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(Radiology. 1999;212:439-444.)
© RSNA, 1999


Gastrointestinal Imaging

Recurrent Gallbladder Carcinoma along Laparoscopic Cholecystectomy Port Tracks: CT Demonstration1

Corinne B. Winston, MD, June W. Chen, MD, Yuman Fong, MD, Lawrence H. Schwartz, MD and David M. Panicek, MD

1 From the Department of Radiology, Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York, NY 10021. Received July 31, 1998; revision requested September 10; revision received October 28; accepted January 11, 1999. Address reprint requests to C.B.W. (e-mail: winstonc@mskcc.org).


    Abstract
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To describe the computed tomographic (CT) appearance of recurrent gallbladder carcinoma along port tracks after laparoscopic cholecystectomy and to assess the effect of recurrence on patient care.

MATERIALS AND METHODS: Seventeen abdominal CT scans in 16 of 19 consecutive patients who underwent hepatic resection for gallbladder carcinoma diagnosed at laparoscopic cholecystectomy were reviewed retrospectively. Medical records were reviewed to determine the clinical effect of tumor recurrence along a port track.

RESULTS: CT revealed 12 tumor recurrences along laparoscopic port tracks in six (32%) patients (mean, two recurrences per patient; range, one to four per patient). Eight (67%) CT-depicted recurrences appeared homogeneous, and nine (75%) directly involved subjacent omental fat. The mass was the only site of recurrence at CT in two (33%) patients. The presence of an abdominal wall tumor recurrence affected patient care in four (67%) of six patients. Histopathologic examination results confirmed recurrent tumor in all five (100%) patients who underwent biopsy.

CONCLUSION: Tumor recurrence along port tracks is a potential complication of laparoscopic cholecystectomy when gallbladder carcinoma is present, even after subsequent hepatic resection is performed for attempted cure. Recurrences appear as a new or enlarging abdominal wall mass, often involving subjacent omental fat, and may be the only site of recurrent disease at CT. Demonstration of abdominal wall tumor recurrence affects patient care.

Index terms: Abdominal wall, 762.331 • Cholecystectomy, 762.1267 • Gallbladder, CT, 762.12112, 762.12115 • Gallbladder, MR, 762.121411 • Gallbladder, neoplasms, 762.32 • Laparoscopic surgery, 762.1267 • Surgery, complications, 762.458


    Introduction
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Laparoscopic cholecystectomy has become increasingly accepted in the treatment of uncomplicated symptomatic cholelithiasis (1). Complications of laparoscopic cholecystectomy previously described include bile duct injury, retained stones, spilled gallstones throughout the abdomen, bowel perforation from trocar insertion, and abdominal wall hematoma (2). An additional serious complication of laparoscopic cholecystectomy with delayed manifestations is the inadvertent dissemination of unsuspected gallbladder carcinoma (316).

Approximately 15%–30% of gallbladder carcinomas are detected incidentally at microscopic review of cholecystectomy specimens (16). Hepatic resection, common bile duct excision, and portal lymphadenectomy have been suggested as treatment for gallbladder carcinoma that is incidentally detected at cholecystectomy (17). Patients are often followed up with computed tomography (CT) after hepatic resection to assess for tumor recurrence. The purpose of our study was to describe the CT appearance of laparoscopic port track tumor recurrences in patients who underwent definitive hepatic resection for gallbladder carcinoma diagnosed at laparoscopic cholecystectomy and to assess the effect of the abdominal wall tumor recurrence on patient care.


    MATERIALS AND METHODS
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Patient Population
In a search of the hepatobiliary tumor database at our institution, we identified 42 patients referred from January 1991 to November 1996 for definitive hepatic resection of gallbladder carcinoma that was diagnosed at laparoscopic cholecystectomy. Carcinoma was suspected prior to the laparoscopic cholecystectomy in three (7%) patients. Laparoscopic cholecystectomy was converted to open cholecystectomy in five patients owing to extensive inflammation within the gallbladder fossa (n = 2), discovery of unsuspected gallbladder carcinoma intraoperatively (n = 2), and detection of unsuspected hepatic metastases (n = 1).

One (2%) patient had a T1 gallbladder carcinoma (ie, tumor confined to the mucosal or muscular layer) (18) for which no additional surgery was considered necessary. Twenty-two patients had lesions that were deemed unresectable at imaging after laparoscopic cholecystectomy or at exploratory laparotomy. Nineteen patients (14 women, five men; mean age, 60 years; age range, 34–78 years) underwent a definitive surgical procedure for potential cure. The mean interval between laparoscopic cholecystectomy and definitive hepatic surgery was 40 days (range, 18–94 days).

Thirteen patients underwent an extended right hepatectomy, common bile duct excision, portal lymphadenectomy, and hepaticojejunostomy. Five patients underwent resection of hepatic segments 4 and 5, excision of the common bile duct, lymphadenectomy, and hepaticojejunostomy. One patient underwent a limited en bloc resection of the liver surrounding the gallbladder fossa, common bile duct excision, lymphadenectomy, and hepaticojejunostomy. The final histopathologic diagnoses were adenocarcinoma (n = 17) and adenosquamous carcinoma (n = 2).

Of the 19 patients who underwent definitive surgical resection, one patient had a T1 tumor with a positive lymph node, eight had T2 tumors (tumor invading the perimuscular connective tissue without extension into the liver), and eight had T3 tumors (tumor invading the serosa and one adjacent organ, or invading into liver less than 2 cm). Two patients had a T4 tumor (more than 2-cm invasion into liver). Seventeen port tracks were resected in eight patients at definitive surgery: Three patients underwent resection of one track, two patients underwent resection of two tracks, two underwent resection of three tracks, and one underwent resection of four tracks. Gallbladder carcinoma was identified at histopathologic examination in three (18%) of the tracks resected.

CT Findings
Retrospective review of abdominal CT scans obtained following definitive hepatic resection was performed by two experienced oncologic radiologists (C.B.W., D.M.P.) in consensus to assess for the presence of anterior abdominal wall tumor recurrence. If multiple postoperative CT scans had been obtained in a single patient, the most recent scan (ie, the examination performed the longest time after hepatic resection) was reviewed. All CT scans were evaluated in conjunction with a prior CT (n = 15) or magnetic resonance (MR) (n = 2) image for comparison. If the comparison examination revealed evidence of an additional anterior abdominal wall mass, data also were obtained from that study (n = 1).

Seventeen CT examinations in 16 (84%) patients (11 women, five men; age range, 34–78 years) were included in this study. No postoperative CT scans were available in three (16%) patients. The mean interval between the definitive hepatic resection and follow-up CT was 18 months (range, 1–62 months). Fifteen CT examinations were performed with use of intravenous contrast material; 17 scans were obtained with use of oral contrast material. Ten of 17 examinations were performed by using a helical technique.

A new or enlarging anterior abdominal wall mass was considered diagnostic of tumor recurrence. Linear infiltration within the anterior abdominal wall was considered to represent postoperative change. The radiologists (C.B.W., D.M.P.) determined the location of the mass and assessed for associated involvement of subjacent omental fat. The relative size of the mass was calculated as the product of the greatest perpendicular diameters obtained from an axial image. Masses were categorized as homogeneous or heterogeneous. The presence of a mesh prosthesis, lymphadenopathy, hepatic metastases, and peritoneal carcinomatosis was recorded.

Clinical Follow-up
Medical records were reviewed to assess for clinical evidence of abdominal wall tumor recurrence and the effect of an abdominal wall tumor recurrence on patient care. Review of histopathology reports and surgical notes was performed to confirm the presence of recurrent tumor in those patients who underwent biopsy and to determine whether any of the laparoscopic port tracks were resected at the time of definitive surgery.


    RESULTS
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
CT revealed 12 abdominal wall tumor recurrences along the laparoscopic port tracks in six (32%) patients. Five (83%) of the six patients had more than one recurrence (four patients had two recurrences and one patient had three). The mean interval between definitive hepatic resection and abdominal wall tumor recurrence seen at CT was 17 months (range, 6–41 months). Four recurrences were along the port track near the lateral aspect of the right rectus abdominis muscle, four were located just anterior to or within the right rectus abdominis muscle port track, and two were located within the left rectus abdominis muscle port track. One recurrence was located along the periumbilical port track, and one was along the subxiphoid port track. Two patients had a prior abdominal wall tumor recurrence surgically resected with placement of a mesh prosthesis; CT revealed recurrent tumor along the prosthesis in both patients.

The mean bidimensional product of the abdominal wall mass was 29.7 cm2 (range, 1.2–217.0 cm2). Nine (75%) recurrent masses directly involved the subjacent omental fat (Figs 13). All nine of these recurrences had peritoneal carcinomatosis elsewhere in the abdomen at CT. None of the anterior abdominal wall tumor recurrences without extension into the omental fat had peritoneal carcinomatosis at CT. Eight (67%) masses were of homogeneous soft-tissue attenuation. Ten patients had no evidence of recurrent tumor within the anterior abdominal wall muscles at CT.



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Figure 1a. Tumor recurrence along the port track near the lateral border of the right rectus abdominis muscle. (a) Axial CT image obtained following laparoscopic cholecystectomy reveals postsurgical change in the anterior abdominal wall along the laparoscopic port site (arrow). (b, c) Follow-up axial CT images obtained 6 months after a reveal a new mass along the initial laparoscopic port track (arrow, b); the mass extends into the omental fat (arrow, c). Histopathologic examination results confirmed the presence of recurrent gallbladder carcinoma.

 


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Figure 1b. Tumor recurrence along the port track near the lateral border of the right rectus abdominis muscle. (a) Axial CT image obtained following laparoscopic cholecystectomy reveals postsurgical change in the anterior abdominal wall along the laparoscopic port site (arrow). (b, c) Follow-up axial CT images obtained 6 months after a reveal a new mass along the initial laparoscopic port track (arrow, b); the mass extends into the omental fat (arrow, c). Histopathologic examination results confirmed the presence of recurrent gallbladder carcinoma.

 


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Figure 1c. Tumor recurrence along the port track near the lateral border of the right rectus abdominis muscle. (a) Axial CT image obtained following laparoscopic cholecystectomy reveals postsurgical change in the anterior abdominal wall along the laparoscopic port site (arrow). (b, c) Follow-up axial CT images obtained 6 months after a reveal a new mass along the initial laparoscopic port track (arrow, b); the mass extends into the omental fat (arrow, c). Histopathologic examination results confirmed the presence of recurrent gallbladder carcinoma.

 


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Figure 2a. Tumor recurrence along the large laparoscopic port track. (a) Axial spin-echo T1-weighted (repetition time, 650 msec; echo time, 9 msec) MR image obtained following laparoscopic cholecystectomy reveals linear postsurgical change within the subcutaneous fat along the laparoscopic track (arrow). (b) Axial CT image obtained 1 year after definitive hepatic surgery reveals a large mass (arrows) in the location of the laparoscopic track seen in a; the mass involves subcutaneous fat, abdominal wall muscles, and omental fat.

 


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Figure 2b. Tumor recurrence along the large laparoscopic port track. (a) Axial spin-echo T1-weighted (repetition time, 650 msec; echo time, 9 msec) MR image obtained following laparoscopic cholecystectomy reveals linear postsurgical change within the subcutaneous fat along the laparoscopic track (arrow). (b) Axial CT image obtained 1 year after definitive hepatic surgery reveals a large mass (arrows) in the location of the laparoscopic track seen in a; the mass involves subcutaneous fat, abdominal wall muscles, and omental fat.

 


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Figure 3a. Tumor recurrence along the subxiphoid port track. (a) Axial CT image reveals soft-tissue nodules within the subcutaneous fat of the anterior abdominal wall along the subxiphoid laparoscopic port track (arrows). (b) Axial CT image obtained 2 cm caudad to a reveals soft-tissue nodules (arrow) within the omental fat. Histopathologic examination results confirmed the presence of recurrent gallbladder carcinoma.

 


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Figure 3b. Tumor recurrence along the subxiphoid port track. (a) Axial CT image reveals soft-tissue nodules within the subcutaneous fat of the anterior abdominal wall along the subxiphoid laparoscopic port track (arrows). (b) Axial CT image obtained 2 cm caudad to a reveals soft-tissue nodules (arrow) within the omental fat. Histopathologic examination results confirmed the presence of recurrent gallbladder carcinoma.

 
Histopathologic examination results confirmed the presence of recurrent gallbladder carcinoma in all five (100%) of the patients with CT evidence of anterior abdominal wall tumor who underwent biopsy, three by means of fine-needle aspiration and two by means of wide excisional biopsy. Because one patient refused treatment, no biopsy was performed; however, an abdominal wall tumor recurrence was suspected clinically. Five (42%) of the 12 abdominal wall tumor recurrences appeared in port tracks that were surgically resected at definitive surgery; only three (60%) of these sites had revealed foci of tumor at initial resection.

The abdominal wall tumor recurrence was the only site of recurrent abdominal disease seen at CT in two (33%) of the six patients. One of these patients developed additional anterior abdominal wall masses and peritoneal carcinomatosis at a subsequent CT examination. Information from that subsequent CT examination was included in the data. Four patients (67%) had disease elsewhere seen at CT (two patients had carcinomatosis; two had both lymphadenopathy and carcinomatosis). None of the six had hepatic metastases.

Clinical follow-up results obtained a minimum of 1 month following definitive hepatic resection were available in 17 (89%) patients: in six (100%) patients with CT evidence of port track tumor recurrences and in 10 (100%) patients without CT evidence of abdominal wall tumor recurrence. One patient had clinical follow-up but no postoperative CT scan. The two patients without clinical follow-up did not have a postoperative CT scan available for evaluation. None of the 10 patients without CT evidence of recurrent tumor in the anterior abdominal wall had clinical evidence of an abdominal wall mass (mean clinical follow-up, 22 months; range, 1–63 months after definitive hepatic resection). One of these patients died of sepsis 1 month following surgery.

The presence of an abdominal wall tumor recurrence affected patient care in four (67%) of six patients. One patient underwent chemotherapy, one underwent surgical resection of the abdominal wall mass, one underwent surgical resection and chemotherapy, and one underwent radiation therapy. An abdominal wall tumor recurrence potentially affected management in all patients; one patient died of sepsis prior to the initiation of therapy, and one patient refused treatment.


    DISCUSSION
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Laparoscopic cholecystectomy has become increasingly accepted as an alternative treatment for symptomatic uncomplicated cholelithiasis owing to the decreased postoperative pain, shorter hospitalization, and lower cost as compared with open cholecystectomy (1,19,20). It has been estimated that approximately 80% of cholecystectomies nationwide are performed laparoscopically (21). However, if gallbladder carcinoma is suspected preoperatively, on the basis of either clinical or radiologic findings, laparoscopic cholecystectomy should not be performed and open cholecystectomy, hepatic resection, and lymph node dissection may be indicated (3,4,10,12,13,16,2225).

Typically, 3–4 L of carbon dioxide is introduced into the peritoneal cavity via a periumbilical port site. A laparoscopic camera usually is placed through this port site. After insufflation of the peritoneal cavity, three additional trocars are introduced into the anterior abdominal wall with direct laparoscopic visualization, which provides portals for the laparoscopic instruments. One portal usually is located in the subxiphoid region, one in the right upper quadrant (along the right midclavicular line), and the third further caudad, lateral to the right rectus abdominis muscle (19). If additional traction is required, a trocar may be inserted in the left upper quadrant (26). This procedure enables the surgeon to remove the gallbladder without a large abdominal wall incision. An estimated 70,000 laparoscopic cholecystectomies were performed in 1990 (16).

A potentially serious complication of laparoscopic cholecystectomy is the inadvertent dissemination of unsuspected gallbladder carcinoma. Clinical symptoms of gallbladder carcinoma are similar to chronic cholecystitis; include weight loss, pain, and jaundice; and often mask the preoperative diagnosis of gallbladder carcinoma. In a study of 50 patients by Kumar and Aggarwal (27), a preoperative clinical diagnosis of gallbladder carcinoma was made in less than half of the patients with histopathologic proof of gallbladder carcinoma. Shirai et al (18) examined 241 consecutive patients with gallbladder carcinoma treated with surgical resection; only 102 (42%) of these patients had disease diagnosed correctly preoperatively. Even with thorough preoperative evaluation, 15%–30% of gallbladder carcinomas are detected incidentally at microscopic review of the surgical specimens (16). The subgroup of patients with only microscopic evidence of disease has a better prognosis (16).

Because all 19 patients in our study underwent laparoscopic cholecystectomy at outside institutions, we did not have access to the preoperative imaging studies and could not assess whether findings suggestive of gallbladder carcinoma were present. However, even if gallbladder carcinoma is not evident on preoperative imaging studies, the surgeon needs to scrutinize the surgical specimen carefully at the time of the laparoscopic cholecystectomy and obtain a frozen section if a suspicious lesion is detected (10,16,24,28). If gallbladder carcinoma is detected intraoperatively, a more complete staging procedure and hepatic resection, as well as resection of the port sites, may be indicated.

In our study, three (18%) of the 17 port tracks resected at subsequent definitive surgery revealed foci of adenocarcinoma, which likely resulted from seeding at laparoscopy. Han-Joo and Tapan (29) reported a case of microscopic tumor foci detected in a port track that was resected at the time of definitive hepatic surgery performed 18 days after laparoscopic cholecystectomy.

Six (32%) of the 19 patients in our study who underwent definitive hepatic surgery for potential cure had tumor recurrence along a laparoscopic track seen at CT a mean of 17 months after the initial laparoscopic procedure. Because most outside surgical reports were not available, it was not possible to determine the specific port site through which the gallbladder was laparoscopically removed. However, given the presence of multiple abdominal wall tumor recurrences in a single patient (five [83%] patients had more than one anterior abdominal wall tumor recurrence), we conclude that tumor also recurred along other laparoscopic port tracks. Nine (75%) of the 12 anterior abdominal wall masses extended directly into the subjacent omental fat, presumably along the track of the laparoscopic instruments.

There are surgical case reports (38,1016,30) of abdominal wall tumor recurrence following laparoscopic cholecystectomy and occurring both at the site through which the gallbladder was removed as well as along trocar sites through which the laparoscopic instruments were inserted. Several hypotheses have been proposed to explain these findings. Direct tumor spread to the anterior abdominal wall may occur at removal of the gallbladder. The laparoscopic instruments used to mobilize the gallbladder during surgery may be inoculated with tumor cells and may seed the anterior abdominal wall at their removal (3,23,28). In addition, tumor cells may undergo aerosolization at insufflation of the peritoneum and may seed the port sites at the time of deflation (31).

The gallbladder may be torn when extensive retraction is required to obtain adequate exposure of the porta hepatis or at extraction through the anterior abdominal wall incision site (32). The rate of gallbladder rupture at removal from the abdomen during laparoscopic cholecystectomy has been reported to be as high as 24%–33% (32). It has been suggested that the wound site has increased capillary formation and thus provides an ideal milieu for tumor implantation (7,28,30).

Wibbenmeyer et al (24) have reported that gallbladder carcinoma recurs more rapidly after laparoscopic cholecystectomy than after open cholecystectomy. The pattern of tumor recurrence also differs between these procedures. Whereas local peritoneal tumor recurrence by direct tumor extension is more common after open cholecystectomy, port site tumor recurrence and diffuse peritoneal disease is more common after laparoscopic cholecystectomy (24).

Owing to increased awareness of laparoscopic port site tumor recurrence, it has now become the standard surgical practice at our institution to excise the laparoscopic port sites at the time of definitive hepatic resection. Five (42%) of the 12 abdominal wall tumor recurrences in our study occurred at port tracks that had been resected at the time of definitive surgery. No tumor was detected at histopathologic examination in two of the sites resected in which gallbladder carcinoma subsequently recurred.

A possible explanation for this is that the spatial relation of the skin, anterior abdominal wall muscles, and the intervening fascia changes at the time of the laparoscopic surgery; when the abdomen is insufflated with carbon dioxide, the abdominal wall muscles are in a different position in relation to the skin incision site than when the abdomen is deflated (as it is at definitive hepatic resection). Thus, when the surgeon excises the port track on the basis of the skin incision, the actual oblique track through the abdominal wall may not be completely excised. In addition, tumor may seed the fascial planes at the time of the laparoscopic cholecystectomy and spread between the muscle layers.

The goals of definitive resection of gallbladder carcinoma following routine cholecystectomy include removal of any potential residual tumor within the gallbladder bed, resection of portal and paraaortic lymph nodes, and reestablishment of biliary drainage (17). Patients with T2 or greater gallbladder carcinoma that is detected incidentally at cholecystectomy have improved survival if a radical second operation is performed (17,18). For patients with T1 tumor with clear surgical margins obtained at cholecystectomy, close-interval follow-up without a second resection is recommended (28).

The actual prevalence of abdominal wall tumor recurrence in the patient group in our study is likely higher than our data suggest. Patients who underwent treatment on the basis of physical examination without CT documentation were not included in our study group. One patient who had three port track tumor recurrences at CT had a fourth recurrence that was detected at physical examination and that was resected immediately prior to CT, which then revealed only a postoperative fluid collection in that region. In addition, it is possible that if we obtained CT follow-up in those patients considered to have inoperable gallbladder carcinoma after laparoscopic cholecystectomy, the number of abdominal wall tumor recurrences would have been even higher. However, we chose to evaluate that subgroup of patients who were treated with definitive hepatic surgery—theoretically, the group with the best prognosis.

Several other limitations of our study should be noted. We did not have access to the surgical reports from the laparoscopic cholecystectomies performed at other institutions and cannot determine if the gallbladder was torn at surgery or if gallstones were spilled into the abdomen. As this is a retrospective study, the interval we report between definitive hepatic surgery and CT evidence of recurrent tumor is an overestimation of the true interval before the abdominal wall tumor recurrence might have been visible at CT. Some patients may have undergone CT examinations elsewhere that were not available to us or may have had clinical evidence of a mass prior to the CT examination. In at least one patient, CT provided the initial depiction of an abdominal wall tumor recurrence. A prospective study with CT scans obtained at frequent, regular intervals would be required to determine the rate of tumor recurrence. Our study was not intended to determine the sensitivity or specificity of CT in the detection of abdominal wall recurrence of gallbladder carcinoma but rather to assess the CT appearance of tumor seeding along laparoscopic tracks.

Finally, it is possible that recurrences in some patients may have occurred along surgical drain tracks rather than along laparoscopic port tracks. However, when surgical drains are inserted at laparoscopic cholecystectomy, they usually are placed through a laparoscopic port incision. Regardless, the principles involved in both types of recurrence are essentially the same.

In conclusion, gallbladder carcinoma can recur in laparoscopic port tracks even if surgical resection of the port sites is performed at subsequent hepatic resection for attempted cure. Recurrent tumor may appear as a new or enlarging mass along the anterior abdominal wall with extension into the subjacent omental fat. Owing to the increasing performance of laparoscopic cholecystectomy, port site tumor recurrence of unsuspected gallbladder carcinoma may become a more common event. Our findings underscore the desirability for preoperative identification of gallbladder carcinoma, as this will substantially affect initial surgical planning. In addition, the anterior abdominal wall should be closely scrutinized at postoperative CT, as the discovery of tumor recurrence affects patient care.


    Footnotes
 
Author contributions: Guarantors of integrity of entire study, C.B.W., J.W.C., D.M.P.; study concepts, C.B.W., J.W.C., Y.F., D.M.P.; study design, C.B.W., J.W.C., D.M.P.; definition of intellectual content, all authors; literature research, C.B.W.; data acquisition, C.B.W., J.W.C., D.M.P.; data analysis, C.B.W.; manuscript preparation, C.B.W., D.M.P.; manuscript editing and review, all authors.


    References
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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RADIOLOGY RADIOGRAPHICS RSNA JOURNALS ONLINE