International Journal of Rheumatic Diseases 2015

REVIEW ARTICLE

The saga of diagnostic/classification criteria in Behcet’s disease Fereydoun DAVATCHI, Bahar SADEGHI ABDOLLAHI, Cheyda CHAMS-DAVATCHI, Farhad SHAHRAM, Hormoz SHAMS, Abdolhadi NADJI, Tahereh FAEZI, Massoomeh AKHLAGHI, Zahra GHODSI, Negin MOHTASHAM and Farimah ASHOFTEH Behcet’s Disease Unit, Rheumatology Research Center, Tehran University of Medical Sciences, Tehran, Iran

Abstract There are 17 sets of diagnosis/classification criteria for Behcet’s disease: Curth (1946), Hewitt (1969), Mason (1971), Japan (1972), Hubault (1974), O’Duffy (1974), Cheng (1980), Dilsen (1986), Japan revised criteria (1988), International Study Group on Behcet’s disease (ISG criteria, 1990), Iran traditional criteria (1993), Iran Classification Tree (1993), Dilsen revised criteria (2000), Korea Criteria (2003), International Criteria for Behcet’s Disease (ICBD, 2006) and the revised ICBD (2010). This review is intended to show how to use them and show their performance in patients from different parts of the world. The major sets of patients (patient numbers, control numbers, year) on which the criteria were tested are: ISG set (886/97/1990), Iran (2069/1540/ 1993), Asia and Pacific League of Associations for Rheumatology (APLAR: 216/145/1998), Russia (105/233/ 2000), USA (50/NA/2000 [NA: not available]), India (50/NA/2004), Singapore (37/NA/2004), China (98/NA/ 2004), Korea (1454/NA/2004), Iran (4900/2020/2004), ICBD (2556/1163/2006), Germany (86/38/2008), China (322/118/2008), Iran (6128/3400/2010) and Iran (7011/5226/2013). For the following criteria sets (O’Duffy, Dilsen, Japan revised, ISG, Korea, ICBD, revised ICBD), the sensitivity in ISG cohort was 82/95/93/ 91/NA/NA/NA%, in APLAR 62.5/75/73/72/NA/NA/NA%, in Russia 91/92/92/86/NA/NA/NA%, USA 88/85/82/ 76/NA/NA/NA%, ICBD 83/87/88/82/90/96/96%, China 64/71/66/65/85/87/NA% and in Iran (2013) 69.5/81/ 86/77.5/86/98/97%. Specificity in ISG was 83/79/89/96/NA/NA/NA%, in APLAR 98/96/99/99/NA/NA/NA%, in Russia 88/91/92/100/NA/NA/NA%, ICBD 95/91/92/96/93/89/91%, China 97.5/95/98/99/97/94/NA% and in Iran (2013) 99/95/98/99/98/96/97%. Accuracy in ISG was 82.5/87/91/93.5/NA/NA/NA%, in APLAR 80/85/ 86/86/NA/NA/NA%, in Russia 89.5/92/92/93/NA/NA/NA%, ICBD 87/88/89/87/91/94/94.5%, China 72/78/ 74/74/88/89/NA% and in Iran (2013) 82/87/91/87/91/97/97%. ISG criteria has very good specificity, but lacks good sensitivity and accuracy. In contrast, ICBD has much better sensitivity, a little less specificity and better accuracy. Key words: Behcet’s disease, classification criteria, diagnostic criteria.

INTRODUCTION Behcet’s disease (BD) was first described in 1937 by Hulucßi Behcßet, a Turkish dermatologist.1 Before him,

Correspondence: Professor Fereydoun Davatchi, Rheumatology Research Center, Shariati Hospital, Jalal Al-Ahmad Avenue, Tehran 14117, Iran. Email: [email protected]

the disease was presented by a Greek ophthalmologist, Benediktos Adamantiades2,3 in 1930. Therefore, the disease is also known as Adamantiades–Behcet’s disease.4 However, the symptoms have been known since antiquity, but Behcßet was the first to recognize their association as a separate entity. No disease has ever incited to so many diagnostic criteria as BD. The first set of criteria was presented by Curth5 in 1946. In 1969, 23 years later, the second set

© 2015 Asia Pacific League of Associations for Rheumatology and Wiley Publishing Asia Pty Ltd

F. Davatchi et al.

of criteria was presented in France6 by Hewitt, a renowned French dermatologist. It is customary to say that 2 years later, Hewitt and colleagues revised their criteria,7 but they really did not; they only confirmed their original criteria and how to use it. The same year (1971), in the UK, Mason and Barnes presented their criteria.8 In 1972, the Japan Research Committee for Behcet’s Disease introduced the Japan criteria, which had large success.9 In 1974, in a collaborative work between France and Tunisia, Hubault and Hamza presented their criteria.10 This was the first international collaborative work for a BD diagnostic/classification criteria. The same year, O’Duffy presented an American version of the criteria.11 Six years later, Cheng and Zhang created the Chinese version of BD criteria.12 Although performing well, the criteria remained largely unknown. It is the only criteria set that keeps its performance with or without using the results of a pathergy test.13 In 1986, Dilsen, a pupil of Hulucßi Behcet, presented the Turkish criteria, which were based essentially on the presence of pathergy phenomena.14 Two years later, in 1988, the Japan criteria were revised.15 In 42 years, nine sets of criteria were proposed from different countries and there was no consensus on any of them. To overcome the situation, the International Study Group on Behcet’s Disease, composed of seven countries (France, Iran, Japan, Tunisia, Turkey, UK and USA), started to gather BD and control patients from their respective countries. After long debate during the International Conference on Behcet’s Disease in Rochester, Minnesota, USA,16 the ISG criteria was presented in 199017 and 1992.18 The aim of this review is to describe how these criteria can be used and to show their performance in different sets of patients and controls, from different parts of the world.

HOW THE CRITERIA WORK AND THEIR PERFORMANCE In the Curth criteria5 four categories of manifestations were considered for diagnosis: oral aphthosis (OA), genital aphthosis (GA), skin manifestations (SM) and ophthalmological manifestations (OM). SM were erythema nodosum (EN), pseudo-folliculitis (PF) and positive pathergy test (PT). The presence of two symptoms, one from each of the four categories, was necessary for diagnosis. Hewitt6 opted for a system point. Disease manifestations were divided into two categories: major manifestations and secondary signs. Major manifestations were

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iridocyclitis (40 points), OA (30 points) and GA (30 points). Secondary signs were subcutaneous nodules, recurrent phlebitis or large vein thrombosis, meningeal features and pseudo bulbar signs. They each scored 30 points. Neurological signs mimicking multiple sclerosis gained 25 points. Other skin lesions (except subcutaneous nodules) and other ocular manifestations (except iridocyclitis) were given 20 points each. Psychiatric features, epididymitis and inflammatory arthritis or arthralgia received 15 points. Prolonged fever and other systemic manifestations (intestinal attacks, cardiac manifestations and adenopathy) received 10 points each. For diagnosis, the presence of at least one major manifestation was mandatory. The diagnosis was then made with a total of 100 points or more. In the Mason and Barnes criteria,8 symptoms were divided into two categories: major and minor criteria. Major criteria were OA, GA, skin (PF, EN, PT) and OM. Minor criteria were arthritis/arthralgia (A), gastrointestinal manifestations (GI), vessel thrombosis (VT), neurological manifestations (NM), cardiac manifestations (CM), epididymitis (E) and family history of BD (FH). The presence of three major criteria, or two major and two minor were required for the diagnosis. The Japan criteria,9 proposed by the Japan Research Committee for Behcet’s Disease, was based on four major symptoms: OA, GA, SM (as with Curth criteria) and OM. In the absence of OM, the presence of three criteria was necessary for the diagnosis. In the presence of OM, only one other criterion was enough to make the diagnosis. Once the diagnosis was made, if the four major manifestations were present, the patient was classified as having the complete form of the disease, otherwise, the incomplete form. In Hubault and Hamza criteria,10 symptoms were divided into major (OA, GA, OM, PT) and minor manifestations (PF, A, phlebitis). The presence of three major manifestations was required for the diagnosis. If PT was present, then two major and one minor manifestations were enough for the diagnosis. O’Duffy11 proposed five major symptoms. They were OA, GA, SM, OM and A. The presence of OA or GA, plus two other symptoms was necessary for the diagnosis. For Cheng and Zhang (China),12 major manifestations were OA, GA, OM. Minor manifestations were SM (PF, EN, PT), A, GI, NM, epididymitis, pulmonary lesions and hematuria. The presence of two major, or one major and two minor manifestations, was required for the diagnosis.

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Diagnostic/classification criteria in BD

In the Dilsen criteria14 (Turkey) major manifestations were OA, GA, skin lesions (PF, EN), OM and thrombophlebitis. Minor manifestations were A, GI, arterial thrombosis, neuropsychiatric manifestations, CM, pleuropulmonary manifestations, epididymitis, FH and history of hyper-reactivity to needle pricks. In the Dilsen criteria, the pathergy test (PT) plays a pivotal role. If PT is positive, one major or one minor manifestation is enough to make the diagnosis. In the presence of a suspect positive PT, two major, or one major and one minor manifestation, is required for the diagnosis. If PT is negative, three major, or two major and two minor manifestations, will be necessary for the diagnosis. The revised version of the Japan criteria15 added minor manifestations to the original set of major manifestations. They were A, GI, VT, NM and epididymitis. Two minor manifestations could replace one missing major manifestation. The ISG criteria16–18 were built on 886 patients and 97 controls. For the first time, in the process of criteria-making for BD, scientific methods at their best, were used. Patients and controls were divided into two groups of training and validation samples. The criteria set was built on the training sample and the results were validated on the validation sample. To fulfill the criteria, the presence of OA was mandatory. Two of the following four items were necessary to classify a patient as having BD: GA, SM (PF, EN), OM and positive PT. The performance of the ISG criteria was very good.18 The sensitivity was 91% with the training sample, 95% with the validation sample and 92% of the entire sample. The specificity was 96%, 98% and 97%, and the relative values were 187, 193 and 189, respectively. It was interesting to compare the performance of some other criteria in the cohort of ISG patients and controls. No statistical methods were used for these comparisons, because due to the large number of patients, small percentage differences would give significant P-values, while not clinically relevant. The sensitivity, specificity and relative value of the Mason and Barnes, O’Duffy, Japan revised, Cheng and Zhang, and Dilsen criteria in the training sample were: sensitivity 86%, 80%, 92%, 98%, 93%; specificity 84%, 80%, 89%, 62%, 75%; and relative value (sensitivity + specificity) 170, 160, 181, 160, 168, respectively. ISG was classified fourth in sensitivity, first in specificity and first in relative value.18

International Journal of Rheumatic Diseases 2015

In the validation sample, sensitivity was 93%, 85%, 94%, 99%, 98%; specificity 95%, 95%, 93%, 74%, 91%; and relative value 188, 180, 187, 173, 189, respectively. ISG was classified third in sensitivity, first in specificity and first in relative value.18 The overall performance of the criteria in all patients and controls was: sensitivity 89%, 82%, 95%, 98%, 93%; specificity 89%, 87%, 81%, 67%, 91%; and relative value 178, 169, 176, 165, 184, respectively. ISG was classified fourth in sensitivity, first in specificity and first in relative value.18 For a better comparison of the performance with other studies, in other samples, instead of relative value, which was used only for ISG criteria, accuracy (percent agreement) was calculated. The accuracy in the entire group of patients and controls was, respectively, 89, 82.5, 94, 95, 93 and 92.5% for Mason and Barnes, O’Duffy, Japan revised, Cheng and Zhang, Dilsen, and ISG criteria. The optimization (100-difference between sensitivity and specificity) was respectively 100 (same sensitivity and same specificity), 95, 86, 69, 98 and 95%. Finally, the efficiency calculated as (optimization/ 100) 9 accuracy, became respectively 89, 78, 81, 66, 91 and 88%.

THE RACE FOR NEW CRITERIA When the ISG criteria were presented to the 6th International Conference on Behcet’s Disease, in Paris (1993), some concerns were formulated on its sensitivity.19 From 1990 to 2004, many studies evaluated the performance of existing diagnosis/classification criteria for BD.19–25 These studies showed that the ISG criteria had a high specificity, giving very little chance for other conditions to be erroneously classified as BD, but the price to pay was high. Many BD patients were unable to be classified by the ISG, due to its low sensitivity. Practically, one-fifth of patients were eliminated from research projects, leading to discoveries and decisions not applicable to all patients. Looking at the sensitivity of Mason and Barnes criteria, O’Duffy, Dilsen, Japan revised and ISG criteria in nine studies, the following results were obtained. In China25 ISG ranked second. In the cohorts of Iran (1993),19 APLAR series,22 Korea25 and in Iran (2004),25 ISG ranked third. In Russia,23 USA,24 India25 and Singapore,25 ISG ranked fifth. All these validation studies showed a low sensitivity of the ISG criteria (Table 1). For specificity (Table 2), ISG ranked first in Russia, first with Mason and Barnes in Iran (1993) and second in the APLAR series and Iran (2004).

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4 75 72.7 72.2 78.7 88.4

91.7 93.2 86.2 96.7 97.1

92.4 92.4 85.7 88.6 92.4

91.4

86.7

%

2000 23 105

Russia

82.3 84.8 75.6 82.9 91.5

88.4

77.4

%

2000 24 164

USA

100 80 46 90 38 84 100 80 90 72 86 96 74 88 100 96 100 100

%

2004 25 50

India

97 68 46 59.5 27 68 97 54 65 46 59.5 86.5 46 78 86.5 86.5 86.5 86.5

%

2004 25 37

Singapore

58 61 58 80

91.7

59

55

%

2004 25 1454

Korea

86 79 81

70

67

%

2004 25 98

China

99 67 51 86 64 71 93 86 87 82 92 96 83 88 97.5 94 95 89

%

2004 25 4900

Iran

98.6 79.3 85.7 86.2 82.5 83.2 96.4 86.9 87.9 82.4 88.2 94.6 84.0 90.4 96.1 94.6 96.0 94.3

%

2006 30,39,40 2556

ICBD

96.5

83.7

%

2008 30 86

Germany

94.3 60.2 84.3 63 85.8 63.8 88.6 71.4 66 65.4 67.2 86.1 65.7 84.9 87

%

2008 32 322

China

APLAR, Asia and Pacific League of Associations for Rheumatology; ICBD, International Criteria for Behcet’s Disease; ISG, International Study Group; PT, pathergy test. For more explanation on the methods, see the section ‘Performance of ICBD criteria’.

62.5

80.3

82 98 95 93 91, 95

57.9

%

1998 22 216

APLAR

74.2

%

1993 19,26 2069

Iran

89

%

Criteria/performance

Curth Mason Hewitt Japan Original Hubault and Hamza O’Duffy Cheng and Zhang Dilsen Japan revised ISG Iran Iran- Classification Tree Dilsen revised Korea ICBD ICBD Classification Tree ICBD revised ICBD revised (no PT)

1990 16–18 886

ISG

Year of publication Reference No. patients

Sets of patients

Table 1 Sensitivity of different criteria sets in different sets of patients

99.7 64.3 51.2 84.7 61.1 68.8 78.1 82.2 85.8 78.1 90.6 97.1 79.6 86.4 98.2 95.3 96.4 90.4

%

2010 33 6128

Iran

99.7 64.7 50.9 84.8 60.2 69.5 94.2 81.4 85.9 77.5 90.4 97.3 79.0 86.2 98.3 95.7 96.8 91.0

%

2013 42 7011

Iran

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Table 2 Specificity of different criteria sets in different sets of patients Sets of patients Year of publication Reference No. patients Criteria/performance Curth Mason Hewitt Japan Original Hubault and Hamza O’Duffy Cheng and Zhang Dilsen Japan revised ISG Iran Classification Tree Dilsen revised Korea ICBD ICBD Classification Tree ICBD revised ICBD revised (no PT)

ISG

Iran

APLAR

Russia

Iran

ICBD

Germany

China

Iran

Iran

1990 16–18 97

1993 19,26 1540

1998 22 145

2000 23 233

2004 25 2020

2006 30,39,40 1163

2008 30 38

2008 32 118

2010 33 3400

2013 42 5226

%

%

%

85.6 98.3 89 98.3 96.6 97.5 76.3 94.9 98.3 99.2 98.3 95.8 99.2 96.6 94.1

84.4 99.7 96.5 97.7 98.9 98.4 93.9 93.8 97.6 98.8 96.8 97.3 98.7 97.9 95.6 97.3 97.1 97.9

87.9 99.8 96.9 97.7 99.2 98.9 93.6 95.1 97.7 99.2 97.1 97.3 99.1 98.4 96.2 97.4 97.2 97.7

%

%

%

%

89

99.4

100

94.8

83 59 79 89 96, 98

97.6

97.9

87.6

89.3 96.4 97.5 94.5 95.1

95.9 98.6 99.3 97.9 97.9

91.4 91.8 100 94.8 95.7

%

%

77.4 99.6 96.0 96.9 98.1 97.5 91.5 90.4 96.8 98.0 95.3 96.1 97.9 96.5 93.6 96.1 95.7 97.0

83.2 96.1 90.2 92.4 91.5 94.6 78.3 90.9 92.0 96.0 92.3 90.3 95.8 92.9 88.7 91.8 91.2 91.5

%

89.5

73.7

APLAR, Asia and Pacific League of Associations for Rheumatology; ICBD, International Criteria for Behcet’s Disease; ISG, International Study Group; PT, pathergy test. For more explanation on the methods, see the section ‘Performance of ICBD criteria’.

For accuracy (Table 3), ISG ranked first in Russia, first with the Japan revised criteria in the APLAR Series, second with Dilsen criteria in Iran (1993) and third in Iran (2004). After the presentation of ISG in 1990, Iran presented during the International Conference of Behcet’s Disease in Paris (1993), a modified version of the ISG criteria called the Iran criteria (the traditional format).19 Iran criteria were created to overcome the low sensitivity and the low accuracy of the ISG criteria. It used the same five items as the ISG criteria (OA, GA, skin, OM, PT). The difference was that OA was no longer mandatory. Each item received one point, except OM, which obtained two points, as with the Japan criteria. Three points were necessary to reach the diagnosis.19 The sensitivity of the criteria was 96.7%, the specificity 94.5% and the accuracy 95.8%. In 1993, Iran also presented a new type of criteria, based on the Classification and Regression Tree method, called the Classification Tree.26 The criteria recognized five subsets of BD which were OA + GA, OA + skin + positive PT, OA + OM, GA + OM, and

International Journal of Rheumatic Diseases 2015

positive PT + OM. Each subset was enough to classify a patient as having BD. The sensitivity was 97.1%, the specificity 95.1% and the accuracy 96.2%. Although the classification tree had a good performance, the race on proposing new criteria with better sensitivity and better accuracy continued. Dilsen revised its original criteria27 in 2000. He proposed a simplified version of the original criteria. In the new criteria, six items are present: OA, GA, skin (PF, EN), OM, thrombophlebitis and PT. The presence of three of these would classify the patient. The last country to present its own criteria was Korea28,29 in 2003. Six items were used for the criteria: OA, GA, skin, OM, GI, PT. All items received one point, except GA which received two points. BD was diagnosed with three points or more. The sensitivity of the criteria, checked in seven tertiary medical centers in Korea29 (155 patients and 170 controls) was 94.2%, the specificity 98.1% and the accuracy 96.3%. In the same cohort of patients and controls, the ISG performance was 79.4% (sensitivity), 99.4% (specificity) and 89.8% (accuracy). For Japan revised criteria, it was 80.6%, 95.3% and 88.3%.

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F. Davatchi et al.

Table 3 Accuracy of different criteria sets in different sets of patients Sets of patients Year of publication Reference No. patients

ISG 1990 16–18 983

Criteria/performance Curth Mason Hewitt Japan Original Hubault and Hamza O’Duffy Cheng and Zhang Dilsen Japan revised ISG Iran Iran Classification Tree Dilsen revised Korea ICBD ICBD Classification Tree ICBD revised ICBD revised (no PT)

%

Iran

China

APLAR

Russia

Iran

ICBD

Germany

China

Iran

Iran

1993 19,26 3609

1996 20 114

1998 22

2000 23

2004 25 6920

2006 30,39,40 3719

2008 30 124

2008 32 440

2010 33 9528

2013 42 12237

%

%

%

%

%

%

%

%

%

93.3 78.0 63.7 89.6 74.5 80.3 92.7 88.5 91.3 87.1 93.5 96.9 87.8 91.0 97.0 95.4 96.1 92.0

93.8 84.6 68.9 88.2 69.2 86.7 90.7 88.2 89.2 86.7 89.5 93.3 87.7 91.2 93.8 93.8 94.5 93.4

92 70.2 85.6 72.2 88.7 72.4 85.3 77.6 74.4 74.2 75.3 88.7 74.4 88 88.9

94.2 76.9 67.3 89.3 74.6 79.3 93.7 86.3 90.0 85.5 92.8 97.2 86.4 90.5 97.3 96.0 96.7 93.1

89

84.9

78.9

90.8

82.5 78.5 87 91 93.5, 96.5

87.6

80.2

89.5

90.7 94.7 91 95.8 96.2

85.4 85.7 85.8 88.3 93.2

91.9 92.1 92.9 91.7 94

79.8 85.1

%

85.5

89.5

94.6 79.7 70.6 90.3 76.9 82.1 93.9 87.3 90.9 86.8 93.2 97.3 87.6 91.4 97.4 96.4 97 93.9

APLAR, Asia and Pacific League of Associations for Rheumatology; ICBD, International Criteria for Behcet’s Disease; ISG, International Study Group; PT, pathergy test. For more explanation on the methods, see the section ‘Performance of ICBD criteria’.

THE ADVENT OF THE INTERNATIONAL CRITERIA OF BEHCETS DISEASE (ICBD) In 2003 (April 2–5), the First International Workshop of Behcet’s Disease took place in Kuhtai, Austria. At the end of the Workshop, it was concluded: ‘There is a need for agreed entry criteria into clinical studies.’ Participants agreed that the ISG criteria should be used until a better/revised/updated scheme was available. Following the conclusion of the Kuhtai workshop, a preliminary team was formed from the following countries: Austria (M. Schirmer), China (Y. Dong), Egypt (S. Assaad-Khalil), Germany (Ch. Zouboulis), Iran (F. Davatchi), Italy (I. Olivieri), Morocco (S. Benamour), UK (C.G. Barnes) and USA (K. Calamia). The team had to prepare a proposal on how to evaluate and validate the ISG criteria, and in case of failure of ISG to be validated, to revise it to obtain better performing criteria. In 2004, during the 11th International Conference on Behcet’s Disease in Antalya (Turkey) the International Team for the Revision of the ISG criteria was formed by the participation of 27 countries. The coun-

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tries (in alphabetic order), and the experts were: Austria (M. Schirmer, M. Baltaci), Azerbaijan (A. Isayeva), China (Y. Dong, Z. Zhang), Egypt (S. Assaad-Khalil), France (B. Wechsler), Germany (C. Zouboulis, A. Altenburg), Greece (Ph. Kaklamani), India (A. Kumar), Iran (F. Davatchi, B. Sadeghi-Abdollahi, F. Shahram, A. Nadji, C. Chams-Davatchi, H. Shams, N. Zia’i, M. Akhlaghi, A.R. Jamshidi), Iraq (K. Sharquie, R. Hayani), Israel (Eldad Ben-Chetrit), Italy (I. Olivieri, C. Salvarani, N. Pipitone), Japan (Sh. Ohno, K. Namba), Jordan (W. Madanat), Libya (K. Elmuntaser), Morocco (S. Benamour), Pakistan (A. Ali), Portugal (J. Crespo, C. Vasconcelos, J. Correia, L. Carvalho, M. Bastos, M.J. Serra, C. Resende, F. Ramos, M. Rosa, V. Queir os, J. Vedes, C. Dias, J.V. Patto, F.P. Duarte), Russia (Z. Alekberova, A. Elonakov), Saudi Arabia (A. Al Dalaan), Singapore (C. Yew Kuang), Spain (G. Grana Gil), Taiwan (W.C. Chen), Thailand (A. Emvalee), Tunisia (H. Houman, I. Ben Ghorbel, M. Sliti-Khanfir), Turkey (A. Boyvat) and USA (K. Calamia). Patients and controls were to be selected by expert opinion, not based on a given classification/diagnosis criteria. They were to be

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Diagnostic/classification criteria in BD

consecutive patients. From March 2005 to June 2006, 2556 BD patients and 1163 control patients were gathered from these countries. The performances of existing criteria (14 sets) were checked in this cohort of internationally gathered BD and control patients. For sensitivity, the Curth criteria obtained the first rank with 98.6% and ISG the 13th rank with 82.4%.30 The difference (Diff) was 16.2%. In specificity, Mason and Barnes ranked first (96.1%) and ISG second (96%), Diff 0.1%. For accuracy, Curth criteria ranked first (93.8%) and ISG 11th (86.7%), Diff 7.1%. For optimization, Korean criteria ranked first (difference between sensitivity and specificity 2.5%) and ISG 11th (Diff 13.6%); Diff between the two sets was 11.1%. For efficiency, the Classification Tree ranked first with 89.3% and ISG 12th with 74.9%, Diff 14.4%. The validation of ISG failed and a new set of criteria was created, named the International Criteria for Behcet’s Disease (ICBD).31

HOW ICBD CRITERIA WORK? The original ICBD had two formats,32–40 the traditional format, and the Classification Tree (as with the Iran criteria19,26). The Classification Tree works the same way as the Iran Classification Tree. The items are quite the same. Here, there are again five items: OM + OA, OM + vascular lesions, OM + GA, GA + OA, and skin + OA + positive PT. Like the Iran Classification Tree, the presence of each subset was enough to classify the patient as having BD. The only difference between the two Classification Trees was the subset OM + positive PT for the Iran Classification Tree and OM + vascular lesions for ICBD. The traditional format of ICBD used six items: OA, GA, skin (PF, EN, skin aphthosis), OM, vascular manifestations (arterial and venous) and PT. All items obtained one point, except GA and OM. They were given two points each. Getting three points or more will classify the patient as having BD. In 2006, during the 12th International Conference on Behcet’s Disease (Lisbon, Portugal), the validation process30 and the new International Criteria for Behcet’s Disease (ICBD) were presented.31 The next year, in 2007, ICBD was presented to the American College of Rheumatology Congress.32 The traditional format of ICBD was then validated in Germany,33 China34 and Iran.35 The criteria were published in 2008 in the dermatology textbook, Fitzpatrick’s Dermatology in General Medicine, in the chapter on Adamantiades-Behcet’s Disease (by CC. Zouboulis).36 It was lately published in

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the last edition of Kelley’s Textbook of Rheumatology, by Kaufman.37 Both textbooks published the traditional format and the Classification Tree format of the ICBD. In 2010, in a tentative move to improve the specificity and the accuracy of the criteria, the traditional format of the ICBD was revised and presented to the 14th International Conference on Behcet’s Disease, held in London in July 2010. It was lately published, in 2013, in the Journal of the European Academy of Dermatology and Venereology (online, ahead of print), and in 2014 in printed format.38 It was validated in Italy41 and in Iran (7011 BD patients and 5226 controls)42 in 2013, the same year as the publication of the criteria. The revised ICBD has a new criterion, neurological manifestations, which gets one point. OA instead of one point, gets two points. Therefore, OA, GA, OM each gets two points. Skin, NM, vascular manifestations and positive pathergy test get each one point. Table 4 Predictive value, likelihood ratio, diagnostic odds ratio, and Youden’s Index in Iranian Patients (7011 Behcet’s patients, 5226 control patients – Reference 42) Criteria

PPV

NPV

PLR

NLR

DOR

YI

Curth Mason Hewitt Japan original Hubault and Hamza O’Duffy Zhang Dilsen Japan revised ISG Iran Iran Classification Tree Dilsen revised Korea ICBD ICBD revised ICBD revised (no PT) ICBD Classification Tree

89.1 99.7 94.3 97.4

99.7 73.9 66.4 86.6

8.2 323 16.4 36.9

0 0.35 0.51 0.16

2392 915 32 237

0.88 0.64 0.48 0.82

98.7

71.4

75.2

0.40

188

0.59

98.4 93.6 94.3 97.4 99.0 96.9 97.3

76.4 94.2 83.6 87.4 81.5 91.0 97.3

63.2 14.7 16.6 37.3 96.9 31.2 36.0

0.31 0.06 0.20 0.14 0.23 0.10 0.03

205 238 84.9 259 427 315 1299

0.68 0.88 0.76 0.84 0.77 0.88 0.95

98.9 98.2 96.3 97.2 97.5

82.5 87.7 98.3 96.8 91.6

87.8 53.9 25.9 34.6 39.6

0.21 0.14 0.02 0.03 0.09

414 384 1464 1050 429

0.78 0.85 0.94 0.94 0.89

97.4

95.8

36.8

0.04

834

0.93

DOR, diagnostic odds ratio; NLR, negative likelihood ratio; NPV, negative predictive value; PLR, positive likelihood ratio; PPV, positive predictive value; PT, pathergy test; YI, Youden’s Index. For more explanation on the methods, see the section ‘Performance of ICBD criteria’.

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Getting four points or more will classify the patient as having BD. It is interesting to look at why no other criteria set, after the ISG criteria, did not use the OA criterion as mandatory. In 2010, a review showed the lack of OA in 1–10% of Behcet’s patients in the reports of 14 countries.43 The absence of OA was even much higher at the beginning of the disease,20,44,45 from 18% to 22%.

centage (number of diagnosed BD patients multiplied by 100, and the result divided by the total number of BD patients). Table 1 shows the sensitivity of different criteria in different studies.17–20, 26–29, 31, 34–36, 39, 42 Specificity is the number of non-BD patients, correctly recognized as not having BD. It is expressed by percentage (number of non-BD patients, correctly recognized as not having BD, multiplied by 100, and then divided by the total number of non-BD patients). Table 2 shows the specificity of different criteria in different studies.17–20, 26–27, 29, 31, 34–36, 39, 42 Accuracy or percent agreement, is a combination of sensitivity and specificity. The formula is the number of diagnosed BD + non-BD (correctly diagnosed as not having BD), multiplied by 100, and the result divided by the sum of the total number of BD and non-BD patients. Table 3 shows the accuracy of different criteria in different studies.17–20, 24, 26–27, 29, 31, 34–36, 39, 42 The positive predictive value (PPV) calculates how much will be the probability of a positive test to be a true positive. The negative predictive value (NPV) calculates how much will be the probability of a negative test to be a true negative. The prevalence of the disease, in

PERFORMANCE OF ICBD CRITERIA Many ways can be used to evaluate the performance of a criteria set. The most commonly used are sensitivity, specificity and accuracy (percent agreement). Other methods are positive predictive value (PPV), negative predictive value (NPV), positive likelihood ratio (PLR), negative likelihood ratio (NLR), diagnostic odds ratio (DOR) and Youden’s index (YI).46–49 We personally use two other parameters: optimization and the ffficiency of the criteria. Sensitivity is the number of BD patients correctly classified (diagnosed) by the criteria. It is expressed as perTable 5 Diagnostic odds ratio in different sets of patients Sets of patients Year of publication Reference No. patients Criteria/performance Curth Mason Hewitt Japan Original Hubault and Hamza O’Duffy Cheng and Zhang Dilsen Japan revised ISG Iran Iran Classification Tree Dilsen revised Korea ICBD ICBD Classification Tree ICBD revised ICBD revised (no PT)

ISG 1990 16–18 983 % 65

22 71 71 107 243, 931

Iran

APLAR

Russia

Iran

ICBD

1998 22 361

2000 23 338

2004 25 6920

2006 30, 39, 40 3719

%

%

%

%

%

476

1374

119

166

78

75

92 367 244 503 650

70 188 368 172 355

129 136 5987 142 271

339 506 25 192 92 95 143 62 202 223 233 591 228 202 570 386 423 262

349 94 55 76 51 87 97 66 84 112 90 163 120 123 193 196 249 178

1993 19, 26 3609

Germany

China

Iran

Iran

2008 30 124

2008 32 440

2010 33 9528

2013 42 12237

%

%

%

1798 599 29 235 141 136 55 70 246 294 292 1207 296 296 1185 731 897 439

2414 915 32 237 188 205 238 85 259 427 315 1299 414 384 1464 834 1050 430

%

44

77

98 87 43 98 172 69 25 46 112 234 118 141 238 160 107

APLAR, Asia and Pacific League of Associations for Rheumatology; ICBD, International Criteria for Behcet’s Disease; ISG, International Study Group; PT, pathergy test. For more explanation on the methods, see the section ‘Performance of ICBD criteria’.

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Diagnostic/classification criteria in BD

Table 6 Youden’s index in different sets of patients Sets of patients Year of publication Reference No. patients Criteria/performance Curth Mason Hewitt Japan Original Hubault and Hamza O’Duffy Cheng and Zhang Dilsen Japan revised ISG Iran Iran Classification Tree Dilsen revised Korea ICBD ICBD Classification Tree ICBD revised ICBD revised (no PT)

ISG

APLAR

Russia

Iran

ICBD

1998 22 361

2000 23 338

2004 25 6920

2006 30,39,40 3719

%

%

%

%

%

0.78

0.74

0.58

0.81

0.65 0.57 0.74 0.82 0.87, 0.93

0.78

0.60

0.79

0.81 0.90 0.84 0.91 0.92

0.71 0.71 0.71 0.77 0.86

0.84 0.84 0.86 0.83 0.88

0.76 0.67 0.47 0.83 0.62 0.69 0.85 0.76 0.84 0.80 0.87 0.92 0.81 0.85 0.91 0.90 0.91 0.86

0.82 0.75 0.76 0.79 0.74 0.78 0.75 0.78 0.80 0.78 0.81 0.85 0.80 0.83 0.85 0.86 0.87 0.86

1990 16–18 983 %

Iran 1993 19,26 3609

Germany

China

Iran

Iran

2008 30 124

2008 32 440

2010 33 9528

2013 42 12237

%

%

%

0.80 0.59 0.73 0.61 0.82 0.61 0.65 0.66 0.64 0.65 0.65 0.82 0.65 0.81 0.81

0.84 0.64 0.48 0.82 0.60 0.67 0.72 0.76 0.83 0.77 0.87 0.94 0.78 0.84 0.94 0.93 0.94 0.88

0.88 0.64 0.48 0.82 0.59 0.68 0.88 0.76 0.84 0.77 0.88 0.95 0.78 0.85 0.94 0.93 0.94 0.89

%

0.73

0.70

APLAR, Asia and Pacific League of Associations for Rheumatology; ICBD, International Criteria for Behcet’s Disease; ISG, International Study Group; PT, pathergy test. For more explanation on the methods, see the section ‘Performance of ICBD criteria’.

the studied population, affects the value of PPV and NPV. Table 4 shows the results. The likelihood ratio (LR) gives the odds of having or not having the disease depending on positive or negative values. The prevalence of the disease does not affect the values of LR. Therefore, the results of LR may be utilized anywhere. PLR calculates the odds of having the disease, while the NLR the odds of not having the disease. A PLR superior to 5 shows the ability of a positive test to confirm the disease. A NLR inferior to 0.20 shows the ability of a negative test to refute the disease (Table 4). The DOR is the combination of PLR and NLR; a value of 1 means the criteria do not discriminate between patients and controls. Higher values are synonymous of better discrimination (Tables 4 and 5). YI is a simple way of combining sensitivity and specificity. YI demonstrates in a way the precision of the diagnosis criteria. The lowest figure is 0 and the highest 1. The more the result approaches 1, the more the criteria set is performing (Tables 4 and 6). Optimization is the difference between sensitivity and specificity. A value of zero shows the ability of the criteria set to recognize with the same performance

International Journal of Rheumatic Diseases 2015

both BD patients and non-BD patients. The ideal will be a value of zero. Efficiency takes into account the accuracy (sensitivity and specificity) and the optimization. It can be calculated from the formula: 100-optimization, divided by 100, and the result multiplied by accuracy. Table 4 shows the PPV, NPV, PLR, NLR, DOR and YI calculated on the BD registry of the Rheumatology Research Center, Tehran University of Medical Sciences (7040 patients and 5300 controls).42 Table 5 demonstrates the DOR of different sets of patients with different criteria sets. Table 6 demonstrates the YI of different sets of patients with different criteria sets. Overall the five most sensitive criteria on the ICBD (2556 patients) were Curth with 98.6%, Cheng and Zhang 96.4%, ICBD 96.1%, ICBD revised 96%, and ICBD Classification Tree and Iran Classification Tree with equal value at 94.6%. The most sensitive criteria in Iranian patients (cohort of 7011 patients) were Curth with 99.7%, ICBD 98.3%, Iran Classification Tree 97.3%, ICBD revised 96.8%, and ICBD Classification Tree with 95.7% (Table 1).

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The five most specific criteria on the ICBD (1163 patients) were Mason with 96.1%, ISG 96%, Dilsen revised 95.8%, O’Duffy 94.6% and Korea with 92.9%. The revised ICBD ranked 10th with 91.2%. The most specific criteria for Iranian patients (cohort of 5226 patients) were Mason with 99.7%, ISG 98.8%, Dilsen revised 98.7%, O’Duffy 98.9% and Korea 97.9%. The ICBD Classification Tree ranked seventh with 97.4% and revised ICBD ninth with 97.2% (Table 2). The five most accurate criteria on the ICBD (3719 patients) were ICBD revised 94.5%, ICBD 93.8%, ICBD Classification Tree 93.8%, Curth 93.8% and Iran Classification Tree 93.3%. ISG ranked 15th with 86.7%. The most accurate criteria in Iranian patients (cohort of 12237 patients) were ICBD 97.4%, Iran Classification Tree 97.3%, ICBD revised 97%, ICBD Classification Tree 96.4% and Curth 94.6%. ISG ranked 13th with 86.8% (Table 3). The five most optimized criteria on the ICBD (3719 patients) were Korea 2.5%, Dilsen 4%, Iran 4.1%, Japan revised 4.1% and Classification Tree 4.3%. Revised ICBD ranked seventh (4.8%), original ICBD ninth (7.4%), and ISG 13th (13.6%). The five most optimized criteria in Iranian patients (cohort of 12 237 patients) were Classification Tree 0.2%, Cheng and Zhang 0.3%, ICBD revised 0.4%, ICBD 0.6% and Iran 6.2%. ISG ranked 14th with an optimization of 20.7%. The five most efficient criteria on the ICBD (3719 patients) were revised ICBD 90.0%, Classification Tree 89.3%, Korea 88.9%, ICBD 86.9% and Iran 85.8%. ISG ranked 14th (74.9%). The five most efficient criteria in Iranian patients (cohort of 12 237 patients) where Classification Tree 97%, revised ICBD 96.6%, ICBD 94.8%, Cheng and Zhang 93.4% and Iran 87%. ISG ranked 12th with an efficiency of 67.8%.

CONCLUSION During the past 68 years and among the 17 sets of criteria, the most used were the O’Duffy criteria, the Japan criteria, the Dilsen criteria, the ISG and finally the ICBD criteria. Among the 17 sets of criteria only the ISG and the ICBD criteria were international criteria, made by the collaboration of several countries. It is the reason why, since 1990, ISG became the most cited criteria. However, ISG criteria having a very good specificity, lacks good sensitivity and accuracy. In contrast, ICBD has much better sensitivity (97% vs. 77.5%), a little less

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specificity (97% vs. 99%) and a better accuracy (97% vs. 87%). Of course, without several validation studies, from different countries, the above conclusions may not be true. This is what happened with the ISG criteria. Future validation studies will show if the ICBD criteria needs a new revision or not. As some experts think that the clinical picture of BD may be changing, it would be interesting in future studies to compare the performance of the criteria in patients diagnosed in the past with patients diagnosed in recent times. Perhaps a new revision would be necessary in the future. However, for now, it seems that both the original ICBD, and the revised ICBD, are actually the best performing criteria, and the ones that should be used for classification or for diagnosis.

CONFLICT OF INTEREST None.

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26 Davatchi F, Shahram F, Akbarian M et al. (1993) Classification Tree for the diagnosis of Behcet’s Disease. In: Wechsler B, Godeau P (eds), Behcet’s Disease, pp 245–8. Excerpta Medica International Congress Series 1037, Amsterdam. 27 Dilsen N (2000). About diagnostic criteria for Behcet’s Disease: our new proposal. In: Bang D, Lee ES, Lee S (eds) Behcet’s Disease, pp 101–4. Design Mecca Publishing Co., Seoul. 28 Chang HK, Kim SY (2003) Survey and validation of the criteria for Behcet’s Disease recently used in Korea: a suggestion for modification of the International Criteria. J Korean Med Sci 18, 88–92. 29 Chang HK, Lee SS, Bai HJ et al. (2004) Validation of the classification criteria commonly used in Korea and a modified set of preliminary criteria for Behcet’s Disease: a multi-center study. Clin Exp Rheumatol 22 (Suppl. 34), S21–6. 30 International Team for the Revision of the International Criteria for Behcet’s Disease (2006) Evaluation of the International Criteria for Behcet’s Disease (ICBD). Clin Exp Rheumatol 24 (Suppl. 42), S13. 31 International Team for the Revision of the International Criteria for Behcet’s Disease (2006) Revision of the International Criteria for Behcet’s Disease (ICBD). Clin Exp Rheumatol 24 (Suppl. 42), S14–5. 32 Davatchi F, Schirmer M, Zouboulis C, Assad-Khalil S, Calamia KT, on behalf International Team for the Revision of the International Criteria for Behcet’s Disease (2007) Evaluation and Revision of the International Study Group Criteria for Behcßet’s Disease. American College of Rheumatology Meeting, Boston, MA, USA, November 2007, abstract 1233. 33 Altenburg A, Bonitsis NG, Papoutsis N, Pasak M, Krause L, Zouboulis CC (2008) Evaluation of diagnostic criteria including ICBD (2006) in Adamantiades-Behcet’s Disease patients in Germany. Clin Exp Rheumatol 26 (Suppl 50), S3. 34 Zhang Z, Zhou W, Hao Y, Wang Y, Dong Y (2008) Validation of the International Criteria for Behcet’s Disease (ICBD) in China. Clin Exp Rheumatol 26 (Suppl 50), S6–7. 35 Davatchi F, Sadegh Abdollahi B, Shahram F et al. (2010) Validation of the International Criteria for Behcet’s Disease in Iran. Int J Rheum Dis 13, 55–60. 36 Zouboulis CC (2008). Adamantiades-Behcet’s Disease. In: Wolf K, Goldsmith LA, Katz SI, Gilchrest BA, Paller AS, Leffell DJ (eds) Fitzpatrick’s Dermatology in General Medicine. 7th edn, pp 1620–6. McGraw-Hill Companies, New York. 37 Kaufman WS, Kaufman Macnamara E, Jorizzo JL (2013). Behcet’s Disease. In: Firestein GS, Budd RC, Gabriel SE, McInnes IB, O’Dell JR (eds) Kelley’s Textbook of Rheumatology. 9th edn, pp 1525–32. Elsevier Saunders, Philadelphia. 38 International Team for the Revision of the International Criteria for Behcßet’s Disease (ITR-ICBD): Davatchi F,

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International Journal of Rheumatic Diseases 2015

classification criteria in Behcet's disease.

There are 17 sets of diagnosis/classification criteria for Behcet's disease: Curth (1946), Hewitt (1969), Mason (1971), Japan (1972), Hubault (1974), ...
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