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. 2023 Mar 28;3(3):CD006127.
doi: 10.1002/14651858.CD006127.pub3.

Blood pressure control for diabetic retinopathy

Diana V Do  1 , Genie Han  2 , Samuel A Abariga  2 , Gina Sleilati  3 , S Swaroop Vedula  4 , Barbara S Hawkins  5
Affiliations

Blood pressure control for diabetic retinopathy

Diana V Do et al. Cochrane Database Syst Rev. .

Abstract

Background: Diabetic retinopathy is a common complication of diabetes and a leading cause of visual impairment and blindness. Research has established the importance of blood glucose control to prevent development and progression of the ocular complications of diabetes. Concurrent blood pressure control has been advocated for this purpose, but individual studies have reported varying conclusions regarding the effects of this intervention.

Objectives: To summarize the existing evidence regarding the effect of interventions to control blood pressure levels among diabetics on incidence and progression of diabetic retinopathy, preservation of visual acuity, adverse events, quality of life, and costs.

Search methods: We searched several electronic databases, including CENTRAL, and trial registries. We last searched the electronic databases on 3 September 2021. We also reviewed the reference lists of review articles and trial reports selected for inclusion.

Selection criteria: We included randomized controlled trials (RCTs) in which either type 1 or type 2 diabetic participants, with or without hypertension, were assigned randomly to more intense versus less intense blood pressure control; to blood pressure control versus usual care or no intervention on blood pressure (placebo); or to one class of antihypertensive medication versus another or placebo.

Data collection and analysis: Pairs of review authors independently reviewed the titles and abstracts of records identified by the electronic and manual searches and the full-text reports of any records identified as potentially relevant. The included trials were independently assessed for risk of bias with respect to outcomes reported in this review.

Main results: We included 29 RCTs conducted in North America, Europe, Australia, Asia, Africa, and the Middle East that had enrolled a total of 4620 type 1 and 22,565 type 2 diabetic participants (sample sizes from 16 to 4477 participants). In all 7 RCTs for normotensive type 1 diabetic participants, 8 of 12 RCTs with normotensive type 2 diabetic participants, and 5 of 10 RCTs with hypertensive type 2 diabetic participants, one group was assigned to one or more antihypertensive agents and the control group to placebo. In the remaining 4 RCTs for normotensive participants with type 2 diabetes and 5 RCTs for hypertensive type 2 diabetic participants, methods of intense blood pressure control were compared to usual care. Eight trials were sponsored entirely and 10 trials partially by pharmaceutical companies; nine studies received support from other sources; and two studies did not report funding source. Study designs, populations, interventions, lengths of follow-up (range less than one year to nine years), and blood pressure targets varied among the included trials. For primary review outcomes after five years of treatment and follow-up, one of the seven trials for type 1 diabetics reported incidence of retinopathy and one trial reported progression of retinopathy; one trial reported a combined outcome of incidence and progression (as defined by study authors). Among normotensive type 2 diabetics, four of 12 trials reported incidence of diabetic retinopathy and two trials reported progression of retinopathy; two trials reported combined incidence and progression. Among hypertensive type 2 diabetics, six of the 10 trials reported incidence of diabetic retinopathy and two trials reported progression of retinopathy; five of the 10 trials reported combined incidence and progression. The evidence supports an overall benefit of more intensive blood pressure intervention for five-year incidence of diabetic retinopathy (11 studies; 4940 participants; risk ratio (RR) 0.82, 95% confidence interval (CI) 0.73 to 0.92; I2 = 15%; moderate certainty evidence) and the combined outcome of incidence and progression (8 studies; 6212 participants; RR 0.78, 95% CI 0.68 to 0.89; I2 = 42%; low certainty evidence). The available evidence did not support a benefit regarding five-year progression of diabetic retinopathy (5 studies; 5144 participants; RR 0.94, 95% CI 0.78 to 1.12; I2 = 57%; moderate certainty evidence), incidence of proliferative diabetic retinopathy, clinically significant macular edema, or vitreous hemorrhage (9 studies; 8237 participants; RR 0.92, 95% CI 0.82 to 1.04; I2 = 31%; low certainty evidence), or loss of 3 or more lines on a visual acuity chart with a logMAR scale (2 studies; 2326 participants; RR 1.15, 95% CI 0.63 to 2.08; I2 = 90%; very low certainty evidence). Hypertensive type 2 diabetic participants realized more benefit from intense blood pressure control for three of the four outcomes concerning incidence and progression of diabetic retinopathy. The adverse event reported most often (13 of 29 trials) was death, yielding an estimated RR 0.87 (95% CI 0.76 to 1.00; 13 studies; 13,979 participants; I2 = 0%; moderate certainty evidence). Hypotension was reported in two trials, with an RR of 2.04 (95% CI 1.63 to 2.55; 2 studies; 3323 participants; I2 = 37%; low certainty evidence), indicating an excess of hypotensive events among participants assigned to more intervention on blood pressure.

Authors' conclusions: Hypertension is a well-known risk factor for several chronic conditions for which lowering blood pressure has proven to be beneficial. The available evidence supports a modest beneficial effect of intervention to reduce blood pressure with respect to preventing diabetic retinopathy for up to five years, particularly for hypertensive type 2 diabetics. However, there was a paucity of evidence to support such intervention to slow progression of diabetic retinopathy or to affect other outcomes considered in this review among normotensive diabetics. This weakens any conclusion regarding an overall benefit of intervening on blood pressure in diabetic patients without hypertension for the sole purpose of preventing diabetic retinopathy or avoiding the need for treatment for advanced stages of diabetic retinopathy.

Trial registration: ClinicalTrials.gov NCT00542178 NCT00237549 NCT00185159 NCT00320008 NCT003200087-2452 NCT00134160.

PubMed Disclaimer

Conflict of interest statement

Diana V Do: no conflicts to declare

Genie Han: no conflicts to declare

Samuel A Abariga: no conflicts to declare

Gina Sleilati: no conflicts to declare

S Swaroop Vedula: no conflicts to declare

Barbara S Hawkins: no conflicts to declare

Figures

1
1
Study flow diagram.
2
2
Risk of bias summary: review authors' judgements about each risk of bias item for each included study. Missing cells indicate that study did not measure corresponding review outcomes.
3
3
Incidence of diabetic retinopathy by 5 years: more blood pressure control versus less blood pressure control.
4
4
Progression of diabetic retinopathy by 5 years: more blood pressure control versus less blood pressure control.
5
5
Combined incidence and progression of diabetic retinopathy by 5 years: more blood pressure control versus less blood pressure control.
6
6
Progression to PDR, CSME, or VH by 5 years: more blood pressure control versus less blood pressure control.
7
7
Loss of visual acuity: more blood pressure control versus less blood pressure control.
8
8
Death from all causes, 4 to 9 years: more blood pressure control versus less blood pressure control.
1.1
1.1. Analysis
Comparison 1: More blood pressure control versus no (or less) control , Outcome 1: Incidence of retinopathy by 5 years
1.2
1.2. Analysis
Comparison 1: More blood pressure control versus no (or less) control , Outcome 2: Progression of retinopathy by 5 years
1.3
1.3. Analysis
Comparison 1: More blood pressure control versus no (or less) control , Outcome 3: Combined incidence and progression of retinopathy by 5 years
1.4
1.4. Analysis
Comparison 1: More blood pressure control versus no (or less) control , Outcome 4: Incidence of PDR, CSME, or VH by 5 years
1.5
1.5. Analysis
Comparison 1: More blood pressure control versus no (or less) control , Outcome 5: Loss of visual acuity
1.6
1.6. Analysis
Comparison 1: More blood pressure control versus no (or less) control , Outcome 6: Adverse effect: death, 4 to 9 years
1.7
1.7. Analysis
Comparison 1: More blood pressure control versus no (or less) control , Outcome 7: Adverse effect: hypotension
1.8
1.8. Analysis
Comparison 1: More blood pressure control versus no (or less) control , Outcome 8: Adverse effect: hyperkalemia
1.9
1.9. Analysis
Comparison 1: More blood pressure control versus no (or less) control , Outcome 9: Progression to PDR, CSME, or VH by 4 to 9 years
2.1
2.1. Analysis
Comparison 2: Outcomes by type of diabetes: More blood pressure control versus no (or less) control, Outcome 1: Incidence of diabetic retinopathy by 5 years
2.2
2.2. Analysis
Comparison 2: Outcomes by type of diabetes: More blood pressure control versus no (or less) control, Outcome 2: Progression of diabetic retinopathy by 5 years
2.3
2.3. Analysis
Comparison 2: Outcomes by type of diabetes: More blood pressure control versus no (or less) control, Outcome 3: Combined incidence and progression by 5 years
2.4
2.4. Analysis
Comparison 2: Outcomes by type of diabetes: More blood pressure control versus no (or less) control, Outcome 4: Incidence of PDR, CSME, or VH by 5 years
2.5
2.5. Analysis
Comparison 2: Outcomes by type of diabetes: More blood pressure control versus no (or less) control, Outcome 5: Adverse effect: death, 4 to 9 years
3.1
3.1. Analysis
Comparison 3: Outcomes by blood pressure status at entry: More blood pressure control versus no (or less) control, Outcome 1: Incidence of diabetic retinopathy by 5 years
3.2
3.2. Analysis
Comparison 3: Outcomes by blood pressure status at entry: More blood pressure control versus no (or less) control, Outcome 2: Progression of diabetic retinopathy by 5 years
3.3
3.3. Analysis
Comparison 3: Outcomes by blood pressure status at entry: More blood pressure control versus no (or less) control, Outcome 3: Combined incidence and progression of diabetic retinopathy by 5 years
3.4
3.4. Analysis
Comparison 3: Outcomes by blood pressure status at entry: More blood pressure control versus no (or less) control, Outcome 4: Incidence of PDR, CSME, or VH by 5 years
3.5
3.5. Analysis
Comparison 3: Outcomes by blood pressure status at entry: More blood pressure control versus no (or less) control, Outcome 5: Adverse effect: death, 4 to 9 years
4.1
4.1. Analysis
Comparison 4: Outcomes by 7 to 9 years: More blood pressure control versus no (or less) control, Outcome 1: Incidence of retinopathy
4.2
4.2. Analysis
Comparison 4: Outcomes by 7 to 9 years: More blood pressure control versus no (or less) control, Outcome 2: Progression of retinopathy
4.3
4.3. Analysis
Comparison 4: Outcomes by 7 to 9 years: More blood pressure control versus no (or less) control, Outcome 3: Combined incidence and progression of retinopathy
4.4
4.4. Analysis
Comparison 4: Outcomes by 7 to 9 years: More blood pressure control versus no (or less) control, Outcome 4: Incidence of PDR, CSME, or VH
4.5
4.5. Analysis
Comparison 4: Outcomes by 7 to 9 years: More blood pressure control versus no (or less) control, Outcome 5: Blind eyes
See this image and copyright information in PMC

Update of

Comment in

References

References to studies included in this review

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BENEDICT {published data only}
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Chase {published data only}
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DEMAND {published data only}
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DIRECT Prevent 1 {published data only}
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DIRECT Protect 1 {published data only}
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DIRECT Protect 2 {published data only}
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    1. Mauer M, Zinman B, Gardiner R, Suissa S, Sinaiko A, Strand T, et al. Renal and retinal effects of enalapril and losartan in type 1 diabetes. New England Journal of Medicine 2009;361(1):40-51. - PMC - PubMed
Ravid 1993 {published data only}
    1. Ravid M, Savin H, Jutrin I, Bental T, Katz B, Lishner M. Long-term stabilizing effect of angiotensin-converting enzyme inhibition on plasma creatinine and on proteinuria in normotensive type II diabetic patients. Annals of Internal Medicine 1993;118(8):577-81. - PubMed
ROADMAP {published data only}
    1. Haller H, Ito S, Izzo JL, Januszewica A, Katayama S, Menne J, et al for the ROADMAP Investigators. Olmesartan for the delay or prevention of microalbuminuria in type 2 diabetes. New England Journal of Medicine 2011;364(10):907-17 [with Supplementary Appendix]. [CTG: ] - PubMed
    1. Haller H, Viberti GC, Mimran A, Remuzzi G, Rabelink AJ, Ritz E, et al. Preventing microalbuminuria in patients with diabetes: rationale and design of the Randomised Olmesartan and Diabetes Microalbuminuria Prevention (ROADMAP) study. Journal of Hypertension 2006;24(2):403-8. - PubMed
    1. Menne J, Fitz E, Ruilope LM, Chatzikyrkou C, Viberti G, Haller H. The Randomized Olmesartan and Diabetes Microalbuminuria Prevention (ROADMAP) observational follow-up study: benefits of RAS blockade with olmesartan treatment are sustained after study discontinuation. Journal of the American Heart Association 2014;3:e000810. [DOI: 10.1161/JAHA.114.000810] [CLINICALTRIALS.GOV: NCT00185159] - DOI - PMC - PubMed
    1. Menne J, Izzo JL, Ito S, Januszewicz A, Katayama S, Chatzykirkou C, et al for the ROADMAP Investigators. Prevention of microalbuminuria in patients with type 2 diabetes and hypertension. Journal of Hypertension 2012;30:811-8. [DOI: 10.1097/HJH.0b013e328351856d] - DOI - PubMed
Steno‐2 {published data only}
    1. Gaede J, Oellgaard J, Ibsen R, Gaede P, Nortoft E, Parving H-H, et al. A cost analysis of intensified vs conventional multifactorial therapy in individuals with type 2 diabetes: a post hoc analysis of the Steno-2 study. Diabetologia 2019;62:147-55. [CTG: ] [DOI: 10.1007/s00125-017-4739-3] - DOI - PMC - PubMed
    1. Gaede P, Lammert M, Valentine WJ, Parving H-H, Palmer AJ, Pedersen O, et al. Cost-effectiveness of intensified versus conventional multifactorial intervention in type 2 diabetes. Diabetes Care 2008;31(8):1510-5. [CTG: ] [DOI: 10.2337/dc07-2452] - DOI - PMC - PubMed
    1. Gaede P, Oellgaard J, Carstensen B, Rossing P, Lund-Andersen H, Parving H-H, et al. Years of life gained by multifactorial intervention in patients with type 2 diabetes mellitus and microalbuminuria: 21 years follow-up on the Steno-2 randomised trial. Diabetologia 2016;59:2298-307. [CTG: ] [DOI: 10.1007/s00125-016-4065-6] - DOI - PMC - PubMed
    1. Gaede P, Vedel P, Larsen N, Jensen GVH, Parving HH, Pedersen O. Multifactorial intervention and cardiovascular disease in patients with type 2 diabetes. New England Journal of Medicine 2003;348(5):383-93. - PubMed
    1. Gaede P, Vedel P, Parving HH, Pedersen O. Intensified multifactorial intervention in patients with type 2 diabetes mellitus and microalbuminuria: the Steno type 2 randomised study. Lancet 1999;353(9153):617-22. - PubMed
UKPDS/HDS {published data only}
    1. Clarke PM, Gray AM, Briggs A, Stevens RJ, Matthews DR, Holman RR, et al. Cost-utility analyses of intensive blood glucose and tight blood pressure control in type 2 diabetes (UKPDS 72). Diabetologia 2005;48(5):868-77. - PubMed
    1. Gray A, Clarke P, Farmer A, Holman R. Implementing intensive control of blood glucose concentration and blood pressure in type 2 diabetes in England: cost analysis (UKPDS 63). BMJ 2002;325(7369):860. - PMC - PubMed
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    1. Hypertension in Diabetes Study Group. Hypertension in Diabetes Study III. Prospective study of therapy of hypertension in type 2 diabetic patients: efficacy of ACE inhibition and β-blockade. Diabetic Medicine 1994;11(8):773-82. - PubMed
Wang {published data only}
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Zhao {published data only}
    1. Zhao C-M, Cui X-L, Wan G, Lu Y-Z, Niu Y-Q, Su C-Y, et al. Analysis of the effect of nine consecutive years’ intensive management and number of times achieving the target control on endpoint events in T2DM patients in Sanlitun Community Health Service Center in Beijing. International Journal of Endocrinology 2020;2020:Article ID 3646342. [DOI: 10.1155/2020/3646342] - DOI - PMC - PubMed

References to studies excluded from this review

Aro 2019_new {published data only}
    1. Aro A, Kauppinen A, Kivinen N, Selander T, Kinnunen K, Tuomilehto J, et al. Life style intervention improves retinopathy status—The Finnish Diabetes Prevention Study. Nutrients 2019;11(7):1691. - PMC - PubMed
Auyanet 2010 {published data only}
    1. Auyanet I, Rodriguez LJ, Esparza N, Cabrera F, Rossique P, Suria S, et al. Does carvedilol minimize the requirements for laser photocoagulation in diabetic retinopathy? [Minimiza el carvedilol los requerimientos de fotocoagulacion laser en la retinopatia diabetica?]. Nefrologia 2010;30(4):473-4. - PubMed
CALM‐II {published data only}
    1. Andersen NH, Knudsen ST, Poulsen PL, Poulsen SH, Helleberg K, Eiskjaer H, et al. Dual blockade with candesartan cilexetil and lisinopril in hypertensive patients with diabetes mellitus: rationale and design. Journal of the Renin-Angiotensin-Aldosterone System 2003;4(2):96-9. - PubMed
    1. Andersen NH, Poulsen PL, Knudsen ST, Poulsen SH, Eiskjaer H, Hansen KW, et al. Long-term dual blockade with candesartan and lisinopril in hypertensive patients with diabetes: the CALM II study. Diabetes Care 2005;28(2):273-7. - PubMed
Chang 2011 {published data only}
    1. Chang CH, Chuang LM. Effects of medical therapies on retinopathy progression in type 2 diabetes: is blood pressure control the lower the better? Journal of Diabetes Investigation 2011;2(2):101-3. - PMC - PubMed
DCCT {published data only}
    1. Genuth S, Lipps J, Lorenzi G, Nathan DM, Davis MD, Lachin JM, et al. Effect of intensive therapy on the microvascular complications of type 1 diabetes mellitus. JAMA 2002;287(19):2563-9. - PMC - PubMed
    1. The Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group. Epidemiology of Diabetes Interventions and Complications (EDIC). Design, implementation, and preliminary results of a long-term follow-up of the Diabetes Control and Complications Trial cohort. Diabetes Care 1999;22(1):99-111. - PMC - PubMed
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Durruty 2000 {published data only}
    1. Durruty P, Carpentier C, Krause P, Garcia de los Rios M. Evaluation of retinal involvement in type 2 diabetics with microalbuminuria [Evaluacion del compromiseo retinal en diabeticos tipo 2 microalbuminuricos]. Revista Medica de Chile 2000;128(10):1085-92. - PubMed
Faguer de Moustier 1989 {published data only}
    1. Faguer de Moustier B, Paoli V, Tchobroutsky G. Metabolic controlled trial of nicardipine in type 2 diabetic patients with slight hypertension. Current Therapeutic Research, Clinical and Experimental 1989;45(4):690-704.
Harrold 1969 {published data only}
    1. Harrold BP, Marmion VJ, Gough KR. A double-blind controlled trial of clofibrate in the treatment of diabetic retinopathy. Diabetes 1969;18(5):285-91. - PubMed
Jackson 1992 {published data only}
    1. Jackson WE, Holmes DL, Garg SK, Harris S, Chase HP. Angiotensin-converting enzyme inhibitor therapy and diabetic retinopathy. Annals of Ophthalmology 1992;24(3):99-103. - PubMed
JDCS 2011 {published data only}
    1. Kawasaki R, Tanaka S, Tanaka S, Yamamoto T, Sone H, Ohashi Y, et al. Incidence and progression of diabetic retinopathy in Japanese adults with type 2 diabetes: 8 year follow-up study of the Japan Diabetes Complications Study (JDCS). Diabetologia 2011;54(9):2288-94. - PubMed
    1. Sone H, Tanaka S, Iimuro S, Tanaka S, Oida K, Yamasaki Y, et al. Long-term lifestyle intervention lowers the incidence of stroke in Japanese patients with type 2 diabetes: a nationwide multicentre randomised controlled trial (the Japan Diabetes Complications Study). Diabetologia 2010;53(3):419-28. - PMC - PubMed
Lehsten 1996 {published data only}
    1. Lehsten K, Becker B, Michaelis D, Eggert HJ, Rjasanowski I, Salzsieder E. On the prospective significance of age at onset of diabetes, metabolic control, and hypertension for the development of diabetic retinopathy in patients with IDDM. Diabetes und Stoffwechsel 1996;5(1):18-25.
Malik 1998 {published data only}
    1. Malik RA, Williamson S, Abbott C, Carrington AL, Iqbal J, Schady W, et al. Effect of angiotensin-converting-enzyme (ACE) inhibitor trandolapril on human diabetic neuropathy: randomised double-blind controlled trial. Lancet 1998;352(9145):1978-81. - PubMed
MCSG 1995 {published data only}
    1. Microalbuminuria Collaborative Study Group. Intensive therapy and progression to clinical albuminuria in patients with insulin dependent diabetes mellitus and microalbuminuria. BMJ 1995;311(7011):973-7. - PMC - PubMed
Mehlsen 2011 {published data only}
    1. Mehlsen J, Jeppesen P, Erlandsen M, Poulsen PL, Bek T. Lack of effect of short-term treatment with amlodipine and lisinopril on retinal autoregulation in normotensive patients with type 1 diabetes and mild diabetic retinopathy. Acta Ophthalmologica 2011;89(8):764-8. - PubMed
Newsom 1991 {published data only}
    1. Newsom RS, Rassam SM, Kohner EM. The effect of beta blockers on retinal blood flow in diabetic patients. European Journal of Ophthalmology 1991;1(3):131-6. - PubMed
OSCAR {published data only}
    1. Ogawa H, Mitsuyama K, Jinnouchi T, Matsui K, Arakawa K for the OSCAR Study Group. Rationale, design, and patient baseline characteristics of OlmeSartan and Calcium Antagonists randomized (OSCAR) study: a study comparing the incidence of cardiovascular events between high-dose angiotensin II receptor blocker (ARB) monotherapy and combination therapy of ARB with calcium channel blocker in Japanese elderly high-risk hypertensive patients. Hypertension Research 2009;32:575-80. [CTG: ] [DOI: 10.1038/2009.60] - DOI - PubMed
Patel 1998 {published data only}
    1. Patel V, Rassam SM, Chen HC, Jones M, Kohner EM. Effect of angiotensin-converting enzyme inhibition with perindopril and beta-blockade with atenolol on retinal blood flow in hypertensive diabetic subjects. Metabolism: Clinical and Experimental 1998;47(12 Suppl 1):28-33. - PubMed
Porush 2000 {published data only}
    1. Porush JG. The benefits of angiotensin II receptor antagonists in high-risk hypertensive patients with diabetes. European Heart Journal Supplements 2000;2(B):B22-7.
Rachmani 2000 {published data only}
    1. Rachmani R, Lidar M, Levy Z, Ravid M. Effect of enalapril on the incidence of retinopathy in normotensive patients with type 2 diabetes. European Journal of Internal Medicine 2000;11(1):48-50.
Rassam 1997 {published data only}
    1. Rassam SMB, Patel VJ, Kohner E. Effect of ACE-inhibitors on retinopathy score and retinal hemodynamics in normotensive diabetic subjects. American Academy of Ophthalmology 1997;38:S207.
Schwartz 1998 {published data only}
    1. Schwartz MM, Lewis EJ, Leonard-Martin T, Lewis JB, Batlle D, The Collaborative Study Group. Renal pathology patterns in type II diabetes mellitus: relationship with retinopathy. Nephrology Dialysis Transplantation 1998;13(10):2547-52. - PubMed

References to studies awaiting assessment

ABCD‐2V (2) {published data only}
    1. Bedigian M. Improving the prognosis of diabetic patients: evaluating the role of intensive versus moderate blood pressure control with selective angiotensin II receptor block (ARB) therapy. Journal of the Renin-Angiotensin-Aldosterone System 2000;1(Suppl 2):25-8. - PubMed
    1. Bedigian MP, Estacio RO, Jefferes BW, Biggerstaff S, Schrier RW. Baseline characteristics of the hypertensive cohort of the appropriate blood pressure control in diabetes trial—part 2 with valsartan (ABCD-2V). American Journal of Hypertension 2000;13(4 Pt 2):56-7A.
    1. Estacio RO, Coll JR, Tran ZV, Schrier RW. Effect of intensive blood pressure control with valsartan on urinary albumin excretion in normotensive patients with type 2 diabetes. American Journal of Hypertension 2006;19(12):1241-8. - PubMed
    1. Shrier RW, Estacio RO, Jeffers BW, Biggerstaff S, Krinsk E, Pincus JR, et al. ABCD-2V: Appropriate blood pressure control in diabetes—part 2 with valsartan. American Journal of Hypertention 1999;12(4 Pt 2):141A.

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References to other published versions of this review

Do 2015b
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