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Original Report |
1 Department of Radiology, Hadassah University Hospital, Ein-Kerem, P.O.B.
12000, Jerusalem, Israel.
2 Department of Pathology, Hadassah University Hospital, Jerusalem,
Israel.
3 Department of Hematology, Hadassah University Hospital, Jerusalem,
Israel.
Received July 12, 2002;
accepted after revision April 15, 2003.
Presented at the annual meeting of the Israeli Radiological Association,
Eilat, 2001.
Abstract
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CONCLUSION. Imaging-guided small-bore cutting-edge needle biopsy of splenic lesions is a safe procedure. In most patients with primary or recurrent lymphoma, the disease subtype can be diagnosed reliably.
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We present our experience with imaging-guided small-bore cutting-edge needle biopsy (Turner, Cook, Bloomington, IN) of splenic lesions for establishing the diagnosis of malignant lymphoma.
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During the study period, 35 patients underwent 43 imaging-guided splenic small-bore cutting-edge needle biopsies for the diagnosis of a wide spectrum of diseases. Of these 43 biopsies, 24 were performed in 20 patients with a diagnosis of lymphoma. The study group comprises these patients. In 16 of these patients, the diagnosis of lymphoma was new, and in four, disease relapse was suspected before the biopsy. There were 13 men and seven women, with a median age of 47 years (range, 16–77 years).
The reason for choosing the spleen as the target for biopsy in 10 patients was the presence of discrete lesions confined to the spleen. The other 10 patients showed radiographic evidence of nonsplenic disease such as celiac lymphadenopathy and small hepatic lesions; however, these were not accessible for biopsy in five patients, and in the remaining five patients, prior nondiagnostic imaging-guided biopsy specimens had already been obtained from those nonsplenic locations.
Normal clotting parameters were the only prebiopsy requirements: partial thromboplastin time (normal range, 28–42 sec), prothrombin time (normal range, 10–13 sec), and a normal platelet count (normal range, 130–400 x 103/µL). Patients gave written informed consent, and an IV line was placed. Vital signs were not monitored during the procedure because no conscious IV sedation was administered. As soon as the biopsy was completed, the patient was transferred to the recovery area, where vital signs were monitored.
CT guidance was used in 22 biopsies; sonographic guidance was used in two. After we reviewed the diagnostic abdominal CT, we placed the patient in a prone or supine position. During the first half of the study period, the biopsy was performed using standard CT protocols on a multidetector CT (MDCT) scanner (Excel 2400, twin flash multidetector CT, Elscint-Marconi, Haifa, Israel). Biopsies were performed in most cases without IV contrast material. In three patients, IV contrast material was injected because the lesion could not be identified without it.
Sonographically guided biopsies were performed using a freehand technique with a 2-5–MHz frequency transducer (ATL HDI-5000, Philips Medical Systems, Bothell, WA). The most peripheral splenic lesion was selected for biopsy to pass through the least volume of healthy splenic tissue, and the most peripheral portion of the focal lesion was chosen to avoid sampling of necrotic tissue in the central region (Fig. 1).
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After administration of local anesthesia (lignocaine hydrochloride 2%, hospital preparation) a 20- or 22-gauge aspiration cutting-edge core biopsy Turner needle (Cook) was placed at the periphery of the splenic lesion. It was then rapidly and repeatedly advanced and withdrawn 1–2 cm in the lesion until material was seen in the hub. In no case was an abundance of blood withdrawn in the syringe. Suction was released, and the needle was removed. A small-bore cutting-edge needle biopsy performed using this technique on one lesion was defined as a "single pass."
A pathologist was present at the time of the procedure to evaluate each specimen microscopically for adequacy of sampling. If the material was inadequate, a second pass was made immediately. In most cases, only one pass was necessary. Multiple passes performed during the same session were defined as one biopsy. A biopsy performed on a different occasion was defined as a repeated biopsy. A limited MDCT or sonographic examination was performed immediately after the procedure to rule out bleeding.
Biopsy material, in the form of small pieces of tissue, was sent for histologic examination preserved in a tube containing formalin. The remainder of the specimen was smeared on a slide, immersed in 96% ethyl alcohol, and sent for cytologic examination. Immunohistochemical staining was routinely performed. A biopsy was considered successful if it provided sufficient material for pathologic diagnosis.
In the presence of high clinical suspicion of lymphoma, if the biopsy result was negative for lymphoma, a decision was made by a team including a hematologist, a pathologist, and a radiologist to repeat the biopsy.
Biopsies were performed on an outpatient basis. Patients were monitored for 3 hr in the recovery area before discharge. A chest radiograph was not routinely obtained.
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A single splenic lesion was depicted in 12 patients (60%), multiple lesions were revealed in seven patients (35%), and in one patient (5%) diffuse splenic involvement was noted. Splenomegaly, as determined by measuring the cephalocaudal axis (median, 15 cm), was noted in 16 patients.
A diagnosis of lymphoma was reached by splenic small-bore cutting-edge needle biopsy in 18 patients (90%). In 14 patients, biopsy led to diagnosis of non-Hodgkin's lymphoma: follicular mixed large and small B-cell lymphoma, three; diffuse large B-cell lymphoma, seven; T-cell-rich diffuse large B-cell lymphoma, two; large B-cell lymphoma, one; and B-cell lymphoblastic lymphoma, one (REAL classification). Four patients had Hodgkin's disease.
In 15 patients (75%), a single biopsy was diagnostic, and in three patients, four repeated biopsies were performed: In one patient the first biopsy was diagnostic for high-grade lymphoma but did not yield the exact subtype. A second biopsy led to a diagnosis of B-cell lymphoblastic lymphoma. In the second patient, the first two splenic biopsies yielded necrotic material, and the third led to a diagnosis of diffuse large B-cell lymphoma. In the third patient, the first biopsy contained necrotic material, and the second led to a diagnosis of diffuse large B-cell lymphoma.
Suspected false-negative results were obtained in two patients (10%) owing to a negative first biopsy result and a decision not to repeat the biopsy. The first patient had a history of metastatic breast cancer and was treated in another hospital, where a lung biopsy performed later proved positive for small cell lymphocytic lymphoma. In the second patient, in whom a relapse of Hodgkin's disease was suspected, findings of splenic biopsy were inconclusive. He developed iliac lymphadenopathy 2 months later, which was easier and safer for repeated biopsy. Recurrent Hodgkin's disease was diagnosed.
Cytologic samples alone were diagnostic for lymphoma in six patients (30%) and suspicious for lymphoma in four (20%). By contrast, histologic samples were diagnostic for lymphoma in 17 (85%).
Subclassification of lymphoma was established by cytologic samples in three patients (15%); histologic samples resulted in subclassification in 13 (65%). The diagnostic yield was raised when cytologic and histologic results were combined: lymphoma was diagnosed in 18 (90%) and subclassified in 14 (70%, all with non-Hodgkin's lymphoma).
Only the histologic specimens were sent for immunohistochemical staining except in one case in which inadequate material was collected. Immunohistochemical staining was performed on the cytologic specimen from that patient, the only case in which lymphoma was subclassified on the basis of cytologic evidence alone.
Two cases (10%) of subcapsular splenic and intraperitoneal hemorrhage were noted on the CT examination performed immediately after the biopsy (Fig. 2). The patients were admitted to the hospital and treated conservatively. One required transfusion with two units of packed RBCs to raise the hematocrit level from 24% to 29% (normal male values, 38–52; normal female values, 36–46). The other patient did not require transfusion because the hematocrit level was stable at 30%.
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Recent publications in the English-language literature describe the result of splenic fine-needle aspiration [4–8] or biopsy [7–11] in patients with lymphoma only [9, 11] or in a mixed group of patients, some of whom had lymphoma [4–8, 10]. Limitations of these reports include small numbers of patients [8, 9] and performance of biopsy in many patients with healthy splenic architecture in whom the diagnosis of lymphoma was known [7, 9–11].
Civardi et al. [7] reported the experience of eight Italian centers with sonographically guided splenic fine-needle aspiration or core needle biopsy in 398 patients, 183 of whom were known to have lymphoma. Among the patients with lymphoma, biopsy was performed for staging, for restaging after treatment, or for suspicion of recurrence. Lymphoma was diagnosed by biopsy in 104 patients (57%).
Our report represents one of the larger samples of patients in whom splenic biopsy was performed for the initial diagnosis of lymphoma or suspected relapse. In our practice, splenic biopsies are performed only when lymphoma is suspected and the spleen is the only available target because current practice suggests that lymphoma may be staged using the combination of CT and hematologic examinations, including bone marrow biopsy for non-Hodgkin's lymphoma. A biopsy performed on normal splenic architecture is not likely to show signs of disease, but a biopsy of a splenic lesion in a patient with lymphoma is likely to prove positive for the presence of lymphoma [7, 10, 11].
The most peripheral lesion should be chosen for biopsy to avoid traversing normal splenic tissue that might bleed [12]. The biopsy sample should be taken from the periphery of the lesion itself to decrease the possibility of sampling necrotic material from the center. In our series, five patients had lesions that showed significant central necrosis. In two of the three patients in whom the biopsy was repeated, the negative findings of first biopsies contained necrotic material.
In our experience, a repeated biopsy is likely to give positive results despite a negative first result in patients in whom there is a high suspicion for lymphoma. Therefore, we recommend repeating the imaging-guided biopsy before performing open or laparoscopic procedures.
We performed small-bore cutting-edge needle core biopsy to obtain tissue for both cytologic and histologic examination and for immunohistochemical staining. The latter two are particularly important in the diagnosis of lymphoma and its subtypes and, hence, to therapeutic decision-making. Cytologic evidence alone led to a diagnosis of lymphoma in only 30% of our patients, although we suspected it in another 20%, and we could subclassify the lymphoma in only 15% of patients. This low success rate was attributed to the small quantity of material obtained and to the difficulty in differentiating malignant from healthy lymphocytes in the case of well-differentiated lymphocytic lymphoma or Hodgkin's disease. In other studies, fine-needle aspiration of the spleen had a success rate of up to 87.5% in the diagnosis of lymphoma [5, 7, 8] but was not accurate in diagnosing subtypes.
In contrast, we found that histologic samples with immunohistochemical staining revealed the diagnosis in 85% of patients and allowed further subtyping in 65% of patients. Despite the collection method using a small-bore cutting-edge needle, the tissue architecture is adequately preserved for subclassification of non-Hodgkin's lymphoma. In patients with Hodgkin's disease (n = 4), further subclassification was not performed because the treatment of Hodgkin's disease does not depend on the exact subtype.
In one patient with large cell lymphoma, the cytologic examination yielded the diagnosis despite a negative histologic biopsy. Therefore, the combination of cytologic and histologic sources raised the overall diagnostic accuracy in this series from 85% to 90% and improved subclassification from 65% to 70%. This finding is consistent with those of other reports [7, 8].
Most previous studies have reported a low complication rate after both fine-needle aspiration and small-bore cutting-edge needle biopsy of the spleen. Hemorrhage is the most common complication [7]. Other complications include pneumothorax [7], pleural effusion [2], and colonic injury [2]. The reported incidence of hemorrhage was 0–1.5% in series using either fine-needle aspiration or small-bore cutting-edge needle biopsy [2, 4–9]. Lindgren et al. [10] observed bleeding in four (13%) of 32 patients after splenic core needle biopsy using a 14-gauge needle (Tru-Cut, Baxter Healthcare, Valencia, CA). All patients required blood transfusions, and one underwent splenectomy because of uncontrolled hemorrhage. The high incidence of hemorrhage reported by Lindgren et al. probably resulted from the use of a large-bore needle.
We observed subcapsular and intraperitoneal hemorrhage in 2 (8.3%) of 24 biopsies, who were hospitalized for observation and were treated conservatively. Splenectomy was not required after the procedure. We did not obtain routine chest radiographs after biopsy, so the incidence of asymptomatic pneumothorax is unknown.
In conclusion, small-bore cutting-edge needle biopsy of the spleen using 20- or 22-gauge needles in patients with suspected lymphoma appears to be an accurate and safe procedure. It provides a high diagnostic yield with a low complication rate.
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