INTRODUCTION
In the United States, colorectal cancer (CRC) is the second leading cause of cancer death in men and the third leading cause of cancer death in women; overall it is the second leading cause of U.S. cancer mortality, with 56,600 deaths each year (Seer Cnacer Statistics Review, 2000, 2003). Each year 129,000 new patients are diagnosed with colon or rectal cancer; nearly half will develop liver metastases. Liver metastases are involved in the vast majority of patients dying of CRC (Scheele & Altendorf-Hofmann, Reference Scheele and Altendorf-Hofmann1999). Although most CRC patients with liver metastases will receive chemotherapy, surgical resection and/or ablation of liver metastases offers the only possibility of long-term cure (Scheele et al., Reference Scheele, Stang and Altendorf-Hofmann1995; Fong et al., Reference Fong, Fortner and Sun1999). The percentage of patients with CRC liver metastases eligible for surgery is low, ranging from 10% to 20% (Walsh & Poston, Reference Walsh and Poston2002; Adam et al., Reference Adam, Delvart and Pascal2004). Liver metastases are considered unresectable if they are too large, too numerous, or in challenging anatomic locations that make complete resection or the identification of extra-hepatic metastases impossible. Criteria for resection are not standardized, however, and can vary considerably based on local expertise in hepatic surgery and may also be influenced by regional physician treatment biases (Folprecht et al., Reference Folprecht, Grothey and Alberts2005).
There is growing acceptance that long-term cure of patients with CRC liver metastases is best achieved with a complete resection of all hepatic metastases (Tomlinson et al., Reference Tomlinson, Jarnagin and DeMatteo2007). Efforts to increase the number of patients who receive curative intent surgical therapy of metastases is currently being evaluated (Adam et al., Reference Adam, Huguet and Azoulay2003, Reference Adam, Delvart and Pascal2004; Hemming et al., Reference Hemming, Reed and Howard2003; Folprecht et al., Reference Folprecht, Grothey and Alberts2005). Various techniques may potentially increase the total number of patients actually achieving a curative resection from an estimated 10%–20% to as much as 33% (Adam et al., Reference Adam, Delvart and Pascal2004).
Patients who have newly identified CRC liver metastases can be easily overwhelmed by both the gravity of having metastatic disease and by the complexities of trying to identify treatment options. Adding to this burden is whether their disease is potentially curable and whether they are candidates for surgical resection of the metastases. This comes at a time of significant emotional and physical burden of metastatic disease. It is important for cancer clinicians to better understand the patient experience for specific clinical scenarios. So far, the patient experience of major surgery for CRC liver metastases has not been studied. One way of gaining additional insight into patients’ perceptions, understanding, and satisfaction with a treatment experience is to conduct detailed interviews with patients who have undergone the treatment of concern. This qualitative research method offers depth of understanding into patients’ lived experiences and can help identify potential barriers and misunderstandings of patients. The purpose of this study was to gain insight into the lived experience of a group of patients who experienced major surgery for the treatment of CRC liver metastases.
METHODS
A phenomenological qualitative research approach was used to explicate the structure and essence of patients’ experience with the treatment of their CRC liver metastases (Leininger, Reference Leininger1985; Speziale & Carpenter, Reference Speziale and Carpenter2007). As noted by Spiegelberg, descriptive phenomenology involves “direct exploration, analysis, and description of particular phenomena, as free as possible from unexamined presuppositions, aiming at maximum intuitive presentation” (Spiegelberg, Reference Spiegelberg1975). In-depth interviews were conducted from July 2005 through August 2006 in patients’ homes. The research was approved by the University of Vermont Institutional Review Board; moreover, participants gave informed consent and HIPAA approval prior to their interviews.
Participants’ Characteristics and Sampling
Participants were 18 years of age or older and had a prior history of CRC confirmed by pathology report. All patients were screened preoperatively with both computed tomography scans and positron emission tomography and were identified to have liver only metastases prior to surgery. All had been referred to a single surgeon by various medical oncologists. Participants underwent surgery for metastases (resection, ablation, or both) by a single surgeon between January 2003 and June 2006. Participants were purposively selected to represent a mixture in gender and age as well as for their ability and willingness to articulate their perceptions of their experiences. Moreover, participants were sought who had positive, uncertain, or negative treatment outcomes in terms of disease recurrence following liver surgery.
Procedures
Participants were initially contacted by phone by the interviewing nurse researcher who had no previous association with patients’ clinical care. The study was described and permission was obtained to conduct an interview in a nonclinical setting. Written consent was obtained at the initial home interview. A total of 13 patients were contacted and 12 agreed to participate in the study.
Data were collected via in-depth, semistructured interviews. An interview guide was developed after reviewing the literature and based on previous work regarding patient understanding of surgery for advanced malignancies. Participants’ expectations prior to surgical consultation and their understanding of their situation afterward were explored in detail. Their role in the decision-making process for liver surgery was explored. They were asked to discuss if they felt they had enough, too much, or not enough information to make their decision (see Table 1). Having experienced the surgery, participants were asked for suggestions for others in similar circumstances. Further exploratory questions helped to gain understanding of the relative importance or impact of various factors on decisions to proceed with surgery and to allow for a more in-depth understanding of patients’ experiences.
Table 1. Guiding questions for interview
Interviews lasted from 60 to 180 min and were audiotaped both for content clarity and for better recall of subtleties of patient emphasis and emotions best identified through listening and observation. Interviews were transcribed verbatim by a single transcriptionist.
Qualitative Analysis
The analysis provided a detailed description and understanding of the patient experience as lived by participants. The three-step analysis process consisted of intuiting, analyzing, and describing (Speziale & Carpenter, 1999). The interviewer listened to the tapes while reading the transcriptions for accuracy. Handwritten notes were made after interviews and while listening to verbally transcribed accounts to achieve comprehensiveness and accuracy of description. Common themes emerged from the data as the researcher listened to the participants’ descriptions of their quality of life. Colaizzi's procedural steps were followed: collecting participants’ descriptions of their experiences, reading all participants’ descriptions, returning to the verbatim transcripts and extracting significant statements, trying to spell out the meaning of each significant statement, and organizing the aggregate meanings into clusters of themes. The transcriptions were read by a second investigator, and themes identified in the first pass analysis were discussed and revised and agreed upon by both investigators. Data saturation began appearing at the eighth interview; thus, the total sample size of 12 was deemed adequate (Colaizzi, Reference Colaizzi, Valle and King1978; Speziale & Carpenter, 1999).
RESULTS
Seven men and five women with a mean age of 63 (range 43–75) participated in the interviews. All participants had previously been treated with both chemotherapy and major surgery for treatment of their liver metastases. Participant characteristics at the time of their interviews are listed in Table 2. Participants uniformly described themselves as asymptomatic from their liver metastases at the time of diagnosis. Metastases were generally identified by clinicians through disease surveillance. Participants recalled their decision to undergo major liver surgery as one of several major health care choices made in the context of the “battle with cancer.” They viewed the decision for liver surgery as involving several steps initiating with the idea to go ahead with this option, next undergoing the surgery, enduring the recovery, and living out the consequences. Several emphasized that they would not have known about the option of liver surgery without their oncologist, as this information appeared to be widely missing from available brochures and Internet information. Several indicated that they learned about the ability of the liver to regenerate during their surgical consultation, and that this information made the decision for surgery easier. Participants appeared to have clear and realistic outcome expectations of the surgery. They saw surgery as holding no guarantees for disease cure and involving many risks, yet being an opportunity to extend their lives.
Table 2. Decision-making study participants
RFA: radiofrequency ablation; NED: no evidence of disease; HAI: hepatic arterial infusion.
Seven common themes emerging from the data analysis are described below with examples of participants’ supporting statements. For each theme, participants identified factors associated with their degree of satisfaction with their treatment. Factors were identified as “positive” if patients perceived these as helpful in making their decision to have surgery, or to increase the comfort level with their decision, or were felt to be associated with a positive impression of the treatment experience. “Negative” factors were associated with additional difficulty, burden, or stress in making their decision or were factors that contributed to a negative impression of their treatment experience.
Communication with the Health Care Provider
A primary factor influencing the treatment experience was how well the surgeon and/or oncologist or nurses described their health situation and choices for treatment. Most spoke about the importance of the thoroughness and understandability of the explanation. It was important that words, concepts, and procedures were voiced in accordance with their level of knowledge, were clarified in an unhurried manner if not understood, and that time was allowed for processing the implications for choices in health care. Drawings of procedures and anatomical parts were valuable. Patients appreciated direct and honest elaboration and appraisals of risks and expected outcomes. The manner and nonverbal communication style of the health care provider enhanced trust and confidence beyond the obvious expertise of the clinician when it included ability to develop a comfortable rapport, attentiveness, acknowledgement of the patient's choice, respectfulness, inclusion of family members, and the intent to treat the patient as a partner in his or her care. Participants felt further “cared for” when physicians took the extra time to follow up concerns with additional appointments and telephone calls to home and/or to family members and when the various specialists met and agreed with each other's treatment approaches. Negative factors identified about health care providers were if the clinician was hurried, did not take time to listen, was forceful in manner, or told the patient what to do.
We talked about all sorts of things. Dr. [surgeon] was really good about that and I have never felt that he has not explained something to my satisfaction. … The options and the scenarios and the facts and everything have been presented to me in a way that I was able to make informed decisions. It wasn't, “just go have surgery” or “just go have chemotherapy.” (Participant 1)
He doesn't talk to you in great big words. He explains it for you to understand. If I looked like I was confused to him, he'd draw it for me. He never made me feel like I had to hurry up. He's always got time for you. My oncologist and surgeon have worked hand-in-hand. He [surgeon] took the time to do that and gave me the attention I needed. (Participant 4)
I wasn't making any decisions or anything. So she [oncologist] did come in, but I thought she was awful forceful. She sits down and she told me, she said I think you've got extensive coverage of the liver with cancer. … She wanted to get going on chemo already, to set it up. … So I didn't say anything. … I kind of doubted her word when she said extensive coverage, not that, but extensive spread. I didn't think she had enough facts in front of her to make a decision like that without no biopsies and nothing on the liver part. (Participant 9)
Support from Others
All participants emphasized the importance of support from others as they decided on a particular treatment option, underwent the treatment, and lived with the consequences of the treatment. This support came from spouses, children, parents, siblings, friends, coworkers, animals (pets), church and club groups, information from Internet sites, and chat room discussions. Patients perceived that they would not have carried out their decisions as well or even made the trips to treatment without this support and partnership. Patients appreciated it when, once they made a decision, it was supported by the family members whether the family agreed or not. Encouragement from family and friends helped patients maintain hope and persevere during treatment. Family and friends were also a motivation for desiring to live longer. Negative influences were experienced when a family member was overzealous, anxious, or tried to influence the patient's decision.
It was probably just as well that my wife had the summer off because somebody had to drag me to chemotherapy and drag me back kicking and screaming because I didn't want to go at all. At one point, I almost quit. (Participant 1)
My husband is very positive that everything will work out fine. I don't know what his inner thoughts were. … I was very lucky to have a lot of people around me who were encouraging. … My tennis group every week would send me cards after I'd come back from chemo. People kept track of me and said they were praying for me. … My daughter, who is a physician, called almost every week. I knew … she was thinking about it and checking up on what was going on. … Encouraging, yes. Perhaps being overzealous as far as I was concerned because she wanted me to be sure to check on what was being injected and whatever, so nobody was making mistakes because she said it was possible. (Participant 3)
Yeah, it just gives you that extra push to go on, when it's just like, God I don't want to go for another chemo treatment but you've got two kids, that you've got to go, you've got to give it your all. Yeah, you're sick, you're tired, but you just can't give up. (Participant 7)
The Patient's Own Attitude
All participants overwhelmingly described the necessity of having a positive attitude and the belief in being able to resolve their disease situation through their decision to choose liver surgery. This positive attitude was viewed as a mindset and cognitive stance that one can recover and is strong enough to persevere. They noted the importance of dealing with their disease head on, mustering up personal strength and courage to face the treatment options with the latest and up-to-date technologies. They believed that taking this positive view of life promotes a positive outcome. Three participants described that what they once saw as meaningful in life changed to enjoying the moments with loved ones and to allow care and assistance from others.
You go through all this stuff and then you get cancer or you find out you have it and it is like … most of all that other stuff is really not that meaningful. The job isn't that meaningful. Politics is not that meaningful. … You've just got to get your mind in the right place and just say I am dealing with this. (Participant 1)
I think for anybody who has got to deal with surgery or cancer in general, I guess the first thing you've got to do is have your mindset. It is all in your head. You can be sick or whatever else, but if you've got your mindset, this is okay. … I know it is not for everybody, but for me, my faith in God and a little bit of time praying first before you make those decisions is really important. (Participant 4)
Unwavering? Belief that you're strong enough you can recover. It's the optimistic view of life that even facing some pretty challenging health care procedures, I personally will persevere and get out in record time. I figured out early on if you want to get out of the hospital, you have to walk out. Good health is really a state of mind. A very positive attitude about staying well is how you stay well. (Participant 6)
Cure Uncertainty
All participants reported being well aware that disease cure was uncertain after they became aware of cancer metastasis to the liver. Each participant expressed an understanding that the liver surgery was an opportunity to potentially extend his or her life expectancy but recognized the possibility that metastatic disease could come back. Many expressed a bias toward “just cutting it out,” even if that would not necessarily guarantee any further disease recurrence. Most did not recall the exact statistics that were discussed prior to surgery regarding prognosis or risks of surgery, yet they were willing to undergo surgery and/or chemotherapy to prolong their lives. One half of the participants did not have a curative outcome following liver surgery at the time of the interview. In spite of this outcome, these six participants were comfortable with their decision to have undergone the surgery.
Well, I think that depends on the person. I think that for me, I don't know that I could have too much information. I think maybe Dr. [colorectal surgeon] or the radiologist saw something on some of those first CTs. They saw a spot. They didn't know what it was and they weren't necessarily going to say, “Oh boy that could be cancer,” … but in some respects, how much do you tell a patient that you may be unsure about something and want to really figure something out. How much do you tell the patient and get them worried? So, there is that factor. Some people would sit around wringing their hands for months until they got to the next CT to see if it was 1 mm bigger or smaller or whatever it was. That is a tough thing I think. (Participant 1)
I just feel Dr. [oncologist] is going do another CT scan in November. I sometimes kind of wish that he would do it sooner or that because if anything shows up I want it taken care of right away. I don't want to give it a chance to do anything that we don't know about. (Participant 2)
I think the hardest part is the waiting for the results and then to turn around waiting for the PET scan to come back, finding out that was cancer in your liver, but now there is something else in your pelvis. Then, it was back to waiting again to get the biopsy done. Then the day before the biopsy, they called and said it was normal ovarian function and I was, like, wait a minute. Who are you? How do I know you know anything about it?” … I was glad that was nothing, but that is the toughest is the waiting. Once you know, you can deal with it. It is the not knowing. (Participant 4)
Coping Strategies
Participants described a variety of ways they coped during the decision-making process and throughout their illness experience. Positive strategies for getting through the initial shock of the diagnosis and/or the recurrence were identified as the following: living in the moment, taking one day at a time, and appreciating one's blessings. Ways that they faced the reality of the disease were by learning as much as one can and asking questions. Identifying feelings and stopping worrisome thoughts helped them to think more rationally about options. They found that following daily routines and participating in normal activities such as exercising were essential basics for their lives. They encouraged facing and struggling through depressing and anxious emotions rather than avoiding emotions. Crying was a helpful catharsis. Having faith and praying to a higher power helped them to make peace with themselves and accept the situation for the remainder of their life. A few spoke about exploring alternative healing methods such as therapeutic touch to complement their medical treatment.
If you had come last week, there were a few days when I felt really depressed and wondered if this was a natural thing when you have been struggling along and then all of a sudden, it is all sort of over and kind of post-partum depression here. We've had a nice four or five days, so that has gone away. … Weepy. That is about it. It comes to a head and you sort of just cry a little and it goes away. (Participant 3)
I try to turn it around and remember the fact that the blessings that we have throughout the day, … my grandchildren, my children, all those little things; you look at them and you realize that they are all a gift. Everything is a gift. Every day is a gift. Once you realize that and you know that the worst thing that is going to happen and can happen to me today is I might die and pray to God in his mercy I would go to heaven. Once you know that and that is reality every day, cancer can't hurt you. (Participant 4)
Hospital Care Concerns
Seven participants described hospital care conditions as an important factor in their overall impression about the quality of care. Some participants identified expertise of multiple inpatient care providers as a concern and lack of communication among inpatient hospital staff as well as the lack of staffing as leaving negative impressions of their treatment experience. Participants also described positive influences during their inpatient care in the form of caring providers offering their help.
Sometimes I got the feeling they didn't even know what you were in the hospital for, but do all the nurses who are working with you in the hospital or around you, do they all know what surgery you had or whatever? … I guess it is that feeling that you don't know who is who and of course, part of it up here at this hospital where it is a learning hospital and there are all these extra people, that you are introduced to maybe once and they do come back and sometimes and it is hard to keep track of who everybody is. That bothers me a little.” (Participant 3)
I felt that the questions of care to me revolved around inadequate staffing. I really felt that the numbers of nurses were inadequate. They keep them busy enough that they are forced to do those medications that require the degree and knowledge. The other support care is kind of tough to get. (Participant 6)
Then they wanted to get in my port, but it wasn't healed really. … I said, “You can get blood anywhere. I am easy to get. Leave the port alone.” I said, “Furthermore, you better come back with someone big because you are not touching it. That was the end of it.” (Participant 9)
Internet Information
Although seen as an informational source of support used by family members, the Internet was described by six participants as lacking in information about liver resection for colon rectal metastasis and as very negative about the prognosis.
I think back in 2001, my husband got on the Internet and he was very, very concerned. Very concerned … that I was in stage IV. … I'm not sure, six months (to live) maybe. My husband was very upset and concerned, as well as my daughters. … I would say that they should listen to their physician and go by what they say and do what they say. Don't pay attention to other people or even … well, in my case the Internet was kind of, I don't know if you can call it false information, but it certainly didn't help my husband. It was considered stage IV cancer. (Participant 2)
Well, you know the things that could have gone wrong during the surgery, which, you know, I didn't go into it with my eyes closed. I researched everything on the Internet to find out how often. … I went through WebMD for a lot of it and just read what the risks of surgeries would be. (Participant 7)
I've read survivor stories and they've been very encouraging from what I've read from these people who have chosen to submit stories, but the clinical stuff, the technical stuff, I read it and I just get so depressed that I end up sitting there crying. … There were places where people could submit their chat room comments, bad experiences with an original chemo drug that they were prescribed and having to switch. … And I'm thinking, holy cow, let's just hope he hits on the right combination the first time because to stop this and then to try something else … (Participant 10)
DISCUSSION
Over the past 25 years, it has been demonstrated that surgical resection of CRC liver metastases is a safe and effective therapy for patients with CRC liver metastases. Two very large patient series have demonstrated that it is possible to perform liver resections in patients with metastatic CRC with an operative mortality of 4%, a 5-year survival rate of 39%, and a 10-year survival rate of 22% (Scheele et al., Reference Scheele, Stang and Altendorf-Hofmann1995; Fong et al., Reference Fong, Fortner and Sun1999). As such, liver resection for medically fit CRC patients with liver metastases amenable to resection has become a standard of care. Despite the growing utilization of liver surgery, there has been no qualitative research evaluating the patient treatment experience.
Previous studies evaluating the patient experience with CRC have been limited to patients with earlier stage disease. Salkeld and Solomon of the University of Sydney identified factors of greatest importance to patients in deciding upon primary treatment for nonmetastatic CRC through qualitative methods and interviews (Solomon et al., Reference Solomon, Pager and Keshava2003; Salkeld et al., Reference Salkeld, Solomon and Short2004, Reference Salkeld, Solomon and Butow2005). Similar to our findings, they identified that patients’ trust in their surgeon and the surgeon's specialty training are of paramount importance. They also demonstrated that treatment preferences of patients can differ considerably from that of the treating physicians (Solomon et al., Reference Solomon, Pager and Keshava2003). Subsequent survey work indicated that decision-making roles for patients varied by age, sex, and prior treatment experience of the patient (Salkeld et al., Reference Salkeld, Solomon and Short2004). The Australian group demonstrated that 80% of CRC patients were willing to trade off survival time in order to avoid chemotherapy or radiation treatment, but were less willing to trade off survival time for a less invasive surgery (laparoscopic vs. open surgery; Solomon et al., Reference Solomon, Pager and Keshava2003). A limitation in interpreting these earlier studies, however, was that participants were only required to have had previous surgery for colorectal cancer. Therefore, few or none would have had any experience with chemotherapy or radiation on which to base their expressed treatment preferences. The applicability of this work to our study population is also limited as their patients had an earlier stage disease.
This is the first qualitative study that specifically looks at the lived experience of patients with metastatic CRC who have undergone liver surgery. All patients had prior experience with both chemotherapy and initial cancer surgery on which to base treatment decisions. These patients face challenging decisions that balance their desire to prolong survival yet maintain a good quality of life. Findings indicate that the most significant factor for a successful treatment experience begins with the communication style/characteristics of their surgeon/medical oncologist. Patients appreciated direct, realistic, informative, honest discussions in an unhurried manner and with plans for short term follow-up discussions. Surgeon/oncologist agreement on treatment was another positive factor, as was family members’ support of the patient's choice.
Previous studies of patients undergoing surgery for advanced malignancies have shown that patients can overestimate the curative potential of the operation, despite surgeons’ recollection of having discussed limited opportunity for cure (McCahill & Ferrell, Reference McCahill and Ferrell2002; McCahill et al., Reference McCahill, Krouse and Chu2002a, Reference McCahill, Krouse and Chu2002b; Ferrell et al., Reference Ferrell, Chu and Wagman2003). Qualitative research by this group focused on understanding patients’ expectations, their anticipated goals and outcomes of surgery when life expectancy was limited, and how treatment outcomes affected their later interpretation of whether communication about surgery had been effective (Ferrell et al., 2002; Bornemann et al., Reference Borneman, Wagman and Ferrell2003). These studies demonstrated that patients undergoing planned palliative surgery recognized that surgeons had articulated preoperatively that surgery was largely intended for symptom relief. Nevertheless, patients also indicated that hope for a curative procedure or extension of their survival time was a major motivating factor for surgery. In comparison with Ferrell et al. (2002), our findings concur, as our participants viewed surgery as an opportunity to extend life expectancy with lesser long-term side effects than chemotherapy. Both treatment options were regarded as opportunities to continue “the battle with cancer.”
Our study had several limitations that lessen its applicability to a broader patient population. All patients in this study chose to undergo liver surgery. Other patients may have been suitable for surgical resection but chose not to pursue surgery. As such, interpretation of their fairly positive acceptance of surgical therapy may not be applicable to all patients. Future research into patient treatment preferences and decision making for management of CRC liver metastases will need to incorporate a broader population of these patients. Our study represents initial pilot work and has identified factors of importance in a small group of patients treated by a limited number of health care professionals. We believe the factors identified in our pilot work might also serve to develop surveys or research instruments for quantitative studies that could be applied to a larger population of CRC patients with liver metastases. These factors should be validated in a larger population. We believe this research has shed some insight into the patient's treatment experience of major surgery for the treatment of metastatic disease. No currently available data exist regarding the percentage of patients with potentially resectable CRC liver metastases who are evaluated to discuss surgical options. We believe our study indicates a high level of acceptance and treatment satisfaction of patients following liver surgery, even when patients sustained disease recurrence. This finding may be underappreciated by health care providers caring for these patients.
ACKNOWLEDGMENT
Research funding was provided by the Department of Surgery, University of Vermont.
