"Arterial stiffness is not associated with changes in the circadian pattern of blood pressure in patients with type 1 diabetes mellitus and cardiovascular autonomic dysfunction"

Lía Nattero-Chávez, Ane Bayona Cebada, Elena Fernández-Durán, Alejandra Quintero Tobar, Beatriz Dorado Avendaño, Héctor Escobar-Morreale, Manuel Luque-Ramírez, Lía Nattero-Chávez, Ane Bayona Cebada, Elena Fernández-Durán, Alejandra Quintero Tobar, Beatriz Dorado Avendaño, Héctor Escobar-Morreale, Manuel Luque-Ramírez

Abstract

Introduction: Cardiovascular autonomic neuropathy (CAN) associates an abnormal circadian pattern in blood pressure (BP) regulation that might be aggravated by the coexistence of arterial stiffness. We aimed to evaluate the effect of arterial stiffness in the circadian rhythm of BP in patients with type 1 diabetes and CAN.

Methods: Cross-sectional study including 56 consecutive patients with type 1 diabetes and CAN, with (n = 28) or without (n = 24) arterial stiffness as defined by an ankle-brachial index above 1.2. CAN was diagnosed by BP and heart rate responses to active standing and cardiovascular autonomic reflex tests. Absence of nocturnal decrease in BP-"non-dipping" pattern- was defined by a daytime to nighttime decrease in mean BP smaller than 10%.

Results: The study's subjects mean age was 40 ± 11 years-old, their mean duration of diabetes was 22 ± 10 years, and their mean A1c was 7.9 ± 1.5%. A "non-dipping" pattern was observed in 28 patients (54%) regardless of the presence or absence of arterial stiffness. Age, waist circumference, body mass index, and A1c, were introduced as independent variables into a multiple regression analysis. The stepwise model (R2: 0.113, p = 0.016) retained only A1c levels (β: ‒ 0.333, 95% confidence interval [CI]: -3.10 to -0.33) as significant predictor of the percentage of nighttime decrease in mean BP.

Conclusions: A non-dipping pattern in BP is very common in patients with type 1 diabetes presenting with subclinical CAN and is associated with a poorer metabolic control. On the contrary, coexistence of arterial stiffness is not associated with abnormalities in circadian BP regulation.

Keywords: Arterial stiffness; cardiovascular autonomic neuropathy; non-dipping; type 1 diabetes.

Conflict of interest statement

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Figures

Figure 1.
Figure 1.
Heart rate variability to orthostatism (30:15 ratio) in patients with concomitant arterial stiffness and evidence of subclinical atherosclerosis compared with those subjects with arterial stiffness but without atherosclerosis (panel A). Heart rate (HR) change to active standing in patients with arterial stiffness and those with normal ankle-brachial index (ABI) (panel B).
Figure 2.
Figure 2.
Decrease in mean blood pressure (BP) during the nighttime in subjects with arterial stiffness compared with those showing a normal ankle-brachial index (ABI).
Figure 3.
Figure 3.
Results of a multiple regression model introducing the nighttime decrease in blood pressure (BP) expressed as percentage of daytime values as dependent variable, and age, waist circumference, body mass index, heart rate variability to orthostatism (30:15 ratio), and glycated hemoglobin (A1c) levels as independent variables.

References

    1. Spallone V. Blood pressure variability and autonomic dysfunction. Curr Diab Rep 2018; 18(12): 137.
    1. Benhamou PY, Halimi S, De Gaudemaris R, et al.Early disturbances of ambulatory blood pressure load in normotensive type I diabetic patients with microalbuminuria. Diabetes Care 1992; 15(11): 1614–1619.
    1. Stella P, Tabak AG, Zgibor JC, et al.Late diabetes complications and non-dipping phenomenon in patients with Type 1 diabetes. Diabetes Res Clin Pract 2006; 71(1): 14–20.
    1. Dost A, Klinkert C, Kapellen T, et al.Arterial hypertension determined by ambulatory blood pressure profiles: contribution to microalbuminuria risk in a multicenter investigation in 2,105 children and adolescents with type 1 diabetes. Diabetes Care 2008; 31(4): 720–725.
    1. Poulsen PL, Ebbehøj E, Hansen KW, et al.24-h blood pressure and autonomic function is related to albumin excretion within the normoalbuminuric range in IDDM patients. Diabetologia 1997; 40(6): 718–725.
    1. Duvnjak L, Vucković S, Car N, et al.Relationship between autonomic function, 24-h blood pressure, and albuminuria in normotensive, normoalbuminuric patients with Type 1 diabetes. J Diabetes Complications 2001; 15(6): 314–319.
    1. Afsar B. Disruption of circadian blood pressure, heart rate and the impact on glycemic control in type 1 diabetes. Diabetes Metab Syndr 2015; 9(4): 359–363.
    1. Poulsen PL. Blood pressure and cardiac autonomic function in relation to risk factors and treatment perspectives in Type 1 diabetes. J Renin Angiotensin Aldosterone Syst 2002; 3(4): 222–242.
    1. Spallone V, Maiello MR, Morganti R, et al.Usefulness of ambulatory blood pressure monitoring in predicting the presence of autonomic neuropathy in type I diabetic patients. J Hum Hypertens 2007; 21(5): 381–386.
    1. Urbina EM, Wadwa RP, Davis C, et al.Prevalence of increased arterial stiffness in children with type 1 diabetes mellitus differs by measurement site and sex: the SEARCH for diabetes in youth study. J Pediatr 2010;156(5):731–737.
    1. Jensen-Urstad K, Reichard P, Jensen-Urstad M. Decreased heart rate variability in patients with type 1 diabetes mellitus is related to arterial wall stiffness. J Intern Med 1999; 245(1): 57–61.
    1. Nattero-Chávez L, Redondo López S, Alonso Díaz S, et al.Association of cardiovascular autonomic dysfunction with peripheral arterial stiffness in patients with type 1 diabetes. J Clin Endocrinol Metab 2019; 104(7): 2675–2684.
    1. Prince CT, Secrest AM, Mackey RH, et al.Cardiovascular autonomic neuropathy, HDL cholesterol, and smoking correlate with arterial stiffness markers determined 18 years later in type 1 diabetes. Diabetes Care 2010;33(3) (1935-5548 (Electronic)):652–657.
    1. Jaiswal M, Urbina EM, Wadwa RP, et al.Reduced heart rate variability is associated with increased arterial stiffness in youth with type 1 diabetes: the SEARCH CVD study. Diabetes Care 2013; 36(8): 2351–2358.
    1. Zhou TL, Henry RMA, Stehouwer CDA, et al.Blood pressure variability, arterial stiffness, and arterial remodeling. Hypertension 2018; 72(4): 1002–1010.
    1. Lithovius R, Gordin D, Forsblom C, et al.Ambulatory blood pressure and arterial stiffness in individuals with type 1 diabetes. Diabetologia 2018; 61(9): 1935–1945.
    1. Park JS, Shin JH, Park JB, et al.Relationship between arterial stiffness and circadian pattern of blood pressure. Medicine (Baltimore) 2019; 98(12): e14953.
    1. Nattero-Chávez L, Redondo López S, Alonso Díaz S, et al.The peripheral atherosclerotic profile in patients with type 1 diabetes warrants a thorough vascular assessment of asymptomatic patients. Diabetes Metab Res Rev 2019; 35(2): e3088.
    1. American Diabetes Association . 2. Classification and Diagnosis of Diabetes: Standards of Medical Care in Diabetes-2021. Diabetes Care 2021; 44(Suppl 1): S15–S33.
    1. Leng GC, Fowkes FG. The Edinburgh Claudication Questionnaire: an improved version of the WHO/Rose Questionnaire for use in epidemiological surveys. J Clin Epidemiol 1992; 45(10): 1101–1109.
    1. American Diabetes Association . Microvascular Complications and Foot Care: Standards of Medical Care in Diabetes-2021. Diabetes Care 2021; 44(Suppl 1): S151–S167.
    1. Williams KV, Erbey JR, Becker D, et al.Can clinical factors estimate insulin resistance in type 1 diabetes? Diabetes 2000; 49(4): 626–632.
    1. Ewing DJ, Martyn CN, Young RJ, et al.The value of cardiovascular autonomic function tests: 10 years experience in diabetes. Diabetes Care 1985; 8(5): 491–498.
    1. Pop-Busui R, Boulton AJ, Feldman EL, et al.Diabetic neuropathy: a position statement by the american diabetes association. Diabetes Care 2017; 40(1): 136–154.
    1. Silva TP, Rolim LC, Sallum Filho C, et al.Association between severity of hypoglycemia and loss of heart rate variability in patients with type 1 diabetes mellitus. Diabetes Metab Res Rev 2017; 33(2): e2830.
    1. Aboyans V, Ricco JB, Bartelink MLEL, et al.2017 ESC Guidelines on the Diagnosis and Treatment of Peripheral Arterial Diseases, in collaboration with the European Society for Vascular Surgery (ESVS): Document covering atherosclerotic disease of extracranial carotid and vertebral, mesenteric, renal, upper and lower extremity arteriesEndorsed by: the European Stroke Organization (ESO)The Task Force for the Diagnosis and Treatment of Peripheral Arterial Diseases of the European Society of Cardiology (ESC) and of the European Society for Vascular Surgery (ESVS). Eur Heart J 2018;39(9):763–816, doi:10.1093/eurheartj/ehx095.
    1. Rabkin SW, Chan SH, Sweeney C. Ankle-brachial index as an indicator of arterial stiffness in patients without peripheral artery disease. Angiology 2012;63(2) (1940-1574(Electronic)):150-154.
    1. O'Rourke MF, Nichols WW. Aortic diameter, aortic stiffness, and wave reflection increase with age and isolated systolic hypertension. Hypertension 2005; 45(4): 652–658.
    1. Whelton PK, Carey RM, Aronow WS, et al.2017 ACC/AHA/AAPA/ABC/ACPM/AGS/APhA/ASH/ASPC/NMA/PCNA guideline for the prevention, detection, evaluation, and management of high blood pressure in adults: a report of the american college of cardiology/american heart association task force on clinical practice guidelines. J Am Coll Cardiol 2018; 71(19): e127-e248.
    1. Parati G, Stergiou G, O'Brien E, et al.European society of hypertension practice guidelines for ambulatory blood pressure monitoring. J Hypertens 2014; 32(7): 1359–1366.
    1. Mancia G, Verdecchia P. Clinical value of ambulatory blood pressure: evidence and limits. Circ Res 2015; 116(6): 1034–1045.
    1. Costa A, Bosone D, Ramusino MC, et al.Twenty-four-hour blood pressure profile, orthostatic hypotension, and cardiac dysautonomia in elderly type 2 diabetic hypertensive patients. Clin Auton Res 2016; 26(6): 433–439.
    1. Nagai M, Hoshide S, Nishikawa M, et al.Sleep duration and insomnia in the elderly: associations with blood pressure variability and carotid artery remodeling. Am J Hypertens 2013; 26(8): 981–989.
    1. Nagai M, Kario K.Visit-to-visit blood pressure variability, silent cerebral injury, and risk of stroke. Am J Hypertens 2013; 26(12): 1369–1376.
    1. Ahlgren AR, Sundkvist G, Wollmer P, et al.Increased aortic stiffness in women with type 1 diabetes mellitus is associated with diabetes duration and autonomic nerve function. Diabet Med 1999; 16(4): 291–297.
    1. van Ittersum FJ, Schram MT, van der Heijden-Spek JJ, et al.Autonomic nervous function, arterial stiffness and blood pressure in patients with type I diabetes mellitus and normal urinary albumin excretion. J Hum Hypertens 2004; 18(11): 761–768.
    1. Lafferty AR, Werther GA, Clarke CF. Ambulatory blood pressure, microalbuminuria, and autonomic neuropathy in adolescents with type 1 diabetes. Diabetes Care 2000; 23(4): 533–538.
    1. Failla M, Grappiolo A, Emanuelli G, et al.Sympathetic tone restrains arterial distensibility of healthy and atherosclerotic subjects. J Hypertens 1999; 17(8): 1117–1123.
    1. Evrard S, Delanaye P, Kamel S, et al.Vascular calcification: from pathophysiology to biomarkers. Clin Chim Acta 2015; 438(1873–3492(Electronic)): 401–414.
    1. Spallone V. Update on the impact, diagnosis and management of cardiovascular autonomic neuropathy in diabetes: what is defined, what is new, and what is unmet. Diabetes Metab J 2019; 43(1): 3–30.
    1. Poulsen PL, Hansen KW, Ebbehøj E, et deleterious effects of tight blood glucose control on 24-hour ambulatory blood pressure in normoalbuminuric insulin-dependent diabetes mellitus patients. J Clin Endocrinol Metab 2000; 85(1): 155–158.
    1. Krause M, Rüdiger H, Bald M, et al.Autonomic blood pressure control in children and adolescents with type 1 diabetes mellitus. Pediatr Diabetes 2009; 10(4): 255–263.
    1. Azar ST, Birbari A. Nocturnal blood pressure elevation in patients with type 1 diabetes receiving intensive insulin therapy compared with that in patients receiving conventional insulin therapy. J Clin Endocrinol Metab 1998; 83(9): 3190–3193.
    1. Page MM, Watkins PJ. Provocation of postural hypotension by insulin in diabetic autonomic neuropathy. Diabetes 1976; 25(2): 90–95.
    1. Mäkimattila S, Mäntysaari M, Schlenzka A, et al.Mechanisms of altered hemodynamic and metabolic responses to insulin in patients with insulin-dependent diabetes mellitus and autonomic dysfunction. J Clin Endocrinol Metab 1998; 83(2): 468–475.
    1. Peters A, Gromeier S, Kohlmann T, et al.Nocturnal blood pressure elevation is related to adrenomedullary hyperactivity, but not to hyperinsulinemia, in nonobese normoalbuminuric type 1 diabetes. J Clin Endocrinol Metab 1996; 81(2): 507–512.
    1. Saad MF, Knowler WC, Pettitt DJ, et al.Insulin and hypertension Relationship to obesity and glucose intolerance in Pima Indians. Diabetes 1990; 39(11): 1430–1435.
    1. O'Brien T, Young WF, Jr., Palumbo PJ, et al.Hypertension and dyslipidemia in patients with insulinoma. Mayo Clin Proc 1993; 68(2): 141–146.
    1. Sawicki PT, Heinemann L, Starke A, et al.Hyperinsulinaemia is not linked with blood pressure elevation in patients with insulinoma. Diabetologia 1992; 35(7): 649–652.
    1. Lane-Cordova AD, Kalil GZ, Wagner CJ, et al.Hemoglobin A1c and C-reactive protein are independently associated with blunted nocturnal blood pressure dipping in obesity-related prediabetes. Hypertens Res 2018; 41(1): 33–38.
    1. Goldberg RB. Cytokine and cytokine-like inflammation markers, endothelial dysfunction, and imbalanced coagulation in development of diabetes and its complications. J Clin Endocrinol Metab 2009; 94(9): 3171–3182.
    1. Kanter JE, Bornfeldt KE. Inflammation and diabetes-accelerated atherosclerosis: myeloid cell mediators. Trends Endocrinol Metab 2013; 24(3): 137–144.
    1. Wołoszyn-Durkiewicz A, Myśliwiec M. The prognostic value of inflammatory and vascular endothelial dysfunction biomarkers in microvascular and macrovascular complications in type 1 diabetes. Pediatr Endocrinol Diabetes Metab 2019; 25(1): 28–35.
    1. Shao L, Feng B, Zhang Y, et al.The role of adipose-derived inflammatory cytokines in type 1 diabetes. Adipocyte 2016; 5(3): 270–274.

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