Compassion fatigue in healthcare providers: A systematic review and meta-analysis

Abstract

Background:

Compassion fatigue is recognized as impacting the health and effectiveness of healthcare providers, and consequently, patient care. Compassion fatigue is distinct from “burnout.” Reliable measurement tools, such as the Professional Quality of Life scale, have been developed to measure the prevalence, and predict risk of compassion fatigue. This study reviews the prevalence of compassion fatigue among healthcare practitioners, and relationships to demographic variables.

Methods:

A systematic review was conducted using key words in MEDLINE, PubMed, and Ovid databases. Data were extracted from a total of 71 articles meeting inclusion criteria, from studies measuring compassion fatigue in healthcare providers using a validated instrument. Quantitative and qualitative data were extracted and compiled by three independent reviewers into an evidence table that included basic study characteristics, study strength and quality determination, measurements of compassion fatigue, and general findings. Meta-analysis, where data allowed, was stratified by Professional Quality of Life version, heterogeneity was quantified, and pooled means were reported with 95% confidence interval. A table of major study characteristics and results was created.

Ethical consideration:

This paper contains no primary data obtained directly from research participants. Data obtained from previously published resources have been acknowledged within references. Psychological distress, particularly compassion fatigue, can be insidious, no health profession is immune, and may significantly impact the ability to provide care.

Results:

A total of 71 studies were included. Compassion fatigue was reported across all practitioner groups studied. Relationships to most demographic variables such as years of experience and specialty were either not statistically significant or unclear. Variability in reporting of Professional Quality of Life results was found.

Interpretation:

Compassion fatigue exists across diverse practitioner groups. Prevalence is highly variable, and its relationship with demographic, personal, and/or professional variables is inconsistent. Questions are raised about how to mitigate compassion fatigue.

Keywords

Burnout compassion fatigue healthcare practitioner nursing Professional Quality of Life secondary trauma

Introduction

Compassion fatigue is described as a healthcare practitioner’s diminished capacity to care as a consequence of repeated exposure to the suffering of patients, and from the knowledge of their patient’s traumatic experiences.¹ Compassion fatigue is a result of providing patient care, and is more often considered as the result of many events, though it could arise from the experience of caring for an individual patient or event. Compassion fatigue is closely related to the concepts of “vicarious trauma” and “secondary traumatic stress (STS),” both of which also result from exposure to the trauma experienced by patients, rather than to the trauma itself.² However, other factors contribute to the development of compassion fatigue, for example, burnout (BO) may develop through factors such as work hours (i.e. shift work) and work environment, impacting an individual’s capacity to care.³

Instruments have been developed to measure the prevalence of, and examine risk factors for, compassion fatigue in care providers. One such instrument is the Professional Quality of Life (ProQOL) scale developed by Stamm. The ProQOL began as the “Compassion Satisfaction and Fatigue Test (1993),” and was developed to measure both the positive and negative elements experienced by persons who act as professional helpers.⁴ The instrument uses three subscales: Compassion Satisfaction (CS), BO, and STS/compassion fatigue (depending on the version). The subscales are scored separately, and scores are not considered cumulatively; there is no accepted method of combining subscales to report an overall score.⁴ Instead, combinations of high and low scores in the subscales indicate an overall level of compassion fatigue. Within each of the 3 domains, a score greater than 42 is considered as high, 23–41 as average, and 22 or less as low. CS indicates the positive feelings associated with doing a type of work, and a higher score is suggestive of more contentment. Higher scores in STS and BO would indicate more negative feelings and distress. The ProQOL does not have a scale specific control value for use as a diagnostic instrument. The scale has evolved as more is learned about the factors contributing to compassion fatigue; the current instrument represents the understood relationships between the positive and negative effects of work on care providers.

Aim and objectives

This systematic review sought to describe and summarize the prevalence of compassion fatigue in healthcare practitioners using narrative synthesis, and meta-analytic methods where data presented permitted. We asked the following:

What is the frequency of reported compassion fatigue and in which care providers?

What variables impact compassion fatigue?

What are the common values reported in the subscales of ProQOL?

Methods

Search strategy

A broad electronic search was conducted using the MEDLINE (Ovid interface) and PubMed databases, using MeSH term “compassion fatigue,” with additional keyword searches for “secondary traumatic stress,” “secondary traumatization,” and “vicarious traumatization.” Search terms were combined using Boolean operator “OR.” Articles were included from earliest available content up to 31 December 2017. The bibliographies of articles meeting inclusion criteria were also searched by reviewers for any additional articles.

Inclusion criteria

To be included in this review, studies were required to meet the following inclusion criteria: English language, containing data that included a measurement of “compassion fatigue,” using a validated measurement tool and reporting mean or median scores, using a participant sample consisting of practitioners from a professional healthcare discipline providing frontline patient care, and originating from a peer reviewed scientific journal. Studies that were specific to an examination of interventions or mitigation strategies were excluded.

Study selection and reporting

This systematic review and meta-analysis was conducted consistent with recommendations from “The Meta-analysis of Observational Studies in Epidemiology” guidelines, and reported in accordance with the PRISMA statement.^5,6 No protocol was registered. A total of 1302 records were returned from the electronic search strategy. An additional 46 records were found through reference searches. Two reviewers (N.L.C. and C.H.) reviewed the abstracts of those articles and included them for full review if the abstract suggested they met inclusion criteria. Of the 113 abstracts identified, the same reviewers independently and in parallel stringently applied the inclusion and exclusion criteria to the full text of the articles to identify the 71 articles that remained for this study. See the PRISMA diagram (Figure 1). Fifteen studies were excluded due to an issue with data reporting (including incomplete data), 17 did not specifically report prevalence, 4 studies did not use a validated instrument, 3 studies were not presented as journal articles, and 2 did not study healthcare practitioners.

Figure 1.

PRISMA diagram of study selection.

Data extraction

After the final list of articles for inclusion was identified, data were extracted by two authors (N.L.C. and G.C., or N.L.C. and C.D.) with all data independently verified by each author, and discrepancies resolved by consensus. Quantitative data used in the meta-analysis (e.g. mean score, standard deviation, sample size) were abstracted by two authors (C.D. and L.D.) and any discrepancies were resolved through discussion.

Full text review of included articles resulted in a list of study characteristics for extraction. These characteristics were used to develop an evidence table that included the following: the study’s demographic details (source, year, country, number of participants) and information pertaining to the overall strength and design (population, total sample size, sampling method, research design, level of statistical analysis, response rate, method of assessment, and the measurement tools utilized). Study result data were recorded as quantitative results (mean scores, risk/incidence) and narrative summary.

Assessment of quality

Compassion fatigue is most often investigated using descriptive cross-sectional survey methodology, which is appropriate for this subject matter. During full-text review, studies were assessed under guidelines from the National Health Institute Quality Assessment Tool for Observational Cohort and Cross-Sectional Studies.

Data synthesis and analysis

As described, the ProQOL is measured on three sub scales: CS, BO, and compassion fatigue/STS. The third scale is sometimes measured as “compassion fatigue” and sometimes as “STS,” and each is scored differently. The versions of the ProQOL used in the reviewed studies varied (when reported) among versions III, IV, and V, and both “compassion fatigue” and “STS” were reported as the third subscale.

Data were reported in individual studies one of three ways: (1) a detailed measure of risk based on participant’s mean score on each of three subscales compared with established cut off scores, (2) a limited measure of risk based on participant’s mean scores in two subscales (usually the CS and BO scales), (3) a proportional analysis where the proportion of participants reporting values above (or below) established cut-off scores are reported, or (4) a combination of the above. For all studies, we applied standard content analysis of study results and discussion to create a narrative summary. In studies with detailed measure of risk, mean subscale scores (and accompanying standard deviations) were pooled using random effects meta-analysis in STATA 14. Meta-analyses were stratified by the version of the ProQOL to ensure appropriate pooling. Heterogeneity was quantified using the I² statistic and accompanying Q p-value. Pooled means are reported with 95% confidence intervals (CIs). In cases where studies reported estimates from multiple groups (e.g. nurses, physicians, social workers), results were pooled as long as the groupings were mutually exclusive. A summary evidence table was created presenting the study results (title, author, year, country, sample population, measurement tools used, overall findings, quantitative prevalence, or risk measured by ProQOL).

Results

Study characteristics

Table 1 presents a summary of the study characteristics and major quantitative and overall findings, including narrative summary. Of the 71 articles, 50 (70.4%) were exclusive to one professional care provider group, whereas the remaining 21 (29.6%) included 2 or more care providers. Of the 50 studies restricted to one profession, nursing professionals were most commonly represented (n = 30), followed by physicians or medical trainees (n = 7), social workers (n = 3), genetic counselors (n = 3), and a mix of other care providers (n = 7). Nursing professionals included were as follows: (1) broadly representative of care environments such as acute care hospitals—including emergency departments, critical care units, and acute care wards—and varied settings outside of hospital including clinics and outpatient treatment settings; and (2) broadly representative of clinic conditions and patient groups cared including examples such as palliative care, pediatrics, geriatrics, oncology and as transplant coordinators, and oncology. Of the 21 studies that included multiple providers, these studies were not as expansive in care environments or patients served but did include mental health providers/therapists, hospice care providers, and care in hospitals or acute care.

Table 1.

Summary of studies.

Author (reference)	Year	Country	Samplen	Measurement instruments	Overall findings	Quantitative findings
Abendroth and Flannery⁷	2006	United States	Hospice care RNs n=216	ProQOL-III	Overall sample at risk for compassion fatigue; 91% scoring moderate high risk for BO also scored moderate high risk for compassion fatigue. No correlation with personal demographics, some correlation with work-related variables. 35% of those diagnosed with depression or PTSD scored high risk.	26.4% high risk, 52.3% moderate risk, and 21.3% low risk Mean STS: 13.6
Adams et al.⁸	2006	United States	Social workers n=274	Compassion Fatigue Scale General Health Questionnaire	Supported notion that job burnout and secondary trauma were separate contributors to psychological distress.	No scores provided
Benoit et al.⁹	2007	United States	Genetic counselors n=12	Focus Group questions	All participants described experience indicating compassion fatigue. Themes included being overwhelmed due to caring, feeling responsible, and not being able to control patient suffering. Difficulty differentiating experience of compassion fatigue from BO. Delivering bad news prevalent trigger of compassion fatigue. Traumatic memories also a trigger. Emotional responses from work interfered with ability to cope in personal life.	None reported
Alkema et al.¹⁰	2008	United States	Hospice healthcare practitioners n=37	ProQOL Self Care Assessment Worksheet	Burnout and compassion fatigue negatively correlated to all aspects of self-care except physical care. CS significantly positively correlated to emotional care, spiritual care, and work life balance. As compassion fatigue increased, reported self-care decreased.	Mean CS: 40.5 (high), BO: 23.8 (average), and compassion fatigue: 17.5 (high) SCAW showed higher scores for self-care activities.
Yoder¹¹	2008	United States	RNs from special care units n=106	ProQOL-IV Narrative response	BO and compassion fatigue scales strongly correlated. 15.8% of the sample fell into area of risk for compassion fatigue. CS found to be higher in those working longer shifts in ICU and with less experience.	Mean overall scores: CS = 40.3, BO = 19.2, and compassion fatigue = 12.3
Craig and Sprang¹²	2009	United States	Trauma treatment therapists n=532	ProQOL-III Trauma Practices Questionnaire	Sample reported significantly lower compassion fatigue than in other studies of mental health professionals. Younger, less experienced reported higher burnout; more experience had higher CS.	32% above cut off for CS 6% above cut off for compassion fatigue 12% above cut off for BO Mean CS: 43.8 Mean BO: 7.4
Meadors et al.¹³	2009	United States	Pediatric healthcare providers n=167	ProQOL (version not specified) Secondary Traumatic Stress Scale Impact of Events Scale-Revised	No statistically significant relationships between professional groups and subscales. Higher compassion fatigue scores for those who had experienced a loss within the last 30 days.	1.2% of the participants showed high BO scores, 76% scored low. 7.3% scored high on compassion fatigue, 43% scored low. Mean CS: 38.2 Mean BO: 14.8 Mean STS: 9.1
Hooper et al.¹⁴	2010	United States	Emergency department RNs n=114	ProQOL-IV	ED nurses found to have lower levels of CS compared to other services. 82% had moderate–high levels of BO, 86% had moderate–high levels of compassion fatigue.	Risk percentages: 20.2% low risk for CS, 26.6% high risk for BO, 28.4% high risk for compassion fatigue.
Potter et al.¹⁵	2010	United States	Oncology RNs n=153	ProQOL-IV	Risk of compassion fatigue relatively equal between work settings (inpatient/outpatient units). Higher level of BO for those on outpatient units. Staff with 11–20 years experience showed highest risk scores on all sub scales.	Mean overall scores: CS = 38.3, BO = 21.5, and compassion fatigue = 15.2
Circenis and Millere¹⁶	2011	Latvia	Acute care hospital RNs n=129	ProQOL-V Workplace questionnaire Maslach Burnout Inventory	53% of the sample had higher than the mean score for CS, 54% had higher than the mean score for BO, and 50% had higher than the mean score for STS.	Mean scores: CS = 37.42, BO = 23.5, and STS = 19.59
Slocum-Gori et al.¹⁷	2011	Canada	Palliative care providers n=630	ProQOL (version not specified)	Practitioners providing care for psychological, emotional, and physical distress had significantly higher levels of compassion fatigue and BO. Nurses reported highest level of compassion fatigue. Those who worked part time had higher CS.	Mean scores: CS = 43.9, compassion fatigue = 18.6, and BO = 20.8
Young et al.¹⁸	2011	United States	Cardiovascular RNs n=70	ProQOL-V	Statistically significant differences between nursing units for CS and BO subscales.	Mean scores HVICU: CS = 36.6, BO = 24.82, and STS = 21.88 HVIMC: CS = 41.84, BO = 19.48, and STS = 19.44
Bhutani et al.¹⁹	2012	India	Non-physician clinicians n=60	ProQOL-V Questionnaire including personal, professional, anthropometric, and metabolic profiles	CS highest for those with most years of practice or in private practice. Those reported “poor working conditions” had higher BO. No significant correlation between sub scales and demographic variables.	Mean scores: CS = 40.63, BO = 22.8, and STS = 23.52
Rossi et al.³	2012	Italy	Mental health providers n=260	ProQOL-III General Health Questionnaire (GHQ-12)	Those with reported psychological distress had significantly lower CS. Distress and prior trauma showed higher BO and compassion fatigue.	Mean scores: CS = 32, BO = 21.15, and compassion fatigue = 10.2
Severn et al.²⁰	2012	New Zealand	Audiologists n=82	ProQOL-III Audiology Occupational Stress Questionnaire (AOSQ)	Highest level of CS in private practice. Lower CS and higher BO with increased age. Stress associated with patient contact strongest predictor of compassion fatigue.	25% high level CS, 22% low 20% high level risk of BO, 26% low 22% high risk of compassion fatigue, 29% low
El-Bar et al.²¹	2013	Israel	Physicians n=128	CFST	Compassion fatigue most prevalent. Sharp divide in risk for compassion fatigue, either extremely high or extremely low. Immigration can involve a great deal of personal trauma, which increases risk for compassion fatigue. Levels found here significantly higher than other studies. Being born abroad/having no academic affiliation increased compassion fatigue risk. No impact with other variables.	35.2% at extremely high risk for compassion fatigue, 9.4% high risk for BO, and 21.1% at risk for low CS.
Kim²²	2013	United States	Liver and kidney nurse transplant coordinators n=14	ProQOL-V	No significant correlation between demographic variables and subscale scores. Majority of sample had average levels of CS, BO, and STS.	Mean scores: CS = 40, BO = 24, and STS = 23
Michalec et al.²³	2013	United States	Nursing students n=436	ProQOL-V Maslach Burnout Inventory (MBI) Semi-structured interview	Significantly lower levels of BO in first year students than second year, but no significant increase in third and fourth year.	Overall sample categorization: CS levels = high, BO levels = average, and STS levels = low
Mizuno et al.²⁴	2013	Japan	Nurses Midwives n=255	ProQOL Frankfurt Emotional Work Scale	ProQOL scores significantly associated with stress factors and emotion work. Particularly making value judgments, and having to control emotions. No relationship seen between scores and work experience. Negative feelings about accepting certain aspects of the work significantly associated with compassion fatigue. No significant differences in ProQOL scores between nurses/midwives. No high risk for compassion fatigue.	Mean CS: 33.5 Mean BO: 26.9 Mean compassion fatigue: 21.3
Sodeke-Gregson et al.²⁵	2013	United Kingdom	Trauma therapists n=253	ProQOL-V Coping Strategies Inventory	Majority in average range for CS and BO, and high range for STS. CS negatively correlated with BO, BO positively correlated with STS. Age, managerial support positive predictors of CS. Perceived management support and older age significant negative predictors of BO. More self-care, past trauma for self-positive predictors for STS.	CS: 8% low, 53.2% average BO: 64.2% average, 25.8% high STS: 70% high, 30% average
Whitebird et al.²⁶	2013	United States	Hospice care providers of various designations n=547	ProQOL-III Short Form-12 Health Survey Version 2 (SF-12) Generalized Anxiety Disorder Scale (GAD-7) Patient Health Questionnaire (PHQ-8) Medical Outcomes Social Support Survey (MOS6) Job Satisfaction question Coping Strategies	Higher levels of BO than compassion fatigue, both less than average for norms associated with ProQOL. Both were moderately correlated with anxiety and depression.	Mean scores: Compassion fatigue = 9.9, BO = 13.9.
Zeidner et al.²⁷	2013	United States	Health professionals of various designations and specialties n=182	ProQOL-III Schutte Self Report Inventory Emotion-management subscale of the Mayer-Salovey-Caruso emotional intelligence test Coping inventory for stressful situations-situation specific coping Mood subscales of the Dundee stress state questionnaire	Women reported higher levels of compassion fatigue. No significant difference between professional groups.	No overall scores provided. Scores by practice/gender.
Ariapooran²⁸	2014	Iran	RNs n=164	ProQOL Multidimensional Scale of Perceived Social Support	Inverse correlation between social support and BO; no meaningful correlation between social support and compassion fatigue. May indicate that nurses working with victims or survivors could be at risk for developing compassion fatigue or BO. Social support, a key variable in determining risk for compassion fatigue and BO.	45.7% at risk for compassion fatigue 54.3% of ER and 35.4% on non-ER nurses suffered from compassion fatigue; 15.03% at risk for BO 19.2% of ER and 11.4% of non-ER at risk for BO
Bellolio et al.²⁹	2014	United States	Resident physicians n=188	ProQOL-V	No statistically significant impact of any demographic variable in any of the subscales. BO scores higher when more hours and night shifts worked. Found average levels of CS, low levels of BO and STS in sample; no difference in comparison to other specialties. Higher risk of developing compassion fatigue with night shifts.	CS: 59% average level, 41% high level BO: 57% low, 43% average STS: 77% low, 23% average Mean CS: 40.4 Mean BO: 21.8 Mean STS: 19.8
Hegney et al.³⁰	2014	Australia	RNs n=132	ProQOL-V DASS	Approximately 20% in sample showed potential risk and higher compassion fatigue. 12% high risk, 7.6% very distressed. STS and BO related and associated with negative mood. No significant correlation with variables. Lower levels of CS in nurses with less experience.	Mean CS: 35.66 Mean BO: 23.66 Mean STS: 18.6 Positively correlated with age and years in nursing.
Hinderer et al.³¹	2014	United States	RNs n=128	ProQOL-V Penn Inventory	35.9% nurses scored for high BO, 27.3% for compassion fatigue, and more than 75% high for CS. Compassion fatigue less prevalent than BO. BO related to longer shifts, work relationships. Compassion fatigue triggered by challenging patients, futile care, environment, and personal experience. High prevalence of CS, particularly in older nurses.	Mean BO: 20.56 (suggested higher risk of BO) Mean compassion fatigue: 13.94 (reported by 27.3% of the sample) Mean CS: 37.96 (majority above average CS)
Martin et al.³²	2014	United States	Abortion providers (range of clinicians) n=79	ProQOL Ways of Coping Questionnaire Workgroup Characteristics Measure People and Organizational Culture Profile APSS	Significantly higher CS and lower BO than other healthcare providers. Compassion fatigue consistent with other studies.	CS: 49% high, 30% average, and 21% low BO: 4% high, 21% average, and 75% low compassion fatigue: 46% average, 43% low
Mason et al.³³	2014	United States	RNs n=26	ProQOL-V Utrecht Work Engagement Scale Moral Distress Scale	As work engagement increases, so does CS. No other relationships between scores and variables.	CS: 73.1% average, 26.9% high BO: 42.3% low, 57.7% average STS: 61.5% low, 38.5 average
Smart et al.³⁴	2014	United States	RNs Physicians Nursing assistants n=139	ProQOL-V	Mean scores did not differ among departments. General medical workers showed evidence of higher burnout. Significant increase in level of BO for caregivers of non-critical patients (compared to those in ED or ICU). Findings contrary to other studies. Night shifts associated with higher BO, less CS.	Mean CS: 39.1 Mean BO: 23.4 Mean STS: 19.0
Amin et al.³⁵	2015	India	NICU RNs n=129	ProQOL-V Perceived Stress Scale 14	Perceiving high stress experienced prolonged distress, might be higher risk of BO, STS, or low CS. Weak to moderate positive correlation between perceived stress and BO/STS. Almost 25% positive for BO and STS. Similar to reports in western literature.	Perceived stress: most nurses perceived moderate stress (47.3%), mild stress in 29.5%, and high stress in 23.2%. High CS found in 19.4%, high BO in 23.3%, and high STS in 23.3%.
Berger et al.³⁶	2015	United States	Pediatric RNs n=239	ProQOL-V Two open ended questions	STS due to frequent traumatic patient situations. End of life situations particularly difficult. Continually caring for critical patients’ frequent trigger of compassion fatigue and BO. Respondents reported decrease in care and issues in personal life. Younger nurses had lower CS, higher BO and STS. Lower CS with 6–10 years experience, higher after 20 years experience. Lower CS, higher BO on medical/surgical units.	71.5% moderate to high CS. Over a quarter had low CS, high BO, and high STS. Mean CS: 49.1 Mean BO: 50.2 Mean STS: 50.1
Branch and Klinkenberg³⁷	2015	United States	Pediatric RNs, social workers, RTs, PTs, OTs, psychologists, child life therapists, PCAs n=296	ProQOL-V	Staff on units with long periods of stability and support showed higher CS, lower BO. Oncology units avoid compassion fatigue through meaningful interactions with patients. Significant score differences by clinical unit.	25% high risk for CS, 30.9% high risk for BO, and 26.9% high risk for STS. Mean CS: 50.3 Mean BO: 49.7 Mean STS: 50
Dasan et al.³⁸	2015	United Kingdom	Emergency medicine consultants in United Kingdom ED n=681	ProQOL Potential impacts of compassion fatigue questionnaire Qualitative interview	Levels of compassion fatigue found to be low. Those with compassion fatigue more likely to report irritability and reduced standards of care, as well as intent to retire earlier. Mean CS reduced marginally over first 10 years, increased after 20 years. Job demand, control, and support impacted levels of satisfaction or fatigue in interviews.	98% of the consultants were average or high for CS, only 2.3% low. Of the 2.3%, only two consultants had high BO, and one of those also high STS. Mean CS: 50.9 Mean BO: 50.8 Mean STS: 50.5
Hunsaker et al.³⁹	2015	United States	Nurses n=284	ProQOL-V	Overall low to average level of compassion fatigue and BO among ED nurses. Compassion fatigue less prevalent with increasing age/experience. Less compassion fatigue and BO with increased managerial support. Older nurses had higher levels of CS, younger nurses had higher levels of BO. More years nurse had practiced, higher the level of CS, lower the level of BO. Lower BO with shorter shifts.	Mean CS: 39.77 compassion fatigue: 21.57 BO: 23.66 56.8% average CS; 65.9% low compassion fatigue; 54.1% average BO.
Kelly et al.⁴⁰	2015	United States	RNs n=491	ProQOL-V	Nurses would be in normal range for BO and CS, low range for STS. Some findings related to demographics: “millennial” generation more likely to be experiencing higher BO/STS and lower CS than “Baby boomer” nurses. As nurses gained experience, increased compassion fatigue and lowered CS.	Overall mean ProQOL scores: BO = 25.63, STS = 20.86, CS = 40.51
Kim et al.⁴¹	2015	Korea	RNs n=488	ProQOL-V Ethical Dilemmas Questionnaire Professional Nursing Values Questionnaire	Significant differences in CS and BO by age, marital status, religion, educational status, position, and number of years in practice. Low CS and high BO associated with nurses with less than 3 years experience. Level of CS higher than levels of BO and STS. CS increases as age increases.	Mean CS: 32.8 Mean BO: 29.0 Mean STS: 27.3
Lee et al.⁴²	2015	United States	Genetic counselors n=467	ProQOL-V STAI	High CS found in counselors at high risk for compassion fatigue; both can exist together. Burnout a significant predictor of compassion fatigue.	Mean CS: 41.15 (4% low range) Mean BO: 21.11 (19% high, 68% average) Mean STS: 19.37 (61% high, 39% average)
Mangoulia et al.⁴³	2015	Greece	RNs n=174	ProQOL-V	Overall showed low CS, high risk for BO and compassion fatigue. No relationship shown between previous trauma and STS. Knowledge powerful protective factor.	Mean CS: 28.36 (low) Mean BO: 25.17 (average) Mean compassion fatigue: 16.45 (borderline high)
Meyer et al.⁴⁴	2015	United States	RNs starting pediatric residency program n=231	ProQOL Mueller McCloskey Satisfaction Scale Life Events Checklist		Compassion fatigue: 23.56 ± 13.29 CS: 93.56 ± 16.77 BO: 24.01 ± 11.67
Osland⁴⁵	2015	Australia	Dieticians n=87	ProQOL-V	Significantly higher STS in those working with pediatrics. Overall showed average CS, average BO, and low STS; overall positive professional quality of life. Higher STS in high risk areas (ICU, mental health). More years of practice showed higher STS/BO.	CS: 78% average, 20% high BO: 37% low, 63% average STS: 66% low, 34% average
Sacco et al.⁴⁶	2015	United States	RNs n=221	ProQOL-V	Overall, nurses scored in average range for all three sub scales. Suggested that age has impact on ProQOL, nurses over 50 had higher CS, lower BO and STS. Younger less experienced nurses, higher risk for compassion fatigue. Significant difference in compassion fatigue by age, unit acuity, and management/practice change.	CS = 51.7 STS = 48.7 BO = 48.2
Harker et al.⁴⁷	2016	Australia	Psychology, social work, counseling n=133	General Well Being Scale (GWBS) ProQOL-V Resilience Factor Inventory (RFI) Freiburg Mindfulness Inventory (FMI)	Higher level resilience significant predictor of lower distress (BO and STS); age predictor of resilience and mindfulness, not BO or STS. No other variable found to be predictors.	Mean scores: BO = 49.4, STS = 49.3
Kolthoff and Hickman⁴⁸	2016	United States	Geriatric RN n=42	ProQOL-V	Average levels of compassion fatigue and BO. Higher BO and compassion fatigue in newer nurses.	Mean scores: BO = 26.7, STS = 23, CS = 37.4
Weintraub et al.⁴⁹	2016	United States	Neonatology physicians n=443	Compassion Fatigue and Satisfaction Self-Test (modified)	The prevalence of compassion fatigue, BO, and CS 15.7%, 20.8%, and 21.9%, respectively.	Mean scores: BO = 19.4, STS = 17, CS = 37.5
Wu et al.⁵⁰	2016	Canada/United States	Oncology nurses n=549	ProQOL-V Abendroth Demographic Questionnaire	No statistical differences in CS, BO, and STS between United States and Canada. Younger nurses experienced more STS. Cohesive team environment buffered negative feelings.	Mean scores Canada: BO = 22.5, STS = 22.4, CS = 42.6 Mean scores United States: BO = 22.7, STS = 22.7, CS = 42.4
Beaumont et al.⁵¹	2016	United Kingdom	Midwife students n=103	ProQOL Self-Compassion Scale Short Warwick and Edinburgh Mental Well-being Scale Compassion for Others Scale	Above average BO in just over 50% of the sample. Participants with less self-compassion reported higher compassion fatigue and BO.	Mean scores: BO = 22.9, STS = 21.8, CS = 41.6
Duarte and Pinto-Gouveia⁵²	2016	Portugal	Oncology nurses n=48	ProQOL	Decrease in compassion fatigue and BO with mindfulness intervention.	Mean scores, intervention: BO = 26.6, STS = 25.7, CS = 40
Montross-Thomas et al.⁵³	2016	United States	Hospice staff and volunteers n=390	ProQOL Questionnaire re: personal rituals and practices	Personal rituals, personal and professional support, and age correlated with higher CS and lower BO.	No overall mean scores available.
Yu et al.⁵⁴	2016	China	Oncology nurses n=650	ProQOL Jefferson Scales of Empathy Simplified Coping Styles Questionnaire Perceived Social Support Scale Chinese Big Five Personality Inventory	More years experience, passive coping, and working in secondary hospitals associated with higher compassion fatigue and BO. “Perspective taking” strong predictor of CS.	Mean scores: BO = 21.1, STS = 21.4, CS = 31.8
Muliira and Ssendikadiwa⁵⁵	2016	Uganda	Midwives n=224	ProQOL	Overall average levels of CS, STS, and BO. CS related to psychological well-being and job satisfaction.	Mean scores: BO = 36.9, STS = 22.9, CS = 19
Pruginin et al.⁵⁶	2016	Israel	Social workers n=125	ProQOL	Average levels of CS, STS, and BO. No difference between study groups.	Mean scores, urban: BO = 22.8, STS = 22.4, CS = 38.6 Mean scores, regional: BO = 23.1, STS = 22.8, CS = 38.7
Cragun et al.⁵⁷	2016	United States	Military emergency department personnel n=105	ProQOL-V	Comparison between those who had been deployed and those who had not. No statistically significant differences between groups in any of the sub scales.	Mean scores, deployed: BO = 22.3, STS = 20.7, CS = 37.2 Mean scores, never deployed: BO = 21.8, STS = 18.9, CS = 39
Craigie et al.⁵⁸	2016	Australia	Hospital nursing staff n=273	ProQOL Depression Anxiety Stress Scale State-Trait Anxiety Inventory	Trait-negative affect important factor in compassion fatigue and STS. CS protective factor to BO, not to STS.	Mean scores: BO = 23.5, STS = 19.6, CS = 37.6
Allsbrook et al.⁵⁹	2016	United States	Genetic counselors n=320	ProQOL State-Trait Anxiety Inventory Supervision questionnaire	Overall, supervision not associated with increase compassion fatigue. Less experienced supervisors reported more STS, more likely to be at risk.	Overall mean scores: BO = 53, STS = 59.6, CS = 54.1
Tucker et al.⁶⁰	2017	Canada	Medical students n=59	ProQOL-V Self-Reflection exercises	Decrease in compassion fatigue and increase in burnout during medical student’s training; workshop on compassion fatigue at start of program had limited impact.	Mean scores: BO = 22.1, STS = 20.4, CS = 40
Wu et al.⁶¹	2017	United States	Surgeons n=178	ProQOL-V	CS significantly lower in trauma surgeon sub-group; female surgeons across specialties reported higher compassion fatigue and BO.	Overall mean scores: BO = 25.3, STS = 22.6, CS = 39.2
Mooney et al.⁶²	2017	United States	Nurses n=86	ProQOL-V Demographic survey	CS lower and BO higher in ICU nurses compared to oncology. CS higher and BO lower in male nurses.	Overall mean scores: BO = 25, STS = 20.5, CS = 38.7
Davidson et al.⁶³	2017	United States	Multidisciplinary hospital staff n=164	ProQOL	48% of the participants reported a stressful event at work.	Overall mean scores: BO = 21.7, STS = 21.8, CS = 40.8
Galiana et al.⁶⁴	2017	Spain/Brazil	Palliative care professional s n=546	ProQOL	Study to report scores as well as validate the instrument in Spanish. Study found ProQOL to be valid.	Mean scores Spain: BO = 15.6, STS = 12.4, CS = 41.1 Mean scores Brazil: BO = 15.1, STS = 14.2, CS = 41.6
Zajac et al.⁶⁵	2017	United States	Oncology care providers n=107	ProQOL Press Ganey survey	Average levels of CS and STS, low BO in sample.	Mean scores: BO = 22.5, STS = 24.2, CS = 40.8
Kelly and Lefton⁶⁶	2017	United States	ICU nurses n=1136	ProQOL	Sample reported average CS and STS, low BO. Significantly higher CS, lower BO in nurses who had received meaningful recognition.	Mean scores: BO = 23.5, STS = 22, CS = 38.8
Cohen et al.⁶⁷	2017	Israel	Midwives n=93	ProQOL PSS-SR	Relatively high levels CS reported, seniority positively correlated with BO.	Mean scores: BO = 13.2, STS = 12.6, CS = 43.1
Cetrano et al.⁶⁸	2017	Italy	Mental health professionals n=416	ProQOL Quality of Working Life Questionnaire	Ergonomic problems and work impacting personal life associated with higher compassion fatigue and BO.	Mean scores: BO = 22.9, STS = 14.4, CS = 32.7
Kim et al.⁶⁹	2017	South Korea	Nurses n=875	ProQOL Type D Personality Scale-14	Type D personality significantly associated with all three sub scales.	Mean scores: BO = 28.7, STS = 25.6, CS = 32.1
Allen et al.⁷⁰	2017	Australia	Obstetricians/Gynecologists n=23	ProQOL	Intervention-based study. Scores in BO and STS decreased with intervention, CS increased.	No mean scores available
Austin et al.⁷¹	2017	United States	Physicians/nurses n=330	Moral Distress Scale-revised ProQOL	Participants scoring as most at risk for STS and BO also scored highest for moral distress.	Mean scores physicians: BO = 19.4, STS = 20, CS = 40.7 Mean scores nurses: BO = 20.6, STS = 20.2, CS = 39.7
Trowbridge et al.⁷²	2017	United States	Pediatric hospital social workers n=33	ProQOL Mindful Attention and Awareness Scale Caring Efficacy Scale	Intervention-based study. Mindfulness intervention related to decrease in STS scores.	Mean scores: BO = 24.2, STS = 21.5, CS = 38.7
Klein et al.⁷³	2017	United States	Palliative care professionals n=12	ProQOL	Intervention-based study. Education-based program resulted in increase in CS, slight decrease in BO, and no change in STS.	Mean scores: BO = 27.3, STS = 26.1, CS = 35.2
Pfaff et al.⁷⁴	2017	Canada	Palliative care professionals n=12	ProQOL	Evaluation of pilot program intervention for compassion fatigue. Reduced clinical stress seen at program completion.	Mean scores: BO = 22.1, STS = 24.8, CS = 42.2
Hamid and Musa⁷⁵	2017	UAE	Psychologists and social workers n=502	ProQOL General Health Questionnaire Maslach Burnout Inventory (HSS) Endler and Parker’s Coping Inventory	Coping seen as factor in mediating relationship between BO and STS. BO positively related to STS. CS negatively associated with STS.	No overall mean scores available
Duarte and Pinto-Gouveia⁷⁶	2017	Portugal	Oncology nurses n=221	ProQOL	Psychological factors accounted for 26% of CS, 29% of BO, and 18% of compassion fatigue.	Overall mean scores: BO = 25.3, STS = 25.8, CS = 38

CS: Compassion Satisfaction; BO: Burnout; STS: Secondary Traumatic Stress; RN: registered nurse; PTSD: posttraumatic stress disorder; SCAW: self care assessment worksheet; ICU: intensive care unit; ED: emergency department; ER: emergency room; NICU: neonatal intensive care unit; CFST: Compassion Satisfaction and Fatigue Test; HVIMC: Heart and Vascular Intermediate Care Unit; HVICU: Heart and Vascular Intensive Care Unit; APSS: Accumulated Pain/Stressor Scale; DASS: Depression Anxiety Stress Scale; PCAs: Patient Care Associates; STAI: State-Trait Anxiety Inventory; PSS-SR: PTSD Symptom Scale-Self Report; MBI-HSS: Maslach Burnout Inventory: Human Services Survey.

The studies had a significant focus on economically developed western healthcare systems with most (41/71, 57.8%) being from North America and 37 of these exclusively the United States, Europe being the next most frequent (10/71, 14.1%)—with 1 study comparing Brazil and Portugal, and 6 (8.5%) from Australia–New Zealand. Only 4 of 71 studies (5.6%) were from Asian rim countries, and 2 of 71 (2.8%) from the Indian sub-continent despite the large populations served by healthcare providers in these regions. There was only one study from the African continent, and no study exclusively from South America (apart from the aforementioned one study examining Portugal and Brazil).

Of the 71 articles, 67 (94.4%) used the ProQOL scale: 6 (9.0%) used version 3, 3 (4.5%) used version 4, and 28 (41.8%) used version 5. Thirty of the 67 (44.8%) studies did not explicitly identify which ProQOL version was used. All studies included some form of demographic questionnaire, and 56% (40/71) of studies used one or more additional tools to further assess domains of psychological distress. Fifty six (78.9%) of studies were published in the last 5 years, with 30 (42.3%) published since 2016, suggesting a recent increased interest in this subject. The reporting of the results from the 71 studies varied. Of the 67 studies that reported results from ProQOL, 41 studies reporting detailed measures of risk only from the 3 subscales (61.2%), 12 (17.9%) studies reported only a proportional or percentage risk, 2 (3.0%) reported limited results on only two of the three subscales, and the remaining 10 (14.9%) reported a combination of mean results from the 3 subscales and proportional values above cutoffs.

The correlations between demographic and work variables and reported values on the ProQOL were inconsistent between study results. A number of studies demonstrated that psychological distress and underlying mental health conditions were associated with worse scores, but as cross-sectional surveys, it was not possible to determine if one or the other was causal, or simply part of the same experience. CS was variably reported with some studies suggesting it increased with experience^15,20,39,41 or age,^46,47 and other studies suggesting it was inversely associated.^12,19,30,38 BO and compassion fatigue were correlated^{8
–10,25,30}; higher scores in BO scales in particular were more commonly associated with the work environment such as location, shift type, or level of oversight responsibility.^19,29,31,34 Factors associated with lower scores, or improved CS, included positive work environments (including social support networks),^{25,28,50,53,66} work in private clinics,²⁰ and support from management/leadership.^35,37,39 Recent negative events were more likely overall to be associated with worse scores.^31,36,63

Table 2 presents a summary of those studies that used the ProQOL tool as the primary measure of compassion fatigue, and reported mean scores for all three sub scales (CS, BO, and STS/compassion fatigue). The summary shows the scores between practitioner groups (nurses vs other health practitioners) to be relatively consistent albeit, the scores for BO appeared to less variable across nurses. The results were particularly interesting in that the scores for BO and STS/compassion fatigue were in the average to high range, whereas the CS scores were not particularly “low”; this may raise the question as to the impact of different domains on the overall effect on compassion fatigue.

Table 2.

Summary of studies using ProQOL tool, reporting all three sub scales.

Study	Author (reference)	Year	Sample	CS	BO	STS
10	Alkema et al.	2008	Other	40.5	23.8	17.5
11	Yoder	2010	Nurses	40.3	19.2	12.3
15	Potter et al.	2010	Nurses	38.3	21.5	15.2
17	Slocum-Gori et al.	2011	Other	43.9	20.8	18.6
19	Bhutani et al.	2012	Other	40.63	22.8	23.52
16	Circenis and Millere	2011	Nurses	37.42	23.5	19.59
3	Rossi et al.	2012	Other	32	21.15	10.2
18	Young et al.	2011	Nurses	36.6	24.82	21.88
22	Kim	2013	Nurses	40	24	23
24	Mizuno et al.	2013	Nurses	33.5	26.9	21.3
30	Hegney et al.	2014	Nurses	35.66	23.66	18.66
31	Hinderer et al.	2014	Nurses	37.96	20.56	13.94
34	Smart et al.	2014	Other	39.1	23.4	19
39	Hunsaker et al.	2015	Nurses	39.77	23.66	21.57
40	Kelly et al.	2015	Nurses	40.51	25.63	20.86
41	Kim et al.	2015	Nurses	32.8	29	27.3
42	Lee et al.	2015	Other	41.15	21.11	19.37
43	Mangoulia et al.	2015	Nurses	28.36	25.17	16.45
48	Kolthoff and Hickman	2016	Nurses	37.4	26.7	23
49	Weintraub et al.	2016	Other	37.5	18.4	17
50	Wu et al.	2016	Nurses	42.6	22.5	22.4
51	Beaumont et al.	2016	Other	41.6	22.9	21.8
52	Duarte and Pinto-Gouveia	2016	Nurses	40	26.6	25.7
54	Yu et al.	2016	Nurses	31.8	21.1	21.4
55	Muliira and Ssendikadiwa	2016	Other	19	36.9	22.9
56	Pruginin et al.	2016	Other	38.6	22.8	22.4
57	Cragun et al.	2016	Other	37.2	22.3	20.7
58	Craigie et al.	2016	Nurses	37.6	23.5	19.6
59	Allsbrook et al.	2016	Other	54.1	53	59.6
60	Tucker et al.	2017	Other	40	22.1	20.4
61	Wu et al.	2017	Other	39.2	25.3	22.6
62	Mooney et al.	2017	Nurses	38.7	25	20.5
63	Davidson et al.	2017	Other	40.8	21.7	21.8
64	Galiana et al.	2017	Other	41.1	15.6	12.4
65	Zajac et al.	2017	Other	40.8	22.5	24.2
66	Kelly and Lefton	2017	Nurses	38.8	23.5	22
67	Cohen et al.	2017	Other	43.1	13.2	12.6
68	Cetrano et al.	2017	Other	32.7	22.9	14.4
69	Kim et al.	2017	Nurses	32.1	28.7	25.6
71	Austin et al.	2017	Nurses and other	39.7	20.6	20.2
72	Trowbridge et al.	2017	Other	38.7	24.2	21.5
73	Klein et al.	2017	Other	35.2	27.3	26.1
74	Pfaff et al.	2017	Other	42.2	22.1	24.8
76	Duarte et al.	2017	Nurses	38	25.3	25.8

CS: Compassion Satisfaction; BO: Burnout; STS: Secondary Traumatic Stress.

Meta-analysis

In studies that used version 5 of the ProQOL (n = 28), the pooled mean CS score was 41.8 (95% CI: 40.1–43.5) (Figure 2), mean BO score was 28.4 (95% CI: 26.3–30.4) (Figure 3), and mean STS score was 25.8 (95% CI: 23.3–28.3) (Figure 4). This indicates average levels of BO and STS and average high levels of CS. Heterogeneity was above 99.5% (p < 0.00001) on all version 5 subscale analyses. For the CS subscale, there was an outlier value of 93.60; this study was conducted in a sample of 231 novice, pediatric RNs.

Figure 2.

ProQOL-V pooled mean scores by subscale: Compassion Satisfaction.

Figure 3.

ProQOL-V pooled mean scores by subscale: Burnout.

Figure 4.

ProQOL-V pooled mean scores by subscale: Secondary Traumatic Stress.

In studies that used version 3 of the ProQOL (n = 6), the pooled mean BO score was 18.2 (95% CI: 13.6–22.9) (Supplemental Figure 1), mean CS was 43.3 (95% CI: 36.2–50.4) (Supplemental Figure 2), and mean STS was 16.6 (95% CI: 14.4–18.8) (Supplemental Figure 3). These scores indicate average high levels of BO, average levels of CS, and low levels of STS. There was significant heterogeneity in all analyses (I² > 89%, p < 0.00001).

Discussion

The results of our systematic review and meta-analysis demonstrate that across diverse healthcare practitioner groups, most studies report results BO and compassion fatigue subscale results that fall into the average risk groups within the ProQOL scoring matrix. The “BO” subscale had the highest mean value (and therefore potentially most significant impact on compassion fatigue) across studies. This was also the subscale that had the highest number of studies with heterogeneous results with 10 studies significantly above the pooled mean. The synthesis of existing work as presented here demonstrates an association between personal factors such as an existing diagnosis of anxiety or depression,^7,8 and prior negative life events³ and increased levels of compassion fatigue. Although the subscale scores for BO and compassion fatigue were correlated, it was not as clear how factors related to the work environment such as shift time and length,^9,11,19,20 and the type of caring work being done,¹⁷ explicitly impacted compassion fatigue levels. The pooled results of this meta-analysis are important for future research as reasonable summary estimates for comparison. The high proportion of studies that were either exclusively in nursing professionals, or included nurses in a diverse group of healthcare professionals reflects the important role of nurses in our healthcare system, and their proportionally large cohort of healthcare providers. The similarity in results across healthcare providers suggests that comparisons within and between health professionals are possible and for non-nursing healthcare professionals, comparisons are still possible and relevant.

The finding that compassion fatigue exists across diverse practitioner groups can have a serious impact on professional practice and workforce. Compassion fatigue, BO, post-traumatic stress disorder, and other types of psychological/emotional distress are often associated and sometimes conflated. It is important to differentiate these conceptually, as well as to recognize overlap as approaches to mitigating and treating the issues differ. Compassion fatigue is triggered by the continual use of empathy and emotional energy, previous exposure to trauma, prolonged exposure to secondary trauma (a consequence of being witness to the trauma of others, and being in a position of having to care for those who are suffering, rather than being the primary subject of the trauma themselves), and the work environment.¹⁶ BO is defined as a “psychological syndrome that involves a prolonged response to stressors in the workplace.” Specifically, BO involves the chronic strain that results from an incongruence, or misfit, between the worker and the job.⁷ BO is primarily triggered by work-related and organizational characteristics, with some predisposing personal characteristics.¹⁶ Considering that BO develops in large part as a result of stressors that are organizational and structural (i.e. related to working environment), changes in the work environment may potentially mitigate negative impacts to patients, and be relatively easier to implement. However, BO may also be related to personal characteristics or a disrupted care provider that is more difficult to address such as inter-personal conflicts in or outside the work place, or personal financial stresses.

Although BO and other distress may affect providers, compassion fatigue may more severely affects patients as it is the direct effect of a healthcare provider’s diminished capacity to care that results from repeated exposure to the suffering of their patients, as well as from the knowledge of their patient’s traumatic experiences.¹ Nimmo and Huggard,¹ in a review of compassion fatigue in physicians, report that issues are “often reflected in outcomes of emotional distress, pain, and suffering, and may manifest in increased rates of absenteeism, reduced service quality, low levels of efficiency, and high attrition rates and eventually, workforce dropout.” This evidence of compassion fatigue and the effect on providers and patient care raises an important question on what strategies and programs health systems should consider to prevent or mitigate its effect. As mentioned in a number of the studies included in this review, there are programs in existence, which include general wellness programs that encourage self-care, and increased social and managerial support. Education to practitioners, from students to the most experienced, about the existence and impact of compassion fatigue could assist with identification of the condition, and also mitigate stigma in practitioners about the prevalence and impact of psychological distress in health professions. Prior to the implementation of any treatment or mitigation program, organizations should attempt to understand issues that affect their practitioners, and implement programs tailored to meet specific mitigating causes and concerns. This may be one specific benefit of a measurement tool such as the ProQOL as the effect of different domains can be measured, and more focused interventions considered.

Strengths and limitations

Our study used robust methods and analysis. A limitation of cross-sectional studies in general is the inability to infer causality from observed associations, and this includes in the synthesis of data in meta-analytic techniques. There was significant heterogeneity in the pooled mean subscale scores on all versions of the ProQOL; however, the 95% CIs were narrow indicating precision in the reported estimates.

Conclusion

Compassion fatigue exists across diverse practitioner groups and specialties and can be successfully measured using the ProQOL. Compassion fatigue’s relationship to demographic, personal, and professional characteristics is unclear, as demonstrated by the variability in studies reviewed. Future research should be directed to identifying specific triggers as root causes of compassion fatigue, impact of support programs for providers, and developing education programs to mitigate the prevalence and severity of compassion fatigue.

Supplemental material

Supplemental Material, Supp_Figure_1 - Compassion fatigue in healthcare providers: A systematic review and meta-analysis

Supplemental Material, Supp_Figure_1 for Compassion fatigue in healthcare providers: A systematic review and meta-analysis by Nicola Cavanagh, Grayson Cockett, Christina Heinrich, Lauren Doig, Kirsten Fiest, Juliet R Guichon, Stacey Page, Ian Mitchell and Christopher James Doig in Nursing Ethics

Supplemental material

Supplemental Material, Supp_Figure_2 - Compassion fatigue in healthcare providers: A systematic review and meta-analysis

Supplemental Material, Supp_Figure_2 for Compassion fatigue in healthcare providers: A systematic review and meta-analysis by Nicola Cavanagh, Grayson Cockett, Christina Heinrich, Lauren Doig, Kirsten Fiest, Juliet R Guichon, Stacey Page, Ian Mitchell and Christopher James Doig in Nursing Ethics

Supplemental material

Supplemental Material, Supp_Figure_3 - Compassion fatigue in healthcare providers: A systematic review and meta-analysis

Supplemental Material, Supp_Figure_3 for Compassion fatigue in healthcare providers: A systematic review and meta-analysis by Nicola Cavanagh, Grayson Cockett, Christina Heinrich, Lauren Doig, Kirsten Fiest, Juliet R Guichon, Stacey Page, Ian Mitchell and Christopher James Doig in Nursing Ethics

Footnotes

Conflict of interest

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iDs

Nicola Cavanagh

Christopher James Doig

Supplemental material

Supplemental material for this article is available online.

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