The Open Rheumatology Journal




ISSN: 1874-3129 ― Volume 13, 2019
RESEARCH ARTICLE

Interethnic Variations and Clinical Features of Spondyloarthropathies in a Middle Eastern Country



Mohammed Kamil Quraishi1, *, Humeira Badsha2, Bhavna Khan3, Muhammad Shahzeb4, Srilakshmi Hegde5, Ayman Mofti5, Kong Kok Ooi6
1 Department of Urology, Medway Maritime Hospital, Kent, England, UK
2 Department of Rheumatology. Dr. Humeira Badsha Medical Center, Dubai, UAE.
3 Integrated Rheumatology and Arthritis Centre, Dubai Healthcare City, Dubai.
4 Department of Medicine, Jinnah Medical College Hospital, Karachi, Pakistan.
5 Department of Rheumatology, Al Biraa Arthritis & Bone Center, Dubai, UAE.
6 Department of Rheumatology, Tan Tock Seng Hospital, Singapore

Abstract

Objectives:

The study aimed to demonstrate the interethnic differences and clinical features of Spondyloarthropathy(SpA) patients in a diverse Middle Eastern Country.

Methods:

A retrospective review of medical records to collect the required data was conducted for SpA patients at two study institutions in the United Arab Emirates.

Results:

Of 141 SpA patients found, 88 AS(Ankylosing Spondylitis) patients and 53 ‘other SpA’ patients were identified. Males constituted 81% of AS and 55% of ‘other SpA’ patients. Patients with AS and ‘other SpA’ had a mean age of symptom onset of 28 and 34 years, respectively.

49% and 40% of AS and ‘other SpA’ patients had a history of Anti-TNF therapy usage. Enthesitis and Uveitis were noted in 16% and 18% of AS patients whilst 53% and 11% in ‘other SpA’ patients, respectively.

Caucasian, Indian Subcontinent and Arabs constituted 93% of our cohort. Mean age of onset of symptoms in the Indian Subcontinent ‘other SpA’ group was much greater than the other two ethnicities. Duration of symptoms to diagnosis was 3.5 and 4 years in AS and other SpA patients' respectively. HLA-B27 positivity was found in 53%, 80% and 93% of Arab, Indian Subcontinent and Caucasian AS patients, respectively, whilst seen in 50%, 25% and 33% of the same respective ethnicties in ‘other SpA’ patients.

Conclusion:

This study on 141 patients is the largest to analyse inter-ethnic variations in SpA patients in the region. Our cohort shows a short delay in diagnosis with a relatively higher Anti-TNF usage.

Keywords: Ankylosing Spondylitis, Spondyloarthropathy, spondyloarthritis, UAE, Emirates, ethnicity, HLA B27.


Article Information


Identifiers and Pagination:

Year: 2018
Volume: 12
First Page: 10
Last Page: 18
Publisher Id: TORJ-12-10
DOI: 10.2174/1874312901812010010

Article History:

Received Date: 21/09/2017
Revision Received Date: 12/12/2017
Acceptance Date: 12/01/2018
Electronic publication date: 19/01/2018

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© 2018 Quraishi et al.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: (https://creativecommons.org/licenses/by/4.0/legalcode). This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at the Department of Urology, Medway Maritime Hospital, Windmill Road, Gillingham, Kent, UK ME7 5NY; E-mail: MKQURAISHI@doctors.org.uk




1. INTRODUCTION

Spondyloarthropathies (Spondyloarthritis)(SpA) are a collection of chronic inflammatory rheumatic conditions that share multiple clinical features including axial and/or peripheral arthritis, enthesitis, absence of the serum rheumatoid factor and presence of common extra articular manifestations [1Ehrenfeld M. Spondyloarthropathies Best Pract Res Clin Rheumatol 2012; 26: 135-45.[http://dx.doi.org/10.1016/j.berh.2012.01.002] [PMID: 22424199] ]. The spondyloarthropathy family comprises of Ankylosing Spondylitis(AS), psoriatic arthritis, reactive arthritis, inflammatory bowel disease associated SpA, juvenile SpA and undifferentiated SpA(uSpA) [2Reveille JD, Arnett FC. Spondyloarthritis: Update on pathogenesis and management. Am J Med 2005; 118(6): 592-603.[http://dx.doi.org/10.1016/j.amjmed.2005.01.001] [PMID: 15922688] ]. These diseases are strongly associated with the genes of the Major Histocompatibility Complex (MHC), in particular, the Human Leucocyte Antigen(HLA) B27 [3Khan MA. Update on spondyloarthropathies. Ann Intern Med 2002; 136(12): 896-907.[http://dx.doi.org/10.7326/0003-4819-136-12-200206180-00011] [PMID: 12069564] , 4Reveille JD. HLA-B27 and the seronegative spondyloarthropathies. Am J Med Sci 1998; 316(4): 239-49.[http://dx.doi.org/10.1016/S0002-9629(15)40414-8] [PMID: 9766485] ].

Research in recent years has documented the clinical features of Ankylosing Spondylitis in the Middle East. The data highlighted the wide variation in HLA-B27 positivity across the region [5Alharbi SA, Mahmoud FF, Al Awadi A, Al Jumma RA, Khodakhast F, Alsulaiman SM. Association of MHC class I with spondyloarthropathies in Kuwait. Eur J Immunogenet 1996; 23(1): 67-70.[http://dx.doi.org/10.1111/j.1744-313X.1996.tb00265.x] [PMID: 8834924] -10Abdelrahman MH, Mahdy S, Khanjar IA, et al. Prevalence of HLA-B27 in patients with Ankylosing Spondylitis in Qatar. Int J Rheumatol 2012.] There is an even greater paucity of documentation of non-AS SpA in the Middle East, which may affect the management of these patients [11Uppal SS, Abraham M, Chowdhury RI, Kumari R, Pathan EM, Al Rashed A. Ankylosing spondylitis and undifferentiated spondyloarthritis in Kuwait: A comparison between Arabs and South Asians. Clin Rheumatol 2006; 25(2): 219-24.[http://dx.doi.org/10.1007/s10067-005-1162-1] [PMID: 16240074] ]. Uppal et al. found several interesting differences between AS and undifferentiated SpA patients amongst the South Asian and Middle Eastern patients in Kuwait. However there remains a lack of information on whether similar inter-ethnic SpA profiles exist amongst other Middle Eastern countries. With the exception of a small case series on AS patients in the UAE, there has been no other comparison of inter-ethnic profiles of any SpA subtype in the Middle East [8al Attia HM, Sherif AM, Hossain MM, Ahmed YH. The demographic and clinical spectrum of Arab versus Asian patients with ankylosing spondylitis in the UAE. Rheumatol Int 1998; 17(5): 193-6.[http://dx.doi.org/10.1007/s002960050033] [PMID: 9542780] ].

In recent years, UAE has seen significant reforms in demographic and health care organization [12Health Systems Profile-UAE Regional Health Systems Observatory- EMRO (2006) World Health Organisation 2006. Available from: http://apps.who.int/medicinedocs/documents/s17313e/s17313e.pdf]. As an emerging market in medical tourism, Dubai in particular boasts a very diverse patient population. With only 11% of the UAE population constituting the native Emiratis, there remains a respectable opening for studying inter-ethnic profiles in the country [13Population Estimates 2006 – 2010 UAE National Bureau of Statistics 2011. Available from: http://www.uaestatistics.gov.ae]. The inter-ethnic profiling may be of clinical benefit if there is an awareness of the prevalence of certain features in specific patient groups [14Nazarinia MA, Ghaffarpasand F, Heiran HR, Habibagahi Z. Pattern of ankylosing spondylitis in an Iranian population of 98 patients. Mod Rheumatol 2009; 19(3): 309-15.[http://dx.doi.org/10.3109/s10165-009-0153-5] [PMID: 19266255] ].

This case series is the first of its kind in studying all the subtypes of SpA in the UAE. The primary aim of our study was to demonstrate the interethnic variations and clinical features of Spondyloarthritis (SpA) patients from a specialized arthritis center and a Rheumatology department at a multi-specialty center in Dubai, United Arab Emirates.

2. MATERIALS AND METHODS

We conducted a retrospective study on patients with a diagnosis of SpA at a specialized arthritis centre and a rheumatology department of a multi-specialty medical centre in Dubai, UAE. Payment modalities for the patients at these private centres range from self-funding to comprehensive insurance cover. Patients were identified by examining electronic records for ICD 9 codes during the month of August 2012. Reviews of medical records were carried out to obtain the required data. The study was approved by an internal ethics committee at the specialized arthritis centre and was conducted in accordance with the recommendations of the Declaration of Helsinki.

The socio-demographic data collected included age, gender, smoking status, ethnicity and family history of SpA. Clinical data included the age of symptom onset, age of diagnosis, characteristic of back pain (inflammatory back pain was defined as low back pain and stiffness for more than three months that improves with exercise, but not relieved by rest), presence of peripheral arthritis, extra-articular manifestations (enthesitis, uveitis, psoriasis and inflammatory bowel disease), Human Leucocyte Antigen-27(HLA-B27) status, and treatment were recorded. The relevant information was obtained by accessing the last clinic consultation notes, when appropriate. HLA-B27 status was based on the result of the standard assay on peripheral blood as conducted by the local pathology laboratory. HLA-B27 subtype data was not recorded in our cohort due to inconsistent testing. The Bath AS Disease Activity Index(BASDAI) and Schoebers test are routinely conducted by the physician at every consultation for AS patients, but only the last documented entry was used for our analysis. Radiological evaluation was used to assess the evidence of unilateral or bilateral sacroiliitis on X-ray. A Magnetic Resonance Imaging (MRI) scan was used when the diagnosis was unclear.

Both centres adopted the same diagnostic criteria for the management of SpA. Patients were categorised as Ankylosing Spondylitis (AS) based on the modified New York criteria. Patients who fulfilled the European Spondyloarthropathy Study Group(ESSG) criteria but who did not meet the modified New York criteria were classed in the ‘other SpA’ group. In recent years, the terminology has evolved to classify as radiographic and non-radiographic SpA, however they were not classified in this manner at the time of diagnosis.

The analysis was conducted on the statistical package SPSS v20. The mean values were calculated for all continuous variables. The Unpaired Student’s t test was utilised to compare the means of continuous variables, whilst the Fischer’s exact test was used to evaluate percentages. A One-way ANOVA test was performed to study differences in means of more than two groups. A p-value of <0.05 was deemed to be of statistical significance for this analysis.

3. RESULTS

3.1. Socio-demographic Features

A total of 141 patients were identified, of whom 88 held a diagnosis of AS and 53 of other SpA. Table 1 summarises the socio-demographic characteristics of the patient populations. The ‘other SpA’ group constituted 2 IBD related SpA, 5 psoriasis related SpA, 2 reactive arthritis related SpA and 44 undifferentiated SpA. The difference in the mean age of symptom onset(p<0.01) and diagnosis(p<0.001) between AS and ‘other SpA’ patients was statistically significant. Nine AS patients were known to have a family history of AS, but their HLA-B27 status were unknown. No ‘other SpA’ patients were known to have any family history of SpA. HLA-B27 was positive in 76% of our AS patients but only 36% in the ‘other SpA’ cohort.

Table 1
Clinical and laboratory features seen in our Spondyloarthropathy cohort.


3.2. Clinical Features

The clinical characteristics of the patients are summarised in Table 2.

Table 2
Clinical features of the Ankylosing spondylitis and other Spondyloarthropathy patients.


Vitamin D insufficiency was observed in 42 (48%) AS and 26 (49%) ‘other SpA’ patients at some point during their follow-up care. The knees were the most commonly affected joint in ‘other SpA’ patients (49%) with 58% of these patients having bilateral knee involvement. Twenty three (43%) and five (9%) ‘other SpA’ patients showed back and neck involvement respectively. Eight AS patients had a characteristic bamboo spine whilst this feature was not observed in the ‘other SpA’ patients.

Achilles enthesitis was the most common form of enthesitis and was found in 28% and 13% of ‘other SpA’ and AS patients respectively. Plantar Fascitis was noted in 9(17%) ‘other SpA’ and 2(2%) AS patients Seventeen (32%) of ‘other SpA’ patients were on anti-TNF therapy at the last follow-up, whilst four(8%) other patients had previously utilised it. Anti-TNF was prescribed to 29 (33%) AS patients at the last follow up, whilst 14 (16%) others previously used this treatment modality. Nine(10%) AS and four(8%) ‘other SpA’ patients were on Methotrexate at the last follow-up; but seventeen(19%) AS and twelve (23%) ‘other SpA’ patients were on Sulfasalazine at the last follow-up.

3.3. Ethnic Variations

The inter-ethnic variations in the features of SpA were studied in the Arab, Caucasian and Indian Subcontinent patients since they contributed to the large majority of the cohort(93%). Table 3 summarises some of the features.

Table 3
Clinical and laboratory features of Ankylosing Spondylitis and other Spondyloarthropathy patients of the three major ethnicities.


Uveitis occurred in 5%, 23% and 12% of Arab, Indian Subcontinent and Caucasian AS patients, respectively. In ‘other SpA’ patients, uveitis occurred in 9% of Caucasians, 18% of Indian Subcontinent and none in Arab patients. The inter-ethnic differences in uveitis were not statistically significant in the patient populations. Enthesitis was observed in 10% of Arab, 15% of Indian Subcontinent and 24% of Caucasian AS patients. It was seen in 75% of Arab, 44% of Indian Subcontinent and 45% of Caucasian ‘other SpA’ patients. Of the eight AS patients that had a bamboo spine, six(15%) were from the Indian subcontinent, one(6%) patient was Caucasian and another(5%) was Arab. The mean(SE) BASDAI for the AS patients was 2.7(0.49) for Caucasian, 3.3(0.68) for Arab, And 3.6(0.41) for the Indian Subcontinent patients.

In patients with AS, HLA-B27 was positive in 53% of Arabs, 80% of Indian subcontinent and 93% of Caucasians. This contrasted to the low HLA-B27 positivity in the ‘other SpA’ population with 50% in Arabs, 25% in Indian Subcontinent and 33% in Caucasian patients. The difference in HLA positivity between the ethnic groups was statistically significant in the AS patients but not in the ‘other SpA’ patients.

4. DISCUSSION

The presence of variations in clinical features of spondyloarthropathies across various ethnicities and geographical demographics is well recognized [15Zhang S, Li Y, Deng X, Huang F. Similarities and differences between spondyloarthritis in Asia and other parts of the world. Curr Opin Rheumatol 2011; 23(4): 334-8.[http://dx.doi.org/10.1097/BOR.0b013e32834640a9] [PMID: 21494185] , 16Snoj J. UAE’s population - by nationality 2015. Available from: https://web.archive.org/web/20170321184658/http://www.bq-magazine.com/ economy/socioeconomics/2015/04/uae- population-by-nationality]. The UAE offers a great insight into studying such conditions owing to its diverse ethnic population. This ethnic diversity in our cohort reflects to a certain degree the general demographics of the UAE, with Indian Subcontinent expats and Arab nationals comprising an estimated 54.7% and 27.5% of the UAE population [17Gulf Research Center. Gulf Labour Markets & Migration 2014. Available from: http://gulfmigration.eu/uae-estimates-of- population-residing-in-the-uae-by-country-of- citizenship-selected-countries-2014/, 18Lau CS, Burgos-Vargas R, Louthrenoo W, Mok MY, Wordsworth P, Zeng QY. Features of spondyloarthritis around the world. Rheum Dis Clin North Am 1998; 24(4): 753-70.[http://dx.doi.org/10.1016/S0889-857X(05)70040-5] [PMID: 9891709] ]. Our results, based on a relatively large patient cohort, will provide a stepping stone for setting up local guidelines for better standardised management.

4.1. Clinical Features

AS and uSpA form the largest subgroups of spondyloarthropathies [19Baddoura R, Awada H, Okais J, Habis T, Attoui S, Abi Saab M. Validation of the European Spondylarthropathy Study Group and B. Amor criteria for spondylarthropathies in Lebanon. Rev Rhum Engl Ed 1997; 64(7-9): 459-64.[PMID: 9338927] , 20Brandt J, Bollow M, Häberle J, et al. Studying patients with inflammatory back pain and arthritis of the lower limbs clinically and by magnetic resonance imaging: Many, but not all patients with sacroiliitis have spondyloarthropathy. Rheumatology (Oxford) 1999; 38(9): 831-6.[http://dx.doi.org/10.1093/rheumatology/38.9.831] [PMID: 10515643] ]. USpA constituted 83% of the ‘other SpA’ group, and together with AS, they formed 94% of the total cohort. Due to lack of published data on ‘other SpA’ and since uSpA amounted to the large majority of this group, we decided to make comparisons with other documented uSpA data, mentioned in the discussion section. 6% of the AS patients did not have inflammatory back pain but were diagnosed on the basis that they still fulfilled the Modified New York criteria. Inflammatory back pain is one of the main clinical features of uSpA [20Brandt J, Bollow M, Häberle J, et al. Studying patients with inflammatory back pain and arthritis of the lower limbs clinically and by magnetic resonance imaging: Many, but not all patients with sacroiliitis have spondyloarthropathy. Rheumatology (Oxford) 1999; 38(9): 831-6.[http://dx.doi.org/10.1093/rheumatology/38.9.831] [PMID: 10515643] ], but only 53% of the ‘other SpA’ cohort exhibited it. This prevalence is similar to those documented in other uSpa studies [21Sampaio-Barros PD, Bértolo MB, Kraemer MH, Marques-Neto JF, Samara AM. Undifferentiated spondyloarthropathies: A 2-year follow-up study. Clin Rheumatol 2001; 20(3): 201-6.[http://dx.doi.org/10.1007/s100670170066] [PMID: 11434474] , 22Prakash S, Mehra NK, Bhargava S, Malaviya AN. HLA B27 related ‘unclassifiable’ seronegative spondyloarthropathies. Ann Rheum Dis 1983; 42(6): 640-3.[http://dx.doi.org/10.1136/ard.42.6.640] [PMID: 6606400] ].

4.2. Gender Distribution

The male predominance in the Caucasian populations of our AS and ‘other SpA’ groups was similar to those AS and uSpA data published in other literature [20Brandt J, Bollow M, Häberle J, et al. Studying patients with inflammatory back pain and arthritis of the lower limbs clinically and by magnetic resonance imaging: Many, but not all patients with sacroiliitis have spondyloarthropathy. Rheumatology (Oxford) 1999; 38(9): 831-6.[http://dx.doi.org/10.1093/rheumatology/38.9.831] [PMID: 10515643] , 23Carbone LD, Cooper C, Michet CJ, Atkinson EJ, O’Fallon WM, Melton LJ III. Ankylosing spondylitis in Rochester, Minnesota, 1935-1989. Is the epidemiology changing? Arthritis Rheum 1992; 35(12): 1476-82.[http://dx.doi.org/10.1002/art.1780351211] [PMID: 1472124] , 24Brophy S, Calin A. Ankylosing spondylitis: Interaction between genes, joints, age at onset, and disease expression. J Rheumatol 2001; 28(10): 2283-8.[PMID: 11669170] ]. The patients from our Indian subcontinent cohort however, exhibited a much poorer male to female ratio than the previously published data on Indian AS and uSpA groups, which ranged from 5:1 – 16:1 [22Prakash S, Mehra NK, Bhargava S, Malaviya AN. HLA B27 related ‘unclassifiable’ seronegative spondyloarthropathies. Ann Rheum Dis 1983; 42(6): 640-3.[http://dx.doi.org/10.1136/ard.42.6.640] [PMID: 6606400] , 25Singh G, Lawrence A, Agarwal V, Misra R, Aggarwal A. Higher prevalence of extra-articular manifestations in ankylosing spondylitis with peripheral arthritis. J Clin Rheumatol 2008; 14(5): 264-6.[http://dx.doi.org/10.1097/RHU.0b013e31817b8789] [PMID: 18824928] -27Prakash S, Mehra NK, Bhargava S, Vaidya MC, Malaviya AN. Ankylosing spondylitis in North India: A clinical and immunogenetic study. Ann Rheum Dis 1984; 43(3): 381-5.[http://dx.doi.org/10.1136/ard.43.3.381] [PMID: 6611138] ]. The Indian Subcontinent category included countries such as Pakistan and Sri Lanka which had not been featured in these reported studies. The inclusion of spondyloarthropathy patients from these other countries perhaps explains the distinct differences in gender ratio. The Arab AS cohort displayed a very high male prevalence(95%) than that documented in similar Middle Eastern patient groups [7Mustafa KN, Hammoudeh M, Khan MA. HLA-B27 prevalence in arab populations and among patients with ankylosing spondylitis. J Rheumatol 2012; 39(8): 1675-7.[http://dx.doi.org/10.3899/jrheum.120403] [PMID: 22753660] , 14Nazarinia MA, Ghaffarpasand F, Heiran HR, Habibagahi Z. Pattern of ankylosing spondylitis in an Iranian population of 98 patients. Mod Rheumatol 2009; 19(3): 309-15.[http://dx.doi.org/10.3109/s10165-009-0153-5] [PMID: 19266255] , 28Askari A, Al-Bdour MD, Saadeh A, Sawalha AH. Ankylosing spondylitis in north Jordan: Descriptive and analytical study. Ann Rheum Dis 2000; 59(7): 571-3.[http://dx.doi.org/10.1136/ard.59.7.571] [PMID: 10873969] ] including the Arab group of the previous UAE study [8al Attia HM, Sherif AM, Hossain MM, Ahmed YH. The demographic and clinical spectrum of Arab versus Asian patients with ankylosing spondylitis in the UAE. Rheumatol Int 1998; 17(5): 193-6.[http://dx.doi.org/10.1007/s002960050033] [PMID: 9542780] ]. Our series is the first to list the male to female sex ratio for any non-AS SpA patients of Arab ethnicity at 2:1.

4.3. Onset & Diagnosis

The mean age at the onset of symptoms in AS Arab and Indian subcontinent patients was similar to those in the Arab and Indian populations of the Kuwaiti and UAE study [8al Attia HM, Sherif AM, Hossain MM, Ahmed YH. The demographic and clinical spectrum of Arab versus Asian patients with ankylosing spondylitis in the UAE. Rheumatol Int 1998; 17(5): 193-6.[http://dx.doi.org/10.1007/s002960050033] [PMID: 9542780] , 11Uppal SS, Abraham M, Chowdhury RI, Kumari R, Pathan EM, Al Rashed A. Ankylosing spondylitis and undifferentiated spondyloarthritis in Kuwait: A comparison between Arabs and South Asians. Clin Rheumatol 2006; 25(2): 219-24.[http://dx.doi.org/10.1007/s10067-005-1162-1] [PMID: 16240074] ]. Interestingly, the onset of symptoms in ‘Other SpA’ patients occurred 8.2 and 9.8 years later in Arabs and Indian Subcontinent(South Asian) patients, respectively, than the Kuwaiti uSpA cohort [11Uppal SS, Abraham M, Chowdhury RI, Kumari R, Pathan EM, Al Rashed A. Ankylosing spondylitis and undifferentiated spondyloarthritis in Kuwait: A comparison between Arabs and South Asians. Clin Rheumatol 2006; 25(2): 219-24.[http://dx.doi.org/10.1007/s10067-005-1162-1] [PMID: 16240074] ]. The age at the onset of symptoms in Caucasian populations reflected those observed in a larger Caucasian dominant series [23Carbone LD, Cooper C, Michet CJ, Atkinson EJ, O’Fallon WM, Melton LJ III. Ankylosing spondylitis in Rochester, Minnesota, 1935-1989. Is the epidemiology changing? Arthritis Rheum 1992; 35(12): 1476-82.[http://dx.doi.org/10.1002/art.1780351211] [PMID: 1472124] , 24Brophy S, Calin A. Ankylosing spondylitis: Interaction between genes, joints, age at onset, and disease expression. J Rheumatol 2001; 28(10): 2283-8.[PMID: 11669170] , 29Sampaio-Barros PD, Bortoluzzo AB, Conde RA, Costallat LT, Samara AM, Bértolo MB. Undifferentiated spondyloarthritis: A longterm followup. J Rheumatol 2010; 37(6): 1195-9.[http://dx.doi.org/10.3899/jrheum.090625] [PMID: 20436080] ].

Spondyloarthropathies usually take 5-6 years to be diagnosed after symptom onset, particularly in the presence of early limited features [30Khan MA. Thoughts concerning the early diagnosis of ankylosing spondylitis and related diseases. Clin Exp Rheumatol 2002; 20(6)(Suppl. 28): S6-S10.[PMID: 12463439] ]. This delay may even stretch to over 10 years depending on circumstances [31Sieper J, Rudwaleit M, Khan MA, Braun J. Concepts and epidemiology of spondyloarthritis. Best Pract Res Clin Rheumatol 2006; 20(3): 401-17.[http://dx.doi.org/10.1016/j.berh.2006.02.001] [PMID: 16777573] ]. Most patients in our study had a very short delay to diagnosis. These results are much better than those published in other Middle Eastern [11Uppal SS, Abraham M, Chowdhury RI, Kumari R, Pathan EM, Al Rashed A. Ankylosing spondylitis and undifferentiated spondyloarthritis in Kuwait: A comparison between Arabs and South Asians. Clin Rheumatol 2006; 25(2): 219-24.[http://dx.doi.org/10.1007/s10067-005-1162-1] [PMID: 16240074] , 14Nazarinia MA, Ghaffarpasand F, Heiran HR, Habibagahi Z. Pattern of ankylosing spondylitis in an Iranian population of 98 patients. Mod Rheumatol 2009; 19(3): 309-15.[http://dx.doi.org/10.3109/s10165-009-0153-5] [PMID: 19266255] , 28Askari A, Al-Bdour MD, Saadeh A, Sawalha AH. Ankylosing spondylitis in north Jordan: Descriptive and analytical study. Ann Rheum Dis 2000; 59(7): 571-3.[http://dx.doi.org/10.1136/ard.59.7.571] [PMID: 10873969] ] countries and elsewhere [24Brophy S, Calin A. Ankylosing spondylitis: Interaction between genes, joints, age at onset, and disease expression. J Rheumatol 2001; 28(10): 2283-8.[PMID: 11669170] , 32Bodur H, Ataman S, Akbulut L, et al. Characteristics and medical management of patients with rheumatoid arthritis and ankylosing spondylitis. Clin Rheumatol 2008; 27(9): 1119-25.[http://dx.doi.org/10.1007/s10067-008-0877-1] [PMID: 18357499] -34Bakland G, Nossent HC, Gran JT. Incidence and prevalence of ankylosing spondylitis in Northern Norway. Arthritis Rheum 2005; 53(6): 850-5.[http://dx.doi.org/10.1002/art.21577] [PMID: 16342091] ]. The

Arab subset of our ‘Other SpA’ group was an exception, with long delays to diagnosis compared to the other Arab uSpA data. We speculate that the Arab ‘other SpA’ cohort possibly initially presented with slowly progressive non-specific or peripheral joint symptoms which further exacerbated by delays in seeking medical attention.

4.4. Extra-articular Features

Enthesitis was seen twice in as many ‘other SpA’ patients as AS patients and the difference was strongly significant. The occurrences of enthesitis amongst the ethnicities were similar to the large range of 20-60% occurrence reported in the literature which varied with the study population [8al Attia HM, Sherif AM, Hossain MM, Ahmed YH. The demographic and clinical spectrum of Arab versus Asian patients with ankylosing spondylitis in the UAE. Rheumatol Int 1998; 17(5): 193-6.[http://dx.doi.org/10.1007/s002960050033] [PMID: 9542780] , 11Uppal SS, Abraham M, Chowdhury RI, Kumari R, Pathan EM, Al Rashed A. Ankylosing spondylitis and undifferentiated spondyloarthritis in Kuwait: A comparison between Arabs and South Asians. Clin Rheumatol 2006; 25(2): 219-24.[http://dx.doi.org/10.1007/s10067-005-1162-1] [PMID: 16240074] , 22Prakash S, Mehra NK, Bhargava S, Malaviya AN. HLA B27 related ‘unclassifiable’ seronegative spondyloarthropathies. Ann Rheum Dis 1983; 42(6): 640-3.[http://dx.doi.org/10.1136/ard.42.6.640] [PMID: 6606400] , 23Carbone LD, Cooper C, Michet CJ, Atkinson EJ, O’Fallon WM, Melton LJ III. Ankylosing spondylitis in Rochester, Minnesota, 1935-1989. Is the epidemiology changing? Arthritis Rheum 1992; 35(12): 1476-82.[http://dx.doi.org/10.1002/art.1780351211] [PMID: 1472124] , 26Aggarwal R, Malaviya AN. Clinical characteristics of patients with ankylosing spondylitis India Clin Rheumatol 2009; 28: 1199-205., 28Askari A, Al-Bdour MD, Saadeh A, Sawalha AH. Ankylosing spondylitis in north Jordan: Descriptive and analytical study. Ann Rheum Dis 2000; 59(7): 571-3.[http://dx.doi.org/10.1136/ard.59.7.571] [PMID: 10873969] , 35Tayel MY, Soliman E, El Baz WF, El Labaan A, Hamaad Y, Ahmed MH. Registry of the clinical characteristics of spondyloarthritis in a cohort of Egyptian population. Rheumatol Int 2012; 32(9): 2837-42.[http://dx.doi.org/10.1007/s00296-011-2068-7] [PMID: 21879376] ]. The Arab AS patients in our study had lower occurrences of enthesitis than those reported in other Arab studies [8al Attia HM, Sherif AM, Hossain MM, Ahmed YH. The demographic and clinical spectrum of Arab versus Asian patients with ankylosing spondylitis in the UAE. Rheumatol Int 1998; 17(5): 193-6.[http://dx.doi.org/10.1007/s002960050033] [PMID: 9542780] , 9al-Arfaj A. Profile of ankylosing spondylitis in Saudi Arabia. Clin Rheumatol 1996; 15(3): 287-9.[http://dx.doi.org/10.1007/BF02229709] [PMID: 8793262] , 11Uppal SS, Abraham M, Chowdhury RI, Kumari R, Pathan EM, Al Rashed A. Ankylosing spondylitis and undifferentiated spondyloarthritis in Kuwait: A comparison between Arabs and South Asians. Clin Rheumatol 2006; 25(2): 219-24.[http://dx.doi.org/10.1007/s10067-005-1162-1] [PMID: 16240074] ].

Uveitis rates in our ethnic cohorts were also similar to the overall ranges(9-22%) reported in other studies with similar ethnicities and SpA subsets [8al Attia HM, Sherif AM, Hossain MM, Ahmed YH. The demographic and clinical spectrum of Arab versus Asian patients with ankylosing spondylitis in the UAE. Rheumatol Int 1998; 17(5): 193-6.[http://dx.doi.org/10.1007/s002960050033] [PMID: 9542780] , 20Brandt J, Bollow M, Häberle J, et al. Studying patients with inflammatory back pain and arthritis of the lower limbs clinically and by magnetic resonance imaging: Many, but not all patients with sacroiliitis have spondyloarthropathy. Rheumatology (Oxford) 1999; 38(9): 831-6.[http://dx.doi.org/10.1093/rheumatology/38.9.831] [PMID: 10515643] , 23Carbone LD, Cooper C, Michet CJ, Atkinson EJ, O’Fallon WM, Melton LJ III. Ankylosing spondylitis in Rochester, Minnesota, 1935-1989. Is the epidemiology changing? Arthritis Rheum 1992; 35(12): 1476-82.[http://dx.doi.org/10.1002/art.1780351211] [PMID: 1472124] , 25Singh G, Lawrence A, Agarwal V, Misra R, Aggarwal A. Higher prevalence of extra-articular manifestations in ankylosing spondylitis with peripheral arthritis. J Clin Rheumatol 2008; 14(5): 264-6.[http://dx.doi.org/10.1097/RHU.0b013e31817b8789] [PMID: 18824928] , 27Prakash S, Mehra NK, Bhargava S, Vaidya MC, Malaviya AN. Ankylosing spondylitis in North India: A clinical and immunogenetic study. Ann Rheum Dis 1984; 43(3): 381-5.[http://dx.doi.org/10.1136/ard.43.3.381] [PMID: 6611138] , 35Tayel MY, Soliman E, El Baz WF, El Labaan A, Hamaad Y, Ahmed MH. Registry of the clinical characteristics of spondyloarthritis in a cohort of Egyptian population. Rheumatol Int 2012; 32(9): 2837-42.[http://dx.doi.org/10.1007/s00296-011-2068-7] [PMID: 21879376] ] [. Al Attia reported a much higher occurrence in Arab and lower occurrence in South Asian(Indian Subcontinent) population of uveitis in AS patients [8al Attia HM, Sherif AM, Hossain MM, Ahmed YH. The demographic and clinical spectrum of Arab versus Asian patients with ankylosing spondylitis in the UAE. Rheumatol Int 1998; 17(5): 193-6.[http://dx.doi.org/10.1007/s002960050033] [PMID: 9542780] ]. Our findings suggested the prevalence of uveitis in Indian subcontinent and Arab patients similar to those reported in other Indian and Arab dominant studies [9al-Arfaj A. Profile of ankylosing spondylitis in Saudi Arabia. Clin Rheumatol 1996; 15(3): 287-9.[http://dx.doi.org/10.1007/BF02229709] [PMID: 8793262] , 26Aggarwal R, Malaviya AN. Clinical characteristics of patients with ankylosing spondylitis India Clin Rheumatol 2009; 28: 1199-205., 27Prakash S, Mehra NK, Bhargava S, Vaidya MC, Malaviya AN. Ankylosing spondylitis in North India: A clinical and immunogenetic study. Ann Rheum Dis 1984; 43(3): 381-5.[http://dx.doi.org/10.1136/ard.43.3.381] [PMID: 6611138] , 35Tayel MY, Soliman E, El Baz WF, El Labaan A, Hamaad Y, Ahmed MH. Registry of the clinical characteristics of spondyloarthritis in a cohort of Egyptian population. Rheumatol Int 2012; 32(9): 2837-42.[http://dx.doi.org/10.1007/s00296-011-2068-7] [PMID: 21879376] ]. The absence of uveitis amongst the Arab ‘other Spa’ patients could be associated with the low predominance of uveitis amongst Arab SpA patients or a consequence of a small Arab cohort.

4.5. Smoking

A significant proportion of the patients had a history of smoking. Smoking is associated with poor functional outcomes in spondyloarthropathy patients [36Kaan U, Ferda O. Evaluation of clinical activity and functional impairment in smokers with ankylosing spondylitis. Rheumatol Int 2005; 25(5): 357-60.[http://dx.doi.org/10.1007/s00296-004-0451-3] [PMID: 14991231] ]. Furthermore, spondyloarthropathy patients are at an independently increased risk of cardiovascular disease [37Mathieu S, Motreff P, Soubrier M. Spondyloarthropathies: An independent cardiovascular risk factor? Joint Bone Spine 2010; 77(6): 542-5.[http://dx.doi.org/10.1016/j.jbspin.2010.05.001] [PMID: 20646947] ]. It is therefore vital for patient education to form an integral component of management.

4.6. Anti TNF

Anti TNF usage has been poorly reported in the Arab countries. The usage in our cohort is much greater than 9% reported in an Egyptian spondyloarthropathy registry [35Tayel MY, Soliman E, El Baz WF, El Labaan A, Hamaad Y, Ahmed MH. Registry of the clinical characteristics of spondyloarthritis in a cohort of Egyptian population. Rheumatol Int 2012; 32(9): 2837-42.[http://dx.doi.org/10.1007/s00296-011-2068-7] [PMID: 21879376] ]. This may be because of the tertiary nature of the clinics which tend to deal with the more severe cases. The long term follow up seen in this database may explain the increasing prevalence of anti-TNF usage with time as patients deteriorate justifying anti-TNF usage.

4.7. HLA-B27 Positivity

The association between HLA-B27 and SpA has led to significant research into HLA-B27 and its subtypes. There appears to be a rough correlation between the incidences of HLA-B27 in the general population with the incidences in the same ethnic SpA population [38Zochling J, Smith EU. Seronegative spondyloarthritis. Best Pract Res Clin Rheumatol 2010; 24(6): 747-56.[http://dx.doi.org/10.1016/j.berh.2011.02.002] [PMID: 21665123] , 39Hajaj-Hassouni N, Burgos-Vargas R. Ankylosing spondylitis and reactive arthritis in the developing world. Best Practice & Clinical Rheumatology 2008; 22(4): 709723.].

The prevalence of HLA-B27 is known to vary only slightly amongst the resident population of the Arab countries. It has been found to be 4% in Kuwait [5Alharbi SA, Mahmoud FF, Al Awadi A, Al Jumma RA, Khodakhast F, Alsulaiman SM. Association of MHC class I with spondyloarthropathies in Kuwait. Eur J Immunogenet 1996; 23(1): 67-70.[http://dx.doi.org/10.1111/j.1744-313X.1996.tb00265.x] [PMID: 8834924] ], 1.4% in Lebanon [6Awadia H, Baddoura R, Naman R, et al. Weak association between HLA-B27 and the spondylarthropathies in Lebanon. Arthritis Rheum 1997; 40(2): 388-9.[http://dx.doi.org/10.1002/art.1780400226] [PMID: 9041952] ], 2.4% in Jordan [7Mustafa KN, Hammoudeh M, Khan MA. HLA-B27 prevalence in arab populations and among patients with ankylosing spondylitis. J Rheumatol 2012; 39(8): 1675-7.[http://dx.doi.org/10.3899/jrheum.120403] [PMID: 22753660] ], 6.4% in UAE [40al-Attia HM, al-Amiri N. HLA-B27 in healthy adults in UAE. An extremely low prevalence in Emirian Arabs. Scand J Rheumatol 1995; 24(4): 225-7.[http://dx.doi.org/10.3109/03009749509100878] [PMID: 7481586] ] and 0.3% in Oman [41White AG, Leheny W, Kuchipudi P, et al. Histocompatibility antigens in Omanis: Comparison with other Gulf populations and implications for disease association. Ann Saudi Med 1999; 19(3): 193-6.[http://dx.doi.org/10.5144/0256-4947.1999.193] [PMID: 17283451] ]. Arab and Indian Subcontinent people in the UAE were found to have a background HLA-B27 prevalence of 5.7% and 7.4%, however no data is available on Caucasians in this cohort. The HLA prevalence in the general Indian population was found to be varying between 26% [22Prakash S, Mehra NK, Bhargava S, Malaviya AN. HLA B27 related ‘unclassifiable’ seronegative spondyloarthropathies. Ann Rheum Dis 1983; 42(6): 640-3.[http://dx.doi.org/10.1136/ard.42.6.640] [PMID: 6606400] , 42Dhurandhar PS, Shankarkuma U. HLA Association in Seronegative Spondyloarthritis Patients From Mumbai, India. Int J Hum Genet 2007; 7(3): 235-9.[http://dx.doi.org/10.1080/09723757.2007.11886000] , 44Khan MA. HLA-B27 and its subtypes in world populations. Curr Opin Rheumatol 1995; 7(4): 263-9. [Editorial].[http://dx.doi.org/10.1097/00002281-199507000-00001] [PMID: 7547102] ] with relatively lower positivity seen in the South Indian population [45Shankarkumar U, Ghosh K, Mohanty D. HLA B27 polymorphism in Western India. Tissue Antigens 2002; 60(1): 98-101.[http://dx.doi.org/10.1034/j.1399-0039.2002.600115.x] [PMID: 12366791] ]. However specific geographical populations in India have been found to have HLAB27 as high as 19.6-29% [46Shankarkumar U. HLA-B27 allele diversity in Indians: Impact of ethnic origin and the caste system. Br J Biomed Sci 2003; 60(4): 223-6.[http://dx.doi.org/10.1080/09674845.2003.11783704] [PMID: 14725340] ]. In Caucasian, the background prevalence of HLA-B27 was found to be approximately 8-10% [3Khan MA. Update on spondyloarthropathies. Ann Intern Med 2002; 136(12): 896-907.[http://dx.doi.org/10.7326/0003-4819-136-12-200206180-00011] [PMID: 12069564] , 47Feltkamp TE, Mardjuadi A, Huang F, Chou CT. Spondyloarthropathies in eastern Asia. Curr Opin Rheumatol 2001; 13(4): 285-90.[http://dx.doi.org/10.1097/00002281-200107000-00007] [PMID: 11555729] ]. We would therefore expect to find higher HLA-B27 prevalence in our Indian subcontinent and Caucasian population, which is the case.

The HLAB27 prevalence in Caucasians amongst our cohorts was observed to be similar to 90% reported in Caucasian AS patients but was much lower than the 70% in Caucasian uSpA patients [3Khan MA. Update on spondyloarthropathies. Ann Intern Med 2002; 136(12): 896-907.[http://dx.doi.org/10.7326/0003-4819-136-12-200206180-00011] [PMID: 12069564] ].

There is a marked variation between HLA-B27 prevalence of AS patients in Arab countries, but is known to be generally lower than the global figures [10Abdelrahman MH, Mahdy S, Khanjar IA, et al. Prevalence of HLA-B27 in patients with Ankylosing Spondylitis in Qatar. Int J Rheumatol 2012.]. A review derived the prevalence of HLA-B27 to be 64% in Arab AS patients, by pooling together several studies [10Abdelrahman MH, Mahdy S, Khanjar IA, et al. Prevalence of HLA-B27 in patients with Ankylosing Spondylitis in Qatar. Int J Rheumatol 2012.]. HLA-B27 prevalence was found to vary between 76 – 94% in Indian AS patients [29Sampaio-Barros PD, Bortoluzzo AB, Conde RA, Costallat LT, Samara AM, Bértolo MB. Undifferentiated spondyloarthritis: A longterm followup. J Rheumatol 2010; 37(6): 1195-9.[http://dx.doi.org/10.3899/jrheum.090625] [PMID: 20436080] , 30Khan MA. Thoughts concerning the early diagnosis of ankylosing spondylitis and related diseases. Clin Exp Rheumatol 2002; 20(6)(Suppl. 28): S6-S10.[PMID: 12463439] , 48Madhavan R, Parthiban M, Rajendran CP, Chandrasekaran AN, Zake L, Sanjeevi CB. HLA class I and class II association with ankylosing spondylitis in a southern Indian population. Ann N Y Acad Sci 2002; 958: 403-7.[http://dx.doi.org/10.1111/j.1749-6632.2002.tb03013.x] [PMID: 12021150] ]. Our results in fact are very similar to those seen in the study on UAE AS population where Arab and Indian Subcontinent patients had HLA-B27 prevalence of 56% and 81%, respectively [8al Attia HM, Sherif AM, Hossain MM, Ahmed YH. The demographic and clinical spectrum of Arab versus Asian patients with ankylosing spondylitis in the UAE. Rheumatol Int 1998; 17(5): 193-6.[http://dx.doi.org/10.1007/s002960050033] [PMID: 9542780] ]. It is however slightly different to the Qatar resident Arab(74%), Asian(61%), Kuwait resident Arab(86.7%) and Indian subcontinent(75%) AS patients [10Abdelrahman MH, Mahdy S, Khanjar IA, et al. Prevalence of HLA-B27 in patients with Ankylosing Spondylitis in Qatar. Int J Rheumatol 2012., 11Uppal SS, Abraham M, Chowdhury RI, Kumari R, Pathan EM, Al Rashed A. Ankylosing spondylitis and undifferentiated spondyloarthritis in Kuwait: A comparison between Arabs and South Asians. Clin Rheumatol 2006; 25(2): 219-24.[http://dx.doi.org/10.1007/s10067-005-1162-1] [PMID: 16240074] ].

Our Indian Subcontinent ‘other SpA’ demographic had a much lower HLA-B27 prevalence than the previously reported 45% and 84% amongst Indian uSpA patients [25Singh G, Lawrence A, Agarwal V, Misra R, Aggarwal A. Higher prevalence of extra-articular manifestations in ankylosing spondylitis with peripheral arthritis. J Clin Rheumatol 2008; 14(5): 264-6.[http://dx.doi.org/10.1097/RHU.0b013e31817b8789] [PMID: 18824928] , 43Mishra MN, Singal V. Human leukocyte antigen B27 in 453 Asian Indian patients with seronegative spondyloarthropathy. Iran J Immunol 2010; 7(4): 252-6.[PMID: 21189449] ]. Our ‘other SpA’ patient profile had a markedly lower HLA-B27 prevalence than the Kuwaiti uSpA population both in Arab(66.7%) and Indian subcontinent(71.4%) patients [11Uppal SS, Abraham M, Chowdhury RI, Kumari R, Pathan EM, Al Rashed A. Ankylosing spondylitis and undifferentiated spondyloarthritis in Kuwait: A comparison between Arabs and South Asians. Clin Rheumatol 2006; 25(2): 219-24.[http://dx.doi.org/10.1007/s10067-005-1162-1] [PMID: 16240074] ].

4.8. Vitamin D Insufficiency

Vitamin D insufficiency characterized as <30ng/ml was found to be nearly 50% in our SpA cohort during testing performed at any random point in their follow up. Its significance was found in its association with higher SpA disease activity and severity [49Hmamouchi I, Paternotte S, Molto A, et al. Disease activity and comorbidities in early spondyloarthritis. Clin Exp Rheumatol 2016; 34(3): 396-403., 50Guillot X, Prati C, Wendling D. Vitamin D and spondyloarthritis. Expert Rev Clin Immunol 2014; 10(12): 1581-9.].

5. LIMITATIONS

Not everyone had HLA-B27 testing which may explain the low prevalence, particularly in the ‘other SpA’ group(55% were tested). This may be due to the fact that the results of the test were perhaps lost or the clinician felt that the result did not add enough diagnostic evidence to justify the cost of the test. Insurance cover was not recorded for patients, which may have been a possible source of bias in view of the high usage of Anti-TNF therapy in our cohort. Despite 83% of ‘other SpA’ group being constituted by uSpA, the ‘other SpA’ might have markedly affected the results, perhaps accounting for the differences in the results between other uSpA study groups.

CONCLUSION

Our study demonstrates the largest database of clinical features of Spondyloarthropathy patients in the UAE. It also appears to be a noteworthy research work analysing inter-ethnic variations in SpA patients in the region. The study highlights that HLA-B27 prevalence is relatively poorer amongst Arab AS patients and ‘other SpA’ patients. Spondyloarthropathy patients in the UAE generally have a very short delay in diagnosis. The study also highlights the relatively higher prevalence of Anti-TNF usage in the UAE. Greater emphasis should be placed on patient and clinician awareness regarding uveitis in Indian Subcontinent SpA patients in view of its high prevalence. Improvements need to be made for awareness among primary care physicians and rheumatologists regarding the varied presentations of ‘other SpA’ Arab patients in order to minimise the remarkably long delay in diagnosis.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

The study was approved by an internal ethics committee at the specialized arthritis centre and was conducted in accordance with the recommendations of the Declaration of Helsink.

HUMAN AND ANIMAL RIGHTS

No Animals were used in this research. All human research procedures followed were in accordance with the ethical standards of the committee responsible for human experimentation (institutional and national), and with the Helsinki Declaration of 1975, as revised in 2008.

CONSENT FOR PUBLICATION

Not Applicable.

CONFLICT OF INTEREST

The authors declare no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENTS

The authors would like to acknowledge the support offered by the staff members of the study centres.

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