Advertisement





Click here for more guidelines.
CME Topic Collections Past Issues Search Current Issue Home
     

J Am Coll Cardiol, 2003; 42:110-115, doi:10.1016/S0735-1097(03)00563-1
© 2003 by the American College of Cardiology Foundation
This Article
Right arrow Abstract Freely available
Right arrow Figures Only
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Tung, S.
Right arrow Articles by Stevenson, W. G.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Tung, S.
Right arrow Articles by Stevenson, W. G.

CLINICAL RESEARCH: ELECTROPHYSIOLOGIC DISORDERS

Recognition of far-field electrograms during entrainment mapping of ventricular tachycardia

Stanley Tung, MDa, Kyoko Soejima, MDa, William H. Maisel, MDa, Makoto Suzuki, MDa, Laurence Epstein, MD, FACCa and William G. Stevenson, MD, FACCa,*

a Cardiovascular Division, Department of Internal Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts, USA

Manuscript received December 15, 2002; revised manuscript received February 8, 2003, accepted February 25, 2003.

* Reprint requests and correspondence: Dr. William G. Stevenson, Cardiovascular Division, Brigham and Women’s Hospital, Harvard Medical School, 75 Francis Street, Boston, Massachusetts 02115, USA.
wstevenson{at}partners.org


    Abstract
 Top
 Abstract
 Methods
 Results
 Discussion
 References
 
OBJECTIVES: The goal of this study was to assess entrainment for distinguishing far-field potentials (FFP) due to depolarization of tissue at a distance from the mapping catheter from the local potential (LP) due to depolarization of tissue at the catheter electrode during mapping of ventricular tachycardia (VT).

BACKGROUND: Electrograms with multiple peaks commonly complicate mapping and identification of catheter ablation targets in infarcts.

METHODS: Retrospective analysis of catheter mapping data from eight patients with prior infarction was performed to evaluate multipotential electrograms at sites where pacing entrained VT. Potentials that were visible and not altered during pacing were defined as FFP. Potentials obscured by the pacing stimulus were designated possible LPs. The criteria for FFP were then assessed in a second cohort of five patients.

RESULTS: At 32 of 39 (82%) sites with multiple potentials, entrainment identified one of the potentials as an FFP. Radiofrequency ablation, assessed at 15 sites, reduced the amplitude of LPs by 62%, without significant effect on FFP amplitude. At 56% of sites with multiple potentials, measuring the postpacing interval to an FFP would lead to erroneous classification of the site location relative to the reentry circuit. In prospective evaluation, double potentials were identified at 77 sites in infarcts; entrainment demonstrated an FFP at 66 (86%) sites.

CONCLUSIONS: Far-field potentials are common during mapping in infarcts. Many can be distinguished from local potentials by entrainment, improving the accuracy of mapping.

Abbreviations and Acronyms
  FFP
  far-field potential
  FPPI
  false post-pacing interval
  LP
  local potential
  PPI
  post-pacing interval
  RF
  radiofrequency
  TCL
  tachycardia cycle length
  TPPI
  true post-pacing interval
  VT
  ventricular tachycardia


Cardiac mapping procedures are predicated on the assumption that the recorded electrogram indicates timing of depolarization of the tissue beneath the recording electrode. In normal myocardium the discrete peak of the bipolar electrogram indicates local activation time (1,2). In infarct scars, electrograms with multiple deflections are commonly recorded, often referred to as "multiple potentials," "isolated potentials," or "double potentials"(3–8). These potentials indicate depolarization of myocyte bundles that are separated by areas of fibrosis and consequently depolarized at different times. All bundles can lie beneath the recording electrode. Alternatively, some potentials can be "far-field" signals from depolarization of tissue remote from the recording electrode (4).

Far-field potentials (FFP) can impair the accuracy of mapping and impede successful ablation. Ablation, targeting an "FFP" is likely to fail if the damage cannot reach the tissue generating the FFP. Assigning local activation time to an FFP can create misleading maps of the activation sequence. Analysis of the post-pacing interval (PPI) during entrainment mapping also relies on correct identification of the timing of local activation at the pacing site (9,10). Measurement of the PPI to a far-field signal is a recognized limitation of entrainment (9,10).

Pacing from the recording electrodes provides a potential means of distinguishing the "near-field" or "local" potentials from "far-field" potentials. The electrical field of the pacing stimulus directly depolarizes (directly captures) some of the tissue beneath the recording electrode, and adjacent and distant myocardium is depolarized by the resulting excitation wavefront that propagates through the tissue. The tissue responsible for the local potential is expected to be depolarized immediately after the pacing stimulus. Thus, we hypothesized that potentials that are visible and separate from the stimulus artifact are FFPs.

This study assesses the use of entrainment for identifying FFPs and local potentials (LP). In addition, the potential magnitude of error due to measurement of the PPI to an FFP during mapping is demonstrated, and a method for avoiding this error is proposed.


    Methods
 Top
 Abstract
 Methods
 Results
 Discussion
 References
 
Data were retrospectively analyzed from eight patients (five males; age 63 ± 12 years; left ventricular ejection fraction, 0.31 ± 0.09) who were referred for catheter ablation of ventricular tachycardia (VT) late after myocardial infarction (anterior in two, inferior in four, and both in two). Mapping was performed during 15 different VTs, which had a mean cycle length (TCL) of 404 ± 61 ms (range, 303 to 562 ms). Consecutive sites were included for this analysis if: 1) the electrogram had two or more discrete potentials consistently related to the QRS complexes of the VT, 2) pacing at the site was performed and entrained VT (either with or without QRS fusion), and 3) the electrograms during or after entrainment were not completely obscured by pacing artifact (11–13).

To further assess the frequency of multipotential electrograms and FFPs in patients undergoing catheter ablation, mapping data was then analyzed from a second cohort of five consecutive patients referred for ablation who had at least one VT that allowed entrainment mapping (mean age, 68 ± 3 years; left ventricular ejection fraction, 0.26 ± 0.06; four inferior and two anterior wall infarcts).

Entrainment mapping and ablation were performed as previously described according to protocols approved by the Brigham and Women’s Hospital Human Research Committee (11). Left ventricular mapping was performed with a 7F or 8F catheter with a 4-mm tip electrode and three proximal ring electrodes with 2 to 2.5 mm spacing. Bipolar recordings were simultaneously obtained from the distal (BI 1–2), and proximal (BI 3–4) electrode pairs and filtered at 30 to 500 Hz. Entrainment was performed by pacing from the mapping catheter distal electrode at a cycle length 10 to 40 ms shorter than the VT cycle length. Unipolar stimulation from the distal electrode (cathode) and an electrode in the inferior vena cava (anode) was used to avoid capture at a proximal ring electrode during bipolar stimulation. The stimulus strength was 10 mA at a pulse width of 2 ms. Ablation with radiofrequency (RF) energy (EP Technologies, Boston Scientific, Billerica, Massachusetts) was performed at selected sites. Power was titrated to a maximum of 50 W to achieve a fall in impedance of 5 to 10 Ohms and/or a temperature of 60°C. Maximum duration was 2 min.

FFP and LP.   From analyses during entrainment, an FFP was defined as one that was visible during pacing with no change in morphology compared with that present in the absence of pacing (Figs. 1A and 2). When one or more potentials met the definition of an FFP during entrainment, any other potential was defined as an LP if it was not visible during pacing and reappeared after pacing, consistent with direct depolarization of the tissue causing this potential by the electrical field of the stimulus (Figs. 1A and 2).



View larger version (32K):
[in this window]
[in a new window]
 
Figure 1 Distinguishing far-field (FFP) and local potentials (LP) from analysis of entrainment (A) or the effect of radiofrequency ablation (B) are shown. In both panels ventricular tachycardia with a cycle length of 550 ms is present. From the top are surface electrocardiogram leads (I, aVF, V1, V6) and bipolar intracardiac electrograms recorded from the distal (Abl D) and proximal (Abl P) electrode pairs of the ablation catheter. Potentials are labeled 1, 2, and 3. Entrainment indicates potential 1 is an FFP. Radiofrequency ablation reduces the amplitude of potential 3 (B) indicating it is an LP, but does not affect potentials 1 and 2. See text for discussion. Time lines are 20 ms.

 


View larger version (38K):
[in this window]
[in a new window]
 
Figure 2 Entrainment of ventricular tachycardia (VT) at a site with a double potential is shown. From the top are surface electrocardiogram leads (I, II, III), and bipolar intracardiac electrograms recorded from the distal (Abl D) and proximal (Abl P) electrode pairs of the ablation catheter; VT with a cycle length of 410 ms is present. Pacing at a cycle length of 390 ms entrains tachycardia without altering the QRS morphology (concealed fusion). Recordings at the pacing site show two potentials marked with an asterisk and arrowhead, respectively. During entrainment, the potential marked with the asterisk is present and accelerated to the pacing cycle length. The tissue generating this potential is not directly depolarized by the pacing stimulus and is, therefore, designated as far-field (FFP). The local potential (indicated by an arrowhead) is not discernable during pacing, consistent with direct capture, but reappears after the last stimulus. The true post-pacing interval (PPI) (TPPI), which is measured from the last stimulus to the local potential, is 425 ms. The false PPI (FPPI), which is measured from the last stimulus to the FFP, is 210 ms, or, if measured to the next FFP electrogram one cycle later, would be 620 ms. Radiofrequency ablation at this site abolished tachycardia. Time lines are 20 ms.

 
To determine the relation of potentials to the reach of RF ablation from the recording distal electrode, the effects of ablation on the amplitude of the potentials was analyzed. Because electrogram characteristics often change with the sequence of activation, only sites where ablation during VT failed to terminate VT, allowing the potential to be assessed during the same rhythm before and after ablation, were included for this analysis (Fig. 1B).

PPI measurement.   For analysis of the PPI, the interval from the last capturing stimulus to the following potentials was determined. When stimulation saturated the amplifier of the distal bipolar recording such that the signal was not available during pacing, the bipolar recordings from the electrode 2-mm proximal to the distal electrode were used for analysis provided that the potentials on that recording were identical in timing to those recorded from the distal electrodes (electrodes 1–2) (10). The PPI measured from the last stimulus that entrained tachycardia to the LP was designated the true PPI (TPPI). The PPI measured from the last stimulus to the far-field signal was designated the false PPI (FPPI) (Fig. 1A). Continuous data are expressed as mean ± SD.


    Results
 Top
 Abstract
 Methods
 Results
 Discussion
 References
 
In the retrospective eight-patient cohort, a total of 39 sites during 15 VTs met entry criteria for analysis; two discrete potentials were present at 36 sites, and three discrete potentials were present at three sites. During entrainment, a potential meeting the definition for an FFP was clearly identified at 32 of the 39 sites (82%) (Figs. 1 and 2). The mean interval from the pacing stimulus to the FFP was 188 ± 83 ms (range, 61 to 338 ms), and the mean interval from the FFP to the following stimulus was 179 ± 104 ms (range, 12 to 402 ms). Effects of RF ablation could be assessed at 15 of these sites and further supported the ability of entrainment to identify the FFPs (Fig. 1A). After RF ablation, the amplitude of the LP decreased by 62% compared with only an 8% reduction in amplitude of the FFP (p = 0.0001 LP vs. FFP).

At seven of the 39 sites (18%), both potentials were obscured during entrainment, but RF ablation reduced the amplitude of one potential by a mean of 69% without reducing the amplitude of the other potential. Thus, not all FFPs could be identified by entrainment.

Figure 1 illustrates the use of entrainment (Fig. 1A) and the effect of RF ablation (Fig. 1B) on FFP and LPs. During VT three potentials, labeled 1, 2, and 3, are present with each beat in the simultaneous recordings from the proximal and distal electrode pairs. In Figure 1A, pacing from the mapping catheter distal electrode entrains VT with QRS fusion. During pacing, electrograms from the distal electrodes of the mapping catheter are obscured by saturation of the recording amplifier by the stimulus artifact. At the proximal electrodes, potential 1 is clearly visible during pacing, preceding each stimulus artifact by <100 ms. Thus, potential 1 is an FFP. Measurement of the PPI to this potential yields an FPPI of 417 ms (arrow). The potentials marked 2 and 3 are not distinct during pacing, although a deflection that could represent one of them is evident after the pacing stimulus (indicated by the arrowhead). The response to radiofrequency ablation (Fig. 1B) indicates that potential 3 is the local potential. The left side of Figure 1B shows electrograms before ablation; the right side shows that electrograms recorded immediately after ablation failed to terminate VT. Ablation reduces the amplitude of potential 3 in the distal electrode recordings from 0.47 mV to 0.19 mV and alters its morphology, consistent with an LP. In contrast, the amplitude and morphology of potential 1, the FFP identified during entrainment, and of potential 2, are not altered by ablation, consistent with FFPs. The PPI measured to potential 3 is 725 ms (Fig. 1A).

The relative amplitudes of multiple potentials did not reliably distinguish FFP from LP (Fig. 2). Although the FFP amplitude was usually smaller (0.19 ± 0.18 mV) than that of the LP (0.24 ± 0.26 mV), at 36% (14/39) of sites the FFP was larger than the LP.

Effect of FFPs on PPI measurement.   The difference between the TPPI and FPPI ranged from –330 to 200 ms with a mean absolute difference of 102 ± 60 ms. A PPI-VT cycle length difference ≤30 ms is a marker for reentry circuit sites (14). At 44% of sites, measurement of the PPI to either the LP (TPPI) or the FFP (FPPI) did not change the classification of the site; the PPI-TCL difference was >30 ms measured to either potential. At 56% of sites, however, classification of the site based on the true PPI differed from that using the false PPI. At five sites (12%), the TPPI indicated that the site was a bystander, but the FPPI misidentified the site as in the circuit. At 17 sites (44%) the TPPI identified the site as in the circuit, but the FPPI identified the site as a bystander (Fig. 3).



View larger version (33K):
[in this window]
[in a new window]
 
Figure 3 The relation between false post-pacing interval (FPPI) determined from the far-field potential (FFP), and the true post-pacing interval (TPPI) for classifying circuit sites are shown. A circuit site is defined as having a TPPI-ventricular tachycardia cycle length difference of ≤30 ms (14). At 12% of the sites where a TPPI >30 ms indicated a bystander site, measurement to the FFP yielded a false PPI-tachycardia cycle length difference ≤30 ms that falsely classified the site as in the reentry circuit. At 44% of sites where the TPPI-tachycardia cycle length difference ≤30 ms classified the site as in the circuit, the FPPI was >30 ms, classifying the site as remote from the circuit. At 44% of the sites, both FPPI and TPPI classified the site as a bystander.

 
Entrainment at sites with double potentials.   In a second cohort of five patients, entrainment was performed at 77 sites with double potentials identified in an infarct region during ventricular tachycardia. During entrainment, an FFP was visible at 66 (86%) sites.


    Discussion
 Top
 Abstract
 Methods
 Results
 Discussion
 References
 
Origin of multipotential electrograms.   Surviving strands and sheets of myocardium are the substrate for reentry in areas of infarction and other scars causing VT (3,4,15). Asynchronous depolarization of separated muscle bundles often gives rise to multiple discrete potentials. Our results indicate that one of these potentials is often sufficiently distant from the mapping catheter and that it is not directly depolarized (directly "captured") by pacing and is not damaged by RF ablation from the mapping catheter. These potentials are referred to here as "far-field" potentials. Although the possibility of FFPs is widely appreciated, this is the first clinical study to evaluate a method for identifying them during catheter mapping in humans.

The relative amplitude of two potentials does not reliably identify the FFP. The larger potentials are not necessarily closer to the recording electrode. A large mass of myocardium in the infarct border, remote from the recording electrode, may produce a larger potential than that produced by a strand of myocardium immediately beneath the recording electrode. Additional signal processing techniques could potentially be helpful, but none have been available other than simple filtering (1).

Pacing to identify FFPs.   This study demonstrates that analysis of the electrograms recorded during entrainment can often distinguish FFPs from LPs. The stimulus artifact obscures the potential produced in the tissue immediately after the stimulus. Thus, the LP is not visible during pacing, but reappears after the last entrained QRS complex. At most of the sites studied, FFPs fall sufficiently late, after the pacing stimulus, to be visible during entrainment. These FFPs are accelerated to the pacing rate, but are not changed in morphology compared with those observed during tachycardia. The FFPs often precede the next stimulus by a short interval (Fig. 1) such that the tissue generating the FFP is probably refractory at the time of the next stimulus. Hence, the stimulus is not directly depolarizing the tissue generating the FFP. That these potentials are distant from the distal recording electrode is further supported by the lack of effect of RF ablation on the FFP.

Study limitations.   Although FFPs can be recognized when visible during entrainment, a potential that is obscured by the pacing artifact may be either an LP or a FFP that occurs immediately after the stimulus, such that the stimulus artifact obscures it even though it is not directly captured. A short interval between stimulus and apparent FFP prevented FFP detection by entrainment at seven of the 39 sites in the present study. In some cases the potential evident in the recording from the distal bipole was also evident in the recordings from more proximal electrodes, allowing this signal to be assessed during entrainment (10).

Bipolar electrogram morphology is influenced by the direction of wavefront activation and heart rate. Thus, the morphology of some FFP electrograms may change during entrainment. We expect that this would be most likely when there is a short conduction time from pacing site to stimulus site, in which case the FFP may be obscured by the stimulus artifact. Pacing at a rate only slightly faster than the tachycardia, which minimizes the amount of ventricle depolarized by stimulated antidromic wavefronts during entrainment, is likely to reduce the occurrence of changes in FFP morphology during entrainment.

These findings are likely dependent on the recording and pacing techniques used. We analyzed bipolar recordings during unipolar pacing. An FFP identified by this method could be close to the proximal recording electrode. Bipolar pacing from the distal electrode pair might capture a potential that would be identified as far field by unipolar pacing on the distal electrode. Ablation is applied only at the distal electrode, however. We paced at a single stimulus strength of 10 mA to minimize procedure duration. Pacing at lower strengths, near threshold, would reduce stimulus artifact and might improve detection of FFPs.

Clinical implications for mapping.   Far-field potentials have profound implications for mapping. Assignment of an incorrect time of activation will render activation sequence maps misleading. The presence of FFPs also reduces the accuracy of entrainment mapping using the PPI (9,10,16). The PPI is the conduction time from the last capturing stimulus during entrainment to the subsequent activation at the pacing site as assessed by the electrogram recorded from the pacing site. At sites in the circuit, this interval is equal to the revolution time through the circuit. At sites remote from the circuit, the PPI is the conduction time from the pacing site to the circuit, then through the circuit and back to the pacing site, and, therefore, exceeds the tachycardia cycle length. Measurement of the PPI to an FFP introduces an error, the magnitude of which is related to the conduction time between the pacing site and the source of the FFP (9,10). When the PPI appears to be shorter than the TCL, the potential used for measurement is likely an FFP. Far-field potentials may have contributed to the poor relation of the PPI to reentry circuit sites in a previous study (16).

Conclusions.   Far-field potentials are common during catheter mapping of infarct-related VT and can confound interpretation of the PPI. Analysis of the potentials recorded during entrainment often allows identification of the FFP so that it can be excluded from activation maps and the PPI measurement. These methods should improve the accuracy of mapping scar-related arrhythmias.


    References
 Top
 Abstract
 Methods
 Results
 Discussion
 References
 
1. Anderson KP, Walker R, Ershler PR, et al. Determination of local myocardial electrical activation for activation sequence mapping: a statistical approach. Circ Res. 1991;69:898–917[Abstract/Free Full Text]

2. de Bakker JMT, Hauer RNW, Simmers TA. Activation mapping: unipolar versus bipolar recording. Zipes DP, Jalife J. Cardiac Electrophysiology: From Cell to Bedside. 2nd edition. Philadelphia, PA: W.B. Saunders; 1995. p. 1068

3. de Bakker JM, van Capelle FJ, Janse MJ, et al. Fractionated electrograms in dilated cardiomyopathy: origin and relation to abnormal conduction. J Am Coll Cardiol. 1996;27:1071–1078[Abstract]

4. de Bakker JM, van Capelle FJ, Janse MJ, et al. Slow conduction in the infarcted human heart: "zigzag" course of activation. Circulation. 1993;88:915–926[Abstract/Free Full Text]

5. Kocovic DZ, Harada T, Friedman PL, et al. Characteristics of electrograms recorded at reentry circuit sites and bystanders during ventricular tachycardia after myocardial infarction. J Am Coll Cardiol. 1999;34:381–388[Abstract/Free Full Text]

6. Bogun F, Bahu M, Knight BP, et al. Response to pacing at sites of isolated diastolic potentials during ventricular tachycardia in patients with previous myocardial infarction. J Am Coll Cardiol. 1997;30:505–513[Abstract]

7. Bogun F, Knight B, Goyal R, et al. Discrete systolic potentials during ventricular tachycardia in patients with prior myocardial infarction. J Cardiovasc Electrophysiol. 1999;10:364–369[Medline]

8. Fitzgerald DM, Friday KJ, Wah JA, et al. Electrogram patterns predicting successful catheter ablation of ventricular tachycardia. Circulation. 1988;77:806–814[Abstract/Free Full Text]

9. Khan HH, Stevenson WG. Activation times in and adjacent to reentry circuits during entrainment: implications for mapping ventricular tachycardia. Am Heart J. 1994;127:833–842[CrossRef][Medline]

10. Hadjis TA, Harada T, Stevenson WG, et al. Effect of recording site on postpacing interval measurement during catheter mapping and entrainment of postinfarction ventricular tachycardia. J Cardiovasc Electrophysiol. 1997;8:398–404[Medline]

11. Stevenson WG, Friedman PL, Kocovic D, et al. Radiofrequency catheter ablation of ventricular tachycardia after myocardial infarction. Circulation. 1998;98:308–314[Abstract/Free Full Text]

12. Brugada P, Abdollah H, Wellens HJ. Continuous electrical activity during sustained monomorphic ventricular tachycardia: observations on its dynamic behavior during the arrhythmia. Am J Cardiol. 1985;55:402–411[CrossRef][Medline]

13. Miller JM, Vassallo JA, Hargrove WC, et al. Intermittent failure of local conduction during ventricular tachycardia. Circulation. 1985;72:1286–1292[Abstract/Free Full Text]

14. Stevenson WG, Khan H, Sager P, et al. Identification of reentry circuit sites during catheter mapping and radiofrequency ablation of ventricular tachycardia late after myocardial infarction. Circulation. 1993;88:1647–1670[Abstract/Free Full Text]

15. Downar E, Saito J, Doig JC, et al. Endocardial mapping of ventricular tachycardia in the intact human ventricle. III. Evidence of multiuse reentry with spontaneous and induced block in portions of reentrant path complex. J Am Coll Cardiol. 1995;25:1591–1600[Abstract]

16. Bogun F, Knight B, Goyal R, et al. Clinical value of the postpacing interval for mapping of ventricular tachycardia in patients with prior myocardial infarction. J Cardiovasc Electrophysiol. 1999;10:43–51[Medline]




This article has been cited by other articles:


Home page
EuropaceHome page
E. M. Aliot, W. G. Stevenson, J. M. Almendral-Garrote, F. Bogun, C. H. Calkins, E. Delacretaz, P. D. Bella, G. Hindricks, P. Jais, M. E. Josephson, et al.
EHRA/HRS Expert Consensus on Catheter Ablation of Ventricular Arrhythmias: Developed in a partnership with the European Heart Rhythm Association (EHRA), a Registered Branch of the European Society of Cardiology (ESC), and the Heart Rhythm Society (HRS); in collaboration with the American College of Cardiology (ACC) and the American Heart Association (AHA)
Europace, June 1, 2009; 11(6): 771 - 817.
[Full Text] [PDF]


Home page
Circ Arrhythmia ElectrophysiolHome page
F. Sacher, U. B. Tedrow, M. E. Field, J.-M. Raymond, B. A. Koplan, L. M. Epstein, and W. G. Stevenson
Ventricular Tachycardia Ablation: Evolution of Patients and Procedures Over 8 Years
Circ Arrhythmia Electrophysiol, August 1, 2008; 1(3): 153 - 161.
[Abstract] [Full Text] [PDF]


This Article
Right arrow Abstract Freely available
Right arrow Figures Only
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Tung, S.
Right arrow Articles by Stevenson, W. G.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Tung, S.
Right arrow Articles by Stevenson, W. G.

 
  CME Topic Collections Past Issues Search Current Issue Home

Advertisement