Skip to main content
Download PDF

Homogeneous and heterogeneous risk and prognostic factors for lung metastasis in colorectal cancer patients

BMC Gastroenterology volume 22, Article number: 193 (2022) Cite this article

A Correction to this article was published on 17 May 2022

This article has been updated

Abstract

Background

The lung is one of the most frequent distant metastasis sites in colorectal cancer (CRC) patients; however, lung metastasis risk and prognostic factors have not been comprehensively elucidated. This study aimed to identify the homogeneous and heterogeneous lung metastasis risk and prognostic factors in CRC patients using the Surveillance, Epidemiology, and End Results (SEER) database.

Methods

CRC patients registered in the SEER database between 2010 and 2016 were included to analyse risk factors for developing lung metastasis by using univariable and multivariable logistic regression. Patients diagnosed between 2010 and 2015 were selected to investigate prognostic factors for lung metastasis by conducting Cox regression. Kaplan–Meier analysis was used to estimate overall survival outcomes.

Results

A total of 10,598 (5.2%) patients with synchronous lung metastasis were diagnosed among 203,138 patients with CRC. The median survival time of patients with lung metastasis was 10.0 months (95% CI 9.6–10.5 months). Older age, unmarried status, uninsured status, poor histological differentiation, more lymphatic metastasis, CEA positivity, liver metastasis, bone metastasis and brain metastasis were lung metastasis risk and prognostic factors. Black patients and those with left colon, rectum, and stage T4 disease were more likely to develop lung metastasis, while patients with right colon cancer and no surgical treatment of the primary tumour had poor survival outcomes.

Conclusion

The incidence of lung metastasis in CRC patients was 5.2%. CRC patients with lung metastasis exhibited homogeneous and heterogeneous risk and prognostic factors. These results are helpful for clinical evaluation and individual treatment decision making.

Peer Review reports

Introduction

Colorectal cancer (CRC) has become the third most commonly diagnosed cancer worldwide and is the second leading cause of cancer-related death [1]. Patients with localized stage CRC commonly have a 90% 5-year survival rate; however, the survival rate worsens when the cancer spreads to distant organs [2, 3]. The lung is one of the most common distant metastasis sites in CRC patients. It has been reported to be the second most common metastatic site [3, 4]. Previous studies revealed that the incidence of lung metastasis in CRC patients ranges from 2.40 to 11.0% [5, 6]. Early detection of the high-risk population susceptible to lung metastasis is important for clinical decision-making. Chest CT, 18F-FDG-PET/CT, puncture biopsy through the wall of the chest, and bronchoscopy are commonly applied for the detection of lung metastasis [7, 8]. However, these examinations commonly involve exposure to radioactivity and are invasive and expensive, increasing the economic burden on patients. Therefore, it is necessary to identify risk factors to improve lung metastasis screening in CRC patients.

CRC patients with lung metastasis usually have poor survival outcomes. A previous study revealed that the 1-year cause-specific survival rate of CRC patients with and without lung metastasis was 55.5% and 90.2%, respectively, which was worse than that of patients with liver metastasis [3]. CRC patients with different pathological or clinical characteristics usually show different prognoses. Although some studies have investigated the risk factors for distant metastases (such as liver metastasis) in CRC, the lung metastasis risk and prognostic factors are still unclear [6, 9], and homogeneous and heterogeneous lung metastasis risk and prognostic factors have not been explored. Identifying these specific factors associated with lung metastasis will help clinicians identify high-risk patients.

The purpose of this study was to analyse the risk factors for lung metastasis and estimate the lung metastasis-associated prognosis in patients newly diagnosed with CRC based on data from the Surveillance, Epidemiology, and End Results (SEER) database. We further identified the heterogeneous and homogeneous risk and prognostic factors.

Methods

Population

In this population-based study, CRC patient data were acquired from a US National Cancer Institute (NCI) open public database, the SEER database. SEER*Stat version 8.3.5 (https://seer.cancer.gov/seerstat/) (Information Management Service, Inc. Calverton, MD, USA) was used to generate the patient list. CRC patients diagnosed with lung metastasis between 2010 and 2016 were included in this study. Patients who were diagnosed at autopsy or via a death certificate were excluded. Patients with unspecified follow-up, a primary tumour outside of the colorectal region, and unavailable lung metastasis information were excluded. A flowchart showing the patient inclusion and exclusion process is presented in Fig. 1. Patients newly diagnosed with CRC between 2010 and 2016 were used to analyse lung metastasis risk factors, and patients diagnosed from 2010 to 2015 with a follow-up of at least 1 year were used to investigate the overall survival rate after lung metastasis.

Fig. 1
figure 1

Flowchart of colorectal cancer patient selection

Full size image

Statistical analysis

This study included the following variables: age (< 50, 51–60, 61–70, 71–80, 81–90, ≥ 91); sex (male and female); race (white, black, other (American Indian/Alaska Native and Asian or Pacific Islander); marital status (unmarried and married); insurance status (uninsured and insured); site of primary tumour (left colon, right colon and rectum); histological types (Grade I, Grade II, Grade III, Grade IV); N stage (N0, N1, N2); T stage (T1, T2, T3, T4); carcinoembryonic antigen (CEA) (negative, positive); without or with liver metastasis; without or with bone metastasis; without or with brain metastasis; and surgical treatment for the primary cancer (yes or no).

Quantitative data are presented as the mean ± standard deviation (SD), and categorical data are described as numbers and percentages (N, %). Univariate and multivariate logistic regression were used to identify the factors associated with synchronous lung metastasis. The Kaplan–Meier method was used to estimate overall survival outcomes. Univariate and multivariate Cox regression analyses were conducted to identify potentially associated prognostic factors. Statistically significant levels were two-tailed and set at P < 0.05. Statistical analyses were conducted with the IBM Statistical Package for the Social Sciences (SPSS) version 23.0 software package for Windows (SPSS, Inc., Chicago, IL, USA). MedCalc 18.0 was used to generate survival curves.

Results

Patient characteristics

A total of 203,138 CRC patients were initially identified between 2010 and 2016. Of these patients, 10,598 (5.2%) patients were initially diagnosed with lung metastasis, and 192,540 (94.8%) patients were without lung metastasis. The mean age of all patients was 64.88 ± 14.32 years. A total of 105,727 (52.0%) patients were male. A total of 51.3% were married (N = 104,171). Over half of the patients were white (76.7%, N = 155,877). Most patients were insured (83.0%, N = 168,577). Regarding the site of the primary tumour, 40.3% (N = 81,903) of cancers were located in the right colon, 33.3% (N = 67,565) were in the left colon, and 23.5% (N = 47,660) were in the rectum. Most CRC patients were diagnosed at grade III (59.1%, N = 111,971), N0 (58.5%, N = 118,929) and stage T3 (41.7%, N = 84,747). The detailed demographic and clinical characteristics are displayed in Table 1.

Table 1 Logistic regression for characteristics to develop initial lung metastasis in patients with colorectal cancer (diagnosed 2010–2016)
Full size table

Risk factors for developing lung metastasis

The univariate logistic regression analysis showed that age, sex, race, marital status, insurance status, primary site, histological grade, lymphatic metastasis, T stage, CEA, liver metastasis, bone metastasis and brain metastasis were all correlated with the occurrence of lung metastasis. The multivariate logistic regression confirmed that older age, black race, unmarried status, uninsured status, site, poor histological differentiation, more lymphatic metastasis, T4/T1 stage, CEA positivity and liver metastasis, bone metastasis and brain metastasis were associated with lung metastasis (see Table 1). Only sex was not significantly associated with lung metastasis. After excluding stage T1 and stage T2 CRC patients, there were only 143,054 patients remaining. Univariate and multivariate logistic regression analyses were then performed, which revealed that most of the factors were still risk factors for metastasis, and only sex was not significantly associated with lung metastasis. The results are shown in the Additional file 1: Table S1. These data are consistent with the results obtained when stage T1 and stage T2 CRC patients were not excluded (see Table 1).

Survival estimation and prognostic factors for lung metastasis

A total of 8,867 CRC patients diagnosed with lung metastasis between 2010 and 2015 were included to estimate survival and identify prognostic factors. The median survival of CRC patients with lung metastasis was 10.0 months (95% CI 9.6–10.5 months). The 1-year, 3-year, and 5-year survival rates for lung metastasis patients were 44.3%, 13.5%, and 5.2%, respectively. When the cancers were located in the right colon or had poorly differentiated grade, were CEA positive, or involved different metastatic organs, the median survival of lung metastasis patients was reduced (see Table 2). CRC patients with lung metastasis who received surgery had longer median survival times than those who did not have surgery (19.0 months vs. 7.0 months, P < 0.001). Kaplan–Meier analysis was performed for CRC patients with lung metastasis (Fig. 2A, overall). The overall survival outcomes of patients stratified by age (Fig. 2B), sex (Fig. 2C), race (Fig. 2D), marital status (Fig. 2E), insurance status (Fig. 2F), primary site (Fig. 2G), grade (Fig. 2H), lymphatic metastasis (Fig. 2I), T stage (Fig. 2J), CEA (Fig. 2K), liver metastasis (Fig. 2L), bone metastasis (Fig. 2M), brain metastasis (Fig. 2N), and surgical treatments of the primary site (Fig. 2O) are shown in Fig. 2.

Table 2 Cox regression for analyzing the mortality among lung metastasis patients in colorectal cancer (diagnosed 2010–2015)
Full size table
Fig. 2
figure 2

Kaplan–Meier analysis of overall survival for colorectal cancer patients with lung metastasis. Overall (A), age (B), sex (C), race (D), marital status (E), insurance status (F), primary site (G), grade (H), lymphatic metastasis (I), T stage (J), CEA (K), liver metastasis (L), bone metastasis (M), brain metastasis (N), and surgical treatments of the primary site (O)

Full size image

The univariate analysis suggested that older age, unmarried status, insurance status, right colon, poor histological differentiation, N stage, T stage, CEA positivity, liver metastasis, bone metastasis, brain metastasis and no surgical treatments of the primary tumour were associated with poor prognosis. Multivariable Cox regression confirmed that older age, unmarried status, uninsured status, right colon, poor histological differentiation, more lymphatic metastasis, positive CEA, liver metastasis, bone metastasis, brain metastasis and no surgical treatments of the primary tumour were all risk factors for poorer prognosis. See Table 2 for more details.

Homogeneous and heterogeneous risk and prognostic factors

According to the results of multivariable logistic regression and multivariable Cox regression analyses, the homogeneous lung metastasis risk and prognostic factors in CRC were older age, unmarried status, uninsured status, poor histological differentiation, more lymphatic metastasis, CEA positivity, liver metastasis, bone metastasis, and brain metastasis. However, patients with black race, left colon, rectum, and T4 stage disease were more likely to develop lung metastasis, while patients with right colon disease without surgical treatment of primary tumours had poor survival outcomes (Fig. 3).

Fig. 3
figure 3

Homogeneous and heterogeneous risk factors for the occurrence and prognosis of synchronous lung metastasis in colorectal cancer

Full size image

Discussion

We investigated the incidence of synchronous lung metastasis in newly diagnosed CRC patients using SEER database information. Synchronous lung metastasis occurred in 5.2% of CRC patients. This incidence was lower than those reported in Mitry’s study (11.3%) [5] and Yahagi’s study (6.9%) [10] but higher than those reported in Huang’s study (2.4%) [6]. This is presumably due to the different sample sizes of the study population. In addition, the SEER database only records confirmed patients who have been comprehensively evaluated, and some asymptomatic patients may be missed. Therefore, the incidence in this study may be underestimated.

Accurately identifying the population at high risk for lung metastasis is helpful for subsequent individualized treatment. Our results showed that patients with older age, black race, left colon, rectum, poorly differentiated grade, more lymphatic metastasis, T4 stage, CEA positivity and liver metastasis, bone metastasis and brain metastasis were more likely to develop lung metastasis. Given that stage T1 and stage T2 CRC patients have much lower risk of metastasis, another univariate and multivariate logistic regression analyses were performed which only included patients with stage T3 and stage T4 CRC (see Additional file 1: Table S1). We found the results were comparable when the sample was restricted to stages T3 and stage T4 patients. This also suggests that it is necessary to screen lung metastasis in CRC patients with higher T stage. In addition, unmarried and uninsured patients were also at high risk for lung metastasis. Nevertheless, previous studies did not investigate the impact of marital status and insurance status on the incidence of lung metastasis [5, 6]. A 30-year population-based study found that only the primary site of CRC was significantly associated with synchronous lung metastasis [5]. The results of another study are similar to ours, except for marital status and insurance status [6]. Therefore, the relationship between marital status, insurance status, and lung metastasis incidence warrants further investigation. Regardless, patients with the above risk factors are recommended for lung metastasis screening.

In addition to risk factors, identifying prognostic factors is important in cancer management. We found 11 prognostic factors, including older age, unmarried status, insurance status, right colon, poor histological differentiation, more lymphatic metastasis, CEA positivity, liver metastasis, bone metastasis, brain metastasis and no surgery. Surprisingly, there was no significant correlation between T stage and prognosis of lung metastasis patients, which was consistent with the findings of Huang’s study [6]. Notably, the survival time in patients with stage T1 disease was lower than that in patients with stage T2 to T4 disease. In addition, T stage was found to be a prognostic factor in the univariate Cox regression, while it became a nonsignificant factor in the multivariate Cox regression. T stage has also been found not to be a prognostic factor in patients with brain metastasis [11]. Therefore, we conclude that T stage cannot be used to estimate survival in CRC patients. However, T stage has been reported as an independent prognostic factor in CRC patients with liver metastasis or bone metastasis [9, 12]. Accordingly, the relationship between T stage and the prognosis of distant metastases in CRC patients is still controversial and requires further investigation.

Based on the analysis of risk and prognostic factors, the most important findings in this research were the nine homogeneous factors. To the best of our knowledge, this is the first report to describe the homogeneous factors associated with lung metastasis in CRC patients. These factors can be used to predict the occurrence of lung metastasis, estimate the prognosis, and improve lung metastasis screening for CRC patients. Among the nine homogeneous factors, different metastatic organs ranked much higher in both odds ratio and hazard ratio. Liver metastasis ranked highest, followed by bone metastasis and brain metastasis, indicating that lung metastasis was closely related to liver metastasis. One previous study found that the expression of several key genes plays an important role in determining the distant metastasis of CRC to these two organs [13, 14]. However, the specific molecular mechanisms by which CRC cells affect the liver and lung remain unclear and need to be further studied [15]. Nonetheless, our results suggest that routine liver scanning is necessary for patients with lung metastatic CRC.

In terms of heterogeneous factors, we found that patients with tumours located in the left colon and rectum were more likely to develop lung metastasis, which was consistent with the results of Qiu’s study [3]. The results of this study also showed that patients with lung metastasis from right colon cancer had worse survival than those with metastasis from left colon cancer. This finding is also consistent with the results of previous studies [16,17,18]. In addition to the primary site, surgical treatment is another heterogeneous factor. Patients who underwent surgical resection of the primary tumour survived longer than those who did not [19]. Some studies have shown that resection of lung metastasis also has a positive effect on improving survival outcomes [20,21,22,23]. Therefore, surgical resection of both the primary tumour and the metastasis is an effective measure for CRC patients with lung metastasis.

This study has some limitations. Only patients with synchronous lung metastasis were studied, and the incidence and prognosis of patients with metachronous lung metastasis are still unclear. Meanwhile, the incidence of lung metastasis may be underestimated. In addition, since other important information, including chemotherapy and radiotherapy, was not available from the SEER database, their impact on survival in CRC patients still needs to be further studied. Despite these limitations, our study based on a large cohort of CRC patients demonstrated homogeneous and heterogeneous risk and prognostic factors for lung metastasis. These findings may be helpful for clinicians to identify high-risk patients and improve lung metastasis screening for CRC patients.

Conclusion

In this study, we found that the incidence of lung metastasis in CRC patients was 5.2%, and the median survival of CRC patients with lung metastasis was 10.0 months. Some lung metastasis risk and prognostic factors were found. A total of nine homogeneous risk factors and several heterogeneous factors were identified. These results are helpful for clinicians to conduct clinical evaluations and individualize treatment strategies.

Availability of data and materials

The data that support the fndings of this study are available from the corresponding author upon reasonable request.

Change history

Abbreviations

CEA:

Carcinoembryonic antigen

CRC:

Colorectal cancer

NCI:

National Cancer Institute

SEER:

Surveillance, Epidemiology, and End Results

SD:

Standard deviation

SPSS:

Statistical Package for the Social Sciences

References

  1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424.

    Article  Google Scholar 

  2. American Cancer Society. Cancer Facts & Figures 2021 [updated 2021. Atlanta; 2021. Available from: https://www.cancer.org/content/dam/cancer-org/research/cancer-facts-and-statistics/annual-cancer-facts-and-figures/2021/cancer-facts-and-figures-2021.pdf.

  3. Qiu M, Hu J, Yang D, Cosgrove DP, Xu R. Pattern of distant metastases in colorectal cancer: a SEER based study. Oncotarget. 2015;6(36):38658–66.

    Article  Google Scholar 

  4. Luo T, Wang Y, Shan X, Bai Y, Huang C, Li G, Wang H. Nomogram based on homogeneous and heterogeneous associated factors for predicting distant metastases in patients with colorectal cancer. World J Surg Oncol. 2021;19(1):30.

    Article  Google Scholar 

  5. Mitry E, Guiu B, Cosconea S, Jooste V, Faivre J, Bouvier AM. Epidemiology, management and prognosis of colorectal cancer with lung metastases: a 30-year population-based study. Gut. 2010;59(10):1383–8.

    Article  Google Scholar 

  6. Huang Y, Zhao M, Yin J, Lu T, Yang X, Yuan G, et al. Pulmonary metastasis in newly diagnosed colon-rectal cancer: a population-based nomogram study. Int J Colorectal Dis. 2019;34(5):867–78.

    Article  Google Scholar 

  7. Jung HN, Chung MJ, Koo JH, Kim HC, Lee KS. Digital tomosynthesis of the chest: utility for detection of lung metastasis in patients with colorectal cancer. Clin Radiol. 2012;67(3):232–8.

    Article  CAS  Google Scholar 

  8. Kodama H, Yamakado K, Takaki H, Suzawa N, Yamada T, Takeda K. Impact of 18F-FDG-PET/CT on treatment strategy in colorectal cancer lung metastasis before lung radiofrequency ablation. Nucl Med Commun. 2013;34(7):689–93.

    Article  Google Scholar 

  9. Tang M, Wang H, Cao Y, Zeng Z, Shan X, Wang L. Nomogram for predicting occurrence and prognosis of liver metastasis in colorectal cancer: a population-based study. Int J Colorectal Dis. 2021;36(2):271–82.

    Article  Google Scholar 

  10. Yahagi M, Tsuruta M, Hasegawa H, Okabayashi K, Toyoda N, Iwama N, Morita S, Kitagawa Y. Smoking is a risk factor for pulmonary metastasis in colorectal cancer. Colorectal Dis. 2017;19(9):O322–8.

    Article  CAS  Google Scholar 

  11. Michl M, Thurmaier J, Schubert-Fritschle G, Wiedemann M, Laubender RP, Nuessler NC, et al. Brain metastasis in colorectal cancer patients: survival and analysis of prognostic factors. Clin Colorectal Cancer. 2015;14(4):281–90.

    Article  Google Scholar 

  12. Li X, Hu W, Sun H, Gou H. Survival outcome and prognostic factors for colorectal cancer with synchronous bone metastasis: a population-based study. Clin Exp Metastasis. 2021;38(1):89–95.

    Article  CAS  Google Scholar 

  13. Tang L, Lei YY, Liu YJ, Tang B, Yang SM. The expression of seven key genes can predict distant metastasis of colorectal cancer to the liver or lung. J Dig Dis. 2020;21(11):639–49.

    Article  CAS  Google Scholar 

  14. Pereira AA, Rego JF, Morris V, Overman MJ, Eng C, Garrett CR, et al. Association between KRAS mutation and lung metastasis in advanced colorectal cancer. Br J Cancer. 2015;112(3):424–8.

    Article  CAS  Google Scholar 

  15. Urosevic J, Garcia-Albéniz X, Planet E, Real S, Céspedes MV, Guiu M, et al. Colon cancer cells colonize the lung from established liver metastases through p38 MAPK signalling and PTHLH. Nat Cell Biol. 2014;16(7):685–94.

    Article  CAS  Google Scholar 

  16. Benedix F, Kube R, Meyer F, Schmidt U, Gastinger I, Lippert H, Colon/Rectum Carcinomas Study G. Comparison of 17,641 patients with right- and left-sided colon cancer: differences in epidemiology, perioperative course, histology, and survival. Dis Colon Rectum. 2010; 53(1):57–64.

  17. Zhou Z, Mo S, Dai W, Xiang W, Han L, Li Q, et al. Prognostic nomograms for predicting cause-specific survival and overall survival of stage I-III colon cancer patients: a large population-based study. Cancer Cell Int. 2019;19(1):355.

    Article  CAS  Google Scholar 

  18. Hansen IO, Jess P. Possible better long-term survival in left versus right-sided colon cancer—a systematic review. Dan Med J. 2012;59(6):A4444.

    PubMed  Google Scholar 

  19. Zong Z, Zhou TC, Tang FX, Tian HK, Wang A, Yi CH. Impact of site-specific metastases on surgical value and survival among metastatic colorectal cancer patients. Am Surg. 2020;86(3):220–7.

    Article  Google Scholar 

  20. Tampellini M, Ottone A, Bellini E, Alabiso I, Baratelli C, Bitossi R, et al. The role of lung metastasis resection in improving outcome of colorectal cancer patients: results from a large retrospective study. Oncologist. 2012;17(11):1430–8.

    Article  Google Scholar 

  21. Hishida T, Tsuboi M, Okumura T, Boku N, Ohde Y, Sakao Y, et al. Does repeated lung resection provide long-term survival for recurrent pulmonary metastases of colorectal cancer? Results of a retrospective Japanese Multicenter Study. Ann Thorac Surg. 2017;103(2):399–405.

    Article  Google Scholar 

  22. Davini F, Ricciardi S, Zirafa CC, Romano G, Alì G, Fontanini G, Melfi FMA. Lung metastasectomy after colorectal cancer: prognostic impact of resection margin on long term survival, a retrospective cohort study. Int J Colorectal Dis. 2020;35(1):9–18.

    Article  Google Scholar 

  23. Gonzalez M, Robert JH, Halkic N, Mentha G, Roth A, Perneger T, Ris HB, Gervaz P. Survival after lung metastasectomy in colorectal cancer patients with previously resected liver metastases. World J Surg. 2012;36(2):386–91.

    Article  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the National Cancer Institute for providing the SEER dataset.

Funding

This project was supported by the Innovation Research Group in Colleges and Universities Program of Chongqing Municipal Education Commission (No. CXQT20012) and the Postgraduate Tutor Team Development Program of Chongqing Municipal Education Commission (No. dstd201807).

Author information

Author notes

  1. Hongmei Wang and Xuefeng Shan contributed equally to this work and should both be considered first authors

Authors and Affiliations

  1. Department of Pharmacology, College of Pharmacy, Chongqing Medical University, 1 Yixueyuan Road, Yuzhong District, Chongqing, 400016, China

    Hongmei Wang & Weiying Zhou

  2. Chongqing Key Laboratory of Drug Metabolism, Chongqing Medical University, Chongqing, 400016, China

    Hongmei Wang & Weiying Zhou

  3. Key Laboratory for Biochemistry and Molecular Pharmacology of Chongqing, Chongqing Medical University, Chongqing, 400016, China

    Hongmei Wang & Weiying Zhou

  4. Department of Pharmacy, The First Affiliated Hospital of Chongqing Medical University, Chongqing, 400016, China

    Hongmei Wang & Xuefeng Shan

  5. Department of Epidemiology and Health Statistics, School of Public Health and Management, Chongqing Medical University, Chongqing, 400016, China

    Min Zhang

  6. Department of Gastrointestinal Surgery, The First Affiliated Hospital of Chongqing Medical University, Chongqing, 400016, China

    Kun Qian

  7. Department of Pharmacy, Yongchuan Hospital of Chongqing Medical University, 439 Xuanhua Road, Yongchuan District, Chongqing, 402160, China

    Zhengze Shen

Authors
  1. Hongmei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xuefeng Shan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Min Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kun Qian
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhengze Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Weiying Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

HW, XS, MZ: Research design, data collection, interpretation and analysis, manuscript drafting. KQ, ZS, WZ: Research design, data analysis, results interpretation, paper writing, and critical manuscript revision. All authors contributed to the data analyses and the drafting and revising of the paper and agree to be accountable for all aspects of the work. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Zhengze Shen or Weiying Zhou.

Ethics declarations

Ethics approval and consent to participate

As the data used was from SEER which is an open public database, the present study was exempt from the ethical review of the ethics board of the First Affiliated Hospital of Chongqing Medical University. The present study complied with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no conflicts of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Additional file 1

. Table S1. Logistic regression for characteristics to develop initial lung metastasis in patients with colorectal cancer (excluding stage T1 and stage T2 patients).

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visithttp://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, H., Shan, X., Zhang, M. et al. Homogeneous and heterogeneous risk and prognostic factors for lung metastasis in colorectal cancer patients. BMC Gastroenterol 22, 193 (2022). https://0-doi-org.brum.beds.ac.uk/10.1186/s12876-022-02270-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://0-doi-org.brum.beds.ac.uk/10.1186/s12876-022-02270-5

Keywords

BMC Gastroenterology

ISSN: 1471-230X

Contact us