Redefining treatment interval in lung cancer surgery in the era of prehabilitation: a systematic review

Introduction

Surgery is the cornerstone of curative lung cancer treatment. Despite the development of minimally invasive techniques and enhanced recovery programs, morbidity and mortality remain a major concern. A short time-to-treatment interval is seen as an indicator for quality of care. Early surgery is regarded as beneficial to prevent disease progression and irresectability, thereby possibly improving disease-free and long-term survival.

Previous systematic reviews on time-to-treatment aimed to demonstrate an association between timely treatment and beneficial oncologic outcomes for all stages and all kinds of treatments for lung cancer (1-3). Results were inconsistent and no clear recommendations could be made regarding an optimal time-to-treatment interval.

Besides timely initiation of treatment, the quality of surgical care is also represented by postoperative complications, mortality, and length of hospital stay. Minimally invasive surgery, as well as “enhanced recovery after thoracic surgery” (ERATS) protocols, have reduced postoperative morbidity and length of stay (4,5). Preoperative completion of a multimodal prehabilitation program—including exercise physiotherapy, protein and vitamin supplementation, smoking cessation, mental support, and patient empowerment, and optimization of respiratory status—may further enhance recovery after lung cancer surgery (6,7).

The goal of this systematic review is to redefine the concept of timely surgery, in order to allow the conduction of prehabilitation during the interval to surgery. Therefore, we explored the evidence on an optimal time-to-surgery interval—with no negative impact on disease progression or oncological outcomes—and which would allow for improvement of patient factors and subsequent care, through the implementation of prehabilitation during this time interval.

The following research questions are addressed:

• What definition regarding starting point is used to define treatment interval for lung cancer surgery?
• How is timely and delayed surgery currently defined in the literature?
• What is the relation of duration of treatment interval until lung cancer surgery regarding postoperative outcomes?

We present this article in accordance with the PRISMA reporting checklist (available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-688/rc) (8).

Methods

Prospectively, the study protocol was registered for this study in PROSPERO under the ID CRD42025646793.

Search strategy

A systematic literature search was performed on January 30^th, 2025, of the databases Embase.com, Medline (Ovid), and the Cochrane Central Register of Controlled Trials (Wiley). The search strategy, designed and performed by a biomedical information specialist (IH), was developed in Embase.com, and translated into the other databases, using a combination of thesaurus terms in combination with free text search of synonyms in title and abstract. The search strategy was composed of three elements: (I) time-to-treatment; (II) lung cancer; and (III) surgery for cancer/lungs. Targeted search terms were used to exclude animal studies, studies not written in English or Dutch, conference abstracts, and case reports, as well as studies with “lung transplantation” in the title. No limitations regarding publication date were applied. Duplicates were removed in Endnote (version 21) using the Bramer method (9). In addition to the systematic literature search, the reference list of one other systematic review was checked for additional publications (10). The complete search strategy is provided in Appendix 1.

Identification and article selection

All studies were screened independently by two researchers (L.D.G. and Q.C.A.v.S.) in Rayyan, first on title and abstract, thereafter in full text (11). Any discrepancies were resolved by discussion or by consulting a third researcher (F.J.C.v.d.B.). All studies were screened for clear definition of the treatment interval (article selection for research question 1). Furthermore, a second screening on these studies was performed for reported results on outcomes (selection for research question 2 and 3).

Inclusion criteria were: patients aged ≥18 years with lung cancer, treated with surgical resection, and a described treatment interval definition related to surgery. Exclusion criteria were: lung transplantation, neoadjuvant therapy, stage IV lung cancer, lung metastasis, lung resection for recurrence, benign lung pathology, and a sample size <20 patients.

Outcomes of interest were any outcomes related to the treatment interval: overall survival (OS), disease-free survival (DFS), recurrence, readmission, and upstaging.

Data extraction and analysis

The following data were extracted with a predefined collection form: first author, publication date, country, lung cancer type, study design, sample size, starting point of treatment interval, outcomes, and results. Continuous data were reported as mean (standard deviation), median [interquartile range] or |range|, depending on how results were reported in the included articles. Narrative synthesis was used to summarize the overall findings of the studies per outcome. Possible associations between the treatment interval and the outcomes were noted, based on a P value of 0.05 for statistical significance. If only subgroups of a study were of interest, only the results for these subgroups were reported.

A risk of bias assessment on all articles concerning time-to-surgery in relation to the most common outcome measure was completed according to the PRISMA guidelines. The Risk Of Bias In Non-randomized Studies-of Interventions (ROBINS-I) tool was used for the non-randomized controlled trials (12). Assessment was performed independently by two reviewers (L.D.G. and Q.C.A.v.S.) and any disagreements were resolved.

Results

Search strategy

The literature search resulted in 2,255 unique studies after duplicate removal. After screening, 86 studies were included for the determination of treatment interval definition (research question 1). Figure 1 shows the PRISMA flowchart of the search. Most studies originated from the United States of America (US) (n=42). Of those 86 studies, 36 studies met the inclusion criteria for the analysis on association between treatment interval and outcomes (research question 2 and 3). These studies were all retrospective, with a publication year ranging from 2002 to 2025. Notably, 13 studies originated from the American National Cancer Database (NCDB) (13-25). The population size of the studies ranged from 42 to 193,058 patients. Nineteen studies included more than 1,000 lung cancer patients. No preoperative enhancement program of the patient’s functional capacity (prehabilitation) was conducted in the included studies.

Figure 1 PRISMA 2020 flow diagram of study selection. ^†, subanalysis on association between treatment interval and outcomes. LC, lung cancer.

Definition treatment interval to lung cancer surgery

The definition reported for the treatment interval until lung cancer surgery, varies widely in the starting point of the 86 included studies (Table 1). Ten studies included more than one starting point, resulting in 97 reported starting points and subsequent intervals. The most reported starting point was “diagnosis” by 50 studies. However, different diagnosis definitions were used, and some studies used more than one definition (n=60 total): pathological confirmation (n=16), radiography confirmation (n=9), clinical confirmation (n=8), and not further specified (n=27).

Timely and delayed surgery

The definition of delay in treatment interval in the 36 included studies varied from >21 days to over 90 days. Most studies (n=18) used a tipping point beyond 42 days (6 weeks) to differentiate between timely and delayed surgery. Seven studies put the division under 42 days. Eight studies compared categorical treatment intervals, two were not specifically defined, and one used an increase in days compared to a reference cohort.

Association between outcomes and length of treatment interval

Thirty-six studies reported on the association between the length of treatment interval and lung cancer surgery outcomes (Table 2). A proportion of 47% of the included studies associated a delay in treatment interval with worse outcomes (OS, DFS, upstaging, recurrence), 33% found no association (OS, DFS, upstaging, tumor growth), and in 19% the association differed per lung cancer stage or type of outcome. In Table 2, the studies are stratified by the studied lung cancer stage category, resulting in 43 studied categories: stage I (n=16), stage I–II (n=8), stage II (n=5), stage I–III (n=7), stage III (n=3), and missing specific stage (n=4). Five studies reported on more than one staging category, one study reported different results per starting point (75), and one study performed two analyses on different populations (propensity score matched and single center) (22), resulting in 60 studied outcomes (Table 2).

The most frequently reported outcome in relation to treatment interval was OS (n=38), followed by upstaging (n=11), DFS (n=6), recurrence (n=3), readmission (n=1), and tumor growth (n=1). Associations with OS are reported in section “OS and treatment interval”. Upstaging was defined in all groups as clinical staging to pathological staging (n=11). An association between delayed treatment interval and upstaging was reported in 6 out of 11 groups. Four groups found no association, and one associated a delay with downstaging. Of the six groups reporting about DFS, two associated a delayed treatment interval with inferior DFS, and four groups found no association. Recurrence of lung cancer was reported in three groups, and all associated a higher recurrence with a delayed treatment interval. Readmission was reported once by Banks et al., and was associated with a delayed treatment interval with fewer readmissions (66). Finally, Bhat et al. found no association between the treatment interval and tumor growth (56).

Seven studies (19,22,33,39,66,72,75) reported mixed outcomes, ranging from worse outcome, no association to better outcomes. There were differences in the outcome category, starting point of treatment interval, and the substage category. Most studies reported a combination of worse and no association (n=5). Furthermore, two studies included a delay in treatment interval that was associated with a better outcome. This was reported for stage I in relation to upstaging (22), and stage I–II in relation to readmission (66). These studies showed, respectively, no association for OS (22), and worse association for OS and recurrence (66).

Due to the considerable heterogeneity in the reported outcomes, further comparisons were deemed unfeasible. OS, being the most frequently reported outcome measure, was analyzed separately in the subsequent section.

OS and treatment interval

Figure 2 depicts an overview of 30 articles, with the treatment interval on a timeline in relation to OS as the outcome, sorted by stage in alphabetical order (n=38). Associations are related to their definition of the treatment interval, where studies are compared to their chosen threshold of timely and delayed treatment interval.

Figure 2 Results of the association between treatment interval and OS in lung cancer surgery, plotted per study. Results are sorted by lung cancer stage and starting points of the treatment interval are noted. Each horizontal bar represents the length of the treatment interval of the studied populations, expressed in days, equally (unless otherwise indicated with //). Each horizontal bar is separated by one or more bold black lines, indicating the delay definition. A few studies contain more than one bold black line, because they compared several categories with each other. The end of a delayed treatment interval was in most studies not defined, depicted as ^¶. Associations between the treatment interval and OS were better (=green), none (=grey) or worse (=red) compared to the other treatment interval group(s) studied. Results of RoB assessment with ROBINS-I tool are depicted in the second column as high (H), moderate (M) and low (L) risk of bias. *Zhang et al. reported hazard ratios compared to the earliest group, which became worse with more delay and this is shown with increasing red colored bars. ^†Studies that did not specify delay definition into a number, therefore the median of the group was used as separation. 1, diagnosis specified as histologic. 2, diagnosis specified as radiologic. OS, overall survival; PSM, propensity score matched; RoB, risk of bias.

The positive and negative associations for OS are stratified by their threshold of delayed treatment interval. Eighteen percent used a starting point different from diagnosis. Sixty-six percent associated delayed treatment interval with worse OS, which was applicable for stage I (9/15 groups), stage II (4/4), stage I–II (5/7), early stage (3/3), stage I–III (3/6), and stage III (1/2). Thirty-four percent reported no association, of which one (1/1) for local stage, and none reported that delayed treatment interval was associated with better OS.

The overall bias assessment, as determined by the ROBINS-I tool, is presented in the second column of Figure 2. This categorizes the studies as having a high (n=3), moderate (n=26), and low (n=1) risk of bias. The full risk of bias assessment is described in Appendix 2. Valuable comparisons could not be made for other outcome measures (e.g., upstaging or DFS), due to insufficient comparable data being available.

Discussion

This systematic review provides insight into the available evidence on the length of treatment interval prior to lung cancer surgery, and its relationship with patient-related outcomes. Although this interval has been studied extensively, definitions varied widely, regarding starting point—mostly defined as the time of pathological diagnosis. Moreover, the definition of timely versus delayed treatment varied widely, with the most reported tipping points at 6 weeks or beyond. A delayed treatment interval was inconsistently associated with poorer or comparable outcomes, mainly studied in OS. One-third of the studies found no association, and a few reported better outcomes in delayed cases.

There is currently no internationally accepted definition for the treatment interval in lung cancer surgery. Starting points ranged from first onset of symptoms to surgical consultation, leading to heterogeneity when comparing studies on the duration of treatment interval. Even when “diagnosis” was used, it was inconsistently defined as pathologic, radiographic, or clinical diagnosis. In the Netherlands, the guidelines consider the date of the completed diagnostic pathway (i.e., the time of the multidisciplinary team meeting) as the starting point of the treatment interval (98). Using the pathological diagnosis confirmation as starting point for treatment interval was mostly used in this systematic review, and corresponds with the internationally recommended starting point as defined in the Aarhus statement (99). Within other malignancies like colorectal cancer, an identical recommendation for the date of diagnosis with pathological biopsy confirmation was seen (100). We support this as a pragmatic and clinically relevant approach, which is supported by the majority of included studies in this review.

Not only the definition, but also the reported length of the treatment interval varied widely across the 36 studies, ranging from 21 to 90 days, indicating variation in the lung cancer care treatment pathways between studies. Interestingly, the recommended time-to-treatment interval differs between different countries, reflecting the lack of evidence regarding the optimal treatment interval. This variation could be explained by inclusion of studies from different countries, having their own guidelines, healthcare structures, and clinical workflows. Internationally, there are different guidelines available for lung cancer treatment intervals; however, they are often not incorporated into national guidelines. The British Thoracic Society guideline is most commonly referred to in the literature, in which treatment interval is defined as 56 days (8 weeks) from consultation with a lung cancer specialist until surgery (101). Furthermore, the National Comprehensive Cancer Network (NCCN) recommends starting surgery within 8 weeks after diagnosis (102). The Dutch national guideline advises surgery within 2 weeks after complete diagnostics, which is audited by the Dutch Institute of Clinical Auditing (DICA), who maintain a 3-week timeline from multidisciplinary team meeting (98,103). Compared to studies included in this review and the above-mentioned guidelines, the Dutch guideline is stricter and not supported by evidence from this systematic review. In the DICA, the median national benchmark from time between multidisciplinary team meeting and surgery is 20 days (IQR, 13–28 days) (104). To enable better benchmarking and comparison, and define optimal intervals, it is crucial for hospitals and health systems to transparently report their treatment intervals.

Overall, 66% of the included study groups associated a delay in treatment interval with worse OS. However, the validity of these associations is hindered by dichotomization, retrospective nature, and heterogeneity. Moreover, they are inconsistent with previous systematic reviews. Most studies (37.5%) within Guirado et al. described a better prognosis with a delayed treatment interval (1), and Olsson et al. concluded that most studies (53.3%) found no association with survival (2). Also, an umbrella review by Zhang et al. concluded that there is no consistency in the association between OS and waiting time, with studies reporting no association between the treatment interval and OS, or a negative association—meaning that a longer treatment interval resulted in better OS (3). This difference between our review and earlier reviews is possibly due to the fact that these reviews did not focus specifically on surgery, but rather on all types of treatment for lung cancer. However, Hall et al. did actually perform a subanalysis of 12 articles for surgery only, and they found a trend in the same direction as our systematic review. They concluded that 73 percent of the articles associated a timely treatment interval with improved OS (10). This suggests that the length of the treatment interval might be more relevant for surgery compared to other treatments. However, Hall et al. encountered the same problem: a binary and inconsistent definition of timely versus delayed treatment, which created difficulty in establishing comparative trends.

In the current systematic review, a waiting time of around 6 weeks seems to be a general tipping point for delayed treatment interval, as reported in most included studies for OS. Thirteen groups included a delay definition of the treatment interval somewhere before 6 weeks, of which ten associated a delayed interval with worse OS, and three found no association. Furthermore, 25 groups had their delay threshold beyond 6 weeks, of which fifteen groups associated a delay with worse OS and ten found no association. However, these results should be treated with caution, as most studies used dichotomization, meaning that the treatment interval was not considered as a continuum. Therefore, the exact threshold is unknown and could be before or after the chosen time point. This dichotomization problem arises because the guidelines prefer to use a specific threshold in order to make auditing easier.

Earlier stages of lung cancer, stage I and II, seem to benefit the most from a timely treatment. This is an interesting trend, as it is often expected that early-stage lung cancer patients have more time before progression of their disease, compared to late-stage patients. Furthermore, Mayne et al. showed different results in OS for stage Ia1 versus stage Ia2 patients, separated by adenocarcinoma and small cell carcinoma (19). This indicates that more studies are needed that specifically study substages.

This review is limited by the retrospective nature of all included studies, resulting in unobserved confounding and possible selection bias. It is important to note that 42 percent of the studies included in the paper by Hall et al. (10), and 36 percent of the studies included in our systematic review, reported data from NCDB with overlapping periods, possibly resulting in different forms of selection bias and replication of individual patient data. Furthermore, in the NCDB, comorbidity details and pulmonary functional data are missing. Therefore, patients with a higher operative risk for surgery may experience a delayed treatment interval due to an extended preoperative workup (24). This was also pointed out by Zhang et al., identifying one or more comorbidities as patient risk factors for longer treatment intervals (3), which may also be associated with decreased OS. In the scoping review of Malalasekera et al., treatment delay was mostly related to patient factors like lack of clinical symptoms (105). Detailed information about the time of diagnosis and workup was also not available in the NCDB (17). Besides the use of NCDB data, Mayne et al. excluded patients with a waiting time of 31–89 days in their analysis of timely and delayed surgery within their three studies (19-21), and were assessed as having a high risk of bias. These NCDB studies represent a substantial part of the available evidence to this review, which should therefore be weighed with caution. Moreover, most studies originated from the US, making the results less generalizable to the rest of the world. Furthermore, the quality of all the OS studies was most commonly assessed as moderate risk of bias when evaluated using the ROBINS-I tool. Due to the heterogeneity of the studies regarding starting points, definition of timely surgery, outcome of interest, data sources, as well as studied populations, it was not possible to perform a meta-analysis. Even after filtering on these variables, considerable heterogeneity remained in the statistical approaches used, in the definition of time-to-event, and in follow-up durations. These inconsistencies prevented us from pooling the results into a single, coherent effect estimate. Despite these limitations, this review provides a full overview of the evidence available on definition of timely surgery in lung cancer surgery and relations to outcomes, without publication year restrictions. All reported outcomes were included in the current study.

The frequently reported absence of any association between treatment interval and outcomes is an important finding, indicating that a (short) delay in surgery could be acceptable. In this systematic review, about 6 weeks was the most reported tipping point for timely surgery. This time-to-surgery can be reframed into potential time to perform prehabilitation and optimize patients’ conditions. None of the 36 included studies in this review have noted the use of prehabilitation (or another preoperative intervention to prepare the patient for surgery) in the time until surgery. Prehabilitation is becoming the standard of care in several other oncological specialties, like colorectal cancer, as many studies have shown that prehabilitation reduces complications, length of hospital stay, and readmissions (106-109). First studies on survival after prehabilitation have shown no negative effects (110-112). Therefore, there is more interest for prehabilitation within lung cancer with promising results (7). A Cochrane review from Granger et al. showed that preoperative exercise training for non-small cell lung cancer (NSCLC) patients largely reduces the risk of a pulmonary complication postoperatively (113). Brat et al. recently confirmed these results with their randomized controlled trial, and even showed that multimodal prehabilitation reduced hospital stay, with improved quality of life (114). The ideal length of a multimodal prehabilitation program in a lung cancer treatment pathway is currently not clear yet, but Carli et al. proposed a shorter prehabilitation program for lung cancer, compared to other care pathways, of about 4 weeks (115). Moreover, in 2019, the ERATS guidelines for thoracic surgery were published and included the recommendation of a prehabilitation program of 4 weeks for patients with borderline lung function or exercise capacity (4). A recent pilot study on multimodal prehabilitation in the Netherlands demonstrated that a 3-week prehabilitation program, dictated by the DICA, was feasible in two centers already specialized in prehabilitation, which led to improvements in functional capacity (6). However, implementation of this prehabilitation program into the lung cancer treatment pathway proved challenging, even in these already specialized centers. Implementation of prehabilitation programs would probably be even more successful with more time-to-surgery, which is supported by “timely surgery” of about 6 weeks reported in the current systematic review.

New systematic reviews will probably not solve the heterogeneity in the definition of treatment interval, nor how the interval can lead to adverse outcomes. At the same time, these results do not support the current strict Dutch time-to-surgery interval compared to most other European guidelines. We recommend reaching a consensus on the definition and time-to-surgery in international guidelines, based either on current literature or on analysis of available individual patient data regarding treatment interval. This could also clarify whether the patients in the “delayed” group are frailer and therefore associated with worse outcomes, such as survival. Furthermore, after establishing the period of timely surgery, additional prehabilitation can be investigated to benefit patient outcomes.

Conclusions

There is currently no internationally accepted definition for the treatment interval in lung cancer surgery, nor a targeted time frame, with a highly inconsistently defined delayed time-to-surgery. Most studies defined the starting point as the time of pathological diagnosis and chose the tipping point for delayed surgery at or beyond 6 weeks. Outcomes related to the length of the treatment interval are inconsistent, although more than half of the study groups in this overview found a heavily biased association between surgical delay and worse survival. Heterogeneity on several levels impairs thorough analysis of this association.

With unequivocal evidence for a very restrictive window, as in the Dutch guidelines, and growing evidence of opportunities to improve surgical outcomes by prehabilitation, the above-mentioned starting point and timeframe could form a basis for future consensus on defining “timely surgery”, instead of “as soon as possible”, without significantly compromising oncological safety. Defining an interval can reframe waiting time into structured preoperative preparation time, aiming to improve patient outcomes.

Acknowledgments

The authors would like to thank M. Regis, senior statistician at TU Eindhoven, and J.P. Dieleman, epidemiologist at Máxima MC, for their support with possibilities of conducting a meta-analysis.

The authors acknowledge the use of AI-assisted tools, including Microsoft Copilot, that was used solely for language editing and punctuation checking during the preparation of this manuscript. All content, interpretations, and conclusions are the sole responsibility of the authors.

Footnote

Provenance and Peer Review: This article was commissioned by the Guest Editors (Erik R. de Loos, Aimée J. P. M. Franssen and Peter B. Licht) for the series “Current Advances and Innovations in Surgical Lung Cancer Treatment” published in Translational Lung Cancer Research. The article has undergone external peer review.

Reporting Checklist: The authors have completed the PRISMA reporting checklist. Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-688/rc

Peer Review File: Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-688/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-688/coif). The series “Current Advances and Innovations in Surgical Lung Cancer Treatment” was commissioned by the editorial office without any funding or sponsorship. G.D. Slooter received speaker fees from Johnson & Johnson for organizing courses on prehabilitation. Moreover, he is an unpaid board member of the not-for-profit foundation ‘Fit4Surgery’ that aims to facilitate prehabilitation in Dutch hospitals. Lastly, he is an unpaid board member of the ‘iPOETTS’ organization that promotes the professional practice of prehabilitation and exercise testing. The authors have no other conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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