- Email: [email protected]
Effectiveness and Safety of Percutaneous CT-Guided Rib Biopsy
CLINICAL STUDY
Effectiveness and Safety of Percutaneous CT-Guided Rib Biopsy Francis I. Baffour, MD, Michael R. Moynagh, MB BCh BAO, Patrick W. Eiken, MD, PhD, Brian T. Welch, MD, A. Nicholas Kurup, MD, Thomas D. Atwell, MD, and Grant D. Schmit, MD
ABSTRACT Purpose: To retrospectively evaluate effectiveness and safety of percutaneous CT-guided rib biopsy. Materials and Methods: CT-guided core rib biopsies were performed in 249 consecutive patients between January 2002 and June 2016. Mean patient age was 64.8 years ± 13.8. Additional patient demographics, rib lesion characteristics, and procedural techniques were reviewed. Diagnostic yield was assessed, and complications were classified using SIR criteria. Results: Mean maximal diameter of 249 rib lesions was 2.7 cm ± 1.8, and 107 (43%) rib lesions had an associated extraosseous soft tissue component. Of rib lesions, 172 (69%) were lytic, 75 (30%) were sclerotic, and 2 (1%) were identifiable only with positron emission tomography/CT correlation. Specimens from 241 (96.8%) biopsies were adequate for pathologic diagnosis, whereas 8 (3.2%) were nondiagnostic. Of diagnostic biopsies, 168 (69.7%) were positive for malignancy; 73 (30.3%) revealed benign etiologies. There was a significant difference in diagnostic biopsy rate depending on size of the rib lesion (mean 2.8 cm ± 1.8 for diagnostic biopsies vs mean 1.3 cm ± 0.5 for nondiagnostic biopsies; P ¼ .007). Of rib lesions, 170 (99%) lytic lesions and 69 (92%) sclerotic lesions yielded diagnostic biopsies; diagnostic biopsy rate was significantly higher for lytic lesions than sclerotic lesions (P ¼ .01). There were 14 (5.6%) minor complications and no major complications. Conclusions: Percutaneous CT-guided core rib biopsy resulted in high diagnostic yield and low complications. Diagnostic biopsy rates were higher with larger lesion size and lytic rib lesions.
The evaluation of rib lesions relies heavily on diagnostic imaging to guide clinical decision making (1). When tissue diagnosis is required, previous percutaneous core needle bone biopsy studies that included rib biopsies have shown a 70%–88% diagnostic yield and a pathologic congruency of 96% compared with open surgical resection (1–10). A single prior study evaluating only percutaneous rib biopsies by Jakanani et al (1) included 51 patients and reported a diagnostic yield of 88%. Percutaneous biopsy of rib lesions can be technically challenging, and although percutaneous bone biopsy is generally considered a very safe procedure (4,5,11), the safety of core rib biopsies specifically has not been previously evaluated. The purpose of this retrospective
From the Divisions of Musculoskeletal Radiology (F.I.B.), Ultrasound (M.R.M., B.T.W., A.N.K., T.D.A.), Thoracic Radiology (P.W.E.), and Abdominal Imaging (G.D.S.), Department of Radiology, Mayo Clinic, 200 First Street SW, Rochester, MN 55905. Received April 16, 2018; final revision received July 17, 2018; accepted August 6, 2018. Address correspondence to F.I.B.; E-mail: [email protected] None of the authors have identified a conflict of interest. © SIR, 2018 J Vasc Interv Radiol 2018; ▪:1–5 https://doi.org/10.1016/j.jvir.2018.08.004
study was to evaluate the diagnostic yield and safety of computed tomography (CT)–guided percutaneous core rib biopsy in a large contemporary series.
MATERIALS AND METHODS This single-center retrospective study was approved by the local institutional review board and is compliant with the Health Insurance Portability and Accountability Act. Data were obtained from an institutional registry of image-guided biopsy procedures and review of patient medical records. Adult patients were eligible for inclusion if they had undergone a CT-guided core needle biopsy of a rib lesion and had follow-up after the procedure. Patients who were excluded from the study included patients who declined research participation, pediatric patients (< 18 years old), and patients who underwent only rib fine needle aspiration without core needle biopsy (Fig 1). Biopsy was indicated when pathologic characterization of either a possible primary or a metastatic tumor was required, with all cases reviewed and approved by an interventional radiologist before the procedure. All specimens were analyzed by subspecialty fellowship–trained oncologic pathologists. Between January 2002, when the image-guided biopsy registry was established, and June 2016, when the data were
2 ▪ Percutaneous CT-Guided Rib Biopsy
Baffour et al ▪ JVIR
Registry of image-guided biopsy procedures • January 2002 – June 2016 • Paent consented • Lab data pertaining to bleeding risk: INR and platelet concentraon • Site of biopsy and needle gauge • 24 hour follow up call by radiology registered nurse • Chart review aer biopsy to assess for delayed complicaons
CT guided percutaneous rib biopsy (n = 285) Exclusion criteria: • Fine needle aspiraon biopsies • Paents <18 years old Study cohort (n = 249)
• •
Malignant (n = 168) Benign (n = 73)
Diagnosc samples (n = 241)
Non-diagnosc samples (n = 8)
Figure 1. Study cohort and exclusion criteria. INR ¼ international normalized ratio.
accessed, 285 consecutive patients underwent rib biopsy. The final study cohort included 249 patients, who underwent 249 core rib biopsies during the study period. Mean patient age was 64.8 years ± 13.8. Additional patient demographics and tumor characteristics are presented in Table 1.
Biopsy Technique All biopsies were performed at an academic teaching hospital and were either performed by or supervised by a staff radiologist with subspecialty fellowship training in body imaging and intervention and/or interventional radiology (median years of experience, 10; range, 3–30). Patients were required to have a platelet count of > 50 109/L and an international normalized ratio of 1.6 before biopsy. In general, patients were asked to hold aspirin therapy (81 mg or 325 mg) for at least 5 days before the procedure. Patients were also required to discontinue additional common and novel anticoagulation medications for the time frame recommended in the Society of Interventional Radiology (SIR) anticoagulation consensus guidelines (12,13). Biopsies were performed under fluoroscopic CT guidance (GE LightSpeed 16-slice scanner; GE Healthcare, Waukesha, Wisconsin) using sterile technique and local anesthesia. Monitored moderate sedation with fentanyl and midazolam was available for all cases. Using a standard technique, the biopsy route and coaxial device were selected according to
Table 1. Patient Demographics and Tumor Characteristics Variable
Value
Patient demographics Age, y, mean (SD)
64.8 (13.8)
Platelet count, 50 109/L, mean (SD)
265 (97)
INR, mean (SD)
1.0 (0.2)
Female, n (%) Tumor characteristics Lytic, n (%) Sclerotic, n (%) PET/CT correlation only, n (%) Associated soft tissue mass, n (%)
78 (31) 172 (69) 75 (30) 2 (1) 107 (43)
Biopsy with bone biopsy device, n (%)
128 (51)
Biopsy with spring-loaded device, n (%)
121 (49)
Diagnostic biopsy sample, n (%) Nondiagnostic biopsy sample, n (%)
241 (96.8) 8 (3.2)
Tumor size, cm, mean (SD)
2.7 (1.8)
Needle diameter, gauge, mean (SD)
16 (3)
Number of passes, mean (SD)
4 (2)
INR ¼ international normalized ratio; PET ¼ positron emission tomography.
the preference of the performing radiologist based primarily on tumor size, location, and morphology as previously described (14). For tumors with a predominantly soft tissue or lytic component and absence of an intact overlying
Volume ▪ ▪ Number ▪ ▪ Month ▪ 2018
Figure 2. Percutaneous guided biopsy of a 3.5-cm lytic lesion with an associated soft tissue component in the right fourth rib of a patient with prostate adenocarcinoma (arrow). Using a tangential approach, biopsy samples were obtained with a spring-loaded coaxial biopsy system (17/18-gauge). Histopathologic diagnosis was a plasmacytic neoplasm consistent with myeloma or solitary plasmacytoma.
cortex, a coaxial spring-loaded biopsy device (size 14–18 gauge) and specifically designed to yield a core specimen was used (BARD MONOPTY; Bard Medical, Covington, Georgia). For lytic tumors with an intact overlying cortex, a manual or power-driven coaxial 10- to 13-gauge access device was used to gain access to the target lesion through which either a 14- to 18-gauge spring-loaded biopsy device or 14-gauge trephine was used to gain core samples (OsteoSite Bone Biopsy Needle Set; Cook, Inc, Bloomington, Indiana; or OnControl Bone Biopsy Needle Set; Teleflex Inc., Wayne, Pennsylvania). For osteoblastic lesions, a manual or power-driven device with a 10- to 13-gauge outer needle was also used, through which a 12- to 16-gauge coaxial biopsy needle was used to take core samples. Representative images of the biopsy technique are shown in Figures 2 and 3. Samples obtained were submitted for both cytologic and pathologic analysis, as per standard technique. No cytopathologist was present during the biopsy procedure. Patients were monitored for a minimum of 1 hour after the procedure in the outpatient radiology recovery area before being dismissed.
Complications The definition and gradation of complications was guided by the SIR Standards of Practice Complication Classification System (15,16). At the time of biopsy, patients were asked to provide a telephone number so that a dedicated radiology registered nurse could contact them within 24–72 hours after the biopsy to inquire about possible complications using a standardized format employed in the biopsy
3
Figure 3. Percutaneous guided biopsy of an 0.8-cm sclerotic lesion rib with no associated soft tissue component in the left sixth rib of a patient with prostate adenocarcinoma (arrow). Using a tangential approach, biopsy samples were obtained with an Osteo-Site Bone Biopsy Needle Set (13-gauge). Histopathologic evaluation revealed nondiagnostic biopsy samples.
database registry. Patients’ electronic medical records were also reviewed by a single author (F.I.B.) to assess for additional possible delayed complications. If there was any confusion regarding the association of core needle biopsy and a potential complication, the patient’s history was reviewed by an additional author (G.D.S.), and consensus was achieved. Minor complications included procedural site pain not requiring overnight admission to the hospital. Major complications included procedural site infection; pneumothorax; bleeding after the procedure requiring intervention, such as a transfusion or angiography; and procedural site pain requiring hospital admission for pain management. The patient’s reported pain was graded on a 10-point scale. Substantial pain was defined as pain > 5 out of 10 or pain in addition to increasing analgesia requirements. Additional collected information included specific laboratory data used to screen for bleeding risk (platelet count and international normalized ratio), biopsy site, biopsy needle size/device, and number of passes.
Endpoints Primary endpoints for this study were diagnostic and nondiagnostic biopsy samples and the occurrence of complications. Lesion characteristics related to these measures of effectiveness, such as lesion size, lytic versus sclerotic appearance, the presence of a soft tissue component, and the type of biopsy device used, were also evaluated. Secondary endpoints included the spectrum of pathology identified.
Statistical Analysis Summary statistics for patient demographics and clinical characteristics as well as complications were reported as percentage with mean and SD. Comparison of diagnostic
4 ▪ Percutaneous CT-Guided Rib Biopsy
Baffour et al ▪ JVIR
Table 2. Pathology from Rib Biopsies Pathology
Number of cases (%)
Malignant Metastatic disease to bone Primary malignant tumor
144 (57.9) 24 (9.6)
Benign Primary benign tumor No tumor Nondiagnostic samples
4 (1.6) 69 (27.7) 8 (3.2)
and nondiagnostic biopsies was performed using the Wilcoxon rank sum test for lesion size and Fisher exact test for lytic versus sclerotic lesions, presence of a soft tissue component, and use of a spring-loaded biopsy device. P values < .05 were considered statistically significant.
RESULTS Mean maximal diameter of the 249 biopsied rib lesions was 2.7 cm ± 1.3, and 107 (43%) rib lesions had an associated extraosseous soft tissue component. Of rib lesions, 172 (69%) were lytic, 75 (30%) were sclerotic, and 2 (1%) were identifiable only with fluorodeoxyglucose positron emission tomography/ CT correlation. Specimens from 241 (96.8%) biopsies were considered adequate for diagnostic purposes, whereas 8 (3.2%) were nondiagnostic. Of diagnostic biopsies, 168 (69.7%) were positive for malignancy; 73 (30.3%) revealed benign etiologies. Specific pathologic diagnoses of rib lesions are presented in Table 2. The most common malignant diagnoses included metastatic lung adenocarcinoma (60/168; 36%), multiple myeloma/plasmacytoma (21/168; 13%), metastatic breast adenocarcinoma (13/168; 8%), and metastatic prostate adenocarcinoma (12/168; 7%). The most common benign diagnoses included normal bone or cartilage (69/73; 94.5%), fibrous dysplasia (3/73; 4.1%), and brown tumor of hyperparathyroidism (1/73; 1.3%). The mean maximal rib lesion diameter that yielded a diagnostic biopsy was 2.8 cm ± 1.8, and the mean maximal rib lesion size that yielded a nondiagnostic biopsy was 1.3 cm ± 0.5 (Fig 4). There was a significant difference in the diagnostic biopsy rate depending on the size of the rib lesion (P ¼ .007). Of rib lesions, 170 (99%) lytic lesions and 69 (92%) sclerotic lesions yielded diagnostic biopsies. There was a significant increase in the diagnostic biopsy rate for lytic lesions versus sclerotic lesions (P ¼ .01). One of the 8 (12.5%) nondiagnostic biopsies was in a lesion with an extraosseous soft tissue component. There was no significant difference between the presence or absence of an extraosseous soft tissue component and diagnostic biopsy rate (P ¼ .14). Of 128 rib biopsies performed with a bone biopsy device, 121 (94.5%) yielded diagnostic samples, and of 121 biopsies performed with a spring-loaded device, 120 (99.2%) yielded diagnostic samples. There was not a significant difference in
Figure 4. Jitter plot showing the spread of lesion size between diagnostic and nondiagnostic biopsy samples.
diagnostic rate for rib lesion biopsies using bone biopsy devices versus spring-loaded devices (P ¼ .07). Because of high clinical concern for malignancy, 4 (5.5%) of 73 patients with a benign core biopsy result underwent subsequent open surgical biopsy. Metastatic bone lesions were diagnosed in 3 (75%) of these 4 patients, whereas 1 patient was confirmed to have no malignancy. Despite a benign core rib biopsy and no subsequent surgical biopsy, 2 (2.7%) additional patients with high clinical concern for metastatic disease were treated empirically with radiation therapy. Of the remaining 67 patients with a benign core rib biopsy result, 41 (61.2%) underwent follow-up imaging (mean 2.6 y ± 3.2; range, 1 month to 14 years). One (2.4%) patient had a slight interval increase in size and sclerosis of the rib lesion on follow-up, and this was presumed to represent progression of an osseous metastasis. However, neither surgical biopsy nor therapeutic intervention was pursued in this patient. There was no concern for malignancy in the remaining 40 (97.6%) of 41 patients with a benign core rib biopsy who had undergone follow-up imaging. There were no major complications, including bleeding complications, pneumothorax, site infection after the procedure, or pain requiring hospital admission for pain management. Minor complications were experienced by 14 (5.6%) patients, all related to pain (> 5 on a 10-point scale) at the procedural site. These patients required oral analgesics for pain control, including acetaminophen or oxycodone.
DISCUSSION Despite inherent technical challenges, this study demonstrates acceptable diagnostic yield and safety in a large cohort of patients who underwent percutaneous CT-guided biopsy of rib lesions. Diagnostic biopsies were achieved in 96.8% of patients, and no major complications were observed. Smaller lesions and sclerotic lesions were more likely to result in nondiagnostic biopsies. This is not surprising given that extraosseous tumor extension, which is more likely in larger lesions, has been previously shown to be a predictor of successful biopsy and diagnostic accuracy
Volume ▪ ▪ Number ▪ ▪ Month ▪ 2018
(1). Moreover, lesions with extraosseous extension are routinely sampled using larger, spring-loaded biopsy devices (14). Similar to previous studies (1,17,18), metastatic lesions were the most common malignant tumors identified after biopsy. The diagnostic yield reported in the present study is higher than that reported in prior studies. In a study of 51 rib biopsies, Jakanani et al (1) reported a diagnostic yield of 88%. In a review of 2,027 cases of musculoskeletal system biopsies that included 15 rib lesions, Rimondi et al (10) reported a diagnostic rate of 82.1%. Hwang et al (9) reported a diagnostic yield of 70% in their series including 63 rib biopsies. The higher yield reported in this more contemporary study may be a result of advances in biopsy device technology and biopsy techniques over time. Previous studies have not specifically evaluated the safety profile of percutaneous rib biopsy. The largest published series evaluating percutaneous biopsy of rib lesions included 63 subjects and reported only on diagnostic yield (9). The current study found no major complications, including clinically relevant bleeding or pneumothorax. However, 5.6% of patients reported pain requiring oral analgesics following the procedure. Limitations of this study include the retrospective design and associated potential selection bias. Patients with complications who may have presented to another institution for care may not have been identified, thereby underestimating the complication rate. Biopsy device selection, extent of lesional sampling, and approach all were at the discretion of the performing radiologist. Moreover, variation in biopsy technology and technique is inevitable given the time course of the study over nearly 15 years. The low number of nondiagnostic biopsies (8 biopsies) limited robust statistical analysis and precluded multivariate analysis. Finally, surgical pathologic correlation was not available in most cases, and initiation of radiation therapy and chemotherapy for metastatic disease relied on percutaneous biopsy only. In conclusion, the goal of the present study was to determine whether percutaneous CT-guided rib biopsy is efficacious and safe. The results demonstrate a diagnostic biopsy rate of 96.8% and no major complications, with a few patients reporting pain following the procedure. Diagnostic biopsy rates were higher in larger lesions and lytic lesions compared with smaller lesions and sclerotic lesions.
5
REFERENCES 1. Jakanani GC, Saifuddin A. Percutaneous image-guided needle biopsy of rib lesions: a retrospective study of diagnostic outcome in 51 cases. Skeletal Radiol 2013; 42:85–90. 2. Fraser-Hill MA, Renfrew DL. Percutaneous needle biopsy of musculoskeletal lesions. 1. Effective accuracy and diagnostic utility. AJR Am J Roentgenol 1992; 158:809–812. 3. Yao L, Nelson SD, Seeger LL, Eckardt JJ, Eilber FR. Primary musculoskeletal neoplasms: effectiveness of core-needle biopsy. Radiology 1999; 212:682–686. 4. Jelinek JS, Murphey MD, Welker JA, et al. Diagnosis of primary bone tumors with image-guided percutaneous biopsy: experience with 110 tumors. Radiology 2002; 223:731–737. 5. Leffler SG, Chew FS. CT-guided percutaneous biopsy of sclerotic bone lesions: diagnostic yield and accuracy. AJR Am J Roentgenol 1999; 172: 1389–1392. 6. Wu JS, Goldsmith JD, Horwich PJ, Shetty SK, Hochman MG. Bone and soft-tissue lesions: what factors affect diagnostic yield of image-guided core-needle biopsy? Radiology 2008; 248:962–970. 7. Skrzynski MC, Biermann JS, Montag A, Simon MA. Diagnostic accuracy and charge-savings of outpatient core needle biopsy compared with open biopsy of musculoskeletal tumors. J Bone Joint Surg Am 1996; 78: 644–649. 8. Chang IJ, Ilaslan H, Sundaram M, Schils J, Subhas N. CT-guided percutaneous biopsy of sclerotic bone lesions: diagnostic outcomes. Skeletal Radiol 2018; 47:661–669. 9. Hwang S, Lefkowitz RA, Landa J, et al. Percutaneous CT-guided bone biopsy: diagnosis of malignancy in lesions with initially indeterminate biopsy results and CT features associated with diagnostic or indeterminate results. AJR Am J Roentgenol 2011; 197:1417–1425. 10. Rimondi E, Rossi G, Bartalena T, et al. Percutaneous CT-guided biopsy of the musculoskeletal system: results of 2027 cases. Eur J Radiol 2011; 77: 34–42. 11. Welker JA, Henshaw RM, Jelinek J, Shmookler BM, Malawer MM. The percutaneous needle biopsy is safe and recommended in the diagnosis of musculoskeletal masses—outcomes analysis of 155 patients at a sarcoma referral center. Cancer 2000; 89:2677–2686. 12. Patel IJ, Davidson JC, Nikolic B, et al. Consensus guidelines for periprocedural management of coagulation status and hemostasis risk in percutaneous image-guided interventions. J Vasc Interv Radiol 2012; 23: 727–736. 13. Patel IJ, Davidson JC, Nikolic B, et al. Addendum of newer anticoagulants to the SIR Consensus Guideline. J Vasc Interv Radiol 2013; 24:641–645. 14. Welch BT, Welch TJ, Maus TP. Percutaneous image-guided biopsy in an elderly population. J Vasc Interv Radiol 2010; 21:96–100. 15. Omary RA, Bettmann MA, Cardella JF, et al. Quality improvement guidelines for the reporting and archiving of interventional radiology procedures. J Vasc Interv Radiol 2002; 13:879–881. 16. Omary RA, Bettmann MA, Cardella JF, et al. Quality improvement guidelines for the reporting and archiving of interventional radiology procedures. J Vasc Interv Radiol 2003; 14(9 Pt 2):S293–S295. 17. Tateishi U, Gladish GW, Kusumoto M, et al. Chest wall tumors: radiologic findings and pathologic correlation. Part 2. Malignant tumors. Radiographics 2003; 23:1491–1508. 18. Guttentag AR, Salwen JK. Keep your eyes on the ribs: the spectrum of normal variants and diseases that involve the ribs. Radiographics 1999; 19:1125–1142.
Effectiveness and Safety of Percutaneous CT-Guided Rib Biopsy Francis I. Baffour, MD, Michael R. Moynagh, MB BCh BAO, Patrick W. Eiken, MD, PhD, Brian T. Welch, MD, A. Nicholas Kurup, MD, Thomas D. Atwell, MD, and Grant D. Schmit, MD
ABSTRACT Purpose: To retrospectively evaluate effectiveness and safety of percutaneous CT-guided rib biopsy. Materials and Methods: CT-guided core rib biopsies were performed in 249 consecutive patients between January 2002 and June 2016. Mean patient age was 64.8 years ± 13.8. Additional patient demographics, rib lesion characteristics, and procedural techniques were reviewed. Diagnostic yield was assessed, and complications were classified using SIR criteria. Results: Mean maximal diameter of 249 rib lesions was 2.7 cm ± 1.8, and 107 (43%) rib lesions had an associated extraosseous soft tissue component. Of rib lesions, 172 (69%) were lytic, 75 (30%) were sclerotic, and 2 (1%) were identifiable only with positron emission tomography/CT correlation. Specimens from 241 (96.8%) biopsies were adequate for pathologic diagnosis, whereas 8 (3.2%) were nondiagnostic. Of diagnostic biopsies, 168 (69.7%) were positive for malignancy; 73 (30.3%) revealed benign etiologies. There was a significant difference in diagnostic biopsy rate depending on size of the rib lesion (mean 2.8 cm ± 1.8 for diagnostic biopsies vs mean 1.3 cm ± 0.5 for nondiagnostic biopsies; P ¼ .007). Of rib lesions, 170 (99%) lytic lesions and 69 (92%) sclerotic lesions yielded diagnostic biopsies; diagnostic biopsy rate was significantly higher for lytic lesions than sclerotic lesions (P ¼ .01). There were 14 (5.6%) minor complications and no major complications. Conclusions: Percutaneous CT-guided core rib biopsy resulted in high diagnostic yield and low complications. Diagnostic biopsy rates were higher with larger lesion size and lytic rib lesions.
The evaluation of rib lesions relies heavily on diagnostic imaging to guide clinical decision making (1). When tissue diagnosis is required, previous percutaneous core needle bone biopsy studies that included rib biopsies have shown a 70%–88% diagnostic yield and a pathologic congruency of 96% compared with open surgical resection (1–10). A single prior study evaluating only percutaneous rib biopsies by Jakanani et al (1) included 51 patients and reported a diagnostic yield of 88%. Percutaneous biopsy of rib lesions can be technically challenging, and although percutaneous bone biopsy is generally considered a very safe procedure (4,5,11), the safety of core rib biopsies specifically has not been previously evaluated. The purpose of this retrospective
From the Divisions of Musculoskeletal Radiology (F.I.B.), Ultrasound (M.R.M., B.T.W., A.N.K., T.D.A.), Thoracic Radiology (P.W.E.), and Abdominal Imaging (G.D.S.), Department of Radiology, Mayo Clinic, 200 First Street SW, Rochester, MN 55905. Received April 16, 2018; final revision received July 17, 2018; accepted August 6, 2018. Address correspondence to F.I.B.; E-mail: [email protected] None of the authors have identified a conflict of interest. © SIR, 2018 J Vasc Interv Radiol 2018; ▪:1–5 https://doi.org/10.1016/j.jvir.2018.08.004
study was to evaluate the diagnostic yield and safety of computed tomography (CT)–guided percutaneous core rib biopsy in a large contemporary series.
MATERIALS AND METHODS This single-center retrospective study was approved by the local institutional review board and is compliant with the Health Insurance Portability and Accountability Act. Data were obtained from an institutional registry of image-guided biopsy procedures and review of patient medical records. Adult patients were eligible for inclusion if they had undergone a CT-guided core needle biopsy of a rib lesion and had follow-up after the procedure. Patients who were excluded from the study included patients who declined research participation, pediatric patients (< 18 years old), and patients who underwent only rib fine needle aspiration without core needle biopsy (Fig 1). Biopsy was indicated when pathologic characterization of either a possible primary or a metastatic tumor was required, with all cases reviewed and approved by an interventional radiologist before the procedure. All specimens were analyzed by subspecialty fellowship–trained oncologic pathologists. Between January 2002, when the image-guided biopsy registry was established, and June 2016, when the data were
2 ▪ Percutaneous CT-Guided Rib Biopsy
Baffour et al ▪ JVIR
Registry of image-guided biopsy procedures • January 2002 – June 2016 • Paent consented • Lab data pertaining to bleeding risk: INR and platelet concentraon • Site of biopsy and needle gauge • 24 hour follow up call by radiology registered nurse • Chart review aer biopsy to assess for delayed complicaons
CT guided percutaneous rib biopsy (n = 285) Exclusion criteria: • Fine needle aspiraon biopsies • Paents <18 years old Study cohort (n = 249)
• •
Malignant (n = 168) Benign (n = 73)
Diagnosc samples (n = 241)
Non-diagnosc samples (n = 8)
Figure 1. Study cohort and exclusion criteria. INR ¼ international normalized ratio.
accessed, 285 consecutive patients underwent rib biopsy. The final study cohort included 249 patients, who underwent 249 core rib biopsies during the study period. Mean patient age was 64.8 years ± 13.8. Additional patient demographics and tumor characteristics are presented in Table 1.
Biopsy Technique All biopsies were performed at an academic teaching hospital and were either performed by or supervised by a staff radiologist with subspecialty fellowship training in body imaging and intervention and/or interventional radiology (median years of experience, 10; range, 3–30). Patients were required to have a platelet count of > 50 109/L and an international normalized ratio of 1.6 before biopsy. In general, patients were asked to hold aspirin therapy (81 mg or 325 mg) for at least 5 days before the procedure. Patients were also required to discontinue additional common and novel anticoagulation medications for the time frame recommended in the Society of Interventional Radiology (SIR) anticoagulation consensus guidelines (12,13). Biopsies were performed under fluoroscopic CT guidance (GE LightSpeed 16-slice scanner; GE Healthcare, Waukesha, Wisconsin) using sterile technique and local anesthesia. Monitored moderate sedation with fentanyl and midazolam was available for all cases. Using a standard technique, the biopsy route and coaxial device were selected according to
Table 1. Patient Demographics and Tumor Characteristics Variable
Value
Patient demographics Age, y, mean (SD)
64.8 (13.8)
Platelet count, 50 109/L, mean (SD)
265 (97)
INR, mean (SD)
1.0 (0.2)
Female, n (%) Tumor characteristics Lytic, n (%) Sclerotic, n (%) PET/CT correlation only, n (%) Associated soft tissue mass, n (%)
78 (31) 172 (69) 75 (30) 2 (1) 107 (43)
Biopsy with bone biopsy device, n (%)
128 (51)
Biopsy with spring-loaded device, n (%)
121 (49)
Diagnostic biopsy sample, n (%) Nondiagnostic biopsy sample, n (%)
241 (96.8) 8 (3.2)
Tumor size, cm, mean (SD)
2.7 (1.8)
Needle diameter, gauge, mean (SD)
16 (3)
Number of passes, mean (SD)
4 (2)
INR ¼ international normalized ratio; PET ¼ positron emission tomography.
the preference of the performing radiologist based primarily on tumor size, location, and morphology as previously described (14). For tumors with a predominantly soft tissue or lytic component and absence of an intact overlying
Volume ▪ ▪ Number ▪ ▪ Month ▪ 2018
Figure 2. Percutaneous guided biopsy of a 3.5-cm lytic lesion with an associated soft tissue component in the right fourth rib of a patient with prostate adenocarcinoma (arrow). Using a tangential approach, biopsy samples were obtained with a spring-loaded coaxial biopsy system (17/18-gauge). Histopathologic diagnosis was a plasmacytic neoplasm consistent with myeloma or solitary plasmacytoma.
cortex, a coaxial spring-loaded biopsy device (size 14–18 gauge) and specifically designed to yield a core specimen was used (BARD MONOPTY; Bard Medical, Covington, Georgia). For lytic tumors with an intact overlying cortex, a manual or power-driven coaxial 10- to 13-gauge access device was used to gain access to the target lesion through which either a 14- to 18-gauge spring-loaded biopsy device or 14-gauge trephine was used to gain core samples (OsteoSite Bone Biopsy Needle Set; Cook, Inc, Bloomington, Indiana; or OnControl Bone Biopsy Needle Set; Teleflex Inc., Wayne, Pennsylvania). For osteoblastic lesions, a manual or power-driven device with a 10- to 13-gauge outer needle was also used, through which a 12- to 16-gauge coaxial biopsy needle was used to take core samples. Representative images of the biopsy technique are shown in Figures 2 and 3. Samples obtained were submitted for both cytologic and pathologic analysis, as per standard technique. No cytopathologist was present during the biopsy procedure. Patients were monitored for a minimum of 1 hour after the procedure in the outpatient radiology recovery area before being dismissed.
Complications The definition and gradation of complications was guided by the SIR Standards of Practice Complication Classification System (15,16). At the time of biopsy, patients were asked to provide a telephone number so that a dedicated radiology registered nurse could contact them within 24–72 hours after the biopsy to inquire about possible complications using a standardized format employed in the biopsy
3
Figure 3. Percutaneous guided biopsy of an 0.8-cm sclerotic lesion rib with no associated soft tissue component in the left sixth rib of a patient with prostate adenocarcinoma (arrow). Using a tangential approach, biopsy samples were obtained with an Osteo-Site Bone Biopsy Needle Set (13-gauge). Histopathologic evaluation revealed nondiagnostic biopsy samples.
database registry. Patients’ electronic medical records were also reviewed by a single author (F.I.B.) to assess for additional possible delayed complications. If there was any confusion regarding the association of core needle biopsy and a potential complication, the patient’s history was reviewed by an additional author (G.D.S.), and consensus was achieved. Minor complications included procedural site pain not requiring overnight admission to the hospital. Major complications included procedural site infection; pneumothorax; bleeding after the procedure requiring intervention, such as a transfusion or angiography; and procedural site pain requiring hospital admission for pain management. The patient’s reported pain was graded on a 10-point scale. Substantial pain was defined as pain > 5 out of 10 or pain in addition to increasing analgesia requirements. Additional collected information included specific laboratory data used to screen for bleeding risk (platelet count and international normalized ratio), biopsy site, biopsy needle size/device, and number of passes.
Endpoints Primary endpoints for this study were diagnostic and nondiagnostic biopsy samples and the occurrence of complications. Lesion characteristics related to these measures of effectiveness, such as lesion size, lytic versus sclerotic appearance, the presence of a soft tissue component, and the type of biopsy device used, were also evaluated. Secondary endpoints included the spectrum of pathology identified.
Statistical Analysis Summary statistics for patient demographics and clinical characteristics as well as complications were reported as percentage with mean and SD. Comparison of diagnostic
4 ▪ Percutaneous CT-Guided Rib Biopsy
Baffour et al ▪ JVIR
Table 2. Pathology from Rib Biopsies Pathology
Number of cases (%)
Malignant Metastatic disease to bone Primary malignant tumor
144 (57.9) 24 (9.6)
Benign Primary benign tumor No tumor Nondiagnostic samples
4 (1.6) 69 (27.7) 8 (3.2)
and nondiagnostic biopsies was performed using the Wilcoxon rank sum test for lesion size and Fisher exact test for lytic versus sclerotic lesions, presence of a soft tissue component, and use of a spring-loaded biopsy device. P values < .05 were considered statistically significant.
RESULTS Mean maximal diameter of the 249 biopsied rib lesions was 2.7 cm ± 1.3, and 107 (43%) rib lesions had an associated extraosseous soft tissue component. Of rib lesions, 172 (69%) were lytic, 75 (30%) were sclerotic, and 2 (1%) were identifiable only with fluorodeoxyglucose positron emission tomography/ CT correlation. Specimens from 241 (96.8%) biopsies were considered adequate for diagnostic purposes, whereas 8 (3.2%) were nondiagnostic. Of diagnostic biopsies, 168 (69.7%) were positive for malignancy; 73 (30.3%) revealed benign etiologies. Specific pathologic diagnoses of rib lesions are presented in Table 2. The most common malignant diagnoses included metastatic lung adenocarcinoma (60/168; 36%), multiple myeloma/plasmacytoma (21/168; 13%), metastatic breast adenocarcinoma (13/168; 8%), and metastatic prostate adenocarcinoma (12/168; 7%). The most common benign diagnoses included normal bone or cartilage (69/73; 94.5%), fibrous dysplasia (3/73; 4.1%), and brown tumor of hyperparathyroidism (1/73; 1.3%). The mean maximal rib lesion diameter that yielded a diagnostic biopsy was 2.8 cm ± 1.8, and the mean maximal rib lesion size that yielded a nondiagnostic biopsy was 1.3 cm ± 0.5 (Fig 4). There was a significant difference in the diagnostic biopsy rate depending on the size of the rib lesion (P ¼ .007). Of rib lesions, 170 (99%) lytic lesions and 69 (92%) sclerotic lesions yielded diagnostic biopsies. There was a significant increase in the diagnostic biopsy rate for lytic lesions versus sclerotic lesions (P ¼ .01). One of the 8 (12.5%) nondiagnostic biopsies was in a lesion with an extraosseous soft tissue component. There was no significant difference between the presence or absence of an extraosseous soft tissue component and diagnostic biopsy rate (P ¼ .14). Of 128 rib biopsies performed with a bone biopsy device, 121 (94.5%) yielded diagnostic samples, and of 121 biopsies performed with a spring-loaded device, 120 (99.2%) yielded diagnostic samples. There was not a significant difference in
Figure 4. Jitter plot showing the spread of lesion size between diagnostic and nondiagnostic biopsy samples.
diagnostic rate for rib lesion biopsies using bone biopsy devices versus spring-loaded devices (P ¼ .07). Because of high clinical concern for malignancy, 4 (5.5%) of 73 patients with a benign core biopsy result underwent subsequent open surgical biopsy. Metastatic bone lesions were diagnosed in 3 (75%) of these 4 patients, whereas 1 patient was confirmed to have no malignancy. Despite a benign core rib biopsy and no subsequent surgical biopsy, 2 (2.7%) additional patients with high clinical concern for metastatic disease were treated empirically with radiation therapy. Of the remaining 67 patients with a benign core rib biopsy result, 41 (61.2%) underwent follow-up imaging (mean 2.6 y ± 3.2; range, 1 month to 14 years). One (2.4%) patient had a slight interval increase in size and sclerosis of the rib lesion on follow-up, and this was presumed to represent progression of an osseous metastasis. However, neither surgical biopsy nor therapeutic intervention was pursued in this patient. There was no concern for malignancy in the remaining 40 (97.6%) of 41 patients with a benign core rib biopsy who had undergone follow-up imaging. There were no major complications, including bleeding complications, pneumothorax, site infection after the procedure, or pain requiring hospital admission for pain management. Minor complications were experienced by 14 (5.6%) patients, all related to pain (> 5 on a 10-point scale) at the procedural site. These patients required oral analgesics for pain control, including acetaminophen or oxycodone.
DISCUSSION Despite inherent technical challenges, this study demonstrates acceptable diagnostic yield and safety in a large cohort of patients who underwent percutaneous CT-guided biopsy of rib lesions. Diagnostic biopsies were achieved in 96.8% of patients, and no major complications were observed. Smaller lesions and sclerotic lesions were more likely to result in nondiagnostic biopsies. This is not surprising given that extraosseous tumor extension, which is more likely in larger lesions, has been previously shown to be a predictor of successful biopsy and diagnostic accuracy
Volume ▪ ▪ Number ▪ ▪ Month ▪ 2018
(1). Moreover, lesions with extraosseous extension are routinely sampled using larger, spring-loaded biopsy devices (14). Similar to previous studies (1,17,18), metastatic lesions were the most common malignant tumors identified after biopsy. The diagnostic yield reported in the present study is higher than that reported in prior studies. In a study of 51 rib biopsies, Jakanani et al (1) reported a diagnostic yield of 88%. In a review of 2,027 cases of musculoskeletal system biopsies that included 15 rib lesions, Rimondi et al (10) reported a diagnostic rate of 82.1%. Hwang et al (9) reported a diagnostic yield of 70% in their series including 63 rib biopsies. The higher yield reported in this more contemporary study may be a result of advances in biopsy device technology and biopsy techniques over time. Previous studies have not specifically evaluated the safety profile of percutaneous rib biopsy. The largest published series evaluating percutaneous biopsy of rib lesions included 63 subjects and reported only on diagnostic yield (9). The current study found no major complications, including clinically relevant bleeding or pneumothorax. However, 5.6% of patients reported pain requiring oral analgesics following the procedure. Limitations of this study include the retrospective design and associated potential selection bias. Patients with complications who may have presented to another institution for care may not have been identified, thereby underestimating the complication rate. Biopsy device selection, extent of lesional sampling, and approach all were at the discretion of the performing radiologist. Moreover, variation in biopsy technology and technique is inevitable given the time course of the study over nearly 15 years. The low number of nondiagnostic biopsies (8 biopsies) limited robust statistical analysis and precluded multivariate analysis. Finally, surgical pathologic correlation was not available in most cases, and initiation of radiation therapy and chemotherapy for metastatic disease relied on percutaneous biopsy only. In conclusion, the goal of the present study was to determine whether percutaneous CT-guided rib biopsy is efficacious and safe. The results demonstrate a diagnostic biopsy rate of 96.8% and no major complications, with a few patients reporting pain following the procedure. Diagnostic biopsy rates were higher in larger lesions and lytic lesions compared with smaller lesions and sclerotic lesions.
5
REFERENCES 1. Jakanani GC, Saifuddin A. Percutaneous image-guided needle biopsy of rib lesions: a retrospective study of diagnostic outcome in 51 cases. Skeletal Radiol 2013; 42:85–90. 2. Fraser-Hill MA, Renfrew DL. Percutaneous needle biopsy of musculoskeletal lesions. 1. Effective accuracy and diagnostic utility. AJR Am J Roentgenol 1992; 158:809–812. 3. Yao L, Nelson SD, Seeger LL, Eckardt JJ, Eilber FR. Primary musculoskeletal neoplasms: effectiveness of core-needle biopsy. Radiology 1999; 212:682–686. 4. Jelinek JS, Murphey MD, Welker JA, et al. Diagnosis of primary bone tumors with image-guided percutaneous biopsy: experience with 110 tumors. Radiology 2002; 223:731–737. 5. Leffler SG, Chew FS. CT-guided percutaneous biopsy of sclerotic bone lesions: diagnostic yield and accuracy. AJR Am J Roentgenol 1999; 172: 1389–1392. 6. Wu JS, Goldsmith JD, Horwich PJ, Shetty SK, Hochman MG. Bone and soft-tissue lesions: what factors affect diagnostic yield of image-guided core-needle biopsy? Radiology 2008; 248:962–970. 7. Skrzynski MC, Biermann JS, Montag A, Simon MA. Diagnostic accuracy and charge-savings of outpatient core needle biopsy compared with open biopsy of musculoskeletal tumors. J Bone Joint Surg Am 1996; 78: 644–649. 8. Chang IJ, Ilaslan H, Sundaram M, Schils J, Subhas N. CT-guided percutaneous biopsy of sclerotic bone lesions: diagnostic outcomes. Skeletal Radiol 2018; 47:661–669. 9. Hwang S, Lefkowitz RA, Landa J, et al. Percutaneous CT-guided bone biopsy: diagnosis of malignancy in lesions with initially indeterminate biopsy results and CT features associated with diagnostic or indeterminate results. AJR Am J Roentgenol 2011; 197:1417–1425. 10. Rimondi E, Rossi G, Bartalena T, et al. Percutaneous CT-guided biopsy of the musculoskeletal system: results of 2027 cases. Eur J Radiol 2011; 77: 34–42. 11. Welker JA, Henshaw RM, Jelinek J, Shmookler BM, Malawer MM. The percutaneous needle biopsy is safe and recommended in the diagnosis of musculoskeletal masses—outcomes analysis of 155 patients at a sarcoma referral center. Cancer 2000; 89:2677–2686. 12. Patel IJ, Davidson JC, Nikolic B, et al. Consensus guidelines for periprocedural management of coagulation status and hemostasis risk in percutaneous image-guided interventions. J Vasc Interv Radiol 2012; 23: 727–736. 13. Patel IJ, Davidson JC, Nikolic B, et al. Addendum of newer anticoagulants to the SIR Consensus Guideline. J Vasc Interv Radiol 2013; 24:641–645. 14. Welch BT, Welch TJ, Maus TP. Percutaneous image-guided biopsy in an elderly population. J Vasc Interv Radiol 2010; 21:96–100. 15. Omary RA, Bettmann MA, Cardella JF, et al. Quality improvement guidelines for the reporting and archiving of interventional radiology procedures. J Vasc Interv Radiol 2002; 13:879–881. 16. Omary RA, Bettmann MA, Cardella JF, et al. Quality improvement guidelines for the reporting and archiving of interventional radiology procedures. J Vasc Interv Radiol 2003; 14(9 Pt 2):S293–S295. 17. Tateishi U, Gladish GW, Kusumoto M, et al. Chest wall tumors: radiologic findings and pathologic correlation. Part 2. Malignant tumors. Radiographics 2003; 23:1491–1508. 18. Guttentag AR, Salwen JK. Keep your eyes on the ribs: the spectrum of normal variants and diseases that involve the ribs. Radiographics 1999; 19:1125–1142.