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Effects of Preoperative Nutritional Status and Lymphocyte Count on the Development of Early-term Atrial Fibrillation After Coronary Artery Bypass Grafting: A Retrospective Study

ABSTRACT

Introduction:

Although there are publications in the literature stating that parameters related to the nutritional status of patients are associated with the clinical outcomes of those with coronary artery disease, it is also stated that there is insufficient data on the relationship between nutritional indices and long-term outcomes and major adverse cardiovascular events in patients undergoing isolated coronary artery bypass grafting.

Methods:

This retrospective study was conducted with patients who underwent isolated elective on-pump coronary artery bypass grafting in our hospital. Patients who underwent emergency coronary artery bypass grafting or those with known atrial fibrillation in the preoperative period were excluded. Patients were analyzed and compared in two groups according to the development of postoperative atrial fibrillation.

Results:

The data of 93 coronary artery bypass grafting patients (71 [76%] males) with a mean age of 62.86 ± 9.53 years included in the study were evaluated. Both groups had similar preoperative ejection fraction value, hemoglobin level, age, number of distal bypasses, and postoperative mortality rates. Although the mean cardiopulmonary bypass and aortic cross-clamping times were higher in Group 1, they were not statistically significant. In our study, the mean prognostic nutrition index value was 51.76 ± 3002.

Conclusion:

According to our study results, there was no statistically significant difference between prognostic nutrition index values and the development of atrial fibrillation after coronary artery bypass grafting, which is similar to some publications in the literature. We think that it would be beneficial to conduct randomized studies involving more patients on this subject.

Keywords:
Coronary Artery Disease; Nutrition Assessment; Atrial Fibrillation; Lymphopenia; Cardiopulmonary Bypass

INTRODUCTION

Abbreviations, Acronyms & Symbols AF = Atrial fibrillation CABG = Coronary artery bypass grafting CAD = Coronary artery disease CPB = Cardiopulmonary bypass CRP = C-reactive protein DM = Diabetes mellitus ECG = Electrocardiogram EF = Ejection fraction IABP = Intra-aortic balloon pump PNI = Prognostic Nutrition Index

Coronary artery bypass grafting (CABG) is still been reported as the recommended treatment for coronary artery disease (CAD)[11 Tasbulak O, Guler A, Duran M, Sahin A, Bulut U, Avci Y, et al. Association between nutritional indices and long-term outcomes in patients undergoing isolated coronary artery bypass grafting. Cureus. 2021;13(7):e16567. doi:10.7759/cureus.16567.
https://doi.org/10.7759/cureus.16567...
], which is a major health problem worldwide, especially in patients with diabetes mellitus or left main coronary disease[22 Moran AE, Forouzanfar MH, Roth GA, Mensah GA, Ezzati M, Murray CJ, et al. Temporal trends in ischemic heart disease mortality in 21 world regions, 1980 to 2010: the global burden of disease 2010 study. Circulation. 2014;129(14):1483-92. doi:10.1161/CIRCULATIONAHA.113.004042.
https://doi.org/10.1161/CIRCULATIONAHA.1...
,33 Singh AK. Percutaneous coronary intervention vs coronary artery bypass grafting in the management of chronic stable angina: a critical appraisal. J Cardiovasc Dis Res. 2010;1(2):54-8. doi:10.1016/s0975-3583(10)12003-8.
https://doi.org/10.1016/s0975-3583(10)12...
]. It has been stated that an important complication after CABG is rhythm problems, the most common of which is atrial fibrillation (AF), and its incidence is reported to be 10-40%[44 Engin M, Ozsin KK, Savran M, Guvenc O, Yavuz S, Ozyazicioglu AF. Visceral adiposity index and prognostic nutritional index in predicting atrial fibrillation after on-pump coronary artery bypass operations: a prospective study. Braz J Cardiovasc Surg. 2021;36(4):522-9. doi:10.21470/1678-9741-2020-0044.
https://doi.org/10.21470/1678-9741-2020-...

5 Topal D, Korkmaz UTK, Velioglu Y, Yuksel A, Donmez I, Uçaroğlu ER, et al. Systemic immune-inflammation index as a novel predictor of atrial fibrillation after off-pump coronary artery bypass grafting. Rev Assoc Med Bras (1992). 2022;68(9):1240-6. doi:10.1590/1806-9282.20220295.
https://doi.org/10.1590/1806-9282.202202...
-66 Velioglu Y, Yuksel A. Predictors of postoperative atrial fibrillation after beating-heart coronary artery bypass surgery: is cardiopulmonary bypass a risk factor? Acta Cardiol Sin. 2019;35(5):468-75. doi:10.6515/ACS.201909_35(5).20190325A.
https://doi.org/10.6515/ACS.201909_35(5)...
]. This adverse condition is an important cause of mortality and morbidity after CABG, and it has been reported that advanced age, low ejection fraction (EF), thyroid disease, and chronic obstructive pulmonary disease are among the main known risk factors[77 Jaimes MC, Torrado LAA, Reyes NFS, Mackenzie JC, Mallarino JPU. Hypothyroidism is a risk factor for atrial fibrillation after coronary artery bypass graft. Braz J Cardiovasc Surg. 2017;32(6):475-80. doi:10.21470/1678-9741-2017-0080.
https://doi.org/10.21470/1678-9741-2017-...
]. It has been stated that many factors, such as surgical trauma, use of cardiopulmonary bypass (CPB), non-use of beta-blocker agents, hypoxia, and electrolyte imbalance, have been implicated in the pathogenesis of newly occurring AF after CABG[55 Topal D, Korkmaz UTK, Velioglu Y, Yuksel A, Donmez I, Uçaroğlu ER, et al. Systemic immune-inflammation index as a novel predictor of atrial fibrillation after off-pump coronary artery bypass grafting. Rev Assoc Med Bras (1992). 2022;68(9):1240-6. doi:10.1590/1806-9282.20220295.
https://doi.org/10.1590/1806-9282.202202...
]. In addition to the fact that the inflammatory process is known to be one of the pathophysiologic factors contributing to the occurrence of AF[88 Rezaei Y, Peighambari MM, Naghshbandi S, Samiei N, Ghavidel AA, Dehghani MR, et al. Postoperative atrial fibrillation following cardiac surgery: from pathogenesis to potential therapies. Am J Cardiovasc Drugs. 2020;20(1):19-49. doi:10.1007/s40256-019-00365-1.
https://doi.org/10.1007/s40256-019-00365...
], it has also been reported that a high body mass index increases the development of postoperative AF[99 Hernandez AV, Kaw R, Pasupuleti V, Bina P, Ioannidis JP, Bueno H, et al. Association between obesity and postoperative atrial fibrillation in patients undergoing cardiac operations: a systematic review and meta-analysis. Ann Thorac Surg. 2013;96(3):1104-16. doi:10.1016/j.athoracsur.2013.04.029.
https://doi.org/10.1016/j.athoracsur.201...
].

Although there are publications in the literature stating that parameters related to the nutritional status of patients are associated with clinical outcomes in those with CAD[11 Tasbulak O, Guler A, Duran M, Sahin A, Bulut U, Avci Y, et al. Association between nutritional indices and long-term outcomes in patients undergoing isolated coronary artery bypass grafting. Cureus. 2021;13(7):e16567. doi:10.7759/cureus.16567.
https://doi.org/10.7759/cureus.16567...
,1010 Chen SC, Yang YL, Wu CH, Huang SS, Chan WL, Lin SJ, et al. Association between preoperative nutritional status and clinical outcomes of patients with coronary artery disease undergoing percutaneous coronary intervention. Nutrients. 2020;12(5):1295. doi:10.3390/nu12051295.
https://doi.org/10.3390/nu12051295...
] and that they are effective in predicting mortality in patients undergoing CABG, it is also stated that there is insufficient data on the relationship between nutritional indices and long-term outcomes and major adverse cardiovascular events in patients undergoing isolated CABG[11 Tasbulak O, Guler A, Duran M, Sahin A, Bulut U, Avci Y, et al. Association between nutritional indices and long-term outcomes in patients undergoing isolated coronary artery bypass grafting. Cureus. 2021;13(7):e16567. doi:10.7759/cureus.16567.
https://doi.org/10.7759/cureus.16567...
]. Although it has been reported that a low lymphocyte count may be a risk factor for poor postoperative outcomes and an indicator of poor survival in the same patient group[1111 Aghdaii N, Ferasatkish R, Mohammadzadeh Jouryabi A, Hamidi SH. Significance of preoperative total lymphocyte count as a prognostic criterion in adult cardiac surgery. Anesth Pain Med. 2014;4(3):e20331. doi:10.5812/aapm.20331.
https://doi.org/10.5812/aapm.20331...
], the Prognostic Nutrition Index (PNI)[1212 Dolapoglu A, Avci E, Kiris T, Bugra O. The predictive value of the prognostic nutritional index for postoperative acute kidney injury in patients undergoing on-pump coronary bypass surgery. J Cardiothorac Surg. 2019;14(1):74. doi:10.1186/s13019-019-0898-7.
https://doi.org/10.1186/s13019-019-0898-...
] which is formulated by serum albumin and lymphocyte count and is a marker used for simple and objective assessment of the nutritional status of individuals, may be a risk factor for postoperative AF[44 Engin M, Ozsin KK, Savran M, Guvenc O, Yavuz S, Ozyazicioglu AF. Visceral adiposity index and prognostic nutritional index in predicting atrial fibrillation after on-pump coronary artery bypass operations: a prospective study. Braz J Cardiovasc Surg. 2021;36(4):522-9. doi:10.21470/1678-9741-2020-0044.
https://doi.org/10.21470/1678-9741-2020-...
]. In addition, even in the presence of similar risk factors, there are significant differences in the development of new AF in some patients, and the reasons for this are still unknown[1313 Yilmaz Y, Kelesoglu S, Elcik D, Ozmen R, Kalay N. Predictive values of systemic immune-inflammation index in new-onset atrial fibrillation following coronary artery bypass grafting. Braz J Cardiovasc Surg. 2023;38(1):96-103. doi:10.21470/1678-9741-2021-0278.
https://doi.org/10.21470/1678-9741-2021-...
].

Our study aimed to assess the factors contributing to the onset of postoperative AF in isolated elective on-pump CABG patients. Additionally, we investigated the impact of preoperative PNI and lymphocyte values on the development of postoperative AF in this patient group. Finally, we discussed our findings concerning the existing literature.

METHODS

Our study was conducted with patients who underwent isolated elective on-pump CABG in our tertiary care hospital between December 2021 and June 2022. Declaration of Helsinki criteria were followed, and the ethical approval was obtained (Ethics Committee Unit, 2023-215115237). Our retrospective study included patients who underwent elective isolated on-pump CABG in our hospital with available study data. Patients who underwent emergency CABG operation, patients who underwent off-pump CABG operation, patients who underwent cardiac or major vascular surgery simultaneously with CABG operation, patients who underwent another open-heart operation other than CABG operation, patients who previously underwent open-heart surgery, patients with severe left ventricular dysfunction, and patients with known AF or severe cardiac arrhythmia in the preoperative period were excluded. Preoperative and postoperative medical data (preoperative baseline clinical characteristics, comorbidities, laboratory parameters, intraoperative data, and significant postoperative complications) of the patients included in the study were reviewed and recorded from the hospital automation system and hospital file archives. A total of 93 patients included in the study were analyzed and compared in two groups according to the development of postoperative AF - Group 1, patients with postoperative AF; and Group 0, patients without postoperative AF.

Fasting (6-8 hours) venous blood tests and biochemical markers were measured in all patients during hospitalization for the operation. Hematologic parameters and serum albumin, lymphocyte, and creatinine values were measured in the laboratory before CABG. The preoperative PNI value of the patients was calculated using the formula [albumin (g/dl) × 10 + lymphocyte count (permm3) × 0.005] as stated in a publication in the literature[1212 Dolapoglu A, Avci E, Kiris T, Bugra O. The predictive value of the prognostic nutritional index for postoperative acute kidney injury in patients undergoing on-pump coronary bypass surgery. J Cardiothorac Surg. 2019;14(1):74. doi:10.1186/s13019-019-0898-7.
https://doi.org/10.1186/s13019-019-0898-...
].

Coronary Artery Bypass Surgery Procedure

CABG operations were generally made with general anesthesia through standard median sternotomy. CABG was performed under CPB guidance in all patients. In all patients, myocardial protection was achieved with antegrade cold blood cardioplegia from the aortic root with intermittent retrograde cold blood cardioplegia from the coronary sinus, and complete revascularization was made. After the operation, the patients were admitted to the cardiovascular surgery intensive care unit and immediately monitored and followed up for 24 hours with a standard D2 lead. They were extubated when they were sufficiently awake and spontaneously breathing, and there was no abnormality in their blood gas parameters and hemodynamic status. Blood transfusions were administered when necessary (if the hematocrit level was < 24-25%).

New-onset AF after CABG was defined as an episode of AF lasting > 5 minutes, detected (by monitoring or 12-lead electrocardiogram [ECG]) during hospitalization. The patients’ immediate monitoring and daily ECG findings determined the presence or absence of AF.

Statistical Analysis

We conducted all statistical analyses using IBM Corp. Released 2015, IBM SPSS Statistics for Windows, version 23.0, Armonk, NY: IBM Corp. Continuous variables were expressed as mean ± standard deviation. Where appropriate, categorical variables were compared using the chi-square test and Fisher’s exact test. Continuous variables with normal distribution were compared using independent samples t-test. Non-parametric data were compared using the Mann-Whitney U test. A P-value ≤ 0.05 was statistically significant.

RESULTS

The data of 93 CABG patients (71 [76%] males) with a mean age of 62.86 ± 9.53 years included in the study were evaluated in the Cardiovascular Surgery Department of our hospital during the study period. Demographic data of the patients are demonstrated in Table 1. Both groups had similar preoperative EF value, hemoglobin level, age, number of distal bypasses, and postoperative mortality rates. Although the mean CPB and cross-clamping times were higher in Group 1, they were not statistically significant. The characteristics of the patients in Groups 0 and 1 are demonstrated in Table 2. In our study, the mean PNI value was 51.76 ± 30.02, and the data regarding the development of AF according to PNI value and lymphocyte count are shown in Table 3 and Table 4, respectively. All patients in the study group were started on oral beta-blocker therapy in the preoperative period since their hospitalization.

Table 1
Demographic data of study patients.
Table 2
Demographic characteristics and laboratory findings of the groups.
Table 3
Data on postoperative AF development by level of PNI value.
Table 4
Data on postoperative AF development by level of lymphocyte count.

DISCUSSION

It has been reported that CABG is still the recommended treatment method for CAD, especially in diabetic or left main coronary disease patients[33 Singh AK. Percutaneous coronary intervention vs coronary artery bypass grafting in the management of chronic stable angina: a critical appraisal. J Cardiovasc Dis Res. 2010;1(2):54-8. doi:10.1016/s0975-3583(10)12003-8.
https://doi.org/10.1016/s0975-3583(10)12...
]. One of the important complications that develop after CABG is rhythm problems, and the most common one is AF, which is reported to be observed in approximately 50% of this patient group[44 Engin M, Ozsin KK, Savran M, Guvenc O, Yavuz S, Ozyazicioglu AF. Visceral adiposity index and prognostic nutritional index in predicting atrial fibrillation after on-pump coronary artery bypass operations: a prospective study. Braz J Cardiovasc Surg. 2021;36(4):522-9. doi:10.21470/1678-9741-2020-0044.
https://doi.org/10.21470/1678-9741-2020-...

5 Topal D, Korkmaz UTK, Velioglu Y, Yuksel A, Donmez I, Uçaroğlu ER, et al. Systemic immune-inflammation index as a novel predictor of atrial fibrillation after off-pump coronary artery bypass grafting. Rev Assoc Med Bras (1992). 2022;68(9):1240-6. doi:10.1590/1806-9282.20220295.
https://doi.org/10.1590/1806-9282.202202...
-66 Velioglu Y, Yuksel A. Predictors of postoperative atrial fibrillation after beating-heart coronary artery bypass surgery: is cardiopulmonary bypass a risk factor? Acta Cardiol Sin. 2019;35(5):468-75. doi:10.6515/ACS.201909_35(5).20190325A.
https://doi.org/10.6515/ACS.201909_35(5)...
]. The main risk factors for newly AF after cardiac operations, stated as an important cause of mortality and morbidity, are reported to be old age, low EF, and thyroid disease[77 Jaimes MC, Torrado LAA, Reyes NFS, Mackenzie JC, Mallarino JPU. Hypothyroidism is a risk factor for atrial fibrillation after coronary artery bypass graft. Braz J Cardiovasc Surg. 2017;32(6):475-80. doi:10.21470/1678-9741-2017-0080.
https://doi.org/10.21470/1678-9741-2017-...
]. Besides surgical trauma and CPB use, many factors, such as hypoxia and electrolyte imbalances, are responsible for the pathogenesis of newly AF in the postoperative CABG period[55 Topal D, Korkmaz UTK, Velioglu Y, Yuksel A, Donmez I, Uçaroğlu ER, et al. Systemic immune-inflammation index as a novel predictor of atrial fibrillation after off-pump coronary artery bypass grafting. Rev Assoc Med Bras (1992). 2022;68(9):1240-6. doi:10.1590/1806-9282.20220295.
https://doi.org/10.1590/1806-9282.202202...
]. In addition to the fact that the systemic inflammation is known to be a pathophysiological factor contributing to the occurrence of AF[88 Rezaei Y, Peighambari MM, Naghshbandi S, Samiei N, Ghavidel AA, Dehghani MR, et al. Postoperative atrial fibrillation following cardiac surgery: from pathogenesis to potential therapies. Am J Cardiovasc Drugs. 2020;20(1):19-49. doi:10.1007/s40256-019-00365-1.
https://doi.org/10.1007/s40256-019-00365...
], it is also stated that a high body mass index increases the occurrence of postoperative AF[99 Hernandez AV, Kaw R, Pasupuleti V, Bina P, Ioannidis JP, Bueno H, et al. Association between obesity and postoperative atrial fibrillation in patients undergoing cardiac operations: a systematic review and meta-analysis. Ann Thorac Surg. 2013;96(3):1104-16. doi:10.1016/j.athoracsur.2013.04.029.
https://doi.org/10.1016/j.athoracsur.201...
]. In the literature, it is stated that there is a relationship between the nutritional status of patients undergoing isolated CABG and long-term important undesirable events and morbidity, that nutritional degree has a critical role in terms of organ and tissue functions, and that in case of malnutrition, the supply of food required for basal organ functions decreases, and disruption in protein turnover occurs[11 Tasbulak O, Guler A, Duran M, Sahin A, Bulut U, Avci Y, et al. Association between nutritional indices and long-term outcomes in patients undergoing isolated coronary artery bypass grafting. Cureus. 2021;13(7):e16567. doi:10.7759/cureus.16567.
https://doi.org/10.7759/cureus.16567...
,1414 Bhamidipati CM, LaPar DJ, Mehta GS, Kern JA, Upchurch GR Jr, Kron IL, et al. Albumin is a better predictor of outcomes than body mass index following coronary artery bypass grafting. Surgery. 2011;150(4):626-34. doi:10.1016/j.surg.2011.07.056.
https://doi.org/10.1016/j.surg.2011.07.0...
].

Malnutrition has been reported to be related to bad prognosis, especially in old age patients with chronic diseases such as heart failure or CAD or malignancies[11 Tasbulak O, Guler A, Duran M, Sahin A, Bulut U, Avci Y, et al. Association between nutritional indices and long-term outcomes in patients undergoing isolated coronary artery bypass grafting. Cureus. 2021;13(7):e16567. doi:10.7759/cureus.16567.
https://doi.org/10.7759/cureus.16567...
,1515 Gomes F, Emery PW, Weekes CE. Risk of malnutrition is an independent predictor of mortality, length of hospital stay, and hospitalization costs in stroke patients. J Stroke Cerebrovasc Dis. 2016;25(4):799-806. doi:10.1016/j.jstrokecerebrovasdis.2015.12.017.
https://doi.org/10.1016/j.jstrokecerebro...
], some markers such as PNI scores have been developed to determine nutritional status, and the relationship between these parameters and cardiovascular diseases has been shown in some studies[11 Tasbulak O, Guler A, Duran M, Sahin A, Bulut U, Avci Y, et al. Association between nutritional indices and long-term outcomes in patients undergoing isolated coronary artery bypass grafting. Cureus. 2021;13(7):e16567. doi:10.7759/cureus.16567.
https://doi.org/10.7759/cureus.16567...
,1010 Chen SC, Yang YL, Wu CH, Huang SS, Chan WL, Lin SJ, et al. Association between preoperative nutritional status and clinical outcomes of patients with coronary artery disease undergoing percutaneous coronary intervention. Nutrients. 2020;12(5):1295. doi:10.3390/nu12051295.
https://doi.org/10.3390/nu12051295...
,1616 Kawamiya T, Suzuki S, Ishii H, Hirayama K, Harada K, Shibata Y, et al. Correlations between geriatric nutritional risk index and peripheral artery disease in elderly coronary artery disease patients. Geriatr Gerontol Int. 2017;17(7):1057-62. doi:10.1111/ggi.12828.
https://doi.org/10.1111/ggi.12828...
].

It has been reported that several studies have shown a link between the development of postoperative AF and inflammatory biomarkers[1313 Yilmaz Y, Kelesoglu S, Elcik D, Ozmen R, Kalay N. Predictive values of systemic immune-inflammation index in new-onset atrial fibrillation following coronary artery bypass grafting. Braz J Cardiovasc Surg. 2023;38(1):96-103. doi:10.21470/1678-9741-2021-0278.
https://doi.org/10.21470/1678-9741-2021-...
,1717 Erdolu B, As AK, Engin M. The relationship between the HATCH score, neutrophil to lymphocyte ratio and postoperative atrial fibrillation after off-pump coronary artery bypass graft surgery. Heart Surg Forum. 2020;23(1):E088-E092. doi:10.1532/hsf.2771.
https://doi.org/10.1532/hsf.2771...
]. Surgical stress and CPB were reported as cause of immune response, which is influenced by lymphocytes and other anti-inflammatory factors[55 Topal D, Korkmaz UTK, Velioglu Y, Yuksel A, Donmez I, Uçaroğlu ER, et al. Systemic immune-inflammation index as a novel predictor of atrial fibrillation after off-pump coronary artery bypass grafting. Rev Assoc Med Bras (1992). 2022;68(9):1240-6. doi:10.1590/1806-9282.20220295.
https://doi.org/10.1590/1806-9282.202202...
,1212 Dolapoglu A, Avci E, Kiris T, Bugra O. The predictive value of the prognostic nutritional index for postoperative acute kidney injury in patients undergoing on-pump coronary bypass surgery. J Cardiothorac Surg. 2019;14(1):74. doi:10.1186/s13019-019-0898-7.
https://doi.org/10.1186/s13019-019-0898-...
]. Also, it has been reported that preoperative lymphocyte count is a straight forward inflammatory marker that can be obtained easily, and lymphopenia may indicate poor survival after cardiac surgery and be associated with important undesirable events[1212 Dolapoglu A, Avci E, Kiris T, Bugra O. The predictive value of the prognostic nutritional index for postoperative acute kidney injury in patients undergoing on-pump coronary bypass surgery. J Cardiothorac Surg. 2019;14(1):74. doi:10.1186/s13019-019-0898-7.
https://doi.org/10.1186/s13019-019-0898-...
]. Preoperative lymphocyte count is reported to be an important predictor of mortality in patients undergoing cardiac surgery, and there is an association between low preoperative lymphocyte count and the length of CPB[1111 Aghdaii N, Ferasatkish R, Mohammadzadeh Jouryabi A, Hamidi SH. Significance of preoperative total lymphocyte count as a prognostic criterion in adult cardiac surgery. Anesth Pain Med. 2014;4(3):e20331. doi:10.5812/aapm.20331.
https://doi.org/10.5812/aapm.20331...
,1818 Azab B, Shariff MA, Bachir R, Nabagiez JP, McGinn JT Jr. Elevated preoperative neutrophil/lymphocyte ratio as a predictor of increased long-term survival in minimal invasive coronary artery bypass surgery compared to sternotomy. J Cardiothorac Surg. 2013;8:193. doi:10.1186/1749-8090-8-193.
https://doi.org/10.1186/1749-8090-8-193...
]. In addition, malnutrition and the severity of cardiovascular disease have been reported to cause preoperative lymphocyte count reduction and dysfunction[1111 Aghdaii N, Ferasatkish R, Mohammadzadeh Jouryabi A, Hamidi SH. Significance of preoperative total lymphocyte count as a prognostic criterion in adult cardiac surgery. Anesth Pain Med. 2014;4(3):e20331. doi:10.5812/aapm.20331.
https://doi.org/10.5812/aapm.20331...
,1919 Nishida T, Sakakibara H. Association between underweight and low lymphocyte count as an indicator of malnutrition in Japanese women. J Womens Health (Larchmt). 2010;19(7):1377-83. doi:10.1089/jwh.2009.1857.
https://doi.org/10.1089/jwh.2009.1857...
,2020 Szigligeti P, Neumeier L, Duke E, Chougnet C, Takimoto K, Lee SM, et al. Signalling during hypoxia in human T lymphocytes--critical role of the src protein tyrosine kinase p56Lck in the O2 sensitivity of Kv1.3 channels. J Physiol. 2006;573(Pt 2):357-70. doi:10.1113/jphysiol.2006.109967.
https://doi.org/10.1113/jphysiol.2006.10...
]. In our study, although the mean preoperative lymphocyte count was lower in the group with AF compared to the other group (1.84 ± 0.57 vs. 1.98 ± 0.78, respectively, P=0.084), it was not statistically significant. In addition, there was no statistical difference between the group with lymphocyte count < 1.5 (109/L) and the group with lymphocyte count > 1.5 (109/L) in terms of the development of new postoperative AF, in our study. In the literature, it is reported that inflammation and immune-based prognostic scores, as well as established pro-inflammatory biomarkers such as C-reactive protein (CRP) levels, predict mortality and morbidity after cardiac surgery[2121 Uğuz B, Topal D, Badem S, Kahraman N, Uğuz İ. Systemic immune-inflammation index: a novel predictor for risk of postoperative atrial fibrillation in patients undergoing isolated coronary artery bypass grafting. Heart Surg Forum. 2022;25(5):E665-73. doi:10.1532/hsf.4861.
https://doi.org/10.1532/hsf.4861...
,2222 Iliopoulos I, Alder MN, Cooper DS, Villarreal EG, Loomba R, Sahay RD, et al. Pre-operative neutrophil-lymphocyte ratio predicts low cardiac output in children after cardiac surgery. Cardiol Young. 2020;30(4):521-5. doi:10.1017/S1047951120000487.
https://doi.org/10.1017/S104795112000048...
]. Although it has been reported that CRP and natriuretic peptides are promising biological markers for the development of AF[2323 Noubiap JJ, Sanders P, Nattel S, Lau DH. Biomarkers in atrial fibrillation: pathogenesis and clinical implications. Card Electrophysiol Clin. 2021;13(1):221-33. doi:10.1016/j.ccep.2020.10.006.
https://doi.org/10.1016/j.ccep.2020.10.0...
], in the same study, they report that the relationship between preoperative and postoperative CRP levels and postoperative AF development in CABG patients cannot be detected[2121 Uğuz B, Topal D, Badem S, Kahraman N, Uğuz İ. Systemic immune-inflammation index: a novel predictor for risk of postoperative atrial fibrillation in patients undergoing isolated coronary artery bypass grafting. Heart Surg Forum. 2022;25(5):E665-73. doi:10.1532/hsf.4861.
https://doi.org/10.1532/hsf.4861...
]. In another study in the literature, CRP levels are high in patients with AF, however, it has been reported that there is no correlation between CRP levels measured before cardioversion and AF, and therefore CRP cannot be considered pathogenic for AF and does not help predict postoperative AF[2121 Uğuz B, Topal D, Badem S, Kahraman N, Uğuz İ. Systemic immune-inflammation index: a novel predictor for risk of postoperative atrial fibrillation in patients undergoing isolated coronary artery bypass grafting. Heart Surg Forum. 2022;25(5):E665-73. doi:10.1532/hsf.4861.
https://doi.org/10.1532/hsf.4861...
,2424 Zhou X, Dudley SC Jr. Evidence for inflammation as a driver of atrial fibrillation. Front Cardiovasc Med. 2020;7:62. doi:10.3389/fcvm.2020.00062.
https://doi.org/10.3389/fcvm.2020.00062...
]. A retrospective study published by Uguz B et al.[2121 Uğuz B, Topal D, Badem S, Kahraman N, Uğuz İ. Systemic immune-inflammation index: a novel predictor for risk of postoperative atrial fibrillation in patients undergoing isolated coronary artery bypass grafting. Heart Surg Forum. 2022;25(5):E665-73. doi:10.1532/hsf.4861.
https://doi.org/10.1532/hsf.4861...
], which was conducted in 116 CABG patients, reported that postoperative AF was developed in 22.4% of the patients and preoperative lymphocyte (103/µL) value was found to be 2.5 (1-5.3) and 1.3 (0.4-2.8) in the postoperative AF group and postoperative non-AF group, respectively (P<.001); also, the preoperative CRP (mg/L) value was 6.8 (0.6-121.1) and 6.6 (1.2-67.1) in their study, respectively, it and was not statistically significant (P=0.866). In the same study, it was reported that CRP value at the 72nd postoperative hour was found to be 61.6 (1.4-327.4) and 49.8 (9.4-219.9), respectively, and it was not found to be statistically significant (P=0.369)[2121 Uğuz B, Topal D, Badem S, Kahraman N, Uğuz İ. Systemic immune-inflammation index: a novel predictor for risk of postoperative atrial fibrillation in patients undergoing isolated coronary artery bypass grafting. Heart Surg Forum. 2022;25(5):E665-73. doi:10.1532/hsf.4861.
https://doi.org/10.1532/hsf.4861...
]. Similarly, in our study, preoperative CRP values (mg/l) were determined as 8.60 ± 16.84 in the new postoperative AF group and 15.56 ± 23.38 in the group without new AF, and no statistical difference was detected (P=0.478).

It has been reported that albumin cells are important because of their anti-inflammatory and anticoagulant features[44 Engin M, Ozsin KK, Savran M, Guvenc O, Yavuz S, Ozyazicioglu AF. Visceral adiposity index and prognostic nutritional index in predicting atrial fibrillation after on-pump coronary artery bypass operations: a prospective study. Braz J Cardiovasc Surg. 2021;36(4):522-9. doi:10.21470/1678-9741-2020-0044.
https://doi.org/10.21470/1678-9741-2020-...
,2525 Arques S. Human serum albumin in cardiovascular diseases. Eur J Intern Med. 2018;52:8-12. doi:10.1016/j.ejim.2018.04.014.
https://doi.org/10.1016/j.ejim.2018.04.0...
] and that hypoalbuminemia may be a marker for the development of arterial atherosclerosis and thrombosis, but it has also been reported that hypoalbuminemia associated with malnutrition is an independent predictor of some cardiovascular diseases such as CAD[11 Tasbulak O, Guler A, Duran M, Sahin A, Bulut U, Avci Y, et al. Association between nutritional indices and long-term outcomes in patients undergoing isolated coronary artery bypass grafting. Cureus. 2021;13(7):e16567. doi:10.7759/cureus.16567.
https://doi.org/10.7759/cureus.16567...
,44 Engin M, Ozsin KK, Savran M, Guvenc O, Yavuz S, Ozyazicioglu AF. Visceral adiposity index and prognostic nutritional index in predicting atrial fibrillation after on-pump coronary artery bypass operations: a prospective study. Braz J Cardiovasc Surg. 2021;36(4):522-9. doi:10.21470/1678-9741-2020-0044.
https://doi.org/10.21470/1678-9741-2020-...
,2626 Keskin M, İpek G, Aldağ M, Altay S, Hayıroğlu Mİ, Börklü EB, et al. Effect of nutritional status on mortality in patients undergoing coronary artery bypass grafting. Nutrition. 2018;48:82-6. doi:10.1016/j.nut.2017.10.024.
https://doi.org/10.1016/j.nut.2017.10.02...
].

PNI, calculated by albumin and lymphocyte values and a valuable malnutrition parameter, was reported as a possible risk factor for postoperative AF[44 Engin M, Ozsin KK, Savran M, Guvenc O, Yavuz S, Ozyazicioglu AF. Visceral adiposity index and prognostic nutritional index in predicting atrial fibrillation after on-pump coronary artery bypass operations: a prospective study. Braz J Cardiovasc Surg. 2021;36(4):522-9. doi:10.21470/1678-9741-2020-0044.
https://doi.org/10.21470/1678-9741-2020-...
]. There are studies reporting that PNI can also be used as a predictor of prognosis and poor results in patients undergoing CABG[44 Engin M, Ozsin KK, Savran M, Guvenc O, Yavuz S, Ozyazicioglu AF. Visceral adiposity index and prognostic nutritional index in predicting atrial fibrillation after on-pump coronary artery bypass operations: a prospective study. Braz J Cardiovasc Surg. 2021;36(4):522-9. doi:10.21470/1678-9741-2020-0044.
https://doi.org/10.21470/1678-9741-2020-...
,2727 Teker Açıkel ME, Korkut AK. Impact of controlling nutritional status score (CONUT) and prognostic nutritional index (PIN) on patients undergoing coronary artery bypass graft surgery. Heart Surg Forum. 2019;22(4):E294-7. doi:10.1532/hsf.2493.
https://doi.org/10.1532/hsf.2493...
]. In a recent study in the literature, the importance of PNI value in patients undergoing CPB-guided heart surgery was expressed, and it was reported that patients were divided into two groups based on PNI value (< 46.13 and > 46.13; PNI value < 46.13 = high risk) and that early-term undesirable events were higher in the lower PNI group[44 Engin M, Ozsin KK, Savran M, Guvenc O, Yavuz S, Ozyazicioglu AF. Visceral adiposity index and prognostic nutritional index in predicting atrial fibrillation after on-pump coronary artery bypass operations: a prospective study. Braz J Cardiovasc Surg. 2021;36(4):522-9. doi:10.21470/1678-9741-2020-0044.
https://doi.org/10.21470/1678-9741-2020-...
,2828 Lee SI, Ko KP, Choi CH, Park CH, Park KY, Son KH. Does the prognostic nutritional index have a predictive role in the outcomes of adult cardiac surgery? J Thorac Cardiovasc Surg. 2020;160(1):145-53.e3. doi:10.1016/j.jtcvs.2019.08.069.
https://doi.org/10.1016/j.jtcvs.2019.08....
]. PNI was also expressed to be a predictor of early-term mortality[44 Engin M, Ozsin KK, Savran M, Guvenc O, Yavuz S, Ozyazicioglu AF. Visceral adiposity index and prognostic nutritional index in predicting atrial fibrillation after on-pump coronary artery bypass operations: a prospective study. Braz J Cardiovasc Surg. 2021;36(4):522-9. doi:10.21470/1678-9741-2020-0044.
https://doi.org/10.21470/1678-9741-2020-...
]. In light of these results, it was reported that the easily calculable preoperative PNI value is a precious parameter for predicting early-term results in CPB-guided open-heart surgery operations[44 Engin M, Ozsin KK, Savran M, Guvenc O, Yavuz S, Ozyazicioglu AF. Visceral adiposity index and prognostic nutritional index in predicting atrial fibrillation after on-pump coronary artery bypass operations: a prospective study. Braz J Cardiovasc Surg. 2021;36(4):522-9. doi:10.21470/1678-9741-2020-0044.
https://doi.org/10.21470/1678-9741-2020-...
,2828 Lee SI, Ko KP, Choi CH, Park CH, Park KY, Son KH. Does the prognostic nutritional index have a predictive role in the outcomes of adult cardiac surgery? J Thorac Cardiovasc Surg. 2020;160(1):145-53.e3. doi:10.1016/j.jtcvs.2019.08.069.
https://doi.org/10.1016/j.jtcvs.2019.08....
]. In a study, PNI was found to be a predictor of AF development in the postoperative CABG period and it was also reported that old age and chronic obstructive pulmonary disease were also predictors[44 Engin M, Ozsin KK, Savran M, Guvenc O, Yavuz S, Ozyazicioglu AF. Visceral adiposity index and prognostic nutritional index in predicting atrial fibrillation after on-pump coronary artery bypass operations: a prospective study. Braz J Cardiovasc Surg. 2021;36(4):522-9. doi:10.21470/1678-9741-2020-0044.
https://doi.org/10.21470/1678-9741-2020-...
,1717 Erdolu B, As AK, Engin M. The relationship between the HATCH score, neutrophil to lymphocyte ratio and postoperative atrial fibrillation after off-pump coronary artery bypass graft surgery. Heart Surg Forum. 2020;23(1):E088-E092. doi:10.1532/hsf.2771.
https://doi.org/10.1532/hsf.2771...
]. In our study, although the mean preoperative lymphocyte and PNI values were found to be lower in the group that developed postoperative AF compared to the other group, this was not statistically significant (P=0.084, P=0.877, respectively). The only statistically significant parameter in terms of postoperative AF development in both groups was cross-clamping time compared to our study (Group 1: 88.96 ± 16.51 min, Group 0: 81.24 ± 24.5min, P=0.008). In addition, although not statistically significant, lymphocytes and albumin, whose anti-inflammatory effects are known and whose predictive roles in terms of postoperative adverse events have been reported in some publications, and the PNI value in their formulation were lower in the group that developed postoperative AF[44 Engin M, Ozsin KK, Savran M, Guvenc O, Yavuz S, Ozyazicioglu AF. Visceral adiposity index and prognostic nutritional index in predicting atrial fibrillation after on-pump coronary artery bypass operations: a prospective study. Braz J Cardiovasc Surg. 2021;36(4):522-9. doi:10.21470/1678-9741-2020-0044.
https://doi.org/10.21470/1678-9741-2020-...
,99 Hernandez AV, Kaw R, Pasupuleti V, Bina P, Ioannidis JP, Bueno H, et al. Association between obesity and postoperative atrial fibrillation in patients undergoing cardiac operations: a systematic review and meta-analysis. Ann Thorac Surg. 2013;96(3):1104-16. doi:10.1016/j.athoracsur.2013.04.029.
https://doi.org/10.1016/j.athoracsur.201...
]. We investigated the effect of PNI on postoperative adverse events and AF in our study. There was no statistically significant difference between the patient groups in our study in terms of the patients’ weight (P=0.171) and no statistically significant difference between the PNI values (P=0.877). However, although not statistically significant, the mean PNI values of patients in the AF group were lower than those in the no-AF group (50.91 ± 5.29 vs. 52.07 ± 5.55, respectively). In addition, the group of patients with a PNI value < 51.76 ± 5.48, which was the mean PNI value in our study, had a higher rate of newly developed AF compared to the other group (30 ± 0.46% vs. 23 ± 0.42%, respectively).

It has been stated that in the presence of similar risk factors, there are significant differences in the development of new AF in some patients, and the reasons for this are still unknown[1313 Yilmaz Y, Kelesoglu S, Elcik D, Ozmen R, Kalay N. Predictive values of systemic immune-inflammation index in new-onset atrial fibrillation following coronary artery bypass grafting. Braz J Cardiovasc Surg. 2023;38(1):96-103. doi:10.21470/1678-9741-2021-0278.
https://doi.org/10.21470/1678-9741-2021-...
]. It has been reported in several studies a potent and independent relation between an increase in some inflammatory markers and new-onset AF in the postoperative CABG period[1313 Yilmaz Y, Kelesoglu S, Elcik D, Ozmen R, Kalay N. Predictive values of systemic immune-inflammation index in new-onset atrial fibrillation following coronary artery bypass grafting. Braz J Cardiovasc Surg. 2023;38(1):96-103. doi:10.21470/1678-9741-2021-0278.
https://doi.org/10.21470/1678-9741-2021-...
,2929 Gungor H, Babu AS, Zencir C, Akpek M, Selvi M, Erkan MH, et al. Association of preoperative platelet-to-lymphocyte ratio with atrial fibrillation after coronary artery bypass graft surgery. Med Princ Pract. 2017;26(2):164-8. doi:10.1159/000453614.
https://doi.org/10.1159/000453614...
], on the other hand, it has been expressed that there is a lack of data on the relationship between nutritional status and long-term results and important undesirable events in isolated CABG patients[11 Tasbulak O, Guler A, Duran M, Sahin A, Bulut U, Avci Y, et al. Association between nutritional indices and long-term outcomes in patients undergoing isolated coronary artery bypass grafting. Cureus. 2021;13(7):e16567. doi:10.7759/cureus.16567.
https://doi.org/10.7759/cureus.16567...
]. Again, although there are publications stating that they are effective in predicting mortality in CABG patients, it is also stated that there is insufficient data on the relationship between nutritional status and long-term results and important undesirable events in isolated CABG patients[11 Tasbulak O, Guler A, Duran M, Sahin A, Bulut U, Avci Y, et al. Association between nutritional indices and long-term outcomes in patients undergoing isolated coronary artery bypass grafting. Cureus. 2021;13(7):e16567. doi:10.7759/cureus.16567.
https://doi.org/10.7759/cureus.16567...
]. In our study, although the mean preoperative lymphocyte and PNI values were lower in the group with postoperative AF compared to the other group, this was not statistically significant (P=0.084, P=0.877, respectively). In addition, cross-clamping time was longer in patients with new postoperative AF compared to patients without AF (88.96 ± 16.51 min. vs. 81.24 ± 24.5 min., respectively, P=0.008) in our study.

In a study conducted in patients undergoing off-pump CABG, it was reported that patients in the newly developed AF group were older than patients who did not develop AF, and platelet and systemic immune-inflammation index levels were found to be significantly higher in multivariate analysis among white blood cell, platelet, neutrophil, neutrophil/lymphocyte ratio, and systemic immune-inflammation index levels[55 Topal D, Korkmaz UTK, Velioglu Y, Yuksel A, Donmez I, Uçaroğlu ER, et al. Systemic immune-inflammation index as a novel predictor of atrial fibrillation after off-pump coronary artery bypass grafting. Rev Assoc Med Bras (1992). 2022;68(9):1240-6. doi:10.1590/1806-9282.20220295.
https://doi.org/10.1590/1806-9282.202202...
]. In our study, no significant statistically difference was found between the mean ages of the patients in both groups, but the male sex ratio was higher in the newly developed AF group compared to the other group (84 ± 0.37% vs. 74 ± 0.44%, respectively).

Limitations

Our article has limitations as a relatively small sample size, a single center, short follow-up period, and a retrospective design. Another limitation of the study is that some possible risk factors for the development of AF were excluded from the evaluation due to the inaccessibility of the information on these risk factors in the hospital automation system.

CONCLUSION

As a conclusion, although it has been stated in some studies in the literature that there is a relationship between low PNI values and the development of AF after CABG, according to our study results, there was no statistically significant difference between PNI values and the development of AF after CABG, which is similar to some publications in the literature. There are publications in the literature that are compatible or not compatible with our study results and considering that our study was conducted with a relatively low number of patients, we think that it would be beneficial to conduct studies involving more patients focused on this subject.

  • This study was carried out at the Department of Cardiovascular Surgery, Giresun Education and Research Hospital, Giresun, Turkey.
  • No financial support.

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    » https://doi.org/10.1016/j.jtcvs.2019.08.069
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Publication Dates

  • Publication in this collection
    27 May 2024
  • Date of issue
    2024

History

  • Received
    28 Sept 2023
  • Accepted
    31 Dec 2023
Sociedade Brasileira de Cirurgia Cardiovascular Rua Afonso Celso, 1178 Vila Mariana, CEP: 04119-061 - São Paulo/SP Brazil, Tel +55 (11) 3849-0341, Tel +55 (11) 5096-0079 - São Paulo - SP - Brazil
E-mail: bjcvs@sbccv.org.br