The Impact of Arteriovenous Fistulae on the Myocardium: The Impact of Creation and Ligation in the Transplant Era Juan Camilo Duque,*† Camilo Gomez,† Marwan Tabbara,* Carlos E. Alfonso,‡ Xiaoyi Li,* Roberto I. Vazquez-Padron,* Arif Asif,§ Oliver Lenz,¶ Patricia L. Briones,** and Loay H. Salman** *DeWitt Daughtry Family Department of Surgery, Leonard M. Miller School of Medicine, University of Miami, Miami, Florida, †Department of Medicine, Leonard M. Miller School of Medicine, University of Miami, Miami, Florida, ‡Division of Cardiology, University of Miami Miller School of Medicine, Miami, Florida, §Albany Medical College, Albany, New York, ¶Division of Nephrology, University of Miami Miller School of Medicine, Miami, Florida, and **Section of Interventional Nephrology, University of Miami Miller School of Medicine, Miami, Florida
ABSTRACT Cardiac hypertrophy is a relatively common complication seen in patients with advanced chronic kidney disease (CKD) and end-stage renal disease (ESRD). Moreover, cardiac hypertrophy is even more frequently seen in patients with ESRD who have an arteriovenous (AV) access. There has been substantial evidence pertaining to the effects of AV access creation on the heart structure
and function. Similarly, there is increasing evidence on the effects of AV access closure, flow reduction, transplantation, and immunosuppressive medication on both endpoints. In this review, we present the evidence available in the literature on these topics and open the dialog for further research in this interesting field.
Cardiac hypertrophy, specifically left ventricular hypertrophy (LVH), is a common complication seen in patients with advanced chronic kidney disease (CKD) and end-stage renal disease (ESRD) (1–3). Cardiac hypertrophy is even more frequently seen in patients who have an arteriovenous fistula (AVF) as a vascular access for hemodialysis (HD) (2). Interestingly, it is reported that more than 75% of patients with CKD already have established LVH immediately before the dialysis initiation and the prevalence in earlier CKD stages varies in a wide range from 32% to 75%. (4,5) CKD and ESRD have been identified as independent risk factors for the development of cardiovascular diseases as well as heart failure (HF) with their subsequent morbidities and mortalities (1–3). Records from the US renal data system (USRDS) showed HD as an independent risk factor for de novo and recurrent HF with a 51% mortality rate (6). Moreover, epidemiological studies revealed that HF prevalence in HD patients is considerably high,
accounting for 29 events per 1000 patient-years in long-term HD patients (7,8). AVF is considered the vascular access of choice for ESRD patients on hemodialysis (9). However, arteriovenous (AV) access is recognized as an important risk factor for high output heart failure. This is due to hemodynamic alterations and neurohormonal changes subsequent to the procedure (7,8). Even though the hemodynamic effects of AV access have been well studied, there are still multiple unanswered questions about the relation of AV access to cardiac remodeling. These cardiac changes are typically seen at the time of AV access closure after kidney transplant and in situations where the AV access flow is modified by surgical techniques. Principles of Cardiac Hypertrophy Left ventricular hypertrophy (LVH) is a physiological and adaptive response to the increased chronic work imposed on the heart (10). By definition, LVH is an increase in the ventricular mass due to the hypertrophy of existing myocytes conversely to hyperplasia that results in increases in ratio of wall thickness/chamber dimensions (11). According to the Framingham study, LVH is diagnosed when the left ventricular mass index (LVMI) is more than
Address correspondence to: Loay Salman, Section of Interventional Nephrology, Leonard M. Miller School of Medicine, University of Miami Miller School of Medicine, Miami, FL, or e-mail:
[email protected]. Seminars in Dialysis—Vol 28, No 3 (May–June) 2015 pp. 305–310 DOI: 10.1111/sdi.12313 © 2014 Wiley Periodicals, Inc. 305
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131 g/m in men and more than 100 g/m in women (5). When pathological stressors are continuous, the heart undergoes a remodeling process resulting in heart failure, commonly seen in the pathophysiology of hypertensive heart disease, in which the left ventricular wall thickness changes in response to the elevated blood pressure trying to compensate for the most important mechanical factor in LVH development, the wall stress (10). Cardiac hypertrophy is considered the interface between normal and failing heart, in which the main change is myocardial remodeling (12). This phenomenon is defined by molecular, cellular, and interstitial changes that result in anatomic and functional modifications in the left ventricle (LV) (1,11). As the remodeling begins, the anatomical contour transforms from an elliptical to a more spherical shape, disrupting the normal function (1,12). A thickened and enlarged heart wall characterizes the cardium. This remodeling is associated with an unfavorable prognosis through the development of arrhythmias, sudden death, and HF. It is described that the risk of cardiovascular morbidity and mortality is increased by a two-to-four-fold when compared with patients with normal left ventricular mass (13). Cardiac hypertrophy results from the production and deposition of fibrous tissue, (14) developing into a mismatch between physiological supply and demand. It is described that cardiac remodeling goes through a sequence of different stages until it reaches the last and critical point. Initially, the process begins with the hypertrophy developing, in which load exceeds output; secondly, compensatory hypertrophy initiates, in which the workload/mass ratio is normalized and resting cardiac output is maintained; and finally, this leads to overt heart failure (11,15). Moreover, and supporting this remodeling phenomena, there are two different types of cardiac hypertrophy known as concentric and eccentric (12). The concentric hypertrophy is represented by an increase of the h/R ratio (h = wall thickness and R = radius) usually higher than 0.42 (12,16), however, when the relative wall thickness is not increased LVH is classified as eccentric form. The concentric type is the main form of hypertrophy seen in hypertensive patients, however other medical conditions common in hypertensive subjects such as diabetes mellitus, obesity, and coronary artery disease, can also affect the pattern of hypertrophic response. Interestingly, high blood pressure is the second leading cause of kidney failure in the United States after diabetes. Both conditions are present in CKD patients and lead to heart thickening, especially the concentric type (16,17). The eccentric type develops in cardiac conditions such as aortic and mitral insufficiency that allow an increase in the volume overload as seen frequently in HD
patients. Interestingly, in HD patients, these conditions are present because of the pressure overload and also the volume overload that they carry, turning this problem into a vicious cycle. (14). Molecular Factors in CKD that Contribute to Cardiac Hypertrophy Physiological stimuli for ventricular growth in patients with renal disease other than hypertension, the main mechanical cause of concentric type and the second cause of CKD, have been widely described (16,17). These conditions such as anemia, parathyroid hormone activity, AV access, and the repetitive silent ischemia, all pathognomonic of CKD patients, play an important role and are recognized as promoter factors in the heart thickening (1). Patients with glomerular filtration rate (GFR) lower than 30 ml/minute per 1.73 m2 have more than two-fold increased risk of developing LVH when compared with patients with GFR higher than 60 ml/minute per 1.73 m2. This risk is believed to be mediated by uremia and/or worsening in renal function, which are both described as important promoter factors in cardiac remodeling (4). More recently, it has been reported that early initiation of dialysis has no beneficial or negative effect on the cardiac structure in patients with ESRD (18). However, the accumulation of intermediary molecules in CKD patients plays an important role as nonhemodynamic factors that may modulate cardiac hypertrophy (19). Consequences of this accumulation trigger abnormal neurohormonal and metabolic modifications, affecting the remodeling process. Activation of multiple inflammatory signaling pathways is considered a promoting factor for hypertrophy (20). Elevation of markers and metabolites such as catecholamines, angiotensin II, aldosterone, endothelin, proinflammatory cytokines like tumor necrosis factor alpha (TNF-a) (21), interleukin-b (IL-b), interleukin-6 (IL-6), and growth factors develop inside cardiac cells (2,22–24). The role of TNF-a level on cardiac remodeling and HF has been recognized in human and in animal models given that myocardium neutrophils, fibroblasts, and vascular smooth muscle cells are all able to synthesize it in response to the pressure overload (21,25,26). Acute phase reactants such as C-reactive protein (CRP) and IL-6 levels are strong predictors of cardiovascular risk and independent cardiovascular mortality markers in the general and renal populations. Interestingly, CRP and other markers are associated with interventricular septum thickness (IVST) and increased left ventricle mass index (LVMI) (27). Despite this, 37.6% of the predialysis patients present elevated CRP levels suggesting that uremia per se increases serum CRP levels. In
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addition, patients presenting with elevated postdialysis CRP and IL-6 are associated with a higher mortality risk (27,28). Noninflammatory molecule precursors such as the renin/angiotensin system (RAS) (an independent predictor of cardiovascular disease in the general population) play a remarkable role in HD patients. RAS has been shown in animal models to contribute directly to the cardiac remodeling (29,30). Moreover, it is known that RAS can act as a fibroblast growth factor independently of the hemodynamic effects (20,31,32). Endothelin 1, well known as a vasoactive peptide produced by various cells, plays a role as a potent growth factor especially on myocardium (33). It has been shown that the stretching caused by pressure and volume overload increases the cardiomyocyte endothelin 1 production (33). This increase activates the protein kinase cascade and will contribute to the final myocardium hypertrophy (33). Recently, fibroblast growth factor (FGF), more specifically fibroblast growth factor receptor 1 (FGFR1), which is expressed in the adult myocardial cells, was associated with left ventricular hypertrophy (32,34). This association is independent of the altered serum phosphate levels in CKD and has a clear correlation with FGF levels (32). Finally anemia, a frequent entity in CKD and ESRD patients, is a strong cardiac remodeling promoter. A strong relationship between low hemoglobin level and increased myocyte growth has been established (35). Moreover, it is reported that changes in hemoglobin level trigger similar cardiac responses in patients with progressive renal disease as patients with absolute anemia (35). Cardiac Measurements and Diagnostic Test Changes in the heart chambers after AV access placement, during HD and interdialysis sessions have been widely reported (36,37). The echocardiographic parameters changes depend on fluid overload and variability in preload between each dialysis session. However, it was suggested that the interdialytic volume alternations play an important role in the echographic measurements and can predispose the observer to biased interpretations (36,38). Recently, echograms of the left atrial volume (LAV) measurements emerged as a potential barometer for risk stratification and risk monitoring in end-stage renal disease (ESRD) patients (39). Over time, LAV measurement changes predict death and cardiovascular outcomes and can serve as markers of high CV risk, like left ventricular mass (LVM) and LV systolic function (40). It has been reported that LAV minimize the measurement error compared with left ventricular mass index (LVMI) because its estimation is based on automatic computation constructed on the left auricle contour and chamber volume, whereas LVMI is calculated on
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the basis of three different variables (41–43). Despite this, echocardiography can provide relatively accurate measurements of the heart with a described specificity and sensitivity higher than 80% (16). Based on this, LVM is commonly calculated using the American Society of Echocardiography formula: LV mass = 0.8 {1.04 9 [(LVIDD (left ventricle internal diameter during diastole) + IVSd (interventricular septal thickness during diastole) + PWTd (posterior Wall thickness during diastole)) 3 LVIDD3]} + 0.6 g. The (LVMI) is calculated by dividing the LVM result by body mass surface area (5,11,44). Imaging studies and serological markers have also been correlated with each other. It is known that comparing the relationship between atrial natriuretic peptide (ANP), brain natriuretic peptide (BNP), and LAV in ESRD patients BNP was shown to have more discriminatory power when compared with ANP (39). However, both serological levels are tightly correlated with LAV. Finally, supporting previous publications, a significant correlation between LVMI, LAV, and serum levels of BNP has been described suggesting that N-terminal prohormone of brain natriuretic peptide (NT- proBNP) may be a good predictor of left ventricle dysfunction (41,42,45). Cardiovascular Effects and AV Access The effects of AV access creation on the cardiovascular system have been widely studied. Systemic vascular resistance is first lowered, followed by an increase in the stroke volume, and a subsequent increase in cardiac work and output (46). This effect was first described by Nicoladoni in 1875 and revalidated in 1890 by Btanham and has not changed since. Literature shows that immediately after AVF creation, the cardiac output increases by 10 to 20%, leading to an increased volume in the left atrium, the inferior vena cava, and end diastolic volume (46). Moreover, it was reported that cardiac work increases substantially in uremic patients by 0.42 J and up to 0.62 J in HD patients (36). The subsequent neurohormonal and autonomic nervous system responses appear shortly after AVF creation and increase the heart rate, stroke volume, and cardiac output (47). During this phase, the myocardial cells increase the rate of energy expenditure, propagating an imbalance between energy expenditure and production. This discordance of energy results in myocyte death and tissue fibrosis. This could lead to a vicious cycle with progressive cardiosclerosis, eventually leading to HF (2). Hemodialysis access is the lifeline for ESRD patients on HD. AV access with low flows is suggestive of access dysfunction and could lead to inadequate HD. In contrast, it has also been shown that
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high AV access flows increase the cardiac output and workload, which could results in HF (48,49). The Vascular Access Society categorizes AV access with a high flow when the flow is higher than 1.0–1.5 l/minute and has a cardio pulmonary recirculation of more than 20% (48). Patients with high output HF present with dyspnea, orthopnea, paroxysmal dyspnea, edema, and the presence of a cardiac index greater than 3.0 l/minute/m2 (50,51). AV access with high flow is a serious but infrequent complication present in 1–8% of the HD patients (52). However, it is reported that mortality in patients with high flow AV access is not different compared to patients with low flow and is also independent of the AV access type. AV access blood flow is different between the anatomical locations with the flow being generally higher when the anastomosis is located proximal to the heart. (42). It is reported that patients with flows greater than 2.0 l/minute (predictive of HF) have increased left ventricle end diastolic volume (LVEDV) when compared to patients with flows less than 1.0 l/ minute (53). Finally, patients with standard AV access flow, ranging between 400 and 800 ml/minute, do not increase preload significantly and represent only 7– 18% of the total left ventricle load. Patients with flow higher than 2,000 ml/minute have 1.5 times higher left ventricle preload compared with those having usual flow (53). Flow Reduction and AV Access Closure: Effect on Cardiac Hypertrophy The effects of the AVF on the heart have been described, however the effects of the fistula closure or even the flow reduction remain debatable. Multiple case reports have shown a sharp resolution of the clinical HF signs and clear improvement of symptoms following AVF surgical modification (43,54–57). However, this situation is described only in symptomatic patients with no evidence of improvement in asymptomatic patients with AV access and high flow. Nevertheless, a reduction in left ventricular mass after AVF closure is a result of the reduction in LVEDV rather than a decrease in wall thickness (58). Postoperative reductions in left ventricle diameter and hypertrophy are best predicted by the dynamic increase in the total peripheral resistance and blood pressure during an acute occlusion of the AVF. Moreover, an increase in the total peripheral resistance more than three times over the baseline predicts more than 5% reduction in the left ventricle size (59). It is reported that following AVF closure, left ventricular ejection fraction did not change (60). However, there was a decrease in left ventricular diameter but not in the thickness (60). On the other
hand, it is reported that the decreased left ventricular hypertrophy was associated with an improvement of the left ventricular ejection fraction, diminished interventricular wall thickness, and a trending of the cardiac structure toward normal geometry (61). However, these changes have been reported only in cases of high output HF and high AV access flow. Kidney Transplantation: Effects on the Heart Kidney transplantation is the treatment of choice for ESRD (62). Kidney transplantation has been shown to decrease cardiovascular mortality rate and prevalence of HF. Despite this, HF and cardiac hypertrophy are still important concerns after transplantation with an incidence of 14.2 cases per 1000 person-years. (48). Patients with history of kidney transplantation have shown a reduced cardiac risk compared to HD patients suggesting that transplantation may be associated with regression of LVH, but this incidence is also higher than the general population (63). However, routine AVF closure after transplantation procedures shows a discrepancy in the results (48). Consequently, it is not routinely recommended to close AV access immediately after transplantation (49). Nevertheless, the effects of transplantation on ventricular hypertrophy regression is not only present in the first year posttransplantation but also reaches a nadir at the second year and stabilizes during third and fourth year postsurgery (51). Moreover, there are established factors that might affect the regression after transplant such as older age, body mass index, lower renal function, and high blood pressure; and it was described that predialysis left ventricular mass is one of the most important predictors of regression after kidney transplantation (64). Immunosuppressive Therapy and Cardiac Hypertrophy Regression Immunosuppressant medications in transplant patients are the main treatment to prevent rejections and complications. However, there are innumerable questions about different effects beyond immunosuppression that have not yet been explained (52,65). Besides the adverse effects of the medications, their benefit toward cardiac hypertrophy regression is clear and supports its use (52,66). Anti-mTOR drugs, sirolimus (SRL), and everolimus (EVE) are potent immunosuppressants with antiproliferative and antimigratory capacity widely used in kidney transplantation. These drugs work by blocking the intracellular signaling that regulates the growth and proliferation of T2 cells present in cardiac hypertrophy (52,53,62). Adminis-
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tration of SRL in mice subjected to cardiac pressure overload showed a 50% decrease in the number of growing cells as well as a reduction in the intramyocardial fibrosis (52,53). In addition, SRL inhibits the angiotensin II activity that increases the protein synthesis previously described (66). It was reported that the cardiac hypertrophy regression in patients on SRL was mostly in the wall thickness, whereas the internal size change was not significant (53). Conclusion The cardiac hypertrophy data available in the general population show tremendous advances in our understanding of the pathways leading up to cardiac remodeling. In spite of the progress in understanding cardiac remodeling in CKD and ESRD patients, the novel advances in understanding the mechanisms of the disease, and the available technological diagnostic tools to elucidate cardiac hypertrophy, it is still a major problem leading to high morbidity and mortality rates with suboptimal response to existing treatment efforts. With the revolution of transplantation and improved knowledge of immunosuppressant medications; the future is promising. Nevertheless, there is a necessity to clarify the AV access flow with further studies to better understand the complex effects AV access might have on cardiac function and structure, especially in patients with baseline ventricular mass alterations; and the importance of early treatment initiation in patients with early CKD stages. Acknowledgments This work was supported by National Institute of Diabetes and Digestive and Kidney Diseases at the National Institutes of Health [R01- DK098511] to R.I.V.-P. and L.H.S.
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