European Journal of Echocardiography Advance Access published online on April 14, 2008
European Journal of Echocardiography, doi:10.1093/ejechocard/jen129
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Anderson-Fabry disease: long-term echocardiographic follow-up under enzyme replacement therapy
1 Division of Cardiology, Cardiovascular Center, University Hospital Zurich, Zurich, Switzerland
2 Department of Cardiology, Cardiovascular Center, Klinik Im Park, Seestr. 220, 8027 Zurich, Switzerland
3 Department of Internal Medicine, University of Zurich, Zurich, Switzerland
4 Division of Biostatistics, University of Zurich, Zurich, Switzerland
Received 16 October 2007; .
* Corresponding author. Tel: +41 44 209 2020; fax: +41 44 209 2029. E-mail address: ch.attenhofer{at}attglobal.net
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Abstract |
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Aims: Anderson-Fabry disease affects various organ systems due to glycosphingolipid accumulation. Enzyme replacement therapy (ERT) has been reported to decrease left ventricular wall thickening (LVWT) and to improve diastolic dysfunction.
Methods and results: This prospective study included 29 patients (patients; mean age 37 ± 13 years) with genetically, enzymatically and/or biopsy-proven Anderson-Fabry disease and long-time ERT. Data on symptoms, cardiac medications and history of hypertension were collected and all patients had comprehensive echocardiographic examination prior to ERT and at follow-up.
Disease was at an early stage with a total mean Mainz severity score index of only 18.6 ± 13.0. Prior to ERT, 79% of patients reported acroparesthesia. The median creatinine level was 121 ± 108 mcmol/L and LVWT was present in nine patients (31%). Binary appearance of the interventricular septum was found in 20% and posterobasal fibrosis in 83%. At median follow-up of 37 months, acroparesthesia decreased to 55% (P = 0.016). There was no change in creatinine levels. The incidence of LVWT was unchanged, only an increase in interventricular septal wall thickness from 11.7 ± 0.4 to 12.5 ± 0.5 was observed (P = 0.009). Left atrial size and the percentage of patients with binary appearance and posterobasal fibrosis were unchanged. There was a small improvement in diastolic function (29% decrease of E/Ea; P < 0.002).
Conclusion: Our Anderson-Fabry cohort had successful long-time ERT with impressive amelioration of subjective symptoms. Although there was not much improvement in cardiac changes apart from a slight improvement of diastolic function, at least, there was no progression of cardiac disease. For complete reversibility of cardiac changes in Anderson-Fabry disease, ERT might have to be started earlier in life and/or prescribed for a longer time.
Keywords: Anderson-Fabry disease; Enzyme replacement therapy; Cardiac function; Long-term follow-up; Left ventricular hypertrophy
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Introduction |
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Anderson-Fabry disease is a rare X-linked recessive metabolic disorder caused by deficiency of the lysosomal enzyme
-galactosidase A with an estimated frequency of one in 40 000–117 000 male births.1,2 The mean time between the onset of the first symptoms and diagnosis is 
15 years in male and up to 40 years in female patients.3 The main characteristic of the disease is progressive intracellular accumulation of neutral glycosphingolipids, mainly globotriaosylceramide GB3, in various organ systems including the cardiovascular system. Typical manifestations include angiokeratoma, hypohidrosis, acroparesthesia, transient ischaemic attacks, vertigo, proteinuria, renal failure, and diarrhea.2 Cardiac involvement includes left ventricular wall thickening (LVWT) mimicking left ventricular hypertrophy, impaired diastolic filling;4 tachy- and mostly bradyarrhythmias, valvular heart disease, and aortic root dilatation.3 More than 50% of hemi- and heterozygous patients complain of angina pectoris mostly due to decreased coronary reserve associated with LVWT.5 Anderson-Fabry disease also affects the vascular endothelium of the coronary arteries, which may result in significant coronary atherosclerosis especially in combination with hypertension and dyslipidemia.
Until a few years ago, supportive measurements were the main therapeutic approach in Anderson-Fabry disease. In Europe, enzyme replacement therapy (ERT) has become a causative treatment in patients with confirmed diagnosis of Anderson-Fabry disease since 2001.6 ERT not only stabilizes renal function, but improves pain perception and echocardiographic parameters compared with placebo.7 However, published data are limited so far.8,9
The goal of the present study was to analyse our data in 29 patients with proven Anderson-Fabry disease and to focus on the incidence of changes of symptoms, left ventricular muscle mass (LVMM) and diastolic function during long-time ERT.
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Methods |
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Study population
Twenty-nine patients with genetically, enzymatically or histologically documented Anderson-Fabry disease were included in this prospective study. None of the patients was receiving ERT before the study entry. Each patient underwent clinical investigation for assessment of different manifestations of Anderson-Fabry disease and—with inclusion of results of renal, neurological, ophthalmological, dermatological, and pulmonary investigations—calculation of the Mainz severity score index (MSSI) was performed.10 The MSSI is the scoring system for measuring the severity of Anderson-Fabry disease and for evaluating the clinical course of the disease in response to ERT. The combination of individual components is used to calculate the total MSSI score, which is divided into three grades of severity: mild (<20), moderate (20–40), and severe (>40). None of the patients was on haemodialysis or had kidney transplantation prior or during this study. Normal creatinine ranges in our laboratory were 53–106 mcmol/L for men, and 44–97 mcmol/L for women; these were used as cut-offs for elevated creatinine levels.
Study protocol
Twenty two patients received agalsidase alfa (ReplagalR) at a dosage of 0.2 mg/kg of body weight intravenously over 40 min every 2 weeks and five patients received agalsidase beta (FabrazymeR) at a dosage of 1 mg/kg of body weight intravenously over 4–6 h every 2 weeks. Two additional patients treated with agalsidase alfa at the beginning of the ERT switched to agalsidase beta (FabrazymeR) by personal request of the patients. All patients underwent comprehensive Doppler echocardiographic examination (echo) prior to ERT and during follow-up with analysis of systolic and diastolic function with inclusion of myocardial Doppler examinations of the mitral annulus as well.11 Data from the first and last exam were compared.
Echocardiographic examinations
All echocardiographic examinations were performed using a Siemens ultrasound machine (Sequoia 512) in the left lateral decubitus position by the same cardiologist (R.J.).
Standard two-dimensional M-mode echocardiography from parasternal long-axis view was used for measurement of left ventricular chamber dimensions including left ventricular end-diastolic diameter (LVEDD), end-systolic diameter (LVESD), septal (IVS) and posterior wall (PW) thickness, diameter of left atrium and radial function as fractional shortening (FS). LVMM was calculated with the formula of Devereux et al.12 LVWT was defined as LVMM index being above 134 g/m2 in males and above 110 g/m2 in females.13 LV (left ventricular) volumes were calculated using area length method.14 The longitudinal left ventricular systolic function was measured with myocardial Doppler imaging (systolic velocities of the mitral medial and lateral annulus) in the standard four apical chamber view. Relative wall index (RWI), calculated by the formula (2 x PW)/LVEDD, describes an increase in LV mass as either concentric (RWI 
0.45) or eccentric (RWI < 0.45) hypertrophy.15
All echocardiographic examinations were retrospectively screened by R.J. by review of videotapes or digitized images for the appearance of posterobasal fibrosis16 and for typical binary apearance.17 Typical examples are shown in Figures 1 and 2. Posterobasal fibrosis could be assessed reliably in 18 and the binary appearance in 25 of the 29 patients.
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Diastolic function was analysed as previously published.18 Pulsed wave Doppler of the mitral valve inflow was used to measure early (E), late (A) diastolic peak velocities and the E-wave deceleration time (Edec). In addition, tissue Doppler imaging (TDI) was used to measure the medial and lateral annulus E and A velocity (Ea, Aa) and corresponding E/Ea ratios were calculated.
Statistical analysis
Continues variables were presented as means with standard deviation and compared using Mann–Whitney test. Categorical variables were compared using Fisher's exact test. Continues variables before therapy were compared with follow-up values using Wilcoxon signed ranks test; those with categorical variables were compared using McNemar test. Analyses were performed using SPSS 13.0 (SPSS Inc Chicago Il) software. A P-value <0.05 was considered statistically significant.
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Results |
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Table 1 summarizes the basic characteristics of all 29 patients (20 males and 9 females) with a mean age of 37 ± 13 years, who were treated for 37 months. Enzyme levels were measured in all patients and were consistent with Anderson-Fabry disease in all. All patients had genetic mutations. Seven men had also biopsy material consistent with Anderson-Fabry disease: in six patients the material was from the kidney and in one from the skin.
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There were 17 patients with a MSSI < 20, 11 with a score between 20 and 40 and one patient with >40 points. No patient had a history of a stroke or a transient ischaemia attack before and under ERT. With a total score of only 18.7 ± 13.0, disease severity was not severe in our study group.
Table 2 shows a comparison of acroparesthesia, serum creatinine level, LVWT and the myocardial features of binary appearance and posterobasal fibrosis at the initial evaluation and at follow-up. Acroparaesthesia decreased from 79% before to 55% at follow-up. A typical binary appearance of the myocardium was found in 20% before and 32% at follow-up (P = 0.22). Posterobasal fibrosis was present in 83% before and in 72% at the end of follow-up (P = 1.0). We also analysed the cardiovascular functional status of our patients with NYHA (New York Heart Association) classification, which did not change significantly. Majority of patients (90%) were in NYHA class I before and after therapy. Functional status deteriorated in one patient and improved in another patient. The mean age of the nine patients with LVWT at baseline was 51 years; only two of them were females. As shown in Table 2, binary appearance at baseline was present in five patients (20%) and posterobasal fibrosis in 15 patients (83%). At follow-up, a binary appearance was present in 32% and posterobasal fibrosis in 72%. This difference was not significant.
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During follow-up, there was a slight increase in ventricular septum thickness from 11.7 to 12.5 mm, P = 0.009), its clinical relevance is unknown. LVWT as defined above was present in only nine patients (31%) before ERT and in 10 patients (34%) at follow-up. There was significant progression in LWT in four patients: In three patients, this occurred despite further despite ERT; another patient who did not fulfil LVWT criteria prior to ERT did develop LVWT during ERT. These four patients (mean age 54 years) with of LVWT had no history of hypertension and no aortic stenosis and were treated with agalsidase alfa. Normalization of LVMM index was observed in one 42-year-old patient with prior LVWT, he received agalsidase beta. Binary appearance and PW fibrosis increased to 32%. Shortening fraction increased slightly during therapy (from 41% to 44%, P = 0.044) (Table 3). Although tissue Doppler data of mitral annulus did not change significantly during follow-up, the longer deceleration time of the mitral E-wave, the higher velocity of the A-wave and the lower E/Ea ratio in the lateral mitral annulus at the end of the study were signs of improvement of diastolic function with lowering of filling pressure (Table 4). There were no significant differences in the above-mentioned parameters between both ERT groups at baseline and at follow-up (P > 0.05); only the E/Ea ratio tended to increase by 1.2 ± 2.7 in patients receiving agalsidase alfa compared with a decrease by 1.3 ± 2.9 in patients receiving agalsidase beta (P = 0.08).
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Discussion |
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Our data on the effects of ERT on LVWT reflected as LVMM and septal wall thickness as well as left ventricular systolic and diastolic function during long-time follow-up under ERT in Anderson-Fabry patients show that the reversibility of pre-existing changes is limited even at an early stage of Anderson-Fabry disease. We could not demonstrate a decrease in LVWT or left atrial size but a small increase of septal wall thickness and improvement of diastolic function. On the other hand, there was no significant progression. We found no significant difference between both enzyme replacement groups.
Left ventricular hypertrophy in Anderson-Fabry disease
Left ventricular hypertrophy (LVWT) is the most widely evaluated parameter for the assessment of cardiomyopathy in Anderson-Fabry disease. There were several prospective studies, which analysed LV mass during ERT with agalsidase alfa and beta; so far, no prospective direct comparisons exist between the two available enzyme preparations on their effectiveness.19 Weidemann et al.20 performed a prospective study in Anderson-Fabry disease, who showed significant regression of end-diastolic thickness of the PW (measurement in 10 patients with magnetic resonance imaging) after 12 months of treatment. We could not document a significant change of PW thickness or LVMM index in our patients. Spinelli et al.21 found a significant reduction in left ventricular mass in nine Anderson-Fabry patients who were treated for 12 months, but their interventricular septal septum thickness was larger than in our patients (13.9 vs. 11.7 mm). In both of these studies, patients were treated with agalsidase beta. The Fabry Outcome Survey (FOS), analysed long-term efficacy of ERT with agalsidase alfa in a cohort of 314 patients with a mean duration of 17 months, and found a significant reduction of left ventricular size in those patients who already had an enlarged heart at baseline.8 We were not able to document a significant regression in LVWT, but we found a marked increase in left ventricular septum thickness. The patient with significant regression was only 42 years old, which is above the mean of our study group but younger than those with progression of the disease and therefore supports the hypothesis that for complete reversibility of cardiac changes, ERT might have to be started earlier. In a recent published follow-up study of a large European registry including patients with a mean age of 35 years it was shown that not only gender and renal function but also age were independent determinants of left ventricular hypertrophy.22 A lack of short-term enzyme treatment with ERT (alpha galactosidase A) on microvascular dysfunction has also been shown in five males with Anderson-Fabry disease in whom coronary flow reserve measured by PET was not improved by ERT.23 Contrarily, a more recent, placebo-controlled study in 15 males with Anderson-Fabry disease showed a regression of left ventricular mass compared with placebo and a 20% reduction in globotriaosylceramide in the endomyocardial biopsy over 6 months of enzyme treatment.24 The lack of significant worsening of most parameters shows that there is indeed a treatment effect of ERT.
Systolic and diastolic function in Anderson-Fabry heart disease
Left ventricular systolic function in Anderson-Fabry patients with heart disease has been reported in other studies to be usually normal.5 Global and longitudinal systolic function were preserved at the beginning of our study and at follow-up and radial systolic function (FS) even significantly increased during ERT (P = 0.044). In a study involving 12 untreated patients with severe Anderson-Fabry disease the shortening fraction decreased progressively by 2.7% per year.25 Thus, ERT seems to halt that deterioration and may reverse the negative impact of the underlying storage disease on shortening fraction.
It has been suggested that TDI can provide early detection of cardiac involvement in Anderson-Fabry disease and is helpful in the assessment of cardiac improvement during ERT.26,27 In our study population, the dimensionless parameter E/Ea was lower after ERT (P = 0.002), indicating lower LV filling pressure than before treatment. Together with a prolongation of the early Edec at follow-up, we were able to document some improvement of diastolic function during ERT.
Binary appearance due to compartmentalization of glycosphingolipids and posterobasal fibrosis
One recent study17 showed that echocardiography could be a reliable method for the detection of the binary appearance in Anderson-Fabry disease, reflecting the endocardial and subendocardial glycosphingolipid compartmentalization as a hallmark of cardiomyopathy of this disease with sensitivity and specificity of 94% and 100%, respectively. This makes this a distinguishing feature between Anderson-Fabry disease and hypertrophic cardiomyopathy or other forms of LVWT in clinical practice, especially in the absence of systemic manifestations of Anderson-Fabry disease. However, although with a mean age of 39 years their patients' age was not different from our study population (37 years), we found this binary appearance in only five (20%) patients before, and in eight (32%) patients at follow-up (P= 0.22). Therefore this seems to be not a hallmark feature in mild Anderson-Fabry disease. Among those five patients with binary appearance before therapy, four patients had LVWT and only one did not have LVWT. At follow-up, the same four patients with LVWT still had binary appearance, and one patient who developed LVWT at follow-up did not have the binary appearance any more. Among new five patients who had binary appearance at follow-up, one developed LVWT. Therefore, one cannot rely only on this binary appearance to make the diagnosis of Anderson-Fabry disease in clinical practice although it might be a helpful feature. However, this sign is not specific and can be seen in other pathologies too.28–32
In addition, we qualitatively analysed the presence of increased echogenicity in posterobasal segments as a possible sign of fibrosis and found it positive in 15 of 18 patients (83%) before, and in 13 patients (72%) at follow-up (P = 1.0). All nine patients with LVWT at the beginning of the study had signs of fibrosis as well as six patients without LVWT. Among these 15 patients, three had lost clear signs of fibrosis at follow-up, and posterobasal fibrosis newly developed in two other patients. These results are comparable with a prospective study published recently by Beer et al.16 They found late enhancement in MRI, as a non-invasive marker of myocardial fibrosis in up to 50% of patients who failed to show significant regression of hypertrophy during ERT. Weidemann et al.33 have recently shown that a ‘double peak sign’ in strain-rate imaging tracings seems to be a reliable tool to diagnose non-ischaemic regional fibrosis, which could be helpful in detecting fibrosis at an earlier stage even with echocardiography.
However, both binary appearance and posterobasal fibrosis can be helpful in the morphological diagnosis of Anderson-Fabry disease and could serve as a potential marker for the prediction of the effects of ERT, but not as an exclusion criterion as the specificity may not be high.
Limitations
This was not a placebo-controlled study and involved only 29 patients, thus, the positive effect of ERT on cardiac disease may be underestimated. Another limitation is the duration of ERT over 37 months, which remains quite small when compared with the 37 years without ERT before. The efficiency of the ERT was not quantified, since we have not measured the level of glycosphingolipid in cardiac biopsies before and after the treatment, neither were enzyme levels measured during ERT; however, ERT was performed due to standard dosage.
Also, the study population—as in most studies with this disease—is small, which results in a small statistical power.
Myocardial strain and strain rate are options to improve sensitivity on myocardial function analysis, but were not implemented in our analysis.
There was no comparison with MRI in this study cohort, which would have made the measurement of LVMM and LVWT more reliable.
The small number of patients with binary appearance in the study can be explained by the mild phenotype of disease and only mild heart disease. However, its quantification is difficult, since it is a subjective analysis so far and a bilayered appearance of LV septum can be observed in normal hearts as well. The changing of cardiac myofibre orientation, resulting in anisotropic structure of the LV wall, influences the propagation of ultrasonic waves and produces the speckle patterns. These effects are specially pronounced in cases of cardiac hypertrophy and infiltrative disorders.28–32 Increased echogenicity in the PW and presence of binary appearance are subjective parameters; in our study, these parameters only assessed by one reviewer (R.J.), with no data on intra- and interobserver variability.
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Conclusions |
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Our Anderson-Fabry cohort had successful long-time ERT with improvement of subjective symptoms such as acroparesthesia and relative lack of progression of left ventricular hypertrophy. Although changes in LV structure were not marked, functional changes such as some amelioration of diastolic function during ERT, obtained by tissue Doppler and transmitral flow Doppler were significant. Binary appearance was not a reliable early marker of Anderson-Fabry cardiomyopathy in our study group but in combination with increased echogenicity in posterobasal segments could be helpful sign in making the diagnosis of Anderson-Fabry cardiomyopathy. ERT might have to be started still earlier in life as cardiac disease in Anderson-Fabry patients is not completely reversible at a certain stage.
Conflict of interest: none declared.
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  M Imbriaco, A Pisani, L Spinelli, A Cuocolo, G Messalli, E Capuano, M Marmo, R Liuzzi, B Visciano, B Cianciaruso, et al. Effects of enzyme-replacement therapy in patients with Anderson-Fabry disease: a prospective long-term cardiac magnetic resonance imaging study Heart, July 1, 2009; 95(13): 1103 - 1107. [Abstract] [Full Text] [PDF]
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