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J Am Coll Cardiol, 1998; 32:717-723
© 1998 by the American College of Cardiology Foundation
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CLINICAL STUDIES

Mechanisms of hemolysis after mitral valve repair: assessment by serial echocardiography

Tiong Cheng Yeo, MRCPb, William K. Freeman, MD, FACCb, Hartzell V. Schaff, MD, FACCa and Thomas A. Orszulak, MD, FACCa

a Division of Cardiovascular Diseases and Cardiovascular Surgery, Rochester, Minnesota, USA
b Mayo Clinic and Mayo Foundation, Rochester, Minnesota, USA

Manuscript received October 31, 1997; revised manuscript received April 24, 1998, accepted May 8, 1998.

Address for correspondence: Dr. William K. Freeman, Division of Cardiovascular Diseases, Mayo Clinic, 200 First Street SW, Rochester, Minnesota 55905
freeman.william{at}mayo.edu


   Abstract
Top
 Abstract
Methods
 Results
 Discussion
 References
 
Objectives. We sought to determine, using serial echocardiography, the hydrodynamic mechanisms involved in the occurrence of hemolysis after mitral valve repair.

Background. Recently, fluid dynamic simulation models have identified distinct patterns of mitral regurgitant flow disturbances in patients with mitral prosthetic hemolysis that were associated with high shear stress and may therefore produce clinical hemolysis. Rapid acceleration, fragmentation, and collision jets were associated with high shear stress and hemolysis whereas slow deceleration and free jets were not.

Methods. We reviewed serial echocardiographic studies of 13 consecutive patients with hemolytic anemia after mitral valve repair who were referred for mitral reoperation between January 1985 and December 1996 (group 1). Thirteen patients undergoing reoperation for mitral regurgitation after mitral valve repair but without hemolysis served as controls (group 2).

Results. The mitral regurgitant jet was central in origin in 12 group 1 patients and 9 group 2 patients (Fisher exact test, p = 0.3). The other patients had para-ring regurgitation. Group 1 patients had collision (n = 11), rapid acceleration (n = 2) or fragmentation (n = 1) jets whereas group 2 patients had slow deceleration (n = 11) or free jets (n = 2) (Fisher exact test, p < 0.0001). One patient with hemolysis had both collision and rapid acceleration jets. The "culprit" jet could be identified on the postbypass transesophageal echocardiography (TEE) study in only 1 patient at the time of initial mitral repair. Twelve group 1 patients underwent reoperation, with subsequent resolution of hemolysis in all patients. At reoperation, the initial repair was found to be intact in 8 (67%) patients.

Conclusion. Distinct patterns of flow disturbance associated with high shear stress were identified by color Doppler imaging in patients with hemolysis after mitral valve repair. The majority (92%) of these color flow disturbances were not present during intraoperative postbypass TEE study after initial mitral repair and subsequently developed in the early postoperative period.

Abbreviations and Acronyms
  AV = aortic valve
  LA = left atrium
  LV = left ventricle
  TEE = transesophageal echocardiography
  TTE = transthoracic echocardiography

Hemolytic anemia following the insertion of intracardiac prosthetic materials is well recognized. It was first reported by Sayed et al. in a patient who had closure of an ostium primum atrial septal defect with a Teflon patch (1). Since then intravascular hemolysis has been reported in a variety of postoperative lesions, including both mechanical and biological prostheses in the aortic as well as mitral positions (2–7). Recently, fluid dynamic simulation models have identified distinct patterns of regurgitant flow disturbances in patients with mitral prosthetic hemolysis that were associated with high shear stress and may therefore produce clinical hemolysis. Rapid acceleration, fragmentation and collision jets were associated with high shear stress and hemolysis whereas deceleration and free jets were not (8).

Although hemolytic anemia has also been reported after mitral valve repair (9–17), it is uncommon and not well described. Therefore, the aim of this study was to examine, by serial two-dimensional and Doppler echocardiography, the characteristics of mitral regurgitant flow and, hence, the mechanisms involved in hemolysis after mitral valve repair.


   Methods
Top
 Abstract
 Methods
Results
 Discussion
 References
 
Patients.   The study group consisted of 13 consecutive patients with symptomatic hemolytic anemia after mitral valve repair who were referred for reoperation between January 1985 and December 1996 (group 1). Patients with associated native valvular disease or other cardiac prostheses that could predispose to hemolysis were excluded. Patients’ clinic charts, hospital progress notes, operative notes and laboratory tests were examined.

The hemolytic nature of the anemia was established by a persistent severe anemia (hemoglobin ≤9.0 g/dL), an elevated reticulocyte count, elevated serum lactic dehydrogenase (≥ twice upper normal value), reduced serum haptoglobin (<10 mg/dL) and the presence of urine hemosiderin. Indirect hyperbilirubinemia was detected in all patients with hemolysis; an exact laboratory cutoff level was not utilized in this study. Furthermore, the diagnosis of valve-induced hemolysis was supported by typical findings in the peripheral blood film (fragmentation, schistocytosis and spherocytosis), and a negative direct Coombs test.

Thirteen patients undergoing reoperation for mitral regurgitation after mitral valve repair but without hemolysis served as controls (group 2).

The study was approved by the Mayo Foundation Institutional Review Board.

Echocardiographic examination.   Transthoracic and transesophageal echocardiography were performed as previously described using various commercially available echocardiographic instruments (18–21). For intraoperative transesophageal study, the probe was passed after induction of general anesthesia. The prebypass study was performed while the chest was opened and the postbypass study was performed immediately after successful weaning from cardiopulmonary bypass. All studies were recorded on 3/4 in. videotape.

We reviewed all serial echocardiographic studies (including the intraoperative transesophageal studies at the initial mitral valve repair and transthoracic and/or transesophageal studies at the time of diagnosis of hemolytic anemia) of all patients in group 1. The serial transthoracic and transesophageal echocardiographic studies of group 2 were similarly analyzed. All studies were retrospectively reviewed by two experienced echocardiographers (TCY, WKF) and the following features noted: 1) Severity of residual mitral regurgitation: this was classified semiquantitatively into 4 grades as previously described (22,23). 2) Site of mitral regurgitation: defined as central or para-ring depending on its site of origin with reference to the annuloplasty ring and mitral leaflets. 3) Characteristics of mitral regurgitant jet: this was classified as previously described (8) into the following patterns. a) Fragmentation—the regurgitant jet is divided by a solid structure such as a suture, ruptured chord or dehisced annuloplasty ring. b) Collision—there is sudden deceleration of the regurgitant jet due to direct impact on a solid structure such as an annuloplasty ring or pledget, which sharply alters the trajectory of the jet. c) Rapid acceleration—a regurgitant jet originates from a small orifice (<2 mm in diam.) such as a leaflet perforation or narrow region of para-ring dehiscence, with no direct impact on a solid structure. d) Free jet—the regurgitant jet (generally with a central trajectory) originates from a wide orifice (>2 mm in diam.) and is not constrained by a solid structure until it extends to the dome of the left atrium. e) Slow deceleration—an eccentric regurgitant jet originates from a large eccentric orifice and adheres to the left atrial wall from its point of origin.

Statistical analysis.   Continuous variables are expressed as mean ± standard deviation (SD). The unpaired t test was used to compare continuous variables between the two groups, and Mann-Whitney U test for continuous variables which are not normally distributed. For noncontinuous variables, the chi-square test or Fisher exact test were used where appropriate to test for a difference between the two groups with regard to severity, site and characteristics of regurgitation jets. Statistical significance was assumed at p < 0.05.


   Results
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 Abstract
 Methods
 Results
Discussion
 References
 
Age and gender in the two groups were similar but patients with hemolytic anemia had significantly lower levels of hemoglobin and shorter interval between the initial mitral valve repair and reoperation (Table 1). Insertion of an annuloplasty ring during initial mitral repair was performed in 12 patients in group 1 and 9 patients in group 2 (Fisher exact test, p = 0.6).


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  		Table 1 Clinical Characteristics of 26 Study Patients

 
All group 1 patients had significant fragmentation hemolytic anemia requiring transfusion. The median number of units of blood transfused was 3.5 (range = 2 to 12 U). The mean hemoglobin level at presentation was 7.8 ± 1.4 g/dL (range = 5 to 10 g/dL). This represents a mean decrease of 4.8 ± 2.2 g/dL compared to the hemoglobin level at hospital discharge after the initial mitral valve repair.

Further details regarding the initial mitral repair procedure, and subsequent findings and intervention at reoperation are listed in Table 2 for group 1 patients. The median time interval between initial repair and diagnosis of hemolytic anemia was 2.9 months (range = 25 days to 6.8 months). Twelve patients underwent reoperation, with resolution of hemolytic anemia in all patients after surgery. At reoperation, the initial repair was found to be grossly intact in 8 patients and disrupted in 4. The causes of recurrent mitral regurgitation in the 8 patients with an intact site of initial repair included ruptured chordae tendineae to anterior leaflet in 3, perforation of the base of the anterior leaflet in 1, a redundant anterior leaflet that was not repaired initially in 1 and was indeterminate in 3 patients. Causes of mitral regurgitation in patients with disrupted initial repair included dehiscence of the annuloplasty ring in 2 patients and disruption of chordal repair in 2 patients. Incomplete endothelialization of the prosthetic material employed in the initial mitral repair was discovered in 11 (92%) patients reoperated for hemolysis.


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  		Table 2 Surgical Procedures in Hemolysis Patients (Group 1)

 
Transesophageal echocardiography in the patient who was not operated on revealed that mitral regurgitation was due to ruptured neochordae of the initial mitral repair.

Characteristics of mitral regurgitation.   The characteristics of mitral regurgitation on echocardiography are shown in Table 3. Mitral regurgitation was mild to moderate in 5 and severe in 8 group 1 patients, and was severe in all group 2 patients. The regurgitant jet was central in 12 patients in group 1 and 9 patients in group 2 (Fisher exact test, p = 0.3). The other patients had para-ring mitral regurgitation.


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  		Table 3 Echocardiographic Findings

 
In group 1, hydrodynamic mechanisms of regurgitation included collision in 11, rapid acceleration in 2, and fragmentation in 1 patient. No patient had either a free jet or slow deceleration. In contrast, patients in group 2 had either slow deceleration (n = 11) or free (n = 2) jets (Fisher exact test, p < 0.0001). One patient in group 1 had two likely mechanisms of hemolysis with both rapid acceleration of one small regurgitant jet through a tiny perforation in the basal portion of the anterior mitral leaflet, and collision of a second regurgitant jet with the annuloplasty ring. In the other 10 patients with collision, the regurgitant jet was directed against the annuloplasty ring in 9 patients with central redirection of the jet (Fig. 1), and primarily against a pledget in 1. In only one patient, the "culprit" collision jet was directed against the annuloplasty ring retrospectively evident on immediate postbypass transesophageal echocardiography (TEE) study at the time of initial mitral valve repair. In the patient with acceleration, the regurgitant jet was para-ring around the annuloplasty ring (Fig. 2). In the patient with fragmentation (patient 6), the regurgitant jet was divided by a dehisced annuloplasty ring (Fig. 3).



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  		Figure 1 Collision mechanism of hemolysis. Follow-up inverted longitudinal multiplane TEE imaging. (A) Central mitral leaflet coaptation is mildly attenuated (large arrow) after mitral repair with Cosgrove-Edwards ring annuloplasty. A cross-section of the ring (arrowhead) with suture material (small arrow) is seen. (B) Color Doppler imaging reveals a jet of mitral regurgitation (large arrow) which immediately collides with the annuloplasty ring (arrowhead), redirecting the jet at an acute angle into the central LA (small arrows).

 


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  		Figure 2 Acceleration mechanism of hemolysis. Parasternal long-axis TTE imaging. (A) Mitral leaflet coaptation is intact status-post repair with neochordal implantation (small arrows) and St. Jude Biflex ring annuloplasty (arrowheads) three months earlier. (B) Color Doppler imaging in early systole reveals a thin jet of mitral regurgitation (large arrows) tracking around the lateral aspect of the annuloplasty ring. Regurgitant blood flow acceleration through this narrow zone of ring dehiscence accounted for the hemolysis.

 


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  		Figure 3 Fragmentation mechanism of hemolysis. Transverse plane TEE imaging. (A) Mild override of the anterior mitral valve leaflet (large arrow) is observed following triangular resection and chordal shortening of this leaflet with Duran ring annuloplasty (arrowhead) three months earlier. (B) Color Doppler imaging demonstrates bisection of a laterally directed mitral regurgitant jet (large arrows), divided by a minimally dehisced portion of the annuloplasty ring (arrowhead).

 
Of the 11 control patients with slow deceleration regurgitant jets, 4 had severe para-ring regurgitation (Fig. 4), 5 had a flail posterior mitral leaflet, and 2 had a flail anterior leaflet. The regurgitant jet was eccentric in all these patients, adherent to and wrapping around the left atrial wall. Both patients with a free jet (Fig. 5) had a central jet through defects of central leaflet coaptation.



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  		Figure 4 Slow deceleration mitral regurgitation associated with nonhemolytic failure of mitral valve repair. Off-axis transverse plane TEE imaging. (A) Gross dehiscence (large arrow) of the lateral aspect of a Duran annuloplasty ring (arrowheads) placed 13 months earlier is readily evident. (B) The para-ring defect is so large that prominent diastolic inflow (large arrow), entering the LV adjacent to the annuloplasty ring (arrowheads), is present on color Doppler imaging. (C) During systole, a large regurgitant volume is entrained (small arrows) into the para-ring site of dehiscence on the ventricular aspect of the annuloplasty ring (arrowheads) and a broad eccentric jet of mitral regurgitation (large arrows) adheres to the lateral freewall of the LA. No hemolysis was caused by this type of regurgitant jet as rapid flow acceleration did not occur through this large regurgitant orifice.

 


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  		Figure 5 Central free jet mitral regurgitation present in nonhemolytic failure of mitral repair. Inverted transverse plane TEE imaging. (A) Incomplete central mitral leaflet coaptation (large arrow) is present 4 months after posterior leaflet quadrangular resection and Duran ring annuloplasty (arrowheads). (B) Severe central mitral regurgitation (large arrows) is detected by color Doppler imaging.

 

   Discussion
Top
 Abstract
 Methods
 Results
 Discussion
References
 
Mechanisms of hemolysis.   Hemolytic anemia is a well recognized complication of mitral valve replacement and has been ascribed to traumatic fragmentation of erythrocytes against prosthetic material or disruption from paravalvular jet shear forces. On the other hand, hemolytic anemia after mitral valve repair (9–17) is not well described and is presented in the literature by case reports or collection of case reports. Various mechanisms have been proposed as the cause for hemolysis in these patients: "whiplash motion" of disrupted sutures (9); dehisced annuloplasty ring producing para-ring regurgitant jets (10,11); protruding paravalvular suture material or pledgets that provided an impact site against circulating red blood cells (12,14); nonendothelialization of foreign materials such as sutures or rings (15); and direction of a small but turbulent regurgitant jet against the left atrial wall (16).

Mitral regurgitant flow patterns associated with hemolysis.   In vitro studies have demonstrated that shear forces >3000 dynes/cm2 are associated with significant red cell destruction (24). A recent report by Garcia et al. provided new insights into the pathophysiology of mitral prosthetic hemolysis (8). Using fluid dynamic simulation models, they showed that rapid acceleration, fragmentation and collision jets were associated with high shear stress and may therefore produce hemolysis, whereas free and slow deceleration jets were not. However, their study included only 3 patients with hemolytic anemia after mitral valve repair.

This study was therefore conducted to determine the hydrodynamic mechanisms involved in the occurrence of hemolysis after mitral valve repair as assessed by serial two-dimensional and color flow Doppler echocardiography. We found that clinically significant hemolysis in patients after mitral valve repair is associated with distinct patterns of regurgitant flow that have been shown (8) to be associated with high shear stress: collision, rapid acceleration and fragmentation. Conversely, all control patients without hemolysis had free or slow deceleration jets. Our findings suggest that hemolysis after mitral valve repair is due to the high shear stress produced by the regurgitant jet and can occur even when the site of initial repair remains intact. In our series, the initial repair was intact in 8 patients (67%) and hemolysis was due to high shear stress produced as a result of collision of the regurgitant jet with the annuloplasty ring, rapid acceleration of the jet through a small perforation in the anterior mitral leaflet. Thus, prosthetic materials like annuloplasty rings, disrupted sutures or pledgets served as pathophysiologic substrates for hemolysis, especially when the regurgitant jet is directed against or divided by them. Predisposition to hemolysis did not appear to be influenced by the particular type of annuloplasty ring used in the initial mitral repair (Table 2).

Prosthetic materials usually become rapidly endothelialized within several weeks after mitral valve repair. However, the recurrent or residual mitral regurgitant jets may denude this endothelium, thereby exposing a portion of the prosthetic surface, hence introducing the risk of hemolysis occurring at that site. The actual site of prosthetic endothelial denudation was not visible on TEE examination in any patient.

Residual mitral regurgitation after mitral repair.   An important finding of our study is that occurrence of hemolysis is independent of the severity of mitral regurgitation, which was mild to moderate in 5 (38%) patients. Previous reports suggested that only para-ring mitral regurgitation is more likely to produce significant hemolytic anemia (14,15). In this study, however, only one patient (8%) with hemolytic anemia had a para-ring regurgitant jet as the mechanism of hemolysis.

Most patients with hemolysis present early after the initial mitral valve repair (median duration = 2.9 months). It is therefore possible that residual mitral regurgitation after repair, albeit mild, may be the "culprit" regurgitant jet because of the configuration of its flow disturbance. If present, such regurgitant jet could be detected on the intraoperative postbypass TEE study after initial mitral valve repair, prompting further surgical correction to prevent future development of hemolytic anemia. Unfortunately, such "culprit" regurgitant jets were present in our experience on the intraoperative postbypass TEE study in only one patient (8%). Therefore, the majority of these color flow disturbances developed in the early period after mitral valve repair. Nevertheless, when assessing the significance of the residual mitral regurgitant jet by intraoperative TEE immediately after mitral valve repair, it is pertinent to consider its hydrodynamic characteristics in addition to severity, as identification and correction of these "culprit" regurgitant jets may prevent subsequent development of hemolytic anemia. Although uncommonly the case, further surgical intervention is recommended should a residual mitral regurgitant jet with collision, fragmentation, or rapid acceleration flow patterns be identified by intraoperative TEE immediately after mitral repair.

Limitations.   The echocardiographic features were assessed retrospectively by review of the videotapes and, therefore, limited by technical limitations inherent in the recordings. However, a significant proportion of the examinations were TEE studies (85%), and therefore allowed excellent assessment of the mitral valve apparatus (25).

Although shear stress contributes significantly to the pathophysiology of hemolysis, other variables may also have an effect, in particular, the type of prosthetic materials and the surface area of exposure. These factors could not be accounted for in our study.

Conclusion.   We found that hemolysis after mitral valve repair is associated with distinct patterns of flow disturbance on color Doppler echocardiography, and is independent of the severity of mitral regurgitation. By far, the most commonly observed mechanism of hemolysis involved direct collision of the regurgitant jet with a prosthetic surface; in general, the annuloplasty ring. Uncommonly, fragmentation of the regurgitant jet by a dehisced annuloplasty ring or rapid acceleration of the jet within a narrow zone of para-ring dehiscence was also observed with hemolysis. Large orifice eccentric regurgitant jets decelerating along the wall of the left atrium and central free jets were not associated with hemolysis. The vast majority of these color flow Doppler disturbances were not present in the postbypass TEE study and subsequently developed in the early postoperative period after mitral valve repair.


   References
Top
 Abstract
 Methods
 Results
 Discussion
 References
 

  1. Sayed HM, Dacie JV, Handley DA, et al. Hemolytic anemia of mechanical origin after open heart surgery. Thorax. 1961;16:356–360[Medline]
  2. Marsh GW. Intravascular hemolytic anemia after aortic valve replacement. Lancet. 1964;ii:986–988
  3. Nitter-Hauge S, Sommerfelt SC, Hall K-V, et al. Chronic intravascular hemolysis after aortic disc valve replacement: Comparative study between Lillehei-Kaster and Bjork-Shiley disc valve prostheses. Br Heart J. 1974;36:781–785[Free Full Text]
  4. Nitter-Hauge S. Hemolysis after mitral valve replacement with the Bjork-Shiley and the Lillehei-Kaster disc valve prostheses. Br Heart J. 1976;38:977–980[Abstract/Free Full Text]
  5. Grosse-Brockhoff F, Gehrmann G. Mechanical hemolysis in patients with valvular heart disease and valve prosthesis. Am Heart J. 1967;74:137–139[CrossRef][Medline]
  6. Weesner KM, Rocchini AP, Rosenthal A, Behrendt D. Intravascular hemolysis associated with porcine mitral valve calcification in children. Am J Cardiol. 1981;47:1286–1288[CrossRef][Medline]
  7. Magilligan DJ, Fisher E, Alam M. Hemolytic anemia with porcine xenograft aortic and mitral valves. Thorac Cardiovasc Surg. 1980;79:628–631
  8. Garcia MJ, Vandervoort P, Stewart WJ, et al. Mechanisms of hemolysis with mitral prosthetic regurgitation: study using transesophageal echocardiography and fluid dynamic simulation. J Am Coll Cardiol. 1996;27:399–406[Abstract]
  9. Gupta SC, Suryaprasad AG. Mechanical hemolytic anemia after repair of ruptured chordae tendineae of mitral valve-apparatus. Angiology. 1979;30:776–779[Medline]
  10. Moisey CU, Manohitharajah SM, Tovey LAD, Deverall PB. Hemolytic anemia in a child in association with congenital mitral valve disease. J Thorac Cardiovasc Surg. 1972;63:765–768[Medline]
  11. Mok P, Lieberman EH, Lilly LS, et al. Severe hemolytic anemia following mitral valve repair. Am Heart J. 1989;117:1171–1173[CrossRef][Medline]
  12. Warnes C, Honey M, Brooks N, et al. Mechanical hemolytic anemia after valve repair operations for nonrheumatic mitral regurgitation. Br Heart J. 1980;44:381–385[Abstract/Free Full Text]
  13. Wilson JH, Rath R, Glaser R, Panke T. Severe hemolysis after incomplete mitral valve repair. Ann Thorac Surg. 1990;50:136–137[Abstract]
  14. Dilip KA, Vachaspathy P, Clarke B, et al. Hemolysis following mitral valve repair. J Cardiovasc Surg. 1992;33:568–569[Medline]
  15. Mestres CA, Soo CS, Sim EKW, et al. Intravascular hemolysis after mitral valve repair: a word of caution. Eur J Cardio-thorac Surg. 1992;6:103–105[Abstract]
  16. Stoschitzky K, Starz I, Anelli-Monti M, et al. Transfusion-requiring hemolytic anemia after mitral valve repair. Lancet. 1996;347:765[CrossRef][Medline]
  17. Lopez JA, Schnee M, Gaos CM, Wilansky S. Left ventricular outflow tract obstruction and hemolytic anemia after mitral valve repair with a Duran ring. Ann Thorac Surg. 1994;58:876–878[Abstract]
  18. Tajik AJ, Seward JB, Hagler DJ, et al. Two-dimensional real time ultrasonic imaging of the heart and great vessels: technique, image orientation, structure identification, and validation. Mayo Clin Proc. 1978;53:271–303[Medline]
  19. Nishimura RA, Miller FA Jr, Callahan MJ, et al. Doppler echocardiography: theory, instrumentation, technique, and application. Mayo Clin Proc. 1985;60:321–334[Medline]
  20. Seward JB, Khandheria BK, Oh JK, et al. Transesophageal echocardiography: technique, anatomic correlations, implementation, and clinical applications. Mayo Clin Proc. 1990;63:649–680
  21. Seward JB, Khandheria BK, Edwards WD, et al. Biplanar transesophageal echocardiography: anatomic correlations, image orientation, and clinical applications. Mayo Clin Proc. 1990;65:1193–1213[Medline]
  22. Helmcke F, Nanda NC, Hsiung MC, et al. Color Doppler assessment of mitral regurgitation with orthogonal planes. Circulation. 1987;75:175–183[Abstract/Free Full Text]
  23. Castello R, Pearson AC, Lenzen P, Labovitz AJ. Effect of mitral regurgitation on pulmonary venous velocities derived from transesophageal echocardiography color-guided pulsed Doppler imaging. J Am Coll Cardiol. 1991;17:1499–1506[Abstract]
  24. Nevaril CG, Lynch EC, Alfrey CP, Hellums JD. Erythrocyte damage and destruction induced by shearing stress. J Lab Clin Med. 1968;74:784–790
  25. Hozumi T, Yoshikawa J, Yoshida K, et al. Direct visualization of ruptured chordae tendineae by transesophageal two-dimensional echocardiography. J Am Coll Cardiol. 1990;16:1315–1319[Abstract]



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