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Increased Salivary Oxytocin and Empathy in Students of Clinical and Health


Psychology After a Mindfulness and Compassion-Based Intervention

Article  in  Mindfulness · April 2020


DOI: 10.1007/s12671-020-01316-7

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Mindfulness
https://doi.org/10.1007/s12671-020-01316-7

ORIGINAL PAPER

Increased Salivary Oxytocin and Empathy in Students of Clinical


and Health Psychology After a Mindfulness
and Compassion-Based Intervention
Miguel Bellosta-Batalla 1 & M. Carmen Blanco-Gandía 2 & Marta Rodríguez-Arias 1 & Ausiàs Cebolla 3,4 &
Josefa Pérez-Blasco 5 & Luis Moya-Albiol 1

# Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract
Objectives Mindfulness and compassion-based interventions (MCBI) have shown to be effective in increasing self-reported
empathy in healthcare professionals. However, no studies described a beneficial effect of MCBI on biological variables related to
empathy. In this study, we analyze the effects of an MCBI on the basal levels of salivary oxytocin (sOXT), empathic accuracy,
and self-reported empathy in students of clinical and health psychology (N = 90).
Methods In the experimental group (n = 37), an MCBI was applied. In the active control group (n = 27), students participated in
basic psychotherapeutic skills training. In the waiting list group (n = 26), students did not participate in any intervention. A
repeated-measures analysis of variance was performed, including pre- and post-intervention evaluations and the follow-up
evaluation.
Results Results indicate a significant interaction between the groups on the basal levels of sOXT (p = .045, ηp2 = .05) and
perspective taking (p = .040, ηp2 = .06), so that the experimental group showed increased sOXT at the end of the MCBI
(p = .009, d = .66) and in perspective taking on the follow-up evaluation (p = .001, d = .52).
Conclusions Introducing MCBI in the university education of clinical and health psychologists can help to improve their empathy
skills, which would ultimately have a beneficial influence on the health of the users of their services. Furthermore, sOXT could be
used as a valid biomarker in the study of the effects of MCBI on biological variables associated with empathy and affective bonds
in different settings.

Keywords Salivary oxytocin . Mindfulness . Empathy . Compassion . Clinical and health psychology

Empathy is the ability to infer the cognitive and emotional


state of others (cognitive empathy) and affectively synchro-
* Ausiàs Cebolla
nize with it (emotional empathy), inhibiting the appearance of
Ausias.Cebolla@uv.es
an affective fusion (Coutinho et al. 2014; Decety and Lamm
2009; Singer and Lamm 2009). Empathy has been associated
1
Department of Psychobiology, University of Valencia, with the success of psychological interventions (Norcross
Valencia, Spain
2011), by helping to establish a beneficial therapeutic bond
2
Department of Psychology and Sociology, University of Zaragoza, (Keijsers et al. 2000; Lambert and Barley 2001; Norcross and
Teruel, Spain
Wampold 2011). In this regard, patients’ evolution and symp-
3
Department of Personality, Evaluation and Psychological Treatment, tomatic relief have been related to perceived empathy from the
University of Valencia, Avda. Blasco Ibáñez, 21,
46010 Valencia, Spain psychotherapist caring for them (Elliott et al. 2011). The ef-
4 fective management of the emotions is essential in these situ-
Ciber Physiopathology of Obesity and Nutrition (CIBEROBN),
Institute of Health Carlos III, Madrid, Spain ations, because it facilitates a healthy bond and keeps the
5 psychotherapist from experiencing a response of empathic
Department of Evolutionary and Educational Psychology, University
of Valencia, Valencia, Spain distress due to coming into contact with others’ suffering
(Klimecki and Singer 2012).
Mindfulness

The importance of empathy in the field of psychotherapy 2016). However, most studies have only used self-reports to
points to the need to foster this ability in clinical and health evaluate empathy, even though some authors point out the
psychologists (Bohart and Greenberg 1997; Norcross 2011; limitations of this approach to the study of empathy, especially
Norcross and Wampold 2011). Various intervention strategies in individuals with high empathy levels, such as healthcare
have been designed to increase empathy in the university ed- professionals (Boellinghaus et al. 2014; Murphy et al. 2018;
ucation of healthcare professionals. These interventions em- Vachon and Lynam 2016). In this regard, empathy is a com-
phasize external and observable aspects of this skill, using plex phenomenon in which different biological, social, psy-
writing exercises, activities related to the dramatic arts, chological, and behavioral factors interact (Gonzalez-Liencres
problem-based learning, and training in social and communi- et al. 2013), so self-reported assessment is not always associ-
cation skills (Batt-Rawden et al. 2013; Teding van Berkhout ated with the individual’s empathy skills (Eyal et al. 2018).
and Malouff 2016). However, most of these interventions do Thus, there is a need to broaden these investigations through a
not include management of internal states and emotions, wide assessment of empathy that includes these factors, ap-
which is quite important in developing healthy and beneficial plying measures of empathic accuracy, in order to analyze the
empathy toward the patient (Coutinho et al. 2014). ability to infer others’ emotional states (Baron-Cohen et al.
In recent years, mindfulness and compassion-based inter- 2001), and focus on biological variables related to empathy
ventions (MCBI) have been established as an important strat- skills (Bachner-Melman and Ebstein 2014; Ebert and Brüne
egy in the healthcare field, due to their extensive benefits for 2018; Shamay-Tsoory and Abu-Akel 2016).
health and well-being (Bellosta-Batalla et al. 2018; Galante Regarding the abovementioned, in recent years, interest has
et al. 2014; Khoury et al. 2015). Likewise, some studies sug- grown in evaluating the levels of oxytocin and their involve-
gest the advantages of including MCBI in the university edu- ment in a series of skills related to empathy, such as emotional
cation of clinical and health psychologists, highlighting their recognition and social cognition (Gonzalez-Liencres et al.
effects on empathy skills (Bellosta-Batalla et al. 2019a; Bruce 2013; Patin et al. 2018). Oxytocin is a neuropeptide secreted
et al. 2010; Davis and Hayes 2011). In this regard, studies in the hypothalamus that acts as a hormone and neurotrans-
have found an association between mindfulness and empathy mitter and has a strong influence on stress buffering, sexual
in psychotherapists, as well as between these variables and the behavior, and social bonds (Ebert and Brüne 2018; Feldman
therapeutic alliance (Leonard et al. 2018) or patients’ symp- 2012; Patin et al. 2018). Although there are other neuropep-
tomatic evolution (Grepmair et al. 2007). tides involved in social behavior, such as vasopressin
Mindfulness is a mental state in which the individual inten- (Bachner-Melman and Ebstein 2014), we chose oxytocin in
tionally pays attention to what happens within and around this study because it modulates its own liberation but also
him/her, with an attitude of curiosity, openness, acceptance, vasopressin and opioid release (Kendrick 2000). Some studies
and kindness (Bishop et al. 2004; Kabat-Zinn 1990; Siegel point out that the intranasal administration of oxytocin in-
2007). These attitudes involve a healthy approach to experi- creases attention to socially relevant information (Hubble
ence, and they function as an implicit form of self-compassion et al. 2017), empathic accuracy (Bartz et al. 2010; Feeser
(Brito et al. 2018). Compassion is understood as a feeling that et al. 2015; Schulze et al. 2011), and emotional empathy
emerges in the presence of suffering – whether in ourselves or (Hurlemann et al. 2010). Hence, measuring salivary oxytocin
in others – helping us to be open to its appearance and attempt (sOXT) can be a useful strategy for studying the effects of
to relieve it (Elices et al. 2017; Gilbert 2005; Siegel and MCBI on biological variables related to empathy skills and
Germer 2012). Meditation practice in which there is an in- affective bonds. Some authors indicate that sOXT is not a
creasing mindfulness state may contribute to a stable trait reliable biomarker (Horvat-Gordon et al. 2005), even though
(Kiken et al. 2015), which is characterized by a greater regu- this evaluation procedure has been validated in human beings
lation of attention, an effective management of emotions, and (Carter et al. 2007) and analyzed satisfactorily in a large num-
an increase in interoceptive sensitivity and self-awareness ber of studies (Feldman et al. 2010; Lebowitz et al. 2016).
(Cebolla et al. 2018; Hölzel et al. 2011). These effects facili- Salivary OXT has been measured to evaluate the effects of
tate an open and kindly approach to others, and when they are different psychological interventions and exercises, which in-
sustained in the social area of the individual, they may exert a fluence beneficially to the biological system of oxytocin
positive influence on empathy skills (Bellosta-Batalla et al. (Holt-Lunstad et al. 2008; Nilsson 2009; Vittner et al. 2018).
2019b). Moreover, compassion is closely related to empathy In the field of psychotherapy, sOXT has been used to study the
because it involves a kind approach to the suffering of others development of the therapeutic alliance, establishing an asso-
(Brito 2014; Siegel and Germer 2012; Vivino et al. 2009). ciation between an increase in this biomarker in patients and
Current studies about the influence of MCBI on empathy episodes of rupture of the alliance (Zilcha-Mano et al. 2018).
reveal that these interventions increase the empathic attitudes In addition, these authors observed a general increase in sOXT
of healthcare professionals in general, and clinical and health in patients throughout the sessions. This indicates that oxyto-
psychologists in particular (Bibeau et al. 2016; Lamothe et al. cin is at the base of salient interpersonal interactions –
Mindfulness

regardless of their emotional valence – among which the es- based on the results of a meta-analysis focused on the effects
tablishment of empathy is included (Shamay-Tsoory and Abu- of MCBI on empathy (Luberto et al. 2018).
Akel 2016).
Mindfulness and compassion practice fosters a greater un- Procedure
derstanding of others’ emotions and a healthy management of
our affective state, facilitating empathy (Hölzel et al. 2011; The sample was recruited by announcing the study to different
Luberto et al. 2018). This emotional approach helps to im- groups of Bachelor and Master’s degree students in Clinical
prove interactions and social bonds, and it is a process in and Health Psychology at the University of Valencia (N =
which the biological system of oxytocin may be involved 163). In addition, we included a group of students enrolled
(Ebert and Brüne 2018; Gonzalez-Liencres et al. 2013; Patin in these degree programs who were going to perform basic
et al. 2018). Along these lines, it has been shown that oxytocin psychotherapeutic skills training as part of their study plan.
increases benefits in emotional states of mindfulness and lov- Different psychotherapy schools in Valencia (Spain) were
ing kindness meditation (Isgett et al. 2016; Van Cappellen contacted which accept these types of students to do their
et al. 2016), although a beneficial influence of MCBI on basal practical training. The study was advertised in three of the
sOXT levels has not been yet described. In fact, a study that schools whose training characteristics matched the MCBI in
analyzed the effects of a mindfulness-based intervention the number of students and frequency and length of the ses-
(MBI) using this biomarker did not find significant results; sions (N = 62). In both cases, a researcher went to the Bachelor
however, it was focused on improving sleep and included and Master’s classrooms, and to the psychotherapy schools, to
some variations on the usual MCBI (Lipschitz et al. 2015). explain the basic objectives of the study and to recruit the
Moreover, these authors observed an increase in the basal sample. The exclusion criteria applied were experience with
levels of sOXT when applying a mind–body bridging inter- meditation and/or previous participation in mindfulness or
vention that included some activities related to mindfulness. compassion training, eliminating six students from the sam-
Thus, MCBI would be expected to have a beneficial influence ple. Likewise, the other exclusion criterion applied was doing
on this biological marker. less than 300 min of meditation during the MCBI because this
Based on the above mentioned, the aim of this study was to was the time spent on the meditation exercises in the training
evaluate the efficacy of an MCBI in increasing basal sOXT sessions. Several information sessions were held with the in-
levels, empathic accuracy, and self-reported empathy in stu- terested students (N = 136) to explain the general lines of re-
dents of clinical and health psychology. We compared the search and MCBI content. The students who decided to par-
effects of MCBI to an active control group, in which students ticipate (N = 95) signed an informed consent form that speci-
participated in basic psychotherapeutic skills training, and a fied the study objective and guaranteed the anonymity and
waiting list group of students who did not participate in any confidentiality of the data. Moreover, they were told that sali-
intervention. We hypothesized an increase in these empathy va samples would be collected in the evaluation sessions. The
indicators in the students who participated in the MCBI, com- study was approved by the Ethics Committee of the
pared to the other groups. University of Valencia, and it was carried out in accordance
with the ethical standards for research in humans (World
Medical Association 2013).
The active control group was composed of students who
Method were going to begin the basic psychotherapeutic skills training
(n = 27). These students could not be randomly assigned be-
Participants cause their choices of practical training were made before the
study began and were integrated in their university education.
The sample in this study was composed of 90 students in the The rest of the students were randomly assigned to the exper-
last courses of the Bachelor and Master’s degrees in Clinical imental group (n = 42) and the waiting list group (n = 26).
and Health Psychology at the University of Valencia Groups were homogenous with regard to gender, age, and
(Valencia, Spain). Regarding sex, 76.7% of the participants academic level, as well as the sociodemographic variables
were women, and 23.3% men. The participants’ ages ranged evaluated. The experimental group (mindfulness and compas-
from 20 to 55 years, with a mean of 23.71 ± 5.30 years. sion, MC) was divided into two groups of 21 students who
Regarding their marital status, 82.2% were single, and participated in an MCBI. Two clinical and health psycholo-
17.8% lived with a partner. In addition, 93.3% rated their gists with extensive experience in the administration of mind-
social network as good and 6.7% did not. The size of the fulness and compassion training applied the intervention joint-
sample was determined with the G*Power program, estimat- ly in both groups. This intervention lasted for 2 months, with
ing the need to include 81 participants. An expected effect size one session per week that lasted approximately 2 h. These
of d = .40 (α = .05 and statistical power = .95) was taken, sessions dealt with the essential aspects of mindfulness and
Mindfulness

compassion, as well as the application of mindfulness atti- The participants were told not to eat or drink (except water),
tudes to the different contents of experience (feelings, smoke, or take any stimulants 60 min before the evaluation
thoughts, and emotions). In addition, they included two 20- sessions, in order to avoid their influence on the sOXT levels
min meditation exercises (at the beginning and end of the and the possible contamination of the saliva samples. The
session), and a series of weekly meditation exercises were students in the BPS group and the WL group were invited to
proposed (Table 1). The students kept a written record of the participate in a brief mindfulness and compassion training
amount of time they meditated per week. Based on this, five once the study had ended.
subjects from the MC group were eliminated from the study
for not doing enough minutes of meditation (n = 37). With Measures
regard to adherence to the MCBI, 13.5% of the students
attended five sessions, 29.7% attended six sessions, 43.2% Basal Levels of Salivary Oxytocin
attended seven sessions, and 13.5% attended the eight ses-
sions of the intervention. These students meditated for a mean Saliva samples were collected from the participants using
of 534.19 ± 208.85 min. During this period, the students in the Salivettes (Sarstedt, Rommersdolf, Germany). The saliva
active control group (basic psychotherapy skills, BPS) per- samples were frozen at − 20 °C immediately after their collec-
formed their practical training, attending one weekly session tion, and they were conserved in this state until their analysis
that lasted approximately 3 h. In these sessions, they studied in the laboratory. We have used the lyophilization process
psychotherapy theory from different approaches, and they per- instead of the chemical process outlined in the manufacturer’s
formed a variety of related activities, such as exercises simu- instructions, since lyophilize (freeze dry) samples effectively
lating clinical situations and observing psychotherapeutic and achieve a similar outcome (Blagrove et al. 2012; Daughters
supervision sessions. These practice sessions took place dur- et al. 2015). Lyophilization has been found to increase the
ing the 5-month period of the study. The control group validity of measuring oxytocin via EIA, although it has not
(waiting list, WL) did not participate in any intervention, been demonstrated to give the same results as extraction
and the students stayed on the waiting list in order to later (Christensen et al. 2014; Leng and Ludwig 2016;
participate in a brief mindfulness and compassion training McCullough et al. 2013). Samples were centrifuged 5 min ×
(Fig. 1). 1000 g, and then from each saliva sample, 1 ml of supernatant
An initial evaluation was performed before starting the in- was frozen at − 40 °C. The samples were lyophilized before
tervention in the MC group and the practical training in the their analysis through freeze-drying (Modulyo® Freeze
BPS group. The second evaluation took place at the end of the Dryers, Thermo Electron Corporation). The samples were
intervention in the MC group, with a follow-up evaluation freeze-dried for approximately 15 h and then dehydrated
3 months later. In the evaluation sessions, first, salivary sam- (Daughters et al. 2015). These samples were reconstituted in
ples were collected, and then the students performed an em- 250 μl of assay buffer following the manufacturers’ instruc-
pathic accuracy exercise and filled out an empathy self-report. tions, resulting in a concentration four times greater than the

Table 1 Mindfulness and


compassion-based intervention Content Weekly exercises
(MCBI)
Session 1 Introduction to mindfulness Full attention to eating
Breathing
Session 2 Basic attitudes Full attention to walking
Body scan
Session 3 Thoughts Full attention to sounds at different moments in the day
Sounds
Session 4 Thoughts II Full attention to thoughts
Mental scenario
Session 5 Emotions Full attention to emotions and their variability during the day
Labelling emotions
Session 6 Emotions II Full attention to emotion and its space in the body
Emotions in the body
Session 7 Self-compassion Loving kindness toward oneself when getting up in the morning
Loving kindness toward
oneself
Session 8 Compassion Generalization of the practice
Loving kindness toward others
Mindfulness

Students of Bachelor and Master’s degrees


in Clinical and Health Psychology
(N = 225)

Students who were Students who could be interested in


in the psychotherapy schools participate in the MCBI
(n = 62) (n = 163)

Excluded (n = 1) Excluded (n = 5)
Experience in meditation Experience in meditation

Attended the information sessions Attended the information sessions


(n = 30) (n = 106)

Students who decided to participate Students who decided to participate


(n = 27) (n = 68)

No random assignment Random assignment

Basic psychotherapy skills Mindfulness and compassion Waiting list


(BPS, n = 27) (MC, n = 42) (WL, n = 26)

Eliminated from the study


Not enough minutes of meditation
(n = 5)

Mindfulness and compassion


(MC, n = 37)

Fig. 1 Assignment of the participants to the study groups

original. Therefore, they would fall within the kit’s sensitivity concentration in the lyophilizer. Recovery was determined by
range and be detectable in the standard curve. The sOXT comparing the assay results from the spiked samples to those
levels were measured using the commercial kit Oxytocin for assay buffer spiked with the same volumes of standard.
EIA kit (Arbor Assays, Inc. Ann Arbor, MI, USA; ref.: Precision of the assay was assessed by the variability in mul-
K048), following the procedure described in previous studies tiple measurements of unknowns (intra-assay CV). A dilution
due to its high sensitivity to saliva samples (Carter et al. 2007; series of pooled saliva resulted in a displacement curve paral-
Lebowitz et al. 2016; MacLean et al. 2018). Neuropeptide lel to the standard curve (y = 1.10x − 6.61; r2 = 0.98). Tests of
cross-reactivity was reported by Arbor Assays as < 0.001%, quantitative recovery resulted in a high correlation between
and limit of detection was 11 pg/ml. The saliva samples were expected and observed values (y = 0.68x − 14.46; r2 = 0.998)
read at 450 nm and all samples were run in duplicate. The and average recovery was 74%. Inter and intra-assay CV av-
chemical validity of the EIA was assessed using tests of par- eraged less than 10%.
allelism by assay of a serial dilution of pooled saliva samples.
Quantitative recovery was examined to determine whether the Empathic Accuracy
sample preparation and lyophilization affected the results.
Salivary samples were spiked with varying amounts of stan- Empathic accuracy was evaluated with the Reading the Mind
dard of known concentration and then prepared for assay by in the Eyes Test (Eyes test; Baron-Cohen et al. 2001). This
Mindfulness

instrument is composed of 36 black-and-white photographs follow-up evaluation. We studied the main effect of “time”
showing the facial zone of the eyes of a series of actors. The (pre- versus post-intervention, and pre-intervention versus fol-
subject must infer the emotional state of the person observed, low-up) in the different groups (using the Bonferroni adjust-
choosing a response from different alternatives (Fig. 2). The ment), and the interaction effects (group x time). The
score on the Eyes test is calculated by adding up the number of Greenhouse-Geisser correction of the degrees of freedom
correct answers. was applied when necessary. The statistical analyses were
performed using the IBM SPSS (version 23).
Self-Reported Empathy

Self-reported empathy was evaluated with the Spanish version Results


of the Interpersonal Reactivity Index (IRI; Davis 1980; Mestre
et al. 2004). The IRI is a self-report with 28 items, rated on a 5- Influence of the MCBI on the Basal sOXT Levels
point Likert scale, from 1 (“Does not describe me well”) to 5
(“Describes me very well”). The IRI subscales are grouped No significant differences were observed in the basal sOXT
according to their cognitive or emotional nature. For the cog- levels (Fig. 3) between the groups before the intervention. In
nitive aspect, perspective-taking (spontaneous attempts to the MC group, there was a main effect of “time” on the basal
adopt the point of view of others in different situations) and levels of sOXT, F(2, 72) = 4.65, p = .013, ηp2 = .11, 95% CI
fantasy (tendency to identify with the feelings and actions of [.01, .25], with a significant increase between the pre- and
characters from films and literature in fictional situations) post-intervention values, p = .009, d = .66, 95% CI [.19,
were evaluated. For the emotional aspect, empathic concern 1.13]. In the BPS group, F(2, 52) = 3.12, p = .053, ηp2 = .11,
(feelings of compassion and concern about the suffering of 95% CI [.00, .26], and the WL group, F(2, 50) = .01, p = .994,
others) and personal distress (feelings of anxiety and discom- ηp2 = .00, 95% CI [.00, .01], no significant differences were
fort arising from observing others’ suffering) were evaluated, observed. The effect of the “group × time” interaction was
with the latter known as empathic distress. These subscales significant, F(4, 174) = 2.49, p = .045, ηp2 = .05, 95% CI
present good validity and variable reliability, with Cronbach’s [.00, .11].
alpha values (α) between .56 and .70. In this study, we con-
ducted reliability analyses in R to calculate the McDonald’s Influence of the MCBI on Empathic Accuracy
omega values (ω): perspective-taking (ω = .67, 95% CI [.54,
.76]), fantasy (ω = .79, 95% CI [.70, .84]), empathic concern In the case of empathic accuracy (Table 2), no significant
(ω = .65, 95% CI [.51, .77]), and personal distress (ω = .76, differences were observed between the groups before the in-
95% CI [.65, .82]). tervention. In the MC group, there was a main effect of “time”
on empathic accuracy, ɛ = .68, F(1.37, 49.19) = 3.72, p = .047,
ηp2 = .09, 95% CI [.00, .25], with a significant increase be-
Data Analyses tween the pre- and post-intervention values, p = .041, d = .40,
95% CI [− .06, .86]. In the BPS group, F(2, 52) = 2.64,
First, after assumptions of normality and homoscedasticity of p = .081, ηp2 = .09, 95% CI [.00, .24], and the WL group,
the variables were checked (using the Kolmogórov-Smirnov F(2, 50) = .53, p = .595, ηp2 = .02, 95% CI [.00, .12], no sig-
and Levene tests, respectively), an analysis of variance nificant differences were observed. The effect of the “group ×
(ANOVA) was carried out, to determine if there were signif- time” interaction was not significant, ɛ = .91, F(3.64,
icant differences between the groups before the intervention. 158.13) = .68, p = .590, ηp2 = .02, 95% CI [.00, .05].
Likewise, a repeated-measures ANOVA was performed, in-
cluding the pre- and post-intervention evaluations and the Influence of the MCBI on Self-Reported Empathy
Embarrassed Fantasizing
In relation to self-reported empathy (Table 2), no significant
differences were observed between the groups on the different
subscales evaluated before the intervention. In the MC group,
there was a main effect of “time” on the perspective-taking
subscale, F(2, 72) = 7.20, p = .001, ηp2 = .17, 95% CI [.03,
.30], with a significant increase between the pre-intervention
values and the follow-up values, p = .001, d = .52, 95% CI
[.05, .98]. Likewise, there was a main effect of “time” on the
Confused Panicked empathic concern subscale, F(2, 72) = 3.57, p = .033,
Fig. 2 Image and choice alternatives on the Eyes test ηp2 = .09, 95% CI [.00, .21], with a significant increase
Mindfulness

Fig. 3 Basal sOXT levels in the pg/mL


different groups pre- and post-
MCBI and in the follow-up
evaluation
200 *

150

Pre-MCBI
100 Post-MCBI
Follow-up

50

0
Mindfulness and Basic psychotherapy Waiting list (WL)
compassion (MC) skills (BPS)
*p < .05

between the pre-intervention values and the follow-up values, the pre-intervention values to the follow-up values, p = .026,
p = .040, d = .42, 95% CI [− .04, .88]. Finally, there was a d = − .46, 95% CI [− 1.00, .08]. On the perspective-taking,
main effect of “time” on the personal distress subscale, F(2, F(2, 52) = .14, p = .874, ηp2 = .01, 95% CI [.00, .07], and em-
72) = 4.81, p = .011, ηp2 = .12, 95% CI [.01, .25], with a sig- pathic concern, F(2, 52) = .49, p = .616, ηp2 = .02, 95% CI
nificant reduction from the pre-intervention values to the [.00, .11], subscales, no significant differences were observed.
follow-up values, p = .033, d = − .43, 95% CI [−.89, .03]. On In the WL group, no significant differences were observed
the fantasy subscale, no significant differences were observed, on any of the subscales: perspective-taking, F(2, 50) = .15,
F(2, 72) = 3.07, p = .053, ηp2 = .08, 95% CI [.00, .20]. p = .863, ηp2 = .01, 95% CI [.00, .08], fantasy, F(2, 50) = .93,
In the BPS group, there was a main effect of “time” on the p = .403, ηp2 = .04, 95% CI [.00, .15], empathic concern, F(2,
fantasy subscale, F(2, 52) = 4.67, p = .014, ηp2 = .15, 95% CI 50) = .13, p = .881, ηp2 = .01, 95% CI [.00, .07], and personal
[.01, .31], with a significant increase from the pre-intervention distress, F(2, 50) = .27, p = .762, ηp2 = .01, 95% CI [.00, .09].
values to the values from the second evaluation, p = .046, The effect of the “group × time” interaction was signif-
d = .39, 95% CI [− .15, .92], and from the pre-intervention icant on the perspective-taking subscale, F(4, 174) = 2.57,
values to the follow-up values, p = .041, d = .41, 95% CI p = .040, ηp2 = .06, 95% CI [.00, .11], but not on the other
[− .13, .95]. In addition, there was a main effect of “time” on subscales: fantasy, F(4, 174) = 1.95, p = .105, ηp2 = .04,
the personal distress subscale, F(2, 52) = 4.27, p = .019, 95% CI [.00, .10], empathic concern, F(4, 174) = 1.02,
ηp2 = .14, 95% CI [.00, .30], with a significant reduction from p = .397, η p 2 = .02, 95% CI [.00, .06], and personal

Table 2 Empathic accuracy (Eyes test) and self-reported empathy (IRI) in the different groups pre- and post-MCBI and in the follow-up evaluation

Mindfulness and compassion (MC) Basic psychotherapy skills (BPS) Waiting list (WL)

Pre-MCBI Post-MCBI Follow-up Pre-MCBI Post-MCBI Follow-up Pre-MCBI Post-MCBI Follow-up

M SD M SD M SD M SD M SD M SD M SD M SD M SD

Empathic accuracy
Eyes test 24.43 4.21 25.92 3.09 25.46 3.44 24.96 2.33 25.74 3.21 26.22 2.87 25.46 2.97 25.81 2.73 26.12 2.96
Self-reported empathy
Perspective-taking 27.73 3.84 28.51 3.69 29.62 3.39 27.74 3.38 27.67 3.27 27.41 4.10 28.54 3.50 28.77 3.96 28.50 3.37
Fantasy 25.84 5.09 26.95 4.66 27.30 4.35 25.81 4.35 27.63 4.92 27.70 4.79 27.69 4.99 26.88 4.85 27.73 5.10
Empathic concern 27.84 3.32 28.51 4.02 29.16 2.94 27.19 3.62 27.26 3.97 27.74 3.13 28.54 3.30 28.62 3.16 28.31 3.22
Personal distress 16.97 4.83 15.54 4.81 15.11 3.67 18.59 3.50 17.56 3.45 16.89 3.79 17.46 5.20 17.04 4.49 17.00 4.17
Mindfulness

distress, ɛ = .93, F(3.71, 161.43) = .73, p = .564, ηp2 = .02, bonds when attitudes related to them are applied in the
95% CI [.00, .05]. social area of the individual (Hölzel et al. 2011; Luberto
et al. 2018). These benefits are closely related to empathy
skills, and the biological mechanism of oxytocin may be
Discussion involved in them (Bachner-Melman and Ebstein 2014;
Gonzalez-Liencres et al. 2013; Shamay-Tsoory and Abu-
The aim of this study was to analyze the effects of an MCBI Akel 2016).
on the basal sOXT levels, empathic accuracy, and self- In addition to its influence on sOXT, the effect of the inter-
reported empathy of clinical and health psychology students, action on cognitive empathy was significant – and specifical-
compared to an active control group that participated in basic ly, on the perspective-taking subscale – so that in the MC
psychotherapeutic skills training and a waiting list group. group, there was a significant increase in the follow-up eval-
First, the results suggest that MCBI can be effective in increas- uation. These results are similar to those obtained in previous
ing the basal levels of sOXT because a significant increase in studies using a self-reported evaluation of empathy (Lamothe
sOXT was observed in the MC group at the end of the inter- et al. 2016). On empathic accuracy and the other self-reported
vention, compared to the other conditions. This increase was empathy subscales, the effect of the interaction was not sig-
not maintained in the follow-up evaluation, in which MC nificant. These results indicate that MCBI increased the ability
group showed similar basal sOXT levels that BPS and WL of students to take the perspective of others in the different
groups, suggesting that ongoing mindfulness and compassion interpersonal situations where they are involved, although this
practice is necessary in order to sustain the beneficial effects of may not influence on other aspects of their cognitive and
the MCBI. It is important to point out that at the beginning of emotional empathy skills (Eyal et al. 2018), including their
the study, the sOXT levels in the BPS group were fairly high; ability to infer affective states through facial expressions.
although they did not reach significant values, they declined However, when analyzing the evolution of the groups sep-
gradually in the following evaluations, approaching the base- arately, results are consistent with findings from previous re-
line levels of the MC and WL groups. These results can serve search, observing an increase in empathic accuracy at the end
as a reference for the general values of sOXT in this popula- of the MCBI and in self-reported empathy at the follow-up
tion because these students were randomly selected. evaluation in the MC group (Lamothe et al. 2016; Mascaro
Moreover, as expected, the sOXT levels in the WL group et al. 2013). On the fantasy subscale, there are no significant
did not vary in the different study evaluations, thus informing differences, although authors suggest interpreting it as an in-
us about the stability of this variable. It is possible that the high dicator of absorption, rather than empathy (Murphy et al.
baseline levels of sOXT in the BPS group are influenced by 2018). Moreover, the lack of significant interaction effect on
some unidentified variable that would be associated with their empathic accuracy and the emotional subscales may be ex-
expectations or interest in receiving training in basic psycho- plained by the variations observed in the BPS group, in which
therapy skills because there was no random assignment in this these skills were trained, as well as the low sensitivity to
group. Likewise, its decrease could be explained by habitua- change of the instrument used for its assessment
tion or adjustment of these expectations and interest through- (Boellinghaus et al. 2014; Murphy et al. 2018). Along these
out training in the psychotherapy schools. However, currently lines, mindfulness and compassion practice increases our at-
there is not enough research on sOXT in this area, which tention to the way we relate to ourselves and others (Elices
makes it difficult to attribute this result to any specific aspect. et al. 2017; Siegel 2007), which can mean that we are aware of
Analyzing the influence of the MCBI on the basal some already established interactions and bonds in which we
sOXT levels, we observe that the effect size on this var- are not empathic, helping us to adopt a more open and kind
iable was higher than described after a mind-body bridg- attitude toward our surroundings. However, this effect might
ing intervention, in which some mindfulness exercises not be immediately reflected in self-report evaluations. In re-
were included (Lipschitz et al. 2015) and after a “warm lation to the above, it is observed that the increase in cognitive
touch” support enhancement intervention (Holt-Lunstad and emotional empathy and the decrease in empathic distress
et al. 2008). Likewise, it was higher than described after in the students who participated in the MCBI did not occur
different exercises related to the biological system of oxy- until the follow-up evaluation; however, there was an increase
tocin, such as listening soothing music during bed rest in the basal levels of sOXT and empathic accuracy in the post-
(Nilsson 2009) or a skin-to-skin contact exercise between intervention evaluation. This result suggests that variations in
parents and infants (Vittner et al. 2018), so these results self-reported empathy require a longer time frame to occur,
are especially relevant. Mindfulness and compassion prac- because they need the application and consolidation of a series
tice fosters an increase in self-awareness and enhances of attitudes and states related to empathy held in the social area
sensitivity to our internal states and others’ emotions, pro- of the individual to become a stable trait. In addition, it would
ducing a beneficial influence on interactions and social explain the results of some studies that found no effects of
Mindfulness

MCBI on self-reported empathy, but did not include a follow- as the supervision of the psychotherapist or a personal analysis
up evaluation (Boellinghaus et al. 2014). – in addition to studying differences between MCBI and spe-
In summary, MCBI can be a useful alternative way to im- cific trainings designed to increase empathy skills (Batt-
prove empathy skills in the university education of clinical Rawden et al. 2013). Along these lines, in recent years, some
and health psychologists (Bruce et al. 2010; Davis and authors have expressed the need for new studies in this re-
Hayes 2011). These interventions are compatible with the dif- search field that would include an active control group to
ferent schools of psychotherapy because they help to develop analyze the effects of the MCBI on empathy skills (Kreplin
a series of skills underlying the practice of this profession, et al. 2018). We included this group, which allows us to com-
regardless of the theoretical approach on which they are based pare the effects of the MCBI to the effects of the practical
(Davis and Hayes 2011). Thus, MCBI has been shown to training currently offered by the university, instead of waiting
increase cognitive and emotional empathy and have a benefi- list or non-active control conditions, so this study increases the
cial influence on the healthy management of this affective evidence about the effects of MCBI on the biological variables
bond (Bibeau et al. 2016; Lamothe et al. 2016), which is associated with empathy skills and affective bonds.
especially important in the field of psychotherapy and facili- It is necessary to extend these results and analyze the
tates the establishment of the therapeutic alliance (Coutinho interaction of oxytocin with other biological aspects that
et al. 2014; Leonard et al. 2018; Norcross and Wampold can influence it, such as vasopressin levels (Bachner-
2011). The results of this study add to the current evidence Melman and Ebstein 2014), μ-opioids (Loseth et al.
about the influence of MCBI on empathy skills by finding an 2014), or dopaminergic system activity (Shamay-Tsoory
increase in the basal levels of sOXT, and applying an empathic and Abu-Akel 2016). In this regard, the use of sOXT as a
accuracy instrument, which has not been done in most previ- biomarker inherently showed several limitations. First,
ous studies (Lamothe et al. 2016). The study of these variables there is still some concern about the extent to which sOXT
is especially important because it helps to complement the is reflective of central oxytocin levels. To date, plasma oxy-
self-reported results obtained until now, increasing the evi- tocin is the most commonly used global biomarker of oxy-
dence about benefits of MCBI on empathy skills in clinical tocin activity (Crockford et al. 2014), but we have to con-
and health psychology students. In addition, these interven- sider that, like saliva, it is a peripheral measure and may
tions may be useful in other students in the health and educa- substantially differ from those of central oxytocin release
tional field, in which empathic skills are particularly relevant. (Valstad et al. 2017). Several studies have reported that oxy-
In this regard, sOXT could be used in the evaluation of the tocin is released in a coordinated fashion within the brain
benefits of MCBI on empathy skills and affective bonds in and from the posterior pituitary to the bloodstream
different areas, acting as a biomarker of the effects of these (Lebowitz et al. 2016; Neumann and Landgraf 2012),
interventions on the biological variables associated with this reaching the salivary glands by active transport mechanisms
skill, as occurs with other biological markers related to stress (Gröschl 2009; Proctor and Carpenter 2014). However, a
and health (Bellosta-Batalla et al. 2018; Black and Slavich recent meta-analysis revealed a positive correlation be-
2016; Sanada et al. 2016). tween plasma and central oxytocin concentrations only un-
der specific contexts, like stressful situations or after intra-
Limitations and Future Research nasal administration (Valstad et al. 2017). Secondly, recent
brushing or flossing may release blood into saliva, although
This study has some limitations. First, the sample receiving previous studies have shown that microinjuries in the oral
the intervention was mainly female, although this difference is mucosa have little effect on the reliability of other saliva
representative of students of clinical and health psychology. In assays (Kivlighan et al. 2004). Thirdly, oxytocin degrada-
addition, the students who were going to receive training in tion small molecules are present in saliva (Szeto et al. 2011)
the psychotherapy schools were not randomly assigned. and may overestimate circulating levels. We did not perform
Moreover, the intervention in the BPS group took place during an extraction procedure with our saliva samples before run-
the 5 months of the study, whereas the MCBI was only applied ning the EIA kit. Therefore, unextracted samples may lead
in the first 2 months, and no record of mindfulness and com- to increase signaling of oxytocin, as the antibodies used to
passion practice was collected from the end of the intervention perform immunoassay can bind to other proteins and pep-
until the follow-up evaluation, in order to avoid overloading tides. It has been reported that oxytocin levels of
participants. Likewise, it is important to highlight that the aim unextracted samples can be from 10- to 100-folds higher
of the sessions in the BPS group was to train students in basic than in extracted samples, which suggest that the assay is
psychotherapeutic skills, rather than establishing an individual detecting substances different from oxytocin (McCullough
space for introspection. Thus, in future studies, it would be et al. 2013; Saxbe and Mendez 2019). Although many re-
interesting to analyze the effects of MCBI compared to some searchers perform extraction to remove these additional
type of experiential approach that fosters introspection – such molecules, some studies have reported inconsistent findings
Mindfulness

regarding the relationship between extracted and Informed Consent Informed consent was obtained from all individual
participants included in the study.
unextracted samples for the measurement of peripheral oxy-
tocin levels (Robinson et al. 2014). In a recent study, oxy-
tocin was measured with and without extraction, and the
authors found that unextracted and extracted oxytocin were
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