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Annals of Surgical Oncology 8:38-43 (2001)
© 2001 Society of Surgical Oncology

ORIGINAL ARTICLES

Role for Surgical Cytoreduction in Multimodality Treatments for Cancer

Martin D. McCarter, MD and Yuman Fong, MD

From the Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York.

Correspondence: Address correspondence and reprint requests to: Dr. Yuman Fong, Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY 10021; Fax: 212-639-4031; E-mail: fongy{at}mskcc.org

Key Words: Surgery— • Cytoreduction— • Liver— • Ovary— • Cancer.


   INTRODUCTION
TOP
 INTRODUCTION
REFERENCES
 
Radical surgery traditionally has been considered for cancer patients only when complete excision of tumor can be achieved. In the era when procedures such as hepatectomy, pancreatectomy, or pneumonectomy were associated with an operative mortality of 10% to 20%, such procedures could be justified only by potentially curative outcome.1–3 Cytoreduction, i.e., treatment that incompletely eradicates tumor, has, therefore, traditionally been reserved for chemotherapy or radiotherapy because of the perception that radical surgery was associated with excessive morbidity and mortality. A number of recent advances demand a reexamination of the role of surgical cytoreduction in the treatment of cancer patients. Progress in anesthetic and surgical techniques has sufficiently reduced the risk of many of the most radical surgical procedures to levels that rival current risk of systemic chemotherapy. The detailed imaging techniques now available allow selection of patients best suited for cytoreduction. The development of cryoablation and radiofrequency and laser ablation has provided additional surgical tools for safe cytoreduction. These factors, combined with the limited success encountered by chemotherapy and radiotherapy in the treatment of solid tumor, prompt a renewed consideration of surgical cytoreduction. Radio- and chemotherapy may be potentially curative for microscopic tumors, but rarely cure the patient with gross tumors. The concept of surgical cytoreduction is based, therefore, on the hypothesis that in select patients, the majority of tumor can exist in limited and surgically accessible body sites so that safe debulking of gross disease by resection or ablation can be combined with chemotherapy or radiotherapy (or both) to result in improved outcome. The goals of this paper are to explain the theory behind cytoreduction, describe pertinent methodologies, discuss several paradigms for the role of cytoreductive surgery, and outline some selection criteria for employing cytoreductive techniques. Rather than challenging traditional chemotherapy, radiotherapy, or immune therapy, our intent is to place the incremental advances in these treatment modalities in perspective with those in surgical therapies. Our paper intends to provoke an examination of the role of surgery as part of a multimodality treatment of patients with classically incurable disease, asking whether surgical cytoreduction will be a useful "adjuvant" to traditional systemic therapies.

Theoretic Basis
The theory underlying the concept of cytoreduction in the treatment of cancer patients is supported by experience from both clinical trials and basic scientific principles. Cytoreduction often improves function and quality of life when performed as a palliative operation intended to remove a bulky symptomatic tumor. The volume reduction also diminishes the metabolic demands made on the host by the tumor. Surgical removal of a bulky tumor may be beneficial in itself; however, an even greater benefit of cytoreduction stems from the improved response to chemotherapy afforded by the reduction in tumor volume.

A general principle of medical oncology is that the potential for cure is inversely proportional to tumor burden. Furthermore, tumor response is related to the intensity of the dose (total chemotherapeutic dose/unit time) that can be delivered to the affected tissue. According to the log-kill hypothesis, chemotherapeutic agents kill a constant fraction of cells, rather than a specific number of cells, after each dose ( Fig. 1).4 Therefore, reducing the initial tumor volume increases the likelihood that repeated cycles of chemotherapy will reduce the number of viable tumor cells toward the desired endpoint of zero. Reducing the total tumor volume to be treated also substantially diminishes the chances of cancer cells developing drug resistance, an event that increases directly with the number of cancer cells and the time it takes to complete treatment.4 Because most chemotherapies are directed at interrupting the process of cellular proliferation, it is also more likely to be effective against tumors that have a more rapid doubling time ( Table 1). Most solid tumors have a relatively slow doubling time, and, therefore, it is not surprising that chemotherapy and radiotherapy are unlikely to cure solid tumors. It is hoped that cytoreductive surgery will be a useful adjunct to accepted systemic therapies in improving patient outcome. Other benefits to cytoreduction include the interruption of the metastatic cascade whereby metastases beget more metastases. Reducing the total tumor burden may provide an immunologic benefit as well, because tumors are known to produce immunosuppressive cytokines, precipitate immune complexes, and produce peptidoglycans that interfere with normal immunologic defenses.5,6



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  		FIG. 1. Log-kill hypothesis. Lines A, B, and C refer to progressively smaller initial tumor volume. Line (a) refers to the size of the log-kill with each dose of chemotherapy, and line (b) refers to the regrowth of tumor prior to the next dose. A smaller initial tumor volume (C) results in the best chance for a cure.4

 

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  		Table 1. Tumor doubling time as related to results of chemotherapy
 
Cytoreductive surgery is not without potential hazards. Although surgical and anesthetic techniques have improved, the inherent risks of any surgical procedure must be considered in the overall assessment of the patient. Despite careful attention to detail, there is always a potential risk of physical dissemination of disease. Furthermore, surgery-induced stress causes a transient immune suppression that could, in theory, temporarily enhance tumor growth or spread. The time spent first in planning surgery and then in recovering from surgery could delay other potentially beneficial treatments. Finally, cytoreductive surgery can be associated with a significant expense. To put the economic considerations in perspective, however, it must be acknowledged that chemotherapeutic treatments also may be expensive. For example, one of the newer chemotherapeutic agents used in metastatic colorectal cancer, CPT-11, has a reported tumor response rate of only around 18% yet can cost $40,000 to $50,000 annually.7

Methods of Cytoreduction
Over the years a number of cytoreduction methods have been developed that are available to assist the surgeon and oncologist in the quest to reduce tumor burden ( Table 2). Surgical resection usually is the first consideration, because it can remove a large volume of tumor while sparing important adjacent structures. Peritoneal cytoreduction, including intestinal resections, has been used for ovarian cancer and other gastrointestinal cancers.8–10 Enucleation and formal resection of hepatic tumors have been used for neuroendocrine tumors of the liver.11,12 There are times, though, when surgery cannot be safely performed and other techniques should assume the primary role in cytoreduction. For example, cryoablation has been used for unresectable hepatic colorectal metastases or for prostate cancer.13 Radiofrequency ablation has been used for similar applications; it can be delivered via minimally invasive or percutaneous techniques.14 In the case of hepatocellular carcinoma, some groups have reported excellent results using ethanol injections in the treatment of cirrhotic patients.15 Finally, interruption of the blood supply through embolization techniques has been successful in controlling the growth of select cancers such as metastatic neuroendocrine tumors,16,17 sarcomas, melanomas, and hepatocellular carcinomas.


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  		Table 2. Cytoreductive methods
 
Surgical Paradigms
The benefits of cytoreduction have been suggested in a range of diseases, including ovarian cancer, peritoneal metastases, metastatic melanomas, and hepatic cancers. These models serve as paradigms that may guide the development of future treatment algorithms. One of the first areas for which surgeons defined the benefit of cytoreduction was in the management of peritoneally disseminated ovarian cancer ( Table 3).18 Earlier studies demonstrated that survival was related to the bulk of residual disease following resection. From this observation came the concept of debulking gross disease to less than 1 or 2 cm3 before chemotherapy and confirming response by a second-look laparotomy. Standard chemotherapy and radiotherapy was then delivered to optimize response to therapy. When analyzed in detail, the combination of the more aggressive surgical techniques with chemotherapy and radiotherapy resulted in the best survival advantage.19 The experience in ovarian cancer shows the results of treatment in a disease for which effective chemotherapeutic options exist and in which surgery is asked merely to reduce the bulk of disease to a level at which the chemotherapy could be expected to be the most effective. Similarly, the surgical oncologist often is called upon to perform extensive retroperitoneal nodal dissections, liver resections, lung resections, and cranial resections for eradication of metastatic germ cell tumor.20 Chemotherapy is highly effective for germ cell tumors, and it is clear that resection of residual disease after initial chemotherapy can improve outcome and that such combined therapy can result in cure.21


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  		Table 3. Cytoreductive surgery for ovarian cancer
 
The benefits of cytoreduction in ovarian cancer have been broadened to include the often difficult management considerations of widespread peritoneal carcinomatosis from appendiceal, gastric, or other mucinous tumors. These gastrointestinal tumors were an attractive target for cytoreduction, because, as with ovarian cancer, they often remain in a single body compartment even when disseminated. Although some consider such carcinomatosis to be a nonoperative situation, Sugarbaker and colleagues9 demonstrated that in select patients, peritonectomy with reduction of residual tumor volume to less than 2.5-mm deposits combined with intraperitoneal or systemic chemotherapy can improve survival. The morbidity and cost of these peritoneal cytoreductive procedures are not inconsiderable. The benefits of this aggressive approach for peritoneal dissemination of gastrointestinal cancer await both confirmation from other centers and support from studies using long-term outcome and economic and quality-of-life analyses.

The management of patients with metastatic malignant melanoma also has been shown to improve in select patients who have undergone cytoreductive surgery. Morton and his group demonstrated improved survival for resection of single-organ metastases to the lung, with 27% 5-year survival, vs. 3% for unresected patients.22 The fact that 88% of patients with stage IV melanoma have metastases to just one organ suggests that there is a window of opportunity to interrupt the metastatic cascade.23 Combining cytoreduction techniques with improved immunologic responses to vaccine therapies has the potential to further improve survival and quality of life.

Cytoreductive surgery also is valuable in the management of metastatic and primary hepatic malignancies. Metastatic neuroendocrine tumors, by virtue of their relatively slow growth rate, represent an area in which surgical resection of bulky disease has been shown to provide significant symptomatic relief and, perhaps, improved survival as well ( Table 4).24 In general, surgical resection provides a more durable response. However, for those metastases that are not amenable to surgical resections, cytoreduction by embolization has effectively provided symptomatic relief.12 The treatment of hepatocellular carcinoma also has evolved to include multimodality approaches to often difficult management situations. Surgical resection of the primary lesion remains the gold standard; however, there are many patients who have multifocal disease or are in the later stages of cirrhosis who are not surgical candidates. For these patients, other cytoreductive techniques, such as transarterial embolization or chemo-embolization, have improved outcomes compared to historical controls.25 Perhaps even more encouraging are some results from other investigators using ethanol injection in treating hepatocellular carcinoma. These treatments can be done with minimal morbidity, even in patients with advanced liver disease, with the 5-year survival reported to fall in the 30% to 40% range.26


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  		Table 4. Cytoreductive surgery for neuroendocrine tumors
 
Since the 1970s, when the first reports of safe hepatic resections for metastatic colorectal cancer appeared, the role of surgery for colorectal metastases to the liver has been further refined.3 Currently, resection of isolated liver metastases can be performed with low morbidity and mortality (<3%) and results in an expected 30% to 35% 5-year survival.27 For many patients with disease that is not completely resectable, the tumor may, nevertheless, be found completely or primarily within the liver. Whether cryoablation, radiofrequency ablation, or combined resection and ablation can be beneficial is the subject of ongoing investigations. Indeed, the utility of the combined use of such hepatic tumor cytoreduction with hepatic arterial infusional floxuridine chemotherapy and systemic chemotherapy with agents such as CPT-11 is one exciting area of current studies.

Although there undoubtedly are situations in which surgical cytoreduction plays a role in improving survival or quality of life, there are clearly limits for safe and reasonable cytoreduction. Because tumor biology governs these limits, the natural history of individual tumor types must be understood before extensive efforts using cytoreduction are made. For example, whereas resection for colorectal metastasis isolated to the liver can prolong survival, the presence of even minimal metastatic disease in the portal nodes is associated with such a poor prognosis that it eliminates any potential benefit, and is, in fact, a contraindication for hepatic resection.28 The natural histories of other metastatic tumors, such as breast and gastric cancers, are such that hepatic and pulmonary resections are associated with universally poor survival.29 Therefore, a thorough appreciation of the specific tumor biology must be applied to the selection of patients who may benefit from cytoreduction.

Selection Criteria
Four general guidelines, drawn from the paradigms discussed in earlier sections of this article, help us identify those patients who may benefit most from cytoreduction. They include those with symptomatic tumors, slow-growing tumors, and tumors responsive to other therapies, and those in whom the surgical procedure can be performed safely. The group best suited for cytoreductive therapy is symptomatic patients. Most surgeons are willing to perform a reasonably safe operation to produce symptomatic relief even if there is no guarantee that life will be prolonged. Full justification of such palliative approaches demands studies using quality of life as the main outcome parameter. The safety of the surgical procedure is central to this and other noncurative cytoreductive approaches. A favorable biologic behavior of the tumor is a good justification for cytoreduction. Slow-growing tumors that remain limited in the extent of dissemination can be expected to have good results with cytoreduction ( Fig. 2), because the patient can expect a durable response to the therapy. However, most attempts at cytoreduction are done in combination with adjuvant therapies. The availability of additional effective systemic therapy allows for the best results of surgical cytoreduction. Indeed, one major theory behind cytoreductive surgery is the concept that chemotherapy will be much more effective when used to treat a smaller volume of tumor. If there are no effective synergistic therapies available, then the benefits of any cytoreduction may be limited. Although cytoreduction sometimes is used for rapidly growing tumors when no other therapy is available, results can be expected to be poor.



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  		FIG. 2. Role of surgical resection or cytoreduction in multimodality care of the cancer patient. Panel A is the schematic of a patient undergoing tumor resection (x) followed by multiple courses of potentially curative adjuvant chemotherapy. Panel B represents cytoreductive surgery (x) followed by effective chemotherapy that reduces tumor to levels below clinical levels. Panel C represents cytoreduction (x) for a patient with a slow-growing tumor. A long period may pass before the tumor regrows (y) to significant levels. At that time, further cytoreduction (z) may be performed by resection or ablation.

 
Most of the studies supporting cytoreduction in select tumors are based on retrospective analysis and historical controls. Prospective studies are lacking. The time has come to attempt to overcome these obstacles and initiate some prospective randomized trials for surgical cytoreduction. Potential studies include randomizing patients with asymptomatic neuroendocrine tumors to early cytoreduction versus delayed treatment until clear progression in volume or symptoms is observed. Patients with dominant hepatic colorectal metastases and small-volume extrahepatic disease can be randomized to treatment by chemotherapy alone or by cytoreduction and chemotherapy. End points for these and other trials of cytoreduction should include not only morbidity and length of survival, but also quality of life and cost.

In summary, improvements in anesthetic and surgical techniques have greatly decreased the risks of even the most extensive procedures. Over recent decades, although small incremental improvements have been made in systemic treatment of disseminated solid organ malignancies, no "magical" cures have emerged. However, much has been learned concerning the biology of metastases and their response to various treatment modalities. In many types of cancer, cytoreductive surgery likely will find a role in a multimodality approach ( Table 5). The best candidates are those with limited, slow-growing tumors, or those patients with reasonably effective systemic therapies. An attractive treatment schema may consist of induction chemotherapy, followed by optimum cytoreductive resection of residual tumor and then by additional chemotherapy. This and other approaches involving surgical cytoreduction will have to be tested in clinical trials conducted by oncologists willing to shed the prejudices of an era when surgery was risky in search of data to determine if cytoreductive surgery is a useful tool for improvement of patient care.


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  		Table 5. Guidelines for identifying patients likely to benefit from cytoreduction
 
Received for publication April 27, 2000. Accepted for publication August 18, 2000.


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