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Review

Multiple Arterial Grafting in CABG: Outcomes, Concerns, and Controversies

by
Shahzad G. Raja
Department of Cardiac Surgery, Harefield Hospital, London UB9 6JH, UK
J. Vasc. Dis. 2025, 4(3), 29; https://doi.org/10.3390/jvd4030029
Submission received: 24 March 2025 / Revised: 29 June 2025 / Accepted: 23 July 2025 / Published: 24 July 2025
(This article belongs to the Section Cardiovascular Diseases)
Versions Notes

Abstract

Coronary artery bypass grafting (CABG) has evolved into a cornerstone treatment for coronary artery disease, with graft selection playing a critical role in long-term outcomes. Multiple arterial grafting (MAG) represents a significant advancement over single arterial grafting, utilizing conduits such as the internal thoracic artery and radial artery to enhance graft durability and patient survival. This review examines the outcomes, challenges, and controversies associated with MAG, highlighting its superior patency rates and reduced need for repeat revascularization procedures. While the technique provides long-term survival benefits, concerns such as the complexity of surgical techniques, increased operative time, and higher resource utilization underscore the importance of surgeon expertise and institutional infrastructure. Patient selection remains critical, as factors like age, comorbidities, and gender influence outcomes and highlight disparities in access to MAG. Emerging evidence addresses debates regarding optimal graft choice and balancing long-term benefits against short-term risks. Future directions focus on ongoing clinical trials, innovations in minimally invasive and robotic-assisted CABG, and technological advancements aimed at improving graft patency. Professional guidelines and best practices underscore the need for personalized approaches to optimize MAG’s potential. This article underscores the promise of MAG in redefining CABG care, paving the way for enhanced patient outcomes and broadened applicability. This article highlights the promise of MAG in transforming CABG care, leading to improved patient outcomes and expanded applicability.

1. Introduction

Coronary artery bypass grafting (CABG) has long been regarded as a cornerstone of surgical treatment for coronary artery disease (CAD), a leading cause of morbidity and mortality worldwide [1]. Since its inception in the late 1960s, the procedure has undergone significant advancements, transitioning from its origins using saphenous vein grafts to more sophisticated techniques that prioritize improved patient outcomes and graft longevity [2]. Early adoption of venous grafts marked a critical turning point in the management of CAD, but subsequent challenges, such as vein graft disease and declining patency rates over time, spurred innovation in surgical approaches and conduit selection [2]. The introduction of arterial grafts, particularly the internal mammary artery (IMA), in the 1970s represented a paradigm shift, offering superior durability and long-term patency compared to venous conduits [3]. These advancements have shaped modern CABG and redefined best practices in the field.
Graft selection has emerged as a pivotal factor in determining the success of CABG, with arterial grafts demonstrating remarkable superiority in long-term performance. Studies consistently show that arterial conduits, particularly the IMA, achieve patency rates exceeding 90% at 10 years, significantly outperforming saphenous vein grafts [4]. Such findings have solidified the IMA as the gold standard for grafting, offering reduced rates of graft failure and repeat revascularization, as well as improved survival [3]. However, as the spectrum of CAD patients broadens, particularly among high-risk populations such as those with diabetes, advanced age, or significant comorbidities, the exploration and optimization of additional arterial grafts, such as the radial artery and others, are of paramount importance to further improve outcomes [5].
This manuscript presents a narrative review synthesizing key findings from the existing literature regarding multiple arterial grafting (MAG) versus single arterial grafting (SAG), providing a broad assessment of its advantages, concerns, and controversies. Unlike a systematic review or meta-analysis, which adhere to structured methodologies such as predefined search criteria, inclusion/exclusion parameters, and bias analysis, this review integrates studies on survival, patency, technical challenges, and emerging innovations to offer a comprehensive perspective on MAG. In the context of coronary artery bypass grafting (CABG), it examines key outcomes such as morbidity, complications, long-term survival, and quality of life while comparing MAG with SAG. It further explores patient selection, technical challenges, resource demands, and ongoing debates regarding gender disparities, graft choice, and balancing long-term benefits against short-term risks. Additionally, the review highlights emerging clinical trials, technological advancements, and updated guidelines, providing valuable insights for clinicians and policymakers seeking to improve patient outcomes and refine clinical practices in MAG.

2. Literature Selection Methodology

To provide a structured synthesis of the available literature, this review incorporated a broad literature search from PubMed, Google Scholar, and Cochrane Library databases using terms such as “multiple arterial grafting”, “bilateral internal mammary artery grafting”, “single arterial grafting”, “coronary artery bypass grafting outcomes”, and “arterial conduit patency”. Preference was given to peer-reviewed studies, randomized controlled trials, systematic reviews, and large observational analyses published in the last 15 years. Key studies were selected based on relevance to survival, patency rates, and technical considerations of MAG, with additional emphasis on emerging clinical trials and guidelines influencing practice recommendations. While this review does not follow the strict methodology of a systematic review, it synthesizes findings from leading research to provide a contemporary analysis of MAG outcomes.

3. Outcomes of Multiple Arterial Grafting

3.1. In-Hospital Outcomes

The evidence indicates a disparity in outcomes between observational studies and randomized controlled trials (RCTs). While observational studies suggest superiority of MAG, the majority of randomized controlled trials report similar in-hospital and mid-term outcomes. Table 1 summarizes key RCTs comparing MAG with SAG [6,7,8,9,10,11,12,13,14,15,16,17,18,19,20]. A recently published systematic review and meta-analysis analyzing 18 RCTs involving over 10,000 patients found that MAG was associated with a significantly lower risk of MI compared to SAG. The hazard ratio (HR) for MI in the MAG group was 0.77 (95% confidence intervals [CI] = 0.59–0.99), indicating a 23% reduction in risk [21]. Subgroup analysis revealed that the right internal mammary artery/radial artery (RIMA/RA) MAG group had a significantly lower incidence of MI compared to the SAG group (HR = 0.69, 95% CI = 0.55–0.88, p = 0.002). There was no significant difference in the incidence of stroke between the MAG and SAG groups (HR = 0.83, 95% CI = 0.62–1.11, p = 0.214). A meta-analysis of 29 observational studies involving 89,399 patients revealed notable benefits associated with MAG using bilateral internal mammary arteries (BIMA) grafting compared to SAG [22]. Patients in the BIMA cohort demonstrated significantly reduced rates of hospital mortality (1.2% vs. 2.1%, p = 0.04), cerebrovascular accidents (1.3% vs. 2.9%, p = 0.0003), and revascularization (4.8% vs. 10%, p = 0.005). However, this approach was associated with an increased incidence of deep sternal wound infection (DSWI) (1.8% vs. 1.4%, p = 0.0008).
Schwann et al. [23] analyzed The Society of Thoracic Surgeons (STS) National Database (2004 to 2015) to assess the operative safety of MAG using BIMA-MAG (n = 73,054) and RA-MAG (n = 97,623) compared to SAG (n = 1,334,511). The primary endpoints were operative (30-day or same hospitalization) mortality and deep sternal wound infections (DSWI). Risk-adjusted odds ratios (AOR) and 95% CIs were derived through logistic regression with sensitivity analyses in multiple subcohorts, including MAG use rate. Patient characteristics varied across groups: SAG (73.8% men; median age, 66 years), BIMA-MAG (85.1% men; median age, 59 years), and RA-MAG (82.5% men; median age, 61 years). Observed mortality rates were lower for BIMA-MAG (1.19%, p < 0.001) and RA-MAG (1.19%, p < 0.001) compared with SAG (1.91% mortality; 0.73% DSWI), though DSWI risk was higher for BIMA-MAG (1.08%, p < 0.001) and similar for RA-MAG (0.71%, p = 0.55). BIMA-MAG showed marginally increased mortality (AOR, 1.14; 95% CI, 1.00 to 1.30; p = 0.05) and doubled DSWI risk (AOR, 2.09; 95% CI, 1.80 to 2.43; p < 0.001), while RA-MAG demonstrated comparable mortality (AOR, 1.01; 95% CI, 0.89 to 1.15; p = 0.85) and DSWI (AOR, 0.97; 95% CI, 0.83 to 1.13; p = 0.70). Results were consistent across subcohorts, with a U-shaped mortality vs. BIMA use relation indicating worse mortality at hospitals with low (<5%: AOR, 1.38; 95% CI, 1.18 to 1.61; p < 0.001) and high (≥40%: AOR, 1.31; 95% CI, 1.00 to 1.70; p = 0.049) BIMA use rates. This study revealed that MAG in the United States is associated with mortality comparable to SAG and increased DSWI risk with BIMA-MAG, underscoring the importance of surgeon experience, institutional expertise, and patient selection in optimizing outcomes. Interestingly, a recently published meta-analysis did not demonstrate any statistically significant difference in the incidence of DSWI following MAG and SAG [21].

3.2. Long-Term Survival

Despite contradictory findings from RCTs regarding long-term survival with MAG and SAG strategies [24,25,26,27] (Table 2), the meta-analysis by Magouliotis et al. [28] provides compelling evidence supporting the superiority of MAG in terms of overall survival. By pooling reconstructed time-to-event data for 180,459 patients across forty-three articles and generating pooled Kaplan–Meier curves, it adds significant value to the existing literature.
The analysis demonstrates that MAG is associated with enhanced long-term survival compared to SAG, findings that are further corroborated through sensitivity and subgroup analyses. Unlike a previous meta-analysis conducted in 2019 [29], this study overcomes key methodological limitations by incorporating critical subgroup analyses (e.g., gender, diabetes) and patient-level data extraction, offering a more comprehensive evaluation. While the conundrum persists given the inconsistent evidence from large RCTs on long-term survival, a recently published meta-analysis of RCTs [21] validates that MAG improves survival compared to SAG, with the survival benefit becoming increasingly pronounced as the duration of follow-up extends.

3.3. Patency Rate and Repeat Revascularization

Graft patency and the need for repeat revascularization are critical outcomes in CABG, and RCTs have provided valuable insights into these aspects (Table 1). Studies by Muneretto et al. [9,10] highlight the superior patency rates in the MAG group, accompanied by reduced late cardiac events. Collins et al. similarly reported significantly better graft patency in patients receiving MAG compared to SAG [11]. Furthermore, Taggart and associates demonstrated a significant reduction in the composite of death, myocardial infarction, stroke, and repeat revascularization with MAG, reflecting the long-term benefits of higher patency rates [30].
On the other hand, some studies, including Buxton et al. [8], Damgaard et al. [13], and Goldman et al. [14], reported similar angiographic graft patency rates between MAG and SAG, particularly in the short to medium term (e.g., 1 to 5 years post-surgery). However, it is important to note that the longer follow-up durations in studies like Thuijs et al. [18] and Buxton et al. [25] provided evidence of better long-term outcomes for MAG, emphasizing the importance of extended observation periods.
While the majority of these studies favor MAG in terms of patency rates, there are variances in outcomes based on patient characteristics, follow-up intervals, and the arterial conduits used (e.g., radial artery or internal mammary artery). Collectively, the data underscore MAG’s potential to deliver superior patency rates over time, contributing to improved survival and reduced need for repeat revascularization in patients undergoing CABG.

3.4. Quality of Life

Many studies have shown a positive impact of CABG on quality of life (QoL) in short-, mid- or long-term follow-up [31,32,33,34]. A 10-year follow-up study assessed QoL in 300 patients with multivessel CAD who underwent MAG using BIMA or single internal mammary artery (SIMA) grafting between January 2005 and October 2010 [35]. The mean follow-up duration was 3568 ± 409 days, and QoL was evaluated subjectively via a Likert scale and objectively using the WHOQOL-BREF questionnaire, with patients interviewed by telephone. Results showed that BIMA patients more frequently reported marked improvement in QoL compared to SIMA patients (58% vs. 43.3%, p = 0.02), while marked deterioration was less common among BIMA patients (2% vs. 3.3%, p = 0.03). The WHOQOL-BREF questionnaire also revealed significantly better overall QoL scores in the BIMA group (median: 15.0) compared to the SIMA group (median: 14.75, p = 0.02). Additionally, BIMA patients had a higher proportion of angina-free outcomes (84%) compared to SIMA patients (72.7%, p = 0.006). QoL was not found to correlate with body mass index (p = 0.10) or residence status (p = 0.51), but there was a weak negative correlation between QoL and age (r = −0.14, p = 0.01). These findings underscore the potential advantages of MAG in enhancing long-term QoL.
The ROMA:QOL trial, a sub-study of the larger ROMA trial, is currently underway and stands as a key investigation into this topic [36]. Its objective is to evaluate the impact of MAG versus SAG on patient-reported outcomes, including physical and mental health, using established tools like the Seattle Angina Questionnaire, Short Form-12v2, and EuroQol-5D (EQ-5D)-5L. Once completed, the trial’s findings are expected to shed light on how MAG influences quality of life (QoL) compared to SAG, potentially confirming the advantages suggested by observational data, such as enhanced long-term survival and symptom relief.

4. Concerns Associated with Multiple Arterial Grafting

4.1. Patient Selection and Risk Stratification

Patient selection is a critical factor in determining the success of MAG. Studies have shown that MAG is most beneficial for patients with a longer life expectancy, as the long-term patency of arterial grafts provides significant survival advantages. For instance, a 2021 analysis of the ART highlighted that younger patients with fewer comorbidities derive the greatest benefit from MAG [37]. Conversely, patients with limited life expectancy due to advanced age or severe comorbidities may not experience the long-term advantages of arterial grafts, as their survival may not extend to the period when the benefits of superior graft patency become evident [38].
Comorbidities such as diabetes mellitus, chronic obstructive pulmonary disease, and reduced left ventricular ejection fraction significantly influence outcomes in MAG. A 2022 study by Taggart et al. demonstrated that patients with diabetes benefit from MAG due to the reduced risk of saphenous vein graft failure [39]. However, older patients and those with severe comorbidities may face higher risks of complications, such as DSWI, particularly with BIMA grafting. Gender differences have also been noted, with women potentially experiencing higher complication rates due to smaller vessel size and increased susceptibility to infections [40].
A recently published study by Sabik et al. provides further insights into patient selection [41]. The study utilized data from The Society of Thoracic Surgeons Adult Cardiac Surgery Database, linking over one million patients undergoing isolated CABG between 2008 and 2019 to the National Death Index to assess long-term survival outcomes. Among the cohort, 100,419 patients (9.83%) received MAG, while 920,943 patients (90.17%) underwent SAG using saphenous vein grafts. After rigorous risk adjustment, MAG was associated with a significant survival advantage at 10 years, with improved hazard ratios across subgroups, including patients with stable coronary disease, acute coronary syndrome, and acute infarction. However, for patients aged 80 years and older or those with severe comorbidities such as heart failure, renal failure, peripheral vascular disease, or obesity, survival outcomes with MAG were comparable to SAG. Notably, patients with a body mass index ≥40 kg/m2 exhibited superior survival with SAG. Additionally, the study highlighted the impact of procedural volume, demonstrating that centers performing at least 10 MAG cases annually achieved optimal survival benefits [41]. These findings reinforce MAG as the preferred strategy for multivessel CABG, with tailored surgical decision-making required for older and high-risk patient populations.

4.2. Technical Challenges and Surgical Expertise

The surgical techniques required for MAG are more intricate and demanding compared to those used in SAG. Employing multiple arterial conduits, such as the RIMA or RA, demands careful surgical planning and execution to ensure optimal graft function and minimize complications like competitive flow or graft spasm. This level of complexity has contributed to a slower adoption of MAG, as less experienced surgeons may face challenges during the learning curve. The success of MAG often relies on specialized training and institutional expertise to overcome technical barriers and deliver consistent, favorable outcomes [37].
Patient selection for MAG is vital, but the expertise of the surgeon and the experience of the center are equally critical. An analysis using the Society of Thoracic Surgeons National Database found that operative mortality for BIMA grafting was notably higher in low-volume centers (where BIMA usage was under 5%) compared to SIMA grafting. However, this difference was not observed in high-experience centers, where BIMA utilization ranged between 20% and 40% [23]. Additionally, a meta-analysis of 34 studies, comprising 27,894 patients, showed an inverse relationship between center volume and long-term mortality (p = 0.02). Higher survival rates were reported in centers with greater BIMA experience [39]. This underscores the need for specialized training and institutional support to expand the use of MAG.
Technical precision is essential, as errors in conduit preparation, anastomotic technique, or flow dynamics can significantly influence long-term graft patency. Arterial grafts demand meticulous handling due to their distinct anatomical and physiological characteristics. Unlike venous conduits, arterial grafts are more susceptible to vasospasm, competitive flow dynamics, and endothelial injury, requiring precise surgical techniques to ensure long-term functionality. Optimal arterial graft performance begins with careful harvesting and preservation. Arterial grafts require preservation of the vascular integrity and avoidance of excessive handling that could compromise the endothelial function. The RA, in particular, necessitates adequate pharmacological preparation to mitigate spasm and promote vasodilation [42]. Failure to adequately precondition the RA can lead to early graft dysfunction due to arterial hyperreactivity. Precision in anastomotic construction is paramount for ensuring optimal flow and minimizing turbulence. Even minor operative lapses—such as conduit redundancy, inappropriate length adjustment, or anastomotic misalignment—may result in flow disturbance and early graft failure. The IMA, for instance, requires careful length adjustment and appropriate sequential or composite grafting strategies to avoid excessive length-related redundancy or kinking. Similarly, RA anastomosis must ensure laminar flow dynamics, particularly when used as a Y-graft or sequential conduit, to minimize competitive flow and distal turbulence. These refinements emphasize that intraoperative imprecision disproportionately affects arterial grafts, making surgical accuracy imperative in achieving durable outcomes in multiple arterial grafting.
Competitive flow presents a unique challenge in MAG where multiple arterial conduits supply the same vascular territory. Patency rates are closely linked to native coronary flow—with the success of arterial grafting dependent on matching graft inflow with downstream coronary demand. In cases where the IMA or RA supplies a well-preserved native coronary artery, competitive flow may reduce graft utility, necessitating flow measurement strategies and careful conduit selection [42]. Intraoperative transit-time flow measurement can provide real-time assessment of graft performance, ensuring adequate flow characteristics before completion of surgery.

4.3. Operative Time and Resource Utilization

Longer operative times are often observed when employing MAG instead of SAG, largely due to the additional steps involved in harvesting and preparing multiple arterial conduits. It is reported that the operative time for MAG was approximately 30–45 min longer than for SAG [43]. While this increase in operative time may be acceptable in low-risk patients, it could pose challenges in high-risk populations or resource-constrained settings.
The resource utilization and cost-effectiveness of MAG have been subjects of debate. While the initial costs of MAG are higher due to longer operative times and the need for specialized equipment, the long-term benefits, such as reduced need for repeat revascularization and lower rates of cardiac events, may offset these costs. Using data from the Arterial Revascularization Trial (ART), the long-term cost-effectiveness of MAG with BIMA versus SAG with SIMA was evaluated from the perspective of the English healthcare system [44]. Over a 10-year follow-up period, resource utilization, healthcare costs, and quality-adjusted life years (QALYs) were analyzed. Multiple imputation techniques were employed to address missing data, and incremental cost-effectiveness ratios were calculated using non-parametric bootstrapping, with results extrapolated beyond 10 years using Gompertz survival functions and linear models for total cost and utility.
The analysis revealed that total mean costs over 10 years were higher for BIMA grafting (£17,594) compared to SIMA grafting (£16,462), with a mean difference of £1133 (95% CI £239 to £2026, p = 0.015). However, the total mean QALYs at 10 years were comparable between the two groups—6.54 in the BIMA arm and 6.57 in the SIMA arm, with an adjusted mean difference of −0.01 (95% CI −0.2 to 0.1, p = 0.883). At the 10-year mark, BIMA grafting demonstrated a 33% probability of being cost-effective compared to SIMA grafting, assuming a cost-effectiveness threshold of £20,000. When extrapolated to a lifetime horizon, this probability increased to 51%.
This study suggests that while BIMA grafting incurs higher upfront costs, its cost-effectiveness potential may improve over a lifetime perspective, suggesting possible long-term economic advantages.

5. Controversies Surrounding Multiple Arterial Grafting

5.1. Gender Disparities and Outcomes

Gender disparities in outcomes following MAG have been a topic of significant concern. A review of the STS Adult Cardiac Surgery Database examined outcomes for 1,212,487 male and female patients who underwent first-time isolated CABG between 1 July 2011, and 28 June 2019. Findings indicated that female patients were typically older and presented with more comorbidities, such as congestive heart failure and cardiogenic shock. After adjusting for these baseline differences, women were found to have lower odds of receiving MAG. Additionally, women had a significantly higher rate of incomplete revascularization compared to men in this cohort [45].
Similarly, a retrospective analysis at the Cleveland Clinic reviewed 57,943 adult CABG patients treated from January 1972 to January 2011, where only 11,009 (19%) were female [46]. Comparable to other studies, women undergoing CABG were older and exhibited more severe symptoms. These patients frequently had additional comorbidities, such as diabetes mellitus, hypertension, peripheral arterial disease, and cerebrovascular disease. Women were less likely to receive arterial grafts, such as BIMA or RA grafts, and had increased reliance on saphenous vein grafts (SVGs), including all-venous grafting strategies. Despite adjustments for baseline differences and revascularization techniques, female sex remained an independent risk factor for early and late mortality following CABG. Survival rates were significantly lower for women receiving SVGs only compared to those receiving BIMA grafting, with 5-, 10-, and 20-year survival rates of 80%, 58%, and 25% for SVGs and 90%, 77%, and 48% for BIMA grafting, respectively. This analysis further emphasized the disparities in MAG utilization between male and female patients and the impact on survival outcomes.
A retrospective analysis of the Ottawa Heart Institute CABG database reviewed 19,557 patients undergoing isolated CABG with more than one distal anastomosis from January 1990 to March 2015 [47]. Less than a quarter of the cohort consisted of female patients, mirroring trends in previous studies. The unmatched cohort revealed that men were significantly more likely to receive BIMA conduits and use multiple arterial conduits in their revascularization strategies. Women, on the other hand, were more likely to undergo CABG without any arterial conduits. Propensity-score matching further reinforced these trends, showing that men had greater use of three arteries for revascularization compared to women. Despite a general trend toward increased MAG utilization among both genders over time, women remained significantly underrepresented in total arterial grafting strategies.
Lastly, data from the Australian and New Zealand Society of Cardiac and Thoracic Surgeons database analyzed 54,275 primary isolated CABG cases from June 2001 to January 2020, where only 20% of patients (10,693) were female [48]. Female patients were generally older, had a higher burden of comorbidities, and presented with more severe cardiovascular symptoms, as quantified by higher New York Heart Association and Canadian Cardiovascular Society classifications. While women were historically less likely to receive MAG, this study suggests that appropriately selected female patients derive survival benefits comparable to those observed in male patients. It demonstrated a significant survival advantage for women undergoing MAG (adjusted hazard ratio 0.83, 95% confidence interval 0.76–0.91, p < 0.001) at a median follow-up of 5.2 years, with no significant interaction effect based on sex (p = 0.08). These findings challenge previous assumptions of inferior outcomes in women and highlight the importance of equitable access to MAG for both sexes.
Despite this demonstrated survival benefit, disparities in access to MAG persist. Anatomical differences, such as smaller vessel luminal diameters—even after adjustment for body surface area—may pose technical challenges to performing MAG in female patients, potentially influencing surgeon preferences and procedural decisions. Furthermore, women continue to face delayed diagnoses and more diffuse coronary artery disease, which can complicate grafting procedures and affect revascularization success [43,44,45,46]. Additionally, women are less likely to receive complete anatomic revascularization further impacting their long-term outcomes [49]. Importantly, studies that previously reported worse outcomes for women undergoing CABG did not always account for age-matched comparisons, which are critical in assessing the true benefits of MAG across different patient cohorts. Age-adjusted analyses consistently indicate that MAG provides superior long-term outcomes compared to SAG in appropriately selected patients, regardless of chronological age. These disparities along with underrepresentation of women in clinical trials and studies evaluating MAG are critical issues that highlight the importance of addressing gender-specific challenges in CABG and ensuring equitable representation of women in future research to optimize outcomes for all patients.

5.2. Debate on Optimal Graft Choice and Configurations

The choice of the second arterial graft in CABG remains a topic of ongoing debate, with RA and RIMA being the most commonly considered options. Each conduit has its own advantages and limitations, and the decision often depends on patient-specific factors, surgeon expertise, and institutional preferences [50].
The RA has gained popularity as a second arterial graft due to its favorable long-term patency rates and ease of harvesting. Studies have shown that the radial artery performs well when grafted to coronary targets with high-grade stenosis, as it is more sensitive to competitive flow compared to the RIMA. A network meta-analysis demonstrated that the RA had superior angiographic outcomes compared to SVGs and comparable patency rates to the RIMA. However, the RA is prone to vasospasm, which necessitates careful intraoperative handling and the use of vasodilators to optimize outcomes [51].
On the other hand, the RIMA is often favored for its anatomical compatibility and excellent long-term patency when used as a graft to the LAD or other coronary targets. Despite these advantages, concerns about increased operative complexity and the risk of sternal wound complications, particularly in diabetic or obese patients, have limited its widespread adoption. A meta-analysis of 8 propensity score matched studies suggests that the use of RIMA compared with RA was associated with superior long-term survival and freedom from repeat revascularization, with similar operative mortality and incidence of sternal wound complications when the skeletonized harvesting technique was used [52].
The choice of graft configuration also plays a critical role in determining outcomes. Total arterial revascularization, which involves the use of multiple arterial grafts such as the LIMA, RIMA, and RA, has been associated with improved long-term survival and reduced need for repeat revascularization [53]. Configurations such as the “T” or “Y” graft technique, where the RIMA or RA is anastomosed to the LIMA, have been explored to maximize the use of arterial conduits while minimizing the need for vein grafts. These techniques allow for complete arterial revascularization without increasing the number of proximal anastomoses, thereby reducing the risk of graft failure. However, the complexity of these configurations requires a high level of surgical expertise and may not be suitable for all patients [54,55].

5.3. Long-Term Benefits Versus Short-Term Risks

This approach has the potential to significantly enhance long-term patient outcomes, although it also presents certain short-term surgical risks that require careful consideration. The outcomes of MAG are shaped by various patient-specific factors that influence the suitability and success of this surgical approach. Age and overall health are significant considerations, as older patients or those with multiple comorbidities face increased perioperative risks that may diminish the potential long-term benefits of MAG. Diabetes status further complicates decision-making, as diabetic patients are more prone to sternal wound infections when undergoing BIMA grafting. In such cases, techniques like graft skeletonization have been explored to reduce the likelihood of infection albeit with a higher rate of graft failure [56].
The expertise of the surgical team and the resources available at the hospital are crucial in determining the success of MAG. Evidence indicates that outcomes are significantly better in high-volume centers where surgeons are experienced in performing complex procedures, as opposed to low-volume centers [37]. This highlights the importance of surgical skill and institutional infrastructure in optimizing patient results.
Another critical factor in evaluating the appropriateness of MAG is the patient’s life expectancy. The durability of arterial grafts makes them particularly advantageous for younger patients and those with longer anticipated lifespans, as these individuals are more likely to reap the long-term benefits of the procedure [27]. For patients with shorter life expectancies, the short-term surgical risks may outweigh the advantages, necessitating a more individualized approach to treatment planning.

5.4. Differentiating MAG from TAG and Its Impact on Outcomes

It is essential to distinguish between MAG and total arterial grafting (TAG), as these terms are sometimes conflated in the literature. MAG refers to the utilization of more than one arterial conduit, which may include a combination of arterial and vein grafts, whereas TAG exclusively involves arterial conduits without any vein grafts. Many studies evaluating MAG do not differentiate these approaches, making direct comparisons complex. For instance, in some trials, including ART [20] and RAPCO [25], patients may have received total arterial revascularization, whereas others may have received a combination of arterial and venous conduits, influencing reported outcomes.
This distinction is particularly significant when assessing survival benefits, graft patency, and postoperative complications. TAG, by eliminating vein grafts, may yield improved long-term patency rates, given the well-documented inferior durability of saphenous vein grafts compared to arterial conduits. However, the omission of vein grafts can also impact short-term surgical success, as arterial conduits may be more susceptible to competitive flow issues and vasospasm, especially when used for less critically stenosed coronary targets. Studies that do not explicitly separate MAG and TAG may overestimate the benefits of MAG if a subset of patients in these trials received exclusively arterial grafting. Similarly, differences in postoperative recovery, graft-related complications, and reintervention rates may be driven by whether vein grafts were included rather than by the number of arterial conduits used. Recognizing this variability is crucial in interpreting trial data, as failing to differentiate MAG from TAG can lead to skewed conclusions regarding long-term benefits and limitations of arterial grafting strategies in CABG.

5.5. Age Cut-Off for the Loss of Benefit from MAG

Traditional perspectives have emphasized age as a critical factor in determining the benefit of MAG in CABG. While arterial grafts, particularly BIMA grafts, have been consistently associated with improved long-term survival, establishing a precise age threshold for their optimal application remains complex. The extent of this survival advantage appears to diminish beyond certain age thresholds, as suggested by earlier studies. Several investigations [57,58,59,60] have examined the age-related survival benefit of MAG using BIMA grafts, identifying points where its effectiveness declines or becomes statistically insignificant. These studies indicated that the advantages of MAG may taper off with advancing age, reinforcing the need for nuanced patient selection and individualized surgical strategies.
Mohammadi et al. [57] demonstrated that the survival advantage of BIMA use is maintained up to 60 years of age, but beyond this threshold, the benefit gradually declines. The study emphasized that, although BIMA grafting provides superior cardiac-specific survival compared to single IMA grafting in younger patients, its additional impact diminishes over time. Benedetto et al. [58] further refined this understanding by identifying 69 years as a critical age threshold beyond which BIMA no longer provides significant survival advantages. Their findings showed that while BIMA use significantly reduced mortality risk in patients aged 69 years and younger, the adjusted hazard ratio for older patients indicated no meaningful benefit. Kieser et al. [59] corroborated these observations, suggesting that BIMA grafting remains a reasonable revascularization strategy in patients up to the age of 70 but that its advantage beyond this point remains unclear.
Sergeant et al. [60] also reported that patients entering their seventh decade of life do not experience a significant survival benefit from MAG with BIMA grafts, reinforcing the importance of individualized risk assessment. Procedural challenges, including increased operative time, heightened risk of sternal wound complications, and susceptibility to infections, become more relevant in elderly patients. These concerns are particularly significant in those with diabetes, obesity, or chronic pulmonary disease, as the potential for postoperative complications increases.
On the contrary, a recently published study by Ren et al. [61] challenges the notion that MAG does not provide a survival advantage beyond 70 years. This large-scale registry analysis demonstrates that MAG remains associated with significant long-term mortality reduction in both younger and elderly patient cohorts, challenging traditional perspectives that suggest diminishing benefits with advancing age. The study reports a hazard ratio of 0.84 (95% CI, 0.79–0.88; p < 0.001) in patients aged 70 and above, indicating a clear survival advantage when compared to SAG. Importantly, the survival curves for both age groups reveal a sustained and incremental divergence favoring MAG, reinforcing the durability of MAG benefits well beyond conventional age thresholds. These findings contradict prior assertions that MAG’s effectiveness declines markedly in older populations and emphasize the need to reevaluate age-based limitations in surgical revascularization strategies.
Based on these contradictory findings, the interpretation of an absolute age cut-off requires caution. The decline in benefit beyond 60 or 69 years does not imply the complete cessation of MAG in older patients but rather underscores the need for careful patient selection and risk stratification. Comorbidities, frailty, and anatomical considerations must be weighed alongside expected survival benefits to determine the most appropriate surgical approach. Alternative strategies, such as using composite Y-grafts or radial artery conduits, may provide a more tailored solution for elderly patients while mitigating the potential risks associated with BIMA harvesting.
While MAG offers superior long-term outcomes in well-selected patients, the diminishing benefit beyond certain age thresholds necessitates a more nuanced approach to its application. The surgical decision should be guided by individualized assessments rather than rigid cut-offs, ensuring that the best possible revascularization strategy is chosen for each patient based on their overall risk profile, life expectancy, and likelihood of deriving meaningful benefit from the procedure. As arterial grafting techniques evolve and long-term data continue to emerge, further research will be essential in refining age-based recommendations to optimize outcomes for CABG patients across different age groups.

6. Future Directions and Research

6.1. Ongoing Clinical Trials and Studies

Recent years have seen a surge in clinical trials and studies aimed at evaluating the efficacy and safety of MAG in CABG. A study presented at the STS 2025 Annual Meeting analyzed over a million CABG cases and highlighted the potential survival benefits of MAG compared to SAG. This research also explored the role of surgeon preference as a variable influencing outcomes, providing new insights into the long-term survival benefits of MAG [62]. Additionally, the ART remains a cornerstone in understanding MAG, despite its limitations in interpreting the broader applicability of MAG due to variations in conduit use [20].
Emerging studies such as ROMA [63] and ROMA:Women [64] are focusing on refining patient selection criteria and optimizing surgical techniques to mitigate risks associated with MAG. These findings are expected to influence clinical guidelines and expand the adoption of MAG in diverse patient populations.

6.2. Innovations in Surgical Techniques and Technology

Advancements in surgical techniques and technology are revolutionizing the practice of MAG. Minimally invasive and robotic-assisted CABG are gaining traction as they reduce surgical trauma and improve recovery times. Techniques such as anaortic, off-pump CABG using multiple arterial grafts have shown promise in minimizing neurological complications and enhancing graft patency [65,66]. These innovations are particularly beneficial for high-risk patients, offering a safer alternative to traditional methods.
Emerging technologies, including intraoperative imaging and graft flow measurement tools, are enhancing the precision of arterial graft placement. These tools not only improve immediate surgical outcomes but also contribute to the long-term success of MAG by ensuring optimal graft functionality [67]. Table 3 summarizes prospective studies and randomized trials that have utilized transit-time flow measurement (TTFM) to identify graft abnormalities or prompt intraoperative revisions [68,69,70,71,72,73,74,75,76,77]. This evidence base underscores the clinical value of TTFM in enhancing graft assessment and refining real-time surgical decision-making during MAG.

6.3. Recommendations for Clinical Practice

Professional societies and expert panels have been instrumental in shaping guidelines for the use of MAG in CABG. The European Society of Cardiology and the European Association for Cardio-Thoracic Surgery have issued consensus statements emphasizing the importance of individualized patient assessments and multidisciplinary care approaches. These guidelines advocate for the use of MAG in patients with longer life expectancies and fewer comorbidities, where the long-term benefits outweigh the short-term risks (Class IIa, Level B) [78].
Best practices for patient selection and surgical approach include thorough preoperative evaluations to identify suitable candidates for MAG. Factors such as age, comorbidities, and anatomical considerations are critical in determining the appropriateness of this technique. High-volume centers with experienced surgical teams are recommended for performing MAG to ensure optimal outcomes.
Determining an appropriate age threshold for the application of MAG in CABG remains a subject of ongoing debate. While previous recommendations often suggested a decline in benefit beyond a certain age, recent evidence indicates that MAG continues to provide survival advantages in older patients. Current best practices suggest that age 70 may serve as a practical reference point for individualized decision-making, ensuring that patient selection accounts for factors such as underlying health conditions, functional status, and anatomical considerations. Instead of a rigid age-based restriction, the surgical strategy should be tailored to balance long-term benefits with potential procedural risks.
Further research is warranted to refine age-related recommendations and bridge the gap between guideline-directed care and real-world practice. As the aging population expands, ensuring optimal revascularization strategies tailored to individual patient profiles remains a priority in modern coronary surgery.

7. Conclusions

The strategy of MAG offers significant long-term survival benefits, particularly in terms of improved graft patency and reduced need for reintervention, although it carries short-term surgical risks that demand careful consideration. Concerns such as operative complexity, complications in patients with elevated risk profile, and variations in surgeon expertise highlight ongoing controversies that necessitate further refinement of approaches. For clinical practice, the importance of personalized patient assessments and adherence to guidelines from professional societies cannot be overstated, as these are crucial for optimizing outcomes and reducing complications. Looking ahead, advancements in surgical techniques, robotic-assisted CABG, and innovative technologies promise to expand the scope and applicability of MAG, paving the way for more effective and less invasive treatments that will redefine patient care in CABG.

Funding

This research received no external funding.

Conflicts of Interest

The author declares no conflicts of interest.

References

  1. Grondin, C.M.; Thornton, J.C. Coronary artery bypass grafting with the saphenous vein. Circulation 1989, 79, 24–29. [Google Scholar]
  2. Garrett, H.E.; Dennis, E.W.; DeBakey, M.E. Aorto-coronary bypass with saphenous vein: A 7-year angiographic follow-up. JAMA 1973, 223, 792–796. [Google Scholar] [CrossRef]
  3. Buxton, B.F.; Galvin, S.D. The history of arterial revascularization: From Kolesov to Tector and beyond. Ann. Cardiothorac. Surg. 2013, 2, 519–526. [Google Scholar]
  4. Ramsingh, R.; Bakaeen, F.G. Coronary artery bypass grafting: Practice trends and projections. Clevel. Clin. J. Med. 2025, 92, 181–191. [Google Scholar] [CrossRef] [PubMed]
  5. Singh, S.K.; Desai, N.D.; Petroff, S.D.; Deb, S.; Cohen, E.A.; Radhakrishnan, S.; Schwartz, L.; Dubbin, J.; Fremes, S.E.; Radial Artery Patency Study Investigators. The impact of diabetic status on coronary artery bypass graft patency: Insights from the radial artery patency study. Circulation 2008, 118 (Suppl. S14), S222–S225. [Google Scholar] [CrossRef] [PubMed]
  6. Morris, J.J.; Smith, L.R.; Glower, D.D.; Muhlbaier, L.H.; Reves, J.G.; Wechsler, A.S.; Rankin, J.S. Clinical evaluation of single versus multiple mammary artery bypass. Circulation 1990, 82 (Suppl. S5), IV214–IV223. [Google Scholar]
  7. Myers, W.O.; Berg, R.; Ray, J.F.; Douglas-Jones, J.W.; Maki, H.S.; Ulmer, R.H.; Chaitman, B.R.; Reinhart, R.A. All-artery multigraft coronary artery bypass grafting with only internal thoracic arteries possible and safe: A randomized trial. Surgery 2000, 128, 650–659. [Google Scholar] [CrossRef]
  8. Buxton, B.F.; Raman, J.S.; Ruengsakulrach, P.; Gordon, I.; Rosalion, A.; Bellomo, R.; Horrigan, M.; Hare, D.L. Radial artery patency and clinical outcomes: Five-year interim results of a randomized trial. J. Thorac. Cardiovasc. Surg. 2003, 125, 1363–1371. [Google Scholar] [CrossRef]
  9. Muneretto, C.; Negri, A.; Manfredi, J.; Terrini, A.; Rodella, G.; Elqarra, S.; Bisleri, G. Safety and usefulness of composite grafts for total arterial myocardial revascularization: A prospective randomized evaluation. J. Thorac. Cardiovasc. Surg. 2003, 125, 826–835. [Google Scholar] [CrossRef]
  10. Muneretto, C.; Bisleri, G.; Negri, A.; Manfredi, J.; Carone, E.; Morgan, J.A.; Metra, M.; Dei Cas, L. Left internal thoracic artery-radial artery composite grafts as the technique of choice for myocardial revascularization in elderly patients: A prospective randomized evaluation. J. Thorac. Cardiovasc. Surg. 2004, 127, 179–184. [Google Scholar] [CrossRef]
  11. Collins, P.; Webb, C.M.; Chong, C.F.; Moat, N.E.; Radial Artery Versus Saphenous Vein Patency (RSVP) Trial Investigators. Radial artery versus saphenous vein patency randomized trial: Five-year angiographic follow-up. Circulation 2008, 117, 2859–2864. [Google Scholar] [CrossRef]
  12. Nasso, G.; Coppola, R.; Bonifazi, R.; Piancone, F.; Bozzetti, G.; Speziale, G. Arterial revascularization in primary coronary artery bypass grafting: Direct comparison of 4 strategies—Results of the Stand-in-Y Mammary Study. J. Thorac. Cardiovasc. Surg. 2009, 137, 1093–1100. [Google Scholar] [CrossRef]
  13. Damgaard, S.; Wetterslev, J.; Lund, J.T.; Lilleør, N.B.; Perko, M.J.; Kelbaek, H.; Madsen, J.K.; Steinbrüchel, D.A. One-year results of total arterial revascularization vs. conventional coronary surgery: CARRPO trial. Eur. Heart J. 2009, 30, 1005–1011. [Google Scholar] [CrossRef]
  14. Goldman, S.; Sethi, G.K.; Holman, W.; Thai, H.; McFalls, E.; Ward, H.B.; Kelly, R.F.; Rhenman, B.; Tobler, G.H.; Bakaeen, F.G.; et al. Radial artery grafts vs. saphenous vein grafts in coronary artery bypass surgery: A randomized trial. JAMA 2011, 305, 167–174. [Google Scholar] [CrossRef] [PubMed]
  15. Song, S.W.; Sul, S.Y.; Lee, H.J.; Yoo, K.J. Comparison of the radial artery and saphenous vein as composite grafts in off-pump coronary artery bypass grafting in elderly patients: A randomized controlled trial. Korean Circ. J. 2012, 42, 107–112. [Google Scholar] [CrossRef] [PubMed]
  16. Le, J.; Baskett, R.J.; Buth, K.J.; Hirsch, G.M.; Brydie, A.; Gayner, R.; Legare, J.F. A pilot randomized controlled trial comparing CABG surgery performed with total arterial grafts or without. J. Cardiothorac. Surg. 2015, 10, 1. [Google Scholar] [CrossRef] [PubMed]
  17. Kim, M.S.; Hwang, H.Y.; Kim, J.S.; Oh, S.J.; Jang, M.J.; Kim, K.B. Saphenous vein versus right internal thoracic artery as a Y-composite graft: Five-year angiographic and clinical results of a randomized trial. J. Thorac. Cardiovasc. Surg. 2018, 156, 1424–1433.e1. [Google Scholar] [CrossRef]
  18. Thuijs, D.J.F.M.; Head, S.J.; Stone, G.W.; Puskas, J.D.; Taggart, D.P.; Serruys, P.W.; Dressler, O.; Crowley, A.; Brown, W.M.; Horkay, F.; et al. Outcomes following surgical revascularization with single versus bilateral internal thoracic arterial grafts in patients with left main coronary artery disease undergoing coronary artery bypass grafting: Insights from the EXCEL trial. Eur. J. Cardiothorac. Surg. 2019, 55, 501–510. [Google Scholar] [CrossRef]
  19. Fomenko, M.S.; Schneider, Y.A.; Tsoi, V.G.; Pavlov, A.A.; Shilenko, P.A. Left or bilateral internal mammary artery employment in coronary artery bypass grafting: Midterm results. Asian Cardiovasc. Thorac. Ann. 2021, 29, 758–762. [Google Scholar] [CrossRef]
  20. Taggart, D.P.; Altman, D.G.; Gray, A.M.; Lees, B.; Nugara, F.; Yu, L.M.; Campbell, H.; Flather, M.; ART Investigators. Randomized trial to compare bilateral vs. single internal mammary coronary artery bypass grafting: 1-year results of the Arterial Revascularisation Trial (ART). Eur. Heart J. 2010, 31, 2470–2481. [Google Scholar] [CrossRef]
  21. Ding, Q.; Zhu, Q.; Lu, L.; Cheng, X.; Ge, M. Comparison of multiple arterial grafts vs. single arterial graft in coronary artery bypass surgery: A systematic review and meta-analysis. Front. Cardiovasc. Med. 2025, 12, 1552807. [Google Scholar] [CrossRef] [PubMed]
  22. Buttar, S.N.; Yan, T.D.; Taggart, D.P.; Tian, D.H. Long-term and short-term outcomes of using bilateral internal mammary artery grafting versus left internal mammary artery grafting: A meta-analysis. Heart 2017, 103, 1419–1426. [Google Scholar] [CrossRef] [PubMed]
  23. Schwann, T.A.; Habib, R.H.; Wallace, A.; Shahian, D.M.; O’Brien, S.; Jacobs, J.P.; Puskas, J.D.; Kurlansky, P.A.; Engoren, M.C.; Tranbaugh, R.F.; et al. Operative Outcomes of Multiple-Arterial Versus Single-Arterial Coronary Bypass Grafting. Ann. Thorac. Surg. 2018, 105, 1109–1119. [Google Scholar] [CrossRef] [PubMed]
  24. Petrovic, I.; Nezic, D.; Peric, M.; Milojevic, P.; Djokic, O.; Kosevic, D.; Tasic, N.; Djukanovic, B.; Otasevic, P. Radial artery vs. saphenous vein graft used as the second conduit for surgical myocardial revascularization: Long-term clinical follow-up. J. Cardiothorac. Surg. 2015, 10, 127. [Google Scholar] [CrossRef]
  25. Buxton, B.F.; Hayward, P.A.; Raman, J.; Moten, S.C.; Rosalion, A.; Gordon, I.; Seevanayagam, S.; Matalanis, G.; Benedetto, U.; Gaudino, M.; et al. Long-Term Results of the RAPCO Trials. Circulation 2020, 142, 1330–1338. [Google Scholar] [CrossRef]
  26. Taggart, D.P.; Benedetto, U.; Gerry, S.; Altman, D.G.; Gray, A.M.; Lees, B.; Gaudino, M.; Zamvar, V.; Bochenek, A.; Buxton, B.; et al. Bilateral versus Single Internal-Thoracic-Artery Grafts at 10 Years. N. Engl. J. Med. 2019, 380, 437–446. [Google Scholar] [CrossRef]
  27. Thuijs, D.J.F.M.; Davierwala, P.; Milojevic, M.; Deo, S.V.; Noack, T.; Kappetein, A.P.; Serruys, P.W.; Mohr, F.W.; Morice, M.C.; Mack, M.J.; et al. Long-term survival after coronary bypass surgery with multiple versus single arterial grafts. Eur. J. Cardiothorac. Surg. 2022, 61, 925–933. [Google Scholar] [CrossRef]
  28. Magouliotis, D.E.; Fergadi, M.P.; Zotos, P.A.; Rad, A.A.; Xanthopoulos, A.; Bareka, M.; Spiliopoulos, K.; Athanasiou, T. Differences in long-term survival outcomes after coronary artery bypass grafting using single vs. multiple arterial grafts: A meta-analysis with reconstructed time-to-event data and subgroup analyses. Gen. Thorac. Cardiovasc. Surg. 2023, 71, 77–89. [Google Scholar] [CrossRef]
  29. Saraiva, F.A.; Leite-Moreira, J.P.; Barros, A.S.; Lourenço, A.P.; Benedetto, U.; Leite-Moreira, A.F. Multiple versus single arterial grafting in coronary artery bypass grafting: A meta-analysis of randomized controlled trials and propensity score studies. Int. J. Cardiol. 2020, 1, 55–63. [Google Scholar] [CrossRef]
  30. Taggart, D.P.; Gaudino, M.F.; Gerry, S.; Gray, A.; Lees, B.; Dimagli, A.; Puskas, J.D.; Zamvar, V.; Pawlaczyk, R.; Royse, A.G.; et al. Effect of total arterial grafting in the Arterial Revascularization Trial. J. Thorac. Cardiovasc. Surg. 2022, 163, 1002–1009.e6. [Google Scholar] [CrossRef]
  31. Emamzadehashemi, K.R.; Khanghah, A.G.; Azizi, A.; Paryad, E.; Noveiri, M.J.S. Quality of life and activities of daily living one year after Coronary Artery Bypass Graft (CABG) surgery: A cross-sectional study. J. Cardiothorac. Surg. 2024, 19, 367. [Google Scholar] [CrossRef]
  32. Alzahrani, A.A.; AlAssiri, A.K.; Al-Ebrahim, K.E.; Ganbou, Z.T.; Alsudais, M.M.; Khafagy, A.M. Impact of Clinical and Sociodemographic Factors on Quality of Life Following Coronary Artery Bypass Grafting: A Mixed-Methods Study. Cureus 2024, 16, e56781. [Google Scholar] [CrossRef]
  33. Li, J.; Deng, Y.; Jiang, Y. The effectiveness of a web-based information-knowledge-attitude-practice continuous intervention on the psychological status, medical compliance, and quality of life of patients after coronary artery bypass grafting surgery: A parallel randomized clinical trial. J. Cardiothorac. Surg. 2024, 19, 125. [Google Scholar]
  34. Creber, R.M.; Dimagli, A.; Spadaccio, C.; Myers, A.; Moscarelli, M.; Demetres, M.; Little, M.; Fremes, S.; Gaudino, M. Effect of coronary artery bypass grafting on quality of life: A meta-analysis of randomized trials. Eur. Heart J. Qual. Care Clin. Outcomes 2022, 8, 259–268. [Google Scholar] [CrossRef]
  35. Zębalski, M.; Bis, J.; Krejca, M.; Deja, M.A. Quality of life in patients after coronary artery bypass grafting with bilateral internal thoracic artery versus single internal thoracic artery. Kardiochirurgia Torakochirurgia Pol. 2020, 17, 24–28. [Google Scholar] [CrossRef] [PubMed]
  36. Masterson Creber, R.; Safford, M.; Ballman, K.; Myers, A.; Fremes, S.; Gaudino, M. Randomized comparison of the clinical Outcome of single versus Multiple Arterial grafts: Quality of Life (ROMA:QOL)—Rationale and Study Protocol. Eur. Heart J. Qual. Care Clin. Outcomes 2022, 8, 510–517. [Google Scholar] [CrossRef] [PubMed]
  37. Audisio, K.; Soletti, G.J.; Robinson, N.B.; Gaudino, M. Multiple Arterial Grafting: For Every Patient and Every Surgeon? Innovations 2021, 16, 214–215. [Google Scholar] [CrossRef] [PubMed]
  38. Raja, S.G. Total arterial coronary grafting: Outcomes, concerns and controversies. Vessel Plus 2019, 3, 23. [Google Scholar] [CrossRef]
  39. Taggart, D.P.; Audisio, K.; Gerry, S.; Robinson, N.B.; Rahouma, M.; Soletti, G.J.; Cancelli, G.; Benedetto, U.; Lees, B.; Gray, A.; et al. Single versus multiple arterial grafting in diabetic patients at 10 years: The Arterial Revascularization Trial. Eur. Heart J. 2022, 43, 4644–4652. [Google Scholar] [CrossRef]
  40. Caliskan, E.; Falk, V.; Emmert, M.Y. Multiarterial grafting in coronary artery bypass grafting. Eur. Heart J. 2019, 40, 2479–2481. [Google Scholar] [CrossRef]
  41. Sabik, J.F., 3rd; Mehaffey, J.H.; Badhwar, V.; Ruel, M.; Myers, P.O.; Sandner, S.; Bakaeen, F.; Puskas, J.; Taggart, D.; Schwann, T.; et al. Multiarterial vs. Single-Arterial Coronary Surgery: 10-Year Follow-up of 1 Million Patients. Ann. Thorac. Surg. 2024, 117, 780–788. [Google Scholar] [CrossRef] [PubMed]
  42. Raja, S.G. Composite arterial grafting. Expert. Rev. Cardiovasc. Ther. 2006, 4, 523–533. [Google Scholar] [CrossRef] [PubMed]
  43. Gaudino, M.; Bakaeen, F.; Benedetto, U.; Rahouma, M.; Di Franco, A.; Tam, D.Y.; Iannaccone, M.; Schwann, T.A.; Habib, R.; Ruel, M.; et al. Use Rate and Outcome in Bilateral Internal Thoracic Artery Grafting: Insights From a Systematic Review and Meta-Analysis. J. Am. Heart Assoc. 2018, 7, e009361. [Google Scholar] [CrossRef] [PubMed]
  44. Little, M.; Gray, A.M.; Altman, D.G.; Benedetto, U.; Flather, M.; Gerry, S.; Lees, B.; Murphy, J.; Gaudino, M.; Taggart, D.P.; et al. Cost-effectiveness of bilateral vs. single internal thoracic artery grafts at 10 years. Eur. Heart J. Qual. Care Clin. Outcomes 2022, 8, 324–332. [Google Scholar] [CrossRef] [PubMed]
  45. Jawitz, O.K.; Lawton, J.S.; Thibault, D.; O’Brien, S.; Higgins, R.S.D.; Schena, S.; Vemulapalli, S.; Thomas, K.L.; Zwischenberger, B.A. Sex Differences in Coronary Artery Bypass Grafting Techniques: A Society of Thoracic Surgeons Database Analysis. Ann. Thorac. Surg. 2022, 113, 1979–1988. [Google Scholar] [CrossRef]
  46. Attia, T.; Koch, C.G.; Houghtaling, P.L.; Blackstone, E.H.; Sabik, E.M.; Sabik, J.F., III. Does a similar procedure result in similar survival for women and men undergoing isolated coronary artery bypass grafting? J. Thorac. Cardiovasc. Surg. 2017, 153, 571–579.e9. [Google Scholar] [CrossRef]
  47. Jabagi, H.; Tran, D.T.; Hessian, R.; Glineur, D.; Rubens, F.D. Impact of Gender on Arterial Revascularization Strategies for Coronary Artery Bypass Grafting. Ann. Thorac. Surg. 2018, 105, 62–68. [Google Scholar] [CrossRef]
  48. Ren, J.; Bowyer, A.; Tian, D.H.; Royse, C.; El-Ansary, D.; Royse, A. Multiple arterial vs. single arterial coronary artery bypass grafting: Sex-related differences in outcomes. Eur. Heart J. 2024, 45, 2536–2544. [Google Scholar] [CrossRef]
  49. Qiu, Y.; Rubens, F.D. Multiple arterial grafting: Are women being left behind? Vessel Plus 2024, 8, 39. [Google Scholar] [CrossRef]
  50. Aboul-Hassan, S.S.; Stankowski, T.; Marczak, J.; Perek, B.; Olasinska-Wisniewska, A.; Urbanowicz, T.; Jemielity, M.; Moskal, L.; Majchrowicz, W.; Sá, M.P.; et al. Long-term outcomes of patients receiving right internal thoracic artery or radial artery as a second arterial conduit. A propensity score matching study. Int. J. Cardiol. 2023, 370, 136–142. [Google Scholar] [CrossRef]
  51. Benedetto, U.; Raja, S.G.; Albanese, A.; Amrani, M.; Biondi-Zoccai, G.; Frati, G. Searching for the second best graft for coronary artery bypass surgery: A network meta-analysis of randomized controlled trials†. Eur. J. Cardiothorac. Surg. 2015, 47, 59–65; discussion 65. [Google Scholar] [CrossRef]
  52. Lau, C.; Di Franco, A.; Ng, C.; Girardi, L.N.; Angelini, G.D. Right internal thoracic artery versus radial artery as the second best arterial conduit: Insights from a meta-analysis of propensity-matched data on long-term survival. J. Thorac. Cardiovasc. Surg. 2016, 152, 1083–1091.e15. [Google Scholar]
  53. Browne, A.; Lamy, A. Selecting conduits for coronary artery bypass grafting: Caution regarding the right internal mammary artery. Vessel Plus 2024, 8, 19. [Google Scholar] [CrossRef]
  54. Ramadan, A.S.; Stefanidis, C.; N’Gatchou, W.; El Oumeiri, B.; Jansens, J.L.; De Smet, J.M.; Antoine, M.; De Cannière, D. Five years follow-up after Y-graft arterial revascularization: On pump versus off pump; prospective clinical trial. Interact. Cardiovasc. Thorac. Surg. 2010, 10, 423–427. [Google Scholar] [CrossRef] [PubMed]
  55. Royse, A.G.; Brennan, A.P.; Ou-Young, J.; Pawanis, Z.; Canty, D.J.; Royse, C.F. 21-Year Survival of Left Internal Mammary Artery-Radial Artery-Y Graft. J. Am. Coll. Cardiol. 2018, 72, 1332–1340. [Google Scholar] [CrossRef] [PubMed]
  56. Dimagli, A.; Gemelli, M.; Kumar, N.; Mitra, M.; Sinha, S.; Fudulu, D.; Harik, L.; Cancelli, G.; Soletti GJr Olaria, R.P.; Bonaros, N.; et al. A systematic review and meta-analysis of internal thoracic artery harvesting techniques: Skeletonized vs. pedicled. Int. J. Cardiol. 2024, 395, 131577. [Google Scholar] [CrossRef] [PubMed]
  57. Mohammadi, S.; Dagenais, F.; Doyle, D.; Mathieu, P.; Baillot, R.; Charbonneau, E.; Perron, J.; Voisine, P. Age cut-off for the loss of benefit from bilateral internal thoracic artery grafting. Eur. J. Cardiothorac. Surg. 2008, 33, 977–982. [Google Scholar] [CrossRef]
  58. Benedetto, U.; Amrani, M.; Raja, S.G.; Harefield Cardiac Outcomes Research Group. Guidance for the use of bilateral internal thoracic arteries according to survival benefit across age groups. J. Thorac. Cardiovasc. Surg. 2014, 148, 2706–2711. [Google Scholar] [CrossRef]
  59. Kieser, T.M.; Lewin, A.M.; Graham, M.M.; Martin, B.J.; Galbraith, P.D.; Rabi, D.M.; Norris, C.M.; Faris, P.D.; Knudtson, M.L.; Ghali, W.A.; et al. Outcomes associated with bilateral internal thoracic artery grafting: The importance of age. Ann. Thorac. Surg. 2011, 92, 1269–1275; discussion 1275–1276. [Google Scholar] [CrossRef]
  60. Sergeant, P.; Blackstone, E.; Meyns, B. Validation and interdependence with patient-variables of the influence of procedural variables on early and late survival after CABG. K.U. Leuven Coronary Surgery Program. Eur. J. Cardiothorac. Surg. 1997, 12, 1–19. [Google Scholar] [CrossRef]
  61. Ren, J.; Royse, C.; Srivastav, N.; Lu, O.; Royse, A. Long-Term Survival of Multiple Versus Single Arterial Coronary Bypass Grafting in Elderly Patients. J. Clin. Med. 2023, 12, 2594. [Google Scholar] [CrossRef] [PubMed]
  62. Surgeon Preference Factors into Survival Outcomes Analyses for Multi- and Single-Arterial Bypass Grafting. Available online: https://www.sts.org/press-releases/surgeon-preference-factors-survival-outcomes-analyses-multi-and-single-arterial-bypass-grafting (accessed on 23 March 2025).
  63. Gaudino, M.; Alexander, J.H.; Bakaeen, F.G.; Ballman, K.; Barili, F.; Calafiore, A.M.; Davierwala, P.; Goldman, S.; Kappetein, P.; Lorusso, R.; et al. Randomized comparison of the clinical outcome of single versus multiple arterial grafts: The ROMA trial-rationale and study protocol. Eur. J. Cardiothorac. Surg. 2017, 52, 1031–1040. [Google Scholar] [CrossRef] [PubMed]
  64. Gaudino, M.; Bairey Merz, C.N.; Sandner, S.; Creber, R.M.; Ballman, K.V.; O’Brien, S.M.; Harik, L.; Perezgrovas-Olaria, R.; Mehran, R.; Safford, M.M.; et al. Randomized Comparison of the Outcome of Single Versus Multiple Arterial Grafts trial (ROMA):Women-a trial dedicated to women to improve coronary bypass outcomes. J. Thorac. Cardiovasc. Surg. 2024, 167, 1316–1321. [Google Scholar] [CrossRef] [PubMed]
  65. Gomes, W.J.; Gomes, E.N.; Bertini, A., Jr.; Reis, P.H.; Hossne, N.A., Jr. The Anaortic Technique with Bilateral Internal Thoracic Artery Grafting—Filling the Gap in Coronary Artery Bypass Surgery. Braz. J. Cardiovasc. Surg. 2021, 36, 397–405. [Google Scholar] [CrossRef]
  66. Ramponi, F.; Seco, M.; Brereton, R.J.L.; Gaudino, M.F.L.; Puskas, J.D.; Calafiore, A.M.; Vallely, M.P. Toward stroke-free coronary surgery: The role of the anaortic off-pump bypass technique. J. Card. Surg. 2021, 36, 1499–1510. [Google Scholar] [CrossRef]
  67. Di Giammarco, G.; Rabozzi, R. Can transit-time flow measurement improve graft patency and clinical outcome in patients undergoing coronary artery bypass grafting? Interact. Cardiovasc. Thorac. Surg. 2010, 11, 635–640. [Google Scholar] [CrossRef]
  68. Hashim, S.A.; Amin, M.A.; Nair, A.; Raja Mokhtar, R.A.; Krishnasamy, S.; Cheng, K. A Flowmeter Technique to Exclude Internal Mammary Artery Anastomosis Error in an Arrested Heart. Heart Lung Circ. 2018, 27, e59–e63. [Google Scholar] [CrossRef]
  69. Hiraoka, A.; Fukushima, S.; Miyagawa, S.; Yoshikawa, Y.; Saito, S.; Domae, K.; Sakaguchi, T.; Toda, K.; Sawa, Y. Quantity and quality of graft flow in coronary artery bypass grafting is associated with cardiac computed tomography study-based anatomical and functional parameters. Eur. J. Cardiothorac. Surg. 2017, 52, 909–916. [Google Scholar] [CrossRef]
  70. Di Giammarco, G.; Canosa, C.; Foschi, M.; Rabozzi, R.; Marinelli, D.; Masuyama, S.; Ibrahim, B.M.; Ranalletta, R.A.; Penco, M.; Di Mauro, M. Intraoperative graft verification in coronary surgery: Increased diagnostic accuracy adding high-resolution epicardial ultrasonography to transit-time flow measurement. Eur. J. Cardiothorac. Surg. 2014, 45, e41–e45. [Google Scholar] [CrossRef]
  71. Harahsheh, B. Transit Time Flowmetry in Coronary Artery Bypass Grafting-experience at Queen Alia Heart Institute, Jordan. Oman Med. J. 2012, 27, 475–477. [Google Scholar] [CrossRef]
  72. Kieser, T.M.; Rose, S.; Kowalewski, R.; Belenkie, I. Transit-time flow predicts outcomes in coronary artery bypass graft patients: A series of 1000 consecutive arterial grafts. Eur. J. Cardiothorac. Surg. 2010, 38, 155–162. [Google Scholar] [CrossRef]
  73. Santarpino, G.; Onorati, F.; Scalas, C.; De Gori, M.; Cristodoro, L.; Zofrea, S.; Renzulli, A. Radial artery achieves better flowmetric results than saphenous vein in the elderly. Heart Vessels 2009, 24, 108–115. [Google Scholar] [CrossRef]
  74. Herman, C.; Sullivan, J.A.; Buth, K.; Legare, J.F. Intraoperative graft flow measurements during coronary artery bypass surgery predict in-hospital outcomes. Interact. Cardiovasc. Thorac. Surg. 2008, 7, 582–585. [Google Scholar] [CrossRef] [PubMed]
  75. Mujanović, E.; Kabil, E.; Bergsland, J. Transit time flowmetry in coronary surgery--an important tool in graft verification. Bosn. J. Basic. Med. Sci. 2007, 7, 275–278. [Google Scholar] [CrossRef] [PubMed]
  76. Onorati, F.; Pezzo, F.; Esposito, A.; Impiombato, B.; Comi, M.C.; Polistina, M.; Renzulli, A. Single versus sequential saphenous vein grafting of the circumflex system: A flowmetric study. Scand. Cardiovasc. J. 2007, 41, 265–271. [Google Scholar] [CrossRef] [PubMed]
  77. Desai, N.D.; Miwa, S.; Kodama, D.; Koyama, T.; Cohen, G.; Pelletier, M.P.; Cohen, E.A.; Christakis, G.T.; Goldman, B.S.; Fremes, S.E. A randomized comparison of intraoperative indocyanine green angiography and transit-time flow measurement to detect technical errors in coronary bypass grafts. J. Thorac. Cardiovasc. Surg. 2006, 132, 585–594. [Google Scholar] [CrossRef]
  78. Neumann, F.J.; Sousa-Uva, M.; Ahlsson, A.; Alfonso, F.; Banning, A.P.; Benedetto, U.; Byrne, R.A.; Collet, J.P.; Falk, V.; Head, S.J.; et al. 2018 ESC/EACTS Guidelines on myocardial revascularization. EuroIntervention 2019, 14, 1435–1534. [Google Scholar] [CrossRef]
Table 1. Key randomized controlled trials comparing short- and mid-term outcomes of MAG and SAG.
Table 1. Key randomized controlled trials comparing short- and mid-term outcomes of MAG and SAG.
Author, Year of PublicationNumber of PatientsDiabetes Mellitus, n (%)Obesity, n (%)COPD, n (%)Previous MI, n (%)LVEF, n (%) or Median (IQR) or Mean ± SDKey Outcomes
SAGMAGSAGMAGSAGMAGSAGMAGSAGMAGSAGMAG
Morris, 1990 [6]420643NRNRNRNRNRNR6 (1.43)5 (0.78)0.51 ± 0.100.49 ± 0.10Similar 30-dat and long-term survival at 4 years.
Myers, 2000 [7]818112 (15)11 (14)NRNRNRNR12 (14.8)13 (16)62.60 60.80Similar early and 5-year outcomes.
Buxton, 2003 [8]8027337 (46)27 (37)NRNRNRNRNRNR26 (32) 22 (30)Similar patency and clinical events at 5 years.
Muneretto, 2003 [9]10010040 (40)41 (41)8 (8)6 (6)22 (22)19 (19)37 (37)41 (41)28 (28)29 (29) Superior clinical results and improved patient outcome with respect to recurrence of angina and a higher graft patency with MAG.
Muneretto, 2004 [10]808044 (55)41 (51)NRNRNRNRNRNRNRNR Significantly higher graft patency rate and a lower incidence of CVA and late cardiac events with MAG.
Collins [11] 2008608210 (17)15 (18)NRNRNRNR29 (48)45 (55)NRNRSignificantly better graft patency in MAG group.
Nasso, 2009 [12]20260178 (38)227 (37)28 (14)84 (14)57 (28)165 (27)61 (30)178 (29)28 (14)85 (14)Better mid-term event free survival in MAG group.
Damgaard, 2009 [13]17016143 (25)39 (24)28 ± 427 ± 4NRNRNRNR42 (25)48 (30)Similar patency index and rate of cardiac events.
Goldman, 2011 [14]367366153 (42)154 (42)NRNRNRNR143 (39)146 (40)NRNR Similar angiographic graft patency at 1 week after CABG, myocardial infarction, stroke, repeat revascularization, and death as well as graft patency at 1 year.
Song, 2012 [15]253513 (52)15 (42.9)7 (28)14 (40)NRNRNRNR3 (13)0 (0) Similar postoperative morbidity, mortality, angiographic patency, and overall survival.
Le, 2015 [16]28306 (20)9 (30)26 (87)27 (90)3 (10)2 (7)4 (13)2 (7)0 (0)1 (3)Similar postoperative morbidity, mortality, and angiographic patency.
Kim, 2018 [17]11211246 (41)51 (46)52 (46)52 (46)NRNRNRNR58 (54, 65)57 (50, 63)Similar midterm clinical outcomes and 5-year graft occlusion rates.
Thujis, 2018 [18]688217198 (30)33 (15)237 (34) 61 (28) 62 (9) 13 (6) 103 (15) 26 (12) 57.0 ± 8.859.0 ± 9.6Similar clinical outcomes at 3 years.
Fomenko, 2021 [19]385387121 (31.4)129 (33.3)30.2 ± 5.730.5 ± 5.1NRNRNRNR58.3% ± 5.6%58.5% ± 5.1%Comparable procedure-related outcomes and survival at 1, 3, and 5 years.
Taggart, 2022 [20]15541548363 (23.4)371 (23.9)NRNRNRNR681 (43.9)619 (40.0)NANA Similar 30-day and 1-year mortality, rates of stroke, myocardial infarction, and repeat revascularization with 1.3% more MAG patients needing sternal wound reconstruction.
CABG = coronary artery bypass grafting; COPD = chronic obstructive pulmonary disease; IQR = interquartile range; LVEF = left ventricular ejection fraction; MAG = multiple arterial grafting; NA = not available; NR = not recorded; SAG = single arterial grafting.
Table 2. Key randomized controlled trials comparing long-term outcomes of MAG and SAG.
Table 2. Key randomized controlled trials comparing long-term outcomes of MAG and SAG.
Author, Year of PublicationNumber of PatientsDiabetes Mellitus, n (%)Obesity, n (%)COPD, n (%)Previous MI, n (%)LVEF, n (%) or Median (IQR) or Mean ± SDKey Outcomes
SAGMAGSAGMAGSAGMAGSAGMAGSAGMAGSAGMAG
Petrovic, 2015 [24]10010043 (43)39 (39)NRNR8 (8)9 (9)56 (56)57 (57)48 ± 1149 ± 11Similar clinical outcomes at 8 years.
Buxton, 2020 [25]11211352 (46)50 (44)NRNRNRNR36 (32)43 (38)>35%>35%Better 10-year patency rate of MAG.
Taggart, 2022 [26] 15541548363 (23.4)371 (23.9)NRNRNRNR681 (43.9)619 (40.0)NANA Similar 10-year survival rate of MAG and SAG.
Thujis, 2022 [27]1001465361 (36.1)141 (30.5)310 (31.0)144 (31.0)89 (8.9)34 (7.3)351/984 (35.7)128/457 (28.0)NRNR Markedly lower all-cause death at 12.6-year follow-up with MAG.
COPD = chronic obstructive pulmonary disease; IQR = interquartile range; LVEF = left ventricular ejection fraction; MAG = multiple arterial grafting; NA = not available; NR = not recorded; SAG = single arterial grafting.
Table 3. TTFM-based detection of graft abnormalities and revisions reported by prospective studies and RCTs.
Table 3. TTFM-based detection of graft abnormalities and revisions reported by prospective studies and RCTs.
Study (Author, Year)Study TypeN. of Grafts/PatientsGraft Type(s)Assessment CriteriaAbnormal Graft RateRevised Graft RateStated Reason(s) for Revision or Abnormality
Hashim (2018) [68]Prospective86/60IMAPI > 1.0 and MGF < 20 mL/min (arrested heart)Not specified3.5% (3 grafts)Not reported
Hiraoka (2017) [69]Prospective104/63IMA, RA, SVGPI > 5.0 and MGF < 20 (ITA)8.7% (9 grafts)Not reportedHigh PI and low MGF consistent with conduit- or anastomosis-related issues
Di Giammarco (2014) [70]Prospective717/333IMA, SVGPI ≥ 3.0 and MGF ≤ 15 mL/min5.4% (39 grafts)0.3% (2 grafts)TTFM + surgical inspection confirmed failing grafts
Harahsheh (2012) [71]Prospective1394/436Not specifiedPI > 5.0, MGF < 20, DF < 50%7.2% (100 grafts)1.0% (14 grafts), 1.1% (5 patients)No explicit cause—reflective of intraoperative malperfusion
Kieser (2010) [72]Prospective1015/336IMA, SVG, RAPI > 5.07% (74 grafts)2.0% (20 grafts)59 patients revised based on clinical judgement, poor TTFM metrics, and DF
Santarpino (2009) [73]Prospective238/238LIMA + RA/LIMA + SVGPI > 4.0 and abnormal systolic waveformsNot applicable1.3% (3 grafts, 3 patients)Thrombosis (n = 2), torsion (n = 1)
Herman (2008) [74]Prospective—/985IMA, SVGPI > 5.018.7% (184 patients)2.0% (20 patients)Anastomotic (9), conduit-related (8), subclavian stenosis (1), unidentified (2)
Mujanovic (2007) [75]Prospective2872/1000Not specifiedNot specifiedNot applicable2.2% (64 grafts), 6.3% (63 patients)Cut-off for revision not disclosed
Onorati (2007) [76]RCT90/90Single vs. sequential SVGPI > 5, MGF not detailed5.6% (5 grafts)5.6% (5 patients), 1.1% (1 graft)“Systolic” curve pattern: MGF 4 mL/min, PI 7.8
Desai (2006) [77]RCT139/106IMA, SVG, RAPI > 5.0, DF < 50%, MGF < 10 mL/min2.6% (3 grafts)1.4% (2 grafts)DF <50%, PI >5.0 and MGF <10 mL/min
DF = diastolic filling; ITA = internal mammary artery; MGF = mean graft flow; PI = pulsatility index; RA = radial artery; RCT = randomized controlled trial; SVG = saphenous vein graft; TTFM = transit-time flow measurement.
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Raja, S.G. Multiple Arterial Grafting in CABG: Outcomes, Concerns, and Controversies. J. Vasc. Dis. 2025, 4, 29. https://doi.org/10.3390/jvd4030029

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Raja SG. Multiple Arterial Grafting in CABG: Outcomes, Concerns, and Controversies. Journal of Vascular Diseases. 2025; 4(3):29. https://doi.org/10.3390/jvd4030029

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Raja, Shahzad G. 2025. "Multiple Arterial Grafting in CABG: Outcomes, Concerns, and Controversies" Journal of Vascular Diseases 4, no. 3: 29. https://doi.org/10.3390/jvd4030029

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Raja, S. G. (2025). Multiple Arterial Grafting in CABG: Outcomes, Concerns, and Controversies. Journal of Vascular Diseases, 4(3), 29. https://doi.org/10.3390/jvd4030029

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