Abstract

Background: This study aims to evaluate the outcomes of bicaval and biatrial techniques in orthotopic heart transplantation.

Methods: Between May 1966 and May 2011, a literature survey was conducted using electronic search engines including PubMed, Medline and Google and manually surveying the magazines on heart and vascular surgery. A total of 36 prospective and retrospective controlled studies which met the inclusion criteria were included in the metaanalysis. The outcomes of both techniques were evaluated using random and fixed-effect method, based on their significant heterogeneous nature. Statistical analysis was performed using Comprehensive Meta Analysis version 2 software.

Results: It was found that the results of eight meta-analyses obtained (tricuspid and mitral insufficiency, the need for permanent or temporary pacemaker, sinus rhythm, survival at 1 and 10 year, the right atrial pressure) were significantly improved in bicaval group, compared to the biatrial group.

Conclusion: Our study results showed that the outcomes of the bicaval technique were better, compared to biatrial technique. We believe that the bicaval anastomosis technique may have a positive effect on morbidity, due to its clinical and hemodynamical benefits.

Heart transplantation has become a widely used treatment choice that increases both the quality of life and expected life span of patients suffering from endstage heart failure.[1,2] Although approximately 3500 heart transplantations have been performed, there are about 800.000 patients who have been identified as New York Heart Association (NYHA) class IV who urgently need a new organ.[3] In 1960, the biatrial orthotopic heart transplantation technique, as defined by Lower and Shumway,[4] was modified by Dr. Christian Barnard,[5] and it became the standard technique. In that technique, both atriums are anastomosed at the mid-atrial level. Additionally, the anatomic structure and geometric shape of the atriums change. Asynchronous atrial contractions can cause the regurgitation of atrioventricular heart valves,[6-8] and the need for a pacemaker could arise due to sinus node dysfunction (SND).[9] Therefore, the search for an alternative technique was started to overcome all of these issues. Bicaval transplantation, in which single left atrium anastomosis is performed, was first used in 1991 by Sievers et al.[10] on two patients. In 1993, Sarsam et al.[11] used the same technique on a broader patient population, and it became known as the “bicaval Wythenshawe technique”. It has been reported that sinus node function is preserved in transplantations where the bicaval anastomosis technique is used, and as a result of the contribution of atrial contractions, stroke volume and heart performance have improved.[12]

Although heart transplantation has been performed all over the world for forty years, there still is no definitive choice for the atrial anastomosis technique. In this study, we aimed to examine the literature related to orthotopic heart transplantations and compare them by means of a systematic review and meta-analysis.

Methods

Our systematic evaluation of the results of the bicaval and biatrial techniques used in orthotopic heart transplantations was based on the analysis of published data and research of both randomized and non-randomized controlled tests. A meta-analysis was used to compare two groups of patients who underwent heart transplantation using either the bicaval or biatrial techniques, and the following items were assessed: tricuspid and mitral valve insufficiency, temporary and the need for a permanent pacemaker, central venous pressure, right atrial pressure, pulmonary artery pressure, length of hospital stay, arrhythmia, pulmonary capillary wedge pressure, left atrial size, perioperative mortality, and the survival rates at one, three, five, and 10 years. After completing the comparison, the weighted mean difference (WMD) and its 95% confidence interval (CI) was then calculated.

Study inclusion and exclusion criteria
Retrospective and prospective controlled studies containing results regarding the bicaval and biatrial techniques of orthotopic heart transplantation were included in our review, which had no age, gender, or ethnic limitations. Case reports and series, letters, brief reports on experimental animals, uncontrolled studies, and review articles were not examined. The demographic characteristics of 36 studies included in the meta-analysis are provided in Table 1.[2,7,8,11,13-43]

Table 1: Demographic characteristics of studies included in the meta-analysis

Search strategy
A literature survey was completed by three independent authors according to caption, abstract, and full text as well as the inclusion and exclusion criteria mentioned above. The survey was conducted using electronic search engines such as PubMed, Medline, and Google and included information found up to May 2011. The terms “bicaval heart transplantation”, “biatrial heart transplantation”, “cardiac transplantation”, and “heart transplantation” were used for the online research. The literature sources included in the study were searched manually, and the related articles provided by Pubmed were also reviewed. A total of 157 studies were retrieved. Ninety-three studies were excluded after reading the title and summary as they did not fit the inclusion criteria. Twenty-eight studies were excluded for reasons that are given in detail in Figure 1. In the end, 36 studies were included in the meta-analysis.

Figure 1: Flow chart of study identification.

Data extraction
The information in each article included in the study was independently extracted by three authors. If the extracted raw data was approved by three authors according to the inclusion and exclusion critera, they were included in the study. The general characteristics of the published study (author, source country of the data, year of publication, study design, sample size, and number of incidents), demographic characteristics (gender, age), monitoring periods, results (tricuspid and mitral valve insufficiency, temporary and permanent pacemaker requirement, central venous pressure, right atrial pressure, pulmonary artery pressure, length of hospital stay, pulmonary capillary wedge pressure, cardiac index, left atrium size, arrhythmia, perioperative mortality, and the survival rates at 1, 3, 5, and 10 years), operation technique, and statistical methods were recorded.

Statistical analysis
A meta-analytical evaluation of the results of the bicaval and biatrial surgical techniques used in orthotopic heart transplantation as found in all of the retrospective and prospective research was included in our study. Statistical analysis was done using the Comprehensive Meta-Analysis (CMA) version 2 software (Biostat, Englewood, New Jersey, USA). The odds ratio (OR) and its 95% CI were used for analyzing continuous variables while WMD and its 95% CI were used for analyzing dichotomous variables. A Cochrane Q test and I2 statistics were used for the evaluation of heterogeneity between the results included in our study. A meta-analysis was performed by using either the fixed or random effect, depending on the availability of significant heterogeneity between the studies. In cases in which the heterogeneity was significant, (p<0.1, I2>50%) a random effect model was used, and if the heterogeneity was not significant (p≥0.1, I²<50%), a fixed effect model was used. The whole effect was analyzed by using a Z score obtained by Fisher’s Z transformation.

Results

The meta-analysis results of all the significant studies are shown in Table 2-9.[2,7,8,10,11,13-18,20-29,31-35,37,38,40,41,44] With regard to tricuspid insufficiency, 14 of the study results have been implemented (Table 2, 3), and 10 (Table 7-9) of the study results for mitral valve insufficiency have been carried out. For atrioventricular valve insufficiencies, only those that were medium and advanced in nature were included in our evaluation. It was discovered that there was a significant decrease tricuspid and mitral valve insufficiency via the bicaval anastomosis technique (OR: 0.38, 95% CI: 0.236- 0.602; OR: 0.48, 95% CI: 0.275-0.841, respectively).

Table 2: Meta analysis for tricuspid regurgitation

Table 3: Meta analysis outcomes for permanent pacemaker

Table 4: Meta analysis outcomes for temporary pacemaker

Table 5: Meta analysis outcomes for sinus rhythm

Table 6: Meta analysis outcomes for survival at one year

Table 7: Meta analysis outcomes for mitral regurgitation

Table 8: Meta analysis outcomes for right atrial pressure

Table 9: Meta analysis outcomes for survival at 10 years

The need for a permanent or temporary pacemaker commonly affects morbidity after orthotopic heart transplantations. A meta-analysis was undertaken with 10 studies involving a permanent pacemaker (Table 2, 3) and five studies involving a temporary pacemaker (Table 4-6). It was showed that the bicaval technique significantly decreased the need for these devices (OR: 0.37, 95% CI: 0.323-0.427; OR: 0.511, 95% CI: 0.323-0.809, respectively). Furthermore, the result of an analysis of four other studies revealed that the number of patients remaining in sinus rhythm with the bicaval technique was significantly high (OR: 0.22, 95% CI: 0.130-0.387).

An analysis of seven studies which looked at right atrial pressure values was carried (Table 7-9), and it was found to be significantly lower in the bicaval group (WMD: -1.54, 95% CI: -2.21 to -0.870). Eight studies involving the one-year (Table 4-6) and two studies focusing on 10-year survival rates (Table 7-9) were examined, and the values in the bicaval group were significantly higher (OR:0.82, 95% CI: 0.716-0.931; OR: 0.77, 95% CI: 0.729-0.817, respectively).

According to the results of the analysis of parameters included in meta-analysis, such as perioperative mortality (OR: 0.43, 95% CI: 0.068-2.766), three and five-year survival rates (OR: 0.76, 95% CI: 0.222-1.989; OR: 0.86, 95% CI: 0.209-3.538, respectively), central venous pressure (WMD: -0.57, 95% CI: -1.207 to -0.069), length of hospital stay (WMD: -.19, 95% CI: -0.506 to -0.125), pulmonary capillary wedge pressure (WMD: -0.19, 95% CI: -0.803-0.426), left atrium size (WMD: -1.91, 95% CI: -4.044-1.661), and arrhythmia (OR: 0.98, 95% CI: 0.098-9.784), no significant differences were found between the bicaval and biatrial groups.

Discussion

Heart transplantation is an accepted treatment choice for end-stage heart failure today, and it has been proven to increase a patient’s life span.[1,2] Although the bicaval surgical technique for orthotopic heart transplantation is commonly preferred, there is still no common consensus regarding the best technique to be used.

When transplantation is performed using the standard technique, the anatomic structure and geometric formation of the atriums are changed, and unsynchronized atrial contractions could cause the regurgitation of the tricuspid and mitral valve.[45] The bicaval anastomosis technique exclusively uses donor atriums, and resection of the recipient atrial tissue is done as much as possible.[11,13] According to this technique, the sinus node function is not impaired, and as a result of the contribution of atrial contractions, stroke volume and cardiac performance usually improves. Furthermore, atrioventricular valve function is preserved due to the protection of right atrial anatomy.[14]

Two separate meta-analyses were published in 2007 by Schnoor et al.,[46] which included uncontrolled tests, and in 2010 by Locali et al.,[47] which included only controlled studies. Schnoor et al.[46] inspected studies up to August 2006, and Locali et al.[47] took into account the studies up to January 2008. Our study added 35 more studies to the mix as we gathered information from articles up to May 2011. This not only increased the number of studies, but added new relevant information to the two previous meta-analyses.

Those who support the bicaval technique have reported that the impairment of atrial geometry coincides with the contractions of the two atrium pieces and that this could lead to tricuspid insufficiency in the early postoperative period. It has also been reported that mitral insufficiency could be related to the bending of the posterior leaflet, which is an extension of the left atrium endocardium that is dependent on the expansion of the anastomosed left atrium part.[15,48] The results of Schnoor et al.[46] and Locali et al.[47] are similar to these findings. In addition, the Locali study showed no significant difference between the bicaval and biatrial groups in terms of mitral insufficiency. In our study, the frequency of tricuspid and mitral insufficiency was significantly lower in the bicaval group, which is similar to the findings in the Locali study. Jeevanandam et al.,[49] reported on a prospective study on the bicaval orthotopic heart transplantation technique, both with and without a prophylactic tricuspid annuloplasty in the vega. That study revealed that the mean pulmonary artery pressure and central venous pressure were lower while the right ventricular performance was higher. Furthermore, it indicated that in the first year, the number of patients suffering from ≥2+ tricuspid insufficiency was significantly lower in the group in which annuloplasty was applied, but there was no difference in renal functions.[49] The results of the metaanalysis for hemodynamic parameters in our study are given in detail in Table 10.[2,4,7,11,13,14,22,26,29,30-32,38,39]

Table 10: The results of the meta-analysis regarding hemodynamic parameters

Sinus node dysfunction is one of the reasons for morbidity after orthotopic heart transplantation, with a frequency rate of between 10%-43%.[50-52] It was also discovered that the permanent pacemaker application rate in SND was 3%-19%.[50-52] The biatrial technique might cause trauma in the sinus node or on its perinodal tissue and could impair its normal atrium morphology.[48,52,16] In the bicaval technique, almost the entire recipient right atrium can be excised, leaving an atrial cuff. The donor vena cava inferior and superior can be anastomosed to the recipient atrial cuff directly. Thus, the right atrium anatomy of the donor can be protected, and any possible sinus node damage can be prevented.[17] The Locali study[47] indicated that the frequency of postoperative arrhythmia decreased significantly in the bicaval group; however, the Schnoor study[46] revealed that the sinus rhythm was higher in the same group.

Meyer et al.[17] reported that although the crossclamping and ischemia period was extended, the need for a permanent pacemaker decreased statistically by a significant margin approximately 30 and 90 days after bicaval heart transplantations, when it was then found to be safe. Grant et al.[18] reported that the atrial geometry was better protected when the bicaval anastomosis technique was used, the incidence of postoperative atrial tachyarrhythmia was low, and the need for a pacemaker was decreased. When this occurred, patients were discharged earlier from the hospital. According to the United Network for Organ Sharing/ Organ Procurement Transplantation Network (UNOS/ OPTN) multivariable analysis results published by Cantillon et al.[19] in 2010, it was reported that the bicaval surgical technique was a powerful protector against the need for a postoperative pacemaker. In the same study, it was also shown that the biatrial surgical technique and increasing donor/recipient age were related to the necessity for a postoperative pacemaker. Our results related to the frequency of pacemaker application showed less occurrence in the bicaval group, similary to the findings in the aforementioned studies. Bouchart et al.[53] reported that patients who were subjected to biatrial transplantation with Doppler echocardiography had significant spontaneous echo contrast and left atrial thrombus. Furthermore, the early-to-late ventricular filling ratio (E:A) for the left ventricular filling pattern from cycle to cycle was higher. Nevertheless, that change reflects the presence of asynchronous contractions in the atrium recipient which could theoretically trigger contrast echo and thrombus formation inside blood flow stasis atrium related to asynchronous contractions.

The Schnoor study[46] stated that the one and threeyear mortality rates decreased in the bicaval group but that there was no significant difference. The Locali study[47] gave no specific figures for mortality rates but reported that they also decreased in the same group. Our results indicated that when these two groups were compared, there was a significant difference between the preoperative and three-year survival rates, and the one and 10-year rates were significantly better in the bicaval group. In contrast, Wei et al.[54] found that both the short and long-term results were more satisfactory with the biatrial technique. In 2010, Davies et al.,[20] using the UNOS data, reviewed 20,999 patients who had undergone a heart transplant between 1997-2007. This data indicated that the surgical technique used from 1997 to 2007 changed significantly in favor of the bicaval method (0.2% in 1997 versus 97.6% in 2007; 62.0% versus 34.7%; p<0.0001). According to the same study, the COX regression analysis confirmed that the mortality rate in the bicaval group had significantly decreased over a 30-day period, and the long-term survival rate had decreased with the biatrial technique.

In conclusion, according to the results of our metaanalysis related to orthotopic heart transplantation, when parameters such as tricuspid insufficiency, mitral insufficiency, the need for a permanent or temporary pacemaker, right atrial pressure, one and 10-year survival rates, and sinus rhythm were compared, the bicaval anastomosis technique produced more satisfactory results than the biatrial anastomosis technique. Although the number of heart transplants varies by country and the number of clinics that can perform this procedure, there has been a considerable increase in the number of available donors and the number of patients who suffer from end-stage heart failure who need a new organ. Consequently, we think that a proper analysis of the results of surgical techniques, especially those dealing with the medium and long-term results, could affect mortality and morbidity considerably, even though survival rates will vary according to the experience of each clinic.

Declaration of conflicting interests
The authors declared no conflicts of interest with respect to the authorship and/or publication of this article.

Funding
The authors received no financial support for the research and/or authorship of this article.

References

1) Hunt SA, Haddad F. The changing face of heart transplantation. J Am Coll Cardiol 2008;52:587-98.

2) Koch A, Remppis A, Dengler TJ, Schnabel PA, Hagl S, Sack FU. Influence of different implantation techniques on AV valve competence after orthotopic heart transplantation. Eur J Cardiothorac Surg 2005;28:717-23.

3) Taylor DO, Edwards LB, Boucek MM, Trulock EP, Waltz DA, Keck BM, et al. Registry of the International Society for Heart and Lung Transplantation: twenty-third official adult heart transplantation report-2006. J Heart Lung Transplant 2006;25:869-79.

4) Lower RR, Shumway NE. Studies on orthotopic homotransplantation of the canine heart. Surg Forum 1960;11:18-9.

5) Barnard CN. What we have learned about heart transplants. J Thorac Cardiovasc Surg 1968;56:457-68.

6) Rees AP, Milani RV, Lavie CJ, Smart FW, Ventura HO. Valvular regurgitation and right-sided cardiac pressures in heart transplant recipients by complete Doppler and color flow evaluation. Chest 1993;104:82-7.

7) Aziz T, Burgess M, Khafagy R, Wynn Hann A, Campbell C, Rahman A, et al. Bicaval and standard techniques in orthotopic heart transplantation: medium-term experience in cardiac performance and survival. J Thorac Cardiovasc Surg 1999;118:115-22.

8) Beniaminovitz A, Savoia MT, Oz M, Galantowicz M, Di Tullio MR, Homma S, et al. Improved atrial function in bicaval versus standard orthotopic techniques in cardiac transplantation. Am J Cardiol 1997;80:1631-5.

9) Herre JM, Barnhart GR, Llano A. Cardiac pacemakers in the transplanted heart: short term with the biatrial anastomosis and unnecessary with the bicaval anastomosis. Curr Opin Cardiol 2000;15:115-20.

10) Sievers HH, Weyand M, Kraatz EG, Bernhard A. An alternative technique for orthotopic cardiac transplantation, with preservation of the normal anatomy of the right atrium. Thorac Cardiovasc Surg 1991;39:70-2.

11) Sarsam MA, Campbell CS, Yonan NA, Deiraniya AK, Rahman AN. An alternative surgical technique in orthotopic cardiac transplantation. J Card Surg 1993;8:344-9.

12) Midei MG, Baughman KL, Achuff SC, Walford GD, Baumgartner W, Brinker JA. Is atrial activation beneficial in heart transplant recipients? J Am Coll Cardiol 1990;16:1201-4.

13) el Gamel A, Yonan NA, Grant S, Deiraniya AK, Rahman AN, Sarsam MA, et al. Orthotopic cardiac transplantation: a comparison of standard and bicaval Wythenshawe techniques. J Thorac Cardiovasc Surg 1995;109:721-9.

14) Leyh RG, Jahnke AW, Kraatz EG, Sievers HH. Cardiovascular dynamics and dimensions after bicaval and standard cardiac transplantation. Ann Thorac Surg 1995;59:1495-500.

15) Küçüker SA, Özatik MA, Tarcan O, Bardakcı H, Tüfekcioğlu O, Erdil N, et al. Analysis of surgical tecniques for heart transplantation. Turk Gogus Kalp Dama 2004;12:151-5.

16) Rothman SA, Jeevanandam V, Combs WG, Furukawa S, Hsia HH, Eisen HJ, et al. Eliminating bradyarrhythmias after orthotopic heart transplantation. Circulation 1996;94:II278-82.

17) Meyer SR, Modry DL, Bainey K, Koshal A, Mullen JC, Rebeyka IM, et al. Declining need for permanent pacemaker insertion with the bicaval technique of orthotopic heart transplantation. Can J Cardiol 2005;21:159-63.

18) Grant SC, Khan MA, Faragher EB, Yonan N, Brooks NH. Atrial arrhythmias and pacing after orthotopic heart transplantation: bicaval versus standard atrial anastomosis. Br Heart J 1995;74:149-53.

19) Cantillon DJ, Tarakji KG, Hu T, Hsu A, Smedira NG, Starling RC, et al. Long-term outcomes and clinical predictors for pacemaker-requiring bradyarrhythmias after cardiac transplantation: analysis of the UNOS/OPTN cardiac transplant database. Heart Rhythm 2010;7:1567-71.

20) Davies RR, Russo MJ, Morgan JA, Sorabella RA, Naka Y, Chen JM. Standard versus bicaval techniques for orthotopic heart transplantation: an analysis of the United Network for Organ Sharing database. J Thorac Cardiovasc Surg 2010;140:700-8, 708.e1-2.

21) Park KY, Park CH, Chun YB, Shin MS, Lee KC. Bicaval anastomosis reduces tricuspid regurgitation after heart transplantation. Asian Cardiovasc Thorac Ann 2005;13:251-4.

22) Solomon NA, McGiven J, Chen XZ, Alison PM, Graham KJ, Gibbs H. Biatrial or bicaval technique for orthotopic heart transplantation: which is better? Heart Lung Circ 2004;13:389-94.

23) Traversi E, Pozzoli M, Grande A, Forni G, Assandri J, Viganò M, et al. The bicaval anastomosis technique for orthotopic heart transplantation yields better atrial function than the standard technique: an echocardiographic automatic boundary detection study. J Heart Lung Transplant 1998;17:1065-74.

24) Aleksic I, Freimark D, Blanche C, Czer LS, Takkenberg JJ, Dalichau H, et al. Resting hemodynamics after total versus standard orthotopic heart transplantation in patients with high preoperative pulmonary vascular resistance. Eur J Cardiothorac Surg 1997;11:1037-44.

25) Grande AM, Rinaldi M, D\'Armini AM, Campana C, Traversi E, Pederzolli C, et al. Orthotopic heart transplantation: standard versus bicaval technique. Am J Cardiol 2000;85:1329-33.

26) Blanche C, Nessim S, Quartel A, Takkenberg JJ, Aleksic I, Cohen M, et al. Heart transplantation with bicaval and pulmonary venous anastomoses. A hemodynamic analysis of the first 117 patients. J Cardiovasc Surg (Torino) 1997;38:561-6.

27) Brandt M, Harringer W, Hirt SW, Walluscheck KP, Cremer J, Sievers HH, et al. Influence of bicaval anastomoses on late occurrence of atrial arrhythmia after heart transplantation. Ann Thorac Surg 1997;64:70-2.

28) Weiss ES, Nwakanma LU, Russell SB, Conte JV, Shah AS. Outcomes in bicaval versus biatrial techniques in heart transplantation: an analysis of the UNOS database. J Heart Lung Transplant 2008;27:178-83.

29) Laske A, Carrel T, Niederhäuser U, Pasic M, von Segesser LK, Jenni R, et al. Modified operation technique for orthotopic heart transplantation. Eur J Cardiothorac Surg 1995;9:120-6.

30) Wang SS, Chu SH, Hsu RB, Chen YS, Chou NK, Ko WJ. Is bicaval anastomosis superior to standard atrial procedure of heart transplantation? Transplant Proc 2000;32:2396-7.

31) Milano CA, Shah AS, Van Trigt P, Jaggers J, Davis RD, Glower DD, et al. Evaluation of early postoperative results after bicaval versus standard cardiac transplantation and review of the literature. Am Heart J 2000;140:717-21.

32) Deleuze PH, Benvenuti C, Mazzucotelli JP, Perdrix C, Le Besnerais P, Mourtada A, et al. Orthotopic cardiac transplantation with direct caval anastomosis: is it the optimal procedure? J Thorac Cardiovasc Surg 1995;109:731-7.

33) Riberi A, Ambrosi P, Habib G, Kreitmann B, Yao JG, Gaudart J, et al. Systemic embolism: a serious complication after cardiac transplantation avoidable by bicaval technique. Eur J Cardiothorac Surg 2001;19:307-11.

34) Jung SH, Kim JJ, Choo SJ, Yun TJ, Chung CH, Lee JW. Long-term mortality in adult orthotopic heart transplant recipients. J Korean Med Sci 2011;26:599-603.

35) Kendall SW, Ciulli F, Biocina B, Mullins PA, Schofield P, Wells FC, et al. Atrioventricular orthotopic heart transplantation: a prospective randomised clinical trial in 60 consecutive patients. Transplant Proc 1993;25:1172-3.

36) Pahl E, Sundararaghavan S, Strasburger JF, Mitchell BM, Rodgers S, Crowley D, et al. Impaired exercise parameters in pediatric heart transplant recipients: comparison of biatrial and bicaval techniques. Pediatr Transplant 2000;4:268-72.

37) Fiorelli AI, Santos RH, Oliveira JL Jr, Da Silva MA, Dos Santos VP Jr, Rêgo FM, et al. Long-term pulmonary vascular reactivity after orthotopic heart transplantation by the biatrial versus the bicaval technique. Transplant Proc 2011;43:229-32.

38) Sun JP, Niu J, Banbury MK, Zhou L, Taylor DO, Starling RC, et al. Influence of different implantation techniques on long-term survival after orthotopic heart transplantation: an echocardiographic study. J Heart Lung Transplant 2007;26:1243-8.

39) Freimark D, Czer LS, Aleksic I, Barthold C, Admon D, Trento A, et al. Improved left atrial transport and function with orthotopic heart transplantation by bicaval and pulmonary venous anastomoses. Am Heart J 1995;130:121-6.

40) Grande AM, Gaeta R, Campana C, Klersy C, Riva L, D\'Armini AM, et al. Comparison of standard and bicaval approach in orthotopic heart transplantation: 10-year followup. J Cardiovasc Med (Hagerstown) 2008;9:493-7.

41) el-Gamel A, Deiraniya AK, Rahman AN, Campbell CS, Yonan NA. Orthotopic heart transplantation hemodynamics: does atrial preservation improve cardiac output after transplantation? J Heart Lung Transplant 1996;15:564-71.

42) Cui G, Tung T, Kobashigawa J, Laks H, Sen L. Increased incidence of atrial flutter associated with the rejection of heart transplantation. Am J Cardiol 2001;88:280-4.

43) Kalra N, Copeland JG, Sorrell VL. Tricuspid regurgitation after orthotopic heart transplantation. Echocardiography 2010;27:1-4.

44) Blanche C, Valenza M, Czer LS, Barath P, Admon D, Harasty D, et al. Orthotopic heart transplantation with bicaval and pulmonary venous anastomoses. Ann Thorac Surg 1994;58:1505-9.

45) Angermann CE, Spes CH, Tammen A, Stempfle HU, Schütz A, Kemkes BM, et al. Anatomic characteristics and valvular function of the transplanted heart: transthoracic versus transesophageal echocardiographic findings. J Heart Transplant 1990;9:331-8.

46) Schnoor M, Schäfer T, Lühmann D, Sievers HH. Bicaval versus standard technique in orthotopic heart transplantation: a systematic review and meta-analysis. J Thorac Cardiovasc Surg 2007;134:1322-31.

47) Locali RF, Matsuoka PK, Cherbo T, Gabriel EA, Buffolo E. Should biatrial heart transplantation still be performed?: A Meta-analysis. Arq Bras Cardiol 2010;94:829-40.

48) Kratochwill C, Schmid S, Koller-Strametz J, Kreiner G, Grabenwöger M, Grimm M, et al. Decrease in pacemaker incidence after orthotopic heart transplantation. Am J Cardiol 1996;77:779-83.

49) Jeevanandam V, Russell H, Mather P, Furukawa S, Anderson A, Raman J. Donor tricuspid annuloplasty during orthotopic heart transplantation: long-term results of a prospective controlled study. Ann Thorac Surg 2006;82:2089-95.

50) Heinz G, Kratochwill C, Koller-Strametz J, Kreiner G, Grimm M, Grabenwöger M, et al. Benign prognosis of early sinus node dysfunction after orthotopic cardiac transplantation. Pacing Clin Electrophysiol 1998;21:422-9.

51) Bacal F, Bocchi EA, Vieira ML, Lopes N, Moreira LF, Fiorelli A, et al. Permanent and temporary pacemaker implantation after orthotopic heart transplantation. Arq Bras Cardiol 2000;74:9-12.

52) Jacquet L, Ziady G, Stein K, Griffith B, Armitage J, Hardesty R, et al. Cardiac rhythm disturbances early after orthotopic heart transplantation: prevalence and clinical importance of the observed abnormalities. J Am Coll Cardiol 1990;16:832-7.

53) Bouchart F, Derumeaux G, Mouton-Schleifer D, Bessou JP, Redonnet M, Soyer R. Conventional and total orthotopic cardiac transplantation: a comparative clinical and echocardiographical study. Eur J Cardiothorac Surg 1997;12:555-9.

54) Wei J, Chang CY, Chuang YC, Chen HL. Updates in heart transplantation. Transplant Proc 2008;40:2594-6.