Aortic Root Disease Research Articles

Aortic Root Volume and Geometry: Ready for Clinical Application?

Aortic Root Volume and Geometry: Ready for Clinical Application?

Aortic root replacement in young adults: disease characteristics and early outcome

Introduction Aortic pathology requiring replacement of the aortic root is rare in young adults and maybe a group prone to atypical presentation and poorer outcomes. Here, we have studied the clinical features, pathological extent of aortic root disease and outcome of young adults undergoing aortic root replacement at this institution between 1995 and 2005.

Aortic Valve Replacement through Right Minithoracotomy in 306 Consecutive Patients

To define the role and early results of aortic valve surgery through a right minithoracotomy. A retrospective analysis was performed on 306 consecutive patients undergoing aortic valve replacement through an 8-cm right minithoracotomy in the second intercostal space. The initial experience was included. The right second and third ribs were detached from the sternum in most cases and repaired at the end of each case. Most operations were performed using anterograde and retrograde cardioplegic arrest with percutaneous femoral venous cannulation and direct aortic cannulation through the incision. Standard instruments were used with direct digital knot tying. Mean age was 65 ± 14 (range, 20-90) years. Aortic valve disease cause was calcific disease in 160 of 306 (52%) patients, bicuspid disease in 95 of 306 (31%) patients, and endocarditis in 9 of 306 (3%) patients. Previous cardiac surgery was present in 13 of 306 (4%) patients. Biologic prostheses were used in 240 of 306 (78%) patients. Median valve size was 23 mm. Mean clamp times and pump times were 103 ± 26 and 158 ± 35 minutes, respectively. Median postoperative length of stay was 5 days. Thirty-day mortality was found in 4 of 306 (1%) cases. There were no deep wound infections or mediastinitis. Stroke occurred in 5 of 306 (1.6%) patients, and new pacemaker required in 11 of 306 (4%) patients. Reoperation for bleeding occurred in 2 of 306 (1%) patients. Conversion to median sternotomy occurred in 15 of 306 (5%) patients caused by chest wall anatomy (n = 7), bleeding (n = 3), coronary disease (n = 2), or aortic disease (n = 3). Patients were allowed to return to driving or preoperative activity in 2 weeks. With a mean follow-up of 2.8 ± 2.2 years, one patient required reoperation for aortic root disease. Right minithoracotomy is a safe but limited alternative to sternotomy in isolated aortic valve replacement. This approach may be particularly valuable in some higher risk, elderly patients and opens options for a hybrid approach combined with percutaneous coronary angioplasty.

Clinical Study of Composite Valve Graft Replacement of the Aortic Root

Background: A composite valve graft replacement has been used for a variety of aortic root diseases. The aim of this study was to evaluate the mid-term results of this technique. Material and Method: We conducted a retrospective analysis of aortic root composite valve graft replacements in 39 patients and these procedures were done at our institution between 1992 and 2009. The mean age of the patients was 49.2±16.4 years. The mean follow-up was 64.2±53.4 months (maximum: 176 months). Result: There were 4 hospital deaths (8.6%) due to emergency aortic dissection and 4 late deaths owing to several causes. The causes of late death were 2 ruptures of a remnant aneurysm, 1 subdural hemorrhage and 1 paravalvular leakage. The calculated survival rate was 93.5%, 85.0% and 85.0% at 1, 5 and 10 years, respectively. There were 3 cerebrovascular accidents during the follow up period. The rate of freedom from cerebrovascular accidents was 97.0%, 92.0% and 80.0% at 1, 5 and 10 years, respectively. All of these brain accidents were hemorrhage-related complications. Conclusion: A composite valve graft replacement of the aortic root was associated with favorable results. So, this technique seems to be a good method to treat various aortic root diseases.

Aortic valve re-implantation technique with Gelweave Valsalva prosthesis: safety, reproducibility and pitfalls of a geometric reconstruction

To evaluate the safety, reproducibility and pitfalls of an aortic valve re-implantation (AVRei) technique. From June 2005 to December 2008, 30 patients underwent aortic valve-sparing re-implantation with Gelweave Valsalva prosthesis. Mean age was 66 +/- 7 years (range 47-81). Mean aortic root diameter was 49 +/- 6 mm (range 37-70) and 12 patients had an aortic insufficiency more than 2+. All the patients were elective, except three who underwent surgery for type A aortic dissection. Two patients had Marfan syndrome and one had a bicuspid aortic valve. Isolated aortic root replacement was performed in 26 patients, whereas hemiarch extension was required in four. All the survivors underwent serial echocardiographic assessment for functional results and multi-detector computed tomography (MDCT) for aortic root morphology evaluation. There was one early death and one re-exploration for bleeding. Two patients suffered from a perioperative stroke and four required a pacemaker implantation because of a complete atrio-ventricular block. Mean follow-up was 12 +/- 10 months (range 1-42) with no late deaths, whereas freedom from reoperation was 100% and freedom from aortic insufficiency 2+ or more was 96.5%. MDCT aortic root reconstruction showed a pseudo-normalization of the neo-sinuses of Valsalva mimicking the human normal aortic root morphology. AVRei with Valsalva conduit is a well-tolerated procedure both in elective and emergency situations. In well-selected patients, good functional and clinical results can be achieved, regardless of the cause of the aortic root disease. Application of simple surgical manoeuvres allows durable clinical efficacy to be obtained without the risk of major complications.

Recommendations for Evaluation of Prosthetic Valves With Echocardiography and Doppler Ultrasound: A Report From the American Society of Echocardiography's Guidelines and Standards Committee and the Task Force on Prosthetic Valves, Developed in Conjunction With the American College of Cardiology Cardiovascular Imaging Committee, Cardiac Imaging Committee of the American Heart Association, the European Association of Echocardiography, a registered branch of the

Recommendations for Evaluation of Prosthetic Valves With Echocardiography and Doppler Ultrasound: A Report From the American Society of Echocardiography's Guidelines and Standards Committee and the Task Force on Prosthetic Valves, Developed in Conjunction With the American College of Cardiology Cardiovascular Imaging Committee, Cardiac Imaging Committee of the American Heart Association, the European Association of Echocardiography, a registered branch of the

Augmentation Index Relates to Progression of Aortic Disease in Adults With Marfan Syndrome

Noninvasive applanation tonometry (APT) is useful to assess aortic stiffness and pulse wave reflection. Moreover, APT can predict outcome in many conditions such as arterial hypertension. In this study, we test whether APT measurements relate to progression of aortic disease in Marfan syndrome (MFS). We performed APT in 50 consecutive, medically treated adults with MFS (19 men and 31 women aged 32 +/- 13 years), who had not undergone previous cardiovascular surgery. During 22 +/- 16 months of follow-up, 26 of these patients developed progression of aortic disease, which we defined as progression of aortic root diameters >or=5 mm/annum (18 individuals), aortic surgery >or=3 months after APT (seven individuals), or onset of acute aortic dissection any time after APT (one individual). Univariate Cox regression analysis suggested an association of aortic disease progression with age (P = 0.001), total cholesterol levels (P = 0.04), aortic root diameter (P = 0.007), descending aorta diameter (P = 0.01), aortic root ratio (P = 0.02), and augmentation index (AIx@HR75; P < 0.006). Multivariate Cox regression analysis confirmed an independent impact on aortic disease progression exclusively for baseline aortic root diameters (hazard ratio = 1.347; 95% confidence interval (CI) 1.104-1.643; P = 0.003) and AIx@HR75 (hazard ratio = 1.246; 95% CI 1.029-1.508; P = 0.02). In addition, Kaplan-Meier survival curve analysis illustrated significantly lower rates of aortic root disease progression both with lower AIx@HR75 (P = 0.025) and with lower pulse wave velocity (PWV) values (P = 0.027). We provide evidence that APT parameters relate to aortic disease progression in medically treated patients with MFS. We believe that APT has a potential to improve risk stratification in the clinical management of MFS patients.

Basal cusp enlargement for repair of aortic valve insufficiency

The aim of this study was to evaluate the clinical and echocardiographic results after aortic valve reconstruction with a novel surgical technique consisting of basal cusp enlargement with an autologous pericardial patch. Between December 2005 and June 2008, a total of 106 consecutive patients underwent elective valve-sparing aortic root repair at Cardiovascular Clinic, Bad Neustadt, Germany. Fifty-nine patients required additional procedures on the aortic cusps; among them, in 10 cases basal cusp enlargement was used for restoration of coaptation area. All these patients had an ascending aortic aneurysm combined with aortic insufficiency, which was severe (4+) in 2 cases and moderate to severe (3+) in 4. The root repair was performed with valve reimplantation (David technique) in 1 case and the author's own single-patch technique in the other 9. Partial and total arch replacements were performed in 3 and 1 cases, respectively. The postoperative echocardiography at discharge showed no aortic regurgitation in 7 cases and trivial regurgitation in 3. The average coaptation height of the leaflets was 9.9 + or - 0.6 mm, and the mean gradient across the valve was 5.4 + or - 1.9 mm Hg. At follow-up as late as 31 months, all patients were alive with echocardiographic findings unchanged from the early postoperative examinations. The technique presented here allows an individualized reconstruction of the aortic cusps, leading to considerable improvement in coaptation area, in patients who have aortic leaflet prolapse or restriction caused by complex aortic root and valve disease.

Stentless versus Stented Bioprosthetic Aortic Valves

: This meta-analysis sought to determine whether stentless bioprosthetic valves improve clinical and resource outcomes compared with stented valves in patients undergoing aortic valve replacement. : A comprehensive search was undertaken to identify all randomized and nonrandomized controlled trials comparing stentless to stented bioprosthetic valves in patients undergoing aortic valve replacement available up to March 2008. The primary outcomes were clinical and resource outcomes in randomized controlled trial (RCT). Secondary outcomes clinical and resource outcomes in nonrandomized controlled trial (non-RCT). Odds ratios (OR), weighted mean differences (WMD), or standardized mean differences and their 95% confidence intervals (CI) were analyzed as appropriate. : Seventeen RCTs published in 23 articles involving 1317 patients, and 14 non-RCTs published in 18 articles involving 2485 patients were included in the meta-analysis. For the primary analysis of randomized trials, mortality for stentless versus stented valve groups did not differ at 30 days (OR 1.36, 95% CI 0.68-2.72), 1 year (OR 1.01, 95% CI 0.55-1.85), or 2 to 10 years follow-up (OR 0.82, 95% CI 0.50-1.33). Aggregate event rates for all-cause mortality at 30 days were 3.7% versus 2.9%, at 1 year were 5.5% versus 5.9% and at 2 to 10 years were 17% versus 19% for stentless versus stented valve groups, respectively. Stroke or neurologic complications did not differ between stentless (3.6%) and stented (4.0%) valve groups. Risk of prosthesis-patient mismatch was numerically lower in the stentless group (11.0% vs. 31.3%, OR 0.30, 95% CI 0.05-1.66), but this parameter was reported in few trials and did not reach statistical significance. Effective orifice area index was significantly greater for stentless aortic valve compared with stented valves at 30 days (WMD 0.12 cm/m), at 2 to 6 months (WMD 0.15 cm/m), and at 1 year (WMD 0.26 cm/m). Mean gradient at 1 month was significantly lower in the stentless valve group (WMD -6 mm Hg), at 2 to 6 month follow-up (WMD -4 mm Hg,), at 1 year follow-up (WMD -3 mm Hg) and up to 3 year follow-up (WMD -3 mm Hg) compared with the stented valve group. Although the left ventricular mass index was generally lower in the stentless group versus the stented valve group, the aggregate estimates of mean difference did not reach significance during any time period of follow-up (1 month, 2-6 months, 1 year, and 8 years). : Evidence from randomized trials shows that subcoronary stentless aortic valves improve hemodynamic parameters of effective orifice area index, mean gradient, and peak gradient over the short and long term. These improvements have not led to proven impact on patient morbidity, mortality, and resource-related outcomes; however, few trials reported on clinical outcomes beyond 1 year and definitive conclusions are not possible until sufficient evidence addresses longer-term effects.

NICE guidance for identification and treatment of familial hypercholesterolaemia: Commentary 2

Although the recently published NICE Guideline on the Identification and Management of Familial Hypercholesterolaemia contains no surprises for those involved in running specialist lipid clinics, it is a landmark in...

Basal cusp enlargement for repair of aortic valve insufficiency

Objective The aim of this study was to evaluate the clinical and echocardiographic results after aortic valve reconstruction with a novel surgical technique consisting of basal cusp enlargement with an autologous pericardial patch. Methods Between December 2005 and June 2008, a total of 106 consecutive patients underwent elective valve-sparing aortic root repair at Cardiovascular Clinic, Bad Neustadt, Germany. Fifty-nine patients required additional procedures on the aortic cusps; among them, in 10 cases basal cusp enlargement was used for restoration of coaptation area. All these patients had an ascending aortic aneurysm combined with aortic insufficiency, which was severe (4+) in 2 cases and moderate to severe (3+) in 4. The root repair was performed with valve reimplantation (David technique) in 1 case and the author's own single-patch technique in the other 9. Partial and total arch replacements were performed in 3 and 1 cases, respectively. Results The postoperative echocardiography at discharge showed no aortic regurgitation in 7 cases and trivial regurgitation in 3. The average coaptation height of the leaflets was 9.9 ± 0.6 mm, and the mean gradient across the valve was 5.4 ± 1.9 mm Hg. At follow-up as late as 31 months, all patients were alive with echocardiographic findings unchanged from the early postoperative examinations. Conclusions The technique presented here allows an individualized reconstruction of the aortic cusps, leading to considerable improvement in coaptation area, in patients who have aortic leaflet prolapse or restriction caused by complex aortic root and valve disease.

Custom-tailored valved conduit for complex aortic root disease

Custom-tailored valved conduit for complex aortic root disease

Composite Valve Graft Replacement of the Aortic Root: Twenty-Seven Years of Experience at One Japanese Center

The aim of this study was to evaluate the early and long-term results of a composite valve graft root replacement for various aortic root diseases. Between 1978 and 2005, 273 patients with various disorders of the aortic root underwent a composite valve graft root replacement. The mean age of the patients was 47.5 +/- 13.2 years. There were 93 patients with Marfan syndrome, 56 aortitis, and 63 type A aortic dissections. Thirty-nine emergency operations and 55 redo operations were included. For the proximal anastomosis, a skirted technique was used in 157 patients. For the coronary reconstruction, Bentall's original inclusion technique was utilized in 36 patients, a direct button technique in 159, and a graft interposition technique in 63. The mean follow-up was 106 months. The in-hospital mortality was 9.5%. An emergency operation emerged as a significant predictor of early death. The actuarial survival rate was 87.0% and 72.9% at 5 and 15 years, respectively. The age at the operation, aortitis, Marfan syndrome, and use of a standard proximal anastomosis emerged as independent determinants of late death. The actuarial reoperation free rate was 96.3% and 89.7% at 5 and 15 years, respectively. In the patients who underwent the skirted technique the incidence of late graft detachment was less frequent than that of the standard technique. A composite valve graft root replacement is a safe and reliable procedure for various aortic root diseases with stable early- and long-term results. The skirted technique seems to be attractive to avoid late graft detachment even in cases with a fragile inflammatory pathology.

Operação de Bentall e De Bono para correção das doenças da raiz aórtica: análise de resultados a longo prazo

A retrospective study was performed in a series of consecutive patients who underwent a Bentall and De Bono procedure. Data were removed of medical records and follow-up data were obtained from clinical records and direct contact with patients. A total of 39 patients were studied between January 1996 and December 2005. The median age was 47 years (range 14-70). There were 33 males and six females. Eleven (25.5%) patients presented Marfan syndrome and one (2.5%) Turner syndrome. Nineteen (48.5%) patients had hypertension, eight (20.5%) had history of smoking, six (15.5%) had history of alcoholism, eight (20.5%) had dyslipidemia, two (5.0%) had diabetes and one (2.56%) had myocardial infarct previously. Twenty-eight (72%) patients were in II-III NYHA class in the moment of the surgery. Annulo-aortic ecstasy was present in 14 (35.9%) patients and aortic aneurysms in 16 (41%). The median time in intensive care unit was 8.79 days with range 2-23 days. Four (10.0%) patients underwent an emergency operation and 35 (90%) elective. The overall hospital mortality was 5% (2/39). The event-free survival is 94.87% at 1 year and 84.61% at in 5 and 10. The median time of follow-up was 46.5 months (range 14-120 months). The Bentall and De Bono technique obtained excellent results in the short-term and long-term, which support the continued use of the compositive graft technique as the preferred method of treatment for patients with aortic root disease. Our findings confirm the current literature data.

Deleterious outcome of No-React–treated stentless valved conduits after aortic root replacement: Why were Warnings ignored?

The implantation of a composite graft is the treatment of choice for patients with aortic root disease if the valve cannot be preserved and the patient is not a suitable candidate for a Ross procedure. Several years ago, the Shelhigh NR-2000C (Shelhigh, Inc, Millburn, NJ) was introduced in Europe. Being a totally biologic conduit and considering the lack of homografts, the graft seemed an ideal conduit for patients with destructive endocarditis, as well as for older patients who were not suitable candidates for oral anticoagulation. From 2001 until 2006, the Shelhigh NR-2000C stentless valved conduit was implanted in 115 patients for various aortic root pathologies. The conduit consists of a bovine pericardial straight graft with an incorporated porcine stentless valve. Aortic root repair was performed during standard cardiopulmonary bypass and mild hypothermia in the majority of patients. Deep hypothermic circulatory arrest combined with selective antegrade cerebral perfusion was used when the repair extended into the arch. Seven patients with uncomplicated early outcome presented with unexpected sudden disastrous findings at the level of the aortic root, although 1-year follow-up computed tomographic scans were normal. Four of these patients underwent emergency operations because of desintegration of the graft, along with rupture of the aortic root. Retrospectively, the main findings were persistent fever or subfebrility over months and a halo-like enhancement on computed tomographic scans. Extensive microbiologic examinations were performed without finding a causative organism. The use of the Shelhigh aortic stentless conduit can no longer be advocated, and meticulous follow-up of patients in whom this device has been implanted has to be recommended.

Custom-tailored valved conduit for complex aortic root disease

Commercially available conduits containing a valve are not always suitable for simultaneous reconstruction of the left ventricular outflow tract and replacement of the aortic root. We describe our experience with custom-made conduits for patients with complex disease of the aortoventricular junction. Twenty-seven patients with a destroyed aortoventricular junction resulting from endocarditis and/or multiple previous operations had reconstruction of the left ventricular outflow tract with a tailored tubular Dacron graft. The graft was tailored to correct the defect in the outflow tract and sutured with continuous polypropylene sutures directly to the interventricular septum and the intervalvular fibrous body or sewing ring of a prosthetic mitral valve. The coronary arteries were reimplanted as high as anatomically possible and a mechanical (16 patients) or bioprosthetic valve (11 patients) was implanted into the graft below the coronary arteries. Median age of the patients was 55 years. The follow-up was complete, with echocardiographic studies and a median period of 32 months. There were 3 operative and no late deaths. One patient required early reoperation for dehiscence of a patch used to reconstruct the posterior mitral valve annulus. Twenty-four patients were alive at the last follow-up and had a normally functioning aortic valve prosthesis and no false aneurysms. Intraoperatively tailored tubular Dacron graft for concomitant reconstruction of the left ventricular outflow tract and replacement of the aortic root is a useful and safe operative technique for patients with destroyed aortoventricular junction.

Ventricular Long-Axis Contraction as an Earlier Predictor of Outcome in Asymptomatic Aortic Regurgitation

The long-term prognostic significance of left ventricular (LV) long-axis contraction was investigated prospectively in 65 consecutive patients aged 58+/-15 years with asymptomatic aortic regurgitation, normal LV ejection fraction at rest, and no coronary artery or aortic root disease. A complete transthoracic echocardiographic study was performed at baseline and 12 months later. In 24 of 65 patients with peak systolic wave velocity at the lateral mitral annulus (LatS)<9 cm/s, LV diameter (p<0.01), volume (p<or=0.01), mass (p<0.001), and end-systolic wall stress (p<0.001) significantly increased after 12 months, whereas LV shortening and ejection fraction (p=0.001) and tissue Doppler right ventricular peak systolic wave velocity (p<0.05) decreased significantly. In patients with peak systolic wave velocity at the lateral mitral annulus>or=9 cm/s, none of these parameters was significantly affected during follow-up. Aortic valve replacement was performed in 6 of 24 patients (25%) with peak systolic wave velocity at the lateral mitral annulus<9 cm/s and none with peak systolic wave velocity at the lateral mitral annulus>or=9 cm/s. In patients with peak systolic wave velocity at the lateral mitral annulus<9 cm/s, a cut-off value of 6.25 cm/s predicted aortic valve replacement within the next year with 97% sensitivity and 83% specificity. In conclusion, ventricular long-axis contraction seems to be a reliable indicator for outcome prediction in patients with asymptomatic aortic regurgitation.

Evaluation and management of aortic valve and root disease

Aortic valve disease manifests in the form of stenosis, regurgitation, or some combination, yielding either excessive afterload and/or excessive preload on the left ventricle. Aortic root disease may affect valvular function, causing regurgitation; may simply be coexistent with stenotic aortic valvular disease; or may exist despite normal aortic valve function. Indications for intervening on aortic valve or root disease are determined by the presence of symptoms, by the pathology's impact on left ventricular function, or by the inherent risk of aortic catastrophe (dissection, disruption, or sudden death). Aortic valvular and root diseases are primarily treated by surgical replacement of the pathologic structures. Mechanical aortic valve replacement has long-term durability but requires continuous anticoagulation. Bioprostheses do not require anticoagulation but have more limited durability. Valve-sparing aortic root replacement and aortic valve repair offer the potential for indefinite durability without the need for anticoagulation but are technically more difficult to perform and require more stringent selection criteria based on determining the reparability of an aortic valve. Emerging percutaneous valve technologies offer new hope for patients who are not candidates for aortic valve surgery, but the applicability and durability of percutaneous aortic valves are not yet known. Timely and appropriate intervention in aortic valve and root disease can result in the restoration of a normal life span for patients with aortic valvular and/or root disease.

Left Ventricular Outflow Obstruction

Left ventricular outflow tract obstructions (LVOTOs) encompass a series of stenotic lesions starting in the anatomic left ventricular outflow tract (LVOT) and stretching to the descending portion of the aortic arch (Figure 1). Obstruction may be subvalvar, valvar, or supravalvar. These obstructions to forward flow may present alone or in concert, as in the frequent association of a bicuspid aortic valve with coarctation of the aorta. All of these lesions impose increased afterload on the left ventricle and, if severe and untreated, result in hypertrophy and eventual dilatation and failure of the left ventricle. LVOTOs are congenital in the vast majority of individuals younger than 50 years in the United States; some variants of subaortic obstruction are the exception. It is imperative to consider all patients with LVOTO at a high risk for developing infective endocarditis, and one should always institute appropriate measures for prophylaxis. The present article is intended as a contemporary review of the causes, manifestations, treatments, and outcomes of LVOTO; it will not address LVOTO in the pediatric population or genetic hypertrophic cardiomyopathy but will focus strictly on congenital malformations in the adult. Figure 1. Artist’s rendering of the LVOTO lesions in sequence as viewed from a superolateral orientation. A, Gradient echo cardiac MR image as viewed from the frontal projection demonstrating flow acceleration at a site of supravalvar aortic stenosis (white arrow) in a patient with Williams syndrome. The black arrow identifies the level of the unrestricted aortic valve. B, Classic radiological signs of coarctation of the aorta: rib notching (white arrows) as seen on a posteroanterior chest x-ray in a patient with coarctation of the aorta. The rib notching is caused by erosion of the inferior rib margins by dilated pulsatile posterior intercostals collateral arteries. The black arrow points to the Figure 3 silhouette that …

Aortic root disease after the Ross procedure

Autograft root pathology is the most common adverse event late after the Ross operation. Therefore, characterization of prevalence, risk factors and natural history of root disease, as well as identification of preventive and therapeutic strategies, is warranted. Autograft root pathology affects up to one third of long-term survivors of the Ross operation. Root replacement technique and preoperative aortic aneurysm are recurrent risk factors. Any age group, except for infants, may be affected. Dilatation is often progressive leading to valve regurgitation, true aneurysm, and, rarely, dissection. Primary prevention involves avoidance of root technique, graft repalcement of aneurysmal aorta, or modifications of the root technique. Use of beta-receptor antagonist or angiotensin converting enzyme-inhibitors for secondary prevention is still empirical. Indications to resection of root aneurysm are based on maximum root area indexed to body height. Reintervention prior to appearance of relevant valve insufficiency increases likelihood of pulmonary valve preservation. Definition of functional outcome after autograft valve-sparing procedures needs longer follow-up. Over a decade after worldwide embracement of the root replacement technique for the Ross procedure, autograft root pathology is emerging as a prevalent complication. Prophylactic and therapuetic strategies are proposed to mitigate the current and future impact of this phenomenon.