ORIGINAL ARTICLE
Incidence of discordant temporal artery biopsy in the diagnosis of giant cell arteritis Bethany Durling, MD,* Andrew Toren, MD,† Vivek Patel, MD,‡ Steven Gilberg, MD,§ Ezekiel Weis, MD, MPH,¶ David Jordan, MD§ ABSTRACT ● RÉSUMÉ Objective: We investigated the rate of discordant biopsy results (i.e., 1 side negative, 1 side positive) in patients who underwent initial bilateral temporal artery biopsies for suspected giant cell arteritis (GCA). Design: A cohort study. Participants: Consecutive patients undergoing temporal artery biopsy were enrolled. Of the 259 patients enrolled, 250 underwent initial bilateral temporal artery biopsies. Methods: Positive biopsies were defined based on accepted histologic definitions. Healed arteritis was considered a positive result. Clinical information was collected for all patients using a questionnaire administered by an ophthalmologist. Pathology results, including biopsy length (as measured by the pathologist), and laboratory information (i.e., serum erythrocyte sedimentation rate [ESR] and C-reactive protein [CRP] levels) were collected from digital patient records for statistical analysis. The main outcome was the rate of discordant biopsy in consecutive patients who underwent initial bilateral temporal artery biopsy. Results: Giant cell arteritis was confirmed in 62 (24.2%) of the 250 patients, including 3 patients with biopsies recorded as healed arteritis. The rate of discordant biopsy was 4.4% with 11 unilaterally positive biopsies. There was no statistical difference between the length of the left- and right-sided biopsies in either the unilaterally or bilaterally positive groups (p ¼ 0.13 and p ¼ 0.79, respectively). The average maximum ESR value for the bilateral group (58.7 mm/h) was significantly higher than the average maximum ESR value for the unilateral group (30.7 mm/h, p ¼ 0.03). The average maximum CRP value for the bilateral group was 59.2 mg/L and 28.6 mg/L for the unilateral group (p ¼ 0.30). Discordance between the localization of symptoms and the side of positive biopsy occurred in 3 patients (i.e., 3 patients had left-sided symptoms only, yet a right-sided positive biopsy). Conclusions: The rate of discordant biopsies in patients who underwent initial bilateral temporal artery biopsies was considerable in our patient cohort. Given this reasonably high rate of discordance between sides, as well as the lack of correlation between side of positivity and laterality of presenting symptoms, we recommend initial bilateral temporal artery biopsies to enhance the diagnostic certainty of the disease. Objet : Nous avons examiné l’incidence de résultats de biopsie discordante (i.e. un côté positif et l’autre négatif) chez les patients qui ont subi une première biopsie bilatérale temporale pour un soupçon d’artérite à cellules géantes (ACG). Nature : Étude prospective de cohorte. Participants : En tout, 259 patients consécutifs ayant subi une biopsie de l’artère temporale ont été inscrits. Parmi eux, 250 ont subi une biopsie initiale bilatérale des artères temporales. Méthodes : La définition des biopsies positives était fondée sur les définitions histologiques acceptées et la guérison de l’artérite était considérée comme résultat positif. L’information clinique a été recueillie pour tous les patients à l’aide d’un questionnaire administré par un ophtalmologiste. Les résultats concernant la pathologie, comprenant la longueur de la biopsie (mesurée par le pathologiste) et l’information du laboratoire (i.e. les taux de sédimentation érythrocytaire [TSE] du sérum et les niveaux de protéines C-réactives (PCR)) a été puisée dans les dossiers médicaux numériques pour l’analyse statistique. Principaux résultats : Le principal résultat obtenu a été l’incidence de biopsie discordante chez les patients consécutifs qui avaient subi une biopsie initiale bilatérale des artères temporales. Résultats : L’ACG a été confirmée chez 62 des 250 patients (24,2 %), y compris 3 patients avec des biopsies enregistrées comme artérite guérie. Le taux de biopsies discordantes était de 4,4 % avec 11 biopsies unilatéralement positives. Il n’y avait pas de différence statistique entre les longueurs des biopsies de droite et de gauche chez les groupes unilatéralement ou bilatéralement positifs (p = 0,13 et p = 0,79 respectivement). Dans le groupe unilatéralement positif, la longueur moyenne post-fixation du côté de la biopsie positive était de 1,18 cm. Cela différait peu du côté de la biopsie négative qui était de 1,17 cm (p = 0,95). La moyenne de la valeur maximale du TSE dans le groupe bilatéral (58,7 mm/h) était significativement plus élevée que celle du groupe unilatéral (30,7 mm/h, p = 0,03). La moyenne de la valeur maximale du PCR du groupe bilatéral était 59.2mg/l et 28,6mg/l pour le groupe unilatéral (p = 0,30). Le pourcentage des patients prenant des stéroïdes oraux au moment de la biopsie était 76 % et 73 % (p = 1,00) dans chacun des groupes, bilatéral et unilatéral, respectivement. Conclusion : L’incidence de biopsies discordantes chez les patients qui subissaient une biopsie initiale bilatérale des artères temporales était considérable dans notre cohorte de patients. L’incidence n’était pas liée à la longueur de la biopsie, ni à l’utilisation de stéroïdes ni au niveau du PCR dans le sérum. Le TSE élevé de sérum était associé aux résultats bilatéralement positifs de la biopsie. Nous recommandons des biopsies initiales bilatérales des artères temporales pour réduire le risque de diagnostiquer à tort une artérite à cellules géantes, vu le taux raisonnablement élevé de désaccord entre les côtés et le manque de corrélation entre le côté de la positivité et la latéralité de la présentation des symptômes discordants.
From the *Department of Ophthalmology and Visual Sciences, Dalhousie University, Halifax, N.S.; †Department of Ophthalmology, Hôpital du Saint Sacrement, Université Laval, Québec, Qué.; ‡Department of Ophthalmology, Wilmer Eye Institute, Johns Hopkins University School of Medicine, Baltimore, Md.; §Department of Ophthalmology, University of Ottawa Eye Institute, Ottawa, Ont.; ¶Department of Ophthalmology, University of Alberta, Edmonton, Alta. Presented at the Canadian Ophthalmological Society Meeting (3rd prize: Canadian Ophthalmological Society Award for Excellence in Research), in Vancouver, B.C., Jun. 9 to 12, 2011.
Originally received Sep. 10, 2013. Final revision Nov. 23, 2013. Accepted Jan. 3, 2014 Correspondence to: David. R. Jordan, MD, 301 O’Connor Street, Ottawa ON K2P1V6.; [email protected] Can J Ophthalmol 2014;49:157–161 0008-4182/14/$-see front matter & 2014 Canadian Ophthalmological Society. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jcjo.2013.12.008
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Temporal arteritis—Durling et al. The timely and definitive diagnosis of giant cell arteritis (GCA) is important to manage morbidity from the disease or from treatment with high-dose corticosteroids.1–5 The diagnosis of GCA is suspected based on the presence of clinical features and serum inflammatory markers,6–9 and is confirmed with a temporal artery biopsy (TAB). TAB is the histologic gold standard to confirm suspected GCA and requires both an adequate length of specimen10 and evaluation in thin sections by an experienced pathologist.11 A biopsy-confirmed diagnosis is made based on the presence of characteristic histologic changes in the artery wall.12 These changes may be unevenly distributed (i.e., skip lesions), and biopsy samples of the unaffected temporal artery segment may produce a false-negative result.13–15 False-negative TAB rates have been reported in 10% to 20% of patients with GCA.15–18 False-negative, unilateral biopsy results subsequently shown to be positive on the contralateral side suggest that performing bilateral initial biopsy may be beneficial to enhance the diagnostic certainty. We report our experience with bilateral initial temporal artery biopsies.
METHODS All patients who were referred to the oculoplastic or neuroophthalmology service for TAB between 2007 and 2010 were invited to participate in the study. Informed consent was obtained from each patient before enrollment and TAB. Consecutive patients were enrolled and had bilateral temporal artery biopsies performed during the same operating room procedure time (i.e., simultaneous). Clinical information, including features associated with GCA, was collected preoperatively using a questionnaire administered by the ophthalmologist. In addition, serum hemoglobin, platelets, erythrocyte sedimentation rate (ESR), and C-reactive protein (CRP) levels were collected from referral information and digital patient records. Westergren’s ESR method and highly sensitive CRP assays were used in all biochemical laboratories. An in vivo biopsy length of at least 20 mm per side was the goal for all patients. Biopsy specimens were reviewed by an experienced pathologist and/or ophthalmic pathologist using the procedures outlined by Gooi et al.11 Healed arteritis was considered a positive result. These pathology results, including biopsy length (as measured by the pathologist), were collected from digital patient records for statistical analysis. Any patients who underwent a unilateral biopsy, or from whom bilateral biopsy results were not available, were excluded from our analysis. Approval from the Ottawa Hospital Ethics Committee was obtained for the study. The primary objective was to determine the rate of discordant biopsy in consecutive patients who underwent initial bilateral TAB. Descriptive data are presented as counts, percentages, and means (⫾ SD). Categorical variables were analyzed using Fisher’s exact and χ2 tests. Normally distributed
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continuous variables were analyzed with a Student t test, and nonparametric variables were analyzed using Wilcoxon rank sums. The ESR measured in millimeters per hour was graded as normal or elevated based on 2 validated formulas from Miller et al.19 and Hayreh et al.20 The range of normal CRP level varies from laboratory to laboratory. For our study, the value was graded as normal based on the established range of r8 mg/L at the Ottawa Hospital laboratory. All statistical tests were 2-tailed. Factors were considered statistically significant at a significance level less than 0.05. Statistical analysis was performed using Excel for Mac (Microsoft, v12.2.7)
RESULTS Of the 259 consecutive patients enrolled, 250 who had initial bilateral temporal artery biopsies were included (Table 1). GCA was confirmed in 62 (24.2%) of these patients, including 3 patients with biopsies recorded as healed arteritis. The rate of discordant biopsy was 4.4% with 11 unilaterally positive biopsies. There were 11 (100%) females in the unilaterally positive biopsy group and 41 (83%) females in the bilaterally positive biopsy group (p ¼ 0.19). The average age of patients in the unilateral and bilateral groups was 74.0 ⫾ 8.1 and 77.4 ⫾ 8.2 years, respectively (p ¼ 0.24). Whenever possible, laboratory values including ESR, CPR, hemoglobin, and platelet levels were collected before and after patients started steroid treatment (Table 2). The percentage of patients on oral steroids at the time of biopsy was 73% of the unilateral group and 76% of the bilateral group (p ¼ 1.00). The average maximum ESR value for the bilateral group (58.7 mm/h) was significantly higher than the average maximum ESR value for the unilateral group (30.7 mm/h, p ¼ 0.03). The average maximum CRP value for the bilateral group was 59.2, and 28.6 mg/L for the unilateral group (p ¼ 0.30). The platelet and hemoglobin levels were not significantly different before and after steroids in the respective groups. The length of the left- and right-sided biopsies in the total biopsy-positive population was not statistically different (p ¼ 0.59). In the unilaterally positive group, the average length of the biopsy-positive side was 1.18 cm. This was not significantly different from the biopsy-negative side, which was 1.17 cm (p ¼ 0.95). All recorded lengths are postfixation. Table 1—Descriptive data
No. of patients Female sex, n (%) Age ⫾ SD, y On steroids, n (%)*
All Positive Biopsies
Unilateral Biopsies
Bilateral Biopsies
62 52 (84) 76.8 ⫾ 8.2 47 (76)
11 11 (100) 74.0 ⫾ 8.1 8 (73)
51 41 (83) 77.4 ⫾ 8.2 39 (76)
*Patients on steroid therapy at time of initial blood work.
p
0.19 0.24 1
Temporal arteritis—Durling et al. Table 2—Laboratory markers according to biopsy results
Highest measurements before biopsy Mean ESR ⫾ SD (mm/h) Mean CRP ⫾ SD (mg/L) On steroids, n Before steroids* Mean ESR ⫾ SD (mm/h) Mean CRP ⫾ SD (mg/L) After steroids* Mean ESR ⫾ SD (mm/h) Mean CRP ⫾ SD (mg/L) Miller ESR elevated,† n Hayreh ESR elevated,† n CRP 4 8.0, n Mean biopsy length ⫾ SD: right sided, cm Mean biopsy length ⫾ SD: left sided, cm Mean combined biopsy length ⫾ SD, cm
All Positive Biopsies (n)
Unilateral Biopsies (n)
Bilateral Biopsies (n)
p
57.9 ⫾ 35.6 (47) 56.2 ⫾ 80.0 (43) 47
30.7 ⫾ 25.2 (9) 28.6 ⫾ 44.4 (8) 8
64.3 ⫾ 34.9 (38) 62.5 ⫾ 84.3 (35) 39
0.30 0.03 1
56.9 ⫾ 32.4 (40) 65.9 ⫾ 87.9 (33)
38.2 ⫾ 27.9 (7) 42.5 ⫾ 52.3 (5)
59.7 ⫾ 32.3 (33) 66.1 ⫾ 91.2 (28)
0.13 0.58
42.9 ⫾ 42.4 (30) 32.8 ⫾ 46.9 (28) 41 44 46 1.25 ⫾ 0.36 1.29 ⫾ 0.40 2.68 ⫾ 0.99
12.2 ⫾ 8.6 (7) 4.3 ⫾ 2.8 (7) 5 4 7 1.23 ⫾ 0.29 1.13 ⫾ 0.36 2.9⫾ 1.84
49.5 ⫾ 43.9 (23) 38.2 ⫾ 49.5 (21) 36 40 39 1.26 ⫾ 0.38 1.33 ⫾ 0.40 2.63⫾ 0.70
0.07 0.19 0.16 0.01 0.45 0.79 0.13 0.39
ESR, erythrocyte sedimentation rate; CRP, C-reactive protein. *Groups are not mutually exclusive; some patients had blood work performed both before and after initiation of steroids. †Two formulas for determining cutoff for elevated ESR in patients suspected of temporal arteritis.
There were no observed cases of infection, unusual bleeding, or seventh nerve injury relating to the biopsy. There were 11 unilaterally positive biopsies, representing 17.7% of the total biopsy positive group and 4.4% of the total biopsy population. Of the 11 patients with unilaterally positive biopsy, 4 had right-sided symptoms, 4 had left-sided symptoms, and 3 had bilateral or systemic symptoms (Table 3). Discordance between the localization of symptoms and the side of positive biopsy occurred in 3 patients (i.e., 3 patients had left-sided symptoms, yet a positive right-sided biopsy).
DISCUSSION The sensitivity of TAB is less than 100%,21 with sensitivities reported between 65% and 95%.21–23 This
decreased sensitivity is, in part, due to the nonuniform involvement of the diseased arteries resulting in skip lesions.13,15,24 Small-artery samples taken from 1 temporal artery may result in a falsely negative biopsy. It is generally agreed that longer specimens taken from multiple sections are preferable and may increase the sensitivity.10,13,22,25,26 Biopsies greater than 10 mm have been reported to increase the diagnostic yield but ideally should be greater than 20 mm (postfixation).10,13,27 A 20-mm postfixation specimen length is generally accepted as the minimal amount necessary for adequate histopathological study.10 In this study, the surgeons aimed to take samples greater than 20 mm, but in most instances, after accounting for shrinkage, they were less than 20 mm. The current practice of TAB among clinicians varies considerably among unilateral, sequential bilateral, and initial bilateral biopsies. In a recent study of clinical
Table 3—Presenting patient characteristics of those with discordant biopsies Postfixation Biopsy Length (cm) Patient No. 1 2 3 4 5 6
7 8 9 10 11
Signs/Symptoms Headache, jaw claudication, TA pain, abnormal TA pulse, neck/shoulder pain, weight loss, fever Headache, scalp tenderness, weight loss, anorexia, myalgias, fatigue Headache, scalp tenderness, permanent diplopia, neck/shoulder pain, weight loss, anorexia, myalgia, arthralgia, fatigue Headache, scalp tenderness, neck/shoulder pain, anorexia, malaise, arthralgia Jaw claudication Headache, jaw claudication, scalp tenderness, temporal artery pain, permanent vision loss, neck/shoulder pain, anorexia, fatigue Headache, transient vision loss, myalgia, arthralgia, fatigue Headache, permanent vision loss Headache, permanent vision loss, arthralgia Headache, scalp tenderness, neck/shoulder pain, arthralgia Headache, scalp tenderness, neck/shoulder pain, anorexia, fatigue
CRP (mg/L) ESR (mm/h) Steroids* Right Side Left Side
Biopsy Result
152
18
Yes
1.4
1.2
Right-sided active arteritis
126
83
No
1.0
1.5
Right-sided active arteritis
6.5
21
No
1.0
0.7
Right-sided active arteritis
7.7
24
Yes
0.8
0.7
Right-sided active arteritis
NA NA
NA NA
Yes Yes
1.1 1.6
1.1 0.9
Right-sided active arteritis Right-sided active arteritis
8.7 8.8 5.4 2.9 62.7
12 18 35 5 60
Yes Yes Yes Yes No
1.5 1.1 1.3 1.7 1.0
1.1 1.7 1.6 1.2 0.7
Right-sided active arteritis Right-sided active arteritis Left-sided healed arteritis Left-sided active arteritis Left-sided active arteritis
ESR, erythrocyte sedimentation rate; CRP, C-reactive protein; TA, temporal artery. *Indicates whether patients were on steroid therapy at time of initial blood work shown.
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Temporal arteritis—Durling et al. practice patterns, 66% preferred initial unilateral biopsy, 18% preferred initial bilateral biopsy, whereas the remaining 16% performed either unilateral or bilateral depending on the clinical suspicion.28 The literature supports both initial bilateral, sequential bilateral (second biopsy done based on frozen section results of first biopsy), and unilateral temporal artery biopsies.15,29,30 Some research suggests that the biopsy discordance rate is not high enough to justify bilateral biopsies,31 whereas other research suggests that bilateral biopsies, including initial and sequential, improves diagnostic yield in at least 3% of cases32 and is 5% more likely to detect histopathologic findings on biopsy.30 We favour initial bilateral biopsies because some research suggests false-negative results may occur with frozen sectioning—a standard technique used for “sequential” temporal artery biopsies.15,29 In this study, initial bilateral biopsy contributed to the diagnosis in 11 unilaterally positive cases. The rate of discordant biopsy in the total study population was 4.4% and 17% in the biopsy-positive group, which is consistent with rates reported previously in the literature.18,30 There were several instances where patients had bilateral or nonlocalizing symptoms with a unilaterally positive biopsy result. Our patient population also included 3 patients who had a positive biopsy on the contralateral side of their symptoms. Based on our results, we believe it is important to perform initial bilateral temporal artery biopsies to enhance diagnostic certainty. Limited follow-up by the surgeons in the study may underestimate potential complications of the biopsy. The referring physician followed the majority of patients after the biopsy. These patients were all given specific instructions to call and/or return if they had any concerns. Only 2 patients in follow-up returned for temporary minor irritation related to the incision. There are also several practical reasons for considering initial bilateral temporal artery biopsies. Doing the biopsies one right after the other takes little additional surgical time and maximizes the efficient use of the procedure area. The same instruments and accessories (bipolar cautery, drapes, sponges, sutures, etc.) may be used. Travel time is reduced for the patient, because there is only 1 operative procedure rather than 2. Although no study has investigated the cost-effectiveness of initial versus sequential bilateral biopsy, we suspect that initial bilateral biopsies would be more efficacious. Potential limitations of this investigation include partial patient laboratory data and biopsy length. For some patients, blood work before the commencement of steroids treatment was not available, because some patients had been started on steroids before referral and enrolment in the study. Although this study population was large when compared with other work investigating patients with GCA, this sample size has limited statistical power. Furthermore, a postfixation length of 20 mm is generally recognized as the minimal amount necessary for adequate histopathologic study.10 Although all
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surgeons attempted to obtain an in vivo sample greater than 20 mm, a postfixation length of 20 mm was not obtained in all patients. In addition, factors related to the study design— observational cohort design—are limiting. However, these limitations are applied evenly across both groups that are compared in this study.
Disclosure: The authors have no proprietary or commercial interest in any materials discussed in this article. REFERENCES 1. Andersson R. Giant cell arteritis as a cause of death. Clin Exp Rheumatol. 2000;18(4 Suppl. 20):S27-8. 2. Chew SS, Kerr NM, Danesh-Meyer HV. Giant cell arteritis. J Clin Neurosci. 2009;16:1263-8. 3. Font C, Cid MC, Coll-Vinent B, Lopez-Soto A, Grau JM. Clinical features in patients with permanent visual loss due to biopsy-proven giant cell arteritis. Br J Rheumatol. 1997;36:251-4. 4. Hall J. Giant-cell arteritis. Curr Opin Ophthalmol. 2008;19:454-60. 5. Miller NR, Newman NJ, Biousse V, Kerrison JB. Walsh and Hoyt’s Clinical Neuro-ophthalmology. 5th ed. Philadelphia, Pa.: Lippincott Williams & Wilkins; 1998. 6. Hayreh SS, Podhajsky PA, Zimmerman B. Ocular manifestations of giant cell arteritis. Am J Ophthalmol. 1998;125:509-20. 7. Parikh M, Miller NR, Lee AG, et al. Prevalence of a normal C-reactive protein with an elevated erythrocyte sedimentation rate in biopsy-proven giant cell arteritis. Ophthalmology. 2006;113:1842-5. 8. Costello F, Zimmerman MB, Podhajsky PA, Hayreh SS. Role of thrombocytosis in diagnosis of giant cell arteritis and differentiation of arteritic from non-arteritic anterior ischemic optic neuropathy. Eur J Ophthalmol. 2004;14:245-57. 9. Gonzalez-Gay MA, Lopez-Diaz MJ, Barros S, et al. Giant cell arteritis: laboratory tests at the time of diagnosis in a series of 240 patients. Medicine (Baltimore). 2005;84:277-90. 10. Murchison AP, Bilyk JR, Eagle RC Jr, Savino PJ. Shrinkage revisited: how long is long enough? Ophthal Plast Reconstr Surg. 2012;28:261-3. 11. Gooi P, Brownstein S, Rawlings N. Temporal arteritis: a dilemma in clinical and pathological diagnosis. Can J Ophthalmol. 2008;43:119-20. 12. Lie JT. Diagnostic histopathology of major systemic and pulmonary vasculitic syndromes Rheum Dis Clin North Am. 1990;16:269-92. 13. Albert DM, Ruchman MC, Keltner JL. Skip areas in temporal arteritis. Arch Ophthalmol. 1976;94:2072-7. 14. Albert DM, Searl SS, Craft JL. Histologic and ultrastructural characteristics of temporal arteritis. The value of the temporal artery biopsy. Ophthalmology. 1982;89:1111-26. 15. Klein RG, Campbell RJ, Hunder GG, Carney JA. Skip lesions in temporal arteritis. Mayo Clin Proc. 1976;51:504-10. 16. Lee AG, Brazis PW. Temporal arteritis: a clinical approach. J Am Geriatr Soc. 1999;47:1364-70. 17. Gonzalez-Gay MA, Garcia-Porrua C, Llorca J, Gonzalez-Louzao C, Rodriguez-Ledo P. Biopsy-negative giant cell arteritis: clinical spectrum and predictive factors for positive temporal artery biopsy. Semin Arthritis Rheum. 2001;30:249-56. 18. Breuer GS, Nesher G, Nesher R. Rate of discordant findings in bilateral temporal artery biopsy to diagnose giant cell arteritis. J Rheumatol. 2009;36:794-6. 19. Miller A, Green M, Robinson D. Simple rule for calculating normal erythrocyte sedimentation rate. Br Med J (Clin Res Ed). 1983;286:266. 20. Hayreh SS, Podhajsky PA, Raman R, Zimmerman B. Giant cell arteritis: validity and reliability of various diagnostic criteria. Am J Ophthalmol. 1997;123:285-96. 21. Bengtsson B, Malmvall BE. Giant cell arteritis. Acta Med Scand. 1982;658(Suppl.):518-30. 22. Hedges TR, Gieger GL, Albert DM. The clinical value of negative temporal artery biopsy specimens. Arch Ophthalmol. 1983;101:1251-4. 23. Hall S, Hunder GG. Is temporal artery biopsy prudent? Mayo Clin Proc. 1984;59:793-6.
Temporal arteritis—Durling et al. 24. Danesh-Meyer HV SP, Bilyk JR, Eagle RC, Sergott RC. Shrinkage: fact or fiction? Arch Ophthalmol. 2001;119:1217. 25. Carroll SC, Gaskin BJ, Danesh-Meyer HV. Giant cell arteritis. Clin Experiment Ophthalmol. 2006;34:159-73; quiz 94. 26. Sharma NS, Ooi J-L, McGarity BH, Vollmer-Conna U, McCluskey P. The length of superficial temporal artery biopsies ANZ J Surg. 2007;77:437-9. 27. Taylor-Gjevre R, Vo M, Shukla D, Resch L. Temporal artery biopsy for giant cell arteritis. J Rheumatol. 2005;32:1279-82. 28. Schallhorn J, Haug SJ, Yoon MK, Porco T, Seiff SR, McCulley TJ. A national survey of practice patterns: temporal artery biopsy. Ophthalmology. 2013;120:1930-4.
29. Nordborg E, Nordborg C, Bengtsson BA. Giant cell arteritis. Curr Opin Rheumatol. 1992;4:23-30. 30. Pless M, Rizzo JF 3rd, Lamkin JC, Lessell S. Concordance of bilateral temporal artery biopsy in giant cell arteritis. J Neuroophthalmol. 2000;20:216-8. 31. McDonnell PJ, Moore GW, Miller NR, Hutchins GM, Green WR. Temporal arteritis. A clinicopathologic study. Ophthalmology. 1986; 93:518-30. 32. Boyev LR, Miller NR, Green WR. Efficacy of unilateral versus bilateral temporal artery biopsies for the diagnosis of giant cell arteritis. Am J Ophthalmol. 1999;128:211-5.
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Incidence of discordant temporal artery biopsy in the diagnosis of giant cell arteritis Bethany Durling, MD,* Andrew Toren, MD,† Vivek Patel, MD,‡ Steven Gilberg, MD,§ Ezekiel Weis, MD, MPH,¶ David Jordan, MD§ ABSTRACT ● RÉSUMÉ Objective: We investigated the rate of discordant biopsy results (i.e., 1 side negative, 1 side positive) in patients who underwent initial bilateral temporal artery biopsies for suspected giant cell arteritis (GCA). Design: A cohort study. Participants: Consecutive patients undergoing temporal artery biopsy were enrolled. Of the 259 patients enrolled, 250 underwent initial bilateral temporal artery biopsies. Methods: Positive biopsies were defined based on accepted histologic definitions. Healed arteritis was considered a positive result. Clinical information was collected for all patients using a questionnaire administered by an ophthalmologist. Pathology results, including biopsy length (as measured by the pathologist), and laboratory information (i.e., serum erythrocyte sedimentation rate [ESR] and C-reactive protein [CRP] levels) were collected from digital patient records for statistical analysis. The main outcome was the rate of discordant biopsy in consecutive patients who underwent initial bilateral temporal artery biopsy. Results: Giant cell arteritis was confirmed in 62 (24.2%) of the 250 patients, including 3 patients with biopsies recorded as healed arteritis. The rate of discordant biopsy was 4.4% with 11 unilaterally positive biopsies. There was no statistical difference between the length of the left- and right-sided biopsies in either the unilaterally or bilaterally positive groups (p ¼ 0.13 and p ¼ 0.79, respectively). The average maximum ESR value for the bilateral group (58.7 mm/h) was significantly higher than the average maximum ESR value for the unilateral group (30.7 mm/h, p ¼ 0.03). The average maximum CRP value for the bilateral group was 59.2 mg/L and 28.6 mg/L for the unilateral group (p ¼ 0.30). Discordance between the localization of symptoms and the side of positive biopsy occurred in 3 patients (i.e., 3 patients had left-sided symptoms only, yet a right-sided positive biopsy). Conclusions: The rate of discordant biopsies in patients who underwent initial bilateral temporal artery biopsies was considerable in our patient cohort. Given this reasonably high rate of discordance between sides, as well as the lack of correlation between side of positivity and laterality of presenting symptoms, we recommend initial bilateral temporal artery biopsies to enhance the diagnostic certainty of the disease. Objet : Nous avons examiné l’incidence de résultats de biopsie discordante (i.e. un côté positif et l’autre négatif) chez les patients qui ont subi une première biopsie bilatérale temporale pour un soupçon d’artérite à cellules géantes (ACG). Nature : Étude prospective de cohorte. Participants : En tout, 259 patients consécutifs ayant subi une biopsie de l’artère temporale ont été inscrits. Parmi eux, 250 ont subi une biopsie initiale bilatérale des artères temporales. Méthodes : La définition des biopsies positives était fondée sur les définitions histologiques acceptées et la guérison de l’artérite était considérée comme résultat positif. L’information clinique a été recueillie pour tous les patients à l’aide d’un questionnaire administré par un ophtalmologiste. Les résultats concernant la pathologie, comprenant la longueur de la biopsie (mesurée par le pathologiste) et l’information du laboratoire (i.e. les taux de sédimentation érythrocytaire [TSE] du sérum et les niveaux de protéines C-réactives (PCR)) a été puisée dans les dossiers médicaux numériques pour l’analyse statistique. Principaux résultats : Le principal résultat obtenu a été l’incidence de biopsie discordante chez les patients consécutifs qui avaient subi une biopsie initiale bilatérale des artères temporales. Résultats : L’ACG a été confirmée chez 62 des 250 patients (24,2 %), y compris 3 patients avec des biopsies enregistrées comme artérite guérie. Le taux de biopsies discordantes était de 4,4 % avec 11 biopsies unilatéralement positives. Il n’y avait pas de différence statistique entre les longueurs des biopsies de droite et de gauche chez les groupes unilatéralement ou bilatéralement positifs (p = 0,13 et p = 0,79 respectivement). Dans le groupe unilatéralement positif, la longueur moyenne post-fixation du côté de la biopsie positive était de 1,18 cm. Cela différait peu du côté de la biopsie négative qui était de 1,17 cm (p = 0,95). La moyenne de la valeur maximale du TSE dans le groupe bilatéral (58,7 mm/h) était significativement plus élevée que celle du groupe unilatéral (30,7 mm/h, p = 0,03). La moyenne de la valeur maximale du PCR du groupe bilatéral était 59.2mg/l et 28,6mg/l pour le groupe unilatéral (p = 0,30). Le pourcentage des patients prenant des stéroïdes oraux au moment de la biopsie était 76 % et 73 % (p = 1,00) dans chacun des groupes, bilatéral et unilatéral, respectivement. Conclusion : L’incidence de biopsies discordantes chez les patients qui subissaient une biopsie initiale bilatérale des artères temporales était considérable dans notre cohorte de patients. L’incidence n’était pas liée à la longueur de la biopsie, ni à l’utilisation de stéroïdes ni au niveau du PCR dans le sérum. Le TSE élevé de sérum était associé aux résultats bilatéralement positifs de la biopsie. Nous recommandons des biopsies initiales bilatérales des artères temporales pour réduire le risque de diagnostiquer à tort une artérite à cellules géantes, vu le taux raisonnablement élevé de désaccord entre les côtés et le manque de corrélation entre le côté de la positivité et la latéralité de la présentation des symptômes discordants.
From the *Department of Ophthalmology and Visual Sciences, Dalhousie University, Halifax, N.S.; †Department of Ophthalmology, Hôpital du Saint Sacrement, Université Laval, Québec, Qué.; ‡Department of Ophthalmology, Wilmer Eye Institute, Johns Hopkins University School of Medicine, Baltimore, Md.; §Department of Ophthalmology, University of Ottawa Eye Institute, Ottawa, Ont.; ¶Department of Ophthalmology, University of Alberta, Edmonton, Alta. Presented at the Canadian Ophthalmological Society Meeting (3rd prize: Canadian Ophthalmological Society Award for Excellence in Research), in Vancouver, B.C., Jun. 9 to 12, 2011.
Originally received Sep. 10, 2013. Final revision Nov. 23, 2013. Accepted Jan. 3, 2014 Correspondence to: David. R. Jordan, MD, 301 O’Connor Street, Ottawa ON K2P1V6.; [email protected] Can J Ophthalmol 2014;49:157–161 0008-4182/14/$-see front matter & 2014 Canadian Ophthalmological Society. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jcjo.2013.12.008
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Temporal arteritis—Durling et al. The timely and definitive diagnosis of giant cell arteritis (GCA) is important to manage morbidity from the disease or from treatment with high-dose corticosteroids.1–5 The diagnosis of GCA is suspected based on the presence of clinical features and serum inflammatory markers,6–9 and is confirmed with a temporal artery biopsy (TAB). TAB is the histologic gold standard to confirm suspected GCA and requires both an adequate length of specimen10 and evaluation in thin sections by an experienced pathologist.11 A biopsy-confirmed diagnosis is made based on the presence of characteristic histologic changes in the artery wall.12 These changes may be unevenly distributed (i.e., skip lesions), and biopsy samples of the unaffected temporal artery segment may produce a false-negative result.13–15 False-negative TAB rates have been reported in 10% to 20% of patients with GCA.15–18 False-negative, unilateral biopsy results subsequently shown to be positive on the contralateral side suggest that performing bilateral initial biopsy may be beneficial to enhance the diagnostic certainty. We report our experience with bilateral initial temporal artery biopsies.
METHODS All patients who were referred to the oculoplastic or neuroophthalmology service for TAB between 2007 and 2010 were invited to participate in the study. Informed consent was obtained from each patient before enrollment and TAB. Consecutive patients were enrolled and had bilateral temporal artery biopsies performed during the same operating room procedure time (i.e., simultaneous). Clinical information, including features associated with GCA, was collected preoperatively using a questionnaire administered by the ophthalmologist. In addition, serum hemoglobin, platelets, erythrocyte sedimentation rate (ESR), and C-reactive protein (CRP) levels were collected from referral information and digital patient records. Westergren’s ESR method and highly sensitive CRP assays were used in all biochemical laboratories. An in vivo biopsy length of at least 20 mm per side was the goal for all patients. Biopsy specimens were reviewed by an experienced pathologist and/or ophthalmic pathologist using the procedures outlined by Gooi et al.11 Healed arteritis was considered a positive result. These pathology results, including biopsy length (as measured by the pathologist), were collected from digital patient records for statistical analysis. Any patients who underwent a unilateral biopsy, or from whom bilateral biopsy results were not available, were excluded from our analysis. Approval from the Ottawa Hospital Ethics Committee was obtained for the study. The primary objective was to determine the rate of discordant biopsy in consecutive patients who underwent initial bilateral TAB. Descriptive data are presented as counts, percentages, and means (⫾ SD). Categorical variables were analyzed using Fisher’s exact and χ2 tests. Normally distributed
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continuous variables were analyzed with a Student t test, and nonparametric variables were analyzed using Wilcoxon rank sums. The ESR measured in millimeters per hour was graded as normal or elevated based on 2 validated formulas from Miller et al.19 and Hayreh et al.20 The range of normal CRP level varies from laboratory to laboratory. For our study, the value was graded as normal based on the established range of r8 mg/L at the Ottawa Hospital laboratory. All statistical tests were 2-tailed. Factors were considered statistically significant at a significance level less than 0.05. Statistical analysis was performed using Excel for Mac (Microsoft, v12.2.7)
RESULTS Of the 259 consecutive patients enrolled, 250 who had initial bilateral temporal artery biopsies were included (Table 1). GCA was confirmed in 62 (24.2%) of these patients, including 3 patients with biopsies recorded as healed arteritis. The rate of discordant biopsy was 4.4% with 11 unilaterally positive biopsies. There were 11 (100%) females in the unilaterally positive biopsy group and 41 (83%) females in the bilaterally positive biopsy group (p ¼ 0.19). The average age of patients in the unilateral and bilateral groups was 74.0 ⫾ 8.1 and 77.4 ⫾ 8.2 years, respectively (p ¼ 0.24). Whenever possible, laboratory values including ESR, CPR, hemoglobin, and platelet levels were collected before and after patients started steroid treatment (Table 2). The percentage of patients on oral steroids at the time of biopsy was 73% of the unilateral group and 76% of the bilateral group (p ¼ 1.00). The average maximum ESR value for the bilateral group (58.7 mm/h) was significantly higher than the average maximum ESR value for the unilateral group (30.7 mm/h, p ¼ 0.03). The average maximum CRP value for the bilateral group was 59.2, and 28.6 mg/L for the unilateral group (p ¼ 0.30). The platelet and hemoglobin levels were not significantly different before and after steroids in the respective groups. The length of the left- and right-sided biopsies in the total biopsy-positive population was not statistically different (p ¼ 0.59). In the unilaterally positive group, the average length of the biopsy-positive side was 1.18 cm. This was not significantly different from the biopsy-negative side, which was 1.17 cm (p ¼ 0.95). All recorded lengths are postfixation. Table 1—Descriptive data
No. of patients Female sex, n (%) Age ⫾ SD, y On steroids, n (%)*
All Positive Biopsies
Unilateral Biopsies
Bilateral Biopsies
62 52 (84) 76.8 ⫾ 8.2 47 (76)
11 11 (100) 74.0 ⫾ 8.1 8 (73)
51 41 (83) 77.4 ⫾ 8.2 39 (76)
*Patients on steroid therapy at time of initial blood work.
p
0.19 0.24 1
Temporal arteritis—Durling et al. Table 2—Laboratory markers according to biopsy results
Highest measurements before biopsy Mean ESR ⫾ SD (mm/h) Mean CRP ⫾ SD (mg/L) On steroids, n Before steroids* Mean ESR ⫾ SD (mm/h) Mean CRP ⫾ SD (mg/L) After steroids* Mean ESR ⫾ SD (mm/h) Mean CRP ⫾ SD (mg/L) Miller ESR elevated,† n Hayreh ESR elevated,† n CRP 4 8.0, n Mean biopsy length ⫾ SD: right sided, cm Mean biopsy length ⫾ SD: left sided, cm Mean combined biopsy length ⫾ SD, cm
All Positive Biopsies (n)
Unilateral Biopsies (n)
Bilateral Biopsies (n)
p
57.9 ⫾ 35.6 (47) 56.2 ⫾ 80.0 (43) 47
30.7 ⫾ 25.2 (9) 28.6 ⫾ 44.4 (8) 8
64.3 ⫾ 34.9 (38) 62.5 ⫾ 84.3 (35) 39
0.30 0.03 1
56.9 ⫾ 32.4 (40) 65.9 ⫾ 87.9 (33)
38.2 ⫾ 27.9 (7) 42.5 ⫾ 52.3 (5)
59.7 ⫾ 32.3 (33) 66.1 ⫾ 91.2 (28)
0.13 0.58
42.9 ⫾ 42.4 (30) 32.8 ⫾ 46.9 (28) 41 44 46 1.25 ⫾ 0.36 1.29 ⫾ 0.40 2.68 ⫾ 0.99
12.2 ⫾ 8.6 (7) 4.3 ⫾ 2.8 (7) 5 4 7 1.23 ⫾ 0.29 1.13 ⫾ 0.36 2.9⫾ 1.84
49.5 ⫾ 43.9 (23) 38.2 ⫾ 49.5 (21) 36 40 39 1.26 ⫾ 0.38 1.33 ⫾ 0.40 2.63⫾ 0.70
0.07 0.19 0.16 0.01 0.45 0.79 0.13 0.39
ESR, erythrocyte sedimentation rate; CRP, C-reactive protein. *Groups are not mutually exclusive; some patients had blood work performed both before and after initiation of steroids. †Two formulas for determining cutoff for elevated ESR in patients suspected of temporal arteritis.
There were no observed cases of infection, unusual bleeding, or seventh nerve injury relating to the biopsy. There were 11 unilaterally positive biopsies, representing 17.7% of the total biopsy positive group and 4.4% of the total biopsy population. Of the 11 patients with unilaterally positive biopsy, 4 had right-sided symptoms, 4 had left-sided symptoms, and 3 had bilateral or systemic symptoms (Table 3). Discordance between the localization of symptoms and the side of positive biopsy occurred in 3 patients (i.e., 3 patients had left-sided symptoms, yet a positive right-sided biopsy).
DISCUSSION The sensitivity of TAB is less than 100%,21 with sensitivities reported between 65% and 95%.21–23 This
decreased sensitivity is, in part, due to the nonuniform involvement of the diseased arteries resulting in skip lesions.13,15,24 Small-artery samples taken from 1 temporal artery may result in a falsely negative biopsy. It is generally agreed that longer specimens taken from multiple sections are preferable and may increase the sensitivity.10,13,22,25,26 Biopsies greater than 10 mm have been reported to increase the diagnostic yield but ideally should be greater than 20 mm (postfixation).10,13,27 A 20-mm postfixation specimen length is generally accepted as the minimal amount necessary for adequate histopathological study.10 In this study, the surgeons aimed to take samples greater than 20 mm, but in most instances, after accounting for shrinkage, they were less than 20 mm. The current practice of TAB among clinicians varies considerably among unilateral, sequential bilateral, and initial bilateral biopsies. In a recent study of clinical
Table 3—Presenting patient characteristics of those with discordant biopsies Postfixation Biopsy Length (cm) Patient No. 1 2 3 4 5 6
7 8 9 10 11
Signs/Symptoms Headache, jaw claudication, TA pain, abnormal TA pulse, neck/shoulder pain, weight loss, fever Headache, scalp tenderness, weight loss, anorexia, myalgias, fatigue Headache, scalp tenderness, permanent diplopia, neck/shoulder pain, weight loss, anorexia, myalgia, arthralgia, fatigue Headache, scalp tenderness, neck/shoulder pain, anorexia, malaise, arthralgia Jaw claudication Headache, jaw claudication, scalp tenderness, temporal artery pain, permanent vision loss, neck/shoulder pain, anorexia, fatigue Headache, transient vision loss, myalgia, arthralgia, fatigue Headache, permanent vision loss Headache, permanent vision loss, arthralgia Headache, scalp tenderness, neck/shoulder pain, arthralgia Headache, scalp tenderness, neck/shoulder pain, anorexia, fatigue
CRP (mg/L) ESR (mm/h) Steroids* Right Side Left Side
Biopsy Result
152
18
Yes
1.4
1.2
Right-sided active arteritis
126
83
No
1.0
1.5
Right-sided active arteritis
6.5
21
No
1.0
0.7
Right-sided active arteritis
7.7
24
Yes
0.8
0.7
Right-sided active arteritis
NA NA
NA NA
Yes Yes
1.1 1.6
1.1 0.9
Right-sided active arteritis Right-sided active arteritis
8.7 8.8 5.4 2.9 62.7
12 18 35 5 60
Yes Yes Yes Yes No
1.5 1.1 1.3 1.7 1.0
1.1 1.7 1.6 1.2 0.7
Right-sided active arteritis Right-sided active arteritis Left-sided healed arteritis Left-sided active arteritis Left-sided active arteritis
ESR, erythrocyte sedimentation rate; CRP, C-reactive protein; TA, temporal artery. *Indicates whether patients were on steroid therapy at time of initial blood work shown.
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Temporal arteritis—Durling et al. practice patterns, 66% preferred initial unilateral biopsy, 18% preferred initial bilateral biopsy, whereas the remaining 16% performed either unilateral or bilateral depending on the clinical suspicion.28 The literature supports both initial bilateral, sequential bilateral (second biopsy done based on frozen section results of first biopsy), and unilateral temporal artery biopsies.15,29,30 Some research suggests that the biopsy discordance rate is not high enough to justify bilateral biopsies,31 whereas other research suggests that bilateral biopsies, including initial and sequential, improves diagnostic yield in at least 3% of cases32 and is 5% more likely to detect histopathologic findings on biopsy.30 We favour initial bilateral biopsies because some research suggests false-negative results may occur with frozen sectioning—a standard technique used for “sequential” temporal artery biopsies.15,29 In this study, initial bilateral biopsy contributed to the diagnosis in 11 unilaterally positive cases. The rate of discordant biopsy in the total study population was 4.4% and 17% in the biopsy-positive group, which is consistent with rates reported previously in the literature.18,30 There were several instances where patients had bilateral or nonlocalizing symptoms with a unilaterally positive biopsy result. Our patient population also included 3 patients who had a positive biopsy on the contralateral side of their symptoms. Based on our results, we believe it is important to perform initial bilateral temporal artery biopsies to enhance diagnostic certainty. Limited follow-up by the surgeons in the study may underestimate potential complications of the biopsy. The referring physician followed the majority of patients after the biopsy. These patients were all given specific instructions to call and/or return if they had any concerns. Only 2 patients in follow-up returned for temporary minor irritation related to the incision. There are also several practical reasons for considering initial bilateral temporal artery biopsies. Doing the biopsies one right after the other takes little additional surgical time and maximizes the efficient use of the procedure area. The same instruments and accessories (bipolar cautery, drapes, sponges, sutures, etc.) may be used. Travel time is reduced for the patient, because there is only 1 operative procedure rather than 2. Although no study has investigated the cost-effectiveness of initial versus sequential bilateral biopsy, we suspect that initial bilateral biopsies would be more efficacious. Potential limitations of this investigation include partial patient laboratory data and biopsy length. For some patients, blood work before the commencement of steroids treatment was not available, because some patients had been started on steroids before referral and enrolment in the study. Although this study population was large when compared with other work investigating patients with GCA, this sample size has limited statistical power. Furthermore, a postfixation length of 20 mm is generally recognized as the minimal amount necessary for adequate histopathologic study.10 Although all
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surgeons attempted to obtain an in vivo sample greater than 20 mm, a postfixation length of 20 mm was not obtained in all patients. In addition, factors related to the study design— observational cohort design—are limiting. However, these limitations are applied evenly across both groups that are compared in this study.
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