Survival outcomes and risk factors after lung transplantation in patients with pre-transplant malignancy: a national cohort study

Introduction

Background

Lung transplantation (LTx) is the final treatment option for end-stage lung disease and substantially enhances survival and quality of life (1). The necessity for immunosuppressive drugs post-transplantation not only elevates the risk of complications, including infections, but also increases the probability of cancer recurrence. This significantly restricts the eligibility of patients with pre-transplant malignancy (PTM) for transplantation (2-4). Despite these concerns, data from the International Society for Heart and Lung Transplantation (ISHLT) indicate that the percentage of PTM patients is increasing, from 2.7% in the 1990s to 7.9% in 2018 (1). Current guidelines suggest that not all neoplastic diseases are equal and that malignancies with a high risk of recurrence and death are absolute contraindications to LTx (5-7). In contrast, certain tumors, like cutaneous non-melanoma skin cancer, can be managed post-transplantation through active surveillance and intervention (5).

Rationale and knowledge gap

Regarding the prognosis of PTM, existing studies present conflicting results. Some studies indicate that these patients face a higher risk of death within 5 years post-transplantation, often due to cancers that develop after transplantation (8). However, a study by Beaty et al. analyzed data on adult lung transplantation recipients (LTRs) in the United Network for Organ Sharing (UNOS) registry between 2000 and 2011 and found no significant association between PTM and increased 5-year mortality (9). ISHLT 2019 report reveals that post-transplant cancer is the second leading cause of death in patients 5 to 10 years after transplantation (17.3%) and more than 10 years after surgery (17.9%) (10). However, current knowledge of potential risk factors for long-term survival in patients with PTM remains limited. Although LTRs are significantly more likely to develop cancer than the general population (4), patient survival has improved significantly with advances in cancer therapy. Therefore, identifying modifiable risk factors that affect patient survival and cancer progression is crucial for improving patient prognosis (6).

Objective

This study was a systematic analysis using the multicenter UNOS (2005–2022) database with the aim of investigating the survival of PTM patients after LTx and the associated risk factors. We present this article in accordance with the STROBE reporting checklist (available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-224/rc).

Methods

Study methodology and exclusion criteria

This retrospective cohort study included all adult patients (≥18 years) in the UNOS registry who underwent double or single LTx from May 5, 2005 to December 31, 2022. Patients with missing post-transplant follow-up time were excluded. Patients who underwent retransplantation or multi-organ transplantation were excluded. Additionally, patients with missing baseline covariates data, including recipient and donor age, gender, and BMI, and the recipient’s history of PTM, were excluded. Written approval with waiver of informed consent was obtained from the Institutional Review Board of Guangzhou Medical University Medical Center prior to the study. Since the data from UNOS public database is anonymized and publicly available, formal consent from participants was unattainable. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments.

Risk factors and outcome definitions

The study evaluated PTM history as a key risk factor, primary outcomes were all-cause mortality at various periods after transplantation, cancer-specific mortality and risk ratios for specific PTM in patients with PTM. Secondary outcomes included cause-of-death analyses and covariates affecting the prognosis of patients with PTM. PTM were categorized as skin melanoma, non-melanoma skin cancer, genitourinary malignancy, breast or thyroid carcinoma, lung cancer, leukemia, other malignancies (for example, central nervous system malignancy, liver cancer, gastrointestinal malignancy, etc.), and multiple malignancies. Causes of death were defined as graft failure, infection, cardiovascular disease, pulmonary disease, hemorrhage, post-transplant malignancy, multiple organ failure, renal failure, and other. Last follow-up was on December 31, 2022, and patients were classified as surviving or dying after transplantation.

Statistical analysis

Statistical analyses were conducted following rigorous methodological protocols. Normality assessment for continuous variables was performed using skewness-kurtosis evaluation. Parametric data were expressed as mean ± standard deviation and analyzed using Student’s t-test, while non-parametric data were presented as median (interquartile range) with Mann-Whitney U-test implementation. Categorical variables were analyzed separately through frequency distributions (%) employing Fisher’s exact test or χ² test with Yates’ continuity correction, as appropriate for cell frequencies.

Risk factors with P values less than 0.05 in univariate analysis were included in the multivariate model. A P value of less than 0.05 was determined to be statistically significant. All statistical analyses were completed using Stata MP18.0 (College Station, TX, version 18).

Results

Baseline characteristics of study population

The final cohort included 31,615 patients. Of these patients, 28,777 (91%) had no history of PTM, whereas 2,838 (9%) were diagnosed with PTM. The PTM type and frequency of our cohort were summarized, and the most common malignant tumor in PTM patients was skin non-melanoma (30.5%). Followed by breast or thyroid cancer (11.8%), genitourinary malignancy (11.2%), skin melanoma (7.6%), leukemia (6.9%), lung cancer (3.2%) (Figure 1).

Figure 1 An overview of the cohort of patients that were included in the analysis. ^†, recipient and donor age, gender, and BMI, and the recipient’s history of pre-transplant malignancy; ^‡, including central nervous system malignancy, liver cancer, gastrointestinal malignancy. BMI, body mass index; LTx, lung transplantation; UNOS, United Network for Organ Sharing.

Of the 31,615 LTRs included in the analysis, compared to patients without PTM, patients with PTM were older (65 vs. 60 years, P<0.001), had a higher proportion of males (62.8% vs. 60.1%, P=0.006), a higher proportion of white patients (91.2% vs. 78.8%, P<0.001), a shorter pre-transplant waitlist days (43 vs. 50, P<0.001), a higher proportion of single LTx (35.3% vs. 27.9%, P<0.001).

Patients with PTM also had a higher proportion of patients with a smoking history (65.5% vs. 58.8%, P<0.001), a lower proportion of patients with diabetes (16.2% vs. 19.0%, P<0.001), a lower lung allocation score (LAS) score (40.2 vs. 40.9, P<0.001), a lower need for pre-transplant ECMO support (2.6% vs. 4.9%, P<0.001), a higher proportion of pre-transplant interstitial pulmonary fibrosis (IPF) and chronic obstructive pulmonary disease (COPD) diagnoses (42.4% vs. 36.0%, P<0.001; and 24.5% vs. 21.8%, P<0.001), respectively.

Regarding donor characteristics, patients with PTM had older donors (34 vs. 33, P=0.003), and a higher proportion of donors with a smoking history (9.8% vs. 8.6%, P=0.046) and diabetes history (9.1% vs. 7.6%, P=0.003). No statistically significant differences were found in recipients’ BMI between the two groups. Similarly, no significant differences were observed in donor gender, BMI, ischemic time, cause of death, and PTM category between the groups.

The number of patients with PTM and their proportion of the transplant population have been increasing. Between 2005 and 2010, PTM patients accounted for 6.9% of the total LTx population, whereas it reached 8.3% between 2011 and 2016, and the percentage reached 10.8% between 2017 and 2022 (Table 1).

Analysis of all-cause mortality and causes of death

By the end of the study, 15,291 (48.4%) LTRs had died. The median survival time of LTR was 2,275 days [95% confidence interval (CI): 2,237–2,311]. Overall survival was significantly lower in patients with PTM than in those without a history of PTM (P<0.001) (Figure 2). In the unadjusted model, any history of PTM was an important risk factor for overall survival [hazard ratio (HR): 1.23; 95% CI: 1.16–1.30, P<0.001]. After adjusting for factors such as patient age, gender, transplant type, and smoking history, PTM remained an independent risk factor affecting post-transplant overall survival (HR: 1.13; 95% CI: 1.07–1.20, P<0.001) (Table S1). Analysis of survival at various post-transplant periods for patients with and without a history of PTM showed no significant difference in mortality rates between the two groups within 30 and 90 days (30 days: P=0.89, 90 days: P=0.33). Patients with PTM had a significantly higher risk of death than those without PTM at 1 year (P=0.02), and also at 3, 5 and 10 years (P<0.001) after transplantation. In addition, patients with PTM were more likely to die of cancer-specific death (17.4% vs. 11.5%, P<0.001). There was no significant difference in the constituent ratio of other causes of death, such as graft failure, infection, cardiovascular and cerebrovascular diseases (Table 2).

Figure 2 Kaplan-Meier survival curves of overall survival in the stratified study cohort based on the presence of PTM. Lung transplant recipients with PTM faced higher mortality than their counterparts without PTM (log-rank P<0.001). CI, confidence interval; PTM, pre-transplant malignancy.

Risk analysis of 5-year mortality in patients with PTM

In the unadjusted Cox regression analysis, recipient age, gender, BMI, previous smoking history, transplant type, preoperative LAS score, donor age, and previous smoking history of the donor had a significant impact on 5-year mortality in PTM patients after transplantation (P<0.05) (Table 3).

Variables with P<0.05 in univariate Cox analysis were included in multivariate Cox analysis. Through the above univariate and multivariate Cox regression analyses, we ultimately identified four independent risk factors affecting the 5-year survival after transplantation of patients with PTM, which were age (HR: 1.02; 95% CI: 1.01–1.03; P<0.001), male gender (HR: 1.25; 95% CI: 1.09–1.43; P=0.001), single LTx (HR: 1.21; 95% CI: 1.06–1.38; P=0.004), high LAS scores (HR: 1.006; 95% CI: 1.002–1.010; P=0.001) (Table 3).

Evaluation of the impact of PTM on survival rates at various periods after transplantation

After stratification of PTM, there was a significant difference in the 5-year post-transplant survival rate according to the type of PTM (P<0.001) (Figure 3).

Figure 3 Five years Kaplan-Meier survival curve of the study cohort stratified by type of PTM. Lung transplant recipients stratified by type of PTM faced different mortality over 5 years (log-rank P<0.001). PTM, pre-transplant malignancy.

To compare the risk ratios of different PTM types for survival at 1, 3, 5, and 10-year post-transplant, we used a multivariate regression model adjusted for four important risk factors (including recipient age, gender, transplant type, and LAS score) for analysis. The hazard ratios of death at different time points after transplantation for different types of PTM are shown in Figure 4.

Figure 4 Risk of all-cause mortality by period stratified by type of pre-transplant malignancy. Cox models were used to estimate the risk of all-cause mortality, stratified by type of pre-transplant malignancy, over a (A) 1-, (B) 3-, (C) 5-, and (D) 10-year period. CI, confidence interval; HR, hazard ratio.

Compared with no history of malignancy before transplantation, only lung cancer before transplantation was associated with 1-year mortality (HR: 2.19; 95% CI: 1.43–3.37; P<0.001). For mid-term mortality, lung PTM (3-year: HR: 1.77; 95% CI: 1.27–2.46; P=0.001; 5 years: HR: 1.61; 95% CI: 1.19–2.18; P=0.002), leukemia PTM (3-year: HR: 1.33; 95% CI: 1.03–1.72; P=0.03; 5-year: HR: 1.33; 95% CI: 1.07–1.66; P=0.01) showed significant effects. For long-term survival (10-year post-transplant survival), pre-transplant cutaneous melanoma, genitourinary malignancy, lung cancer, leukemia, and multiple malignancies all showed significant effects (Figure 4).

Comparisons between the survival of patients with PTM in different categories are shown in Figure S1 (mainly referring to the difference in survival between patients with pre-transplant lung cancer and other specific malignancies).

Situation and risk analysis of cancer-specific mortality in different PTM patients

The occurrence of cancer-specific mortality varied among patients with different PTM (Table S2). A Cox analysis of patient outcomes for post-transplant deaths due to cancer showed that a history of PTM was a significant risk factor (HR: 1.96; 95% CI: 1.70–2.26; P<0.001). After adjustment for important variables (including LTR age, gender, transplant type, and LAS score), any PTM still had a significant effect on the development of malignancy after transplantation (HR: 1.52; 95% CI: 1.31–1.76; P<0.001) (Table 4). After stratification, cutaneous melanoma (HR: 1.68; 95% CI: 1.08–2.62; P=0.02) cutaneous non-melanoma (HR: 1.48; 95% CI: 1.16–1.90; P=0.002), lung cancer (HR: 3.04; 95% CI: 1.72–5.38; P<0.001), leukemia (HR: 2.41; 95% CI: 1.51–3.85; P<0.001), and multiple malignancies (HR: 1.99; 95% CI: 1.33–2.99; P=0.001) were significantly associated with the occurrence of deaths from malignant tumors. Genitourinary tumors, breast or thyroid cancer, and other malignancies were not statistically significant (Figure S2).

Discussion

In an analysis of 31,615 LTRs, we demonstrated that patients with PTM had a significantly increased risk of all-cause and cancer-specific mortality, with mortality rates significantly higher from 1 year onward compared to patients without PTM. Further analysis identified advanced age, male sex, single LTx, and high LAS score as independent risk factors for 5-year survival in patients with PTM, and these results were consistent with previous findings (8,11). Stratified analyses showed that lung PTM was an independent risk factor affecting mortality in all periods, whereas leukemia PTM had little effect on short-term mortality but a significant effect on mid- and long-term mortality.

Our study reveals a significant upward trend in PTM patient proportion over 17 years. This correlates with the aging transplant population, improved cancer survival rates, and evolving transplant eligibility criteria. The ISHLT published consensus on the evaluation of PTM patients in LTx in 2006, 2014, and 2021 (5,12,13). In 2006, malignancies within 2 years (excluding non-melanoma) were listed as an absolute contraindication, and LTx for localized bronchioalveolar cell carcinoma was considered controversial at that time; improvements in diagnosis and treatment have reduced contraindications for PTM patients. By 2021, only malignancies with high recurrence or high mortality risk were listed as absolute contraindications, with early NSCLC responsive to treatment considered for transplantation after 3 years (6). These changes have increased confidence and opportunities for patients with a malignancy history awaiting LTx.

In our study, the median age of PTM patients was 5 years older than that of non-PTM patients, and the proportion of single LTRs was higher, which may be because single LTx was previously considered a more suitable option for patients over 60 years old due to its lower surgical risk (14,15). Meanwhile, existing studies have shown that for patients over 60 years old, a 5-year age difference is not associated with transplant prognosis (16). Despite these differences, the presence of a PTM history remained an independent risk factor in the Cox analysis adjusted for age, smoking history, and transplant type (Table S1). The proportion of PTM patients requiring ECMO was lower. This may be related to the higher selectivity of PTM patients, meaning that because patients have the high-risk factor of PTM, generally only those in better health are more likely to be listed as candidates and receive transplant opportunities.

On the basis of our cohort, we agree that different PTM have different prognoses (5). Acuna et al. and Beaty et al. conducted relevant studies to analyze the influence of different PTM on patient prognosis (9,17), and Acuna suggested that the presence of PTM and specific malignancy types did not significantly affect the survival at any time. Beaty found that melanoma PTM and hematologic PTM were associated with a high risk of death in overall survival (HR: 1.76; 95% CI: 1.12–2.77; HR: 1.68; 95% CI: 1.15–2.46), respectively, which aligns with our results, but no association between lung PTM and the high risk of death in overall survival was found. However, the former did not include lung PTM as an independent study subject, and the number of patients with lung PTM in the latter study was only 14, so the study error in lung PTM may be large. Our study, which separated lung PTM from solid organ PTM, provides new results: a history of lung cancer before transplantation is an independent risk factor for mortality at all time periods after transplantation, and leukemia PTM is not associated with short-term mortality (within 1 year) but reconfirms its significant impact on medium- and long-term mortality. Additionally, cutaneous melanoma PTM and genitourinary PTM are both associated with long-term mortality.

The high mortality in patients with lung PTM may be attributed to the following factors: First, lung cancer has a poor natural prognosis. Global cancer statistics released in 2022 show that the 5-year survival rate of lung cancer is less than 20% in most countries (18). Second, lung cancer has high rates of local recurrence and distant metastasis. According to our cohort, lung cancer was the most significant predictor of cancer-specific mortality (HR: 3.04, 95% CI: 1.72–5.38). Several hypotheses explain the mechanisms of metastasis and recurrence in cancer patients. The tumor dormancy hypothesis suggests (19): that lung cancer patients may have undetected microscopic metastases, and surgery may disrupt their equilibrium, activating dormant tumor cells and causing recurrence. Presence of hidden cancer cells (20-22): existing studies suggest that patients may have hidden cancer cells that are difficult to detect by conventional testing, leading to underestimation of tumor stage and increased risk of recurrence due to the spread of cancer cells during surgery (20). Additionally, poorer outcomes in the transplant population may reflect the harmful effects of immunosuppression in promoting aggressive tumor development and metastasis, especially since lung recipients often experience the highest levels of immunosuppression (6). Therefore, the high mortality rate after LTx may be related to the natural course of lung cancer, high recurrence and metastasis rates, and the harmful effects of immunosuppression.

This also reminds us that those lung cancer patients with cancer-specific deaths before transplantation in our study may have developed new cancers (especially in the context of older age and higher smoking rates), and it is also very likely that there were unknown metastases before or during transplantation (in addition to local recurrence, there may also be unknown metastases before or during transplantation). Previous studies on recurrent metastasis after radical resection of non-small cell lung carcinoma (NSCLC) in lung cancer, and showed that the percentage of distant metastasis in early to mid-stage NSCLC patients who underwent radical resection ranged from 14–25.5%, while the percentage of local recurrence ranged from 3.2–8.7% (23). Current guidelines recommend that all solid organ transplant candidates with combined lung PTM undergo positron emission tomography-computed tomography (PET-CT) scanning and that the interval between transplants be at least 3 years (6). This emphasizes that patients with lung PTM need to be more accurately identified for the presence of distant metastasis before LTx.

The prognosis of PTM patients is closely related to the characteristics of their malignant tumors and immunosuppressive treatment regimens. However, due to the relatively lower volume of LTxs compared to other transplants and the high variability in treatment plans caused by differences in patient disease characteristics, there is currently a lack of research on more detailed characteristics of PTM patients (such as age at malignant tumor diagnosis before transplantation, staging, treatment regimens, and the exact tumor-free survival period before transplantation) and the impact of different immunosuppressive regimens on LTx prognosis.

However, perhaps we can draw some inferential LTx experience from large studies on solid organ transplantation. Two recent consensus statements discuss how to consider the unique risks associated with PTM to determine whether a patient is a good candidate for transplantation with the recommended disease-free interval (5-7). LTx may be an appropriate option if the type and stage of cancer suggests minimal risk of recurrence and a negative metastatic evaluation. Nevertheless, we cannot ignore the relatively higher risks of LTx and the need for the highest level of immunosuppression. Therefore, future research needs to focus more on the characteristics of malignancies and the impact of immunosuppressive therapy on transplantation, in order to develop more accurate assessment criteria and make precise decisions based on cancer type, malignancy characteristics, patient health status, and transplant feasibility, adjusting the optimal immunotherapy regimen to allow patients to achieve the best benefits.

Previous studies have shown that the most common cancers in recipients after LTx are cutaneous non-melanoma, lung cancer, and post-transplant lymphoproliferative disorders (predominantly non-Hodgkin’s lymphoma) (24-26). Furthermore, Magruder et al. concluded that age, male gender, disease etiology, and single LTx are independently associated with the development of de novo malignancies (DNM) (26). Research on the recurrence of pre-transplant malignancies and the development of new cancers after LTx relies on more advanced detection technologies and requires more transplant cases with detailed transplant data support. Since the recurrence of pre-transplant malignancies and the development of new cancers may correspond to different clinical treatment decisions and prognostic assessments for patients, conducting such research in the future is essential to improve patient prevention and treatment outcomes.

Some limitations must be considered when interpreting these findings. This study is a retrospective analysis using registry data, lacking data related to PTM patient characteristics (such as age at diagnosis of PTM, staging, treatment regimen, and exact malignancy-free survival before transplantation), lacking post-transplant immunosuppression regimens, and limited details on causes of death (cancer-specific deaths were not distinguished between malignant tumor recurrence or second primary malignancy). Secondly, we could not determine whether the intensity of post-transplant follow-up was comparable between the PTM and non-PTM groups, and potential detection bias may have influenced patient prognosis. UNOS may have adjusted and optimized transplant criteria and evaluation methods for certain types of cancer at different times, leading to possible differences in PTM inclusion and classification standards across periods, increasing the uncertainty of the study results. Additionally, like all databases, UNOS relies on accurate coding, and we are limited by data accuracy and potential coding errors.

Conclusions

The prognosis of PTM patients after LTx is worse than that of patients with no PTM. When long-term survival is concerned, patients with a history of lung cancer, leukemia, skin melanoma, and genitourinary system malignant tumors before transplantation need to be selected more carefully. Future research can further explore the influencing factors of the prognosis of LTx in patients with different types of PTM, so that LTx resources can be more optimized, and more patients with end-stage lung disease and PTM history can receive more accurate risk assessment and care.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-224/rc

Peer Review File: Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-224/prf

Funding: This work was supported by the Special Project of Guangzhou National Laboratory (GZNL2023A01003 and GZNL2024A03006).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-224/coif). All authors report that this work was supported by the Special Project of Guangzhou National Laboratory (GZNL2023A01003, GZNL2024A03006). 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. This is a publicly available database that does not contain private information such as patient identity. The Institutional Review Board of the First Affiliated Hospital of Guangzhou Medical University determined that formal ethics approval was not required for this study. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments.

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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