Clinical Correlates of Incidental Probable Benign Pulmonary Nodules with Diameters Less than 8 mm in a Healthy Korean Cohort: A Retrospective Study
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design, Data Sources, and Inclusion/Exclusion Criteria
2.2. CT Acquisition Parameters and Data Collection
2.3. Statistical Analysis
3. Results
3.1. Participants’ Sociodemographic Characteristics and Comorbidities
3.2. Laboratory Test Results and Imaging Findings
3.3. Factors Associated with Benign Pulmonary Nodule(s)
3.4. Single vs. Multiple Pulmonary Nodules
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Hansell, D.M.; Bankier, A.A.; MacMahon, H.; McLoud, T.C.; Muller, N.L.; Remy, J. Fleischner Society: Glossary of Terms for Thoracic Imaging. Radiology 2008, 246, 697–722. [Google Scholar] [CrossRef] [PubMed]
- Gould, M.K.; Tang, T.; Liu, I.L.; Lee, J.; Zheng, C.; Danforth, K.N.; Kosco, A.E.; di Fiore, J.L.; Suh, D.E. Recent Trends in the Identification of Incidental Pulmonary Nodules. Am. J. Respir. Crit. Care Med. 2015, 192, 1208–1214. [Google Scholar] [CrossRef] [PubMed]
- Pinsky, P.F.; Gierada, D.S.; Black, W.; Munden, R.; Nath, H.; Aberle, D.; Kazerooni, E. Performance of Lung-Rads in the National Lung Screening Trial: A Retrospective Assessment. Ann. Intern. Med. 2015, 162, 485–491. [Google Scholar] [CrossRef]
- MacMahon, H.; Naidich, D.P.; Goo, J.M.; Lee, K.S.; Leung, A.N.C.; Mayo, J.R.; Mehta, A.C.; Ohno, Y.; Powell, C.A.; Prokop, M.; et al. Guidelines for Management of Incidental Pulmonary Nodules Detected on Ct Images: From the Fleischner Society 2017. Radiology 2017, 284, 228–243. [Google Scholar] [CrossRef] [PubMed]
- Callister, M.E.; Baldwin, D.R.; Akram, A.R.; Barnard, S.; Cane, P.; Draffan, J.; Franks, K.; Gleeson, F.; Graham, R.; Woolhouse, I.; et al. British Thoracic Society Guidelines for the Investigation and Management of Pulmonary Nodules. Thorax 2015, 70, ii1–ii54. [Google Scholar] [CrossRef]
- Gould, M.K.; Donington, J.; Lynch, W.R.; Mazzone, P.J.; Midthun, D.E.; Naidich, D.P.; Wiener, R.S. Evaluation of Individuals with Pulmonary Nodules: When Is It Lung Cancer? Diagnosis and Management of Lung Cancer, 3rd Ed: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines. Chest 2013, 143, e93S–e120S. [Google Scholar] [CrossRef]
- McWilliams, A.M.; Tammemagi, M.C.; Mayo, J.R.; Roberts, H.; Liu, G.; Soghrati, K.; Yasufuku, K.; Martel, S.; Laberge, F.; Gingras, M.; et al. Probability of Cancer in Pulmonary Nodules Detected on First Screening Ct. N. Engl. J. Med. 2013, 369, 910–919. [Google Scholar] [CrossRef]
- Wahidi, M.M.; Govert, J.A.; Goudar, R.K.; Gould, M.K.; McCrory, D.C.; Physicians American College of Chest. Evidence for the Treatment of Patients with Pulmonary Nodules: When Is It Lung Cancer? Accp Evidence-Based Clinical Practice Guidelines (2nd Edition). Chest 2007, 132, 94S–107S. [Google Scholar] [CrossRef]
- Horeweg, N.; van Rosmalen, J.; Heuvelmans, M.A.; van der Aalst, C.M.; Vliegenthart, R.; Scholten, E.T.; Haaf, K.T.; Nackaerts, K.; Lammers, J.W.; Weenink, C.; et al. Lung Cancer Probability in Patients with Ct-Detected Pulmonary Nodules: A Prespecified Analysis of Data from the Nelson Trial of Low-Dose Ct Screening. Lancet Oncol. 2014, 15, 1332–1341. [Google Scholar] [CrossRef]
- Beigelman-Aubry, C.; Hill, C.; Grenier, P.A. Management of an Incidentally Discovered Pulmonary Nodule. Eur. Radiol. 2007, 17, 449–466. [Google Scholar] [CrossRef] [PubMed]
- Mitruka, S.; Landreneau, R.J.; Mack, M.J.; Fetterman, L.S.; Gammie, J.; Bartley, S.; Sutherland, S.R.; Bowers, C.M.; Keenan, R.J.; Ferson, P.F.; et al. Diagnosing the Indeterminate Pulmonary Nodule: Percutaneous Biopsy Versus Thoracoscopy. Surgery 1995, 118, 676–684. [Google Scholar] [CrossRef] [PubMed]
- Ost, D.; Fein, A.M.; Feinsilver, S.H. Clinical Practice. The Solitary Pulmonary Nodule. N. Engl. J. Med. 2003, 348, 2535–2542. [Google Scholar] [CrossRef] [PubMed]
- Mazzone, P.J.; Silvestri, G.A.; Patel, S.; Kanne, J.P.; Kinsinger, L.S.; Wiener, R.S.; Hoo, G.S.; Detterbeck, F.C. Screening for Lung Cancer: Chest Guideline and Expert Panel Report. Chest 2018, 153, 954–985. [Google Scholar] [CrossRef] [PubMed]
- Wysoki, M.G. Clinical Importance of Small Pulmonary Nodules Detected at Ct. Radiology 1997, 204, 583. [Google Scholar] [CrossRef]
- Munden, R.F.; Erasmus, J.J.; Wahba, H.; Fineberg, N.S. Follow-up of Small (4 Mm or Less) Incidentally Detected Nodules by Computed Tomography in Oncology Patients: A Retrospective Review. J. Thorac. Oncol. 2010, 5, 1958–1962. [Google Scholar] [CrossRef]
- Snoeckx, A.; Reyntiens, P.; Desbuquoit, D.; Spinhoven, M.J.; van Schil, P.E.; van Meerbeeck, J.P.; Parizel, P.M. Evaluation of the Solitary Pulmonary Nodule: Size Matters, but Do Not Ignore the Power of Morphology. Insights Imaging 2018, 9, 73–86. [Google Scholar] [CrossRef]
- Malhotra, J.; Malvezzi, M.; Negri, E.; La Vecchia, C.; Boffetta, P. Risk Factors for Lung Cancer Worldwide. Eur. Respir. J. 2016, 48, 889–902. [Google Scholar] [CrossRef]
- Kucharska-Newton, A.M.; Rosamond, W.D.; Schroeder, J.C.; McNeill, A.M.; Coresh, J.; Folsom, A.R.; Study Members of the Atherosclerosis Risk in Communities. Hdl-Cholesterol and the Incidence of Lung Cancer in the Atherosclerosis Risk in Communities (Aric) Study. Lung Cancer 2008, 61, 292–300. [Google Scholar] [CrossRef]
- Dessi, S.; Batetta, B.; Pulisci, D.; Spano, O.; Cherchi, R.; Lanfranco, G.; Tessitore, L.; Costelli, P.; Baccino, F.M.; Anchisi, C.; et al. Altered Pattern of Lipid Metabolism in Patients with Lung Cancer. Oncology 1992, 49, 436–441. [Google Scholar] [CrossRef]
- Umeki, S. Decreases in Serum Cholesterol Levels in Advanced Lung Cancer. Respiration 1993, 60, 178–181. [Google Scholar] [CrossRef]
- Siemianowicz, K.; Gminski, J.; Stajszczyk, M.; Wojakowski, W.; Goss, M.; Machalski, M.; Telega, A.; Brulinski, K.; Magiera-Molendowska, H. Serum Hdl Cholesterol Concentration in Patients with Squamous Cell and Small Cell Lung Cancer. Int. J. Mol. Med. 2000, 6, 307–311. [Google Scholar] [CrossRef]
- Lin, X.; Lu, L.; Liu, L.; Wei, S.; He, Y.; Chang, J.; Lian, X. Blood Lipids Profile and Lung Cancer Risk in a Meta-Analysis of Prospective Cohort Studies. J. Clin. Lipidol. 2017, 11, 1073–1081. [Google Scholar] [CrossRef] [PubMed]
- Chi, P.D.; Liu, W.; Chen, H.; Zhang, J.P.; Lin, Y.; Zheng, X.; Liu, W.; Dai, S. High-Density Lipoprotein Cholesterol Is a Favorable Prognostic Factor and Negatively Correlated with C-Reactive Protein Level in Non-Small Cell Lung Carcinoma. PLoS ONE 2014, 9, e91080. [Google Scholar] [CrossRef] [PubMed]
- Cruz, P.M.; Mo, H.; McConathy, W.J.; Sabnis, N.; Lacko, A.G. The Role of Cholesterol Metabolism and Cholesterol Transport in Carcinogenesis: A Review of Scientific Findings, Relevant to Future Cancer Therapeutics. Front. Pharmacol. 2013, 4, 119. [Google Scholar] [CrossRef]
- Chen, Y.; Zhu, C.; Chen, Y.; Wang, N.; Li, Q.; Han, B.; Zhao, L.; Chen, C.; Zhai, H.; Lu, Y. The Association of Thyroid Nodules with Metabolic Status: A Cross-Sectional Spect-China Study. Int. J. Endocrinol. 2018, 2018, 6853617. [Google Scholar] [CrossRef]
- Liu, J.; Wang, C.; Tang, X.; Fu, S.; Jing, G.; Ma, L.; Sun, W.; Li, Y.; Wu, D.; Niu, Y.; et al. Correlation Analysis of Metabolic Syndrome and Its Components with Thyroid Nodules. Diabetes Metab. Syndr. Obes. 2019, 12, 1617–1623. [Google Scholar] [CrossRef] [PubMed]
- Alberg, A.J.; Samet, J.M. Epidemiology of Lung Cancer. Chest 2003, 123, 21S–49S. [Google Scholar] [CrossRef] [PubMed]
- Ginsberg, M.S.; Griff, S.K.; Go, B.D.; Yoo, H.H.; Schwartz, L.H.; Panicek, D.M. Pulmonary Nodules Resected at Video-Assisted Thoracoscopic Surgery: Etiology in 426 Patients. Radiology 1999, 213, 277–282. [Google Scholar] [CrossRef]
- Stephens, M.J.; Rho, B.H.; Curran-Everett, D.; Carr, L.; Bowler, R.; Lynch, D. Identification of Nonaggressive Pulmonary Nodules Using an Optimized Scoring System. J. Thorac. Imaging 2019, 34, 170–178. [Google Scholar] [CrossRef]
Variables | No Nodule (n = 56) | Nodule(s) (n = 355) | p-Value |
---|---|---|---|
Sex, n (%) | 0.062 | ||
Male | 47 (83.9) | 256 (72.1) | |
Female | 9 (16.1) | 99 (27.9) | |
Age (years), mean (SD) | 52.5 (7.6) | 53.0 (6.4) | 0.616 |
Weight (kg), mean (SD) | 71.7 (9.4) | 69.6 (11.9) | 0.150 |
Height (cm), mean (SD) | 170.4 (6.6) | 168.8 (8.0) | 0.155 |
WC (cm), mean (SD) | 87.8 (7.8) | 86.4 (8.5) | 0.232 |
BMI (kg/m2), mean (SD) | 24.6 (2.7) | 24.3 (2.9) | 0.397 |
Smoking status, n (%) | 0.002 | ||
Never | 10 (18.9) | 129 (36.3) | |
Former | 16 (30.2) | 127 (35.8) | |
Current | 27 (50.9) | 99 (27.9) | |
Drinking frequency, n (%) | 0.283 | ||
None | 5 (9.4) | 54 (15.2) | |
≤1/month | 6 (11.3) | 52 (14.6) | |
2–4/month | 23 (43.4) | 110 (31.0) | |
2–3/week | 11 (20.8) | 99 (27.9) | |
≥4/week | 8 (15.1) | 40 (11.3) | |
Family history of cancer, n (%) | 29 (52.7) | 163 (45.9) | 0.346 |
Taking any medicines, n (%) | 34 (61.8) | 180 (50.7) | 0.125 |
Comorbidities, n (%) | |||
History of cancer | 1 (1.8) | 16 (4.5) | 0.713 |
Hypothyroidism | 1 (1.8) | 8 (2.3) | 1.000 |
DM | 7 (12.7) | 25 (7.0) | 0.172 |
Dyslipidemia | 14 (25.5) | 68 (19.2) | 0.277 |
Hypertension | 17 (30.9) | 93 (26.2) | 0.463 |
CAD | 9 (16.4) | 40 (11.3) | 0.278 |
Variables | No Nodule (n = 56) | Nodule(s) (n = 355) | p-Value |
---|---|---|---|
Glucose (mg/dL), mean (SD) | 105.2 (20.5) | 99.0 (16.8) | 0.035 |
Creatinine (mg/dL), mean (SD) | 0.88 (0.18) | 0.87 (0.16) | 0.553 |
BUN (mg/dL), mean (SD) | 13.5 (3.9) | 13.4 (3.4) | 0.856 |
AST (IU/L), mean (SD) | 28.2 (13.8) | 26.9 (11.0) | 0.505 |
ALT (IU/L), mean (SD) | 27.9 (12.7) | 27.2 (16.7) | 0.723 |
Total cholesterol (mg/dL), mean (SD) | 175.1 (31.5) | 187.2 (37.1) | 0.021 |
Triglyceride (mg/dL), mean (SD) | 138.7 (88.7) | 121.2 (72.5) | 0.165 |
HDL cholesterol (mg/dL), mean (SD) | 52.0 (12.6) | 54.5 (15.1) | 0.230 |
LDL cholesterol (mg/dL), mean (SD) | 112.7 (28.6) | 124.3 (34.1) | 0.016 |
Hemoglobin (g/dL), mean (SD) | 15.0 (1.6) | 14.8 (1.5) | 0.287 |
HbA1C (%), mean (SD) | 5.71 (0.69) | 5.63 (0.52) | 0.439 |
TSH (μU/mL), mean (SD) | 2.26 (1.42) | 2.42 (1.47) | 0.448 |
Free T4 (ng/dL), mean (SD) | 1.43 (0.19) | 1.42 (0.16) | 0.824 |
H. pylori IgG, n (%) | 0.116 | ||
Negative | 36 (64.3) | 178 (50.1) | |
Equivocal | 2 (3.6) | 29 (8.2) | |
Positive | 18 (32.1) | 148 (41.7) | |
Thyroid ultrasound, n (%) | 74 (54.0) | 96 (61.9) | 0.171 |
Abdomen ultrasound, n (%) | 127 (74.3) | 127 (69.0) | 0.274 |
EGD, n (%) | 40 (24.5) | 40 (23.3) | 0.783 |
Colonoscopy, n (%) | 83 (59.3) | 93 (60.8) | 0.794 |
FVC% predicted, mean (SD) | 90.4 (9.2) | 91.6 (9.7) | 0.229 |
FEV1% predicted, mean (SD) | 90.8 (10.0) | 91.0 (9.9) | 0.906 |
Univariate Logistic Regression | Multivariate Logistic Regression | |||
---|---|---|---|---|
Variables | OR (95% CI) | p-Value | aOR (95% CI) | p-Value |
Female sex | 2.02 (0.95–4.27) | 0.066 | 0.88 (0.26–3.00) | 0.844 |
Age (per 10-year increase) | 1.12 (0.72–1.72) | 0.615 | ||
Weight (per 10 kg increase) | 0.86 (0.67–1.10) | 0.221 | ||
Height (per 10 cm increase) | 0.76 (0.52–1.11) | 0.156 | ||
WC (per 10 cm increase) | 0.82 (0.58–1.14) | 0.231 | ||
BMI | 0.96 (0.87–1.06) | 0.397 | ||
Smoking status | ||||
Never | REF | REF | ||
Former | 0.62 (0.27–1.41) | 0.250 | 0.59 (0.18–1.94) | 0.388 |
Current | 0.28 (0.13–0.61) | 0.001 | 0.26 (0.08–0.81) | 0.020 |
Drinking frequency | ||||
None | REF | |||
≤1/month | 0.80 (0.23–2.79) | 0.729 | ||
2–4/month | 0.44 (0.16–1.23) | 0.118 | ||
2–3/week | 0.83 (0.28–2.52) | 0.747 | ||
≥4/week | 0.46 (0.14–1.52) | 0.205 | ||
Family history of cancer | 0.76 (0.43–1.34) | 0.347 | ||
Comorbidities | ||||
History of any cancer | 2.55 (0.33–19.60) | 0.369 | ||
Any medication use | 0.64 (0.35–1.14) | 0.127 | ||
Hypothyroidism | 1.24 (0.15–10.15) | 0.838 | ||
DM | 0.52 (0.21–1.27) | 0.150 | ||
Dyslipidemia | 0.69 (0.36–1.34) | 0.279 | ||
Hypertension | 0.79 (0.43–1.47) | 0.464 | ||
CAD | 0.65 (0.30–1.43) | 0.281 | ||
Glucose (per 10 mg/dL increase) | 0.85 (0.74–0.97) | 0.017 | 0.87 (0.75–1.01) | 0.072 |
Creatinine | 0.59 (0.10–3.40) | 0.552 | ||
BUN | 0.99 (0.91–1.08) | 0.856 | ||
AST | 0.99 (0.97–1.01) | 0.429 | ||
ALT | 1.00 (0.98–1.01) | 0.770 | ||
Total cholesterol (per 10 mg/dL increase) | 1.10 (1.01–1.19) | 0.021 | ||
Triglyceride (per 10 mg/dL increase) | 0.97 (0.94–1.01) | 0.110 | ||
HDL cholesterol | 1.01 (0.99–1.03) | 0.230 | ||
LDL cholesterol (per 10 mg/dL increase) | 1.11 (1.02–1.22) | 0.017 | 1.10 (1.00–1.20) | 0.049 |
Hemoglobin | 0.90 (0.74–1.09) | 0.287 | ||
HbA1C | 0.79 (0.49–1.28) | 0.337 | ||
H. pylori IgG | ||||
Negative | REF | |||
Equivocal | 2.93 (0.67–12.84) | 0.153 | ||
Positive | 1.66 (0.91–3.05) | 0.100 | ||
TSH | 1.08 (0.88–1.34) | 0.447 | ||
Free T4 | 0.82 (0.15–4.55) | 0.824 | ||
Thyroid ultrasound | 0.61 (0.31–1.19) | 0.148 | ||
Abdomen ultrasound | 0.69 (0.35–1.35) | 0.277 | ||
EGD | 0.90 (0.46–1.73) | 0.745 | ||
Colonoscopy | 0.71 (0.37–1.34) | 0.289 | ||
FVC% PRED (per 1% PRED increase) | 1.00 (0.97–1.03) | 0.945 | ||
FEV1% PRED (per 1% PRED increase) | 1.02 (0.99–1.04) | 0.262 |
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Jung, Y.J.; Kim, H.; Kim, Y.; Cho, W.-K. Clinical Correlates of Incidental Probable Benign Pulmonary Nodules with Diameters Less than 8 mm in a Healthy Korean Cohort: A Retrospective Study. J. Clin. Med. 2023, 12, 7501. https://doi.org/10.3390/jcm12237501
Jung YJ, Kim H, Kim Y, Cho W-K. Clinical Correlates of Incidental Probable Benign Pulmonary Nodules with Diameters Less than 8 mm in a Healthy Korean Cohort: A Retrospective Study. Journal of Clinical Medicine. 2023; 12(23):7501. https://doi.org/10.3390/jcm12237501
Chicago/Turabian StyleJung, Young Ju, Hwajung Kim, Youngmee Kim, and Won-Kyung Cho. 2023. "Clinical Correlates of Incidental Probable Benign Pulmonary Nodules with Diameters Less than 8 mm in a Healthy Korean Cohort: A Retrospective Study" Journal of Clinical Medicine 12, no. 23: 7501. https://doi.org/10.3390/jcm12237501