Konstantinos C Fragkos, Ioannis Sotiropoulos, Christos C Frangos

Abstract BACKGROUND Clinical empathy leads to improved patient satisfaction and better clinical outcomes. Currently, there are multiple empathy scales with minimal or no efforts to produce an integrated definition of clinical empathy which can be assessed sufficiently by only a few scales. Moreover, there is an unclear overall reliability of these empathy scales, hence limiting comparative evaluation.AIM To examine which empathy scales have been used in healthcare students and to estimate their overall internal consistency.METHODS A systematic review was performed with inclusion criteria any empirical study with quantitative data examining empathy of healthcare students toward patients between 2012 and 2016. A random effects model was used to produce a pooled estimate of the Cronbach’s alphas. The Hakstian-Whalen transformation was used for analyses based on the Rodriguez-Maeda method. Heterogeneity was quantified using the I2 statistic and further investigated with subgroup analysis and meta-regression. Publication bias was assessed using funnel plots, Egger’s test, Begg’s test, and the trim and fill analysis.RESULTS Thirteen scales have been used to assess clinical empathy in healthcare students from forty nine studies with total sample size 49384 students. The most frequently used scale is the Jefferson Scale of Physician Empathy followed by Davis’ Interpersonal Reactivity Index. The overall reliability was 0.805 (95%CI 0.786-0.823), which is acceptable, but there was heterogeneity and publication bias. Some heterogeneity was explained by the different countries of the studies under investigation and student types but most heterogeneity remained unexplained.CONCLUSION The results indicate that scales have satisfactory internal consistency but there are a multitude of scales, definitions and empathy components. Future research should focus on standardizing scales and creating consensus statements regarding the definition of empathy and use of appropriate scales.

Key words: Empathy; Scale; Reliability; Systematic review; Meta-analysis; Heterogeneity

INTRODUCTION

At its core, empathy is a particular form of interpersonal understanding and stands for a basic sensitivity to the mindedness of other persons[1]. Empathy is commonly distinguished between cognitive empathy and affective empathy[2]. Cognitive empathy denotes the ability to ascribe mental states to others, such as beliefs,intentions, or emotions; and affective empathy essentially involves affect on the part of the empathizer[3]. Its archetypal form is empathy with a person in need (e.g.,someone who is in pain, sad, or in an upsetting situation)[3]. An agreed definition of empathy remains an issue of controversy. A recent systematic review identified 109 suitable articles that could provide a definition of clinical empathy and they first identified three elements to its definition: thinking, feeling and acting. Each definition incorporates one or more of these elements[4]. Components of thinking that emerged from the systematic review were: cognition, perspective-taking,imagination/imagining, apprehension, understanding, seeing, perceiving, processing,comprehend, appreciation of, knowledge, recognize, identification, controlled,intellectually sense, role-taking, grasp, and identify with. Components of feeling were:Compassion, feeling, emotion, concern, joining with patient’s feelings, to enter into or join with feelings, socio-emotional, care, emotional participation, affective, vicarious emotional response, generation of similar feelings, sharing of emotions, sense,emotional contagion, sympathize, match/ experience someone’s emotional state,emotive, and specific feeling words:e.g., angry, enjoy, care, sad. And finally,components of acting were: Communication, conveying, behavioural, express, listen,interrupt, and eye contact[4]. However the authors didn’t arrive at a complete succinct definition.

Affective approaches to empathy are defined as having a matching reaction to the emotions of another individual. More recently, integrated approaches comprising of both types of empathy have emerged and appear to be more pragmatic[5]. Empathy should not be confused with compassion which requires emotion and action on the part of respondents, based on love, vulnerability, and reciprocity, and is actualized by disempowering one’s self and empowering the subject[6]. Similar concepts are sympathy, which is a subjective response based on pity towards another, humanism,caring, altruism, respect and integrity[7]. Empathy also has a strong neurobiological basis, although this is not discussed in the present study[8-11].

Assessing empathy is one of the most important aspects of investigating empathy with over 10 scales currently in use[4,12-14]. Differences between empathy measures depend on the conceptualization of empathy, factor structures and solutions and the target audience. For example, the Jefferson Scale of Physician Empathy traditionally is a 20-item scale and has three or four subscales depending on the sample under analysis: Perspective taking, compassionate care or standing in the patient’s shoes.Davis’ Interpersonal Reactivity Index consists of four subscales, Fantasy and Perspective Taking, which mirror the emotional aspect of empathy; and Empathetic Concern and Personal Distress, which reflect the cognitive dimension[15].

In general, it is considered that clinical empathy leads to improved patient satisfaction, greater adherence to therapy, better clinical outcomes, greater quality of service delivery perception and lower malpractice liability[16,17], while for clinicians and society it promotes the values of humanism[18], reduces professional burnout and increases diagnostic accuracy, and increases public trust to the healthcare system[19,20].Empathy has been found to decline over the course of clinical education, with clinical contact, distress, mistreatment by superiors, vulnerability, lack of social support, high workload, unsuitable learning environments, unsatisfactory role models and short patient admissions contributing towards this[19]. A demographic that plays a role in empathy is gender with females having been reported to usually have higher scores in excess of about 1-10 units in the Jefferson Scale of Physician Empathy[21-33].

Nevertheless, there are unresolved issues. First, there is a multitude of empathy scales with minimal or no efforts to produce an integrated definition of clinical empathy which can be assessed sufficiently by only a few scales. Next, there are 38 systematic reviews in the topic of empathy[4,5,12-14,16,19,34-64], but only six of them are metaanalyses[5,41,44,50,54,62]. The lack of quantitative synthesis does not allow for aggregation of research into meta-studies and umbrella reviews that are better in summarizing evidence and guiding policy and practice. Our hypotheses are that multiple empathy scales are currently in use and their results are heterogeneous. Hence, the present study’s objectives are to answer which empathy scales have been used in the last years (2012-2016) to assess and measure empathy in healthcare students, what their reliability is and which factors contribute to their heterogeneity.

MATERIALS AND METHODS

Study eligibility criteria

Inclusion criteria were any empirical study (full paper) with quantitative data examining empathy of healthcare students towards patients. There was a restriction to English language cross-sectional studies published between 2012 and 2016. Papers had to provide sufficient data to produce an effect measure for the meta-analysis.Empathy was only considered from healthcare students towards patients. Studies were excluded when they had other designs (case studies, pre-post experimental designs, empathy intervention studies), didn’t report quantitative data, were non-English, and investigated other types of empathy: empathy from professionals, nonhealthcare students, teachers (teacher empathy), perceived empathy of patients from their healthcare professionals, empathy among adolescents and high school students,empathy towards HIV patients, cross-cultural empathy, multicultural empathy, and empathy towards particular medical conditions.

Search strategy and terms

PRISMA guidelines for systematic reviews and meta-analyses were followed[65].Electronic database searches were conducted in Google Scholar, PubMed/Medline,Scopus, CINAHL, EMBASE and ERIC. The keywords for searching were: empathy,caring, humanism, cognitive, emotional, healthcare, medical students, nursing students, allied healthcare professionals students, dental students, reliability, validity,psychometric properties, validity, definition, compassion, care, Cronbach’s alpha,reliability, and consistency. The date of search was 1 January 2017 and included articles from 1 January 2012 up until 31 December 2016. The bibliographies from all included manuscripts and hand searching of relevant healthcare education journals(Academic Medicine, Advances in Health Sciences Education, International Journal of Medical Education, Medical Education Online, Medical Teacher, Medical Education,Teaching and Learning in Medicine, Perspectives on Medical Education, BMC Medical Education) were further literature search strategies.

Study selection, data extraction and quality assessment

The abstracts of the resulting studies were evaluated in terms of inclusion criteria. The full text was consulted when reading the abstract was not adequate to warrant inclusion. We extracted the following data from the included studies: Country,sample size, age, gender distribution, field, study design, aim, main results, scale,Cronbach’s alpha and number of items. The quality of studies (risk of bias) was assessed with the criteria suggested by Reillyet al[66].

Statistical analysis

Cronbach’s alpha (or alpha coefficient) is a measure of internal consistency of a test or scale and is expressed between 0 and 1. It essentially examines whether the scale under investigation measures what it claims to measure, by computing the intercorrelations of the items. When Cronbach’s alpha ranges from 0.70 to 0.95, a scale is considered to have acceptable internal consistency. Heterogeneous constructs,apparent lack of correlation between items, and too few scale items can lead to a low value of alpha[67,68].

Quantitative analysis was performed with Review Manager 5.3 and R 3.5.1. A random effects model was used to produce a pooled estimate of the Cronbach’s alphas. The Rodriguez-Maeda method is adopted to normalise the alpha coefficient by transforming it to the Hakstian-WhalenT=(1-alpha)1/3, which is a variable with standard normal distribution[69,70]. All analyses are performed using the transformed values and the results, such as the summary effect and its confidence interval, would then be converted back to alpha coefficients for presentation.

Heterogeneity between studies was quantified using theI2statistic (P≤ 0.10 for significance)[71], with values over 50 % indicating considerable heterogeneity[72-76].Sources of heterogeneity were explored performing subgroup analysis and metaregression. Publication bias was assessed using funnel plots, Egger’s and Begg’s tests,and the trim and fill analysis[77-79]. A funnel plot is a scatter plot of the effect estimates from individual studies against a measurement of the study’s sample size or precision[72]. Resemblance of a symmetrical inverted funnel supports that findings are due to sampling variation alone; thus, absence of bias[79]. In the present study, the funnel plot depicts the Hakstian-WhalenTagainst the study’s sample size, since the standard error of the effect size is dependent of the effect size[70,80].

RESULTS

Studies and quality assessment

The flow chart of study selection is shown in Figure 1. The initial search revealed 2491 studies which after applying the inclusion criteria were reduced to 49 studies. In total,14 scales of empathy were used. The total number of participants was 49384 students,mean age was 23.5 years and average male percentage was 44.6%. Sample sizes ranged from 44 to 5343. The distribution of student types are: dentistry (2 studies),healthcare (medicine, nursing, physiotherapy, occupational therapy, paramedics,midwifery, nutrition and dietetics) (1 study), medicine (31 studies), nursing (7 studies), osteopathic medical students (2 studies), paramedics (1 study), pharmacy and nursing (2 studies), pharmacy (1 study), physician assistant students (1 study),and speech and hearing sciences (1 study). Overall, medicine and dentistry students were 43028, nursing students were 3242 and allied professions students were 3114.Included studies’ information is shown in shown in Table 1. The overall quality of studies was satisfactory indicating low sampling bias and investigator bias with sufficient sample size in almost each study (Figure 2).

Meta-analysis of Cronbach’s alpha

The overall meta-analytic mean of Cronbach’s alpha is 0.805 (95%CI 0.786-0.823)(Figure 3A). The distribution of the alpha coefficients is shown in Figure 3B. There is heterogeneity (I2= 98%) and publication bias is possibly present, as shown with partial asymmetry in the funnel plot (Figure 3C). However, Egger’s and Begg’s tests are not significant (P= 0.076 andP= 0.648, respectively). The average alpha coefficients per scale are shown in Table 2. Trim and fill funnel analysis, indicated that most likely 11 studies more are unpublished due to publication bias and this is significant (P＜ 0.05). The scale with lowest Cronbach’s alpha is the Balanced Emotional Empathy Scale (0.720) and the one with the highest Cronbach’s alpha is theCaring Behaviour Inventory tool (0.921).

Table 1 Scales and studies in the meta-analysis

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Analysis of heterogeneity, sensitivity analysis and cumulative meta-analysis

Subgroup analyses were performed with regards to scale (Figure 4A) and country(Figure 4B), and subject of study (Figure 4C). With respect to country, heterogeneity reduces to non-significant in Portugal, Australia, Italy, Malaysia, Iran, and Germany(Figure 4B). Regarding subject of study, heterogeneity is non-significant only in osteopathic medical students and pharmacy and nursing students (Figure 4C).Finally, a meta-regression of mean age and male percentage as predictors of reliability is not significant for both parameters (Table 3).

Sensitivity analysis did not identify any study which influenced the meta-analytic outcome significantly (Figure 5A). Cumulative meta-analysis shows that after the addition of the meta-analysis’ tenth study in 2013 by Preusche and Wagner-Menghin[81], the outcome overall has trivial variation, indicating stability of the results.

Narrative discussion of studies

Thirteen empathy scales were identified with most of them being used in one study apart from the Jefferson Scale of Physician Empathy, Davis’ Interpersonal Reactivity Index and Caring Behaviour Inventory Tool which were used in 34, 3, and 2 studies respectively. Many studies reported that males had lower empathy scores compared to females. This was observed with the Balanced Emotional Empathy Scale[82], the Toronto Composite Empathy Scale[83], the Toronto Empathy Questionnaire[84], the Narcissism, Aloofness, Confidence, Empathy (NACE) scale-Empathy[85], and the Jefferson Scale of Physician Empathy[28,86-90]. Next, empathy decreased with progression through clinical education and empathy had decreased towards the clinical years with the Caring Ability Inventory[91], the Caring Behaviour Inventory Tool[92], the Toronto Empathy Questionnaire[84], and the Jefferson Scale of Physician Empathy[86,87,93,94].

Figure 1 Flow chart of study selection.

Regarding correlations between concepts and scales, the Jefferson Scale of Physician Empathy was correlated to Davis’ Interpersonal Reactivity Index (0.313)[95],Kiersma-Chen Empathy Scale (P＜ 0.05)[96]and the Toronto Empathy Questionnaire(0.480)[84]. There was a correlation between self-compassion and emotional intelligence(0.400)[97], empathy and interpersonal warmth[98], and empathy and social support[99].Main solutions of the factor analysis of Jefferson scale of Physician Empathy were a two[100]or three factor[101-104]solution comprising of mainly perspective taking and compassionate care followed standing in the patient’s shoes.

DISCUSSION

In the present study, a systematic review of empathy scales in healthcare students was performed. This is the first systematic review that also performed a meta-analysis of the internal consistency (Cronbach’s alpha) of the scales reviewed. Answering the two research questions, 13 scales have been used to assess clinical empathy in healthcare students form 49 studies and total sample size 49384 students. The most frequently used is the Jefferson Scale of Physician Empathy[25]followed by Davis’ Interpersonal Reactivity Index[105]. And secondly, the overall reliability was 0.805 (95%CI 0.786-0.823), which is acceptable, but there was heterogeneity and publication bias. Some heterogeneity was explained by different countries and student types but most heterogeneity remained unexplained. The most reliable scale was the Caring Behaviour Inventory Tool with alpha 0.921; Balanced Emotional Empathy Scale had the lowest reliability of 0.720, while the Jefferson Scale of Physician Empathy and Davis’ Interpersonal Reactivity Index were near the average with values of 0.798 and 0.791, respectively.

Figure 2 Risk of bias assessment. A: Risk of bias graph: review authors’ judgements about each risk of bias item presented as percentages across all included studies; B: Risk of bias summary: Review authors’ judgements about each risk of bias item for each included study.

The present study has certain limitations. First of all, there was heterogeneity in the meta-analysis. This was investigated with subgroup analyses and meta-regression,and a random effects model which sought to reduce the impact of heterogeneity.Heterogeneity could have resulted from population differences and design biases possibly not taken into account. A further limitation was that the meta-analysis was performed at the level of the scale and not the level of subscales for similar scales. The next limitation is the presence of publication bias, as indicated by asymmetry in thefunnel plot. This could indicate that there are possibly studies performed that had low internal consistency in their scales and have not been published or accepted for publication. The next important limitation is that the mean values and standard deviations (overall, females, and males) for each scale were not recorded. This is important considering the gender effect in empathy and the variability that this could produce and hence explain heterogeneity[106]. Other empathy moderators, not examined in the present study, were other psychological or personality constructs and differences in years. Quality assessment found only minimal impact from insufficient sample sizes. Nevertheless, the sample size in many studies is not sufficiently large which might have led to small study effects[107]. This suggests caution when interpreting results because small studies are more likely to report better results[108].

Table 2 Meta-analytic means of Cronbach’s alpha per empathy scale

The meta-analytic mean for Cronbach’s alpha was within the acceptable range(0.805 which is over 0.700) for scales as described in the literature[67,68]. However, it would be preferable if it were closer to 0.900. The most frequent scale used was the Jefferson Scale for Physician Empathy which had an alpha of 0.798. The highest alpha was noted with the Caring Behaviour Inventory Tool which had 0.921. These findings corroborate the concerns mentioned in the Introduction, which suggested that empathy is assessed in many ways with no clear consensus at present with regards to a preferred optimum.

Based on the findings of this meta-analysis, it seems that Caring Behaviour Inventory Tool ought to be utilized more. However, it has been developed mainly for nurses and it hasn’t been adapted for other healthcare specialties. This needs to be addressed and further studies are required with this scale tested in other groups.Nonetheless, the Jefferson Scale of Physician Empathy is currently being used most frequently and is currently dominating the clinical empathy literature. Hence, it seems that this scale could be improved with addition of further items that will increase internal consistency, thus increasing the Cronbach’s alpha. The third scale currently being used most frequently is Davis’ Interpersonal Reactivity Index. Its meta-analytic Cronbach’s alpha has the same issues mentioned for the Jefferson Scale of Physician Empathy.

Another practical implication is the need for a consensus to adopt a certain group of scales with the best internal consistency and widespread use. The present Babel of scales is confusing and disruptive for sound research production. The Jefferson Scale of Physician Empathy seems to be close to an integrated definition of empathy incorporating both cognitive and affective traits. It might benefit from the addition of more items similar to Davis’ Interpersonal Reactivity Index, thus also increasing its alpha. Moreover, empathy is a massive field and its research extends to social neuroscience and neuropsychology. Hence, we believe that clinical empathy as a field might benefit from borrowing concepts from research studies in the field of social neuroscience and neurobiology[109]. This will allow comparative analyses and possible improvements on definition, scales and development of theory. Finally, we believe that more meta-analyses and umbrella reviews are needed with various approaches and research questions in the field of clinical empathy[110]. The data produced by the literature is large and potentially unmanageable for individual researchers. At the same time, narrative reviews are bound by subjectivity, no matter how in-depth they are. The evidence-based approach will allow the most widely accepted definition and scales of clinical empathy to surface. Also, problematic areas will emerge and will stimulate further research.

Figure 3 Meta-analysis of Cronbach’s alpha. A: Forest plot for all studies; B: Distribution of reliabilities (Cronbach’s alpha) in the present study; C: Funnel plot of the effect size against sample size. The empty dots represent the studies from the trim-and-fill analysis. IV: Inverse variance.

In conclusion, this study presented the first meta-analysis of reliability for empathy scales in healthcare education. The results indicate that scales have satisfactory internal consistency but there is a confusion of scales, definitions and empathy components. There is evidently a need to standardize research in clinical empathy with meta-reviews[110]. Future research should focus on standardizing scales that are used throughout healthcare education and production of consensus statements on definition of empathy and use of appropriate empathy scales.

Table 3 Meta-regression results

Figure 5 Sensitivity analysis and cumulative meta-analysis. A: Forest plot for sensitivity meta-analysis; B: Forest plot for cumulative meta-analysis. IV: Inverse variance.

ARTICLE HIGHLIGHTS

Research background

Empathy is a particular form of interpersonal understanding and stands for a basic sensitivity to the mindedness of other persons. In general, it is considered that clinical empathy leads to improved patient satisfaction, greater adherence to therapy, better clinical outcomes, greater quality of service delivery perception and lower malpractice liability, while for clinicians and society it promotes the values of humanism, reduces professional burnout and increases diagnostic accuracy, and increases public trust to the healthcare system. Assessing empathy is one of the most important aspects of investigating empathy with over 10 scales currently in use.

Research motivation

There is a multitude of empathy scales with minimal or no efforts to produce an integrated definition of clinical empathy which can be assessed sufficiently by only a few scales. Next, there are 38 systematic reviews in the topic of empathy but only 6 of them are meta-analyses. The lack of quantitative synthesis does not allow for aggregation of research into meta-studies and umbrella reviews that are better in summarizing evidence and guiding policy and practice.

Research objectives

Our hypotheses are that multiple empathy scales are currently in use and their results are heterogeneous. The present study’s objectives are to answer which empathy scales have been used in the years 2012 to 2016 to assess and measure empathy in healthcare students, what their reliability is and which factors contribute to their heterogeneity.

Research methods

A systematic review was performed with inclusion criteria any empirical study with quantitative data examining empathy of healthcare students toward patients between 2012 and 2016. A random effects model was used to produce a pooled estimate of the Cronbach’s alphas. The Hakstian-Whalen transformation was used for analyses based on the Rodriguez-Maeda method.Heterogeneity was quantified using theI2statistic and further investigated with subgroup analysis and meta-regression. Publication bias was assessed using funnel plots, Egger’s test,Begg’s test, and the trim and fill analysis.

Research results

Thirteen scales have been used to assess clinical empathy in healthcare students from forty nine studies with total sample size 49384 students. The most frequently used scale is the Jefferson Scale of Physician Empathy followed by Davis’ Interpersonal Reactivity Index. The overall reliability was 0.805 (95%CI 0.786-0.823), which is acceptable, but there was heterogeneity and publication bias. Some heterogeneity was explained by the different countries of the studies under investigation and student types but most heterogeneity remained unexplained.

Research conclusions

This study is the first meta-analysis of reliability for empathy scales in healthcare education. The results indicate that scales have satisfactory internal consistency but there is a confusion of scales, definitions and empathy components. The meta-analytic mean for Cronbach’s alpha was within the acceptable range for scales. The Jefferson Scale of Physician Empathy is currently being used most frequently and is currently dominating the clinical empathy literature. In practice, there is need for consensus to adopt a certain group of scales with best internal consistency and widespread use. The Jefferson Scale of Physician Empathy seems to be close to an integrated definition of empathy incorporating both cognitive and affective traits. It might benefit from the addition of more items similar to Davis’ Interpersonal Reactivity Index, thus also increasing its alpha. Finally, more meta-analyses and umbrella reviews are needed with various approaches and research questions in the field of clinical empathy.

Research perspectives

Future research should focus on standardizing scales that are used throughout healthcare education and production of consensus statements on definition of empathy and use of appropriate empathy scales.