Cardiac Involvement is Underdiagnosed in Patients with Biopsy-Proven Systemic AL Amyloidosis
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1 Original Article 41 Cardiac Involvement is Underdiagnosed in Patients with Biopsy-Proven Systemic AL Amyloidosis Haoyi Zheng 1, Amitabha Mazumder 2, Stuart D. Katz 3 1. Cardiac Imaging, The Heart Center, St. Francis Hospital, New York 2. New York University School of Medicine, New York University Cancer Institute 3. New York University School of Medicine, Department of Medicine, New York University Cardiovascular Institute Address for correspondence: Haoyi Zheng, MD Cardiac Imaging, The Heart Center St. Francis Hospital Roslyn, NY haoyi.zheng@chsli.org ABSTRACT Background Clinical recognition of cardiac involvement and cardiac response to therapy is an important element of clinical care in patients with AL amyloidosis. The new criteria including NT-proBNP, troponin, and echocardiography for assessment of cardiac involvement in patients with systemic AL amyloidosis were proposed in 2004, but there are limited data on the utilization of these in clinical practice. Methods We retrospectively reviewed the clinical data of 28 patients with AL amyloidosis. Clinical diagnosis of cardiac amyloidosis was based on medical record documentation of symptomatic heart failure without other causes. Then we used the criteria from the current NCCN Guidelines to reassess cardiac involvement. Results 14 cases (50%) had clinical diagnosis of cardiac amyloidosis at the time of diagnosis and also met the NCCN criteria. An additional 6 cases without clinical diagnosis of cardiac amyloidosis met the NCCN criteria. In total, 20 patients (71.4%) met the NCCN criteria for cardiac involvement. No routine follow-up testing with echocardiography and biomarkers was documented during treatment for any of the patients. Conclusions Diagnosis of cardiac amyloidosis based on presence of heart failure symptoms led to underdiagnosis of cardiac involvement defined by the NCCN criteria. Guideline recommended assessment of cardiac involvement and cardiac response to treatment was not routinely implemented in our cohort. Keywords: Citation: AL cardiac amyloidosis; diagnosis; natriuretic peptides; echocardiography; NCCN guidelines Haoyi Zheng, Amitabha Mazumder, Stuart D. Katz. Cardiac Involvement Is Underdiagnosed in Patients with Biopsy- Proven Systemic AL Amyloidosis. International Cardiovascular Forum Journal. 2016;6: Introduction Cardiac amyloidosis is an unusual cause of heart failure in the general population, but is a common complication of systemic AL amyloidosis. Most patients with AL amyloidosis and symptomatic heart failure are not candidates for autologous stem cell transplantation and carry the worst prognosis. 1 There is substantial variation in the estimated incidence of cardiac amyloidosis in patients with AL amyloidosis, ranging from 50% to 65% based on clinical criteria to 90% based on pathology. 1-3 As heart failure remains the most common cause of mortality in patients with systemic AL amyloidosis, early detection and ongoing assessment of cardiac involvement has become an important means to assess therapeutic response. 4,5 The current NCCN criteria including troponin, NT-proBNP, and echocardiography for assessment of cardiac involvement and staging in patients with systemic AL amyloidosis were proposed in 2004, 4 but there are limited data on the utilization of these criteria in clinical practice. In the present study, we retrospectively reviewed the medical record of patients with biopsy-proven AL amyloidosis between 2006 and 2011 in our institution. The aims of this study were to assess the prevalence of cardiac involvement based on the * Corresponding author. haoyi.zheng@chsli.org ISSN: Barcaray Publishing
2 42 Original Article clinical diagnosis at the time of the diagnosis of AL amyloidosis, the prevalence of cardiac involvement based on the NCCN criteria, and the clinical implementation of the NCCN guidelines-recommended routine testing and follow-up. Methods The Institutional Review Board of the New York University School of Medicine approved the study protocol. ICD-9 diagnosis code was used to identify the patients with a diagnosis of amyloidosis. 28 patients with biopsy-proven AL amyloidosis were identified between 2006 to 2011 from New York University Medical Center. Surgical pathology reports from organ biopsies including abdominal fat, kidney, liver, heart, duodenum, and colon were reviewed. Tissue involvement was confirmed based on positive Congo red staining, apple-green birefringence from polarized light, and/or electronic microscopic detection of amyloid fibrils in pathology specimens. The results from bone marrow biopsy and serum/urine immunofixation were recorded. Relevant demographic data and medical history were extracted from electronic medical records. All electrocardiograms and echocardiograms were reviewed. Serum free light chain (FLC), Troponin I (TnI), and N-terminal pro-brain natriuretic peptide (NT-proBNP) were recorded if available. Echocardiography, NT-proBNP and TnI measurements within 3 months of diagnosis of AL amyloidosis were considered to be part of the initial evaluation of cardiac involvement. New York Heart Association (NYHA) Class was obtained from the history of present illness at admission or clinic notes within 3 months of diagnosis. The diagnostic criteria used in this project are listed below: 1. Clinical diagnosis of cardiac amyloidosis is defined as symptomatic heart failure (NYHA Class II-IV) without other causes. 2. The current NCCN Guidelines Version is used for reassessment of cardiac involvement. The NCCN criteria for cardiac involvement is defined by mean wall thickness >12 mm without other cardiac cause from echocardiography or elevated NT-proBNP (>332 pg/ml) in the absence of renal failure or atrial fibrillation. 3. Elevated TnI is defined as more than two times of upper normal limit (0.04 ng/ml in our laboratory). 4. Low voltage on 12-lead ECG was defined by QRS complex amplitude <0.5mV in each limb lead or < 1mV in each precordial lead, or V1 S wave plus V5 or V6 R wave <1mV. Vital status was determined from the medical record and/or Social Security Death Master Files (accessed November 30, 2011). All follow up was censored as of this date. Data Analysis. Descriptive statistics (means and standard deviation, median and interquartile range, or proportions) were used to characterize clinical data as appropriate for the variable of interest. Baseline characteristics of the patients were compared with the use of chi-square or Fisher s exact test for categorical variables and Student s t-test or non-parametric test for continuous variables. Mortality outcomes over time were assessed with the Kaplan-Meier method and the log-rank test was used to assess differences between survival curves. A 2-tailed p value < 0.05 was considered statistically significant. Results A total 28 patients with biopsy-proven AL amyloidosis were included for the final analysis (Table 1). There were 9 women and 19 men in the cohort (mean age was 64.8 ± 9.9 years, 22 patients with lambda light chain amyloid and 6 patients with Kappa light chain amyloid). 12 patients died (43%) with a median survival 153 days. Prevalence of cardiac amyloidosis and outcomes based on clinical diagnosis and NCCN criteria. Fourteen patients (50%) carried a clinical diagnosis of cardiac amyloidosis at the time of the diagnosis of AL amyloidosis. All 14 patients presented with clinical heart failure with NYHA Class II-IV and were referred to a cardiologist. All 14 patients also met the NCCN criteria for cardiac involvement. Clinical characteristics of the patients with and without a clinical diagnosis of cardiac amyloidosis are summarized in Table 2. The majority of patients (77%) with clinical diagnosis of cardiac amyloidosis had elevated troponin. Patients with a clinical diagnosis of cardiac amyloidosis had greater risk of death during follow-up when compared with those without a clinical diagnosis of cardiac amyloidosis (9 vs. 3 deaths, p=0.02, Figure 1). All the patients who died had either elevated NT-proBNP or TnI or both at the time of the diagnosis, except one patient in whom NT-proBNP was not measured (Table 1). When we reevaluated the remaining 14 patients by using the NCCN criteria, 4 patients met the criteria for cardiac involvement either based on mean wall thickness >12 mm or elevated NT-ProBNP or both (Study ID 21, 22, 23, 24). None of these 4 patients were referred to cardiologist. 3 additional patients (Study ID 3, 20, 26) also met the NCCN criteria of cardiac involvement, but had known history of coronary artery disease and/or myocardial infarction. One of these patients (Study ID 3) with elevated NT-proBNP and TnI presented with heart failure and had significant multi-vessel coronary artery disease confirmed by coronary angiogram. In the other 2 patients (Study ID 20 and 26), TnI was persistently elevated without other evidence of acute coronary syndrome, and is therefore consistent with the diagnosis of cardiac amyloidosis. Accordingly, 6 patients without a clinical diagnosis of cardiac amyloidosis met the NCCN criteria for cardiac involvement. Three patients (study ID 6, 12, 16) did not have echocardiography and NT-proBNP documented and could not be evaluated. Four patients (Study ID 7, 11, 19, 28) had no evidence of cardiac involvement based on the NCCN criteria. In total, 20 patients (20/28, 71.4%) had cardiac amyloidosis or cardiac involvement by either clinical diagnosis or the NCCN criteria. Biomarkers utilization in the initial evaluation Thirteen of 28 patients (46.4%) had NT-proBNP measured as a part of initial evaluation. All but one of these patients had elevated NT-proBNP levels. Eight of 14 patients (57%) with clinical diagnosis of cardiac amyloidosis had NT-proBNP measured as the initial evaluation. Twenty-one of 28 patients (75%) had TnI measured as a part of the initial evaluation. Fourteen of them (70%) had elevated TnI. Thirteen patients with clinical diagnosis of cardiac amyloidosis had TnI measured and 10 (77%) had significantly elevated TnI levels. Six of 28 patients (21.4%, study ID 1, 2, 7, 19, 20, and 22) had baseline serum free light chain (FLC) measured with elevated values in all patients ( mg/l). Biomarkers evaluation during the treatment Seven of 14 patients with clinical diagnosis of cardiac amyloidosis (ID 2, 5, 8, 13, 14, 18, 25) had at least one additional echocardiogram during follow-up. None of the 14 patients with clinical diagnosis of cardiac amyloidosis had routine follow-up measurements for NT-proBNP or TnI during treatment. Of the 6 patients who met the NCCN criteria for cardiac involvement but did not have a clinical diagnosis of cardiac amyloidosis, none had follow-up measurements for NT-proBNP or TnI during treatment. In addition, only six of 28 patients had serial measurement of FLC during treatment.
3 Original Article 43 Table 1. Clinical Characteristics of 28 patients with AL amyloidosis ID Age / Sex LC type NYHA Class HTN CAD/MI ProBNP (ng/dl) Tn I (ng/ dl) VWT (mm) Clinical Diagnosis Diagnosis by NCCN Follow-up (days) Outcome 1 65/F κ III Yes No Yes Yes 270 Alive 2 65/F λ III No No Yes Yes 127 Alive 3 62/M λ III No Yes No No 486 Death 4 61/M λ II Yes No Yes Yes 691 Alive 5 51/F λ III No No NA Yes Yes 152 Death 6 88/F λ NA No No NA 0.06 NA No No 360 Death 7 76/F λ NA No No NA No No 2095 Alive 8 75/M λ III No No NA Yes Yes 65 Death 9 70/F κ III No No NA Yes Yes 2600 Alive 10 74/M λ IV No No NA Yes Yes 54 Death 11 58/M λ NA No No NA NA 0.8 No No 1642 Alive 12 58/M λ NA No No NA 0.04 NA No No 1428 Alive 13 63/F λ II Yes No NA Yes Yes 862 Death 14 77/M λ II Yes No NA Yes Yes 471 Death 15 60/F λ III Yes No Yes Yes 30 Death 16 72/M λ NA No No NA NA NA No No 654 Alive 17 63/F λ III Yes No 3400 NA 1.8 Yes Yes 647 Death 18 56/M λ II No No Yes Yes 317 Alive 19 63/M λ NA No No 25 NA 0.9 No No 1072 Alive 20 50/M λ II No Yes No Yes 320 Alive 21 69/M λ NA No No NA NA 1.3 No Yes 490 Alive 22 50/M κ NA No No 669 NA 0.9 No Yes 92 Alive 23 56/M κ NA No No 4400 NA 1.1 No Yes 1120 Alive 24 60/M λ NA Yes No No Yes 772 Alive 25 65/M λ III Yes No Yes Yes 154 Death 26 76/M κ II Yes Yes NA No Yes 64 Death 27 48/M λ III No No NA Yes Yes 123 Death 28 78/M κ NA Yes Yes NA No No 264 Alive Table 1. LC: light chain; NYHA: New York Heart Association; HTN: hypertension; CAD/MI: coronary artery disease/myocardial infarction; ProBNP: N-terminal probnp; TnI: troponin I; VWT: ventricular wall thickness; NA: not available. Discussion AL amyloidosis is a monoclonal plasma cell dyscrasia associated with over production of amyloidogenic light chain, which acts as the precursor protein and is able to misfold into fibrils. 6 Deposition of these amyloid fibrils in visceral tissues may result in cardiomyopathy, nephropathy, hepatomegaly, and peripheral neuropathy. Overall survival of patients with AL has been improving over the last 30 years. However, 1-year mortality remains high, especially in the group of patients with cardiac involvement and with elevated troponin and / or NT-proBNP. 7 Cardiac involvement is the most important determinant of the prognosis of patients with AL amyloidosis. In our study sample, cardiac amyloidosis diagnosed based on symptomatic heart failure was present in 50% of patients at the time of diagnosis of AL amyloidosis. More than half of these patients died during follow-up. When we assessed all the patients by using the current NCCN criteria of cardiac involvement in amyloidosis, the prevalence rises to 71.4% (20/28). This could be underestimated due to a lack of echocardiographic and NT-pro-BNP data in 3 patients. The high prevalence of cardiac involvement and high risk of mortality in symptomatic patients is consistent with prior reports. In 2004, Dispenzieri and colleagues introduced a cardiac staging system based on two cardiac biomarkers, TnI and NT-proBNP. 4 Patients with significant elevations of both biomarkers have a median survival of only 3.5 months. If one biomarker is elevated, the median survival is 10.5 months. This staging system was further studied and modified by including serum free light chain. 8 The measurement of TnI and NT-proBNP is recommended in the initial evaluation for AL amyloidosis. Our study confirmed the prognostic value of these two biomarkers in AL amyloidosis. The majority of patients (77%) with clinical diagnosis of cardiac amyloidosis had elevated troponin. All the patients who died had either elevated NT-proBNP or TnI level or both at the time of the diagnosis except one who did not have NT-proBNP tested. However, routine use of these biomarkers has not been uniformly incorporated into clinical practice. In our cohort, <40% of the patients had NT-proBNP testing and approximately 70% had Tnl
4 44 Original Article Table 2. Comparison of clinical characteristics in patients with and without clinical diagnosis of cardiac amyloidosis Baseline characteristics Clinical diagnosis positive(n = 14) Clinical diagnosis negative (N = 14) Diagnosis by NCCN criteria only (N = 6) Age (years) 64.1 ± ± ± 4.2 Men (%, n) 85.7 (12) 50 (7) 100 (6) Multiple myeloma (n) LC type-lambda (n) Troponin I (ng/ml) 0.49 ± ± ± 0.16 NT-proBNP (pg/ml) 5221 ± ± ± 1086 NYHA Class II-IV (n) 14 3* 2 EKG Low Voltage (n) 13 2* 2 VWT (mm) 1.58 ± ± 0.22* 1.23 ± 0.08 Death (n) 9 3* 1 Table 2. LC: light chain; NYHA: New York Heart Association; VWT: ventricular wall thickness.* indicates p<0.05 vs. Clinical Diagnosis Positive group testing as the initial part cardiac evaluation. Three patients did not have biomarker or imaging testing at the time of diagnosis with AL amyloidosis. The reduction of serum FLC has been proposed and validated as a key element of hematologic response to the treatment and it has a significant prognostic role. 2,8 However, the FLC testing has not been routinely applied into the clinical practice as shown in our series that only 6 of 28 patients had baseline and follow-up of measurements of FLC despite the fact that this test was available in The prognosis of patients with AL amyloidosis mainly depends on the cardiac involvement or the burden of the amyloid in the heart. NT-proBNP or BNP, troponins, and echocardiography have been recommended as main tools to diagnose cardiac amyloidosis and assess the extent of cardiac involvement. 9 NT-proBNP and troponin are accepted as the best means to stage patients with AL amyloidosis. 4 These have also been recommended as the follow-up tests to assess the cardiac response to the therapies. 10 Our study showed that the diagnosis of cardiac involvement was still mainly based on the clinical heart failure symptoms and the recommended testing and follow-up were not routinely applied into the clinical practice. Our data are derived from a single institution and might not be representative of national practice patterns in the United States. The high prevalence of cardiac involvement is consistent with prior reports. The previous study shows patients with AL amyloidosis who present with clinical heart failure or syncope have median survival of 4 to 6 months; 11 the majority of these patients are not candidates for autologous stem cell transplantation. 1 Given the known high cardiac mortality risk in patients with AL amyloidosis, more consistent application of existing criteria into clinical practice could increase early diagnosis of cardiac involvement and provide opportunity for interventions including autologous stem cell transplantation that could increase the survival of patients. Cardiac magnetic resonance imaging may also be a sensitive modality for early detection of cardiac involvement in patients with systemic AL amyloidosis. 12 Conclusions In summary, in our single center cohort, the cardiac involvement of AL amyloidosis is underdiagnosed. The guidelines-recommended testing for the diagnosis of cardiac involvement and follow-up for cardiac response to the amyloidosis treatment were not routinely implemented in the clinical practice. Since AL amyloidosis is an uncommon disease with an estimate of incidence of new cases per year in US, 13 limited clinical experience among practitioners may be a barrier to implementation of optimal care in this population. Creation of institutional multidisciplinary programs with specialized hematology and cardiology expertise may be considered to increase adherence to the guideline recommended care in these high-risk patients. Declarations of Interest The authors declare no conflicts of interest. Acknowledgements Haoyi Zheng is supported by NIH/NHLBI grant T32HL The authors agree to abide by the requirements of the Statement of publishing ethics of the International Cardiovasular Forum Journal. 14 Figure1. Kaplan-Meier estimates for probability of death in patients with and without clinical diagnosis of cardiac amyloidosis.
5 Original Article 45 References 1. Kyle RA, Gertz MA. Primary systemic amyloidosis: clinical and laboratory features in 474 cases. Semin Hematol 1995;32: Palladini G, Dispenzieri A, Gertz MA, et al. New Criteria for Response to Treatment in Immunoglobulin Light Chain Amyloidosis Based on Free Light Chain Measurement and Cardiac Biomarkers: Impact on Survival Outcomes. Journal of clinical oncology : doi: / JCO Roberts WC, Waller BF. Cardiac amyloidosis causing cardiac dysfunction: analysis of 54 necropsy patients. The American journal of cardiology 1983;52: Dispenzieri A, Gertz MA, Kyle RA, et al. Serum cardiac troponins and N-terminal pro-brain natriuretic peptide: a staging system for primary systemic amyloidosis. Journal of clinical oncology : official journal of the American Society of Clinical Oncology 2004;22: doi: / JCO Palladini G, Campana C, Klersy C, et al. Serum N-terminal pro-brain natriuretic peptide is a sensitive marker of myocardial dysfunction in AL amyloidosis. Circulation 2003;107: doi: /01. CIR B2 6. Sipe JD, Benson MD, Buxbaum JN, et al. Amyloid fibril protein nomenclature: 2012 recommendations from the Nomenclature Committee of the International Society of Amyloidosis. Amyloid : the international journal of experimental and clinical investigation : the official journal of the International Society of Amyloidosis 2012;19: doi: / Kumar SK, Gertz MA, Lacy MQ, et al. Recent improvements in survival in primary systemic amyloidosis and the importance of an early mortality risk score. Mayo Clinic proceedings Mayo Clinic 2011;86:12-8. doi: / mcp Kumar S, Dispenzieri A, Lacy MQ, et al. Revised prognostic staging system for light chain amyloidosis incorporating cardiac biomarkers and serum free light chain measurements. Journal of clinical oncology : official journal of the American Society of Clinical Oncology 2012;30: doi: /JCO Dispenzieri A, Gertz MA, Buadi F. What do I need to know about immunoglobulin light chain (AL) amyloidosis? Blood reviews 2012;26: Palladini G, Lavatelli F, Russo P, et al. Circulating amyloidogenic free light chains and serum N-terminal natriuretic peptide type B decrease simultaneously in association with improvement of survival in AL. Blood 2006;107: doi: /j.blre Gertz MA, Lacy MQ, Dispenzieri A. Amyloidosis: recognition, confirmation, prognosis, and therapy. Mayo Clinic proceedings Mayo Clinic 1999;74: Austin BA, Tang WH, Rodriguez ER, et al. Delayed hyper-enhancement magnetic resonance imaging provides incremental diagnostic and prognostic utility in suspected cardiac amyloidosis. JACC Cardiovascular imaging 2009;2: doi: /j.jcmg Falk RH. Cardiac amyloidosis: a treatable disease, often overlooked. Circulation 2011;124: doi: / CIRCULATIONAHA Shewan LG, Coats AJS, Henein M. Requirements for ethical publishing in biomedical journals. International Cardiovascular Forum Journal 2015;2:2 DOI: /icfj.v2i1.4.
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