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Hyp paring the Keith^Wag classification

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Journal

Original Articlesystemic arterial blood pressure [2]. Routine oph-copic evaluation of the retina, as recommended anded by the Joint National Committee on Prevention,n, Evaluation, and Treatment of High Blood

Received 18 November 2012 Revised 8 January 2013 Accepted 15 January 2013

J Hypertens 31:000000 2013 Wolters Kluwer Health | Lippincott Williams &Wilkins.

DOI:10.1097/HJH.0b013e32835efea3pectrum of retinal vascular signs in patients with Melbo9905;ODUCTIONst described by Liebreich in 1859 [1], hyperten-ive retinopathy is a condition characterized by a

Journal of Hypertension 2013, 31:000000aDepartment of Optometry and Vision Sciences, University of Melbourne, Parkville,bCentre for Eye Research Australia (CERA), University of Melbourne, cVitreo-retinalUnit, The Royal Victorian Eye and Ear Hospital, East Melbourne, Victoria, Australia anddSingapore Eye Research Institute, National University of Singapore, Singapore

Correspondence to Dr Laura E. Downie, Lecturer and Clinical Leader - Cornea andContact Lenses, Department of Optometry and Vision Sciences, University ofse: This study assessed the interobserver andbserver grading reliability of the KeithWagenerr (KWB) system to the proposed MitchellWongified three-grade classification for hypertensivepathy.

ods: Digital retinal images of normal andtensive human fundii (n50 per group) weremly graded by an optometrist and analmologist using the two systems. Interobserverment was compared to a gold standard researchr. Intraobserver agreement was assessed through at grading after 6 months. Cohens kappa coefficientsused to assess the degree of agreement.

ts: Both clinicians demonstrated a good level ofment with the KWB and simplified classificationared with a gold standard grader; there was nocant difference in the level of agreement forof the two classification methods for either observer.mplified classification was found to be equally asious as the KWB system with respect tobserver and intraobserver agreement for bothtioners.

usion: These findings indicate that the simplifiedication of hypertensive retinopathy is both reliablepeatable. The advantage of the simplified methodhe KWB system in correlating retinal microvascularto incident cardiovascular risk supports its adoptionical practice.

ords: arteriovenous nicking, cardiovascular disease,wool patch, hemorrhage, hypertension,

tensive retinopathy, KeithWagenerBarker,vasculature, retina

viation: KWB, KeithWagenerBarker classificationertensive retinopathy

Pressand[35

DroutiretiningwhetPrevtechncorrebetwvascuas th

Th[KeitKeithet alGunncriticwhicretinarterhemintodifficof reretinof th

Wclassthe stensithatertensive retinopathy: comener^Barker to a simplified

ura E. Downiea, Lauren A.B. Hodgsonb, Carly D0Sylvul Connellc, and Tien Y. Wongb,dight Lippincott Williams & Wilkins. Unauthorizedof Hypertensionite these recommendations, few physiciansy examine the retina for signs of hypertensivethy. There is currently no clear consensus regard-classification of hypertensive retinopathy or

r a retinal examination is useful to stratify risk [6].s studies have often been limited by unreliableues with poor interobserver and intraobserverions [7,8]. Furthermore, few studies cite the link

hypertensive retinopathy and incident cardio-signs, frequently only citing increased mortality

ollapsible collective end-point [911].usefulness of the traditional classification schemeagenerBarker (KWB)] originally proposed by

t al. [11] (and subsequently modified by Scheie]) on the basis of clinical descriptions by Marcus12] is questioned [1318]. There are two majors of these original and modified classifications,ategorize the commonly observed hypertensiveigns (i.e. generalized and focal arteriolar narrowing,enous nicking, flame-shaped and blot-shapedages, cotton wool spots and optic disk swelling)r grades of increasing severity. First, it can befor the clinician to distinguish between low gradesopathy (i.e. grade 1 vs. grade 2). Second, thethy grade cannot be easily correlated to the severityypertension [19,20].ave previously proposed a simplified three-gradeation scheme (simplified classification) based onngth of the reported associations between hyper-retinopathy and cardiovascular risk [21]. We suggestmay be more useful than the KWB classification. reproduction of this article is prohibited.www.jhypertension.com 1

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The aim of this study was to assess the interobserver andintraobsclassifichyperte

MATESets ofof two 4disk anhyperteby twomologisgradingclassificImage VSoft).

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TABLE 1. KeithWagenerBarker and simplified classification systems for hypertensive retinopathy

KWB Simplified classification

Grade Features

1 No detectable signs

2 Generalized arteriolar narrowing, focal arteriolar narrowing,arteriovenous nicking, opacity (copper wiring) of arteriolarwall or a combination of these signs

3 Retinal hemorrhages (blot-shaped, dot-shaped, or flame-shaped),microaneurysm, cotton wool spot, hard exudate or a combinationof these signs

4 Signs of moderate retinopathy plus swelling of the optic disk

KWB, Keith

Downie et al.

2 werver grading reliability between the simplifiedation system and KWB classification systems fornsive retinopathy.

RIALS ANDMETHODSdigital retinal images (n 100, which comprised58 fields per set, one image centered on the opticd one on the macula) of normal (n 50) andnsive (n 50) human fundii were randomly gradedclinicians, an optometrist (L.E.D.) and an ophthal-t (P.C., retinal specialist) using two hypertensivesystems: grade 1, KWB and grade 2, simplifiedation (Table 1). Images were assessed on FastStoneiewer for Windows (version 4.0, 2009; FastStone

interobserver level of agreement for the clinicalrs was analyzed for grades 1 and 2. The inter-r agreement of both clinical observers wasmpared with a gold standard research grader.), grading coordinator at the Centre for Eyeh Australia (CERA). The intraobserver level ofent for both hypertensive grading systems wasned through a secondgradingby the sameobservers,randomly selected subgroup of 25 image setsing system, performed 6 months after the original. Cohens kappa coefficients were calculated tothe degree of agreement for both interobserverraobserver correlations. The degree of agreementssed in the form of kappa (standard error). Kappa isted qualitatively using the following criterion: poorent,

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retinopathy in clinical practice. A search of the publishedliterature indicates that this is the first study to havecompared the clinical repeatability and reliability of theKWB and simplified classification of hypertensive retino-pathy. The study design enabled the comparison of tworepresentatives fromprofessional populations that are likelyto commonly observe hypertensive retinopathy in practice,namely practitioners in primary ocular care (optometrists)and those undertaking tertiary ophthalmic care (retinalspecialists). Our findings indicate that the more recently

proposed simplified classification byWong andMitchell [21]was comparable to the KWB system [11] with respect to bothinterobserver and intraobserver agreement for both clinicalobservers. These data confirm that both classificationsystems can be easily performed by clinicians. Furthermore,our findings predict that good agreement should existbetween assessments performed between different practi-tioners and by the same practitioner over time.

Given that both the KWB and simplified classificationsystems demonstrate similar interobserver and intra-observer grading reliability, a decision with regard to theclinical usefulness of each system requires consideration ofthe how the assessment of retinal microvascular changemight be meaningfully correlated to the risk of cardio-vascular pathology. Formulated over 70 years ago, theKWB scale remains the most widely cited grading systemfor hypertensive retinopathy; the system is referred to inleading ophthalmology and cardiology textbooks [2326]and is thus taught to medical students and residents duringtheir training. The KWB system has also been utilized for

TABLE 3. Intra-observer agreement [kappa (standard error),n25 image sets] for KWB and the simplifiedclassification systems

KWB Simplified

Optometrist 0.770 (0.12) 0.879 (0.14)

Retinal specialist 0.702 (0.12) 0.671 (0.14)

KWB, KeithWagenerBarker.

(a) (b)

(c) (d)

AV nicking

AV nicking

Retinal hemorrhage

Retinal hemorrhageRetinal hemorrhages

Retinal hemorrhage

Cotton wool patch

Focal arteriolarnarrowingCopper wiring

FIGURE 1classificatiowall (coppcotton woo

Hypertensive retinopathy: a simplified classification

Journal(e) (f)

Retinal hemorrhage

Hard exudate

Optic disc swelling

Cotton wool patchight Lippincott Williams & Wilkins. Unauthorized

Retinal hemorrhage

Representative digital retinal fundus photographs of mild (a, b), moderate (c, d), and mn. (a) Mild hypertensive retinopathy is indicated by the presence of generalized arteriolarer wiring). (b) Mild hypertensive retinopathy with focal arteriolar narrowing. (c and d) Ml patches. (e and f) Malignant hypertensive retinopathy with swelling of the optic disk, r

of HypertensionRetinal hemorrhage

Hard exudate

Optic disc swelling

Cotton wool patch

Cotton wool patch

alignant (e, f) hypertensive retinopathy, as graded with the simplifiednarrowing, arteriovenous nicking and opacification of the arteriolaroderate hypertensive retinopathy with multiple retinal hemorrhages andetinal hemorrhages, hard exudates, and cotton wool patches.

www.jhypertension.com 3 reproduction of this article is prohibited.

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the classification of retinopathy in many recent clinicalstudies on hypertension [2731].

However, an important limitation of the KWB classifi-cation is the lack of clinical usefulness in differentiatinggrade 1 from grade 2 retinopathy. The Ibaraki PrefecturalHealthy study, involving 87 890 Japanese individuals,identified mild hypertensive retinopathy (i.e. grade 1 or

2 on KWB) as a significant, independent risk factor forcardiovascular mortality [27]. Other recent studies have alsodemonstrated an association between mild hypertensiveretinopathy (i.e. grade 1 or 2 on KWB) and incidentcardiovascular outcomes and indicators of target organdamage. Individual signs of mild hypertensive retino-pathy such as focal arteriolar narrowing and arteriovenous

TABLE 4. Summary of the association between the simplified classification of hypertensive retinopathy and cardiovascular diseaseoutcomes

Grade Retinal signs Cardiovascular disease outcomea

None No detectable signs None

Mild Generalized arteriolar narrowing, focal arteriolar narrowing,arteriovenous nicking, opacity (copper wiring) of arteriolarwall or a combination of these signs

Modest association with risk of incident stroke [23],subclinical stroke [41], renal dysfunction [27],incident coronary heart disease [25,28], and death [43]

Moderate Hemorrhage (blot-shaped, dot-shaped, or flame-shaped),microaneurysm, cotton wool spot, hard exudate or acombination of these signs

Strong association with risk of incident stroke [23,24],cardiovascular mortality [29], cognitive decline [42],transient ischemic attack, and acute ischemic stroke [30],and stroke mortality [31]

Malignant Signs of moderate retinopathy plus swelling of the optic disk Strong association with death [11]

aModest association is denoted by an odds ratio greater than 1 but less than 2. Strong association is denoted by an odds ratio greater than 2.

(a)

(b)

AV nicking

CWS

Microaneurysm

Blot hemorrhage

Focal narrowing

No retinopathy

Generalized narrowing

1.69

6.35

4.71

4.24

1.16

0.74

0 2 4

3-year cumulative incidence of stroke (%)

6 8

1.49

FIGURE 2(data derivrisk of con

Downie et al.

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CWS

Hemorrhage

Microaneurysm

8.0right Lippincott Williams & Wilkins. Unauthorized

Focal narrowing

No retinal signs

Generalized narrowing

7.2

4.8

0.0 5.0 10.0

7-year cumulative inci

8.1

(a) Graph showing the association between the severity of hypertensive retinal miced from Wong et al., 2001) [33]. (b) Graph showing the association between the severitygestive heart failure (data derived from Wong et al., 2005) [47]. AV nicking, arteriovenou

ww.jhypertension.com19.1

18.7

17.3 reproduction of this article is prohibited.

15.0 20.0

dence of heart failure (%)

25.0

rovascular change and the 3-year cumulative risk of incident strokeof hypertensive retinal microvascular change and the 7-year cumulatives nicking; CWS, cotton wool spots.

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nicking are associated with subclinical stroke [32], incidentclinical stroke [33,34], stroke mortality [35], coronary arterydisease [36], left ventricular hypertrophy [37], and renaldysfuncbody ofof progHoweveof cardibetwee

The sis basestudiesthe riskbetwee(grade 3single cand 2.cation sfor the schanges(summa

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value to confirm this. These preliminary results suggest thatthe simplified classification of hypertensive retinopathy isa clinically relevant, reliable, and repeatable method

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Hypertensive retinopathy: a simplified classification

Journaltion [38]. These findings add to the recent growingevidence that evenmild hypertensive retinopathy isnostic significance for patients with hypertension.r, in all these studies, there is no indication that riskovascular disease and target organ damage differsn grade 1 and 2 signs.implified classification of hypertensive retinopathyd upon more recent evidence [39], arising fromthat demonstrate that there are differences inof cardiovascular disease and target organ damagen mild (grades 1 and 2 on KWB) and moderateon KWB) retinopathy, and thus the rationale for a

ategory of mild stage that combines KWB grades 1The primary advantage of the simplified classifi-ystem over the KWB classification is that it allowstratification of clinically observable retinal vascular(see Fig. 1) to the risk of cardiovascular diseaserized in Table 4).is simplified classification, the features of mildnsive retinopathy, which encompass retinal arterio-s only, have been demonstrated to be modestlyed with the risk of coronary heart disease anded disorders [3336,38,40]. However, the presenceerate hypertensive retinopathy on the simplifiedation, including retinal hemorrhage, cotton woolnd hard exudates, is not only indicative of moretial retinal microvascular disorder but also holdsg association with an increased risk of clinicalubclinical stroke, cognitive decline, and death fromascular causes [33,4145]. The association betweenhtened risk of an adverse cardiovascular outcomeher levels of hypertensive retinopathy is evident instratification for both stroke and congestive heartFig. 2). The simplified classification system there-ws the clinician to utilize the eyes vascular status astensive target organ for risk stratification.inued advancements in vascular imaging techno-re allowing the development of newer and moreapproaches for assessing the retinal vasculature,the quantitative measurement of retinal vascularchanges and/or global geometric retinal vascularng [46]. Although these techniques are highlyin improving our understanding of retinal para-

to assess cardiovascular risk, the complexity andthese more advanced analysis techniques currentlyeir application to the domain of clinical research;ese techniques have not yet translated into main-practice. The simplified classification, based upondata and correlated to the severity of systemicr disease, is therefore more relevant to daily clinicaland for the optimal management of patients withnsion.ugh our observers consisted of only one repre-e from each profession, we would expect theance of these individuals to be typical of eachonal population. A follow-up study involvingased number of practitioners, with a larger samplel retinal photographs for assessment, would be of

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of Hypertensionight Lippincott Williams & Wilkins. Unauthorizedsing retinal microvascular pathology. Given thege of this method being correlated to the severitymic vascular disease, we propose the usefulnessmethodology in clinical practice in grading

nsive retinopathy and correlating these changesent cardiovascular risk.

OWLEDGEMENTS

ts of interesthors do not have any potential conflicts of interestto this research. CERA receives operational

cture support from the Government of Victoria.

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lines for the Management of Hypertension. J Hypertens 1999;183.TY. Fred Hollows Lecture: Hypertensive retinopathy a journeyfundoscopy to digital imaging. Clin Exp Ophthalmol 2006;400.a G, De Backer G, Dominiczak A, Cifkova R, Fagard R, Germanol. 2007 Guidelines for the Management of Arterial Hypertension:ask force for the management of arterial hypertension of theean Society of Hypertension (ESH) of the European Society oflogy (ESC). J Hypertens 2007; 25:17511762.TY, Mitchell P. The eye in hypertension. Lancet 2007; 3;369:425

itt SB, West JN, Eames SM, Gibson JM, Gosling P, Littler WA.lness of ophthalmoscopy in mild to moderate hypertension.t 1989; 1:11031106.A, Aureli E, Dobree J. A note on signs in the fundus oculi

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RM. Ophthalmoscopic evidence of (1) arterial changes associ-ith chronic renal diseases and (2) of increased arterial tension.Ophthalmol Soc UK 1892; 12:124125.n PM, Lip GY, Eames SM, Gibson JM, Beevers DG. Hypertensivepathy: a review of existing classification systems and a suggestionsimplified grading system. J Hum Hypertens 1996; 10:9398.ert HD. Ocular manifestations of systemic hypertension.pin Ophthalmol 1998; 9:6972.TY, Klein R, Klein BEK, Tielsch JM, Hubbard LD, Nieto FJ. Retinalvascular abnormalities, and their relationship with hypertension,vascular disease, and mortality. Surv Ophthalmol 2001; 46:.rjee S, Chattopadhyay S, Hope-Ross M, Lip PL. Hypertensione eye: changing perspectives. J Hum Hypertens 2002; 16:667

di C, Salerno M, Salerno DE, Meani S, Esposito A, Catini E, et al.prevalence of retinal vascular changes in never-treated

tial hypertensives: an inter- and intra-observer reproduci-study with nonmydriatic retinography. Blood Press 2004; 13:.

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6 we women. Clin Exp Hypertens 2012. [Epub ahead of print]S, OnderHI, Aslantas Y, Ekinozu I, Kilic AC, Yalcin S, et al.Relationen indices of end-organ damage and mean platelet volume intensive patients. Blood Coagul Fibrinolysis 2012; 23:367369.li A, Kocinaj D, Bakalli A, Krasnigi A. Relationship of hypertensivepathy to thoracic aortic atherosclerosis in patients with severel hypertension. Clin Exp Hypertens 2011; 33:8994.er LS, Wong TY, Klein R, Sharrett AR, Bryan RN, Hubbard LD,Retinal microvascular abnormalities and MRI-defined subclinicalral infarction: the Atherosclerosis Risk in Communities Study.2006; 37:8286.TY, Klein R, Couper DJ, Cooper LS, Shahar E, Hubbard LD, et al.l microvascular abnormalities and incident strokes: the Athero-sis Risk in Communities Study. Lancet 2001; 358:11341140.ya H, Folsom AR, Wong TY, Klein R, Klein BE, Sharrett AR, ARICInvestigators. Retinal microvascular abnormalities and risk of

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ers Summary Evaluations

er 1paper Downie et al. evaluated the inter- and intra-r grading reliability of the three-grade classificationas introduced by Wong and Mitchell in 2004 inison to the traditional four-grade classification sys-hypertensive retinopathy as introduced by Keith,r and Barker in 1939. The authors found that thed intra-observer reliabilities of the two classificationare comparable. This is of interest as the Wong-classification system is based on prognostic

nce of retinal findings on clinical cardiovasculares observed in more recent population basedClearly, current hypertensive patients receiving

rotective treatment might differ from those hyper-patients with uncontrolled blood pressure levelsed at the times of Keith, Wagener and Barker.

Therpathinterperfo

RevTheretinWagBarkdecapatieclinicduciborgathe esuchus be

ww.jhypertension.comright Lippincott Williams & Wilkins. UnauthorizedTY, Klein R, Nieto FJ, Klein BE, Sharrett AR, Meuer SM, et al.l microvascular abnormalities and 10-year cardiovascular mort-a population-based casecontrol study. Ophthalmology 2003;3940.JJ, BakerML, Hand PJ, HankeyGJ, Lindley RI, Rochtchina E, et al.ient ischemic attack and acute ischemic stroke: associations withl microvascular signs. Stroke 2011; 42:404408.ell P, Wang JJ, Wong TY, Smith W, Klein R, Leeder SR. Retinalvascular signs and risk of stroke and stroke mortality. Neurology65:10051009.g CY, Ikram MK, Sabanayagam C, Wong TY. Retinal micro-lature as a model to study the manifestations of hypertension.tension 2012; 60:10941103.TY, Rosamond W, Chang PP, Couper DJ, Sharrett AR, Hubbardal. Retinopathy and risk of congestive heart failure. JAMA 2005;69.

re, a classification system of hypertensive retino-ased on more recent data and its reliability is ofThe study is straight forward. The statistical analysesed are sound. The manuscript is well written.

er 2hors propose a new classification of hypertensivethy that is in good agreement with the Keith,r and Barker classification. The KeithWegenergrading system was widely applied in the lastfor the stratification of risk in hypertensive

. However, several studies have proved a weakusefulness of this classification, due to poor repro-ty and poor association with other indices of targetamage. This limits extensive clinical application ofmination of the fundus oculi. Newer approaches,that proposed by the authors, could potentially giver information about retinal damage in hypertension.

Volume 31 Number 00 Month 2013etinopathy and sex hormone status in newly diagnosed hyper- Stglu M, Bulucu F, Demirbas S, Ay SA, Karaman M, Altun B, et al.elationship between microalbuminuria, left ventrical hypertro-

et al. Retinal microvascular abnormalities and cognitive impairment inmiddle-aged persons: the Atherosclerosis Risk in Communities Study.9:547551.di C, Meani S, Salerno N, Fusi V, Severgnini B, Valerio C, et al.l microvascular changes and target organ damage in untreatedtial hypertensives. J Hypertens 2004; 22:20952102.TY, Mitchell P. Hypertensive retinopathy. N Engl J Med 2004;102317.n DG. Practical statistics for medical research. London, England:an and Hall; 1991, p. 404.

f M, Duker JS. Ophthalmology. 3rd ed. Mosby Elsevier; 2009.D, Worzala K. Atlas of adult physical diagnosis. Philadelphia:cott Williams & Wilkins; 2006.r P, Topol EJ. PanVascular medicine: integrated clinical man-ent. Berlin, Heidelberg: Springer; 2002.lane SI, Bakris GL. Diabetes and hypertension: evaluation andgement. New York: Springer; 2012.chi T, Iso H, Yamagishi K, Irie F, Okubp Y, Gunji J, et al. Mildpathy is a risk factor for cardiovascular mortality in Japanesend without hypertension. The Ibaraki Prefectural Health Study.lation 2011; 124:25022511., Tsuda A, Yata S, Matsuto T, Okada M. Hypertension is arisk factor for future atherosclerotic changes in the Japanese

lation. Ann Clin Biochem 2010; 47 (Pt 2):118124.

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39. Wsig20

40. WetmJA

41. WCeJA

42. Wpathy and incident coronary heart disease in high risk men. Br Jalmol 2002; 86:10021006.is G, Arnett DK, Skelton TN, Taylor HW, Klein R, Couper DJ, et al.l arteriolar narrowing and left ventricular hypertrophy in Africancans. The Atherosclerosis Risk in Communities (ARIC) study.Hypertens 2008; 21:352359.TY, Coresh J, Klein R, Muntner P, Couper DJ, Sharrett AR, et al.l microvascular abnormalities and renal dysfunction: the athero-sis risk in communities study. J Am Soc Nephrol 2004; 15:2469

TY, McIntosh R. Systemic associations of retinal microvasculara review of recent population-based studies.Ophthal Physiol Opt25:195204.TY, Klein R, Sharrett AR, Duncan BB, Couper DJ, Tielsch JM,etinal arteriolar narrowing and risk of coronary heart disease in

and women. The Atherosclerosis Risk in Communities Study.2002; 288:6774.TY, Klein R, Sharrett AR, Couper DJ, Klein BE, Liao DP, et al.ral white matter lesion, retinopathy and incident clinical stroke.2002; 288:6774.TY, Klein R, Sharrett AR, Marino EK, Sharrett AR, Siscovick DS,tients with hypertension in a clinical setting. J Hum Hypertens Ne reproduction of this article is prohibited.

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