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J Am Coll Cardiol, 2007; 49:97-105, doi:10.1016/j.jacc.2006.10.022 (Published online 31 October 2006).
© 2007 by the American College of Cardiology Foundation
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EXPEDITED REVIEW

Diastolic and Systolic Asynchrony in Patients With Diastolic Heart Failure

A Common But Ignored Condition

Cheuk-Man Yu, MD, FRACP, FRCP*, Qing Zhang, MM, Gabriel W.K. Yip, MD, FACC, Pui-Wai Lee, MRCP, Leo C.C. Kum, MRCP, Yat-Yin Lam, MRCP and Jeffrey Wing-Hong Fung, FHKAM

Li Ka Shing Institute of Health Sciences, Division of Cardiology, S.H. Ho Cardiovascular and Stroke Centre, Department of Medicine and Therapeutics, Prince of Wales Hospital, The Chinese University of Hong Kong, Hong Kong, People’s Republic of China.

Manuscript received May 30, 2006; revised manuscript received August 1, 2006, accepted August 21, 2006.

* Reprint requests and correspondence: Dr. Cheuk-Man Yu, Li Ka Shing Institute of Health Sciences, Institute of Vascular Medicine, S.H. Ho Cardiovascular and Stroke Centre, Division of Cardiology, Department of Medicine and Therapeutics, Prince of Wales Hospital, The Chinese University of Hong Kong, Shatin, N.T., Hong Kong, People’s Republic of China. (Email: cmyu{at}cuhk.edu.hk).


   Abstract
Top
 Abstract
Methods
 Results
 Discussion
 References
 
OBJECTIVES: The present study aimed to examine whether diastolic and systolic asynchrony exist in diastolic heart failure (DHF) and their prevalence and relationship to systolic heart failure (SHF) patients.

BACKGROUND: Few data exist on mechanical asynchrony in DHF.

METHODS: Tissue Doppler echocardiography was performed in 373 heart failure patients (281 with SHF and 92 with DHF) and 100 normal subjects. Diastolic and systolic asynchrony was determined by measuring the standard deviation of time to peak myocardial systolic (Ts-SD) and peak early diastolic (Te-SD) velocity using a 6-basal, 6-mid-segmental model, respectively.

RESULTS: Both heart failure groups had prolonged Te-SD (DHF vs. SHF vs. controls subjects: 32.2 ± 18.0 ms vs. 38.0 ± 25.2 ms vs. 19.5 ± 7.1 ms) and Ts-SD (31.8 ± 17.0 ms vs. 36.7 ± 15.2 ms vs. 17.6 ± 7.9 ms) compared with the control group (all p < 0.001 vs. control subjects). Based on normal values, the DHF group had comparable diastolic (35.9% vs. 43.1%; chi-square = 1.48, p = NS), but less systolic asynchrony than the SHF group (39.1% vs. 56.9%; chi-square = 8.82, p = 0.003). Normal synchrony, isolated systolic, isolated diastolic, and combined asynchrony were observed in 39.1%, 25.0%, 21.7%, and 14.1% of DHF patients, respectively, and these were 25.6%, 31.3%, 17.4%, and 25.6%, correspondingly, in SHF (chi-square = 10.01, p = 0.019). The correlation between systolic and diastolic asynchrony, and between the myocardial velocities and corresponding mechanical asynchrony appeared weak. A wide QRS duration (>120 ms) was rare in DHF (10.9% vs. 37.7% in SHF) (chi-square = 16.69, p < 0.001).

CONCLUSIONS: Diastolic and/or systolic asynchrony was common in 61% of DHF patients despite narrow QRS complex. The presence of asynchrony was not related to myocardial systolic or diastolic function. Systolic and diastolic asynchrony were not tightly coupled, implying distinct mechanisms.

Abbreviations and Acronyms
  DHF = diastolic heart failure
  LV = left ventricle/ventricular
  SHF = systolic heart failure
  TDI = tissue Doppler imaging
  Te = time to peak myocardial early diastolic velocity
  Te-diff = maximal difference in Te
  Te-SD = standard deviation of Te
  Ts = time to peak myocardial systolic velocity during the ejection phase
  Ts-diff = the maximal difference in Ts
  Ts-SD = standard deviation of Ts

Systolic asynchrony is a relatively common finding in patients with systolic heart failure (SHF) (1–4). It is believed to indicate a more severe form of heart failure and is prognostically independent of QRS duration (5,6). Although systolic asynchrony often exists in patients with SHF who commonly had wide QRS complexes, recent studies observed that it also exists in about 30% to 40% of patients with a normal QRS duration (1–4). With the introduction of cardiac resynchronization therapy that reduces systolic asynchrony in SHF patients with wide QRS complexes (7,8) and results showing favorable improvement of symptoms and clinical outcome (9–11), quantitative analysis of mechanical asynchrony appears crucial for comprehensive assessment of heart failure patients. Diastolic heart failure (DHF) is common among the heart failure population (12,13). Echocardiography with Doppler studies is a non-invasive tool commonly used to distinguish between DHF and SHF (14,15). Despite it being a common disease, there has been limited published data on evidence-based management of DHF, which is purely based on medial therapy (16,17). Furthermore, whether diastolic and/or systolic asynchrony occurs in DHF has not been explored. Previous studies have reported that tissue Doppler imaging (TDI) is a robust tool for the assessment of regional timing of contraction and relaxation from which indexes of diastolic and systolic asynchrony are derived (1,17,18). Therefore, the aims of the study were to examine whether diastolic and/or systolic mechanical asynchrony occurred in patients with DHF, to estimate their prevalence, and to compare these to patients with SHF as well as the normal control population, in addition to their relationship in both heart failure groups.


   Methods
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 Abstract
 Methods
Results
 Discussion
 References
 
Patients.   Echocardiography was performed in 473 subjects in a university teaching hospital. They included 281 consecutive enrolled patients with SHF and 92 patients with DHF, who met the Framingham criteria for congestive heart failure, as well as 100 healthy volunteers recruited from the community (control group). The heart failure patients had been admitted to the hospital for clinical signs and symptoms of heart failure, with chest roentgenographic evidence of fluid overload. They were stabilized by anti-heart failure medications and underwent elective echocardiography at least 6 weeks after discharge. Patients with atrial fibrillation, restrictive cardiomyopathy, aortic or mitral stenosis, prosthetic valves, severe mitral annular calcification, or presented as acute coronary syndrome were excluded. The SHF group had a left ventricular (LV) ejection fraction <50% by echocardiography (by biplane Simpson’s equation) while the DHF group had preserved systolic function (defined as LV ejection fraction >50%) and evidence of diastolic dysfunction by Doppler echocardiography, which ranged from abnormal relaxation, pseudonormal, or restrictive filling patterns as previously described (Table 1) (14,15). The control group had no history of cardiovascular or systemic diseases, and had a normal physical examination, electrocardiographic, and echocardiographic findings. Written informed consent was obtained from all subjects.


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  		Table 1. Comparison of Baseline Clinical Characteristics and Echocardiographic Parameters Between Patients With DHF and SHF
 
Echocardiography.   Standard echocardiography with Doppler studies were performed (Vivid 5 and Vivid 7, Vingmed-General Electric, Horten, Norway). The LV volumes and ejection fraction were assessed by biplane Simpson’s equation using the apical 4- and 2-chamber views. The presence of LV diastolic dysfunction was confirmed by Doppler echocardiography by interrogation of transmitral flow pattern, pulmonary venous inflow pattern, and TDI assessment of peak myocardial early diastolic velocity (19). At least 3 consecutive beats in sinus rhythm were measured and the average values taken.

Tissue Doppler imaging was performed at apical views (apical 4-chamber, 2-chamber, and long-axis) for the long-axis/major-axis motion of the LV as previously described (1,20). Two-dimensional echocardiography with TDI-color imaging views (apical 4-chamber, 2-chamber, and long-axis views) were optimized for pulse repetition frequency, color saturation, sector size, and depth, that maximized a highest possible frame rate of >100 Hz. At least 3 consecutive beats were stored, and the images were analyzed off-line with the aid of a customized software package (EchoPac PC SW-only, version 5.1.1, Vingmed-General Electric). Myocardial velocity curves were reconstituted off-line using the 6 basal and 6 mid-segmental model, which consisted of septal, lateral, anteroseptal, posterior, anterior, and inferior segments at both basal and mid-levels in the LV (1,18). The basal segments were sampled just above the mitral annulus level, and the middle segments were sampled at the mid-level of the LV. The time to peak myocardial systolic velocity during the ejection phase (Ts) and the time to peak myocardial early diastolic velocity (Te) were measured with referenced to QRS complex (1,21). The timings of beginning and end of ejection (aortic valve opening and closure) and those of diastole (mitral valve opening and closure) were derived from continuous-wave Doppler of aortic forward flow and pulse-wave Doppler of mitral inflow. Markers with valve opening and closing events would appear on the electrocardiogram (ECG) recordings during off-line TDI analysis to ensure only the peak myocardial systolic (Sm) and peak myocardial early diastolic (Em) velocities with their corresponding Ts and Te were measured accurately during ejection and early diastolic phases. For the assessment of synchronicity, the standard deviation of Ts (Ts-SD) and Te (Te-SD) of all the 12 LV segments as well as the maximal difference in Ts (Ts-diff) and Te (Te-diff) between any 2 of the 12 LV segments was calculated (1,18). To assess global cardiac function, the mean myocardial systolic (mean Sm) and early diastolic (mean Em) velocities from the 6 basal segments were calculated (1). The interobserver and intraobserver variabilities for measuring asynchrony have been compared in 60 consecutive measurements and were 4.7% and 3.2%, respectively.

Statistics.   Data were analyzed using a statistical software program (SPSS for Windows, version 11.5.1, SPSS Inc., Chicago, Illinois). For comparison of mechanical asynchrony and other parametric echocardiographic data among various groups, independent t tests and 1-way analysis of variance with Scheffe correction for significance were employed where appropriate. Linear regression was employed to investigate the correlation between 2 parametric variables. Comparison of non-parametric data was performed by Pearson chi-square test. The results were expressed as mean ± SD. A p value of <0.05 was considered as statistically significant.


   Results
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 Abstract
 Methods
 Results
Discussion
 References
 
The age (67.5 ± 11.0 years vs. 65.6 ± 13.1 years vs. 64.2 ± 9.4 years, p = NS) and gender (male: 66% vs. 72% vs. 71%, chi-square = 1.35, p = NS) distributions were similar between DHF, SHF, and control groups. The clinical characteristics for patients with DHF and SHF are shown in Table 1. In SHF, there was a higher prevalence of coronary heart disease, and dilated cardiomyopathy occurred exclusively in this group. On the other hand, hypertension was more prevalent in the DHF group. Patients with SHF had higher New York Heart Association functional class than those with DHF. As expected, a difference in medical therapy was observed between the 2 groups.

Diastolic asynchrony in DHF and SHF.   Diastolic asynchrony was evident in both heart failure groups (Table 2, Fig. 1A). The Te-SD was significantly prolonged in both DHF and SHF when compared with the control group (32.2 ± 18.0 ms vs. 38.0 ± 25.2 ms vs. 19.5 ± 7.1 ms, both Scheffe-corrected p < 0.001 vs. control group), and was more severe in the SHF group (p = 0.04). Similarly, the Te-diff was prolonged in both DHF and SHF (102 ± 59 ms vs. 117 ± 71 ms vs. 63 ± 25 ms, both Scheffe-corrected p < 0.001 vs. control group), but was not different between the 2 heart failure groups (p = 0.07). Using normal cutoff values of ≥34 ms for Te-SD and ≥113 ms for Te-diff, derived from the upper 2 SDs of the mean of the control group, 35.9% (33 of 92) of patients with DHF and 43.1% (121 of 281) with SHF showed prolonged Te-SD (chi-square = 1.48, p = NS) (Fig. 2A). Similarly, 34.8% (32 of 92) DHF patients and 39.5% (111 of 281) SHF patients had significantly prolonged Te-diff and thus evidence of diastolic asynchrony (chi-square = 0.65, p = NS) (Fig. 2B). There was a close correlation between diastolic asynchrony measured by Te-SD and Te-diff (r = 0.955, p < 0.001) (Fig. 3A).


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  		Table 2. Comparison of Indexes of Diastolic and Systolic Asynchrony as Well as Myocardial Systolic and Diastolic Velocities Among Patients With DHF, SHF, and Normal Controls
 

Figure 1
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  		Figure 1 Mechanical Asynchrony in DHF Observed by Tissue Doppler Imaging

(A) An example of a patient with diastolic heart failure (DHF) (ejection fraction 62%) who had evidence of diastolic asynchrony as illustrated by the scattered time to peak early diastolic velocity (arrowheads). The systolic asynchrony is relatively mild (arrows). (B) Another patient with DHF (ejection fraction 55%) who had evidence of systolic asynchrony as illustrated by the scattered time to peak systolic velocity (arrows). This patient had no evidence of diastolic asynchrony (arrowheads).

 

Figure 2
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  		Figure 2 The Distribution of Mechanical Asynchrony in DHF, SHF, and Control

Scatter plot showing the distribution of systolic and diastolic asynchrony in patients with diastolic heart failure (DHF), systolic heart failure (SHF), and the normal control group by: (A) the standard deviation (Te-SD) and (B) maximal difference (Te-diff) of the time to peak myocardial early diastolic velocity of the 12 left ventricular segments, and (C) the standard deviation (Ts-SD) and (D) maximal difference (Ts-diff) of the time to peak myocardial systolic velocity of the 12 left ventricular segments.

 

Figure 3
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  		Figure 3 The Correlation of Parameters for Assessing Mechanical Asynchrony

Scatter plot showing a close relationship between (A) the 2 methods of assessing diastolic asynchrony by Te-SD and Te-diff systolic asynchrony, and (B) the 2 methods of assessing systolic asynchrony by Ts-SD and Ts-diff. Abbreviations as in Figure 2.

 
Systolic asynchrony in DHF and SHF.   In contrast with the above observation that diastolic asynchrony was equally prevalent in DHF and SHF, systolic asynchrony appeared more common in SHF, albeit prevalent in both groups (Table 2, Fig. 1B). The Ts-SD was significantly prolonged in both the SHF and DHF groups when compared with the control group (31.8 ± 17.0 ms vs. 36.7 ± 15.2 ms vs. 17.6 ± 7.9 ms, both Scheffe-corrected p < 0.001 vs. control group), but was more severely prolonged in the SHF than the DHF group (p = 0.01). Similar findings were also observed for Ts-diff (93 ± 46 ms vs. 108 ± 42 ms vs. 54 ± 23 ms, both Scheffe-corrected p < 0.001 vs. control group; SHF vs. DHF group, Scheffe-corrected p = 0.004). Using a normal cutoff value of Ts-SD ≥33 ms based on the upper 2 SDs of normal mean, 39.1% (36 of 92) DHF and 56.9% (160 of 281) SHF patients showed significant systolic asynchrony (chi-square = 8.82, p = 0.003) (Fig. 2C). A similar prevalence was observed using Ts-SD of >100 ms (34.8% [32 of 92] DHF and 55.9% [157 of 281] SHF patients) (chi-square = 12.33, p < 0.001) (Fig. 2D). There was a close correlation between systolic asynchrony measured by Ts-SD and Ts-diff (r = 0.926, p < 0.001) (Fig. 3B).

Relationship between diastolic and systolic asynchrony in DHF and SHF.   When the relationship between systolic and diastolic asynchrony was examined, the 2 conditions did not occur in parallel. Using the cutoff values of Ts-SD (33 ms) and Te-SD (34 ms), there was no asynchrony in 39.1%, isolated diastolic asynchrony in 21.7%, isolated systolic asynchrony in 25.0%, and co-existing diastolic and systolic asynchrony in 14.1% of patients with DHF, and these were correspondingly 25.6%, 17.4%, 31.3%, and 25.6% in the SHF group (chi-square = 10.01, p = 0.019) (Fig. 4A). When the cutoff values of Ts-diff (100 ms) and Te-diff (113 ms) were used, results were similar (chi-square = 12.68, p = 0.005) (Fig. 4B). Therefore, only a small proportion of patients with SHF (and even less in DHF) had co-existing systolic and diastolic asynchrony. In fact, the relationship between systolic and diastolic asynchrony appeared weak for both Ts-SD/Te-SD (r = 0.209, p < 0.001) and Ts-diff/Te-diff (r = 0.251, p < 0.001). In both DHF and SHF, the correlation between myocardial systolic or diastolic dysfunction and mechanical asynchrony appeared weak, albeit significant statistically. For DHF, the mean Em correlated weakly with Te-SD (r = –0.30, p = 0.004) while the mean Sm also correlated weakly with Ts-SD (r = –0.26, p = 0.015). In SHF, the corresponding correlation coefficients were r = –0.15 (p = 0.01) and r = –0.14 (p = 0.02), respectively. In DHF, patients with significant diastolic asynchrony had a lower mean Em than those without (4.1 ± 1.7 cm/s vs. 5.2 ± 1.7 cm/s, p = 0.007), whereas the mean Sm was comparable between those with or without significant systolic asynchrony (4.8 ± 0.9 cm/s vs. 5.3 ± 1.3 cm/s, p = 0.08). However, in SHF, patients with significant systolic or diastolic asynchrony had a significantly lower mean Sm or Em than those without (mean Sm: 3.1 ± 1.2 cm/s vs. 3.5 ± 1.0 cm/s, p = 0.02; mean Em: 3.2 ± 1.4 cm/s vs. 4.0 ± 1.6 cm/s, p ≤ 0.001).


Figure 4
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  		Figure 4 The Distribution of Mechanical Asychrony in DHF and SHF

Bar chart showing the percentage distribution of patients who developed mechanical asynchrony in DHF and SHF according to the (A) cutoff values of Te-SD >34 ms and Ts-SD >33 ms, and (B) cutoff values of Te-diff >113 ms and Ts-diff >100 ms. Patients with DHF had a higher prevalence of diastolic asynchrony or without asynchrony, whereas patients with SHF had more systolic asynchrony or co-existing diastolic and systolic asynchrony. The actual numbers are shown in parentheses. Abbreviations as in Figure 2.

 
Analyses of diastolic and systolic asynchrony in heart failure based on ECG subgroups.   A wide QRS duration of >120 ms was more common in patients with SHF than DHF (37.7% [106 of 281] vs. 10.9% [10 of 92]) (chi-square = 16.69, p < 0.001). The QRS duration was ≤120 ms in all the normal control subjects. Figure 5 showed the distribution of diastolic and systolic asynchrony in heart failure. The majority of the DHF patients with evidence of diastolic (26 of 33 patients) and systolic asynchrony (33 of 36 patients) occurred in the narrow QRS subgroup of ≤120 ms. This was in contrast with the SHF group whereby diastolic and systolic asynchrony occurred with higher prevalence in the wide QRS subgroup (diastolic asynchrony: 60.4% vs. 32.6%, chi-square = 15.97, p ≤ 0.001; systolic asynchrony: 70.8% vs. 48.6%, chi-square = 10.25, p ≤ 0.001).


Figure 5
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  		Figure 5 The Distribution of Mechanical Asynchrony in DHF and SHF Subdivided by QRS Duration

Bar chart showing the distribution of patients who developed (A) diastolic and (B) systolic asynchrony in patients with DHF and SHF according to the QRS duration of ≤120 and >120 ms. As wide QRS is uncommon in DHF, the majority of patients with diastolic and systolic asynchrony occurred in the narrow QRS group. Abbreviations as in Figure 2.

 

   Discussion
Top
 Abstract
 Methods
 Results
 Discussion
References
 
This was the first study that examined the potential existence of diastolic and systolic asynchrony in patients with DHF, and compared them with those with SHF and normal controls. We demonstrated that LV diastolic and/or systolic asynchrony was common and occurred in as many as 60% patients with DHF despite the presence of narrow QRS complex. It was observed that systolic asynchrony and co-existing systolic and diastolic asynchrony were more prevalent in the SHF group, while isolated diastolic dysfunction was more common in the DHF. However, systolic and diastolic asynchronies were not closely coupled in both types of heart failure. Lastly, presence of asynchrony was only a weak determinant of myocardial dysfunction or velocities in DHF.

Mechanical asynchrony in DHF.   Diastolic heart failure is found to be a common cause of heart failure hospitalization (12,13,22). In the past decade, there has been increasing focus on the pathogenesis and management of DHF, and its relationship with SHF (12,13,22,23). Characterization of myocardial systolic and diastolic function in DHF has been performed by conventional echocardiography and TDI, which reported subclinical myocardial systolic dysfunction in DHF (24,25). However, there have been no previous studies that examined mechanical asynchrony in these patients. This study examined a large heart failure cohort of 373 patients that included both DHF and SHF patients, and demonstrated that diastolic and systolic asynchrony did not occur exclusively in the SHF patients, but were also relatively common in DHF patients.

Unlike SHF, in which the occurrence of systolic asynchrony has been well characterized and is related to the prolongation of QRS duration, little is known about that in DHF. The current study observed a relatively high prevalence of both diastolic and systolic asynchrony in DHF, though these conditions were likely to occur in patients with SHF. In particular, co-existing diastolic and systolic asynchrony was nearly 2-fold more common in SHF than DHF. Interestingly, a wide QRS complex was very uncommon in DHF. Therefore, mechanical asynchrony is not related to the QRS duration as most of them occurred in those with narrow QRS complexes. It appeared that diastolic and systolic asynchrony may occur as a result of myocardial disease rather than electromechanical coupling delay (as in the cases with SHF). Our previous studies demonstrated that early "silent" systolic dysfunction is common in DHF as myocardial systolic velocities were reduced in about half of these patients when assessed by sensitive tools such as TDI (24). On the other hand, it seems that the severity of myocardial dysfunction is not the only determinant of mechanical asynchrony, as myocardial early diastolic velocity only had a weak correlation with diastolic asynchrony, and, similarly, myocardial systolic velocity correlated weakly with systolic asynchrony. Further studies are needed to explore how mechanical asynchrony developed in the course of cardiac dysfunction in the DHF.

Is asynchrony in DHF different from that of SHF?.   In SHF, there were more patients who had co-existing diastolic and systolic asynchrony and isolated systolic asynchrony, whereas in DHF more patients had either no or isolated diastolic asynchrony. Moreover, the overall prevalence of systolic asynchrony was higher in SHF than DHF. In patients with SHF, previous studies had shown that QRS duration is a major determinant for the occurrence of systolic (1–4) and diastolic asynchrony (1). As prolongation of QRS duration is rare in DHF, it appears that electromechanical coupling delay is not a major governing factor for the observed asynchrony in the LV. This differs from the SHF in which electrical propagation abnormality had been well described in the LV in patients with wide QRS complexes leading to delay in mechanical contraction (26,27). In fact, both the severity of systolic function and the QRS widening are regarded as markers for more diseased LV in SHF, which accounted for its poorer prognosis than DHF (28,29). These factors also contributed to a higher likelihood of mechanical asynchrony to occur in SHF (1). Interestingly, the relationship between systolic and diastolic asynchrony appeared weak, which implies different pathogenic mechanisms, with the best correlation coefficient value of only 0.25. As a result, diastolic and systolic asynchronies were discordant in about half of the heart failure population, being 47% for DHF and 49% in SHF. Therefore, the 2 conditions should not be regarded as a condition in common. Although diastolic asynchrony was described to be more prevalent than systolic asynchrony in a recent report that used 4 basal segments to assess asynchrony (30), this was not confirmed in the current study when a more comprehensive method was employed.

Study limitations.   Patients were studied 6 weeks after indexed hospitalization for heart failure and medical stabilization, rather than within 72 h of onset of heart failure. There is a possibility of transient ischemic dysfunction of the LV. Most of our DHF patients would thus fit into a probable or possible DHF category (31). However, ischemia may have contributed to diastolic dysfunction without causing a measurable reduction in the ejection fraction or in the extent of regional wall motion (32). Furthermore, patients who presented with acute coronary syndrome were excluded in the present study.

Implication of the study.   Systolic asynchrony is a common finding in SHF with wide QRS complexes. In such patients, cardiac resynchronization therapy had been shown to improve symptoms, systolic function, and mortality (9–11). Mechanistic studies observed that improvement of systolic asynchrony is a key factor for its benefit, while pre-pacing systolic asynchrony is also an important predictor of favorable response to cardiac resynchronization therapy. In view of the pivotal role of regulation of systolic asynchrony in SHF, current studies of cardiac resynchronization therapy focus on possible indication in SHF with narrow QRS complexes (33–35). In contrast with SHF, management of DHF is purely based on medical therapy (13,16,17). The description of mechanical asynchrony, in particular systolic asynchrony in DHF, may provide further insight into the understanding of this heterogeneous group of patients with different phenotypes within one continuous spectrum and may spearhead the exploration of more patient-specific therapeutic strategies in these patients.


   Footnotes
 
This study was supported by a research grant from Li Ka Shing Institute of Health Sciences.


   References
Top
 Abstract
 Methods
 Results
 Discussion
 References
 

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