Preventable Errors in Organ Transplantation: An Emerging Patient Safety Issue?

Abstract

Several widely publicized errors in transplantation including a death due ABO incompatibility, two HIV transmissions and two HCV transmissions have raised concerns about medical errors in organ transplantation. The root cause analysis of each of these events revealed preventable failures in the systems and processes of care as the underlying causes. In each event, no standardized system or redundant process was in place to mitigate the failures that led to the error. Additional system and process vulnerabilities such as poor clinician communication, erroneous data transcription and transmission were also identified. Organ transplantation, because it is highly complex, often stresses the systems and processes of care and, therefore, offers a unique opportunity to proactively identify vulnerabilities and potential failures. Initial steps have been taken to understand such issues through the OPTN/UNOS Operations and Safety Committee, the Disease Transmission Advisory Committee (DTAC), and the current A2ALL ancillary Safety Study. However, to effectively improve patient safety in organ transplantation, the development of a process for reporting of preventable errors that affords protection and the support of empiric research are critical. Further, the transplant community needs to embrace the implementation of evidence-based system and process improvements that will mitigate existing safety vulnerabilities.

A number of high profile patient safety events have occurred in organ transplantation in which errors in the systems and processes of care resulted in patient injury. One of the earliest reported major adverse events in transplantation occurred in 2003, when 17-year old patient, Jessica, with blood type O, received a heart and lung from a blood type A donor.[1] Shortly after the transplant was completed, the error was recognized and, despite receiving a second heart and lung transplant, the patient died as a result of “global cerebral hypoxic injury that was a complication of the rejection of an … incompatible heart-lung transplant.”[1] While the transplanting surgeon publicly assumed responsibility for this tragic event, it became apparent during the review of the event that the fundamental or “root” cause of the medical error was a failure in the systems and processes of care. In essence, the system and process used to verify donor-recipient ABO compatibility during transplantation lacked “high reliability.” In fact, no standardized and redundant processes were in place for confirming blood type compatibility between the donor and the recipient. A policy has since been developed to standardize this process which includes redundant confirmation processes.[1] Specifically, the Organ Procurement and Transplant Network (OPTN) policy now requires that the transplanting surgeon at the transplant center receiving an organ offer must assure the “medical suitability of the donor organ for transplantation,” including the ABO blood type and subtype compatibility between the donor and the transplant candidate (OPTN Policy 3.1.2). It should be noted, however, that the policy does not offer any specific recommendation about the optimal systems and processes of care to assure “medical suitability.”

More recently, a number of infectious disease transmissions have occurred during transplantation that were also found to be directly attributable to failures in the systems and processes of care and, therefore, are highly preventable. In one case, three organs from a human immunodeficiency virus (HIV)-positive donor were transplanted at two hospitals in Tuscany, Italy, resulting in the transmission of HIV to all three recipients.[2] The transmission was found to be due to a transcription error of the donor’s HIV serology result (from positive to negative) during evaluation of the organ suitability for transplantation. The error was detected five days after the transplantation was performed when a positive HIV result was received as part of the donor evaluation for tissue transplantation.[2] Poor reliability and inadequacy in the systems of care, such as a lack of automatic transcription of serology results from the laboratory instruments to the laboratory information system (LIS) and, then, to the donor medical records were identified. To mitigate the occurrence of similar disease transmissions, a committee of transplant experts made several recommendations, including: (1) automatic transcription of test results from laboratory instruments to laboratory information systems and to donors’ medical records, (2) centralization of donor laboratory tests for solid organs and tissues, and (3) training to develop a proactive quality and safety culture in regional donation and transplantation networks.[2] These expert recommendations became incorporated in Italian national transplant regulation and all laboratories supporting the Italian transplant network are presently obtaining national certification and centralization at a regional level.

Despite these recommendations, a hauntingly similar error recently led to the transmission of HIV to one heart, one liver, one lung, and two kidney recipients in Taiwan.[3] The donor had a positive HIV test during evaluation but a transplant team staff member mistakenly heard the English word “nonreactive” in reference to the donor’s positive HIV test result. Although the results of the root cause analysis (RCA) of this event have yet to be made publicly available, evidence suggests that many of the same failures in the systems and processes of care, identified in the adverse event in Italy, also contributed to this HIV transmission.

Two recent hepatitis C virus (HCV) transmissions in the United States (US) reveal additional ways in which failures in the systems and processes of care can lead to significant medical error yet, are highly preventable. In the first case, a vessel from a HCV seropositive donor was inadvertently utilized in a HCV seronegative recipient despite appropriate labeling of the HCV seropositive vessel. [4] During the subsequent investigation, conducted by the Pennsylvania Department of Health and the Centers for Disease Control and Prevention (CDC), two similar adverse events were identified wherein appropriately labeled Hepatitis B (HBV) core antibody positive donor vessels and an appropriately labeled HCV-antibody positive donor vessel, respectively, were utilized in hepatitis seronegative recipients. Fortuitously, in both instances, no disease transmission occurred. Based on these events, the CDC recommended that “transplant centers discontinue the practice of storing vessels from donors who are seropositive for hepatitis.” [4] The OPTN recently approved policy modifications to Policy 5.10.1 (Vessel Recovery and Transplant) and 5.10.2 (Vessel Storage) to prevent this error from occurring by precluding the storage of HCV antibody positive and HBV surface antigen positive extra vessels for subsequent use.

Errors with labeling and packaging have been reported by the OPTN/UNOS Operations and Safety Committee as a recurrent problem across transplant centers and, in 2011, accounted for 38% of the reported errors.[5, 6] This probably results in part due to the current process in which the labeling of vessels requires the manual creation of a label that is then affixed to the storage container. Further, a transplant center staff member is currently expected to verify and document the verification of the UNOS Donor ID, donor ABO type, donor serology results, recipient ABO type, recipient serology results, as well as the container content, and the date of expiration. As a result, this important process relies entirely on human actions and currently has no built in safeguards or redundancies.

In the second case, HCV transmission occurred from a donor with no recognized risk factors for HCV (although the donor’s social history was obtained from individuals unfamiliar with the donor’s recent personal habits and behaviors), who was also found to be HCV antibody negative during the organ and tissue donor serology screening.[7] The donor tissue evaluation included additional HCV nucleic acid testing (NAT) but the result was incorrectly reported as negative because of a misreading of the reaction wells.[7] Once the error was identified repeat NAT was performed and it was confirmed that the donor was HCV NAT-positive at the time of donation. The consequence of this error was that two kidney transplant recipients acquired HCV, while transmission to the liver recipient could not be substantiated, as the recipient was previously infected with genotype 1A HCV, the same genotype as the donor. In addition, a pediatric recipient of a cardiopulmonary tissue patch, procured from the same donor, also acquired HCV. Although the role of NAT for organ donor screening is still under debate and the NAT in this case was performed for subsequent tissue donor screening, many Organ Procurement Organizations (OPO) are using NAT to screen organ donors, without a national mandate. Above mentioned vulnerabilities in the systems and processes of testing and reporting that contributed to this HCV transmission exist in organ screening and need to be taken under consideration to prevent similar errors from being made as part of serology or NAT screening of organ donors.

While patient safety events related to ABO incompatibility and infectious disease transmission have received prominent coverage in the press and in the transplant community, recent data suggest that other failures in the systems and processes of transplantation care may, in fact, be as or more critical and have greater impact on organ availability and transplantation outcomes.[8] The OPTN/UNOS Operations and Safety Committee collects data about preventable errors which show that 55% of reported adverse events are due to miscommunication and errors in documentation and data entry. Separate data about kidney and liver transplantation confirm that failures in communication and coordination of care are significant contributors to preventable errors.[9, 10] Such data likely represent the tip of the iceberg of the true scope of the problem.

While significant patient safety improvements have been achieved during the last decade (e.g., creation of a central line bundle, reduction in respiratory associated pneumonia, implementation of prophylaxis for decubitus ulcers and deep vein thrombosis), a recent Inspector General’s report showed that the number of adverse events with serious or temporary harm attributed to medical errors remains exceedingly high, affecting 13.5% of hospitalized Medicare beneficiaries and leading to 130,000 deaths annually.[11] Similar to other reports [12, 13], 44% of the medical errors identified as the cause of death were considered to be preventable. At present, there are no similar transplantation-specific data available. As shown in Table 1, the safety events reported in this paper can be classified into four of twenty categories from the Joint Commission Classification Root Causes by Event Type.[14] In addition, the table addresses their preventability by showing implemented and potential solutions

Table 1.

Transplant-Specific Categories of System and Process Errors (Modified from the Joint Commission) [14]

Categories	Transplant Error	Implemented Solutions	Potential Solutions
Communication	Mistakenly heard “non-reactive” in reference to donor’s positive HIV test (Taiwan) [3]		-Automated transcription of laboratory results from instrument to information system to electronic medical record (EMR)
	Labeling error of organs [6]		-Using pre-printed labels -Two dimensional bar code label -2 person independent label check
Human Factors	Transcription error of HIV serology result (Italy) [2]	Italian national transplant regulations: Automated transcription of laboratory results from instruments to information system to donor medical record Centralization of donor laboratory tests for solid organs and tissues Training to develop proactive quality and safety culture in transplant community
	Appropriately labeled HCV donor vessels used in donor negative recipient leading to HCV transmission [4]	CDC recommendation: -No storage of hepatitis seropositive vessels [4] UNOS/OPTN: -HCV/HBV positive vessels may not be stored (Policy 5.10.1)
	Misreading of HCV-NAT reaction well [7]		-Two person independent check of reaction well reading -Automated well-reading -Automated transmission of well-reading into EHR
Information Management	ABO-incompatibility between donor and recipient (US) [1]	UNOS/OPTN: -Standardized, redundant confirmation process for ABO compatibility between donor and recipient (OPTN Policy 3.1.2)	-Automated system: Uploading of ABO type of recipient and donor into system with automatic compatibility checking
Leadership	Underreporting of transplant related errors; poor reporting on potential errors or near misses [5]		-Formal, non-punitive system for timely, systematic, comprehensive reporting of errors and potential errors; -Robust feedback system to reporters

Transplant Error: Actual occurrence of transplant related error; Implemented solutions: Solutions that were implemented in response to the transplant related error; Potential Solution: Suggested improvements to mitigate of transplant related errors; lab: laboratory; EHR: electronic health record; HCV: Hepatitis C; HBV: Hepatitis B

In fact, a systematic review of the literature revealed few articles addressing patient safety in transplantation and most manuscripts were expert opinions rather than based on data considered as “high-level of evidence.”[15] Furthermore, many have suggested that organ transplantation is relatively “safe” when considering the limited options of transplant candidates who frequently die as the result of end organ failure.[16, 17] However, the authors believe that tolerating patient safety risks merely because transplant candidates have few options other than transplantation is a poor argument against examining the systems and processes of care in organ transplantation and implementing solutions to mitigate and prevent medical errors.

The OPTN should be commended for its investments in understanding the epidemiology and risk factors of infectious disease transmission through organ transplantation.[8, 18] In response to the ABO incompatible heart-lung transplant in 2003, the OPTN/United Network for Organ Sharing (UNOS) created an ad hoc taskforce to regulate the process of ABO verification. This taskforce evolved into the OPTN/UNOS Operations and Safety Committee, which focuses on broad safety issues beyond ABO compatibility and attempts to study and improve the various systems and processes of care related to transplantation. In addition, the CDC, and the work of the ad hoc Disease Transmission Advisory Committee (DTAC), have gathered a significant body of data to begin to define the epidemiology and outcomes of donor-derived disease transmissions. Data collected by DTAC, CDC and the OPTN/UNOS Operations and Safety Committee reveal that many adverse events are preventable. In fact, the recent revisions made to OPTN policies 2, 4, and 5, sponsored by DTAC and the Operations and Safety Committee, were crafted to address such preventable errors.

Yet, there is still much to be done to fully characterize, understand, and mitigate the underlying failures in the systems and processes of care that lead to preventable medical errors in organ transplantation. The National Health, Lung, and Blood Institute (NHLBI) has funded a number of studies, such as REDS, REDS-II and REDS-III which have dramatically improved blood safety by prospectively studying the epidemiology of disease transmission through blood transfusion.[19] Further, the NHLBI studies have defined the yield of donor screening modalities and led to prioritization of diseases that warrant screening. Studies funded and conducted outside the United States, such as the Spanish RESITRA cohort, have significantly enriched our understanding of donor-derived infections, including risk factors and mitigation techniques. Unfortunately, comparable support for patient safety research and solution implementation in organ transplantation in the United States is lacking.[20] Recently, the National Institute for Digestive Diseases and Kidneys Diseases (NIH/NIDDK) sponsored a study of patient safety in living donor liver transplantation as an ancillary R01 study of the Adult-to-Adult Living Donor Liver Transplant Cohort Study (A2ALL). [21] Similar commitments of research funding are essential to comprehensively study the systems and processes of care and to develop effective solutions to mitigate and prevent medical errors in organ transplantation.

In addition to securing the necessary research funds, numerous other barriers remain. First, there is, in general, a significant underestimation of the magnitude of the problem, and in transplantation, more specifically. Deaths, each year, due to preventable adverse events are higher than deaths by motor vehicle accidents or breast cancer and preventable adverse events are even more common in the setting of high complexity with organ transplantation.[10, 22] Clinicians and surgeons, in particular, traditionally equate medical errors with human shortcomings and often fail to understand the importance of redesigning the systems and processes of care in order to anticipate and mitigate potential failures that can lead to errors.[23] However, clinicians have become considerably more aware of the issues surrounding preventable adverse events[24] with the implementation of CMS’s denial of reimbursement for “never events,” with the introduction of the National Surgery Quality Improvement Program (NSQIP), and with public reporting of center-specific quality parameters (e.g. surgical site infections).[25]

Organ transplantation is a particularly complex context of healthcare and routinely “stresses” nearly all of the systems and processes of surgical care.[26] Studying the systems and processes of surgical care during organ transplantation offers a unique opportunity to proactively expose failures and vulnerabilities that might otherwise remain unrecognized until the occurrence of an adverse event.[27] This complexity has been recognized by CMS [24] with solid organ transplantation receiving one of the highest relative value units (RVUs) in the Medicare Fee Schedule compared to other complex surgical procedures. Organ transplantation offers a context of care in which to efficiently identify patient safety vulnerabilities and to implement potential solutions to improve patient safety that can be generalized to a wide range of other healthcare contexts. [9, 10]

The significant healthcare costs associated with medical errors are an additional aspect that cannot be overlooked. While transplantation–specific costs for injuries related to preventable adverse events are not available, overall costs due to preventable adverse events in the US were estimated at $19.5 billion in 2008 with an average cost of $13,000 per error.[28] These costs are likely to be underestimated, as they do not include costs for medical errors that did not lead to patient injury (e.g., wrong medication administered but without evidence of harm to the patient).[29] In 2010, an actuarial report estimated that there were 5,147 medical errors for transplant patients costing $55,654 per error and amounting to $286 million per year.[28] In comparison, medical errors related to ventral hernia repairs were estimated to occur in 53,810 cases at a cost of $6,359 per error, amounting to a similar amount per year ($342 million). Because transplantation is such a high cost/medical error context of care, the prevention of a single medical error in organ transplantation could conceivably achieve savings comparable to preventing 10 errors in hernia surgery.

Moreover, while OPTN/UNOS currently collects information on “near miss” events and patient safety issues through the Operations and Safety Committee, the lack of protection from sanctions or suspensions for reporting institutions surely contributes to under- or lack of complete reporting. The experience of DTAC highlights the importance of having a formal reporting and review system which affords punitive protection and occurs outside of the Membership and Professional Standards Committee (MPSC) process. The DTAC system started with only 7 reports its first year but reviewed 181 potential disease transmission reports in 2011. With enhanced recognition of errors and of the value of reporting, a more complete picture of the epidemiology of disease transmission in the United States has become possible and, as a result, several risk mitigation strategies have been identified and implemented. The authors believe that to achieve the highest reliability in the systems and processes of care during organ transplantation, a culture that accepts rigorous study of all systems and processes of diagnostic and therapeutic care in organ transplantation is needed. Additionally, the authors feel that a formal system needs to be developed that facilitates timely, systematic, and comprehensive reporting of errors and potential errors through an independent process that is protected from punitive action. Much like the DTAC process, such a reporting system would lead to a description of the epidemiology of transplantation errors, and permit the development of effective risk mitigation strategies.

Outside the US, the European Union Directive 2010/45/EU on “standards of quality and safety of human organs” requires the establishment of robust systems to collect data on serious adverse events and reactions with the goal of having a more comprehensive evaluation of the quality and safety of organs intended for transplantation.[30] It further requires sharing of this information among member states to prevent future errors and improve the overall outcomes of transplantation. The Directive provides clear definitions as to what represents a preventable event and requires member states to have a “reporting system in place to report, investigate, register and transmit relevant and necessary information concerning serious adverse events that may influence the quality and safety of organs and that may be attributed to the testing, characterization, procurement, preservation and transport of organs, as well as any serious adverse reaction observed during or after transplantation.” The Directive was enacted in 2010 and is currently being put into law in each of the EU member states. Although significant work has been put into developing such systems through projects such as the European Framework for the Evaluation of Organ Transplants (EFRETOS, www.efretos.org), implementation into practice is just starting and the first report from each member state is only required by August 27, 2013.

Building upon DTAC and the A2ALL Patient Safety Study[21], a comprehensive study of the epidemiology and the root causes of patient safety adverse events that cause loss of organs and significant post-transplant morbidity or mortality in solid organ transplantation, should be undertaken. Likewise, serious consideration should be given to the implementation of the recommendations already made by the expert review committee following the transmission of HIV in Italy to mitigate such an event from occurring in the US. Improving systems and processes of care to reduce preventable errors in organ transplantation, will, like other innovations before it, significantly improve transplantation outcomes.

Abbreviations

A2ALL

Adult to Adult Living Donor Liver Transplant Cohort Study

CDC

Centers for Disease Control and Prevention

DTAC

Ad Hoc Disease Transmission Advisory Committee

HBV

Hepatitis B

HCV

hepatitis C virus

HIV

Human Immunodeficiency Virus

NAT

Nucleic Acid Testing

OPO

Organ Procurement Organizations

OPTN

Organ Procurement and Transplant Network

UNOS

United Network for Organ Sharing

REDS

Recipient Epidemiology and Donor Evaluation Study