Impact of different visceral metastatic sites on survival in metastatic prostate cancer patients

Abstract

Introduction

Visceral metastasis is an important predictor for poor outcomes in prostate cancer, however, the prognostic significance surrounding the specific sites of visceral metastasis remains unclear. The aim of this study was to evaluate the impact of different visceral metastatic sites on survival in patients with prostate cancer.

Methods

We identified patients with metastatic prostate cancer between January 1, 2010 and December 31, 2023 using the TriNetX database. Patients were divided into 4 cohorts according to their specific metastatic sites: lung metastases, brain metastases, liver metastases, and bone metastases. Survival analysis was calculated using the Kaplan-Meier method and Cox regression models.

Results

In total, 59,875 patients diagnosed with metastatic prostate cancer were identified, with 39,495 (65.2%) having bone metastases, 7,573 (12.5%) lung metastases, 5,240 (8.7%) brain metastases, and 7,567 (12.5%) liver metastases. The median overall survival was 44.4 months for patients with bone metastases, 31.9 months for lung metastases, 9.6 months for brain metastases, and 10 months for liver metastases. Lung metastases were associated with an improved survival when compared with liver and brain metastases. For patients with two visceral metastatic sites or concomitant bone metastases, liver metastases were related to worse outcomes. Asian patients experienced better OS than Caucasian and African American patients in visceral metastatic prostate cancer.

Conclusion

Patients with lung metastases experienced better survival outcomes in prostate cancer with only one visceral metastatic site. Liver metastases were associated with worse outcomes when there were two visceral metastatic sites combined or concomitant bone metastases. Asian patients displayed improved survival rates when compared with both Caucasian and African American patients in visceral metastatic prostate cancer.

Introduction

Prostate cancer is the fourth most frequently diagnosed cancer in men and the eighth leading cause of cancer death worldwide. More than 1.4 million prostate cancer cases were diagnosed, with 397,430 patients dying of the disease in 2022 [1]. Although there are good survival outcomes for those with localized disease, the risk of death still remains high for metastatic prostate cancer (mPC) patients. Several studies have demonstrated the adverse impact of visceral metastases on overall survival (OS) for patients with metastatic prostate cancer (mPC) [2–13]. However, information regarding the significance of specific visceral metastases on patient prognosis remains scarce. A meta-analysis taken from randomized clinical trials conducted by Halabi et al. identified lung and liver metastases, when compared with bone and other non-visceral metastases, as being risk factors for poor prognosis in patient diagnosed with metastatic castration resistant prostate cancer (mCRPC) [9]. Tappero et al., in a population-based analysis, reported on there being better outcomes for patients with lung metastases when compared with other visceral metastases [13]. Despite the results of these studies, there remains limited data regarding the prognostic significance of specific metastatic sites for patient diagnosed with metastatic prostate cancer.

Herein, we performed a retrospective analysis using the TriNetX database in order to investigate the influence of specific sites of visceral metastases on overall survival in metastatic prostate cancer patients. We also evaluated the outcomes of visceral metastases with regard to different non-visceral metastases, as well as to race.

Methods

Data source, study population, and outcomes

We utilized the TriNetX network to conduct a retrospective analysis. Data were retrieved from the US Collaborative Network, which includes 57 healthcare organizations across the United States. Data collection and analysis for this research were performed on the TriNetX platform in February, 2024.

Through the network we identified patients aged ≥18 years who had been diagnosed with mPC during the period of January 1, 2010 and December 31, 2023. The diagnosis of mPC was performed according to the International Classification of Diseases, tenth edition, Clinical Modification (ICD-10-CM): ICD-10-CM C61, as well as ICD-10-CM: C77, C78, C78.7, C79.3, or C79.5 in order to confirm the distant metastases. The index date was set to be the date of diagnosis of distant metastasis. Patients enrolled were divided into 3 cohorts according to the sites of visceral metastases: brain, liver, and lung metastasis, while patients with bone metastasis without visceral metastases were included for comparison. Enrolled patients could either have or not have non-visceral metastasis. The primary end point was OS, which was calculated from the date of diagnosis of distant metastases (the index date) to the date of death or censored at the end of the study, whichever occurred first. We also performed survival analyses for patients with mPC among different races and concomitant non-visceral metastases.

Statistical analyses

For analyzing patients baseline characteristics, mean with standard deviation (SD) was utilized for continuous variables, and number with percentage for categorical variables. Kaplan-Meier survival analysis along with the log-rank test and Cox proportional regression model were used for the evaluation of OS among the different cohorts. All statistical analyses were performed on the TriNetX network with a p value <0.05 being considered statistically significant.

Ethics in research

This research was carried out after receiving approval from the Institutional Review Board (IRB) of Taichung Veterans General Hospital (IRB number: SE:22220A). Given the TriNetX platform provides only de-identified data, the ethics committee approved a waiver of informed consent.

Results

Demographics and characteristics

A total of 59,875 patients with metastatic prostate cancer were identified on the TriNetX database. Of them, 39,495 (65.2%) had bone metastases, 7,573 (12.5%) lung only visceral metastases, 5,240 (8.7%) brain only visceral metastases, and 7,567 (12.5%) liver only visceral metastases. Compared to the patients in the bone metastases cohort, patients in the visceral metastases cohort were at a significantly younger age, possessed a poor Eastern Cooperative Oncology Group (ECOG) performance status, and had more lymph node metastases, comorbidities, and a higher proportion of receiving novel hormone agents or chemotherapy. Patient demographics and characteristics are demonstrated in Table 1.

[Figure omitted. See PDF.]

Outcomes of overall population and different visceral metastatic sites

The median OS for mPC patients with visceral metastases was 15.7 months [95% confidence interval (CI) 15–16.2] and the survival probability at the 12^th month was 24.7% (95% CI 54.1–55.5).

The median OS was 44.4 months (95% CI 43.1–45.5) for patients with bone metastases, 31.9 months (95% CI 29.8–34.4) for lung metastases, 9.6 months (95% CI 8.9–10.4) for brain metastases, and 10 months (95% CI 9.4–10.6) for liver metastases. In the bone metastases cohort, the survival probability at the 12^th month was 72.2% (95% CI 76.7–77.7), 66.4% (95% CI 65.3–67.5) for the lung metastases cohort, 46.3% (95% CI 44.9–47.7) for the brain metastases cohort, and 46.2% (95% CI 45–47.4) for the liver metastases cohort (Fig 1 and S1 File). In Cox regression models, for patients with one site of visceral metastases, mPC patients with brain [Hazard ratio (HR) 1.692, 95% CI 1.623–1.765, p<0.0001] and liver metastases (HR 1.671, 95% CI 1.595–1.749, p<0.0001) experienced a poorer prognosis when compared to the lung metastases patients. There was no statistical difference seen in OS between the brain and liver metastases cohorts (Table 2).

[Figure omitted. See PDF.]

CI: confidence interval; OS: overall survival.

[Figure omitted. See PDF.]

Impact of two visceral metastatic sites on outcomes

We subsequently evaluated the outcomes for mPC patients who had two visceral metastases. The median OS was 8 months (95%CI 6.8–9.2) for patients with brain + lung metastases, 6.6 months (95%CI 5.8–7.4) for liver + lung metastases, and 3.1 months (95% CI 2.4–3.8) for liver + brain metastases (Fig 2 and S2 File). In Cox regression models, patients diagnosed with brain + lung metastases experienced better outcomes when compared to the liver + lung metastases (HR 1.138, 95% CI 1.054–1.23, p<0.0001) and liver + brain metastases patients (HR 1.707, 95% CI 1.529–1.906, p<0.0001). Moreover, liver + brain metastases (HR 1.488, 95% CI 1.349–1.64, p<0.0001) were associated with a poor OS when compared to liver + lung metastases (Table 2).

[Figure omitted. See PDF.]

CI: confidence interval; OS: overall survival.

Impact of concomitant non-visceral metastases on outcomes

In mPC patients with visceral metastases and concomitant bone metastases, median OS was 17 months (95% CI 14.5–19.1) for lung + bone metastases, 8.2 months (95% CI 7.2-.8) for brain + bone metastases, and 5.4 months (95% CI 4.8–6.2) for liver + bone metastases (Fig 3 and S3 File). Patients with liver + bone metastases experienced a worse OS when compared with brain + bone (HR 1.27, 95% CI 1.164–1.138, p<0.0001) and lung + bone metastases patients (HR 1.643, 95% CI 1.524–1.772, p<0.0001) (Table 2).

[Figure omitted. See PDF.]

CI: confidence interval; OS: overall survival.

In mPC patients with visceral metastases and concomitant lymph node metastases, median OS was 42.2 months (95% CI 0.8–54.1) for lung + lymph node metastases, 13.5 months (95% CI 6.9–19.9) for brain + lymph node metastases, and 12.1 months (95% CI 9.9–13.7) for liver + lymph node metastases (Fig 4 and S4 File). Lung + lymph node metastases was shown to be a factor for better OS when compared with brain + lymph node (HR 1.63, 95% CI 1.361–1.952, p<0.0001) and liver + lymph nodes metastases (HR 1.706, 95% CI 1.513–1.922, p<0.0001). There was no significant difference seen in OS between brain + lymph node and liver + lymph node metastases (Table 2).

[Figure omitted. See PDF.]

CI: confidence interval; LN: lymph node; OS: overall survival.

In mPC patients with visceral metastases and concomitant bone and lymph node metastases, median OS was 16 months (95% CI 13.6–18.1) for lung + bone + lymph node metastases, 8 months (95% CI 6.8–10.7) for brain + bone + lymph node metastases, and 5.6 months (95% CI 4.6–6.7) for liver + bone + lymph node metastases (Fig 5 and S5 File). Patients with liver + bone + lymph node metastases experienced a worse survival outcome when compared with both brain + bone + lymph node (HR 1.187, 95% CI 1.056–1.334, p = 0.004) and lung + bone + lymph node metastases (HR 1.641, 95% CI 1.499–1.796, p<0.0001) (Table 2).

[Figure omitted. See PDF.]

CI: confidence interval; LN: lymph node; OS: overall survival.

Impact of race on outcomes

We conducted survival analyses for mPC patients with visceral metastases among different races (Fig 6 and S6 File) and found that Caucasian patients had a poorer OS when compared with African American (HR 0.925, 95% CI 0.881–0.971, p<0.0001) and Asian patients (HR 0.627, 95% CI 0.56–0.702, p<0.0001). Asian patients were associated with an improved survival compared with African American patients (HR 0.681, 95% CI 0.604–0.768, p<0.0001) (Table 2).

[Figure omitted. See PDF.]

CI: confidence interval; OS: overall survival.

Discussion

In his study, we performed a retrospective analysis to compare the impact of specific visceral metastases sites on survival in patients with metastatic prostate cancer in a real-world setting. In patients having one visceral metastatic site with or without lymph node metastases, lung metastases were associated with improved outcomes when compared with brain or liver metastases. When combined with bone metastases or two visceral metastatic sites, liver metastasis was a factor for the worst OS when compared with lung or brain metastases. For OS among different races, Caucasian patients experienced poorer survival, while Asian patients experienced better outcomes.

In this study, we found that mPC patients with liver metastases had a median OS of 10 months. Liver metastases were a factor for worse outcomes than lung and non-visceral metastases. These findings are consistent with the prior studies, which had reported a median OS of 9–14 months for mPC patients with liver metastases, with these patients presenting as a group having a poor prognosis [8–13].

Additionally, we found that patients with lung metastases exhibited a worse OS than those with non-visceral metastases (bone or lymph node). The results are similar to the previous studies and further confirm the poorer outcomes which result from the presence of visceral metastases than those seen in non-visceral metastases [8–12].

Limited data regarding outcomes of prostate cancer with brain metastases have been reported, which may be attributed to the lower incidence of brain metastases. In 2018, Shou et al., in a population-based study using the Surveillance, Epidemiology, and End Results (SEER) database, demonstrated that patients with brain metastases may exhibit better outcomes than those with liver metastases [11]. In 2023, Tappero et al., using the SEER database, reported a poor prognosis for liver and brain metastases when compared with lung metastases, with no difference being seen in survival between liver and brain metastases [13]. In this study, we found that liver and brain metastases were similar in OS for mPC patients with only one visceral metastases site. However, for mPC patients with two visceral metastatic sites or one visceral metastatic site with concomitant bone metastases, brain metastases may be associated with improved survival when compared with liver metastases. These findings may provide clinicians with better risk stratification and evaluation for these patients.

In this study, we found that Asian patients with visceral metastases experienced survival advantages more so than Caucasian and African American patients. This finding is consistent with the available prior literature, which shows Asian patients with metastatic prostate cancer having better OS [14–17]. The differences in genomics, lifestyle and/or treatment responsiveness may have contributed to these results. The survival outcomes seen between African American and Caucasian patients with mPC are controversial. Several studies have reported improved survival rates for African American patients when compared to Caucasian patients when receiving therapies [14, 18–22]. Our study also revealed that African American patients with visceral metastatic prostate cancer exhibited better OS than Caucasian patients. This may be explained by the increased immune response in African American patients during treatments when compared to the Caucasian patients [14].

There were limitations in our study. First, the retrospective design of the present study may have led to selection bias. Second, we could not assess the information regarding disease burden, such as the number or size of a specific visceral metastasis. Third, the detailed data, such as castration sensitive or resistant prostate cancer, BRCA gene mutation status, or family history of prostate cancer, were either not available or inadequate for analysis from the database. Fourth, our research lacked the information on methodology for diagnosis and follow-up, such as computed tomography, magnetic resonance imaging, bone scan or positron emission tomography, and different image tools may affect the diagnostic rate of metastases. Despite these limitations, our analysis included a large population diagnosed with visceral metastatic prostate cancer, and the results may offer clinicians useful information toward predicting a patient’s prognosis or for the better design of trials for these patients.

Conclusion

For prostate cancer patients with visceral metastases, patients with lung metastases experience survival benefits when compared to those with either liver or brain metastases. When combining two visceral metastatic sites or concomitant bone metastases, liver metastases were associated with worse outcomes. Asian patients experienced better OS than both Caucasian and African American patients diagnosed with visceral metastatic prostate cancer.

Supporting information

S1 File. Values for Kaplan-Meier survival analysis in prostate cancer patients with bone or one visceral metastatic site.

https://doi.org/10.1371/journal.pone.0309941.s001

(XLSX)

S2 File. Values for Kaplan-Meier survival analysis in prostate cancer patients with two visceral metastatic sites.

https://doi.org/10.1371/journal.pone.0309941.s002

(XLSX)

S3 File. Values for Kaplan-Meier survival analysis in prostate cancer patients with bone and visceral metastases.

https://doi.org/10.1371/journal.pone.0309941.s003

(XLSX)

S4 File. Values for Kaplan-Meier survival analysis in prostate cancer patients with lymph node and visceral metastases.

https://doi.org/10.1371/journal.pone.0309941.s004

(XLSX)

S5 File. Values for Kaplan-Meier survival analysis in prostate cancer patients with bone, lymph node, and visceral metastases.

https://doi.org/10.1371/journal.pone.0309941.s005

(XLSX)

S6 File. Values for Kaplan-Meier survival analysis among different races in patients with visceral metastatic prostate cancer.

https://doi.org/10.1371/journal.pone.0309941.s006

(XLSX)

Acknowledgments

The data used in this research was from the TriNetX network.

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Citation: Lai G-S, Chen C-S, Cheng JC-H, Li J-R, Yang C-K, Lin C-Y, et al. (2024) Impact of different visceral metastatic sites on survival in metastatic prostate cancer patients. PLoS ONE 19(9): e0309941. https://doi.org/10.1371/journal.pone.0309941

About the Authors:

Gu-Shun Lai

Roles: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Writing – original draft, Writing – review & editing

Affiliations: Institute of Medicine, Chung Shan Medical University, Taichung, Taiwan, Department of Urology, Taichung Veterans General Hospital, Taichung, Taiwan

ORICD: https://orcid.org/0000-0003-1225-9100

Chuan-Shu Chen

Roles: Writing – review & editing

Affiliations: Institute of Medicine, Chung Shan Medical University, Taichung, Taiwan, Department of Urology, Taichung Veterans General Hospital, Taichung, Taiwan, Department of Post-Baccalaureate Medicine, College of Medicine, National Chung Hsing University, Taichung, Taiwan

Jason Chia-Hsien Cheng

Roles: Conceptualization, Writing – review & editing

Affiliation: Division of Radiation Oncology, Department of Oncology, National Taiwan University Hospital, Taipei, Taiwan

Jian-Ri Li

Roles: Methodology, Writing – review & editing

Affiliations: Institute of Medicine, Chung Shan Medical University, Taichung, Taiwan, Department of Urology, Taichung Veterans General Hospital, Taichung, Taiwan, Department of Post-Baccalaureate Medicine, College of Medicine, National Chung Hsing University, Taichung, Taiwan, Division of Radiation Oncology, Department of Oncology, National Taiwan University Hospital, Taipei, Taiwan, Department of Medicine and Nursing, Hungkuang University, Taichung, Taiwan

Cheng-Kuang Yang

Roles: Writing – review & editing

Affiliations: Institute of Medicine, Chung Shan Medical University, Taichung, Taiwan, Department of Urology, Taichung Veterans General Hospital, Taichung, Taiwan, Jenteh Junior College of Medicine, Nursing and Management, Miaoli, Taiwan

Chia-Yen Lin

Roles: Writing – review & editing

Affiliations: Institute of Medicine, Chung Shan Medical University, Taichung, Taiwan, Department of Urology, Taichung Veterans General Hospital, Taichung, Taiwan, College of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan

Sheng-Chun Hung

Roles: Writing – review & editing

Affiliations: Institute of Medicine, Chung Shan Medical University, Taichung, Taiwan, Department of Urology, Taichung Veterans General Hospital, Taichung, Taiwan, Department of Post-Baccalaureate Medicine, College of Medicine, National Chung Hsing University, Taichung, Taiwan

Kun-Yuan Chiu

Roles: Writing – review & editing

Affiliations: Institute of Medicine, Chung Shan Medical University, Taichung, Taiwan, Department of Urology, Taichung Veterans General Hospital, Taichung, Taiwan, Department of Applied Chemistry, National Chi Nan University, Nantou, Taiwan

Shian-Shiang Wang

Roles: Conceptualization, Formal analysis, Methodology, Writing – original draft, Writing – review & editing

E-mail: [email protected]

Affiliations: Institute of Medicine, Chung Shan Medical University, Taichung, Taiwan, Department of Urology, Taichung Veterans General Hospital, Taichung, Taiwan, Department of Applied Chemistry, National Chi Nan University, Nantou, Taiwan

ORICD: https://orcid.org/0000-0003-3032-0198

[/RAW_REF_TEXT]

References

1. Ferlay J, Ervik M, Lam F, et al. Global cancer observatory: cancer today. International Agency for Research on Cancer. Lyon, France https://gco.iarc.fr/today 2024.

2. Armstrong AJ, Garrett-Mayer ES, Yang YCO, et al. A contemporary prognostic nomogram for men with hormone-refractory metastatic prostate cancer: a TAX327study analysis. Clin Cancer Res. 2007;13:6396–6403. pmid:17975152

3. Omlin A, Pezaro C, Mukherji D, et al. Improved survival in a cohort of trial participants with metastatic castration-resistant prostate cancer demonstrates the need for updated prognostic nomograms. Eur Urol. 2013;64:300–306. pmid:23313031

4. Ost P, Decaestecker K, Lambert B, et al. Prognostic factors influencing prostate cancer-specific survival in non-castrate patients with metastatic prostate cancer. Prostate. 2014;74:297–305. pmid:24395565

5. Halabi S, Lin CY, Kelly WK, et al. Updated prognostic model for predicting overall survival in first-line chemotherapy for patients with metastatic castration-resistant prostate cancer. J Clin Oncol. 2014;32:671–677. pmid:24449231

6. Pond GR, Sonpavde G, de Wit R, et al. The prognostic importance of metastatic site in men with metastatic castration-resistant prostate cancer. Eur Urol.2014;65:3–6. pmid:24120464

7. Pezaro CJ, Omlin A, Lorente D, et al. Visceral disease in castration-resistant prostate cancer. Eur Urol. 2014;65:270–273. pmid:24295792

8. Gandaglia G, Karakiewicz PI, Briganti A, et al. Impact of the site of metastases on survival in patients with metastatic prostate cancer. Eur Urol. 2015;68:325–334. pmid:25108577

9. Halabi S, Kelly WK, Ma H, et al. Meta-analysis evaluating the impact of site of metastasis on overall survival in men with castration-resistant prostate cancer. J Clin Oncol. 2016;34:1652–1659. pmid:26951312

10. Mazzone E, Preisser F, Nazzani S, et al. Location of metastases in contemporary prostate cancer patients affects cancer-specific mortality. Clin Genitourin Cancer.2018;16 376–84.e1. pmid:29954690

11. Shou J, Zhang Q, Wang S, Zhang D. The prognosis of different distant metastases pattern in prostate cancer: A population based retrospective study. Prostate. 2018 May;78(7):491–497. Epub 2018 Feb 13. pmid:29436722.

12. Budnik J, Suri J, Bates JE, Bylund KC, Milano MT. Prognostic Significance of Sites of Visceral Metastatic Disease in Prostate Cancer: A Population-based Study of 12,180 Patients. Clin Genitourin Cancer. 2019 Aug;17(4):260–267. Epub 2019 Apr 9. pmid:31101579.

13. Tappero S, Piccinelli ML, Incesu RB, Cano Garcia C, Barletta F, Morra S, et al. Overall Survival of Metastatic Prostate Cancer Patients According to Location of Visceral Metastatic Sites. Clin Genitourin Cancer. 2023 Aug 11:S1558-7673(23)00187-8. Epub ahead of print. pmid:37690970.

14. Freedland SJ, Samjoo IA, Rosta E, Lansing A, Worthington E, Niyazov A, et al. The impact of race on survival in metastatic prostate cancer: a systematic literature review. Prostate Cancer Prostatic Dis. 2023 Sep;26(3):461–474. Epub 2023 Aug 17. pmid:37592001; PMCID: PMC10449629.

15. Würnschimmel C, Wenzel M, Collà Ruvolo C, Nocera L, Tian Z, Saad F, et al. Survival advantage of Asian metastatic prostate cancer patients treated with external beam radiotherapy over other races/ethnicities. World J Urol. 2021 Oct;39(10):3781–3787. Epub 2021 May 12. pmid:33978812; PMCID: PMC8519889.

16. Deuker M, Stolzenbach LF, Pecoraro A, Rosiello G, Luzzago S, Tian Z, et al. PSA, stage, grade and prostate cancer specifi c mortality in Asian American patients relative to Caucasians according to the United States Census Bureau race definitions. World J Urol. 2021;39:787–96. pmid:32458094

17. Ni X, Luu M, Ma W, Zhang T, Wei Y, Freedland SJ, et al. Impact of Asian Race on Prognosis in De Novo Metastatic Prostate Cancer. J Natl Compr Canc Netw. 2023 Jul;21(7):733–741.e3. pmid:37433430.

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19. Zhao H, Howard LE, De Hoedt A, Terris MK, Amling CL, Kane CJ, et al. Racial discrepancies in overall survival among men treated with 223Radium. J Urology. 2020;203:331–7. pmid:31479407

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