Culture and nonverbal expressions of empathy in clinical settings: A systematic review

Accepted Manuscript Title: Culture and Nonverbal Expressions of Empathy in Clinical Settings: A Systematic Review ´ Author: Aine Lori´e Diego A. Reinero Margot Phillips Linda Zhang Helen Riess M.D. PII: DOI: Reference:

S0738-3991(16)30446-3 http://dx.doi.org/doi:10.1016/j.pec.2016.09.018 PEC 5466

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Patient Education and Counseling

Received date: Revised date: Accepted date:

10-12-2015 22-7-2016 23-9-2016

´ Please cite this article as: Lori´e Aine, Reinero Diego A, Phillips Margot, Zhang Linda, Riess Helen.Culture and Nonverbal Expressions of Empathy in Clinical Settings: A Systematic Review.Patient Education and Counseling http://dx.doi.org/10.1016/j.pec.2016.09.018 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Culture and Nonverbal Empathy in Clinical Settings

Culture and Nonverbal Expressions of Empathy in Clinical Settings: A Systematic Review

Áine Lorié*1, Diego A. Reinero*1,2, Margot Phillips1, Linda Zhang1, Helen Riess1 Corresponding Author: Helen Riess, M.D., Empathy and Relational Science Program, Department of Psychiatry, Massachusetts General Hospital/Harvard Medical School. Wang Ambulatory Care Center, Suite 812, 15 Parkman Street, Boston, MA 02114. ([email protected]) T: 617-724-5600. F: 617-726-7451 [* Equal author contribution] 1

Massachusetts General Hospital/Harvard Medical School, Empathy and Relational Science Program, Department of Psychiatry, Boston, MA 2 New York University, Department of Psychology, New York, NY, USA

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Culture and Nonverbal Empathy in Clinical Settings Highlights: 

Nonverbal behaviors can convey culturally specific meaning in the clinical setting

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Discordant patient-physician race is linked with impaired information exchange

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Implicit bias emitted nonverbally negatively impacts communication and outcomes

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Training in identifying culturally-specific nonverbal behavior is suggested

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Culture and Nonverbal Empathy in Clinical Settings Abstract Objective: To conduct a systematic review of studies examining how culture mediates nonverbal expressions of empathy with the aim to improve clinician cross-cultural competency. Methods: We searched three databases for studies of nonverbal expressions of empathy and communication in cross-cultural clinical settings, yielding 16,143 articles. We examined peerreviewed, experimental or observational articles. Sixteen studies met inclusion criteria. Results: Nonverbal expressions of empathy varied across cultural groups and impacted the quality of communication and care. Some nonverbal behaviors appear universally desired and others, culturally specific. Findings revealed the impact of nonverbal communication on patient satisfaction, affective tone, information exchange, visit length, and expression decoding during cross-cultural clinical encounters. Racial discordance, patients’ perception of physician racism, and physician implicit bias are among factors that appear to influence information exchange in clinical encounters. Conclusion: Culture-based norms impact expectations for specific nonverbal expressions within patient-clinician dyads. Nonverbal communication plays a significant role in fostering trusting provider-patient relationships, and is critical to high quality care. Practice Implications: Medical education should include training in interpretation of nonverbal behavior to optimize empathic cross-cultural communication and training efforts should accommodate norms of local patient populations. These efforts should reduce implicit biases in providers and perceived prejudice in patients.

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Culture and Nonverbal Empathy in Clinical Settings INTRODUCTION There is critical need for health care providers to offer culturally competent empathic care [1-3]. Increasing diversity in patient populations and the healthcare workforce can generate crosscultural misunderstandings, contributing to increased medical errors, lack of trust and adherence to treatment [4-7], and decreased patient satisfaction [8-10]. The U.S. confirms this multicultural trend, reporting that by 2043, no individual racial group within the U.S. will make up a majority [11]. In spite of increasing global diversification [12, 13], medical trainees are not adequately prepared to provide cross-culturally competent care [14]. In-group biases (the effect wherein people give preferential treatment to others who are perceived to be in the same group) arise in cross-cultural contexts [15-18] and often disproportionally affect minorities, leading to disparities in treatment, healthcare access, and health outcomes [19-23]. Indeed, a previous literature review of cultural differences in medical communication found that clinicians are more verbally dominant and behave less affectively (e.g., less rapport-building, friendly, or concerned) when interacting with ethnic minority patients compared to White patients [24]. Therefore, competence in cross cultural communication is becoming increasingly critical in practices and policies of health services, with a corresponding need to train medical personnel in these skills to improve the quality of care and patient outcomes [25].

Empathy, a capacity that includes cognitive and affective components enabling individuals to perceive and respond to verbal and nonverbal emotional cues of others [26] is a key component of effective cross-cultural care [9, 20, 26-38]. Empathy is expressed both through verbal and nonverbal behavior [39], and nonverbal behavior (NVB) is estimated to account for 60%-90% of communication [40]. The importance of nonverbal empathy in clinical encounters has been

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Culture and Nonverbal Empathy in Clinical Settings highlighted in previous work [41-47], suggesting that clinician warmth and listening results in greater patient satisfaction [48], and that specific NVBs, including head nodding, forward lean, direct body orientation, uncrossed legs and arms, arm symmetry, and mutual gaze, are associated with positive health outcomes [49]. Providers who are more sensitive to nonverbal cues reinforce the perception of physician sincerity, dedication, and competence, which in turn improves utilization of health services, functional status, and the overall provider-patient relationship [50].

Although existing medical, psychological, and sociological literature abounds with research that examines gaps in cross-cultural communication, in-group bias, and the need for cultural awareness and training [51-55], there is little research integrating cross-cultural differences and patient-clinician NVB [56-61]. One study that focused on the verbal exchange between patients and clinicians reported difficulty in reliably detecting NVB as such expressions can be communicated vaguely, downplayed or masked, and veiled by language barriers [62]. Levine and Ambady’s (2013) review examined the influence of nonverbal behavior on racial disparities in healthcare. The findings suggest that through both historical minority group derogation and clinician disengagement, patient distrust can arise. Moreover, negative stereotyping, and culturally-bound nonverbal expectations obstruct nonverbal communication and engagement in cross-racial patient-clinician encounters [61]. However, this previous review was not systematic and focused primarily on White doctors and African American patients, thus limiting the scope and generalizability of its findings. Our systematic review expands on Levine and Ambady’s work (2013) by broadening the cross-cultural context, and systematically examining a wider range of groups that report culturally specific practices of NVB in healthcare.

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Culture and Nonverbal Empathy in Clinical Settings Culture has been defined as a learned system of knowledge, attitudes, beliefs, behaviors, values, and norms that is shared by a group of people, community, kin, or nation [63]. Our systematic review is guided by the following research questions: 1) Are nonverbal expressions in the clinical setting culturally specific or universal? 2) If culturally specific, in what ways does empathic NVB in the clinical setting differ cross-culturally? 3) What are the effects of empathic cross-cultural NVB on patient outcomes? An examination of these questions will reveal some of the complexities of cross-cultural nonverbal communication and empathy, and may subsequently offer solutions to improve provider training, clinician cross-cultural competency, and the reduction of disparities. Our systematic review will conclude with practice implications and recommendations for future research.

METHODS We searched MEDLINE, PsycINFO, and CINAHL from 1990 through September 18, 2014. An example of our electronic search strategy (MEDLINE) is outlined in Appendix A (PsycINFO and CINAHL search strategies available upon request). The electronic search strategy required that articles: (1) be written in English and published in a peer-reviewed journal; (2) include in the title or abstract at least one word related to culture (e.g., race, ethnicity, immigrant, crosscultural), clinician-patient communication (e.g., empathy, nonverbal, patient centered) and a clinical setting (e.g., hospital, clinic, primary care). For the review by hand, the inclusion criteria were: (1) experimental or observational studies with adults (age ≥ 18) and ≥ 10 subjects, written in English and published in a peer-reviewed journal; (2) clinician-patient interactions addressing health problems; (3) an analysis or discussion of cultural components; (4) an analysis or discussion of clinician-patient NVB communication. Studies were excluded if: (1) not all four of

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Culture and Nonverbal Empathy in Clinical Settings the inclusion criteria were met; (2) the patients had severe psychiatric, neurologic, or facial impairments obstructing communication; (3) the health problems discussed were addressed through non-traditional medical practice, (4) translators were the main focus of the study. For full criteria, see Appendix B. Limitations are presented after the Discussion.

Our electronic search yielded 16,143 articles (MEDLINE: 8,709; PsycINFO: 3,079; CINAHL: 4,355). Removing duplicates yielded 16,025 articles. For the initial review, two pairs of authors each independently reviewed half of the titles. A fifth author resolved disagreements between reviewer-pairs (99% reviewer-pair agreement). Articles were included for the next round of review if the title incorporated at least two of the three main content criteria (“culture”, “communication”, “clinical”) and appeared relevant to the study’s goal. This process yielded 1,040 articles.1 The second round of review examined the abstracts of these remaining articles, again with two pairs of authors each reviewing one half of the results. Articles were included if the abstract included all three content criteria. A fifth author resolved disagreements between reviewer-pairs (95% reviewer-pair agreement). This yielded 116 articles. This new total included two additional articles that were hand selected from the reference list of informative reviews. The final round examined the full text of each article. Authors made independent judgments as to whether the article met inclusion/exclusion criteria with particular focus on quality of nonverbal communication measured. Disagreements were resolved by face-to-face discussion of four

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Although this article selection process is common for systematic reviews, we nevertheless performed a sensitivity check on 100 randomly selected results that had previously been excluded (on the basis of the initial title review by two authors) and systematically reviewed the abstracts of each of these articles. This sensitivity check confirmed that none of the 100 articles met our inclusion criteria and provides evidence that our study selection process is indeed robust. 7

Culture and Nonverbal Empathy in Clinical Settings authors, leading to consensus judgment. Sixteen articles met our inclusion criteria. This selection process adhered to PRISMA guidelines and is illustrated in Figure 1.

(Insert) Figure 1. Flow Chart of Study Selection Process.

RESULTS The systematic review yielded 16 studies (Table 1). Eleven studies were conducted in the United States; other locations included Canada, Slovenia, Sweden, Australia, and Trinidad and Tobago. Six studies examined White Americans and African Americans [64-69]; other cultural groups studied were Australian Aboriginals, Brazilians, Filipinos, South Asians, and Hispanics. Six studies assessed scenarios in which the patients belonged to a minority culture and clinicians belonged to the dominant culture [67, 68, 70-73] , and five studies examined combinations of patients and providers in both majority and minority cultures [64-66, 69, 74]. By contrast, four studies examined scenarios in which the providers belonged to a minority culture [75-78], for example internationally educated nurses or physicians (from countries such as the Philippines (39 total), India (11 total), China (5 total), Korea (3 total), Jordan (1 total), Lebanon (1 total), Nigeria (1 total), and Kenya (1 total)). One study examined providers’ NVBs within the majority culture [79].

The methods of data analysis varied across the included studies. There were nine quantitative studies and seven qualitative studies. One study was a randomized controlled trial [68]; eight were cross-sectional. Three studies used the Roter Interaction Analysis System (RIAS) to code

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Culture and Nonverbal Empathy in Clinical Settings physician and patient behaviors during clinical encounters [67-69]. Seven studies reported acceptable inter-rater reliability. Sample sizes of quantitative studies ranged from 52 to 458. The seven qualitative studies were based on semi-structured interviews or focus groups, and their sample sizes ranged from 10 to 48.

Patient and physician age and gender were reported in all of the quantitative studies. Factors inconsistently reported were number of years in host country, level of education, language proficiency, and use of interpreters. Mood or mental state was assessed in two studies [66, 68].

Clinical specialties included primary care clinics (5 studies), hospitals (5 studies), specialty clinics (2 studies), nursing home (1 study), medical school (1 study), nursing school (1 study), and community center (1 study). Care providers of different specialties and level of training were studied, including: general providers (3 studies), physicians (8 studies), nurses (2 studies), medical students (1 study), nursing students (1 study), and nursing home caregivers (1 study).

Main Findings Findings of nonverbal behaviors influencing empathic cross-cultural care can be grouped into two main categories (Table 2). We focus on quantitative studies demonstrating changes in patient or clinician NVBs in cross-cultural clinical encounters and their outcomes. These include patient satisfaction, affective tone, information exchange, visit length, and expression decoding. Main findings and recommendations from qualitative studies that demonstrate cultural preferences for specific NVBs as part of empathic care are presented in (Table 2).

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Culture and Nonverbal Empathy in Clinical Settings Patient satisfaction. Physician concern, communicated nonverbally, correlated with patient satisfaction in several studies [65, 66, 68, 72, 74]. Aruguete et al. showed that physician nonverbal concern, irrespective of patient or physician race, was the best predictor of patient satisfaction (p < .001) and positive physician recommendation from the participant (p < .001) [65]. When the physician displayed positive emotion, made eye contact, and appeared attentive, physician race was not correlated to participants' evaluations [65]. In another study, poorer decoding of South Asian patients’ facial expressions (regardless of physician race) was correlated with lower visit satisfaction and lower likelihood of adhering to a physician’s recommendations [74]. Similarly, high levels of perceived racism among AA patients interacting with White physicians were associated with low patient ratings of warmth and respectfulness (OR= 0.19, 95% CI= 0.05, 0.72) [67]. Cooper et al. showed that higher rates of physician implicit race bias in racially discordant dyads were correlated with AA patients’ poorer ratings of patient care (e.g., AA patients were less likely to feel that the doctor respects the patient (50.2% vs 34.9%, p = 0.001), were less likely to report liking the physician (46.6% vs 32.7%, p < .001), and less likely to recommend the physician (47.3% vs 34.4%, p = 0.001)). Values for trust, feeling the physician likes him or her, and having confidence in the physician were not significant [66].

Affective tone. Changes in the affective tone (tone of voice, warmth, or responsiveness) of patients and clinicians during cross-cultural clinical encounters were found in several studies. Johnson et al. found that both the patient and physician showed significantly less positive affect during visits with AA patients as compared with White patients (patient positive affect: p < .001; physician positive affect: p < .02) [69]. Stepanikova et al. found that nonverbal communication

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Culture and Nonverbal Empathy in Clinical Settings in concordant AA–AA dyads was more positive, as indicated by more smile, touch, and open body position, compared to communication in any other racial combination [64].

Cooper et al. found a significant association between physician implicit bias as measured on an Implicit Attitude Test (IAT) and patient positive affect, where AA patients were less likely to demonstrate positive affect (as observed by coders) as compared to encounters with physicians without implicit race bias (p = .04). Higher levels of physician implicit race bias were significantly associated with greater clinician verbal dominance, lower patient positive affect, and poorer ratings of interpersonal care among AA patients [66]. Implicit bias also correlated with significantly higher ratings of physician positive affect during visits with White patients, but there was no significant change in positive affect among White patients. Similarly, Hausmann et al. found that encounters in which patients reported high levels of perceived racism had a significant negative association with coder ratings of nonverbal provider positive affect (B = 0.34, 95% CI= -0.66, -0.01) and with patient positive affect (B= -0.41, 95% CI= -0.073, -0.09) [67].

Havranek et al. [68] further explored how race influences communication in race-discordant clinical encounters. In a randomized controlled trial of the effects of a values affirmation exercise (validation of patient self-worth and concerns) given prior to clinic visits, coder ratings of warmth/friendliness and interactivity were significantly higher in the intervention group, whereas ratings of depression/sadness and distress were significantly higher in the control groups.

Information exchange. Racial discordance, patients’ perception of physician racism, and

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Culture and Nonverbal Empathy in Clinical Settings physician implicit bias are among factors that appear to influence information exchange in clinical encounters. In Havranek et al., AA patients randomized to receive values-affirmation training prior to their clinic visit gave and asked for significantly more information about their medical condition than the control group (p = .03) [68].

In racially discordant dyads, physicians were more verbally dominant (p < .001) and less patientcentered (p < .05) with AA patients than with White patients [69]. Physicians with higher rates of implicit bias predicted significantly more clinician-dominated exchanges irrespective of patient race: (p < 0.05, and p < 0.01) [66, 69]. High levels of perceived racism among AA patients were negatively associated with patient ratings of ease of communication (OR= 0.22, 95% CI=0.07, 0.67) [67]. Perceived racism among White patients was negatively associated with patient ratings of visit informativeness (OR= 0.4, 95% CI= 0.23, 0.71), but not among AAs [67].

Visit length. Findings for visit length varied. Visit length remained the same despite significant improvements of information exchange after patients received values affirmation training in Havranek et al. Ratings of physicians’ rate of speech, verbal dominance, and patient centeredness did not differ significantly between the intervention and control groups [68]. In another study, higher levels of physician compliance stereotyping (a measure of the implicit association between race and the concept of the “compliant patient”) were associated with longer visits, slower speech, less patient centeredness, poorer ratings of interpersonal care and lower ratings of patient positive affect among AA patients [66]. In contrast, Johnson et al. showed no difference in speech speed or visit duration when medical visits between AA or White patients were compared [69].

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Culture and Nonverbal Empathy in Clinical Settings

Expression decoding. One study of physicians’ ability to identify nonverbal emotional cues across races was included in our review [74]. South Asian physicians were no better at decoding facial expressions or vocal tones of South Asian or Caucasian patients than Caucasian physicians. Physicians, regardless of their ethnicity, were more accurate at rating Caucasian patients’ facial expressions and vocal tones than South Asian faces and voice tones. Therefore, assumptions cannot be made regarding greater attunement to NVB between similar groups, as the accuracy in NVB decoding appears to be related more to the influence of the dominant culture.

Cultural preferences for NVBs: qualitative studies. The qualitative studies included in our review revealed explicit patient preferences and expectations for certain NVBs as part of empathic care. [70-73, 76-78]. They are summarized in Table 2.

DISCUSSION Our systematic review results indicate that nonverbal expressions of empathy are essential components of cross-cultural clinical competency and quality care. However, optimal expression of empathic NVB can vary across cultural groups, especially in culturally diverse clinical settings. It appears that culture mediates nonverbal empathic expression on several levels, including race, nationality, gender, and occupation [64, 66, 67, 69, 71, 74, 79]. Greater attention to and skill with interpreting and expressing NVB across such cultural groups can improve the provider-patient relationship and help to diminish disparities in quality of care. Several theories inform the interpretation of our findings, discussed below.

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Culture and Nonverbal Empathy in Clinical Settings Emotion expression: Cultural equivalence or cultural advantage model? Extensive research suggests that the expressions of six basic emotions (happiness, sadness, anger, fear, disgust, and surprise) are universal [80]2, though members of the same national or ethnic group may be more able to identify these facially-expressed emotions [82]. There has also been debate as to whether empathy, which encompasses the detection and expression of a broad range of emotions, is a capacity that can be expressed and understood universally (cultural equivalence model) or is subject to cultural norms (cultural advantage model) [58]. This raises the concern of whether specific nonverbal expressions of empathy may be universally interpreted or culturally dependent. For example, culturally determined power and status dynamics may drive certain expectations of nonverbal deference to authority figures, such as reduced or avoidance of direct eye contact with physicians. Such culturally dependent expectations of behavior, as revealed through NVB, may become more pronounced in cross-cultural patient-clinician encounters, risking further miscommunication within and between different cultural groups. These communication missteps may discourage patient participation, reduce shared decision-making and diminish patient-centered care, which could negatively impact the quality of care and ultimately, healthcare outcomes.

Cross-cultural considerations of nonverbal empathy 1) Race Whereas this review’s search terms aimed to capture a broad representation of cultural groups our search yielded a predominance of American reports that focused on race as the cultural variable of interest in the patient-clinician encounter. This emphasis on race may reflect

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Also see [81] Barrett LF. Are emotions natural kinds? Perspect Psychol Sci. 2006;1:28-58. 14

Culture and Nonverbal Empathy in Clinical Settings perceived racial bias in the U.S., belying a lengthy historical context of minority group oppression. Nonetheless, cross-racial communication issues may also extend to other crosscultural communication contexts, particularly those focusing on group prejudices.

Race plays a role in physicians’ NVB and its influence is best understood when physician race and patient race are considered jointly [64]. One study showed that AA physicians exhibited more positive NVB with AA patients than White physicians, in contrast to mixed positive and negative signals found between AA physicians interacting with White patients [64]. These findings suggest that NVB exists at both conscious and unconscious levels of awareness. In another study, high levels of perceived past discrimination by AA patients were correlated with a perceived lack of White physician’s positive affective tone and overall worse care [67]. This implies that clinicians working with discordant groups should be especially aware that past experiences of discrimination could influence how patients perceive the clinician’s nonverbal displays.

2) Nationality Differences in empathic nonverbal expressions were shown across cultural groups [64-68, 73, 74, 79, 83]; however, each cultural group valued and/or employed positive nonverbal signals. Some studies indicated that particular cultural groups have preferences for specific nonverbal expressions (e.g., gaze and proximity) that are context dependent [70, 72, 73, 77]. Western physicians must take caution in cross-cultural contexts not to misinterpret acts of nodding or silence as signs of mutual understanding as these patient expressions could instead be masking confusion or suppressing emotions [71]. Missing or inaccurately decoding such NVB in a cross-

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Culture and Nonverbal Empathy in Clinical Settings cultural context may overlook patients’ physiological and psychological distress and could also decrease clinicians’ diagnostic acumen.

Specific NVBs, such as eye contact, may also have various meanings. For example, a Filipino Canadian community voiced preference for more direct eye contact from providers, especially if the provider is giving instructions [73]. This same group also cautioned against the use of lowered eye contact, which can symbolize respect or shame depending on the context, as well as head-to-foot gaze, which could be interpreted as demeaning [73]. However, in direct contrast, a study with Caribbean medical students cautioned against the use of direct eye contact with some Caribbean elderly as this could be interpreted as a sign of disrespect [77].

In multiple studies, open body posture was assessed [64, 65, 75, 77, 79] and associated with patient ratings of clinician warmth and overall care. Proximity to the patient was generally viewed as empathic (e.g., Brazilians preferred closer proximity and warmth), although Williams et al. noted certain constraints by gender and age in Caribbean cultures (Table 2). These nuanced results further highlight that although training is often shaped by the dominant culture, it should actually be tailored to the norms of the local population. Therefore, a provider’s use and awareness of specific NVB should be aligned with the specific cultural norms of patients to enhance both information exchange and patient satisfaction.

3) Gender and occupation NVB can vary according to gender and profession of the provider, however differences in NVB by gender and occupation are largely unexamined variables in the cross-cultural clinical context,

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Culture and Nonverbal Empathy in Clinical Settings and here we report preliminary findings. Zaletel et al. examined the frequency of NVBs in Slovenian nursing homes and found that male caregivers3 exhibited more negative NVBs (e.g., dropping the eyes, refusing by head shaking, frowning, staring, making grimaces) than female caregivers. Non-physician professional staff exhibited positive NVBs (e.g., making eye contact, smiling, raising the eyebrows, nodding) significantly more frequently than non-professional “helpers” [79]. Additionally, gender differences were noted in which female caregivers demonstrated mixed nonverbal patterns with their male patients [79]. Stepanikova et al. found that female physicians delivered highly positive nonverbal messages using smile and gaze but at the same time, their body position was more closed, suggesting a lack of social ease [64].

Studies of internationally educated nurses and physicians found that NVBs served both as barriers and compensatory strategies for empathic clinical care. Xu et al. [75] found that internationally educated nurses in the U.S. used therapeutic touch less frequently and were perceived as less warm by U.S. raters. The cultural norms regarding touch are particularly important to understand, as touch could be perceived as dominating or controlling, or as an expression of warmth and caring depending on the cultural group or cross-cultural context. In contrast, studies of internationally educated clinicians [76, 78] reported that clinicians attempted to compensate for language gaps by using more touch and emphasizing gestures, eye contact, smile, and friendliness to convey care.

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The group of 267 caregivers (27 men, 240 women) consisted of three groups: nursing staff (graduate nurses and nurse assistants), social helpers (auxiliary personnel), and other nonphysician professionals (physiotherapists, occupational therapists, social workers). 17

Culture and Nonverbal Empathy in Clinical Settings Intergroup and implicit bias In addition to racial and ethnic differences, the patient-clinician relationship may be regarded as an intergroup interaction as there is an inherent power differential in the patient-clinician relationship due to the clinician’s medical knowledge and experience, and the patient’s subordinate role of seeking medical advice. The power differential within the patient-clinician relationship or the concept of “professional dominance” [84] can also be affected by various cultural factors, including nationality, socio-economic status, race, gender, and age. Current intergroup research indicates that prejudice toward different cultural groups often stems from implicit in-group biases, which results in favoring or being selective towards members that share the same group identity [85-88]. Our findings indicate that implicit bias can “leak out” through inadvertent negative nonverbal expressions and can be detected in the form of verbal dominance and lower patient positive affective tone [66]. Implicit biases could likewise be revealed in other inadvertent nonverbal expressions, such as closed body position or reduced eye contact [64]. Such culturally determined dynamics can seriously compromise successful clinical care and therefore require greater awareness of these NVBs to advance and strengthen cross-cultural competency [24].

LIMITATIONS This systematic review has several limitations. First, examining the provider-patient relationship, cultural dynamics, and NVB is a complex undertaking and definitions and naming conventions are heterogeneous. Second, we were limited to reviewing full-text articles in English after 1990, thereby potentially excluding relevant studies published pre-1990 or those published in other languages. Pragmatically, we were limited to English-only papers as we did not have ready

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Culture and Nonverbal Empathy in Clinical Settings access to translators or multilingual authors. Although this presents a serious limitation in crosscultural research, one key area of interest is how other cultures convey and perceive empathy via NVB as it relates to interactions with U.S.-based clinicians. As noted in our introduction, the US is becoming more racially diverse and cross-cultural clinical encounters are on the rise. This is of particular interest as our systematic review allows us to make more concrete recommendations for our U.S.-based clinicians. The recent publication dates of many of the cited studies confirm intensified research and clinical interest in this topic due to rapidly changing demographics.

Additionally, there were methodological limitations of several studies we examined. Two studies [65, 75] included simulated patients, and although this design increases internal validity, it limits external validity. One study used a facial expression computer program to test provider facial expression decoding in lieu of direct clinical observation [74]. The sample sizes of our studies were generally small and insufficiently powered to assess confounding variables such as age, gender, socioeconomic status, clinical setting, language fluency or degree of acculturation. Most studies used convenience samples rather than randomized samples, and most were Western and Eurocentric-based. Furthermore, because members of the dominant culture typically code studies, additional coder bias may have been introduced. Together, these methodological limitations suggest cultural NVB is an important area for further research with larger patient and clinician samples that follow rigorous research methodologies, both in qualitative and quantitative investigations.

PRACTICE IMPLICATIONS

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Culture and Nonverbal Empathy in Clinical Settings Nonverbal communication is a critical component of cross-cultural competency, which includes demonstrating respect for patients and fostering empathy and trust. While these competencies appear to be universally valued, there are cultural differences in how they are expressed and reciprocated. Clinicians’ cultural competence can improve by learning the nonverbal norms of the various cultural backgrounds that they serve. There are cross-cultural nonverbal practices that appear to be widely desired, such as open body posture, smile, and demonstrations of warmth by facial expression. There are also reports of NVBs that convey culturally different meanings, such as length and directness of eye gaze, meaning of hand gestures, and touch, and these must be used judiciously. This review summarized specific and generally desired NVB’s in the cultural studies that met our inclusion criteria (Appendix B). Specific techniques for training in cultural competency are described below.

Empathy is a process that involves both receptive and expressive capacities [26], and clinicians in cross-cultural encounters require skills to perceive patient cues and express culturally sensitive nonverbal behaviors. This can be achieved by promoting clinician awareness of implicit race bias [66, 67] and teaching appropriate responses. Specific techniques may include role-playing, imagery, mindfulness training [67] and nonverbal skills training [26]. Values affirmation exercises prior to race-discordant clinical encounters can also enhance information exchange and perception of providers’ NVBs displays of warmth and respect [68]. Providers more skilled at cross-cultural NVB will also strengthen their perceived dedication and competency amongst patients, as well help improve their diagnostic abilities by eliciting affective cues and establishing rapport with the patient [89]. These techniques are similar to the empathy training for medical trainees, previously reported, [26], which can be applied to cross-cultural

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Culture and Nonverbal Empathy in Clinical Settings interactions. Finally, how we train medical students and clinicians should reflect the diversity of the populations they serve, rather than the norms of the dominant culture in order to promote diagnostic accuracy, mutual respect and trust.

CONCLUSION Nonverbal communication and culture permeate virtually every aspect of health care delivery, and this review demonstrates that additional research is needed. Some cultural groups have context-dependent preferences for certain NVBs [70, 73, 77]. This complicates detection and delivery of nonverbal signals among culturally discordant groups. Though culturally specific NVBs of empathy exist, we recognize that culture is dynamic and constantly changing, particularly in cross-cultural environments [90]. Our review of the literature highlights that culture not only shapes norms for NVB in medical encounters, but it also appears to mediate communication itself [64, 66, 67, 71, 74, 79]. Therefore, greater training efforts are needed to improve perception and interpretation of patients’ NVB, and to enhance clinicians’ awareness of their own displays of empathic NVB. Both undergraduate and graduate medical education initiatives could encourage focus groups and specific training in this emerging area. Medical trainees increasingly represent multinational and multiracial backgrounds, or have worked in medical settings all over the world. Such trainees could be invited to share cultural norms from diverse backgrounds in experiential learning settings to inform traditional patient-doctor courses. Training programs in empathic behavior with patients from all backgrounds are needed.

Further research in empathic NVB is critical to the global health conversation. Currents in today’s world political landscape are creating additional urgency for training in cross-cultural

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Culture and Nonverbal Empathy in Clinical Settings competence. With massive shifts of minority groups into racially and ethnically dominant cultures, the misinterpretation of cultural norms and NVB can have dire consequences if cultural competence is not made a top priority – consequences not only for individuals and patients, but for populations as a whole. This review serves as a springboard to develop training programs that focus on empathic NVB with special attention to cross-cultural communication. Such training is urgently needed at the undergraduate and graduate level to improve cultural competency nationally and internationally in our increasingly diverse world.

Acknowledgments/Funding: All authors gratefully acknowledge that this project was made possible with a grant from The Arnold P. Gold Foundation and the David Judah Fund. The Arnold P. Gold Foundation and the David Judah Fund had no role in study design, collection, analysis, interpretation of data, writing the report, nor in the decision to submit the report for publication. The authors would also like to thank Carole Foxman, Martha Stone, Lidia Schapira, M.D., and Arielle Gordon-Rowe for their invaluable assistance.

Authors’ Contact Information: 1. Áiné Lorié, Ph.D., Empathy and Relational Science Program, Department of Psychiatry, Massachusetts General Hospital/Harvard Medical School. Wang Ambulatory Care Center, Suite 812, 15 Parkman Street, Boston, MA 02114. ([email protected]) T: 617721-9961

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Culture and Nonverbal Empathy in Clinical Settings 2. Diego A. Reinero, B.S., Department of Psychology, New York University. 6 Washington Place, New York, NY 10003. ([email protected]) 3. Margot Phillips, M.D., Empathy and Relational Science Program, Department of Psychiatry, Massachusetts General Hospital/Harvard Medical School. Wang Ambulatory Care Center, Suite 812, 15 Parkman Street, Boston, MA 02114. ([email protected]) 4. Linda Zhang, Empathy and Relational Science Program, Department of Psychiatry, Massachusetts General Hospital/Harvard Medical School. Wang Ambulatory Care Center, Suite 812, 15 Parkman Street, Boston, MA 02114. ([email protected]) 5. Helen Riess, M.D., Empathy and Relational Science Program, Department of Psychiatry, Massachusetts General Hospital/Harvard Medical School. Wang Ambulatory Care Center, Suite 812, 15 Parkman Street, Boston, MA 02114. ([email protected]) T: 617724-5600. F: 617-726-7451

Author Contributions: Helen Riess had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the review. Study concept and design: Lorié, Phillips, Zhang, Riess Acquisition of data: Lorié, Reinero, Phillips, Zhang, Riess Analysis and interpretation of data: Lorié, Reinero, Phillips, Riess Drafting of the manuscript: Lorié, Reinero, Phillips, Riess Critical revision of the manuscript for intellectual content: Lorié, Reinero, Phillips, Riess Obtained funding: Riess

23

Culture and Nonverbal Empathy in Clinical Settings Administrative, technical, or material support: Reinero Study supervision: Riess

All authors gave final approval to the submitted paper.

Ethical Approval: No ethical approval was required for the systematic review.

Conflict of Interest Disclosures: Dr. Riess reports a financial interest in Empathetics, Inc. No other disclosures were reported.

24

Culture and Nonverbal Empathy in Clinical Settings References: [1] Berger JT. Culture and ethnicity in clinical care. Arch Intern Med 1998;158:2085-90. [2] Briggance BB, Burke N. Shaping America's health care professions: the dramatic rise of multiculturalism. Western J Med 2002;176:62-4. [3] Kleinman A, Eisenberg L, Good B. Culture, illness, and care: clinical lessons from anthropologic and cross-cultural research. Ann Intern Med 1978;88:251-8. [4] Petersen LA. Racial differences in trust: reaping what we have sown? Med Care 2002;40:81-4. [5] Thom DH, Campbell B. Patient-physician trust: an exploratory study. J Fam Pract 1997;44:169-76. [6] Safran DG, Taira DA, Rogers WH, Kosinski M, Ware JE, Tarlov AR. Linking primary care performance to outcomes of care. J Fam Pract 1998;47:213-20. [7] Kaiser Family Foundation. Race, Ethnicity and Medical Care, A Survey of Public Perceptions and Experiences. http://kff.org/disparities-policy/poll-finding/race-ethnicitymedical-care-a-survey-of/, 1999 (accessed 16.07.21). [8] Nelson A. Unequal treatment: confronting racial and ethnic disparities in health care. Journal of the National Medical Association 2002;94:666-8. [9] Freshman B, Rubino L. Emotional intelligence: a core competency for health care administrators. The Health Care Manager 2002;20:1-9. [10] Tate DM. Cultural awareness: bridging the gap between caregivers and Hispanic patients. J Continuing Educ Nurs 2003;34:213-7. [11] Census Bureau US. U.S. Census Bureau Projections Show a Slower Growing, Older, More Diverse Nation a Half Century from Now. 25

Culture and Nonverbal Empathy in Clinical Settings https://www.census.gov/newsroom/releases/archives/population/cb12-243.html, 2012 (accessed 16.07.21). [12] Rechel B, Mladovsky P, Ingleby D, Mackenbach JP, McKee M. Migration and health in an increasingly diverse Europe. The Lancet 2013;381:1235-45. [13] Tjale A, De Villiers L. Cultural issues in health and health care: A resource book for Southern Africa. Cape Town: Juta and Company Ltd; 2004. [14] Weissman JS, Betancourt J, Campbell EG, Park ER, Kim M, Clarridge B, et al. Resident Physicians' Preparedness to Provide Cross-Cultural Care. J Am Med Assoc 2005;294:105867. [15] Cheon BK, Im D-m, Harada T, Kim J-S, Mathur VA, Scimeca JM, et al. Cultural influences on neural basis of intergroup empathy. Neuroimage 2011;57:642-50. [16] de Greck M, Shi Z, Wang G, Zuo X, Yang X, Wang X, et al. Culture modulates brain activity during empathy with anger. NeuroImage 2012;59:2871-82. [17] Gutsell JN, Inzlicht M. Intergroup differences in the sharing of emotive states: neural evidence of an empathy gap. Soc Cogn Affect Neur 2012;7:596-603. [18] Han S, Northoff G, Vogeley K, Wexler BE, Kitayama S, Varnum ME. A cultural neuroscience approach to the biosocial nature of the human brain. Annu Rev Psychol 2013;64:335-59. [19] Sabin JA, Nosek BA, Greenwald AG, Rivara FP. Physicians' implicit and explicit attitudes about race by MD race, ethnicity, and gender. J Health Care Poor U 2009;20:896913. [20] Betancourt J, R. , Green AR, Carrillo JE, Park ER. Cultural Competence And Health Care Disparities: Key Perspectives And Trends. Health Affair 2005;24:499-505

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Culture and Nonverbal Empathy in Clinical Settings [21] Betancourt JR, Corbett J, Bondaryk MR. Addressing disparities and achieving equity: cultural competence, ethics, and health-care transformation. Chest 2014;145:143-8. [22] Weathers M, Frank E, Spell LA. Differences in the communication of affect: Members of the same race versus members of a different race. J Black Psychol 2002;28:66-77. [23] van Ryn M, Burke J. The effect of patient race and socio-economic status on physicians' perceptions of patients. Soc Sci & Med 2000;50:813-28. [24] Schouten BC, Meeuwesen L. Cultural differences in medical communication: a review of the literature. Patient Educ and Couns 2006;64:21-34. [25] DiMatteo MR, Hays RD, Prince LM. Relationship of physicians' nonverbal communication skill to patient satisfaction, appointment noncompliance, and physician workload. Health Psychol 1986;5:581. [26] Riess H, Kelley JM, Bailey RW, Dunn EJ, Phillips M. Empathy training for resident physicians: a randomized controlled trial of a neuroscience-informed curriculum. J Gen Intern Med 2012;27:1280-6. [27] Riess H, Kelley JM, Bailey R, Konowitz PM, Gray ST. Improving Empathy and Relational Skills in Otolaryngology Residents A Pilot Study. Otolaryng Head Neck 2011;144:120-2. [28] Hickson GB, Federspiel CF, Pichert JW, Miller CS, Gauld-Jaeger J, Bost P. Patient complaints and malpractice risk. J Am Med Assoc 2002;287:2951-7. [29] Hemmerdinger JM, Stoddart SD, Lilford RJ. A systematic review of tests of empathy in medicine. BMC Med Ed 2007;7:24. [30] Liu X, Rohrer W, Luo A, Fang Z, He T, Xie W. Doctor–patient communication skills training in mainland China: A systematic review of the literature. Patient Educ and Couns 2015;98:3-14.

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Culture and Nonverbal Empathy in Clinical Settings [31] Betancourt JR. Cross‐cultural medical education: conceptual approaches and frameworks for evaluation. Acad Med 2003;78:560-9. [32] Chung RC-Y, Bemak F. The relationship of culture and empathy in cross-cultural counseling. J Couns Dev 2002;80:154-9. [33] Brant C. Communication patterns in Indians: Verbal and non-verbal. Annals of Sex Research 1993;6:259-69. [34] Marsella AJ. Counseling and psychotherapy with Japanese Americans: cross-cultural considerations. Am J Orthopsychiat. 1993;63:200-8. [35] Mitchell JL. Cross-cultural issues in the disclosure of cancer. Cancer Pract 1998;6:15360. [36] Mullin VC, Cooper SE, Eremenco S. Communication in a South African cancer setting: Cross-cultural implications. Int J Rehabil Health 1998;4:69-82. [37] Xu Y, Davidhizar R. Intercultural communication in nursing education: when Asian students and American faculty converge. J Nurs Educ 2005;44:209-15. [38] Juckett G. Cross-cultural medicine. Am Fam Physician 2005;72:2267-74. [39] Riess H, Kraft-Todd G. EMPATHY: A Tool to Enhance Nonverbal Communication Between Clinicians and Their Patients. Acad Med 2014;89:1108-1112. [40] Mehrabian A. Nonverbal communication: Transaction Publishers; 1977. [41] Buetow SA. Something in nothing: negative space in the clinician-patient relationship. Ann Fam Med 2009;7:80-3. [42] Caris-Verhallen WM, Kerkstra A, Bensing JM. Non-verbal behaviour in nurse-elderly patient communication. J Adv Nurs 1999;29:808-18.

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Culture and Nonverbal Empathy in Clinical Settings [43] Duffy A. Non-verbal communication in cancer and palliative care. Nursing Times 2006;102:30-1. [44] Hannawa AF. Shedding light on the dark side of doctor-patient interactions: Verbal and nonverbal messages physicians communicate during error disclosures. Patient Educ Couns 2011;84:344-51. [45] Ishikawa H, Hashimoto H, Kinoshita M, Fujimori S, Shimizu T, Yano E. Evaluating medical students' non-verbal communication during the objective structured clinical examination. Med Ed 2006;40:1180-7. [46] Kacperek L. Clinical. Non-verbal communication: the importance of listening. British Journal of Nursing 1997;6:275-9. [47] Tilson ER, Gibson SD. High-touch patient care in radiology. Seminars in Radiologic Technology 1999;7:1. [48] Henry S, Fuhrel-Forbis A, Rogers M, Eggly S. Association between nonverbal communication during clinical interactions and outcomes: a systematic review and metaanalysis. Patient Educ Couns 2012;86:297-315. [49] Beck RS, Daughtridge R, Sloane PD. Physician-patient communication in the primary care office: a systematic review. J Am Board Fam Pract 2002;15:25-38. [50] Roter DL, Frankel RM, Hall JA, Sluyter D. The expression of emotion through nonverbal behavior in medical visits. J Gen Intern Med 2006;21:S28-S34. [51] Betancourt J, R. , Green AR, Carrillo JE, Ananeh-Firempong O. Defining cultural competence: a practical framework for addressing racial/ethnic disparities in health and health care. Public Health Rep 2003;118:293–302.

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Culture and Nonverbal Empathy in Clinical Settings [52] Betancourt J, Cervantes M. Cross-cultural medical education in the United States: key principles and experiences. Kaohsiung J Med Sci 2009;25:471-8. [53] Maier-Lorentz MM. Transcultural nursing: its importance in nursing practice. Journal of Cultural Diversity 2008;15:37-43. [54] Flores G. Culture and the patient-physician relationship: achieving cultural competency in health care. J Pediatr 2000;136:14-23. [55] Sue DW, Capodilupo CM, Torino GC, Bucceri JM, Holder A, Nadal KL, et al. Racial microaggressions in everyday life: implications for clinical practice. Am Psychol 2007;62:271. [56] Wang Y-W, Davidson MM, Yakushko OF, Savoy HB, Tan JA, Bleier JK. The scale of ethnocultural empathy: development, validation, and reliability. J Couns Psychol 2003;50:221. [57] Segal EA. Social empathy: A model built on empathy, contextual understanding, and social responsibility that promotes social justice. J Soc Serv Res 2011;37:266-77. [58] Soto JA, Levenson RW. Emotion recognition across cultures: the influence of ethnicity on empathic accuracy and physiological linkage. Emotion 2009;9:874. [59] De Maesschalck S, Deveugele M, Willems S. Language, culture and emotions: exploring ethnic minority patients' emotional expressions in primary healthcare consultations. Patient Educ Couns 2011;84:406-12. [60] Kale E, Finset A, Eikeland H-L, Gulbrandsen P. Emotional cues and concerns in hospital encounters with non-Western immigrants as compared with Norwegians: An exploratory study. Patient Educ Couns 2011;84:325-31.

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Culture and Nonverbal Empathy in Clinical Settings [61] Levine CS, Ambady N. The role of non-verbal behaviour in racial disparities in health care: implications and solutions. Med Ed 2013;47:867-76. [62] Kale E, Skjeldestad K, Finset A. Emotional communication in medical consultations with native and non-native patients applying two different methodological approaches. Patient Educ Couns 2013;92:366-74. [63] Smith G. Communication and culture. In: Holt RaW, editor. New York 1966. [64] Stepanikova I, Zhang Q, Wieland D, Eleazer G, Stewart T. Non-verbal communication between primary care physicians and older patients: How does race matter? J Gen Intern Med 2012;27:576-81. [65] Aruguete MS, Roberts CA. Participants' ratings of male physicians who vary in race and communication style. Psychol Rep 2002;91:793-806. [66] Cooper LA, Roter DL, Carson KA, Beach MC, Sabin JA, Greenwald AG, et al. The associations of clinicians' implicit attitudes about race with medical visit communication and patient ratings of interpersonal care. Am J Public Health 2012;102:979-87. [67] Hausmann LR, Hannon MJ, Kresevic DM, Hanusa BH, Kwoh C, Ibrahim SA. Impact of perceived discrimination in healthcare on patient-provider communication. Med Care 2011;49:626-33. [68] Havranek EP, Hanratty R, Tate C, Dickinson LM, Steiner JF, Cohen G, et al. The effect of values affirmation on race-discordant patient-provider communication. Arch Intern Med 2012;172:1662-7. [69] Johnson RL, Roter D, Powe NR, Cooper LA. Patient Race/Ethnicity and Quality of Patient-Physician Communication During Medical Visits. Am J Public Health 2004;94:208490.

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Culture and Nonverbal Empathy in Clinical Settings [70] Bergman AA, Connaughton SL. What Is Patient-Centered Care Really? Voices of Hispanic Prenatal Patients. Health Commun 2013;28:789-99. [71] Shahid S, Finn LD, Thompson SC. Barriers to participation of Aboriginal people in cancer care: communication in the hospital setting. Med J Aust 2009;190:574-9. [72] Roberts TE. Health practices and expectations of Brazilians in the United States. J Cult Divers 2007;14:192-7. [73] Pasco ACY, Morse JM, Olson JK. Cross-Cultural Relationships Between Nurses and Filipino Canadian Patients. J Nurs Scholarship 2004;36:239-46. [74] Coelho K, Galan, C. Physician cross-cultural nonverbal communication skills, patient satisfaction and health outcomes in the physician-patient relationship. Int J Family Med 2012;Article ID 376907:5. [75] Xu Y, Staples S, Shen JJ. Nonverbal Communication Behaviors of Internationally Educated Nurses and Patient Care. Research & Theory for Nursing Practice 2012;26:290308. [76] Jain P, Krieger JL. Moving beyond the language barrier: The communication strategies used by international medical graduates in intercultural medical encounters. Patient Educ Couns 2011;84:98-104. [77] Williams S, Harricharan M, Sa B. Nonverbal Communication in a Caribbean Medical School: “Touch Is a Touchy Issue”. Teach Learn Med 2013;25:39-46. [78] Jirwe M, Gerrish K, Emami A. Student nurses experiences of communication in crosscultural care encounters. Scand J Caring Sci 2010;24:436-44. [79] Zaletel M, Kovacev AN, Mikus RP, Kragelj LZ. Nonverbal communication of caregivers in Slovenian nursing homes. Arch Gerontol Geriat 2012;54:94-101.

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Culture and Nonverbal Empathy in Clinical Settings [80] Ekman P. Emotions Across Cultures. In: Books T, editor. New York 2003. [81] Barrett LF. Are emotions natural kinds? Perspect Psychol Sci 2006;1:28-58. [82] Elfenbein HA, Ambady N. On the universality and cultural specificity of emotion recognition: A meta-analysis. Psychol Bull 2002;128:203-35. [83] Harrigan JA, Rosenthal R. Physicians' Head and Body Positions as Determinants of Perceived Rapport. J Appl Soc Psychol 1983;13:496-509. [84] Freidson E. Profession of medicine: a study of the sociology of applied knowledge. In: Dodd MC, editor. New York 1970. [85] Banaji MR, Greenwald AG. Blindspot: Hidden Biases of Good People: Random House Publishing Group; 2013. [86] Green AR, Carney DR, Pallin DJ, Ngo LH, Raymond KL, Iezzoni LI, et al. Implicit Bias among Physicians and its Prediction of Thrombolysis Decisions for Black and White Patients. J Gen Intern Med 2007;22:1231-8. [87] Tajfel H, Turner JC. An integrative theory of intergroup conflict. In: Brooks/Cole, editor. The social psychology of intergroup relations In W G Austin & S Worchel (Eds). Monterey, CA 1979. p. 33-47. [88] Turner JC. Some current issues in research on social identity and self-categorization theories. Social identity: Context, commitment, content. 1999:6-34. [89] Roter DL, Hall JA, Katz NR. Relations between physicians' behaviors and analogue patients' satisfaction, recall, and impressions. Med Care 1987:437-51. [90] Matsumoto D. Cultural similarities and differences in display rules. Motiv Emotion 1990;14:195–214.

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Culture and Nonverbal Empathy in Clinical Settings

Figure 1. Flow Chart of Study Selection Process.

34

Culture and Nonverbal Empathy in Clinical Settings Appendix A. MEDLINE Electronic Search Strategy Database: Ovid MEDLINE(R) 1946 to Present -------------------------------------------------------------------------------1 Empathy/ or empath*.ti,ab. (16415) 2 compassion*.ti,ab. (4567) 3 affect/ (24011) 4 eye contact.ti,ab. or Eye Movements/ (23679) 5 (gaze* or gazing).ti,ab. (9762) 6 kinesics/ or gestures/ or (gesture* or body language).ti,ab. (4209) 7 nonverbal communication/ or (non-verbal or nonverbal).ti,ab. (9773) 8 facial expression/ or facial.ti,ab. (83410) 9 Voice Quality/ or voice.ti,ab. (19708) 10 Touch/ or touch*.ti,ab. (28443) 11 smiling/ or (smile* or smiling).ti,ab. (3742) 12 (handshake* or shake hand* or hand shake*).ti,ab. (183) 13 lean*.ti,ab. (25884) 14 Posture/ or postur*.ti,ab. (75225) 15 or/1-14 (311111) 16 Physician-Patient Relations/ (59545) 17 Interpersonal Relations/ (54776) 18 "Attitude of Health Personnel"/ (90992) 19 Attitude/ or additude*.ti,ab. (38762) 20 Trust/ or trust.ti,ab. (20571) 21 stereotyping/ or stereotyp*.ti,ab. (22961) 22 Personal Satisfaction/ or satisf*.ti,ab. (198602) 23 communication barriers/ or barrier*.ti,ab. (143193) 24 (doctor patient or patient doctor).ti,ab. (4900) 25 communication/ or communicat*.ti,ab. (191659) 26 clinician*.ti,ab. (114903) 27 (patient adj1 physician).ti. (1816) 28 relations*.ti. (181398) 29 Primary Health Care/ (53504) 30 medicine/ or general practice/ or family practice/ (88263) 31 or/16-30 (1113105) 32 15 and 31 (37998) 33 exp Ethnic Groups/ or ethnic*.ti,ab. (159069) 34 "Minority Groups"/ or minorit*.ti,ab. (43777) 35 refugees/ or "transients and migrants"/ (14289) 36 Racism/ or (race* or racial or racism or biracial).ti,ab. (94970) 37 Prejudice/ or prejudic*.ti,ab. (24724) 38 Healthcare Disparities/ or disparit*.ti,ab. (34508) 39 attitude to health/ (72138) 40 health knowledge, attitudes, practice/ (71692) 41 (culture* or cultural).ti,ab. (784151) 42 cross-cultural comparison/ or cultural characteristics/ or cultural competency/ or cultural

35

Culture and Nonverbal Empathy in Clinical Settings diversity/ (44690) 43 exp geographic locations/ (3206192) 44 exp Continental Population Groups/ (152589) 45 or/33-44 (4116502) 46 32 and 45 (10064) 47 limit 46 to english language (9382) 48 limit 47 to yr="1990 - 2014" (8719) 49 animal/ (5256927) 50 48 not 49 (8586) 51 humans/ and 48 (8330) 52 50 or 51 (8653) NOTE: A second search was run using these same search terms but adding the search statement: “cues/ or (cue*1 or clue*1).ti,ab.” to the top of list, and identifying any new results as a consequence of this addition.

Appendix B. Inclusion and Exclusion Criteria Inclusion Criteria: Experimental or observational studies examining each of the following: 1) Communication, for example, “empathy”, “compassion”, “affective” “relationship”, “nonverbal”, “gaze”, “patient satisfaction”) 2) Cultural groups, for example, “cross-cultural”, “socio-cultural”, various ethnic, racial, and country groups, “cultural competence”; 3) Clinician-patient interactions addressing health problems. 4) Studies reported in English, peer-reviewed papers, subjects > 18 years old, N > 10. Exclusion Criteria: Commentaries, reviews, dissertations, replies, and book chapters Studies on theoretical, hermeneutics, and concept analysis Studies on patients with severe neurologic impairment and disorders of face and neck that interfere communication Studies on patients with active psychosis or developmental disorders Studies on nonverbal healing through massage or dance therapy Studies on sex therapy/ relationship counseling Studies on mother-infant bonding Studies on infants Studies on children Studies on auditory disorders Studies on pharmacy Studies on translator communication 36

Culture and Nonverbal Empathy in Clinical Settings

TABLE 1. Overview of studies: sample, setting, methods, and nonverbal behaviors studied (studies are organized in reverse chronological order within study design)

Patient sample, total n (n of each culture)

Author

Study Design

Havranek, E. P., et al. (2012)

Randomiz ed control trial

USA

Primary care

99 (99 AA)

Coelho, K. R. & Galan, C. (2012)

Crosssectional

USA

Hospitals and clinics

Cooper, L. A., et al. (2012)

Cross sectional

USA

2 Primary care clinics

Country

Practice

Clinician sample, total n (n of each culture)

Inte rrate r relia bilit y

Nonverbal behavior studied

Observatio n Strategy

Instruments

7 (7 non-AA physicians)

Audiotaped clinic visits

RIAS, patient questionnaire

0.98

Emotional tone of patient and physician

Patient satisfaction and provider satisfaction, physician verbal dominance, patient centeredness, visit duration, information exchange

60 (30 South Asian, 30 WA)

30 (16 South Asian, 14 WA physicians)

Computerize d tests of physicians' ability to decode facial expressions and vocal tones

1) Facial expression coding system, 2) Vocal tone assessment, 3) Patient satisfaction survey, 4) authordeveloped Patient Adherence survey

NR

Facial expression decoding accuracy and vocal tones decoding accuracy

Patient satisfaction, self-reported patient adherence

269 (213 AA, 56 WA)

40 (9 AA, 12 Asian, 19 WA physicians)

Audiotaped clinic visits; Implicit Association Tests (IAT) for clinicians

Two IATs for measuring racial attitudes and stereotypes, and patient questionnaire

0.861

Patient and physician positive affect

Implicit race bias and compliance bias of physicians, patient satisfaction, visit length, speech speed, clinician verbal dominance, patient

Outcomes

37

Culture and Nonverbal Empathy in Clinical Settings centeredness

Stepanikova, I., et al. (2012)

Crosssectional

USA

3 Primary care clinics

209 (29 nonWhite, 190 WA)

30 (3 nonwhite, 27 WA physicians)

Videotaped clinic visits

Adaption of the Nonverbal Communicati on in Doctor– Elderly Patient Transactions (NDEPT)

0.830.96

Open body position, eye contact, smile, touch

Patient ease, physician’s mixed signals

Xu, Y., et al. (2012)

Crosssectional

USA

2 Hospitals

1 (1 standardized patient)

52 (IENs: 38 Philippines, 5 India, 3 Korea, 3 China, 1 Kenya, 2 NR)

Videotaped encounter of nursing intake of a standardized patient

Authordeveloped scales

0.82

Eye contact, smile, body position, nodding, gesture, hugging, interpersonal space, and therapeutic touch

Global assessment of communication

Hausmann, L. R., et al. (2011)

Crosssectional

USA

Veterans Affairs Hospitals

353 (100 AA, 253 WA)

63 (63 Orthopedic surgeons)

Audiotaped clinic visits

RIAS, patient questionnaire

0.680.92

Provider warmth/respect fulness

Patient-rated visit informativeness, and ease of communicating with the provider

Zaletel, M., et al. (2012)

Crosssectional

Slovenia

27 Nursing homes

267 (267 Slovenians)

267 (267 Slovenian care givers)

Direct clinical observation by pairs of trained observers

Kovacev Non-Verbal Expression Checklist

NR

Provider facial expressions, head movements, gestures, body position, silence

Distribution of nonverbal behaviors by gender and professional type

38

Culture and Nonverbal Empathy in Clinical Settings Johnson R. L., et al. (2004)

Crosssectional

USA

General clinics

458 (256 AA, 202 WA)

61 (21 AA, 9 Asian, 30 WA, 1 Other physicians)

Audiotaped clinic visits

RIAS, patient questionnaires

0.880.79

Patient and physician positive affect score: dominance/ass ertiveness (patient only), interest/attenti veness (both), friendliness/wa rmth (both), responsiveness /engagement (both), and sympathy/emp athy (both)

Patient positive affect, physician positive affect, verbal dominance, patientcentered orientation, visit duration and speech speed

Aruguete, M. S. & Roberts, C. A. (2002)

Crosssectional

USA

Student health clinic

116 (97 AA, 19 WA)

2 (1 AA, 1 WA physician in a simulated video)

Participants watched 1 of 4 videos

Patient questionnaires

NR

Physician facial expression, distance from patient, concern for patient, understanding of patient

Patient-rated satisfaction, trust, self-disclosure, recommendation, recall, compliance

Bergman, A. A. & Connaughto n, S. L. (2013)

Qualitativ e

USA

Prenatal clinic

48 (48 Hispanic)

NR (American providers)

Semistructured interviews

Qualitative

NR

Physician warmth, friendliness, smile, eye contact, patience, formal greetings

Patient centered care approaches, patient trust, provider credibility

Williams, S., et al. (2013)

Qualitativ e

Trinidad and Tobago

Medical School

N/A

36 (36 medical students)

Videotaped focus groups

Qualitative

NR

Eye contact, personal space, body movements, touch, vocal tone

Provider perceptions of patient expectations

39

Culture and Nonverbal Empathy in Clinical Settings Jain, P. & Krieger, J. L. (2011)

Qualitativ e

USA

Hospital

N/A

12 (Internationa lly educated resident physicians: 6 India, 2 China, 1 Jordan, 1 Lebanon, 1 Nigeria, 1 Philippines)

Semistructured audiorecorded interviews

Qualitative

NR

Eye contact, touch, gestures, warmth

Internationally educated resident physicians’ crosscultural strategies

Jirwe, M., et al. (2010)

Qualitativ e

Sweden

Nursing school

N/A

10 (5 Swedish student nurses, 5 immigrant student nurses)

Semistructured audiorecorded interviews

Qualitative

NR

Eye contact, smile, gestures, warmth

Swedish and nonSwedish student nurse strategies and difficulties in crosscultural encounters

Shahid, S., et al. (2009)

Qualitativ e

Australia

Varied: recruited from oncology centers

30 (30 Australian Aborigines)

NR Australian providers

Semistructured audiorecorded interviews

Qualitative

NR

Patient nodding and silence, physician friendliness

Trust, patient perception of physician knowledge and competence

Roberts, T. E. (2007)

Qualitativ e

USA

Community centers

42 (42 Brazilians)

NR American providers

Semistructured interviews

Qualitative

NR

Perception of physician warmth, touch

Patient satisfaction, patient trust

Pasco, A. C., et al. (2004)

Qualitativ e

Canada

Hospital

24 (24 Filipinos)

NR Canadian nurses

Semistructured interviews

Qualitative

NR

Touch, eye contact and gaze

Patient trust

NOTES: AA = African American, WA = White Americans, IEN = Internationally educated nurse, MD = physician, RN = Registered nurse, N/A = Not applicable, NR = not reported, NVB = Nonverbal behavior, RIAS = Roter Interaction Analysis System, USA = United States of America

40

Culture and Nonverbal Empathy in Clinical Settings

TABLE 2. Studies' Main Nonverbal Findings (Studies are organized in reverse chronological order within study design) Study

Havranek, E. P., et al. (2012)

Coelho, KR., and Galan, C. (2012)

Refer ence # 68

74

Study Design

Research aims

Main nonverbal findings

Implications

Randomi zed control trial

To test the effect of a values affirmation intervention given to AA patients prior to their clinic visit with a non-AA primary care physician

Affective tone: overall communication in the intervention group was significantly more friendly, interactive, and respectful (p=0.02). Patients were rated as less distressed and less depressed (p=.03) Information exchange: patients in the intervention group requested and provided more information about their medical condition (p =.03). Visit length: no significant difference Patient satisfaction: no significant difference Patient trust: no significant difference

• Values affirmation exercise can improve the experience of AA patients in primary care visits with non- AA physicians

To examine physicians’ abilities to decode nonverbal emotions of Caucasian and South Asian patients, and to test the hypothesis that this ability correlates with patient satisfaction and

Facial and vocal tone decoding accuracy: South Asian physicians were no better at decoding the facial expressions or vocal tones of South Asian patients, and both South Asian and Caucasian physicians were better at decoding Caucasian nonverbal stimuli (p < .0001) Patient satisfaction:

• Physicians can have difficulty interpreting South Asian nonverbal cues which is correlated with poorer patient satisfaction and poorer patient adherence

Crosssectional

• Greater exchange of medical information is achieved without increasing visit length, and overall positive affective tone of patients and physicians is significantly greater • Physicians should be aware that their affective tone may be influenced by the patient's level of comfort and monitoring cues such as instructiveness and friendliness may influence patients' affective tone and exchange of medical information

• Physicians should be trained to improve awareness of differences in South Asian facial and vocal tone expression

41

Culture and Nonverbal Empathy in Clinical Settings

Cooper, L. A., et al. (2012)

66

Crosssectional

patient adherence

South Asian patients were more likely to be dissatisfied with the quality of care provided by their physician (p = .032) Patient adherence: South Asian patients reported they were less likely to adhere to recommendations (p < .001)

To examine associations of clinician’s implicit attitudes about race with visit communication and patient ratings of care

Positive Affect: clinician race bias was associated with lower patient positive affect among Black patients and higher physician positive affect among White patients Physician verbal dominance: clinician race bias was associated with greater physician verbal dominance among Black patients and White patients Visit length and speech speed: clinician race compliance bias was associated with longer visits and slower speech among Black patients and faster visits and faster speech among White patients Patient Satisfaction: greater clinician race bias was associated with lower Black patient ratings of clinician respect, liking, (p < .001) or recommending physician (p = .001)

• Training to improve clinician awareness of implicit race bias. • Physician self-awareness can reduce implicit race and compliance bias, with improvements in overall communication and patient ratings of care, particularly among Black patients

42

Culture and Nonverbal Empathy in Clinical Settings Stepanikova, I., et al. (2012)

64

Crosssectional

To examine the influence of race of physicians with patients who are over 65 years old, on nonverbal communication during medical interviews

Open body posture, smile and touch: Concordant race resulted in high use of smile, touch, and open body position for both AA and White physicians, and was highest in AA–AA dyads compared to the average across other dyads (open body posture: p < 0.001; smile: p = 0.048; touch: p < 0.001). Discordant race in AA physicians with White patients resulted in highest use of smile and gaze with lowest use of open body position. Eye contact: White physicians made more eye contact with White patients as compared to their AA patients but it was only marginally significant (p = .08)

• Training in nonverbal behavior across all races with specific focus on open body posture and awareness to avoid sending mixed nonverbal messages, especially in race discordant visits

Xu, Y., et al. (2012)

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Crosssectional

To evaluate nonverbal communication behaviors of internationally educated nurses (IENs) in the United States

Therapeutic touch (p < .01), interpersonal space ( p < .01), and eye contact (p<.05) were positively correlated to overall global impression score

• Provide targeted communication training to newly arrived/hired IENs with focus on therapeutic touch, interpersonal space, and eye contact to improve patient rating of overall clinical care

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Culture and Nonverbal Empathy in Clinical Settings Hausmann, L. R., et al. (2011)

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Zaletel, M., et al. (2012)

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Crosssectional

To examine the relationship between AA and White patients’ perceptions of discrimination from past healthcare encounters and patient-provider communication during a subsequent medical visit

Listening: Feeling that a physician did not listen was the most common form of perceived racism expressed by both races Affective tone: less positive nonverbal affect among patients (Beta = -0.41, 95% CI= -.73, -0.09) and providers (Beta = -0.34, 95% CI= -0.66,-0.01) was associated with high levels of perceived racism among AA patients Warmth/respectfulnes s: high levels of perceived racism was associated with low patient ratings of provider warmth/respectfulness (OR=0.19, 95% CI=0.05, 0.72) and ease of communication (OR =0.22, 95% CI=0.07, 0.67). Perceived classism yielded similar results

• Increase physician awareness of unintentional biases

Crosssectional

To quantify nonverbal communication of caregivers in Slovenian nursing homes

Smile: No significant difference in rates of smiling between gender or type of caregiver Eye contact: No significant difference in rates of eye contact between gender or type of caregiver Gestures: associated with gender and type of caregiver, with nurses and females manifesting fewer negative expressions (p = 0.034)

• Training to improve rates of positive nonverbal communication

• Training to improve positive affective tone, listening, and how to counter negative emotion states through role-playing or mindfulness

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Culture and Nonverbal Empathy in Clinical Settings Johnson R.L., et al. (2004)

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Crosssectional

To examine the association between patient race/ethnicity and patientphysician communication

Affective tone: overall physician affective tone was less positive with AA compared with White patients, and AA patient affective tone was less positive compared with White patients (p = .02) Verbal dominance: physicians were 23% more verbally dominant with AA patients than with White patients (p < .001) Patient-centeredness: content was 33% less patient-centered with AA patients (p < 0.5)

• Training to improve clinician communication skills including affective communication (e.g., rapport-building, minimizing verbal dominance), and empowering minorities for active participation in health care

Aruguete, M. S. and C. A. Roberts (2002)

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Crosssectional

To examine the impact of race (AA vs. White) and nonverbal communication on patient evaluations

Smile, facial expression, eye contact, attentiveness, personal space (sitting < 2 feet from patient), and posture (forward lean): physician display of nonverbal concern via these behaviors was the best predictor of patient satisfaction (p < .001) and positive physician recommendation (p < .001), regardless of physician race

• Increase nonverbal skills training for students and practitioners in same and discordant race encounters, with focus on behaviors that communicate nonverbal concern

Bergman, A. A. and S. L. Connaughton (2013)

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Qualitati ve

To understand the experience and expectations of Hispanic women in prenatal clinics

Friendliness: Patients expressed preference for friendly ("amable") providers Smile: a smile may convey warmth, professionalism, and confidence that the provider was competent Eye contact: patients sought sustained eye contact together with a

• Training to improve awareness of local cultures' expectations for patient-centered communication: e.g., Hispanic women in prenatal clinic visits expressed preferences for physician friendliness, attentiveness, and patience/not rushing

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Culture and Nonverbal Empathy in Clinical Settings smile as signs of provider professionalism and warmth

Williams, S., et al. (2013)

Jain, P. and J. L. Krieger (2011)

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Qualitati ve

Qualitati ve

To understand the challenges of teaching nonverbal communication skills in a Caribbean medical school

Eye Contact: in Tobago, it is considered disrespectful to look into the eyes of an elder Personal Space: in the Bahamas and Jamaica, closer proximities are considered invasive rather than reassuring

• Traditional (Western) teaching of physician nonverbal behavior did not reflect the diversity of patient preferences in Caribbean cultures

To understand the communication strategies international medical graduates use in medical interactions to overcome language and cultural barriers

Internationally educated physicians expressed difficulty knowing how to respond to patients' emotions after giving bad news because in their culture physicians disclose medical information to family members rather than to the patient directly. They may compensate for intercultural differences and language barriers with several strategies, including repeating information using nonverbal communication such as eye contact, friendliness, smile, vocally conveying warmth and care, respectful silence, and supportive touch

• Training to improve communication strategies of internationally educated physicians early in their career, with focus on disclosure of medical information and addressing patients' negative emotions when giving bad news

• Medical education should address culturally specific norms for nonverbal communication

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Culture and Nonverbal Empathy in Clinical Settings Jirwe, M., et al. (2010)

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Qualitati ve

To understand the experiences of student nurses' cross-cultural communication with patients

Lack of skills and language barriers can result in patient and nurse dissatisfaction. Communication strategies included mirroring the patient’s emotions, using pictures and using body language (smile, eye contact, touch). Nurses who had immigrated to Sweden expressed more confidence communicating in crosscultural encounters than Swedish nurses

• Training to improve nursing skills, confidence, and satisfaction, including use of smile, touch, eye contact, and mirroring patient expressions

Shahid, S., et al. (2009)

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Qualitati ve

To report Aboriginal patients' views about effective communication between Aboriginal people and cancer providers in Australia

Warmth: Aboriginal patients tended to act reserved and viewed many physicians as lacking compassion and warmth Silence: Aboriginal patients expressed reluctance to admit to difficulty understanding their physicians and lacked the confidence to ask questions Head Nod: Aboriginal patients may nod rather than admit lack of understanding

• Improve awareness of meaning of Aboriginal patients' silence and nodding, and further integrate Aboriginal clinical support and interpreters in cancer care

Roberts, T. E. (2007)

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Qualitati ve

To understand what health practices and beliefs are common among Brazilian immigrant patients

Warmth: Brazilian immigrants experienced U.S. clinicians as lacking warmth and desired more personal warmth from their providers ("carinho") Personal space: preference for more physical closeness from providers Touch: preference for a hug or a kiss over a

• Lengthen clinical encounters and consider if the patient expects or desires more warmth in nonverbal and verbal behavior from clinicians

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Culture and Nonverbal Empathy in Clinical Settings handshake Smile and eye contact: can convey warmth. Clinician "coldness" can be interpreted by absence of a smile or eye contact

Pasco, A. C., et al. (2004)

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Qualitati ve

To identify FilipinoCanadian values that impact patient-nurse interactions

Touch by nurses helps develop trust in hospitalized Filipino patients. Patients experience a nurses' touch as conveying respect for the patient Eye contact: direct eye contact is valued; lowered eyes may mean respect or shame and is context-dependent. A head-to-toe gaze by a nurse can be perceived as demeaning

• Improve nurse awareness of use of gaze and touch to build relationships with hospitalized Filipino patients

NOTES: AA = African American, IEN = Internationally educated nurse, vs. = versus

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