Annals of Surgical Oncology

, Volume 20, Issue 12, pp 4022–4030 | Cite as

Indeterminate Pulmonary Nodules at Colorectal Cancer Staging: A Systematic Review of Predictive Parameters for Malignancy

  • Andreas Nordholm-Carstensen
  • Peer A. Wille-Jørgensen
  • Lars N. Jorgensen
  • Henrik Harling
Thoracic Oncology



This study aimed to estimate the prevalence of indeterminate pulmonary nodules and specific radiological and clinical characteristics that predict malignancy of these at initial staging chest computed tomography (CT) in patients with colorectal cancer. A considerable number of indeterminate pulmonary nodules, which cannot readily be classified as either benign or malignant, are detected at initial staging chest CT in colorectal cancer patients.


A systematic review based on a search in EMBASE, Medline, the Cochrane library and science citation index, PubMed databases, Google scholar, and relevant conference proceedings was performed in cooperation with the Cochrane Colorectal Cancer Group.


A total of 2,799 studies were identified, of which 12 studies met the inclusion criteria. The studies primarily consisted of case series and included a total of 5,873 patients. Of these patients, 9 % (95 % confidence interval [95 % CI] 8.9–9.2 %) had indeterminate pulmonary nodules at chest CT, of which 10.8 % (95 % CI 10.3–11.2 %) turned out to be colorectal cancer metastases at follow-up. Generally, regional lymph node metastasis, and multiple numbers of indeterminate pulmonary nodules were reported to predict malignancy, whereas calcification of the nodules indicated benign lesions.


It was found that 1 in 100 colorectal cancer patients subjected to preoperative staging chest CT will have an indeterminate pulmonary nodule that proves to be metastatic disease. Such a low risk suggests that indeterminate pulmonary nodules should not cause further preoperative diagnostic workup or follow-up besides routine regimens.


Chest Computerize Tomography Lung Lesion General Study Population Positive Nodal Status International Clinical Trial Registry Platform 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors thank the Trials Search Coordinator of the Cochrane Colorectal Cancer Group Marija Barbateskovic for her kind assistance in conducting the literature search. The study was financially supported by grants from the Danish Cancer Society, Aase and Ejnar Danielsen’s Foundation, and The Einar Willumsen Foundation.


  1. 1.
    Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.PubMedCrossRefGoogle Scholar
  2. 2.
    Kirke R, Rajesh A, Verma R, Bankart MJ. Rectal cancer: incidence of pulmonary metastases on thoracic CT and correlation with T staging. J Comput Assist Tomogr. 2007;31:569–71.PubMedCrossRefGoogle Scholar
  3. 3.
    Tan KK, Lopes Gde L Jr., Sim R. How uncommon are isolated lung metastases in colorectal cancer? a review from database of 754 patients over 4 years. J Gastrointest Surg. 2009;13:642–8.PubMedCrossRefGoogle Scholar
  4. 4.
    McIntosh J, Sylvester PA, Virjee J, Callaway M, Thomas MG. Pulmonary staging in colorectal cancer–is computerised tomography the answer? Ann R Coll Surg Engl. 2005;87:331–3.PubMedCrossRefGoogle Scholar
  5. 5.
    Grossmann I, Avenarius JK, Mastboom WJ, Klaase JM. Preoperative staging with chest CT in patients with colorectal carcinoma: not as a routine procedure. Ann Surg Oncol. 2010;17:2045–50.PubMedCrossRefGoogle Scholar
  6. 6.
    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;59:1383–8.PubMedCrossRefGoogle Scholar
  7. 7.
    National Comprehensive Cancer Network. NCCN clinical practice guidelines in oncology rectal cancer. 2013. Accessed Apr 2, 2013.
  8. 8.
    National Comprehensive Cancer Network. NCCN clinical practice guidelines in oncology colon cancer. 2013. Accessed Apr 2, 2013.
  9. 9.
    The Danish Colorectal Cancer Group. Guidelines for the Management of Colorectal Cancer. 2010. Accessed Feb 2, 2013. In Danish.
  10. 10.
    The Association of Coloproctology of Great Britain and Ireland. Guidelines for the Management of Colorectal Cancer. 2007. Accessed Feb 8, 2013.
  11. 11.
    Griffiths EA, Browell DA, Cunliffe WJ. Evaluation of a pre-operative staging protocol in the management of colorectal carcinoma. Colorectal Dis. 2005;7:35–42.PubMedCrossRefGoogle Scholar
  12. 12.
    Arulampalam TH, Costa DC, Loizidou M, Visvikis D, Ell PJ, Taylor I. Positron emission tomography and colorectal cancer. Br J Surg. 2001;88:176–89.PubMedCrossRefGoogle Scholar
  13. 13.
    Davis SD. CT evaluation for pulmonary metastases in patients with extrathoracic malignancy. Radiology. 1991;180:1–12.PubMedGoogle Scholar
  14. 14.
    Gielen C, Sanli I, Stroeken L, Botterweck A, Hulsewé K, Hoofwijk A. Staging chest radiography is not useful in patients with colorectal cancer. Eur J Surg Oncol. 2009;35:1174–8.PubMedCrossRefGoogle Scholar
  15. 15.
    Hwang MJ JS, Kim JH, Shim MC. Diagnostic usefulness of routinely performed preoperative chest computed tomography for colorectal cancer. J Korean Soc Coloproctol. 2010;26:211–6.CrossRefGoogle Scholar
  16. 16.
    Kronawitter U, Kemeny NE, Heelan R, Fata F, Fong Y. Evaluation of chest computed tomography in the staging of patients with potentially resectable liver metastases from colorectal carcinoma. Cancer. 1999;86:229–35.PubMedCrossRefGoogle Scholar
  17. 17.
    Christoffersen MW, Bulut O, Jess P. The diagnostic value of indeterminate lung lesions on staging chest computed tomographies in patients with colorectal cancer. Dan Med Bull. 2010;57:A4093.PubMedGoogle Scholar
  18. 18.
    Brent A, Talbot R, Coyne J, Nash G. Should indeterminate lung lesions reported on staging CT scans influence the management of patients with colorectal cancer? Colorectal Dis. 2007;9:816–8.PubMedCrossRefGoogle Scholar
  19. 19.
    Cho YK, Lee WY, Park CH, et al. The role of a routine preoperative chest CT in patients with colorectal cancer. Colorectal Dis. 2009;11,suppl 2:44.Google Scholar
  20. 20.
    Parnaby C, Bailey W, Balasingam A, Beckert L, Eglinton T, Fife J, et al. Pulmonary staging in colorectal cancer: a review. Colorectal Dis. 2011;14:660–70.CrossRefGoogle Scholar
  21. 21.
    Sullivan R, Peppercorn J, Sikora K, Zalcberg J, Meropol NJ, Amir E, et al. Delivering affordable cancer care in high-income countries. Lancet Oncol. 2011;12:933–80.PubMedCrossRefGoogle Scholar
  22. 22.
    Austin JH, Muller NL, Friedman PJ, Hansell DM, Naidich DP, Remy-Jardin M, et al. Glossary of terms for CT of the lungs: recommendations of the nomenclature committee of the fleischner society. Radiology. 1996;200:327–31.PubMedGoogle Scholar
  23. 23.
    Phillips B, Ball C, Sackett D, Badenoch D, Straus S, Haynes B, et al. Oxford Centre for Evidence-based Medicine―Levels of Evidence. 2009. Accessed Jun 22, 2012.
  24. 24.
    Scottish Intercollegiate Guidelines Network. Sign 50: a guideline developer’s handbook. 2011. Accessed June 22, 2012.
  25. 25.
    Phillips N, Bhan C, Murphy J, Behar N, Allen C, Rowe PH. T1178 indeterminate lung lesions in patients with colorectal cancer: do they progress? (Abstract) Gastroenterology. 2009;136:A-517.Google Scholar
  26. 26.
    Choi DJ, Kwak JM, Kim J, Woo SU, Kim SH. Preoperative chest computerized tomography in patients with locally advanced mid or lower rectal cancer: its role in staging and impact on treatment strategy. J Surg Oncol. 2010;102:588–92.PubMedCrossRefGoogle Scholar
  27. 27.
    Walter C, Pietroni O, Defirend D. The outcomes of indeterminate lung lesions reported on staging CT scans for colorectal cancer. Colorectal Dis. 2010; 12(suppl. 1):19.Google Scholar
  28. 28.
    McQueen AS, Scott J. CT staging of colorectal cancer: what do you find in the chest? Clin Radiol. 2012;67:352–8.PubMedCrossRefGoogle Scholar
  29. 29.
    Pomerri F, Pucciarelli S, Maretto I, Perrone E, Pintacuda G, Lonardi S, et al. Significance of pulmonary nodules in patients with colorectal cancer. Eur Radiol. 2012;22:1680–6.PubMedCrossRefGoogle Scholar
  30. 30.
    Varol Y, Varol U, Karaca B, Karabulut B, Sezgin C, Uslu R. The frequency and significance of radiologically detected indeterminate pulmonary nodules in patients with colorectal cancer. Med Princ Pract. 2012;21:457–61.PubMedCrossRefGoogle Scholar
  31. 31.
    Restivo A, Zorcolo L, Piga S, Cocco IM, Casula G. Routine preoperative chest computerized tomography does not influence therapeutic strategy in patients with colorectal cancer. Colorectal Dis. 2011;14:e216–21.CrossRefGoogle Scholar
  32. 32.
    Quyn AJ, Matthews A, Daniel T, Amin AI, Yalamarthi S. The clinical significance of radiologically detected indeterminate pulmonary nodules in colorectal cancer. Colorectal Dis. 2012;14:828–31.PubMedCrossRefGoogle Scholar
  33. 33.
    Beigelman-Aubry C, Hill C, Grenier PA. Management of an incidentally discovered pulmonary nodule. Eur Radiol. 2007;17:449–66.PubMedCrossRefGoogle Scholar
  34. 34.
    MacMahon H, Austin JH, Gamsu G, Herold CJ, Jett JR, Naidich DP, et al. Guidelines for management of small pulmonary nodules detected on CT scans: a statement from the Fleischner Society. Radiology. 2005;237:395–400.PubMedCrossRefGoogle Scholar
  35. 35.
    Kim HY, Lee SJ, Lee G, Song L, Kim SA, Kim JY, et al. Should preoperative chest CT be recommended to all colon cancer patients? Ann Surg. 2013. doi:  10.1097/SLA.0b013e3182865080. [Epub ahead of print].
  36. 36.
    Pfannschmidt J, Dienemann H, Hoffmann H. Surgical resection of pulmonary metastases from colorectal cancer: a systematic review of published series. Ann Thorac Surg. 2007;84:324–38.PubMedCrossRefGoogle Scholar
  37. 37.
    De Wever W, Meylaerts L, De Ceuninck L, Stroobants S, Verschakelen JA. Additional value of integrated PET-CT in the detection and characterization of lung metastases: correlation with CT alone and PET alone. Eur Radiol. 2007;17:467–73.PubMedCrossRefGoogle Scholar
  38. 38.
    Maithel SK, Ginsberg MS, D’Amico F, DeMatteo RP, Allen PJ, Fong Y, et al. Natural history of patients with subcentimeter pulmonary nodules undergoing hepatic resection for metastatic colorectal cancer. J Am Coll Surg. 2010;210:31–8.PubMedCrossRefGoogle Scholar
  39. 39.
    Jeon KN, Goo JM, Lee CH, Lee Y, Choo JY, Lee NK, et al. Computer-aided nodule detection and volumetry to reduce variability between radiologists in the interpretation of lung nodules at low-dose screening computed tomography. Invest Radiol. 2012;47:457–61.PubMedCrossRefGoogle Scholar
  40. 40.
    Ginsberg MS, Griff SK, Go BD, Yoo HH, Schwartz LH, Panicek DM. Pulmonary nodules resected at video-assisted thoracoscopic surgery: etiology in 426 patients. Radiology. 1999;213:277–82.PubMedGoogle Scholar
  41. 41.
    Swensen SJ, Silverstein MD, Ilstrup DM, Schleck CD, Edell ES. The probability of malignancy in solitary pulmonary nodules: application to small radiologically indeterminate nodules. Arch Intern Med. 1997;157:849–55.PubMedCrossRefGoogle Scholar
  42. 42.
    Diederich S, Hansen J, Wormanns D. Resolving small pulmonary nodules: CT features. Eur Radiol. 2005;15:2064–9.PubMedCrossRefGoogle Scholar

Copyright information

© Society of Surgical Oncology 2013

Authors and Affiliations

  • Andreas Nordholm-Carstensen
    • 1
  • Peer A. Wille-Jørgensen
    • 1
  • Lars N. Jorgensen
    • 1
  • Henrik Harling
    • 1
  1. 1.Department of Surgery K, Bispebjerg HospitalUniversity of CopenhagenCopenhagenDenmark

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