (CT) shows better sensitivity than x-ray analysis and can detect the
changes of early sacroiliitis before they became apparent on plain films: bilateral, symmetrical
joint narrowing with osseous erosion and then sclerosis [12,13].
As previously mentioned, the arthritis is pauciarticular. Arthritis begins in the lower limb and
the most frequently affected joints are knees, ankles, hips, and elbows, while the finger-joints
are less commonly attacked [6,14-16].
There is a positive association between arthritis and UC in the duration and extent of
symptoms as arthritis usually subsides with the remission of UC, especially after a colectomy
and exacerbations of arthritis [3,6,17].
In another three studies, each one gave a case report with a long history of RA, which was
followed by the association of UC, based on endoscopic and histological findings. However, the
underlying mechanism was unknown [18-20].
Genetics and Antigens
The relationship between UC and RA has not yet become clear. Perhaps specific genes may
predispose to both diseases; however; no genetic risk factor has been identified [21].
2019 Attalla et al. Cureus 11(9): e5695. DOI 10.7759/cureus.5695 4 of 9
Some studies suggested that UC and RA are both associated with the human leukocyte antigen
(HLA-B27) [22]. Klausen et al. reported a patient with both UC and RA who had a positive
association with HLA-B27 [23]. Scarpa et al. studied 79 patients with UC and found a higher
prevalence of HLA-B27 (p <0.05) [24]. Núñez et al. indicated that the development of articular
manifestations in patients with ulcerative colitis was influenced by genetic factors in the major
histocompatibility complex haplotypes [25]. However, while Scarpa et al. and Núñez et al. make
the same points, the latter is better as it contains a greater number of patients and is more
recent [24,25].
In a 2001 study, Mosquera-Marinez et al. state that interleukin 15 is overexpressed in the
inflamed mucosa of patients with inflammatory bowel disease at the level of macrophages.
Also, the study reported that interleukin 15 was present in patients with RA [26].
In 1988, Cooper et al. performed a study to measure the serum titers of IgA in many
inflammatory diseases, revealing that the levels are increased in RA and UC [27].
Chen at al. in their 2008 study “Haplotypes of PADI4 susceptible to RA are also associated with
UC in the Japanese population” studied the haplotypes of peptidyl arginine deiminase type 4
(PADI4) in 114 patients with UC. The results showed that haplotype 2 of (PADI4) is susceptible
to UC. Also, the study indicated that the haplotypes of PADI4 are the RA-susceptible gene [28].
Perdigones performed a study in 2010, on the regulatory element of the prostaglandin receptor
ER4 on 662 UC patients and 605 RA patients. The prostaglandin receptor ER4 is associated with
UC. The result of this study discovered that there is a significant influence between these
polymorphisms and UC and RA predisposition [29].
Effect of Certain Drugs on Ulcerative Colitis and Rheumatoid Arthritis
Many drugs are used for the treatment of both UC and RA. One of these drugs is corticosteroid,
which reduces colonic inflammation and reduces the incidence of RA [9,30].
Asada et al. discussed the effect of the therapeutic agents of RA on patients with UC [19]. Some
of these drugs did not induce colitis, although gold salts induced a form of colitis resembling
UC. At the end of this study, they reported that the therapeutic medications for RA are unlikely
to be the underlying cause of colitis [19].
Ruggiero et al.’s 2009 study reported that the omega-3 polyunsaturated fatty acid (PUFA) in
large doses affects patients with UC and RA. Omega-3 (PUFA) is beneficial in inflammatory
diseases by reducing pain, the number of tender joints, and the duration of stiffness [31].
In 2016, Szeto et al. showed that tocilizumab is an interleukin-6 receptor inhibitor for moderate
and severe rheumatoid arthritis, and they used it for patients with RA and UC. They found
clinical improvement in both diseases, and the laboratory studies supported the role of
interleukin-6 in the pathophysiology of ulcerative colitis [32].
So, we conclude that there is a group of drugs which can be used in the treatment of either UC
or RA. Some of these drugs are used as therapeutic agents for patients who simultaneously have
both diseases, and this proves that there is a link or relation between UC and RA.
Coexistence of Rheumatoid Arthritis and Ulcerative Colitis
We studied 15 studies which included data on the number of patients with both UC and RA and
2019 Attalla et al. Cureus 11(9): e5695. DOI 10.7759/cureus.5695 5 of 9
collated the data in Table 1 below.
Study
Number of
patients with
ulcerative colitis
Number of patients
with rheumatoid
arthritis
Notes
Ansell et
al. [33]
91 (37 males +54
females)
18 (7 males +11
females)
Wright et
al. [6] 269 31 50% rheumatic complain
Russell et
al. [34] 42 4 With x-ray evidence
Nugent et
al. [35] 555 17% (for all types of
arthritis)
All the 17% have articular manifestations respectively
rheumatoid arthritis, rheumatoid spondylitis, arthralgia,
erythema nodosum
Lindsley
et al. [36] 86 18 (21%)
Passo et
al. [14] 44 4
Mosebach
et al. [37] 30 21%
Bernstein
et al. [38] 3873 30.9%
TABLE 1: The number of patients with ulcerative colitis and rheumatoid arthritis
Two studies assessed the risk of RA in patients with UC. The first study (Weng et al.) said that
the risk of RA was 1.9 (95% CI: 1.5-2.3) but the second study (Cohen et al.) said that it was 2.1
(1.8-2.3) [39,40]. The first study seems more accurate as it included more patients (12,601) and
was performed over a longer period (1996-2005); the second study was conducted from 2001 to
2002.
Yüksel et al. enrolled 357 patients with inflammatory bowel disease (IBD) in their research
and showed that 66 patients (18.5%) had IBD-related peripheral arthritis (13.5% ulcerative
colitis) and the most common places were the knee (65.2%) and ankle (62.1%) [41].
In the study by Zippi et al., 595 patients with UC were enrolled, and the results showed that 168
patients had musculoskeletal manifestations, which included 61 with arthritis type 1 and 100
with arthritis type 2 [42].
Finally, two other studies revealed the odd's ratio of the presence of RA with UC. Wilson et al.
reported an odd's ratio of 1.9 (95% CI: 1.5-2.3) [43]. Bae et al. included 28,197 patients with UC,
collected data from 2009 to 2013, and reported an increased risk of RA (OR: 3.474, 95% CI:
2.671-4.519) [44].
2019 Attalla et al. Cureus 11(9): e5695. DOI 10.7759/cureus.5695 6 of 9
These two studies provided further evidence that there is a relation between UC and RA [45,46].
Each one carried a case report about a patient with UC, and then these cases were complicated
by arthritis that resembles that clinical picture of RA [45,46].
Studies Disagreeing on the Relation between Rheumatoid Arthritis and Ulcerative Colitis
On the other side, some studies disagree with the presence of the relationship between the two
diseases. Hammer et al. noted that the polyarthritis of patients with UC is different in many
aspects from that of RA [47]. McEwen showed that arthritis connected with UC differs from that
of RA in being acute in onset, involving few joints and recovering without residual changes
[48]. Finally, Teleuolova et al. showed that the combination of UC and RA is rare [49]. However,
the number of studies which disagree with this study’s proposal is tiny against the number of
studies that prove that there is a relation between the two diseases.
The limitations of this study are that this study is a traditional review, not a systematic review,
and we did not include studies outside English-language. We recommend that future studies
will focus on this relationship and discovering how both diseases affect each other. We also
recommend that future studies be based on clinical trials or case reports as there is currently
only a small number of these studies.
Conclusions
We aimed to find the relationship between UC and RA and how they affect each other. This
review discusses the characteristics of arthritis in patients with UC, which resemble that of RA.
We also collected data on the number of patients that have both conditions from many studies.
All these findings provide sufficient evidence that there is a relation between the two diseases.
This study is beneficial as it reviews data collected from the last 50 years from different
databases, including all cases that have both diseases. It will help scientists and doctors to
understand individual and shared elements of both disorders better.
Additional Information
Disclosures
Conflicts of interest: In compliance with the ICMJE uniform disclosure form, all authors
declare the following: Payment/services info: All authors have declared that no financial
support was received from any organization for the submitted work. Financial relationships:
All authors have declared that they have no financial relationships at present or within the
previous three years with any organizations that might have an interest in the submitted work.
Other relationships: All authors have declared that there are no other relationships or
activities that could appear to have influenced the submitted work.
References
1. Adams SM, Bornemann PH: Ulcerative colitis. Am Fam Physician. 2013, 15:699-705.
2. Charles J, Britt H, Pan Y: Rheumatoid arthritis. Aust Fam Physician. 2013, 42:765.
3. Edwards FC, Truelove SC: The course and prognosis of ulcerative colitis. III. Complications .
Gut. 1964, 5:1-22. 10.1136/gut.5.1.1
4. Bywaters EGL, Ansell BM: Arthritis associated with ulcerative colitis; a clinical and
pathological study. Ann Rheum Dis. 1958, 17:169-183. 10.1136/ard.17.2.169
5. Colìa R, Corrado A, Cantatore FP: Rheumatologic and extraintestinal manifestations of
inflammatory bowel diseases. Ann Med. 2016, 48:577-585. 10.1080/07853890.2016.1195011
6. Wright V, Watkinson G: The arthritis of ulcerative colitis. Br Med J. 1965, 2:670-675.
10.1136/bmj.2.5463.670
7. Raffucci FL: Colitis and arthritis . Br Med J. 1965, 2:663.
2019 Attalla et al. Cureus 11(9): e5695. DOI 10.7759/cureus.5695 7 of 9
8. Momohara S: [Arthritic manifestations in ulcerative colitis] (Article in Japanese) . Nihon
Rinsho. 1999, 57:2566-70.
9. Jalan KN, Prescott RJ, Walker RJ, Sircus W, McManus JP, Card WI: Arthropathy, ankylosing
spondylitis, and clubbing of fingers in ulcerative colitis. Gut. 1970, 11:748-54.
10. Gravallese EM, Kantrowitz FG: Arthritic manifestations of inflammatory bowel disease . Am J
Gastroenterol. 1988, 83:703-9.
11. Clark RL, Muhletaler CA, Margulies SI: Colitic arthritis. Clinical and radiographic
manifestations. Radiology. 1971, 101:585-94. 10.1148/101.3.585
12. Cammisa M, Lomuto M, Bonetti MG: Sacroiliitis in seronegative polyarthritis: CT analysis .
Clin Exp Rheumatol. 1987, 5:105-7.
13. Gore RM, Balthazar EJ, Ghahremani GG, Miller FH: CT features of ulcerative colitis and
Crohn's disease. AJR Am J Roentgenol. 1996, 167:3-15. 10.2214/ajr.167.1.8659415
14. Passo MH, Fitzgerald JF, Brandt KD: Arthritis associated with inflammatory bowel disease in
children. Relationship of joint disease to activity and severity of bowel lesion. Dig Dis Sci.
1986, 31:492-7. 10.1007/bf01320313
15. Arthritis in ulcerative colitis. Br Med J. 1958, 23:500.
16. Hendrickson BA, Gokhale R, Cho JH: Clinical aspects and pathophysiology of inflammatory
bowel disease. Clin Microbiol Rev. 2002, 15:79-94. 10.1128/CMR.15.1.79-94.2002
17. Russell AS: Arthritis, inflammatory bowel disease, and histocompatibility antigens . Ann
Intern Med. 1977, 86:820-1. 10.7326/0003-4819-86-6-820
18. Adachi Y, Hinoda Y, Takahashi, et al.: Rheumatoid arthritis associated with ulcerative colitis . J
Gastroenterol. 1996, 31:590-5.
19. Asada Y, Isomoto H, Shikuwa S, et al.: Development of ulcerative colitis during the course of
rheumatoid arthritis: association with selective IgA deficiency. World J Gastroenterol. 2006,
12:5240-3.
20. Hemminki K, Li X, Sundquist K, Sundquist J: Familial association of inflammatory bowel
diseases with other autoimmune and related diseases. Am J Gastroenterol. 2010, 105:139-47.
10.1038/ajg.2009.496
21. Toyoda H, Wang SJ, Yang HY, et al.: Distinct associations of HLA class II genes with
inflammatory bowel disease. Gastroenterology. 1993, 104:741-8. 10.1016/0016-
5085(93)91009-7
22. Moll JM: Inflammatory bowel disease . Clin Rheum Dis. 1985, 11:87-111.
23. Klausen T, Amris K, Helin P: Ulcerative colitis complicating seronegative HLA-A2-B27
rheumatoid arthritis with sacroiliitis. Ann Rheum Dis. 1992, 51:1009-11.
10.1136/ard.51.8.1009
24. Scarpa R, del Puente A, D'Arienzo A, et al.: The arthritis of ulcerative colitis: clinical and
genetic aspects. J Rheumatol. 1992, 19:373-7.
25. Núñez C, Alecsandru DM, Mendoza JL, Urcelay E, Díaz-Rubio M, de la Concha EG, Martinez A:
Genetic markers linked to rheumatoid arthritis are also strongly associated with
articularmanifestations in ulcerative colitis patients. Hum Immunol. 2006, 67:324-30.
10.1016/j.humimm.2006.02.035
26. Mosquera-Martinez J, Boyer F, Fontanges E, Miossec P: Rheumatoid arthritis associated with
ulcerative colitis. Ann Rheum Dis. 2001, 60:1155. 10.1136/ard.60.12.1155
27. Cooper R, Fraser SM, Sturrock RD, Gemmell CG: Raised titres of anti-klebsiella IgA in
ankylosing spondylitis, rheumatoid arthritis, and inflammatory bowel disease. Br Med J (Clin
Res Ed). 1988, 21:1432-4. 10.1136/bmj.296.6634.1432
28. Chen CC, Isomoto H, Narumi Y, et al.: Haplotypes of PADI4 susceptible to rheumatoid
arthritis are also associated with ulcerative colitis in the Japanese population. Clin Immunol.
2008, 126:165-71. 10.1016/j.clim.2007.09.001
29. Perdigones N, Martín E, Robledo G, et al.: Study of chromosomal region 5p13.1 in Crohn's
disease, ulcerative colitis, and rheumatoidarthritis. Hum Immunol. 2010, 71:826-8.
10.1016/j.humimm.2010.05.010
30. Burt RW, Berenson MM, Samuelson CO, Cathey WJ: Rheumatoid vasculitis of the colon
presenting as pancolitis. Dig Dis Sci. 1983, 28:183-8. 10.1007/bf01315149
31. Ruggiero C, Lattanzio F, Lauretani F, Gasperini B, Andres-Lacueva C, Cherubini A: Omega-3
polyunsaturated fatty acids and immune-mediated diseases: inflammatory boweldisease and
rheumatoid arthritis. Curr Pharm Des. 2009, 15:4135-48. 10.2174/138161209789909746
32. Szeto MCH, Yalçın MD, Khan A, Piotrowicz A: Successful use of tocilizumab in a patient with
2019 Attalla et al. Cureus 11(9): e5695. DOI 10.7759/cureus.5695 8 of 9
coexisting rheumatoid arthritis and ulcerative colitis. Case Reports Immunol. 2016,
2016:7562123. 10.1155/2016/7562123
33. Ansell BM, Wigley RAD: Arthritic manifestations in regional enteritis. Ann Rheum Dis. 1964,
23:64-72. 10.1136/ard.23.1.64
34. Russell AS: Arthritis and ulcerative colitis . Br Med J. 1965, 16:944.
35. Nugent FW, Rudolph NE: Extracolonic manifestations of chronic ulcerative colitis . Med Clin
North Am. 1966, 50:529-34. 10.1016/S0025-7125(16)33207-2
36. Lindsley CB, Schaller JG: Arthritis associated with inflammatory bowel disease in children . J
Pediatr. 1974, 84:16-20. 10.1016/s0022-3476(74)80547-0
37. Mosebach S, Tromm A, Wittenborg A, May B: [Rheumatoid disorders in Crohn disease and
ulcerative colitis. Dominance of non-inflammatoryfactors] (Article in German). Leber Magen
Darm. 1995, 25:79-85.
38. Bernstein CN, Wajda A, Blanchard JF: The clustering of other chronic inflammatory diseases
in inflammatory bowel disease: a population-based study. Gastroenterology. 2005, 129:827-
36. 10.1053/j.gastro.2005.06.021
39. Weng X, Liu L, Barcellos LF, Allison JE, Herrinton LJ: Clustering of inflammatory bowel
disease with immune mediated diseases among members of a northern california-managed
care organization. Am J Gastroenterol. 2007, 102:1429-35.
40. Cohen R, Robinson D Jr, Paramore C, Fraeman K, Renahan K, Bala M: Autoimmune disease
concomitance among inflammatory bowel disease patients in the United States, 2001-2002.
Inflamm Bowel Dis. 2008, 14:738-43. 10.1002/ibd.20406
41. Yüksel I, Ataseven H, Başar O, et al.: Peripheral arthritis in the course of inflammatory bowel
diseases. Dig Dis Sci. 2011, 56:183-7. 10.1007/s10620-010-1260-z
42. Zippi M, Corrado C, Pica R, et al.: Extraintestinal manifestations in a large series of Italian
inflammatory bowel disease patients. World J Gastroenterol. 2014, 14:17463-7.
10.3748/wjg.v20.i46.17463
43. Wilson JC, Furlano RI, Jick SS, Meier CR: Inflammatory bowel disease and the risk of
autoimmune diseases. J Crohns Colitis. 2016, 10:186-93. 10.1093/ecco-jcc/jjv193
44. Bae JM, Choo JY, Kim KJ, Park KS: Association of inflammatory bowel disease with ankylosing
spondylitis and rheumatoid arthritis: a nationwide population-based study. Mod Rheumatol.
2017, 27:435-440. 10.1080/14397595.2016.1211229
45. Speiser JC, Moore TL, Zuckner J: Ulcerative colitis with arthritis and vasculitis . Clin
Rheumatol. 1985, 4:343-7. 10.1007/bf02031620
46. Israel DM, Olson AD, Ilowite NT, Davidson M: Arthritis as the initial manifestation of
inflammatory bowel disease in early infancy. J Pediatr Gastroenterol Nutr. 1989, 9:123-5.
47. Hammer B, Ashurst P, Naish J: Diseases associated with ulcerative colitis and Crohn's disease .
Gut. 1968, 9:17-21. 10.1136/gut.9.1.17
48. McEwen C: Arthritis accompanying ulcerative colitis . Clin Orthop Relat Res. 1968, 57:9-17.
49. Teleuolova AS, Beysenbekova ZhA, Tayzhanova DZh, Teuesheva ZB, Guseinova ZK:
[Nonspecific ulcerative colitis in combination with rheumatoid arthritis (case report)] (Article
in Russian). Georgian Med News. 2015, 70:2.
2019 Attalla et al. Cureus 11(9): e5695. DOI 10.7759/cureus.5695 9 of 9