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Ann Thorac Surg 2008;86:1111-1114. doi:10.1016/j.athoracsur.2008.05.062
© 2008 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Evaluation of Isolated Rib Lesions With Radionuclide-Guided Biopsy

Rafael S. Andrade, MDa,*, Juan J. Blondet, MDb, Teri Kast, RNa, Jose Jessurun, MDc, Michael A. Maddaus, MDa

a Division of Thoracic and Foregut Surgery, University of Minnesota, Minneapolis, Minnesota
b Division of Surgical Critical Care/Trauma, Department of Surgery, University of Minnesota, Minneapolis, Minnesota
c Department of Laboratory Medicine and Pathology, University of Minnesota, Minneapolis, Minnesota

Accepted for publication May 21, 2008.

* Address correspondence to Dr Andrade, Department of Surgery, University of Minnesota, 420 Delaware Street SE, MMC 207, Minneapolis, MN 55455 (Email: andr0119{at}umn.edu).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background: Isolated rib lesions detected on bone scanning can pose a diagnostic challenge, particularly in patients with a known primary cancer. The purpose of our study was to assess the diagnostic value of radionuclide-guided rib biopsy with an intraoperative gamma probe.

Methods: We conducted a retrospective chart review of 10 patients who underwent an intraoperative gamma probe-guided rib biopsy. Rib defects were identified by radionuclide bone scan. Patients received an intravenous dose of technetium 99m methylene diphosphonate within 6 hours before surgery. The approximate location of the rib defect was scanned with a hand-held gamma probe intraoperatively; an excisional rib biopsy was performed in the area with the highest tracer activity.

Results: Median age was 54 years (range, 40 to 83) and median body mass index was 32.5 (range, 23 to 52). Seven patients had a known primary extraosseous cancer and 3 patients had no history of cancer. Seven patients had pain at the time of initial evaluation. The median operative time was 45 minutes, median operative blood loss was 25 mL, and median length of stay was 1 day. Complications occurred in 2 patients: a pneumothorax that did not require treatment and a delayed hemothorax that required tube thoracostomy. Rib biopsy was accurate in all 10 patients; metastatic disease was found in 5 of 7 cancer patients. Pain improved or resolved in 4 patients.

Conclusions: The evaluation of isolated rib lesions using radionuclide-guided rib biopsy with an intraoperative hand-held gamma probe is accurate and potentially therapeutic. Thoracic surgeons and oncologists should be aware of this approach.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Isolated rib lesions detected by radionuclide bone scanning, or by positron-emission tomography (PET) scan, in patients with primary extraosseous cancers do not necessarily represent metastatic disease. Bone metastases are present in 20% to 70% of isolated rib lesions in patients with a primary extraosseous malignancy; hence, rib biopsy is often required. However, intraoperative localization of isolated, nonpalpable radionuclide bone scan-positive rib lesions is challenging, a difficulty compounded by obesity, by body habitus, and by positioning during surgery [1–8].

To improve the yield of image-guided rib biopsy, Little and colleagues [5] described a technique using radionuclide-guided methylene blue injection into the affected site. In their study, 15 patients with primary extraosseous malignancies underwent rib biopsy with 100% accuracy; 53% of lesions were malignant and 47% were benign. Moores and colleagues [6] later used this technique in 33 patients with similar results. Shih and colleagues [9] used a cobalt 57 skin marker directly over the site; rib biopsy was diagnostic in all 10 patients. However, the disadvantage of these techniques is time-consuming preoperative imaging.

Radionuclide-guided rib biopsy with an intraoperative hand-held gamma probe was first described in 10 patients by Robinson and colleagues in 1998 [3]. This technique takes advantage of a hand-held gamma probe originally designed for sentinel lymph node biopsies for breast cancer and melanoma. Patients with a previously detected rib abnormality on a bone scan undergo a standard single-dose injection of radioisotope, within 6 to 12 hours before surgery. The surgeon uses a sterile-wrapped hand-held gamma probe to intraoperatively mark the area of highest tracer activity. A 3- to 4-cm incision is made over the marked area and a portion of rib excised [7]. In a subsequent study of 34 patients with primary extraosseous malignancies, Robinson [10] reported 100% diagnostic accuracy; only 20.1% of these lesions were malignant.

Three additional reports of this hand-held gamma probe technique, in a total of 9 patients, have been published in English-language journals [11–13]. In all these studies the sensitivity and specificity for this diagnostic procedure was 100%.

The published mortality rate is 0%; about 20% of the patients have required postoperative chest tube insertion for pneumothorax [3, 12]. We herein report our experience with this technique in 10 patients.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Acknowledgments
 References
 
We conducted a retrospective chart review, approved on May 12th, 2006 by the Institutional Review Board at the University of Minnesota, Minneapolis. A waiver for patient consent was also obtained. We identified 10 consecutive patients who had undergone a radionuclide-guided rib biopsy with an intraoperative hand-held gamma probe from January 1, 2001, through June 30, 2007. All 10 patients had a rib defect detected on radionuclide bone scan.

Radioisotope Injection
Patients received an intravenous dose of 18 to 26 millecurie technecium (Tc)-99m methylene diphosphonate (MDP). We brought patients to the operating room within 6 hours after injection [3].

Surgical Procedure
We performed the rib biopsy under general anesthesia. Once the area of interest was prepared and draped, it was scanned with a sterile-wrapped hand-held gamma probe (neo2000; Neoprobe Corporation, Dublin, OH). Gamma radiation (counts per second [cps]) was traced, and the area of highest tracer activity was marked. A 2- to 5-cm incision was made; once the rib was exposed, the tracer activity was again measured to verify that the proper area had been identified. A 2- to 6-cm portion of rib was excised; additional surrounding soft tissue was removed if necessary. Final tracer activity was measured on the specimen after it was removed for further confirmation. If the pleural space was entered, either it was evacuated with suction at the time of closure or a chest tube was left in place. The indication to leave a chest tube in place is injury to lung parenchyma or concern for bleeding.

Statistical Analysis
We report all values as median and a range. No further statistical analysis was required for this study.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Acknowledgments
 References
 
Patients' characteristics (demographics, primary diagnosis, symptoms, radiologic findings, and biopsy results) are summarized in Table 1. The median age was 54 years (range, 40 to 83) and median body mass index (BMI) was 32.5 (range, 23 to 52). The median operative time was 45 minutes (range, 28 to 145); the median operative blood loss was 25 mL (range, 10 to 100). Early in our series, one patient with a plasmacytoma required thoracoscopic assistance for rib resection, since surgical margins could be more readily evaluated thoracoscopically. Background tracer activity counts ranged from 200 to 500 cps and tracer activity counts on the target rib ranged from 600 to 2,300 cps. Three patients had a chest tube placed at the end of the procedure. The median length of stay was 1 day (range, 1 to 12).


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  		Table 1 Characteristics of 10 Patients Who Underwent a Radionuclide-Guided Rib Biopsy With an Intraoperative Hand-Held Gamma-Probe
 
Seven patients had pain at initial presentation; 4 had an improvement or resolution of pain, and 2 had no improvement (1 patient had no documentation of pain on follow-up records). Figure 1 represents the radionuclide bone scan of a patient with severe pain, revealing Langerhans cell histiocytosis on biopsy; his pain resolved completely after surgery.


Figure 1
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  		Fig 1. Radionuclide bone scan of a patient with severe chest wall pain. Rib biopsy revealed Langerhans cell histiocytosis; his pain completely resolved after surgery.

 
No rib lesions were palpable prior to incision. Four ribs had no gross visible or palpable abnormality to guide the surgeon intraoperatively (ie, mass or fracture), even after operative exposure. Nine biopsies revealed pathologic diagnoses.

One patient with esophageal cancer had no pathologic abnormality on rib biopsy. An anterior left fifth rib defect was found on both the radionuclide bone and PET scans, without a matching defect on the computed tomographic (CT) scan (Fig 2). He underwent a technically successful localization and excision of a large (4.6 cm) section of rib with surrounding soft tissue. Three weeks later, he underwent an esophagectomy (T3N0 poorly differentiated adenocarcinoma). On a PET-CT scan 10 months thereafter, a pelvic metastasis was detected, but no increased fluorodeoxyglucose (FDG) uptake was seen in the area of the rib resection (Fig 3).


Figure 2
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  		Fig 2. Positron emission tomographic scan (A), radionuclide bone scan (B), and matching computed tomographic (CT) scan (C) of a patient with esophageal cancer and no pathologic abnormality on rib biopsy. The arrows point to the area of increased uptake. No matching abnormality is seen on CT scan.

 

Figure 3
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  		Fig 3. Positron emission tomographic/computed tomographic scan of the same patient as in Fig 2. Ten months after the original rib biopsy the area revealed no pathologic fluorodeoxyglucose uptake (arrow).

 
In our series mortality was 0. One patient had a pneumothorax found on immediate postoperative chest X-ray that did not require intervention. One diabetic patient developed renal failure secondary to ketorolac on the second postoperative day; he then developed a hemothorax on the fourth postoperative day that required tube thoracostomy. Renal failure resolved with conservative measures, the chest tube was removed after 6 days, and he was discharged home on the twelfth postoperative day.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Acknowledgments
 References
 
Rib biopsies for isolated lesions were technically challenging until the advent of the radioisotope-guided biopsy technique using an intraoperative hand-held gamma probe. Our series of 10 patients, the second largest published in the English-language literature, confirms previous reports. The paucity of published data reflects the relative infrequency of isolated rib lesions detected by bone scintigraphy, but likely also reflects the lack of awareness of this diagnostic and potentially therapeutic procedure among thoracic surgeons and oncologists.

Most patients with isolated rib lesions, whether benign or malignant, have pain at the involved site. Of our 10 patients, 7 had pain localized to the area that was abnormal on the bone scan; all 7 patients with pain had a clear pathologic diagnosis. These findings are consistent with those from other reports [8, 12, 13]. Pain resolved or improved in 4 patients, suggesting that this procedure can be of therapeutic value.

The role of CT scanning in patients with isolated rib lesions on radionuclide bone scan is variable, a matching finding on the CT scan is helpful in finding the lesion; however, a negative finding is of no value because the false-negative rate of CT scanning for bone metastases is about 50% [14]. In our series, the CT scan was positive in 80% of patients with a malignant rib lesion and in 60% of patients with a benign rib lesion. The PET scanning did not add information to further characterize the rib lesion. Our findings underscore the difficulty of radiologic characterization and localization of radionuclide bone scan-positive rib defects.

Five of 7 patients (71%) with known malignancies had a malignant rib lesion; our results are in the range of 20% to 70% reported in other studies [3–8]. We emphasize that every effort should be made to biopsy isolated rib lesions in patients with extraosseous primary malignancies.

A clear pathologic diagnosis was provided in 90% of patients. In a single patient in our series, no abnormality was identified by rib biopsy. The rib defect found on the radionuclide bone and PET scans was not visible on the CT scan. A follow-up PET scan 11 months later was negative at the biopsy site, despite development of metastatic disease. We interpret this rib biopsy to be accurate, given that he had no pain initially and there was no evidence of recurrence at that site. The initial radionuclide bone and PET scans were false positive: the specificity for radionuclide bone scans ranges from 61% to 80%, and for PET scans from 88% to 98% [15–17]. Comparatively, radionuclide-guided rib biopsy with a hand-held gamma probe has a specificity of 100% [3,11–13, 18].

This technique is simple and only requires familiarization with the hand-held gamma probe. Tracer activity counts in our experience are generally at least 2 to 3 times higher than the background count, in accordance with the results published by Robinson and colleagues [3]. Once an incision is made, the surgeon can be reassured by remeasuring tracer activity directly on the rib, and again on the specimen after removal, particularly when a gross abnormality is not evident intraoperatively. Four ribs in our series had no visible abnormality to guide the surgeon even after operative exposure; subtle changes may not be visible on the periosteal surface of the rib and can be missed entirely without gamma probe localization, particularly in the presence of obesity. Early in our experience we used thoracoscopic assistance in one patient to aid with the determination of resection margins; however, thoracoscopic assistance is almost never required. Finally, this procedure can be easily performed in obese patients: 8 patients (80%) had a BMI 30 or greater; 2 of these patients were morbidly obese.

One significant complication in our series required prolonged hospitalization. We believe that this complication was largely secondary to the use of ketorolac in a diabetic patient, leading first to renal failure and then to a hemothorax on the fourth postoperative day. Our median length of stay was 1 day; most of our patients required an overnight stay, primarily for pain control.

The main advantages of radioisotope-guided rib biopsy with a hand-held gamma probe are simplicity and precision. A standard injection of intravenous radioisotope and a single image are performed within 6 hours before surgery, the procedure is short and safe, and accuracy is 100%. This equipment is generally available at hospitals that perform for surgery for breast cancer and melanoma, because sentinel lymph node biopsies are standard of care for these malignancies. No specific training or credentialing is required to use the gamma-probe and familiarization with the gamma probe is almost immediate.

No radiologic test is accurate enough to determine the cause of an isolated rib lesion, even in patients with known malignancies. Abnormal findings often require a biopsy. We conclude that radioisotope-guided rib biopsy with an intraoperative hand-held gamma probe is technically easy, safe, and accurate. Thoracic surgeons and oncologists should be aware of this approach.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
References
 
The authors would like to thank Mary Knatterud for editorial assistance on this manuscript.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Corcoran RJ, Thrall JH, Kyle RW, Kaminski RJ, Johnson MC. Solitary abnormalities in bone scans of patients with extraosseous malignancies Radiology 1976;121:663-667.[Abstract]
  2. Robinson LA. Bone localization Surg Oncol Clin N Am 1999;8:565-576.[Medline]
  3. Robinson LA, Preksto D, Muro-Cacho C, Hubbell DS. Intraoperative gamma probe – directed biopsy of asymptomatic suspected bone metastases Ann Thorac Surg 1998;65:1426-1432.[Abstract/Free Full Text]
  4. Ikard RW. A study of rib biopsy Chest 1992;102:1134-1136.[Medline]
  5. Little AG, DeMeester TR, Kirchner PT, Lascone C, Badani N, Golomb HM. Guided biopsies of abnormalities on nuclear bone scans J Thorac Cardiovasc Surg 1983;85:396-403.[Abstract]
  6. Moores DWO, Line B, Dziuban SW, McKneally MF. Nuclear scan-guided rib biopsy J Thorac Cardiovasc Surg 1990;99:620-621.[Abstract]
  7. Thurman SA, Robinson LA, Ahmad N, Pow-Sang JM, Lockhart JL, Seigne J. Investigation of the safety and accuracy of intraoperative {gamma} probe directed biopsy of bone scan detected rib abnormalities in prostatic adenocarcinoma J Urol 2003;169:1341-1344.[Medline]
  8. Ichinose Y, Hara N, Ohta M, et al. Preoperative examination to detect distant metastases is not advocated for asymptomatic patients with stages 1 and 2 non-small cell lung cancer Chest 1989;96:1104-1109.[Medline]
  9. Shih WJ, DeLand FH, Domstad PA, Magoun S, Dillon ML. Open rib biopsy guided by radionuclide technique Ann Thorac Surg 1984;36:59-62.
  10. Robinson LA. Radio-guided surgical biopsy for the diagnosis of suspected osseous metastases QJ Nucl Med 2001;45:38-46.
  11. Sodha S, Nagda S, Lackman R, Donthineni R. Gamma probe assisted biopsy of suspected metastatic rib lesions Clin Ortho Rel Res 2004;422:186-189.
  12. Fernandes DS, Aye RW, Garnett DJ, Denny J. Target-specific rib biopsy using the gamma probe Am J Surg 2000;179:389-390.[Medline]
  13. Axelsson CK, Nielsen BP, Graff J. Radioisotope-guided surgical biopsy of costal metastases in breast cancer patients Scan J Surg 2002;91:333-335.
  14. Nakamoto Y, Cohade C, Tatsumi M, Hammoud D, Wahl R. CT appearance of bone metastases detected with FDG PET as part of the same PET/CT examination Radiology 2005;237:627-634.[Abstract/Free Full Text]
  15. Fogelman I, Cook G, Israel O, Van der Wall H. Positron emission tomography and bone metastases Semin Nucl Med 2005;35:135-142.[Medline]
  16. Gayed I, Vu T, Johnson M, Macapinlac H, Podoloff D. Comparison of bone and 2-deoxy- 2-[18F]fluoro-D-glucose positron emission tomography in the evaluation of bony metastases in lung cancer Mol Imaging Biol 2003;5:26-31.[Medline]
  17. Bury T, Barreto A, Daenen F, Barthelemy N, Ghaye B, Rigo P. Fluorine-18 deoxyglucose positron emission tomography for the detection of bone metastases in patients with non-small cell lung cancer Eur J Nucl Med 1998;25:1244-1247.[Medline]
  18. van Mesdag T, Gommans GM, de Waard JW. Radionuclide-guided minimally invasive rib biopsy for metastases [in Dutch] Ned Tijdschr Geneeskd 2002;146:1539-1542.

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Ann. Thorac. Surg. 2008 86: 1115. [Extract] [Full Text] [PDF]



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Ann. Thorac. Surg., October 1, 2008; 86(4): 1115 - 1115.
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