Is there evidence for a better health care for cancer patients after a second opinion? A systematic review

Abstract

Background

With growing complexity of diagnostics and therapy, as well as increasing involvement of patients in the decision-making process, there is more and more demand for second opinions in oncology. This literature review aims at analyzing the benefits and risks involved, as well as the tools needed to establish a structured program for second opinion within a modern healthcare system.

Methods

A systematic literature search was performed using MEDLINE and Embase and the databases SocINDEX, ERIC and CINAHL. Thirteen articles met the inclusion criteria and offered a relevant insight into the topic of second opinions.

Results

Depending on the study, between 6.5 and 36 % of patients search for a second opinion, due to a variety of reasons. Changes in diagnosis, treatment recommendations or prognosis as a result of the second opinion occurred in 12–69 % of cases. In 43–82 % of cases, the original diagnosis or treatment was verified. Patient satisfaction was high, and the second opinion was deemed as helpful and reassuring in most cases. Yet, data on patient-relevant outcomes or on the quality of the second opinion are missing.

Conclusion

In general, outcome data on second opinion are divergent and scarce. Yet, with patients’ demand for second opinion and influence of second opinion on treatment decisions, a structured, high quality and transparent second-opinion program seems mandatory. Such a program may support patient–physician communication and improve the flow of information, as well as decision-making. Its evaluation should be independent from the provider of the second opinion.

Introduction

Incidence and prevalence of cancer are rising in most western countries (International Agency for Research on Cancer 2015, Robert Koch Institut 2013). At the same time, diagnostic and treatment methods are rapidly evolving and becoming more complex with growing knowledge. Personalization of treatment allows for diverse and specific treatment plans for individual patients.

Oncologists are faced with the challenge of keeping pace with this huge amount and rapidly growing knowledge. Inevitably, specialization will become more and more necessary, and consequently, specialists for rare cancers will be located at few national cancer centers. Most patients will, however, be diagnosed in regional institutions where an oncologist with the corresponding specialization may not be available. In these cases, referral to a specialized institution may help to find the best treatment plan for the individual patient.

Furthermore, patients are becoming more and more involved in the decision-making process. As a result, the need for patient information is growing, as more and more patients actively seek information concerning their disease and their treatment options. Several surveys have analyzed which topics are most important for patients. The two most important issues that were reported are the pros and cons of the different treatment options and the prognosis of diseases (Feldman-Stewart et al. 2009; Keinki et al. 2015; Mistry et al. 2010; Nagler et al. 2010; Rudolph et al. 2015). Information sources seem to be changing, with the Internet gaining more importance. Most patients, however, still prefer human counterparts for seeking information. Accordingly, family, friends and physicians are mostly mentioned as a source of information (Keinki et al. 2015; Nagler et al. 2010; Rudolph et al. 2015).

With patients becoming more and more active and autonomous, looking for a second opinion also implies verifying treatment proposals and even making a choice between different proposals and different institutions. Getting a second opinion may be helpful both for the patient and for the physician/oncologist in charge. On the other hand, patients may also be overstrained with decision-making, when confronted with more than one opinion.

While it has been a consensus in Germany that every cancer patient should have access to a free second opinion, a bill was passed in 2015 (SGB V, § 27b) that codified this right for several non-cancer diseases. While the new law has the primarily goal to reduce costs of expensive procedures, the German Cancer Society and other institutions focus on aspects of cancer care improvement in their discussions. Different aspects such as organization, content and quality assurance are currently being discussed.

In 2006, a network for second opinion for testicular cancer started its work with financial support from the German Cancer Aid. This expert network offers a second opinion to the urologist in charge upon his request. Within a short time after submitting the patient’s data, he receives an answer with a treatment proposal according to the guideline of the European Association for Urology (Zengerling et al. 2014).

To systematically introduce second opinion in oncology, a benefit–risk and benefit–cost analysis in the healthcare system seems mandatory. In preparation for such an analysis, this paper offers a systematic review on publications regarding second opinion in oncology focusing on three issues:

1. Is there evidence for a better quality in the provision of health care for cancer patients who get a second opinion (benefit)?

2. Is there evidence for any risks?

3. Do we have evidence on how to establish a structured program for second opinion in cancer care within a modern healthcare system with certified cancer centers?

Methodology

Literature review

The systematic literature search was performed in January 2015. MEDLINE and Embase were searched via Ovid and the databases SocINDEX, ERIC and CINAHL via EBSCOHost. Search terms included referral, second consultation, second opinion, second counseling, second review and second assessment. Detailed search information can be obtained from the corresponding author.

In addition, lists of references were screened for relevant publications. No publication date restrictions were used. Relevant publication languages were German, English and French.

The amount of hits and the individual steps of the selection of literature are shown in Fig. 1.

Fig. 1.

Literature search and included articles

Selection of studies

Population

Included were publications on treatments of adult patients (>18 years) with hematological or solid malignancies. Second opinions concerning questions arising before a definite cancer diagnosis, such as screening or genetic counseling, were excluded.

Intervention

The second opinion was defined as patient-initiated second assessment of the individual situation regarding the patient’s diagnosis, treatment or prognosis by an independent specialist (Heimpel et al. 1999; Schmidmaier 2006).

Excluded were physician-initiated intraprofessional consultations, e.g., within the second-opinion network for testicular cancer (Zengerling et al. 2014), referrals to a physician with a greater degree of specialization, mandatory second reviews, second opinions for legal reasons and second opinions in pathology or radiology.

Descriptions of healthcare systems, reports and studies from third world countries and other countries with less developed healthcare systems were not considered relevant due to a lack of transferability.

Outcomes

Relevant outcome parameters in cancer studies are overall survival and/or an improvement in quality of life of the patients. There are, however, no studies on patient-initiated second opinions reporting these outcomes.

Therefore, this review focuses on patient characteristics, motivation and satisfaction, the discrepancies concerning diagnosis and treatment recommendations and the consultation setting between the first and second consultations. Possible effects on the patients care path, such as time between the first and the second consultation delaying treatment, the additional efforts made by the second-opinion physicians and a possible change in the treatment location, are also considered relevant.

Study selection

Following the recommendations of the Cochrane Effective Practice and Organization of Care (EPOC) reviews (Effective Practice and Organisation of Care 2013), systematic reviews and meta-analyses, randomized controlled studies (RCT), non-randomized controlled studies, uncontrolled studies (process monitoring, uncontrolled before–after studies and time-series analyses), economic studies and observational studies were included.

Two reviewers evaluated title and abstract of the articles identified through the database searches independently, according to the eligibility criteria. Afterward, the full texts of the included articles were reviewed for final inclusion. Eligibility differences were reconciled through discussion.

The relevant data of the finally included studies were systematically recorded in evidence tables. The tables contain study design, study population, intervention and control intervention, investigated endpoints and the results for these endpoints.

Results

Database searches identified 4701 references. No further publications were found from the reference list screening. One hundred and ninety potentially relevant abstracts were reviewed as full texts. During the full-text review, 177 articles were excluded. Thirteen articles met the inclusion criteria (Table 1).

Table 1.

Overview on studies

Reference and year; location	Type of study	No. of patients	Cancer	Pora	Motb	Charc	Disd	Loce	Satisf	Infg	Consh
Clauson et al. (2002); USA	Survey	231	Breast				X	X
Denberg et al. (2009); USA	Survey, patient data	20	Prostate	X	X
Lund et al. (2009); USA	Survey	5763	Breast	X	X	X
Malfait et al. (2013); Belgium	Patient data	79	Lung		X		X	X	X		X
Mellink et al. (2006); Netherlands	Patient data	403	Various locations			X	X	X
Mellink et al. (2003); Netherlands	Survey	212	Various locations		X	X
Morrow et al. (2009); USA	Survey	1984	Breast	X			X
Philip et al. (2011); Australia	Survey	65	Various locations				X				X
Philip et al. (2010); Australia	Survey	52	Various locations	X	X				X	X
Ramsey et al. (2011); USA	Survey	238	Prostate			X	X
Schook et al. (2011); Netherlands	Patient data	349	Lung				X
Tattersall et al. (2009); Australia	Survey	77	Various locations	X	X	X	X	X	X		X
Zysman et al. (2014); France	Survey	77	Lung	X	X	X					X

^aPortion of patients

^bPatient motivations

^cPatient characteristics

^dDiscrepancies between first consultation and second opinion/changes in diagnosis, treatment or prognosis

^eLocation of further treatment

^fPatient satisfaction

^gInfluence on the patient–physician relationship

^hSecond consultation process/dynamics (e.g., time between first and second consultations, duration, selection criteria for the second physician)

One systematic review on patient-initiated second opinions was found (Payne et al. 2014). Cancer patients are discussed as a subgroup alongside patients seeking a second opinion about elective surgery and patients with other general medical concern. The systematic review is based on 13 observational studies. Six of these studies analyze characteristics and motivations of cancer patients seeking a second opinion and their satisfaction with the consultation (Mellink et al. 2003, 2006; Philip et al. 2010; Ramsey et al. 2011; Tam et al. 2005; Tattersall et al. 2009). All of these studies were also found in the literature search for this review. The study of Tam et al. (2005) was excluded during the full-text review. The remaining five articles were included and used as primary studies. Through the literature search for this review, seven additional articles were identified. The number of additional studies and an interest in further outcomes justify this review.

All of the 13 primary studies use an observational design. Nine studies are surveys (Clauson et al. 2002; Lund et al. 2009; Mellink et al. 2003; Morrow et al. 2009; Philip et al. 2010, 2011; Ramsey et al. 2011; Tattersall et al. 2009; Zysman et al. 2014), three publications use a retrospective evaluation of patient data (Malfait et al. 2013; Mellink et al. 2006; Schook et al. 2011) and the study of Denberg et al. (2009) combines both methods.

The number of patients varies between 20 and 5763. Three studies with 7978 patients in total focused on breast cancer patients (Clauson et al. 2002; Lund et al. 2009; Morrow et al. 2009), three studies with 505 patients on lung cancer patients (Malfait et al. 2013; Schook et al. 2011; Zysman et al. 2014) and two studies with 258 patients on prostate cancer (Denberg et al. 2009; Ramsey et al. 2011). Four publications (Mellink et al. 2003, 2006; Philip et al. 2010; Tattersall et al. 2009) evaluate patients with various types of cancer. In three of these studies, the study populations mainly consisted of women with breast cancer (Mellink et al. 2003, 2006; Tattersall et al. 2009). Altogether, most of the patients were women with breast cancer. Philip et al. (2011) polled medical oncologists about their patient-initiated second-opinion consultations.

Most of the included publications are from the USA and Australia (Clauson et al. 2002; Denberg et al. 2009; Lund et al. 2009; Morrow et al. 2009; Philip et al. 2010, 2011; Ramsey et al. 2011; Tattersall et al. 2009). The remaining five European studies examined patients in the Netherlands (Mellink et al. 2003, 2006; Schook et al. 2011), Belgium (Malfait et al. 2013) and France (Zysman et al. 2014).

The risk of bias for all studies is high. This results mainly from the observational design, the lack of control groups and the use of evaluation instruments lacking validation. Furthermore, most studies only included small numbers of patients and only patients from single institutions.

Patients’ way to interest in a second opinion

The portion of patients seeking a second opinion was measured in six studies (Denberg et al. 2009; Lund et al. 2009; Morrow et al. 2009; Philip et al. 2010; Tattersall et al. 2009; Zysman et al. 2014) and varied between 6.5 % (Tattersall et al. 2009) and 36 % (Lund et al. 2009).

Patients select a specific second-opinion specialist following recommendations by specialists (29 %), friends (27 %), general practitioners (21 %), relatives (19 %) and nurses or someone else from the hospital (9 %) (Tattersall et al. 2009).

What motivates cancer patients to seek or to avoid a second opinion is discussed in six studies (Denberg et al. 2009; Lund et al. 2009; Mellink et al. 2003; Philip et al. 2010; Tattersall et al. 2009; Zysman et al. 2014).

Factors motivating patients to seek a second opinion are (Lund et al. 2009; Mellink et al. 2003; Philip et al. 2010; Tattersall et al. 2009; Zysman et al. 2014) the

• dissatisfaction with the first consultation regarding communication in general, information provided and the way information was provided, manner of discussion, involvement in decision-making,

• need for more information,

• lack of trust in the first physician,

• hope for a different (second) opinion,

• wish to exploit all opportunities,

• need for reassurance of diagnosis and treatment recommendation,

• urging by family, friends and others.

Reasons to avoid second opinions are (Denberg et al. 2009; Zysman et al. 2014):

• lacking knowledge on the existence of second opinion,

• misconceptions about the purpose of second opinions,

• trust or faith in the first physician,

• desire to avoid treatment delay,

• concerns regarding information overload,

• fear of (prolonged) uncertainty,

• fear to disturb the patient–physician relationship.

The knowledge about multidisciplinary-derived first opinions does not influence the motivation for or against a second opinion (Tattersall et al. 2009; Zysman et al. 2014).

Patient characteristics

According to the six studies (Lund et al. 2009; Mellink et al., 2006; Mellink et al. 2003; Ramsey et al. 2011; Tattersall et al. 2009; Zysman et al. 2014) describing the characteristics of cancer patients seeking a second opinion, most patients are female, are younger and have a higher level of education and a higher socioeconomic status.

Discrepancies/changes between first and second opinions

The proportion of discrepancies between the first and the second opinion and the proportion of changes in diagnoses, treatment recommendations or prognosis are described in eight of the included publications (Clauson et al. 2002; Malfait et al. 2013; Mellink et al. 2006; Morrow et al. 2009; Philip et al. 2011; Ramsey et al. 2011; Schook et al. 2011; Tattersall et al. 2009). There is no study comparing the quality of the divergent results. If there are divergent treatment recommendations, no data on the finally chosen therapy are provided.

Diagnosis or treatment recommendations are confirmed or valued as good medical practice in 43 % (Malfait et al. 2013) to 82 % (Philip et al. 2011) of the second-opinion consultations. Additional diagnostics are proposed for 21 % (Malfait et al. 2013) to 65 % (Schook et al. 2011) of the cancer patients. Changes in diagnosis, treatment recommendations or prognosis occur in 12.1 % (Morrow et al. 2009) to 69 % (Schook et al. 2011) of the second-opinion consultations (20.3 % Clauson et al. 2002, 29 % Malfait et al. 2013, 32 % Mellink et al. 2006, 51 % Tattersall et al. 2009).

Location of further treatment

According to the five studies examining this topic (Clauson et al. 2002; Malfait et al. 2013; Mellink et al. 2006; Morrow et al. 2009; Tattersall et al. 2009), the proportion of patients staying with the second-opinion physician for further treatment differs widely, from 16 % (Mellink et al. 2006) across 38 % (Tattersall et al. 2009), 44 % (Morrow et al. 2009), 50 % (Malfait et al. 2013) up to 65.8 % (Clauson et al. 2002).

Patient satisfaction

The patients’ satisfaction regarding waiting times and the quality of the second consultation was generally high (Mellink et al. 2003). Patients found the second consultation to be helpful. They noticed and appreciated differences in the setting and style of communication. They reported having received new information on their disease or treatment options and felt reassured (Philip et al. 2010; Tattersall et al. 2009).

Influence on the patient–physician relationship

In thinking about seeking a second opinion, patients consider their loyalty to the first doctor and the risk to offend the first physician as important (Philip et al. 2010).

Attitude and experiences of physicians

In one survey, however, 48 % of the polled medical oncologists felt comfortable or indifferent about their patients seeking second opinions and staying with the physician (Philip et al. 2010).

According to one study, medical oncologists feel that their second opinions are influenced by the treatment and treatment recommendations of the first doctor, their relationship with the first physician and the awareness that the consultation results will be available to professional colleagues. Fifty-two percent of them would modify their recommendation to what the first physician had advised. The medical oncologists would mostly neither criticize the first doctor (82 %) nor point to mistakes (72 %) (Philip et al. 2011).

Moreover, physicians involved in the second-opinion process seem to be more aware of potential legal relevance of their counseling (Philip et al. 2011).

Discussion

Second opinion is a widespread instrument in oncology. Yet, our systematic review revealed only scarce evidence. The portion of patients seeking a second opinion varied between 6.5 and 36 %. Patients worry on or perceive (possible) deficits in communication and in information and try to resolve these problems by a second opinion. Barriers to second opinion are a low level of education as well as a low socioeconomic status. Yet, as most studies focused on patients with breast cancer, it is questionable whether rate and characteristics of participants may be generalized.

Besides divergence from first opinion (12–69 %), outcome data on second opinion are scarce. While patients’ satisfaction is reported as being high, no patient-relevant outcomes are reported, neither are data on the quality of the second opinion. This high satisfaction must be viewed with caution, since all studies have a high risk of bias due to design, number of participants, lack of control group, single-institution settings and lack of validated instruments. On the other side, it must be considered that patient satisfaction with information is associated with quality of life (Husson et al. 2011). Yet, none of the studies included in this systematic review was able to demonstrate that an intervention designed to improve communication was able to enhance patient satisfaction.

From the data reported, some clues as to potential benefits and harms may be drawn that may help to design a concept for a structured second-opinion program as well as its evaluation.

Provision of a second opinion may support patient–physician communication and improve information as well as decision-making. On the other hand, discrepancies between first and second opinions may be an additional burden to the patient and to caregivers. These discrepancies may be due to a flawed first opinion. In this case, the second opinion may result in improved therapies that may justify disturbances of the patient and the patient–physician relationship. Yet, the provision of a divergent second opinion may also be due to the wish to comply with high expectancies of the patient and the wish not to disappoint or to destroy hope. Furthermore, as a worst-case scenario, competition and economic considerations may be involved.

As two drivers for second opinion exist (growing knowledge and specialization on the side of the physicians and growing need for and interest in information on the side of the patients), professional societies as well as patient organizations should be highly interested in assuring a high quality of the second opinion. In order to conceive a quality-driven second-opinion system in oncology, several issues need to be solved. These issues may be regarded under the aspects of structure, procedures and patient-relevant outcomes. For the healthcare system, also economical outcomes are relevant.

Before turning to second opinion, the most important focus must be a first opinion of high quality. With interdisciplinary tumor conferences and national cancer guidelines, most patients should be provided with such a high-quality first opinion. Certification may be a means to ensure this structural and procedural quality. To ensure high outcome quality, patient-centeredness of communication and decision-making seem mandatory as they are the basics of patient-focused prioritization and adherence to treatment. As Tattersall et al. (2009) as well as Zysman et al. (2014) were able to show, explanation of the involvement of an interdisciplinary team in the treatment decision alone has no influence on the patient’s desire for a second opinion; more detailed information on the reasons for a recommendation may be necessary. Maybe referral to the particular guideline (if available the patients’ issue of this guideline) may help to make the patient understand that the treatment proposal is not the recommendation of a single physician.

Nevertheless, some patients may remain in need of a second opinion. This may be due to uncertainty on the side of the physicians, e.g., in case of a rare cancer or treatment situation, or it may be due to the wish of the patient himself. The first case de facto is no question of a second opinion but of a consultation of an expert as no first opinion should be given in case of the treating physician being uncertain with respect to the treatment decision, in the case of the patient’s wish a true second-opinion situation comes into being.

While our review of the literature mainly points to the relevance of communication, some requirements for a high-quality second opinion should be discussed upfront:

• The provider of a second opinion should have a high qualification on the topic—in case of a reconsideration of a treatment plan, a multidisciplinary and multiprofessional second opinion is to be preferred.

• The second opinion must adhere to high-quality guidelines and/or be based on best available evidence.

• The process of generating the second opinion should be transparent, and the evidence should be clearly described, especially in case of a divergence from the first opinion.

• In case of a divergence, a structured high-quality communication process with the patient of the pros and cons of both opinions must exist. Shared decision-making seems to be the preferred decision process in this case. Yet, patient’s preferences regarding the decision-making must be respected.

• In order to eliminate confounding factors, the provider of a second opinion should not have any personal or economic interest in attracting the patient to his/her institution. This point may be difficult to realize as some reimbursement must be provided for a high-quality program. Considering the reported variable rates of patients staying with the second-opinion physician (from 16 to 66 %), reasons for and against changing the physician should be analyzed. As communication deficits are a main motivation for a second opinion, they may also be a reason to stay with this physician for treatment. Accordingly, those providing the first opinion might be motivated to improve their communication style.

• In case of reimbursement by statutory health services, any influence of insurance companies must be at least transparent.

Several structural as well as procedural questions are open:

• Who is in charge of providing all relevant medical data to the second-opinion institution?

• Should the patient be known to the institution providing the second opinion?

• Who is in charge of asking the patient for his preferences?

• Who will receive the second opinion? (The patient, the first opinion institution or someone else?)

• In case this is not the patient—who is in charge of providing the second opinion to the patient?

• Last but not least: Who is in charge of enabling the patient to include his/her preferences into a process of shared decision-making?

An independent evaluation of such a program should define patient-relevant outcomes of a second-opinion process and control for these parameters in a regular way.

Recommendations should be at least evaluated with respect to guideline adherence. If there are divergent treatment recommendations, data on the finally chosen therapy should be provided and analyzed, e.g., with respect to patient’s preferences. Patient satisfaction as well as quality-of-life data may be analyzed. In the long run, survival data from a structured second-opinion program must be provided.

Communication and communication skills, information and information exchange, knowledge and trust, decision finding, as well as respect and dignity may be parameters that have much more impact on relevant endpoints than structure and processes.

Ratings of these factors differ from patient to patient, happen partly unconsciously and can change throughout the course of disease. Furthermore, particularities of different types of tumors and patient groups as well as socioeconomical, ethnical and geographical impacts may be decisive—structures and processes must be flexible to allow for a patient-centered communication, and high-level communication skills are mandatory for all involved in the direct discourse with the patient. Those involved must be aware of their high responsibility to provide the individual best recommendation for a treatment.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.