Skip to main content

Advertisement

SpringerLink
Log in

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

  • Thoracic Oncology
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Background

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.

Methods

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.

Results

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.

Conclusion

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Reference

  1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  7. National Comprehensive Cancer Network. NCCN clinical practice guidelines in oncology rectal cancer. 2013. http://www.nccn.org/professionals/physician_gls/pdf/rectal.pdf. Accessed Apr 2, 2013.

  8. National Comprehensive Cancer Network. NCCN clinical practice guidelines in oncology colon cancer. 2013. http://www.nccn.org/professionals/physician_gls/pdf/colon.pdf. Accessed Apr 2, 2013.

  9. The Danish Colorectal Cancer Group. Guidelines for the Management of Colorectal Cancer. 2010. http://dccg.dk/03_Publikation/Retningslinier2009revOKT2010.pdf. Accessed Feb 2, 2013. In Danish.

  10. The Association of Coloproctology of Great Britain and Ireland. Guidelines for the Management of Colorectal Cancer. 2007. http://www.acpgbi.org.uk/wp-content/uploads/2007-CC-Management-Guidelines.pdf. Accessed Feb 8, 2013.

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  13. Davis SD. CT evaluation for pulmonary metastases in patients with extrathoracic malignancy. Radiology. 1991;180:1–12.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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. 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.

    Article  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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. http://www.cebm.net/index.aspx?o=1025. Accessed Jun 22, 2012.

  24. Scottish Intercollegiate Guidelines Network. Sign 50: a guideline developer’s handbook. 2011. http://www.sign.ac.uk/pdf/sign50.pdf. Accessed June 22, 2012.

  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. 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.

    Article  PubMed  Google Scholar 

  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. McQueen AS, Scott J. CT staging of colorectal cancer: what do you find in the chest? Clin Radiol. 2012;67:352–8.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  33. Beigelman-Aubry C, Hill C, Grenier PA. Management of an incidentally discovered pulmonary nodule. Eur Radiol. 2007;17:449–66.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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. 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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  42. Diederich S, Hansen J, Wormanns D. Resolving small pulmonary nodules: CT features. Eur Radiol. 2005;15:2064–9.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

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.

Author information

Authors and Affiliations

  1. Department of Surgery K, Bispebjerg Hospital, University of Copenhagen, Copenhagen, Denmark

    Andreas Nordholm-Carstensen MD, Peer A. Wille-Jørgensen MD, DMSci, Lars N. Jorgensen MD, DMSci & Henrik Harling MD, DMSci

Authors
  1. Andreas Nordholm-Carstensen MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peer A. Wille-Jørgensen MD, DMSci
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lars N. Jorgensen MD, DMSci
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Henrik Harling MD, DMSci
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andreas Nordholm-Carstensen MD.

Additional information

Funding was received from the Danish Cancer Society, Aase and Ejnar Danielsen’s Foundation, and The Einar Willumsen Foundation.

Appendix

Appendix

Search strategies for indeterminate pulmonary nodules at colorectal cancer staging: a systematic review of predictive parameters for malignancy

Run by MB

Aim

A. Radiological characteristics of IPN representing true metastatic disease on follow-up

Search Strategies for Aim A

MEDLINE (Ovid) 29.05.12; 1281 hits

[mp=title, abstract, original title, name of substance word, subject heading word, protocol supplementary concept, rare disease supplementary concept, unique identifier]

  1. 1.

    *Lung/

  2. 2.

    *Lung Neoplasms/

  3. 3.

    *Lung Diseases/

  4. 4.

    exp Neoplasm Staging/

  5. 5.

    *Thorax/

  6. 6.

    (indeterminate lung lesion* or nodule* or indeterminate or lesion* or chest or thorax or pulmonary or lung* or staging or stage).m_titl.

  7. 7.

    1 or 2 or 3 or 4 or 5 or 6

  8. 8.

    exp Colorectal Neoplasms/

  9. 9.

    ((colorect* or colon* or rect* or anal* or anus* or intestin* or bowel*) adj (carcinom* or neoplas* or adenocarcinom* or cancer* or tumor* or tumour* or sarcom* or polyp* or adenom*)).mp.

  10. 10.

    8 or 9

  11. 11.

    *Tomography, X-Ray Computed/

  12. 12.

    (compute* adj (tomograph* or x-ray or x ray or xray or assist*) adj (x ray or x-ray or xray or transmission or tomograph*)).mp.

  13. 13.

    (tomography* adj (x ray or x-ray or xray or compute* or transmission or electron) adj (compute* or x-ray or x ray or xray)).mp.

  14. 14.

    ((x ray or x-ray or xray) adj (compute* or cat or tomograph*) adj (tomograph* or assist* tomograph* or axial tomography or scan* or compute*)).mp.

  15. 15.

    (tomodensitometry or beam or ct).mp.

  16. 16.

    11 or 12 or 13 or 14 or 15

  17. 17.

    7 and 10 and 16

  18. 18.

    exp clinical trial/

  19. 19.

    comparative study/

  20. 20.

    exp “Sensitivity and Specificity”/

  21. 21.

    (study or studies or trial or clinical or compare or comparative or placebo or random* or control* or non-control* or rct or specificity or sensitivity or accuracy or abstract*).mp.

  22. 22.

    18 or 19 or 20 or 21

  23. 23.

    17 and 22

EMBASE (Ovid) 29.05.12; 1309 hits

[mp=title, abstract, subject headings, heading word, drug trade name, original title, device manufacturer, drug manufacturer, device trade name, keyword]

  1. 1.

    *lung/

  2. 2.

    *lung tumor/

  3. 3.

    *lung disease/

  4. 4.

    *cancer staging/

  5. 5.

    *thorax radiography/

  6. 6.

    (indeterminate lung lesion* or nodule* or indeterminate or lesion* or chest or thorax or pulmonary or lung* or staging or stage).m_titl.

  7. 7.

    1 or 2 or 3 or 4 or 5 or 6

  8. 8.

    exp colorectal tumor/

  9. 9.

    ((colorect* or colon* or rect* or anal* or anus* or intestin* or bowel*) and (carcinom* or neoplas* or adenocarcinom* or cancer* or tumor* or tumour* or sarcom* or polyp* or adenom*)).m_titl.

  10. 10.

    8 or 9

  11. 11.

    *computer assisted tomography/

  12. 12.

    (compute* adj (tomograph* or x-ray or x ray or xray or assist*) adj (x ray or x-ray or xray or transmission or tomograph*)).mp.

  13. 13.

    (tomography* adj (x ray or x-ray or xray or compute* or transmission or electron) adj (compute* or x-ray or x ray or xray)).mp.

  14. 14.

    ((x ray or x-ray or xray) adj (compute* or cat or tomograph*) adj (tomograph* or assist* tomograph* or axial tomography or scan* or compute*)).mp.

  15. 15.

    (tomodensitometry or beam or ct).mp.

  16. 16.

    11 or 12 or 13 or 14 or 15

  17. 17.

    7 and 10 and 16

  18. 18.

    exp clinical study/

  19. 19.

    exp comparative study/

  20. 20.

    exp diagnostic accuracy/

  21. 21.

    (study or studies or trial or clinical or compare or comparative or placebo or random* or control* or non-control* or rct or specificity or sensitivity or accuracy or abstract*).mp.

  22. 22.

    18 or 19 or 20 or 21

  23. 23.

    17 and 22

Cochrane Library 29.05.12; 1142 hits

  1. #1

    MeSH descriptor Lung explode all trees

  2. #2

    MeSH descriptor Lung Neoplasms explode all trees

  3. #3

    MeSH descriptor Lung Diseases explode all trees

  4. #4

    MeSH descriptor Neoplasm Staging explode all trees

  5. #5

    MeSH descriptor Thorax explode all trees

  6. #6

    (indeterminate lung lesion* or nodule* or indeterminate or lesion* or chest or thorax or pulmonary or lung* or staging or stage):ti,ab,kw

  7. #7

    (#1 OR #2 OR #3 OR #4 OR #5 OR #6)

  8. #8

    MeSH descriptor Colorectal Neoplasms explode all trees

  9. #9

    ((colorect* or colon* or rect* or anal* or anus* or intestin* or bowel*) near (carcinom* or neoplas* or adenocarcinom* or cancer* or tumor* or tumour* or sarcom* or polyp* or adenom*)):ti,ab,kw

  10. #10

    (#8 OR #9)

  11. #11

    MeSH descriptor Tomography, X-Ray Computed explode all trees

  12. #12

    (compute* near (tomograph* or x-ray or x ray or xray or assist*) near (x ray or x-ray or xray or transmission or tomograph*)):ti,ab,kw

  13. #13

    (tomography* near (x ray or x-ray or xray or compute* or transmission or electron) near (compute* or x-ray or x ray or xray)):ti,ab,kw

  14. #14

    ((x ray or x-ray or xray) near (compute* or cat or tomograph*) near (tomograph* or assist* tomograph* or axial tomography or scan* or compute*)):ti,ab,kw

  15. #15

    (tomodensitometry or beam or ct):ti,ab,kw

  16. #16

    (#11 OR #12 OR #13 OR #14 OR 15)

  17. #17

    (#7 AND #10 AND #16)

Science Citation Index 29.05.12; 533 hits

  1. #5

    #4 AND #3 AND #2

  2. #4

    TI=(tomodensitometry or beam or ct or x ray or x-ray or xray or compute* or cat or tomograph* or scan* or transmission or electron)

  3. #3

    TI=(((colorect* or colon* or rect* or anal* or anus* or intestin* or bowel*) and (carcinom* or neoplas* or adenocarcinom* or cancer* or tumor* or tumour* or sarcom* or polyp* or adenom*)))

  4. #2

    TI=((indeterminate lung lesion* or nodule* or indeterminate or lesion* or chest or thorax or pulmonary or lung* or staging or stage))

  5. #1

    TI=((tomodensitometry or beam or ct or x ray or x-ray or xray or compute* or cat or tomograph* or scan* or transmission or electron))

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nordholm-Carstensen, A., Wille-Jørgensen, P.A., Jorgensen, L.N. et al. Indeterminate Pulmonary Nodules at Colorectal Cancer Staging: A Systematic Review of Predictive Parameters for Malignancy. Ann Surg Oncol 20, 4022–4030 (2013). https://doi.org/10.1245/s10434-013-3062-y

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1245/s10434-013-3062-y

Keywords

Search

Navigation