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Laparoscopy in Malignant Disease
LAPAROSCOPY FOR THE GENERAL SURGEON
0039-6109/92 $0.00 + .20
LAPAROSCOPY IN MALIGNANT DISEASE Frederick 1. Greene, MD
HISTORICAL OVERVIEW
Although the first documented laparoscopic examination was performed in 1901 by Ott, a Russian gynecologist,lO the techniques and indications for inspection of the peritoneal cavity have crystallized during the last decade. Kelling of Dresden introduced laparoscopy for the evaluation of gastrointestinal disease in the early 1900s and described the technique of "coelioskopie" using a cystoscope to examine the abdominal cavities of dogs. I5 During the first decade of the 20th century, the concepts of pneumoperitoneum were applied, and further developments to support the diagnostic utility of laparoscopy came from the work of Jacobaeus, who first used the term "laparoscopy." In a 1911 report,r2 Jacobaeus indicated that by using a laparoscope, diagnoses of cirrhosis, metastatic tumors, and tuberculous peritonitis could be confirmed. Although the initial attempt at laparoscopy in the United States took place in 1911 at the Johns Hopkins HospitaV further recognition of the importance of this technique was limited because of instrumentation and the restricted vision that could be realized. These early attempts utilized the cystoscope, which allowed only an acute angle of vision before forward-viewing instruments, introduced in the late 1920s, increased the viewing angle to 135 degrees. During the 1930s, John C. Ruddock and Edward Benedict were active proponents of laparoscopy in North America. 2, 18 Ruddock perfected his technique of "peritoneoscopy" and demonstrated the improvement in diagnostic accuracy using this technique. 18 Benedict reported on the usefulness of intra-abdominal From the Department of Surgery, University of South Carolina School of Medicine, Columbia, South Carolina
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endoscopy in the diagnosis of liver disease, ascites, gastric and colonic neoplasms, and gynecologic disease. 2 The importance of creating a satisfactory pneumoperitoneum was supported by Fervers in the 1930s, who advocated using oxygen or carbon dioxide rather than room air.6 In 1938, Veress, a Hungarian, developed the spring-loaded needle, permitting the safe instillation of gas into the peritoneal cavity.24 Further developments, including the introduction of the quartz light rod, which enhanced light transmission, led to the wider application of laparoscopy. The development of the fiberoptic bundle paved the way for the current rigid laparoscope. With the further advances of videoendoscopy and the inclusion of television monitoring, current techniques of laparoscopy using improved imaging have led to the wider application in the diagnosis of abdominal malignancy.
PATIENT SELECTION AND TECHNIQUE
In selecting patients for laparoscopy, it is important to consider the overall plan for the patient with malignant disease, which would include the possibility of surgical extirpation, chemotherapy, or radiation. While laparoscopy itself may be the prime mode of detection and confirmation of malignancy, more often, patients who undergo laparoscopic examination have had previous histologic confirmation by gastrointestinal endoscopic techniques or peripheral node biopsy. Every physicianendoscopist undertaking laparoscopy should have a clear understanding of the benefits offered by the procedure and should be willing to recommend avoidance of the technique if there is no definable gain for the patient. Diagnostic laparoscopy for abdominal malignancy may be accomplished using general anesthesia or local infiltration with intravenous sedation in the awake patient. While small laparoscopes have become available for use outside the operating-room setting, patients undergoing diagnostic laparoscopy usually require general anesthesia in order to tolerate the pneumoperitoneum required and to allow for open celiotomy as the next step for diagnosis or therapy should this be required. Patients who have had previous abdominal procedures should be evaluated carefully for alternative sites of placement of the initial puncture for establishing pneumoperitoneum. As the skill of the endoscopist increases, patients having previous operations for both benign and malignant processes may be approached, especially to satisfy the needs for a second look without a formal celiotomy. In order to establish a safe pneumoperitoneum in a patient with previous abdominal operations, open techniques using a Hasson cannula and adjunctive methods using ultrasound have been recommended to avoid inappropriate trocar placement. The location for placement of the Veress needle to establish a pneumoperitoneum may be determined by the site of the previous incision or by characteristics of the abdominal ultrasound or CT scan, which may help in decision-making.
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Selection of patients and the technique used for laparoscopy depend heavily on the information to be gained from the study. In patients with significant cardiac and respiratory disease who would not be candidates for open abdominal procedures that require general anesthesia, laparoscopy may in fact prove hazardous because of the establishment of both general anesthesia and a significant pneumoperitoneum. Distention of the abdomen may in fact reduce cardiac output and enhance dysrhythmias and may be contraindicated in patients with severe coronary artery disease. A thorough history and physical examination are required to evaluate a patient for diagnostic laparoscopy and should be prerequisites to determine appropriateness for this procedure. The use of laparoscopy for both diagnosis and staging of abdominal malignancy does not take place in a vacuum. Patients should also undergo diagnostic studies consisting of CT, ultrasound, or other conventional imaging techniques, which may give information not gleaned by inspection of the peritoneal cavity and its contents. An example of the complementary nature of CT scanning and laparoscopy is seen in patients with parenchymal lesions of the liver, which may not be apparent when the hepatic surface is examined laparoscopically. The CT scan, however, may give an indication of the appropriate area to be biopsied during laparoscopy. Similarly, laparoscopic examination discloses surface lesions, which are not readily apparent on the conventional tomogram. In addition, the CT scan may show ascites, which is not definable by physical examination but may be an important consideration when laparoscopy is performed. Appropriate collection of intra-abdominal fluid for cytologic study is an integral part of the laparoscopic examination and may be indicated by tomographic scanning. The surgeon-endoscopist undertaking laparoscopic examination should be prepared to achieve biopsy or cytologic studies using a number of maneuvers. The decision for secondary or tertiary trocar placement is also dictated by both the findings on previous imaging studies and the anatomy that becomes evident on laparoscopic examination. Patients undergoing laparoscopy should have either a nasogastric or an orogastric tube placed for gastric decompression as well as a Foley catheter before the establishment of a pneumoperitoneum. While the absolute necessity for antibiotic coverage in diagnostic laparoscopy has not been established, it is our preference to cover patients with a second- or third-generation cephalosporin prior to the establishment of pneumoperitoneum, because many of these patients are immunosuppressed from their malignancy. The main accessory instruments required for diagnostic laparoscopy include appropriate biopsy forceps with cautery adapters that may be placed through a 5-mm trocar as well as biopsy needles designed for placement through the abdominal wall to be directed to specific lesions noted at laparoscopy. The Tru-Cut needle is especially appropriate and may aid in the biopsy of retroperitoneal masses or lesions of the hepatic parenchyma at the time of laparoscopy. During the
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examination, it is appropriate to look carefully for evidence of ascitic fluid, especially chylous ascites, which may be present in patients with significant retroperitoneal nodal disease. The aspiration and cytologic examination of these abdominal fluids may give additional diagnostic information and should be an integral part of the overall examination. The position of the patient is important in approaching specific areas of the abdominal cavity as well as the retroperitoneum. While patients generally are placed in a steep Trendelenburg position for establishment of the initial pneumoperitoneum, those with ascites may in fact need to be in a reverse Trendelenburg position in order to have the abdominal contents float on the ascitic fluid to allow safe placement of the Veress needle in the lower abdominal region. In addition, ascitic fluid should be aspirated completely prior to the insufflation of CO2 to avoid the nuisance of bubbles that will obscure the view. To reduce further the likelihood of CO2 mixing with ascitic fluid, the Veress needle may be alternatively positioned above the ascitic fluid, allowing CO2 to be introduced above the level of the collection. In order to assess the upper abdominal contents, especially the region of the omentum, the lesser curvature of the stomach, and the liver, the patient should be placed in a reverse Trendelenburg position and tilted to the left on the operating table. Tilting the table to the right will facilitate the approach to the left lobe of the liver, the greater curvature of the stomach, the peripancreatic area, and the spleen. Using these various positions, biopsy and aspiration of ascitic fluid may be facilitated. Even in the absence of ascites, peritoneal washing may help to retrieve malignant cells and give additional information relative to metastatic disease in the peritoneal cavity. To facilitate this, a solution of normal saline (5001000 mL) is placed in the peritoneal cavity, and the patient is moved into various positions to direct flow into all areas of the abdominal cavity. Aliquots of this fluid may be removed from various locations in the peritoneal cavity and sent for cytologic study. If only diagnostic laparoscopy is to be performed, the patient generally will be able to take liquids several hours after the procedure, as only a minimal degree of ileus is produced. The Foley catheter and gastric tube may be removed after the procedure, and oral analgesics are generally adequate to overcome any pain from the trocar sites.
FINDINGS AT DIAGNOSTIC LAPAROSCOPY
Because the largest group of patients who undergo diagnostic laparoscopy are those with presumed or defined malignant processes, patients may be grouped into those with primary intra-abdominal malignancy and those with disease metastatic to the abdominal cavity. Although there are rare tumors that develop primarily from the peritoneal lining, the majority of patients who have defined peritoneal implants will have them as a result of dissemination to this layer from an intra-abdominal or extra-abdominal primary tumor.
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One specific primary peritoneal tumor that may be identified is a mesothelioma. Although benign mesothelioma is a rare entity, the differentiation between benign and malignant mesothelioma may depend on the findings of diffuse peritoneal disease or the concomitant identification of a pleural lesion that may be metastatic to the abdominal cavity. Peritoneal mesothelioma usually presents with multiple plaques or nodules and has a distinctive associated ascitic fluid, which has the consistency of heavy white syrup. The majority of patients with peritoneal mesothelioma have a history of asbestos exposure.Z3 The role of the laparoscopist in this disease is to achieve adequate biopsy of several peritoneal plaques and to recover ascitic fluid, which may be sent for cytologic examination as well as measurements of hyaluronic acid. Although there generally is minimal hepatic parenchymal involvement in primary mesothelioma, biopsy of lesions on Glisson's capsule is important. In contrast to primary mesothelioma, the surgicallaparoscopist will have the greatest experience in identifying and ,staging malignant tumors arising from the gastrointestinal tract or those tumors having an extra-abdominal source such as the lung or breast. Metastatic implants generally reach the peritoneal surface through hematologic or lymphatic spread; therefore, involvement of the liver as well as nodebearing areas is common. During laparoscopy, intrahepatic metastases may be indirectly assessed by noting dimpling of the hepatic capsule, especially in association with lesions that are pale. One specific tumor with an extra-abdominal source that causes pigmented lesions, especially on the surface of the liver, is a melanoma. Because intra-abdominal metastases from melanoma are common and may present as a smallbowel obstruction, the laparoscopist must be aware that the abdominal manifestations of melanoma may appear without a specific primary lesion being elucidated. During recent years, an increasing incidence of Kaposi's sarcoma has been noted in association with the human immunodeficiency virus. Kaposi's lesions may be identified because of a characteristic purple color of the implants on the surface of the liver and peritoneum. Although extrahepatic lesions generally precede the development and identification of liver nodules, a recent report by Hasan and associates l l describes isolated foci of Kaposi's sarcoma identified on the hepatic surface using laparoscopy. The assessment of the intra-abdominal area must include a careful visual inspection of the omentum, especially in patients who may have a primary malignancy in the ovary or endometrium. Identification of lesions on the diaphragm, especially in ovarian malignancy, is important to allow full staging of the abdominal process. Although solitary lesions may be noted, the entire abdominal cavity must be visualized for a meaningful and complete staging procedure. One of the additional roles of laparoscopy is to differentiate benign and malignant processes in the abdominal cavity, especially when ascites is present. One important disease that is characterized by ascites and multiple implants on the peritoneum is tuberculous peritonitis.
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Biopsies of tuberculous implants may fail to show characteristic granuloma formation or Mycobacterium. It is important to note, however, that visual inspection alone in patients with tuberculous ascites may not be definitive in differentiating between a malignant and an inflammatory process. 17 Although primary hepatic malignancy does occur in North America, hepatoma and other varieties of primary liver tumors are generally rare compared with metastatic lesions that involve the hepatic parenchyma. Jeffers and associates 13 report the use of laparoscopy in 27 patients with primary hepatocellular carcinoma. The diagnosis was achieved using laparoscopically directed aspiration with a Chiba needle. The reasons for unresectability in this group were multiple hepatic lesions (78%), association with advanced cirrhosis (85%), and peritoneal metastases (7%). The benefits of using laparoscopy in the evaluation of patients with primary hepatic malignancy are to confirm the diagnosis with biopsy under direct vision, to detect associated cirrhosis or portal hypertension, and to detect small secondary lesions not found by conventional imaging studies. As previously noted, the use of CT and ultrasound for the complete evaluation of the abdomen gives information on the staging of abdominal tumors that may not be available with laparoscopy alone. The main advantage of laparoscopic examination is to help in surgical decisionmaking in the selection of either curative or palliative procedures or the possible decision to avoid an open surgical approach. The ability to provide endoscopic palliative manipulation of the pancreatic and biliary tree with the use of stents or other appropriate drainage devices supports the need for complete staging and the identification of an important subset of patients who may not benefit from a conventional surgical bypass. This is especially true in patients with malignancy of the pancreatic head or distal bile duct, who may have evidence of metastatic disease that is not obvious on routine imaging studies. It has been clearly shown that conventional imaging may underestimate the stage of abdominal malignancy, thus leading to an open surgical procedure that may provide little benefit to the patient. While ultrasound- or CT-guided biopsy is very appropriate to assess isolated lesions in the hepatic parenchyma, the addition of laparoscopy will increase the likelihood of disclosing small implants on the surface of the liver or peritoneum in an additional 40% of patients. As techniques of fine-needle aspiration become more universally accepted, cytologic determination of intra parenchymal tumor may be used in addition to conventional needle biopsy techniques. 4, 5 Recent experience in staging patients with esophageal and gastric malignancy9,26 has shown an increased rate of liver involvement, which supports the use of systemic therapy in addition to conventional resection. Although laparoscopy has not become a standard technique in the staging of colorectal tumors with presumed hepatic metastases, it is likely that recurrence in patients with isolated hepatic metastases may be anticipated through the use of laparoscopic techniques that identify small metastases on the hepatic surface. Even the addition of magnetic
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resonance imaging has failed to identify small metastases in the hepatic parenchyma. Although hepatic metastases are important sources of failure in pancreatic carcinoma, the real staging benefit for laparoscopy in this disease lies in the identification of surface implantation and potentially minimal ascites that may indicate a high likelihood of recurrence despite aggressive surgical extirpation. 25 Approximately 35% to 40% of patients with evidence of localized disease on conventional imaging studies may in fact have disseminated pancreatic carcinoma that will doom the patient to recurrence despite aggressive resection. Warshaw and coworkers25 have reported the evaluation of 88 patients deemed surgical candidates who had carcinomas of the pancreas or ampullary region. Using CT, magnetic resonance imaging, angiography and laparoscopy, 90% of the unresectable tumors were identified. Importantly, laparoscopy and biopsy identified 96% of the patients having small hepatic or peritoneal implants. These patients are much better served using palliative approaches to obstruction. Percutaneous or endoscopic stent placement may, in fact, give the same long-term survival rate as traditional bypass procedures. 20 Although techniques of percutaneous fine-needle aspiration and needle biopsy have been utilized to diagnose pancreatic malignancy, laparoscopic examination and direct needle biopsy are safe and reproducible in the differentiation of masses in the pancreatic parenchyma. 4 The surgical laparoscopist must become skilled at approaching the pancreatic body and tail through the division of the gastrocolic omentum or by entering the retrogastric space via the gastrohepatic ligament along the lesser curve of the stomach. Once these maneuvers are learned, approaches to the node-bearing areas draining the stomach, pancreas, and esophagus are possible and allow for direct biopsy and partial resection of potentially involved nodes. Salky et aP9 report retroperitoneal evaluation by visualization and direct biopsy in 6% of 316laparoscopic examinations. The diagnoses in these patients included primarily Hodgkin's and non-Hodgkin'S lymphoma and were made through obtaining sufficient node-bearing tissue for full cytologic investigation and typing of the lymphomas. Using a laparoscopic approach to the retroperitoneum, celiotomy was avoided in 16 of 19 patients. The approach to the retroperitoneum will be facilitated in the future by the development of laparoscopes that allow direct entry into the lesser omental bursa, expanding the visibility of the endoscopist into these areas.
LAPAROSCOPY FOR SECOND-LOOK PROCEDURES
The role of laparoscopy in the evaluation for recurrent tumor has yet to be defined. The concept of the second look is to base reexploration of the abdomen on studies such as tumor markers, CT
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scanning, or sonography in the hope that identification and removal of residual or recurrent tumor will help to palliate or even cure the patient. The application of laparoscopy in this setting has been limited because of the inability to identify anatomic landmarks or residual tumor in the face of previous exploration. A traditional role for the second look has been in the management of ovarian carcinoma. Marti-Vicente and coworkers 16 have reported 205 laparoscopic studies in this setting, with 72 examinations performed on 52 patients in complete clinical remission. Forty-four laparoscopic studies were performed for a second look, while 28 evaluations were for a third look. In 48.6% of the studies, residual tumor was found, thereby avoiding a second-look laparotomy, according to the authors. This subset of patients may still benefit, however, from an open surgical procedure with further identification of tumor and adequate debulking of residual disease. This view is supported by noting that 31 % of the patients had persistent tumor found at laparotomy when second-look laparoscopy was deemed negative. This finding further supports the axiom that a negative laparoscopic examination for abdominal staging cannot definitely place the patient in a disease-free category but should be complemented by a formal celiotomy if indicated. The value of second-look procedures for abdominal malignancy continues to be debated, especially in regard to colorectal cancer, in which follow-up with assays for carcinoembryonic antigen (CEA) may identify a subset of patients with localized identifiable and resectable disease. There have been no reports assessing the role of laparoscopic examination in these patients because of the difficulty in examining the peritoneal cavity in those having previous celiotomy and resection. As laparoscopic techniques improve and directed imaging using intraabdominal ultrasound or monoclonal antibodies is introduced, there may be a defined role for the laparoscopic second look in abdominal malignancy.
STAGING OF LYMPHOMAS
During the last several decades, a frequent role for the surgeon was to help in the identification of patients with abdominal involvement with Hodgkin's and non-Hodgkin'S lymphomas. Through specific maneuvers, including hepatic wedge and needle biopsy, splenectomy, retroperitoneal and iliac node dissection, and general inspection of the entire peritoneal cavity, the pathologic stage of a lymphoma was increased in approximately 30% of patients. 8 With the application of sensitive CT, lymphangiography, and percutaneous biopsy techniques, celiotomy for the staging and management of lymphomas has become less common. The complete identification of possible abdominal involvement by lymphoma continues to be important and may be enhanced by staging using laparoscopic techniques. Although visceral
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involvement of the abdominal cavity cannot be totally excluded by a negative laparoscopy, the complementary use of laparoscopy and radiologic imaging may be as effective as open celiotomy while avoiding the potential consequences of splenectomy. While some authors have advocated routine biopsy of the spleen using the laparoscope,21 generally, full staging may be accomplished by sampling of the retroperitoneal nodes, hepatic biopsy, and visualization of the abdominal cavity in association with bone marrow aspiration or biopsy. Routine laparoscopic staging for Hodgkin's disease has shown unsuspected hepatic involvement in 6% of patients, occult splenic involvement in 13%, and an upgrading of staging in 23% of patients undergoing laparoscopic study.22 In non-Hodgkin's lymphoma, involvement of the liver was present in 20% of patients, which attests to the greater systemic involvement by this lymphoma. In addition to the initial diagnosis or staging, patients undergoing radiation and chemotherapy for lymphoma may be reassessed using laparoscopic techniques as a possible second look when imaging studies suggest recurrence in the abdominal cavity.
APPROACH TO LYMPH NODES
The approach to node-bearing areas in the abdominal cavity is an important skill for the surgicallaparoscopist who is assessing lymphoma and metastatic spread from solid tumors of the gastrointestinal tract. Isolated lymph nodes may be identified in the mesentery of the small and large bowel and may be easily approached with proper positioning of the patient and placement of additional trocars to facilitate retraction and dissection of the mesentery. The more difficult regions to approach laparoscopically are in the areas surrounding the stomach and pancreas and the nodes in the retroperitoneum. It is extremely important to review carefully the conventional CT scans or sonographic studies prior to beginning the laparoscopic study in order to utilize all the information available in directing the intra-abdominal examination to node-bearing areas that may yield the best information. Imaging studies should be available in the operating room or endoscopy suite for easy reference during laparoscopy. It is important for the laparoscopist to remove enough nodal tissue to allow the pathologist not only to make an appropriate diagnosis of lymphoma, but also to characterize the lymphoma fully according to its B- or T-cell subset. Staging of lymphomas using specific histologic and immunochemical techniques is important in determining the appropriate therapy as well as in assessing the natural history of the disease. Solid tumors of the gastrointestinal tract may have early and significant nodal spread and may, in fact, make conventional surgical resection inappropriate in patients who may otherwise be treated with
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the palliation afforded by stent placement or laser ablation. The assessment of the nodes in these patients is much more specific when approached laparoscopically. A study by Watt and associates 26 in patients with esophageal and gastric carcinoma showed that the sensitivity of laparoscopy in assessing nodal involvement is approximately twice that of conventional ultrasound and CT. In this study, the overall diagnostic accuracy of laparoscopy was 72% while the accuracies of ultrasound and CT were 52% and 57%, respectively. It is clear that appropriate evaluation of nodal areas using laparoscopy may stage disease more thoroughly than conventional imaging techniques.
CONTRAINDICATIONS AND COMPLICATIONS
The principal contraindication to laparoscopy for patients with suspected or proved abdominal malignancy is a situation in which either the information that might be gained will not be meaningful in making future therapeutic decisions or in which an open abdominal exploration is inevitable or strongly indicated. Voltaire, the well-known French satirist, was highly critical of physicians when he wrote, "The art of medicine is to amuse the patient while nature cures the disease." Physicians, especially those using interventional techniques, should act only when the intervention is especially meaningful for the patient. Aside from the place of laparoscopic examination in the algorithmic approach to the cancer patient, specific contraindications exist when introduction of the laparoscope would be hazardous or unrevealing. Abdominal wall sepsis, gastrointestinal distention from ileus or mechanical obstruction, clinical evidence of intra-abdominal sepsis, or significant adhesions from previous abdominal exploration are reasons to abandon laparoscopic approaches. If general anesthesia is chosen, advanced cardiac or pulmonary disease may indicate asignificant risk, especially when pneumoperitoneum may enhance cardiac rhythm disturbances or reduce cardiac output significantly. Specific maneuvers performed through the laparoscope may cause bleeding or viscus perforation. Because a primary goal is to assess the liver for malignancy, biopsy must be used routinely to assess superficial as well as deep lesions. Biopsy sites must be evaluated carefully for both bleeding and bile leaks. Bleeding may be especially troublesome in patients with associated cirrhosis, portal hypertension, and coagulopathy. The presence of advanced cirrhosis and abnormalities of coagulation is a relative contraindication to laparoscopic biopsy. A specific complication, although uncommon, is the development of abdominal wall metastases as a consequence of introducing the laparoscope in patients with peritoneal implants or malignant ascites. Cava et aP reported a subcutaneous metastasis from gastric carcinoma following laparoscopy. Implantation in the presence of ovarian malignancy has also occurred. 3 However, there is no evidence that seeding
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of trocar sites is a common phenomenon, and the possibility should not be viewed as a deterrent to laparoscopic intervention. Management of the trocar site is important, especially in patients with malignant ascites, because ascitic leak or herniation may occur secondary to inadequate closure of these areas. Careful approximation of fascia is necessary to ensure a reduction in future development of hernias. Similarly, diligent attention to hemostasis in the subcutaneous tissue of the trocar site is mandatory in patients with coagulopathy or thrombocytopenia secondary to their malignancies.
FUTURE TRENDS AND CONCEPTS
Along with the fervor for and benefits created by laparoscopic therapeutic intervention in biliary tract disease, appendicitis, abdominal wall hernia, peptic ulcer, and esophageal reflux, new awareness has been kindled of the advantages of laparoscopy for the staging of abdominal malignancy. Surgical training programs are beginning to introduce trainees to the role and techniques of diagnostic laparoscopy and to use the principles and techniques to foster guidelines for training and therapeutic maneuvers. As surgeons begin to realize that ablative or extirpative procedures are doomed to failure in curing patients with diffuse abdominal metastases disclosed on a laparoscopic assessment, palliative measures such as stent placement, balloon dilatation, intraluminal high-dose radiation, and laser techniques will be more commonly employed by surgical endoscopists and gastroenterologists. Similarly, it is hoped that the use of systemic chemotherapy will achieve better specificity in cell destruction in patients identified laparoscopically to have uncontained disease in the abdominal cavity. As more patients are staged through accurate imaging or laparoscopic techniques, current staging systems must remain flexible to include information gained both clinically and pathologically from these techniques. Use of TNM staging, as developed and promulgated by coordinated multispecialty dialogue through the American Joint Committee on Cancer Staging (AJCc), will be strengthened by consideration of staging subsets identified by laparoscopy or laparoscopic secondlook procedures. In addition to staging accuracy, the laparoscope will prove to be a vehicle for allowing other interventional modalities such as intra-abdominal ultrasound to be applied. This technique will extend the use of future generations of laparoscopes in the evaluation of organ parenchyma and the retroperitoneum. The patient with an abdominal malignancy will eventually benefit from direct introduction of therapeutic modalities through laparoscopic means. High-dose brachytherapy or hyperthermia may be applied using endoscopic placement of catheters directed into the common bile duct, pancreatic duct, or liver; photodynamic therapy to the abdominal cavity may be directed using
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appropriate laser energy passed through endoscopic means; and cryoablation for treatment of isolated liver metastases will be possible using transabdominal laparoscopic techniques facilitated by intra-abdominal sonography. The application of laparoscopy, both diagnostic and therapeutic, in the management of patients with abdominal malignancy will be limited only by the creativity and expertise of the physician and the instrument maker.
References 1. Bernheim B: Organoscopy: Cystoscopy of the abdominal cavity. Ann Surg 53:764, 1911 2. Benedict EB: Peritoneoscopy. N Engl J Med 218:713-714, 1938 3. Cava A, Roman J, Quintela AG, et al: Subcutaneous metastasis following laparoscopy in gastric adenocarcinoma. Eur J Surg Oncol 16:63-67, 1990 4. Cuschieri A, Hall AW, Clark J: Value of laparoscopy in the diagnosis and management of pancreatic carcinoma. Gut 19:672-677, 1978 5. Cuschieri A: Laparoscopy for pancreatic cancer: Does it benefit the patient? Eur J Surg Oncol 14:41-44, 1988 6. Fervers C: Die Laparoskopie mit dem Zystoskope. Med Sche Klin 29:1042-1045, 1933 7. Fornari F, Rapaccini GL, Cavanna L, et al: Diagnosis of hepatic lesions: Ultrasonically guided fine needle biopsy or laparoscopy? Gastrointest Endosc 34:422-425, 1988 8. Glatstein E, Guernsey JM, Rosenberg SA, et al: The value of laparotomy and splenectomy in the staging of Hodgkin's disease. Cancer 24:709-715, 1969 9. Gross E, Bancewicz J, Ingram G: Assessment of gastric carcinoma by laparoscopy. Br Med J 288:157-161, 1984 10. Gunning JE: The history of laparoscopy. J Reprod Med 12:223-231, 1974 11. Hasan FA, Jeffers LJ, Welsh SW, et al: Hepatic involvement as the primary manifestation of Kaposi's sarcoma in the acquired immune deficiency syndrome. Am J Gastroenterol 84:1449-1451, 1989 12. Jacobaeus HC: Kurze Obersicht tiber meine Erfahrungen mit der Laparoskopie. Munch Med Wochenschr 58:2017-2019, 1911 13. Jeffers L, Spieglman G, Reddy KR, et al: Laparoscopically directed fine needle aspiration for the diagnosis of hepatocellular carcinoma: A safe and accurate technique. Gastrointest Endosc 34:235-237, 1988 14. Kalk H: Erfahrungen mit der Laparoskopie. Z Klin Med 111:303-348, 1929 15. Kelling G: Zur Celioskopie. Arch Klin Chir 126:226-229, 1923 16. Marti-Vicente A, Sainz S, Soriano G, et al: Utilidad de la laparoscopia como methodo de second-look en las neoplasias de ovario. Rev Esp Enf Digest 77:275-278, 1990 17. Reddy KR, DiPrima RE, Raskin JB, et al: Tuberculous peritonitis: Laparoscopic diagnosis of an uncommon disease in the United States. Gastrointest Endosc 34:422425, 1988 18. Ruddock JC: Peritoneoscopy. Surg Gynecol Obstet 65:623-639, 1937 19. Salky BA, Bauer H, Gerlerent 1M, et al: The use of laparoscopy in retroperitoneal pathology. Gastrointest Endosc 34:227-230, 1988 20. Speer A, Cotton PB, Russell RCG, et al: Randomized trial of endoscopic versus percutaneous stent insertion in malignant obstructive jaundice. Lancet 2:57-62, 1987 21. Spinelli P, Beretta G, Bayetta E, et al: Laparoscopy and laparotomy combined with bone marrow biopsy in staging of Hodgkin's disease. Br Med J 4:554-556, 1975 22. Spinelli P, Difelice G: Laparoscopy in abdominal malignancies. Prob Gen Surg 8:329347, 1991 23. van Gelder T, Hoogsteden HC, Versnel MA, et al: Malignant peritoneal mesothelioma: A series of 19 cases. Digestion 43:222-227, 1989 24. Veress J: Neues Instrument zur Ausftihrung von Brust oder Bauchpunktionen. Dtsch Med Wochenschr 64:1480-1481, 1938
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25. Warshaw AL, Gu Z, Wittenberg
J, et al: Preoperative staging and assessment of resectability of pancreatic cancer. Arch Surg 125:230-233, 1990 26. Watt I, Stewart I, Anderson D, et al: Laparoscopy, ultrasound and computed tomography in cancer of the oesophagus and gastric cardia: A prospective comparison for detecting intra-abdominal metastases. Br J Surg 76:1036-1043, 1989 Address reprint requests to Frederick L. Greene, MD University of South Carolina School of Medicine Department of Surgery Two Richland Medical Park, Suite 402 Columbia, SC 29203
0039-6109/92 $0.00 + .20
LAPAROSCOPY IN MALIGNANT DISEASE Frederick 1. Greene, MD
HISTORICAL OVERVIEW
Although the first documented laparoscopic examination was performed in 1901 by Ott, a Russian gynecologist,lO the techniques and indications for inspection of the peritoneal cavity have crystallized during the last decade. Kelling of Dresden introduced laparoscopy for the evaluation of gastrointestinal disease in the early 1900s and described the technique of "coelioskopie" using a cystoscope to examine the abdominal cavities of dogs. I5 During the first decade of the 20th century, the concepts of pneumoperitoneum were applied, and further developments to support the diagnostic utility of laparoscopy came from the work of Jacobaeus, who first used the term "laparoscopy." In a 1911 report,r2 Jacobaeus indicated that by using a laparoscope, diagnoses of cirrhosis, metastatic tumors, and tuberculous peritonitis could be confirmed. Although the initial attempt at laparoscopy in the United States took place in 1911 at the Johns Hopkins HospitaV further recognition of the importance of this technique was limited because of instrumentation and the restricted vision that could be realized. These early attempts utilized the cystoscope, which allowed only an acute angle of vision before forward-viewing instruments, introduced in the late 1920s, increased the viewing angle to 135 degrees. During the 1930s, John C. Ruddock and Edward Benedict were active proponents of laparoscopy in North America. 2, 18 Ruddock perfected his technique of "peritoneoscopy" and demonstrated the improvement in diagnostic accuracy using this technique. 18 Benedict reported on the usefulness of intra-abdominal From the Department of Surgery, University of South Carolina School of Medicine, Columbia, South Carolina
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endoscopy in the diagnosis of liver disease, ascites, gastric and colonic neoplasms, and gynecologic disease. 2 The importance of creating a satisfactory pneumoperitoneum was supported by Fervers in the 1930s, who advocated using oxygen or carbon dioxide rather than room air.6 In 1938, Veress, a Hungarian, developed the spring-loaded needle, permitting the safe instillation of gas into the peritoneal cavity.24 Further developments, including the introduction of the quartz light rod, which enhanced light transmission, led to the wider application of laparoscopy. The development of the fiberoptic bundle paved the way for the current rigid laparoscope. With the further advances of videoendoscopy and the inclusion of television monitoring, current techniques of laparoscopy using improved imaging have led to the wider application in the diagnosis of abdominal malignancy.
PATIENT SELECTION AND TECHNIQUE
In selecting patients for laparoscopy, it is important to consider the overall plan for the patient with malignant disease, which would include the possibility of surgical extirpation, chemotherapy, or radiation. While laparoscopy itself may be the prime mode of detection and confirmation of malignancy, more often, patients who undergo laparoscopic examination have had previous histologic confirmation by gastrointestinal endoscopic techniques or peripheral node biopsy. Every physicianendoscopist undertaking laparoscopy should have a clear understanding of the benefits offered by the procedure and should be willing to recommend avoidance of the technique if there is no definable gain for the patient. Diagnostic laparoscopy for abdominal malignancy may be accomplished using general anesthesia or local infiltration with intravenous sedation in the awake patient. While small laparoscopes have become available for use outside the operating-room setting, patients undergoing diagnostic laparoscopy usually require general anesthesia in order to tolerate the pneumoperitoneum required and to allow for open celiotomy as the next step for diagnosis or therapy should this be required. Patients who have had previous abdominal procedures should be evaluated carefully for alternative sites of placement of the initial puncture for establishing pneumoperitoneum. As the skill of the endoscopist increases, patients having previous operations for both benign and malignant processes may be approached, especially to satisfy the needs for a second look without a formal celiotomy. In order to establish a safe pneumoperitoneum in a patient with previous abdominal operations, open techniques using a Hasson cannula and adjunctive methods using ultrasound have been recommended to avoid inappropriate trocar placement. The location for placement of the Veress needle to establish a pneumoperitoneum may be determined by the site of the previous incision or by characteristics of the abdominal ultrasound or CT scan, which may help in decision-making.
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Selection of patients and the technique used for laparoscopy depend heavily on the information to be gained from the study. In patients with significant cardiac and respiratory disease who would not be candidates for open abdominal procedures that require general anesthesia, laparoscopy may in fact prove hazardous because of the establishment of both general anesthesia and a significant pneumoperitoneum. Distention of the abdomen may in fact reduce cardiac output and enhance dysrhythmias and may be contraindicated in patients with severe coronary artery disease. A thorough history and physical examination are required to evaluate a patient for diagnostic laparoscopy and should be prerequisites to determine appropriateness for this procedure. The use of laparoscopy for both diagnosis and staging of abdominal malignancy does not take place in a vacuum. Patients should also undergo diagnostic studies consisting of CT, ultrasound, or other conventional imaging techniques, which may give information not gleaned by inspection of the peritoneal cavity and its contents. An example of the complementary nature of CT scanning and laparoscopy is seen in patients with parenchymal lesions of the liver, which may not be apparent when the hepatic surface is examined laparoscopically. The CT scan, however, may give an indication of the appropriate area to be biopsied during laparoscopy. Similarly, laparoscopic examination discloses surface lesions, which are not readily apparent on the conventional tomogram. In addition, the CT scan may show ascites, which is not definable by physical examination but may be an important consideration when laparoscopy is performed. Appropriate collection of intra-abdominal fluid for cytologic study is an integral part of the laparoscopic examination and may be indicated by tomographic scanning. The surgeon-endoscopist undertaking laparoscopic examination should be prepared to achieve biopsy or cytologic studies using a number of maneuvers. The decision for secondary or tertiary trocar placement is also dictated by both the findings on previous imaging studies and the anatomy that becomes evident on laparoscopic examination. Patients undergoing laparoscopy should have either a nasogastric or an orogastric tube placed for gastric decompression as well as a Foley catheter before the establishment of a pneumoperitoneum. While the absolute necessity for antibiotic coverage in diagnostic laparoscopy has not been established, it is our preference to cover patients with a second- or third-generation cephalosporin prior to the establishment of pneumoperitoneum, because many of these patients are immunosuppressed from their malignancy. The main accessory instruments required for diagnostic laparoscopy include appropriate biopsy forceps with cautery adapters that may be placed through a 5-mm trocar as well as biopsy needles designed for placement through the abdominal wall to be directed to specific lesions noted at laparoscopy. The Tru-Cut needle is especially appropriate and may aid in the biopsy of retroperitoneal masses or lesions of the hepatic parenchyma at the time of laparoscopy. During the
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examination, it is appropriate to look carefully for evidence of ascitic fluid, especially chylous ascites, which may be present in patients with significant retroperitoneal nodal disease. The aspiration and cytologic examination of these abdominal fluids may give additional diagnostic information and should be an integral part of the overall examination. The position of the patient is important in approaching specific areas of the abdominal cavity as well as the retroperitoneum. While patients generally are placed in a steep Trendelenburg position for establishment of the initial pneumoperitoneum, those with ascites may in fact need to be in a reverse Trendelenburg position in order to have the abdominal contents float on the ascitic fluid to allow safe placement of the Veress needle in the lower abdominal region. In addition, ascitic fluid should be aspirated completely prior to the insufflation of CO2 to avoid the nuisance of bubbles that will obscure the view. To reduce further the likelihood of CO2 mixing with ascitic fluid, the Veress needle may be alternatively positioned above the ascitic fluid, allowing CO2 to be introduced above the level of the collection. In order to assess the upper abdominal contents, especially the region of the omentum, the lesser curvature of the stomach, and the liver, the patient should be placed in a reverse Trendelenburg position and tilted to the left on the operating table. Tilting the table to the right will facilitate the approach to the left lobe of the liver, the greater curvature of the stomach, the peripancreatic area, and the spleen. Using these various positions, biopsy and aspiration of ascitic fluid may be facilitated. Even in the absence of ascites, peritoneal washing may help to retrieve malignant cells and give additional information relative to metastatic disease in the peritoneal cavity. To facilitate this, a solution of normal saline (5001000 mL) is placed in the peritoneal cavity, and the patient is moved into various positions to direct flow into all areas of the abdominal cavity. Aliquots of this fluid may be removed from various locations in the peritoneal cavity and sent for cytologic study. If only diagnostic laparoscopy is to be performed, the patient generally will be able to take liquids several hours after the procedure, as only a minimal degree of ileus is produced. The Foley catheter and gastric tube may be removed after the procedure, and oral analgesics are generally adequate to overcome any pain from the trocar sites.
FINDINGS AT DIAGNOSTIC LAPAROSCOPY
Because the largest group of patients who undergo diagnostic laparoscopy are those with presumed or defined malignant processes, patients may be grouped into those with primary intra-abdominal malignancy and those with disease metastatic to the abdominal cavity. Although there are rare tumors that develop primarily from the peritoneal lining, the majority of patients who have defined peritoneal implants will have them as a result of dissemination to this layer from an intra-abdominal or extra-abdominal primary tumor.
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One specific primary peritoneal tumor that may be identified is a mesothelioma. Although benign mesothelioma is a rare entity, the differentiation between benign and malignant mesothelioma may depend on the findings of diffuse peritoneal disease or the concomitant identification of a pleural lesion that may be metastatic to the abdominal cavity. Peritoneal mesothelioma usually presents with multiple plaques or nodules and has a distinctive associated ascitic fluid, which has the consistency of heavy white syrup. The majority of patients with peritoneal mesothelioma have a history of asbestos exposure.Z3 The role of the laparoscopist in this disease is to achieve adequate biopsy of several peritoneal plaques and to recover ascitic fluid, which may be sent for cytologic examination as well as measurements of hyaluronic acid. Although there generally is minimal hepatic parenchymal involvement in primary mesothelioma, biopsy of lesions on Glisson's capsule is important. In contrast to primary mesothelioma, the surgicallaparoscopist will have the greatest experience in identifying and ,staging malignant tumors arising from the gastrointestinal tract or those tumors having an extra-abdominal source such as the lung or breast. Metastatic implants generally reach the peritoneal surface through hematologic or lymphatic spread; therefore, involvement of the liver as well as nodebearing areas is common. During laparoscopy, intrahepatic metastases may be indirectly assessed by noting dimpling of the hepatic capsule, especially in association with lesions that are pale. One specific tumor with an extra-abdominal source that causes pigmented lesions, especially on the surface of the liver, is a melanoma. Because intra-abdominal metastases from melanoma are common and may present as a smallbowel obstruction, the laparoscopist must be aware that the abdominal manifestations of melanoma may appear without a specific primary lesion being elucidated. During recent years, an increasing incidence of Kaposi's sarcoma has been noted in association with the human immunodeficiency virus. Kaposi's lesions may be identified because of a characteristic purple color of the implants on the surface of the liver and peritoneum. Although extrahepatic lesions generally precede the development and identification of liver nodules, a recent report by Hasan and associates l l describes isolated foci of Kaposi's sarcoma identified on the hepatic surface using laparoscopy. The assessment of the intra-abdominal area must include a careful visual inspection of the omentum, especially in patients who may have a primary malignancy in the ovary or endometrium. Identification of lesions on the diaphragm, especially in ovarian malignancy, is important to allow full staging of the abdominal process. Although solitary lesions may be noted, the entire abdominal cavity must be visualized for a meaningful and complete staging procedure. One of the additional roles of laparoscopy is to differentiate benign and malignant processes in the abdominal cavity, especially when ascites is present. One important disease that is characterized by ascites and multiple implants on the peritoneum is tuberculous peritonitis.
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Biopsies of tuberculous implants may fail to show characteristic granuloma formation or Mycobacterium. It is important to note, however, that visual inspection alone in patients with tuberculous ascites may not be definitive in differentiating between a malignant and an inflammatory process. 17 Although primary hepatic malignancy does occur in North America, hepatoma and other varieties of primary liver tumors are generally rare compared with metastatic lesions that involve the hepatic parenchyma. Jeffers and associates 13 report the use of laparoscopy in 27 patients with primary hepatocellular carcinoma. The diagnosis was achieved using laparoscopically directed aspiration with a Chiba needle. The reasons for unresectability in this group were multiple hepatic lesions (78%), association with advanced cirrhosis (85%), and peritoneal metastases (7%). The benefits of using laparoscopy in the evaluation of patients with primary hepatic malignancy are to confirm the diagnosis with biopsy under direct vision, to detect associated cirrhosis or portal hypertension, and to detect small secondary lesions not found by conventional imaging studies. As previously noted, the use of CT and ultrasound for the complete evaluation of the abdomen gives information on the staging of abdominal tumors that may not be available with laparoscopy alone. The main advantage of laparoscopic examination is to help in surgical decisionmaking in the selection of either curative or palliative procedures or the possible decision to avoid an open surgical approach. The ability to provide endoscopic palliative manipulation of the pancreatic and biliary tree with the use of stents or other appropriate drainage devices supports the need for complete staging and the identification of an important subset of patients who may not benefit from a conventional surgical bypass. This is especially true in patients with malignancy of the pancreatic head or distal bile duct, who may have evidence of metastatic disease that is not obvious on routine imaging studies. It has been clearly shown that conventional imaging may underestimate the stage of abdominal malignancy, thus leading to an open surgical procedure that may provide little benefit to the patient. While ultrasound- or CT-guided biopsy is very appropriate to assess isolated lesions in the hepatic parenchyma, the addition of laparoscopy will increase the likelihood of disclosing small implants on the surface of the liver or peritoneum in an additional 40% of patients. As techniques of fine-needle aspiration become more universally accepted, cytologic determination of intra parenchymal tumor may be used in addition to conventional needle biopsy techniques. 4, 5 Recent experience in staging patients with esophageal and gastric malignancy9,26 has shown an increased rate of liver involvement, which supports the use of systemic therapy in addition to conventional resection. Although laparoscopy has not become a standard technique in the staging of colorectal tumors with presumed hepatic metastases, it is likely that recurrence in patients with isolated hepatic metastases may be anticipated through the use of laparoscopic techniques that identify small metastases on the hepatic surface. Even the addition of magnetic
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resonance imaging has failed to identify small metastases in the hepatic parenchyma. Although hepatic metastases are important sources of failure in pancreatic carcinoma, the real staging benefit for laparoscopy in this disease lies in the identification of surface implantation and potentially minimal ascites that may indicate a high likelihood of recurrence despite aggressive surgical extirpation. 25 Approximately 35% to 40% of patients with evidence of localized disease on conventional imaging studies may in fact have disseminated pancreatic carcinoma that will doom the patient to recurrence despite aggressive resection. Warshaw and coworkers25 have reported the evaluation of 88 patients deemed surgical candidates who had carcinomas of the pancreas or ampullary region. Using CT, magnetic resonance imaging, angiography and laparoscopy, 90% of the unresectable tumors were identified. Importantly, laparoscopy and biopsy identified 96% of the patients having small hepatic or peritoneal implants. These patients are much better served using palliative approaches to obstruction. Percutaneous or endoscopic stent placement may, in fact, give the same long-term survival rate as traditional bypass procedures. 20 Although techniques of percutaneous fine-needle aspiration and needle biopsy have been utilized to diagnose pancreatic malignancy, laparoscopic examination and direct needle biopsy are safe and reproducible in the differentiation of masses in the pancreatic parenchyma. 4 The surgical laparoscopist must become skilled at approaching the pancreatic body and tail through the division of the gastrocolic omentum or by entering the retrogastric space via the gastrohepatic ligament along the lesser curve of the stomach. Once these maneuvers are learned, approaches to the node-bearing areas draining the stomach, pancreas, and esophagus are possible and allow for direct biopsy and partial resection of potentially involved nodes. Salky et aP9 report retroperitoneal evaluation by visualization and direct biopsy in 6% of 316laparoscopic examinations. The diagnoses in these patients included primarily Hodgkin's and non-Hodgkin'S lymphoma and were made through obtaining sufficient node-bearing tissue for full cytologic investigation and typing of the lymphomas. Using a laparoscopic approach to the retroperitoneum, celiotomy was avoided in 16 of 19 patients. The approach to the retroperitoneum will be facilitated in the future by the development of laparoscopes that allow direct entry into the lesser omental bursa, expanding the visibility of the endoscopist into these areas.
LAPAROSCOPY FOR SECOND-LOOK PROCEDURES
The role of laparoscopy in the evaluation for recurrent tumor has yet to be defined. The concept of the second look is to base reexploration of the abdomen on studies such as tumor markers, CT
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scanning, or sonography in the hope that identification and removal of residual or recurrent tumor will help to palliate or even cure the patient. The application of laparoscopy in this setting has been limited because of the inability to identify anatomic landmarks or residual tumor in the face of previous exploration. A traditional role for the second look has been in the management of ovarian carcinoma. Marti-Vicente and coworkers 16 have reported 205 laparoscopic studies in this setting, with 72 examinations performed on 52 patients in complete clinical remission. Forty-four laparoscopic studies were performed for a second look, while 28 evaluations were for a third look. In 48.6% of the studies, residual tumor was found, thereby avoiding a second-look laparotomy, according to the authors. This subset of patients may still benefit, however, from an open surgical procedure with further identification of tumor and adequate debulking of residual disease. This view is supported by noting that 31 % of the patients had persistent tumor found at laparotomy when second-look laparoscopy was deemed negative. This finding further supports the axiom that a negative laparoscopic examination for abdominal staging cannot definitely place the patient in a disease-free category but should be complemented by a formal celiotomy if indicated. The value of second-look procedures for abdominal malignancy continues to be debated, especially in regard to colorectal cancer, in which follow-up with assays for carcinoembryonic antigen (CEA) may identify a subset of patients with localized identifiable and resectable disease. There have been no reports assessing the role of laparoscopic examination in these patients because of the difficulty in examining the peritoneal cavity in those having previous celiotomy and resection. As laparoscopic techniques improve and directed imaging using intraabdominal ultrasound or monoclonal antibodies is introduced, there may be a defined role for the laparoscopic second look in abdominal malignancy.
STAGING OF LYMPHOMAS
During the last several decades, a frequent role for the surgeon was to help in the identification of patients with abdominal involvement with Hodgkin's and non-Hodgkin'S lymphomas. Through specific maneuvers, including hepatic wedge and needle biopsy, splenectomy, retroperitoneal and iliac node dissection, and general inspection of the entire peritoneal cavity, the pathologic stage of a lymphoma was increased in approximately 30% of patients. 8 With the application of sensitive CT, lymphangiography, and percutaneous biopsy techniques, celiotomy for the staging and management of lymphomas has become less common. The complete identification of possible abdominal involvement by lymphoma continues to be important and may be enhanced by staging using laparoscopic techniques. Although visceral
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involvement of the abdominal cavity cannot be totally excluded by a negative laparoscopy, the complementary use of laparoscopy and radiologic imaging may be as effective as open celiotomy while avoiding the potential consequences of splenectomy. While some authors have advocated routine biopsy of the spleen using the laparoscope,21 generally, full staging may be accomplished by sampling of the retroperitoneal nodes, hepatic biopsy, and visualization of the abdominal cavity in association with bone marrow aspiration or biopsy. Routine laparoscopic staging for Hodgkin's disease has shown unsuspected hepatic involvement in 6% of patients, occult splenic involvement in 13%, and an upgrading of staging in 23% of patients undergoing laparoscopic study.22 In non-Hodgkin's lymphoma, involvement of the liver was present in 20% of patients, which attests to the greater systemic involvement by this lymphoma. In addition to the initial diagnosis or staging, patients undergoing radiation and chemotherapy for lymphoma may be reassessed using laparoscopic techniques as a possible second look when imaging studies suggest recurrence in the abdominal cavity.
APPROACH TO LYMPH NODES
The approach to node-bearing areas in the abdominal cavity is an important skill for the surgicallaparoscopist who is assessing lymphoma and metastatic spread from solid tumors of the gastrointestinal tract. Isolated lymph nodes may be identified in the mesentery of the small and large bowel and may be easily approached with proper positioning of the patient and placement of additional trocars to facilitate retraction and dissection of the mesentery. The more difficult regions to approach laparoscopically are in the areas surrounding the stomach and pancreas and the nodes in the retroperitoneum. It is extremely important to review carefully the conventional CT scans or sonographic studies prior to beginning the laparoscopic study in order to utilize all the information available in directing the intra-abdominal examination to node-bearing areas that may yield the best information. Imaging studies should be available in the operating room or endoscopy suite for easy reference during laparoscopy. It is important for the laparoscopist to remove enough nodal tissue to allow the pathologist not only to make an appropriate diagnosis of lymphoma, but also to characterize the lymphoma fully according to its B- or T-cell subset. Staging of lymphomas using specific histologic and immunochemical techniques is important in determining the appropriate therapy as well as in assessing the natural history of the disease. Solid tumors of the gastrointestinal tract may have early and significant nodal spread and may, in fact, make conventional surgical resection inappropriate in patients who may otherwise be treated with
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the palliation afforded by stent placement or laser ablation. The assessment of the nodes in these patients is much more specific when approached laparoscopically. A study by Watt and associates 26 in patients with esophageal and gastric carcinoma showed that the sensitivity of laparoscopy in assessing nodal involvement is approximately twice that of conventional ultrasound and CT. In this study, the overall diagnostic accuracy of laparoscopy was 72% while the accuracies of ultrasound and CT were 52% and 57%, respectively. It is clear that appropriate evaluation of nodal areas using laparoscopy may stage disease more thoroughly than conventional imaging techniques.
CONTRAINDICATIONS AND COMPLICATIONS
The principal contraindication to laparoscopy for patients with suspected or proved abdominal malignancy is a situation in which either the information that might be gained will not be meaningful in making future therapeutic decisions or in which an open abdominal exploration is inevitable or strongly indicated. Voltaire, the well-known French satirist, was highly critical of physicians when he wrote, "The art of medicine is to amuse the patient while nature cures the disease." Physicians, especially those using interventional techniques, should act only when the intervention is especially meaningful for the patient. Aside from the place of laparoscopic examination in the algorithmic approach to the cancer patient, specific contraindications exist when introduction of the laparoscope would be hazardous or unrevealing. Abdominal wall sepsis, gastrointestinal distention from ileus or mechanical obstruction, clinical evidence of intra-abdominal sepsis, or significant adhesions from previous abdominal exploration are reasons to abandon laparoscopic approaches. If general anesthesia is chosen, advanced cardiac or pulmonary disease may indicate asignificant risk, especially when pneumoperitoneum may enhance cardiac rhythm disturbances or reduce cardiac output significantly. Specific maneuvers performed through the laparoscope may cause bleeding or viscus perforation. Because a primary goal is to assess the liver for malignancy, biopsy must be used routinely to assess superficial as well as deep lesions. Biopsy sites must be evaluated carefully for both bleeding and bile leaks. Bleeding may be especially troublesome in patients with associated cirrhosis, portal hypertension, and coagulopathy. The presence of advanced cirrhosis and abnormalities of coagulation is a relative contraindication to laparoscopic biopsy. A specific complication, although uncommon, is the development of abdominal wall metastases as a consequence of introducing the laparoscope in patients with peritoneal implants or malignant ascites. Cava et aP reported a subcutaneous metastasis from gastric carcinoma following laparoscopy. Implantation in the presence of ovarian malignancy has also occurred. 3 However, there is no evidence that seeding
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of trocar sites is a common phenomenon, and the possibility should not be viewed as a deterrent to laparoscopic intervention. Management of the trocar site is important, especially in patients with malignant ascites, because ascitic leak or herniation may occur secondary to inadequate closure of these areas. Careful approximation of fascia is necessary to ensure a reduction in future development of hernias. Similarly, diligent attention to hemostasis in the subcutaneous tissue of the trocar site is mandatory in patients with coagulopathy or thrombocytopenia secondary to their malignancies.
FUTURE TRENDS AND CONCEPTS
Along with the fervor for and benefits created by laparoscopic therapeutic intervention in biliary tract disease, appendicitis, abdominal wall hernia, peptic ulcer, and esophageal reflux, new awareness has been kindled of the advantages of laparoscopy for the staging of abdominal malignancy. Surgical training programs are beginning to introduce trainees to the role and techniques of diagnostic laparoscopy and to use the principles and techniques to foster guidelines for training and therapeutic maneuvers. As surgeons begin to realize that ablative or extirpative procedures are doomed to failure in curing patients with diffuse abdominal metastases disclosed on a laparoscopic assessment, palliative measures such as stent placement, balloon dilatation, intraluminal high-dose radiation, and laser techniques will be more commonly employed by surgical endoscopists and gastroenterologists. Similarly, it is hoped that the use of systemic chemotherapy will achieve better specificity in cell destruction in patients identified laparoscopically to have uncontained disease in the abdominal cavity. As more patients are staged through accurate imaging or laparoscopic techniques, current staging systems must remain flexible to include information gained both clinically and pathologically from these techniques. Use of TNM staging, as developed and promulgated by coordinated multispecialty dialogue through the American Joint Committee on Cancer Staging (AJCc), will be strengthened by consideration of staging subsets identified by laparoscopy or laparoscopic secondlook procedures. In addition to staging accuracy, the laparoscope will prove to be a vehicle for allowing other interventional modalities such as intra-abdominal ultrasound to be applied. This technique will extend the use of future generations of laparoscopes in the evaluation of organ parenchyma and the retroperitoneum. The patient with an abdominal malignancy will eventually benefit from direct introduction of therapeutic modalities through laparoscopic means. High-dose brachytherapy or hyperthermia may be applied using endoscopic placement of catheters directed into the common bile duct, pancreatic duct, or liver; photodynamic therapy to the abdominal cavity may be directed using
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appropriate laser energy passed through endoscopic means; and cryoablation for treatment of isolated liver metastases will be possible using transabdominal laparoscopic techniques facilitated by intra-abdominal sonography. The application of laparoscopy, both diagnostic and therapeutic, in the management of patients with abdominal malignancy will be limited only by the creativity and expertise of the physician and the instrument maker.
References 1. Bernheim B: Organoscopy: Cystoscopy of the abdominal cavity. Ann Surg 53:764, 1911 2. Benedict EB: Peritoneoscopy. N Engl J Med 218:713-714, 1938 3. Cava A, Roman J, Quintela AG, et al: Subcutaneous metastasis following laparoscopy in gastric adenocarcinoma. Eur J Surg Oncol 16:63-67, 1990 4. Cuschieri A, Hall AW, Clark J: Value of laparoscopy in the diagnosis and management of pancreatic carcinoma. Gut 19:672-677, 1978 5. Cuschieri A: Laparoscopy for pancreatic cancer: Does it benefit the patient? Eur J Surg Oncol 14:41-44, 1988 6. Fervers C: Die Laparoskopie mit dem Zystoskope. Med Sche Klin 29:1042-1045, 1933 7. Fornari F, Rapaccini GL, Cavanna L, et al: Diagnosis of hepatic lesions: Ultrasonically guided fine needle biopsy or laparoscopy? Gastrointest Endosc 34:422-425, 1988 8. Glatstein E, Guernsey JM, Rosenberg SA, et al: The value of laparotomy and splenectomy in the staging of Hodgkin's disease. Cancer 24:709-715, 1969 9. Gross E, Bancewicz J, Ingram G: Assessment of gastric carcinoma by laparoscopy. Br Med J 288:157-161, 1984 10. Gunning JE: The history of laparoscopy. J Reprod Med 12:223-231, 1974 11. Hasan FA, Jeffers LJ, Welsh SW, et al: Hepatic involvement as the primary manifestation of Kaposi's sarcoma in the acquired immune deficiency syndrome. Am J Gastroenterol 84:1449-1451, 1989 12. Jacobaeus HC: Kurze Obersicht tiber meine Erfahrungen mit der Laparoskopie. Munch Med Wochenschr 58:2017-2019, 1911 13. Jeffers L, Spieglman G, Reddy KR, et al: Laparoscopically directed fine needle aspiration for the diagnosis of hepatocellular carcinoma: A safe and accurate technique. Gastrointest Endosc 34:235-237, 1988 14. Kalk H: Erfahrungen mit der Laparoskopie. Z Klin Med 111:303-348, 1929 15. Kelling G: Zur Celioskopie. Arch Klin Chir 126:226-229, 1923 16. Marti-Vicente A, Sainz S, Soriano G, et al: Utilidad de la laparoscopia como methodo de second-look en las neoplasias de ovario. Rev Esp Enf Digest 77:275-278, 1990 17. Reddy KR, DiPrima RE, Raskin JB, et al: Tuberculous peritonitis: Laparoscopic diagnosis of an uncommon disease in the United States. Gastrointest Endosc 34:422425, 1988 18. Ruddock JC: Peritoneoscopy. Surg Gynecol Obstet 65:623-639, 1937 19. Salky BA, Bauer H, Gerlerent 1M, et al: The use of laparoscopy in retroperitoneal pathology. Gastrointest Endosc 34:227-230, 1988 20. Speer A, Cotton PB, Russell RCG, et al: Randomized trial of endoscopic versus percutaneous stent insertion in malignant obstructive jaundice. Lancet 2:57-62, 1987 21. Spinelli P, Beretta G, Bayetta E, et al: Laparoscopy and laparotomy combined with bone marrow biopsy in staging of Hodgkin's disease. Br Med J 4:554-556, 1975 22. Spinelli P, Difelice G: Laparoscopy in abdominal malignancies. Prob Gen Surg 8:329347, 1991 23. van Gelder T, Hoogsteden HC, Versnel MA, et al: Malignant peritoneal mesothelioma: A series of 19 cases. Digestion 43:222-227, 1989 24. Veress J: Neues Instrument zur Ausftihrung von Brust oder Bauchpunktionen. Dtsch Med Wochenschr 64:1480-1481, 1938
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25. Warshaw AL, Gu Z, Wittenberg
J, et al: Preoperative staging and assessment of resectability of pancreatic cancer. Arch Surg 125:230-233, 1990 26. Watt I, Stewart I, Anderson D, et al: Laparoscopy, ultrasound and computed tomography in cancer of the oesophagus and gastric cardia: A prospective comparison for detecting intra-abdominal metastases. Br J Surg 76:1036-1043, 1989 Address reprint requests to Frederick L. Greene, MD University of South Carolina School of Medicine Department of Surgery Two Richland Medical Park, Suite 402 Columbia, SC 29203