Patrick Forde and Albert W. Wu Center for Health Services and Outcome Research, Johns Hopkins Bloomberg School of Health, Baltimore, USA KEY POINTS
• Error prevention and disclosure are important issues in modern oncology.
• Open disclosure of adverse events can foster patient-provider trust while also optimizing the processes involved in complex cancer care.
• Both patients and providers agree that errors should be openly disclosed.
• Frank disclosure of medical errors is unlikely to increase the risk of medicolegal consequences.
• Adoption of formal guidelines on disclosure are to be welcomed and will improve the standard of oncology care.
Introduction There is an increased focus by health systems on delivering safe care to patients, particularly in high risk areas such as cancer care. [1, 2] Each year in the United States, estimates suggest that at least 98 000 and perhaps more than 400 000 patients die as a result of medical errors, and many more experience harm related to preventable errors. [3, 4] Due to high patient throughput and the complex interdisciplinary nature of modern cancer care, preventable errors are not uncommon. International groups such as the American Society of Clinical Oncology (ASCO) have recognized this, with the development of guidelines specifically addressing areas such as management of central venous catheters. [5, 6] While there has been significant progress, errors will occur in oncology as in all other complex and specialized fields. This chapter addresses the issue of patient-provider discussions after an adverse event has occurred, reviewing the evidence related to open disclosure and current best practice for communicating with patients about adverse events. The chapter provides several practical case studies in error disclosure as it relates to cancer patients.
Why should we disclose? Ethical, practical,
and evidence-based support for disclosure of adverse events
Why is open disclosure of errors and adverse events important in oncology?
Good patient-provider communication is dependent on mutual trust and a belief that information regarding care, including adverse events, will be conveyed in a comprehensive and timely manner. There are many reasons why high quality cancer care is intrinsically linked with good communication. The first is due to the potentially fatal nature of the disease and its associated stressors. A second is the narrow therapeutic index of therapies and significant potential for side-effects. A third is the diverse care team involved, ranging from primary care practitioners and community or hospice nurses to oncologists, interventionalists, and surgeons. Non-disclosure or incomplete disclosure when an adverse event occurs may lead to distrust and a breakdown in the patient-provider relationship.  Patients themselves may fear the more nebulous consequences of a medical error, for example the possibility of retribution in terms of poorer treatment if they pursue a complaint or litigation. These concerns are also likely to be reduced by open disclosure.
The vast majority of patients report that they would want to be informed if an adverse event occurred during their care. Providers agree that errors and adverse events should be disclosed. [8, 9] Patients report preferring timely and full disclosure to a piecemeal approach or one guided by medicolegal concerns.  Despite this apparent agreement between patients and providers on the importance of disclosure, it is only in recent years that progress has been made toward open disclosure.
Arguments against disclosure Some have proposed that open disclosure can harm the patient-provider relationship, by adding distress for vulnerable patients, with no tangible benefit in terms of clinical outcomes. There are also concerns about damage to the relationship from loss of trust, and the potential for exposure to medicolegal consequences. [11, 12] However, there are convincing counter-arguments, in particular the loss of autonomy and justice for patients who are not informed of the adverse event, and the potential for future or continued errors.  In addition, patients may be deprived of compensation for harm that they sustain. While the benefits of disclosure almost always outweigh potential negatives, it is important to be aware of cultural and contextual characteristics specific to each case, and to provide information in a sensitive fashion. [14, 15]
Ethics of disclosure It is difficult to communicate information about an adverse event to a patient or family member. However, there are strong ethical imperatives supporting the disclosure of events, even those that are perceived to be minor or to have caused no harm. [16, 17] Several professional bodies, including the American Medical Association and the American College of Physicians, explicitly advocate for disclosure in their codes of ethics. [18, 19] Open disclosure is integral to patient autonomy and allows patients to make a collaborative and informed decision regarding cancer management.  Open and timely disclosure of an error can actually lessen the distress patients experience associated with uncertainty while strengthening the patient-provider relationship. This may be the case particularly when the provider is perceived to have conveyed information regarding the error in a caring and thoughtful manner. 
Should cancer patients be treated differently?
Patients with cancer have many expectations for their care that are similar to those with other medical conditions. However, they may also have additional disease-specific concerns, such as perceived delays in diagnosis, delays in treatment or errors in management. [20, 22] Since cancer treatments are in general more likely to have toxic side-effects than many other therapies, fears about side-effects are common and efforts to minimize risk are paramount.  It is important to put error into an honest context by avoiding minimization and by providing clarity on the likely impact (if any) of what has occurred.
Case Study 10.1
A 47-year-old patient has been diagnosed with non-Hodgkin lymphoma. She undergoes a staging bone marrow biopsy performed at the bedside. Although the patient had been apprehensive about the procedure, she has provided consent to proceed and the biopsy was successfully performed with local anesthesia and without distress. After additional tests, the patient returns for her first dose of chemotherapy. During the consultation, the patient casually asks about the results of the biopsy. On checking the notes, no record of the biopsy can be found and it is unclear what has happened to the sample. Imaging studies performed after the biopsy have confirmed that the patient has stage IV lymphoma, rendering the bone marrow biopsy results largely of academic interest.
Discussion This case brings the issue of patient autonomy to the forefront and highlights how open disclosure can facilitate an honest patient-provider relationship while also reducing the risk of similar errors in the future. While it would be relatively easy to gloss over the biopsy results in this case, this would be fundamentally dishonest. Concealing the error would also have the potential to jeopardize the patient-provider relationship in the future should the information come to light inadvertently or in a delayed fashion. Lack of disclosure might also reduce the chances of properly examining the factors that may have led to the biopsy sample being lost, and reduce the opportunity to prevent recurrence.
One approach to discussing this error with the patient is as follows:
Provider: Ms. X, I have reviewed your medical records and I cannot find a record of the biopsy arriving in my lab or the result. At this time, I do not know what has happened to the sample that was taken from you during the bone marrow biopsy. However, I promise to investigate this urgently and call you with the information later today.
I apologize for this happening after you went through the discomfort of the bone marrow procedure. Although I don't have a record of the biopsy, I want you to know that this should not affect your care or prognosis. I want to assure you that we will investigate this thoroughly and if necessary, change our processes to prevent this happening to another patient.
Case Study 10.2
A 29-year-old patient visits his primary care practitioner for a mass under his left arm. Investigations, including CT scan and a biopsy of the mass, reveal widely metastatic melanoma. On review of the patient's chart, it is noted that he had a skin lesion removed from his back via superficial excision at the practice three years previously. However, while the pathology report was filed in the results section of his paper chart, there is no indication that it was reviewed or acted upon. The pathology report from the current biopsy notes that the histology is consistent with metastasis from his previous melanoma resected three years ago.
Discussion In this situation it is likely that the error led to harm for the patient, that is, the lack of appropriate management of the original lesion. The patient now has a very serious medical condition which is likely to be fatal. While there may well be medicolegal consequences in this case, candor and open disclosure are still advisable. While even with the best communication this may damage the patient-provider relationship, conveying the information respects the patient's autonomy and right to information relevant to his medical condition. It seems likely that the patient would eventually learn about the error and timely disclosure is likely to reduce acrimony. Disclosure will also facilitate a review of the reasons why the report of the initial superficial excision was not seen or acted upon appropriately.
Disclosure of this event to the patient might be approached as follows during an in-person consultation.
Provider: Mr. Y, while reviewing your medical records, it has come to my attention that you had a skin lesion removed at our practice three years ago. I also found that this lesion was consistent with a melanoma of similar type to the cancer you currently have. It is likely that your current cancer represents a recurrence of this tumor. I do not find any follow-up for your original melanoma in your medical record. That was our mistake. We should have arranged follow up for your original skin cancer and considered adjuvant medical and surgical therapy and surveillance. While this may not have prevented relapse of your cancer, it would likely have reduced the risk of this happening. I have commenced an urgent investigation to find out the reasons why your original tumor was not followed-up appropriately after it was removed. I am sorry to have to give you this upsetting news, and would like to sincerely apologize on our behalf for our error. I want to offer the services of our counselor and our medical practice to provide support at this time.
Case Study 10.3
A 62-year-old woman is receiving adjuvant chemotherapy for breast cancer. Five days after her second cycle she is admitted hypotensive and febrile, her neutrophil count is zero. She requires intensive care with antibiotics, pressor support, and a prolonged ICU stay. She eventually recovers but requires prolonged rehabilitation for ICU neuropathy. Due to her prolonged neutropenia lasting over a week, her records are reviewed and it is noticed that she was inadvertently prescribed twice the recommended dose of chemotherapy on her last cycle.
Discussion This error led to direct, life-threatening harm for the patient. Open disclosure in this case is vital once the error is noted. Lack of disclosure could directly affect her medical care by preventing her clinicians from understanding the correct etiology of her neutropenia, for example, whether her prolonged neutropenia was due to a bone marrow failure disorder, and may lead to unnecessary tests such as a bone marrow biopsy. In turn, this may result in treatments that could cause her further harm. This would be unethical and could also lead to a failure to examine the factors that allowed the error to occur, thus putting other patients at risk.
This life-threatening error could be broached with the patient as follows:
Provider: Ms. Z, I am pleased that you are recovered from your illness; it has been a very challenging time for you and your family. Due to your blood counts being low for such a long period, we searched for reasons why this occurred. On reviewing your medical record, I discovered an error in the dosage of chemotherapy that I prescribed for you during your last cycle. I made a calculation error and prescribed twice the recommended dose of one of your chemotherapy drugs. I am truly sorry for the way that my error has affected you. We do have processes in place to pick up and rectify this type of error. Unfortunately, they also failed in this case. I can tell you that it should not cause additional problems for you in the future. In any case, we would like to prevent this kind of thing from happening in the future. Along with my colleagues, I have commenced a complete review of our processes involved in chemotherapy prescription.
What we do at present While the large majority of physicians agree that they should disclose adverse events to patients, a minority of physicians-in-training report having disclosed a serious error (34%) or having received formal training in disclosure (33%). [24, 25] There is evidence that attitudes towards disclosure have changed in recent years, with surveys conducted nine years apart among residents in the same program showing an increase in intention to disclose.  In 1999-2000, 29% surveyed would disclose an adverse outcome case and 38% a no harm case, while in 2008-2009, 55 and 71%, respectively, would disclose.
Commonly cited reasons for non-disclosure include fear of lawsuits, fear of being perceived as incompetent, or fear of experiencing shame. [9, 27, 28] Though in theory physicians may support disclosure, much of the time they may not practice it.  Oncology care places particular emotional and professional demands on providers, which may contribute to burnout. Recent data suggest a direct relationship between numbers of patients seen and self-reported stress.  Some providers who treat cancer patients report a reluctance to disclose errors to patients who are very ill or close to death to avoid adding an additional stress or destroying the patient-doctor relationship at a critical juncture.  The complexity of modern cancer care may make it difficult to accurately ascribe adverse outcomes to disease progression, expected toxicity of treatments, or medical errors. In these circumstances, it is appropriate for open disclosure to provide accurate information about the occurrence of an adverse event, without speculating about the causation of harm.
Interestingly, patients with cancer report that in the event of a medical error, they consider positive actions to prevent similar adverse events recurring and evidence of clinician learning to be of highest importance.  Despite this, many oncology patients who experience a medical error do not have a good experience.  Interestingly, most patients report that financial reparations are not of major importance to them, with only 3% ranking them as an important consideration with regards to successful handling of an error. 
There is encouraging evidence of open disclosure becoming the norm in cancer care, at least when errors occur that affect large populations of patients. However, the success of disclosure communication processes in these cases has varied. [32, 33] Despite the relative frequent occurrence of large-scale adverse events in healthcare, most institutions do not have policies in place to handle them. Systematic attempts to provide a framework for large-scale error disclosure have been developed by some health systems, with the Veterans Health Administration Directive 2008-002 on Disclosure of Adverse Events being a positive example. 
The legal consequences of adverse events and errors tend to vary. In the United States, several states have adopted "Apology laws" which may render comments that physicians make to patients after an error inadmissible as evidence.  Some of these specifically protect the apology, while others protect both the apology and explanation from being introduced into evidence. Within the US context, these may ultimately lessen the traditional inclination for physicians to be guarded with patients after an error has occurred, an approach that has been fostered in the past by hospital attorneys, malpractice insurers, and hospital administrators. This guarded stance may actually worsen communication and prevent the patients from receiving the empathy that they have reported as important after an adverse event. While compensation may be a necessary response to a medical injury, litigation may not be needed. Resolving a claim for compensation without recourse to the courts is likely to be mutually attractive to patient, provider, and hospital.
Overall, while cancer care has come a long way on the road to open disclosure, there are still barriers to overcome.
Communicating adverse events in oncology There is clear consensus between patients and providers, as well as policy-makers and professional bodies and ethicists, that adverse events should be disclosed. The following section attempts to set out a framework for disclosure. Strategies for disclosing a medical error (Table 10.1) and a template for dealing with a mistake from the time it is recognized onward are also provided (Figure 10.1).
When The best time to tell a patient that a harmful or potentially harmful error has occurred is as soon as possible after it comes to light. In some cases, disclosure may be delayed, for example after an error that has catastrophic consequences, leading to severe acute illness or prolonged loss of consciousness. However, early disclosure respects the patient's autonomy and right to information about their care while also helping to maintain trust between the patient and provider. It also reduces the anxiety caused by uncertainty the patient and family may have about the cause of deteriorating health.
Where Discussions regarding medical errors should take place in a confidential manner and in a quiet and comfortable environment where interruptions are at a minimum. All involved parties may be emotional and providing privacy is respectful.
Table 10.1 Disclosure components and examples of things to say.
Component of disclosure
”I am deeply sorry for our oversight.”
"This mistake has clearly caused significant distress for you and your family.”
Consequences for Patient
" While this error has not had serious consequences for you, it should not have happened and I would like to apologize on my behalf and that of the practice.”
"My error has led to you being admitted to hospital and undergoing several procedures, I am deeply sorry for this.”
Consequences for Provider
"We will be reviewing our practice in light of this error occurring and taking steps to prevent it happening again.”
"I have instituted a full review of the processes which led to this error occurring, so that we can learn from it and prevent it happening to another patient. When this review is completed I will inform you fully of the changes we will implement.”
Opportunities should be given to patients to have family members or caregivers present as they wish.
Who Patients often want to hear what happened from "their physician." However, given the multidisciplinary nature of cancer care, there are almost always multiple people and systems involved in a harmful incident. As a rule of thumb, the patient's primary cancer physician should be present at the time of disclosure. However, when it is possible, other providers directly involved in the case might also be present if they can help explain what happened. Junior clinicians may be supported by more senior colleagues who may help with addressing patient concerns and questions. Errors involving systems failures or administrative issues can be disclosed in the presence of a hospital representative if this is necessary to the explanation.
Involvement of the care team including nurses and social workers is to be encouraged as it promotes understanding of what has been disclosed and avoids awkwardness in subsequent communication with the patient.  Healthcare professionals involved in the patient's care who were not present at the disclosure meeting itself should be subsequently informed regarding the discussion so as to avoid confusion regarding what has been disclosed. It is desirable that there be only one story that is shared with both patient and staff.
Legal representation at the disclosure meeting is a controversial subject with several potential pros and cons. In some cases, involvement of risk management can provide clarity while others have reported that it may interfere with the clinical relationship. [38, 39]
Figure 10.1 A template for dealing with a mistake from the time it is recognized onward.
Depth of information As discussed previously, in the event of an adverse event patients want to know what has occurred and the reasons for the event occurring. Ambiguity in discussions can give the impression that clinicians are not being honest. A clear explanation of the events leading up to and around the time of an error can help the patient understand how the incident happened.
Clearly explaining the consequences of the error in understandable terms is vital, and ample time for questions and reaction should be allowed. Patients frequently want to know the practical implications of the incident on their cancer and what steps can be taken to avert any adverse consequences. Questions may include, "will my prognosis be affected" or "will I require additional tests or treatment?"
An apology should be made promptly and in a manner that is appropriate to the specific incident. The disclosing clinician should acknowledge that an error occurred, and should express remorse. Patients expect an apology when it is evident that there was an error. Apologies of sympathy ("I am sorry that this has happened to you") may appear evasive or insincere if applied to a situation in which an apology of regret is called for ("I am sorry that we did this to you"). A sincere and heartfelt apology can improve the relationship, both at the time of disclosure and subsequently. Some insurers may try to dissuade providers from offering an apology, or from using specific language. However, in reality there is no precedent for using a provider's apology against him or her in a subsequent legal case. Avoiding an apology is much more likely to work against a provider, rather than providing protection from legal action.
It is important to describe tangible steps that will occur to investigate or to prevent a medical error from happening again. Clear procedures for investigating the error and setting procedures in place to prevent future recurrence should be detailed to the patient ("After our meeting, I will meet with our ... to investigate ... "). The presence of risk management at the meeting can sometimes be helpful in this regard.
Emotions such as anger and grief should be acknowledged. It is natural and expected that some patients will ask for an alternative provider or a second opinion ("You have a right to be angry"). These requests should be acknowledged and the necessary connection be made available to the patient.
Building a culture of disclosure It is difficult for disclosure to take place if healthcare providers do not feel safe and supported by their institution. This requires that there be a palpable culture of safety that is expressed by top leaders and unit managers. The following are practical steps which can be taken to foster a culture of open disclosure in cancer care.
Formal training in error disclosure As discussed previously, the vast majority of currently trained physicians and other healthcare workers have never received formal training in communication skills focused on error disclosure. Training courses and videos are available and evidence shows that they improve practical skills. [20, 40] Independent organizations such as Medical Induced Trauma Support Services (MITSS)  and SorryWorks!  are available for both clinicians and patients. Courses may address concerns that physicians and trainees might have regarding disclosure discussions and in particular issues such as inflaming emotional upset through disclosure, dealing with strong emotions during a discussion, feelings of personal guilt, and being directly blamed by patients for failure. Training for disclosure should outline the evidence and rationale for why disclosure is necessary, and discuss patient expectations from a disclosure discussion. Misconceptions about disclosure should be addressed and the evidence provided to participants in training sessions. Common pitfalls in discussing errors with patients are reviewed, such as incomplete or inaccurate disclosure regarding the attribution of a medical error. It is instructive to simulate encounters with other participants or actors to practice disclosure conversations and reacting to patient responses.
Institutional and professional body policies on disclosure The adoption of policies favoring disclosure of errors by influential clinicians, individual hospitals, health systems, and leading professional bodies is needed to promote a culture in which disclosure becomes the norm rather than the exception. The American Society of Clinical Oncology has taken steps in this direction in recent years with prominent presentations at Annual Meetings and educational sessions.  Further efforts in this regard are to be encouraged and the development of formal guidelines on disclosure in cancer care would be a welcome step forward.
Conclusion Errors and adverse events are inevitable in cancer care given the complexity of modern treatments and healthcare. Due to the specific nature of cancer care, these incidents can have disastrous consequences. It is now widely recognized that physicians and healthcare organizations have an ethical and professional obligation to promote and practice disclosure of errors. Concerns expressed by physicians regarding the consequences of disclosure on careers are real and we should strive for a culture that does not punish individual failures, but rather undertakes detailed analysis of the processes and contributing factors. Prompt and open disclosure, while not without its challenges, is the best policy in providing the best chance of helping the patient, preserving the physician-patient relationship, and minimizing the trauma of litigation.
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