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. 2021 Dec 2;16(12):e0260359. doi: 10.1371/journal.pone.0260359

Depression, anxiety, burnout and empathy among Spanish medical students

Patricia Capdevila-Gaudens 1, J Miguel García-Abajo 2, Diego Flores-Funes 3, Mila García-Barbero 4, Joaquín García-Estañ 5,*
Editor: Kamran Sattar6
PMCID: PMC8638989  PMID: 34855803

Abstract

Medical Education studies suggest that medical students experience mental distress in a proportion higher than in the rest of the population In the present study, we aimed to conduct a nationwide analysis of the prevalence of mental health problems among medical students. The study was carried out in 2020 in all 43 medical schools in Spain, and analyzes the prevalence of depression, anxiety, empathy and burnout among medical students (n = 5216). To measure these variables we used the Beck Depression Inventory Test for assessing depression, the Maslach Burnout Inventory Survey for Students was used for burnout, the State-Trait Anxiety Inventory (STAI) was used to assess anxiety state and trait and the Jefferson Empathy Scale 12 to obtain empathy scores. In relation to depression, the data indicate an overall prevalence of 41%, with 23.4% of participants having moderate to severe levels, and 10% experiencing suicidal ideation. Burnout prevalence was 37%, significantly higher among 6th year than among 1st year students. Anxiety levels were consistent with those reported previously among medical students (25%), and were higher than in the general population for both trait and state anxiety. The prevalence of trait anxiety was higher among women. Empathy scores were at the top end of the scale, with the highest-scoring group (>130) containing a greater percentage of women. Similarly to those published previously for other countries, these results provide a clear picture of the mental disorders affecting Spanish medical students. Medicine is an extremely demanding degree and it is important that universities and medical schools view this study as an opportunity to ensure conditions that help minimize mental health problems among their students. Some of the factors underlying these problems can be prevented by, among other things, creating an environment in which mental health is openly discussed and guidance is provided. Other factors need to be treated medically, and medical schools and universities should therefore provide support to students in need through the medical services available within their institutions.

Introduction

Depression is highly prevalent in our society, with an estimated 300 million people suffering from this disease [1]. In the general population, depression also affects young people and specifically medical students. Indeed, depression is the second leading cause of death among those aged between 15 and 34 years, the age range to which most medical students belong [2]. Medicine is one of the most demanding university degree courses and mental disorders are more frequent among medical students than is generally recognized. Not only depression has been frequently found in medical students. Burnout and anxiety are also important problems frequently addressed in the medical education field. Some factors that may affect the mental health of this population include high academic work load, proximity to patients’ suffering, limited social life, poor family life, lack of sleep, and inconsistent and distant romantic relationships, among others. These factors can be seen as obstacles that test medical students during their training stage, setting them apart from other university students. A recent JAMA meta-analysis [1] found that 27% of 122,356 participating medical students had depressive symptoms, a higher proportion than in the general population. This exhaustive work, which analyzed a total of 168 cross-sectional and 16 longitudinal studies from 43 different countries, also provided data about suicidal ideation (11.1%). Unfortunately, these authors were unable to include any publications focusing on medical students in Spain, due to the scarcity of studies in this field.

A search in PubMed (October 6, 2020) revealed 859 articles featuring the Spanish word for "depression" and 517 featuring the Spanish term for “medical students". The union of the two terms returned only one record. The same search in EBSCO Health Sciences returned only one article that measured academic stress during the exam period. A search using the popular Google engine, however, revealed several studies not published in scientific journals; all were local analyses and reported prevalence data for poor mental health (anxiety and depression) of between 25% and 47% [36].

This study therefore aims to conduct a nationwide analysis of the prevalence of mental health problems among medical students. The project was approved by the Spanish Council of Medical Students (CEEM) in December 2019. As the representative of all medical students in Spain, the participation of the CEEM in the project was essential, since it ensured data were collected from a significant proportion of this population. The project, called DABE (standing for Depression, Anxiety, Burnout and Empathy, the four variables analyzed), was therefore established with the aim of determining the prevalence of these mental variables among medical students from all 43 medical schools in Spain.

Medical training in Spain follows the so-called Bologna Scheme, with 6 years of theoretical and practical training in a medical school, comprised of two basic years (1st and 2nd), a third one also basic that includes an introduction to clinical specialities, two mainly clinical years (4th and 5th) and a final 6th year, a whole clinical practical year composed of rotations in hospital services and primary care centers. In that way, medical training is usually referred as to having two cycles, a preclinical one (first three years) and a clinical cycle (last three years).

Methods

The DABE project was a multi-center cross-sectional study. All the procedures carried out complied with the 1964 Declaration of Helsinki [7] and were approved by the Ethics Committee of the University of Murcia. The instrument used was a self-administered survey developed from a web questionnaire in Google Forms, based on a previously published questionnaire. The authors of the original questionnaire gave their explicit consent for its use [8]. The participants, all medical students, were recruited through text messages sent by the Student Delegation Offices in each Faculty. They also gave their informed consent before completing the survey. Participation was voluntary and anonymous, and no financial remuneration was offered. The survey was active between February 17 and March 5, 2020. At that time, we estimate the total number of university undergraduates studying medicine in Spain around 42,000 subjects.

Questionnaire

The questionnaire was divided into three parts and administered in spanish. The first part included sociodemographic and academic questions (age, year of degree course, gender, scholarship, sexual orientation, percentage of attendance at activities and part-time or full-time job). The second part comprised the DABE variables that were the object of study. To measure these variables we used the Beck Depression Inventory Test (BDI-II), a 21-question multiple-choice instrument, one of the most used psychometric scales for assessing depression [9]. Burnout was analyzed by the Maslach Burnout Inventory Survey for Students (MBI-SS) [8, 10], a tool with 15 items [8, 10]. The State-Trait Anxiety Inventory (STAI), an instrument with 20 items [11] was used to assess anxiety state (in the moment of the test or STAI-Y1) and trait (feelings habitually, STAI-Y2). Finally, the Jefferson Empathy Scale [12] was used to obtain empathy scores The scale is made up of 20 items with scoring using a 7-points Likert scale and ten of the 20 questions are valued negatively (and rectified positively in the subsequent analysis), in order to reduce the effect of acquiescence when responding. The range of possible scores goes from 20 to 140 points. The highest scores are associated with a greater degree of empathy. The third part of the questionnaire focused on potential predictors, such as academic and curricular performance and some items covering recently (previous 6 months) perceived difficulties or problems with substance abuse, skills/organization, learning, relationships, health, psychological help, social support, and adverse life events.

Cutoff values and ranges

  • Depression. For the BDI-II we used the original scoring range [9], which runs from 0 to 63. Participants are classified as having no/minimal (0–13), mild (14–19), moderate (20–28), or severe depression (29–63).

  • Burnout. The three dimensions of burnout, emotional exhaustion (EX), cynicism (CY) and academic inefficiency (AI) were assessed using the MBI-SS [8, 10]. According to Galán et al. [10], the lower and upper quartiles of each burnout dimension are EX = <1.2 and = >2.8; CY = <0.6 and = >2.25; and AI = <3.84 and = >5.16. In our study, high scores on the exhaustion and cynicism subscales were considered to indicate burnout.

  • Anxiety. The STAI scale [11] was used to identify individuals with high anxiety levels. It measures two types of anxiety–state anxiety, or anxiety about an event, and trait anxiety, or anxiety level as a personal characteristic. Higher scores are positively correlated with higher levels of anxiety. According to their scores, participants were classified as having very low (score 20–31), low (score 32–43), moderate (score 44–55), high (score 56–67), and very high (score 68–80) anxiety. A distinction was made between participants in the first two categories (no anxiety) and those in the latter three (suffering from anxiety), by using p75 (75th percentile).

  • Empathy. It was measured using the Jefferson Empathy Scale [12], with the total empathy score being the sum of all the item scores up to a maximum possible score of 140. Higher scores represent a more empathetic orientation. In our study, scores of over 130 were considered indicative of high empathy (percentile 80).

Psychometric properties

All the tests used have been previously analyzed both in the general population and specifically in medical students, and found to have good psychometric properties. For instance, Galán et al [10] for Burnout, Tempski et al [13] for Anxiety, Silva et al [8] for Depression and both Ferreira-Valente et al [14] and Blanco et al [15)] for Empathy.

Statistical analysis

First, descriptive statistics were calculated for all the variables studied, with qualitative variables being expressed in terms of absolute and relative frequency (percentages). Quantitative variables were expressed as means and standard deviations, or medians and interquartile ranges (IQR), depending on whether or not they followed a normal distribution (according to the Kolmogorov-Smirnov test). Subsequently, the inferential statistics were calculated through a series of bivariate analyses designed to test all variables in accordance with gender (female or male), year of degree (1st to 6th), Burnout Traits (Yes/No), Depression (No/Mild/Moderate/Severe), Empathy (Yes/No), Anxiety (State, Y1, Yes/No) and Anxiety (Trait, Y2, Yes/No), obtaining the Pearson’ chi square. Finally, a multivariate analysis with binary logistic regression was performed for each of the main study variables, taking the main variable as the dependent variable (Burnout Yes/No, Depression Yes/No, Empathy Yes/No, Anxiety (State, Y1) Yes/No and Anxiety (Trait, Y2) Yes/No) and variables for which statistically significant results (p<0.05) had been found previously in the bivariate test or those with special relevance due to their relationship with the dependent variable, as independent variables. The results were expressed in terms of the odds ratio of each independent variable, with a 95% confidence interval. Cronbach’s alpha coefficient was also calculated as a means of determining internal consistency. IBM SPSS Statistics (version 24) was used for the calculations. A p-value of <0.05 was considered indicative of statistical significance.

Results

A total of 5,216 students completed the survey; 76.3% were women, 22.9% men, 0.5% preferred not to say and 0.3% identified themselves as “other”. The mean age (and standard deviation) of all the participants was 21.41 ± 3.44. In men, it was 21.76 ± 3.73 (IC95%, 21.6–22.0) and 21.3 ± 3.13 in women (IC95%, 21.2–21.4).

Academic and sociodemographic data (Table 1)

Table 1. Sociodemographic and general academic data.

Frequency Percentage
Sex Man 1195 22,9
Woman 3979 76.3
I prefer not to say 24 0.5
Year of study 1st 1063 20.4
2nd 985 18.9
3rd 929 17.8
4th 841 16.1
5th 885 17.0
6th 513 9.8
Approximate percentage of attendance to non-compulsory classroom teaching activities <10% 530 10.2
10–25% 549 10.5
25–50% 593 11.4
50–75% 790 15.1
75–90% 1180 22.6
>90% 1574 30.2
Besides studying, do you work? No 4428 84.9
Yes, full time 61 1.2
Yes part time 727 13.9
Do you have a scholarship of any kind? No 3511 67.3
Yes 1705 32.7
Sexual orientation Heterosexual 4029 77.2
Homosexual 254 4.9
Bisexual 737 14.1
I prefer not to say 196 3.8

The sample was drawn from all 43 medical schools in Spain, with an average of 121.3 responses per school. In relation to degree year, the highest percentage of participants were in their 1st year (20.4%), with the percentages decreasing progressively after that. As regards the percentage of engagement in non-compulsory teaching activities, over 67% of participants claimed to attend more than 50% of these classes, and 30% said they attended over 90% of them. The highest percentage of attendance was found in the 1st year of the degree course, with 43% attending more than 90% of the classes (data not shown). Most (85%) participants did not have a job; 32.7% had a scholarship of some kind and 67.3% did not, with this latter group (data not shown) having significantly more men (35.7%) than women (31.8%). Students from the 1st year of the degree course had the highest percentage of scholarships (43%), with this figure being around 30% in subsequent years (data not shown). In relation to sexual orientation, 77% identified themselves as heterosexual, 14.1% as bisexual, 4.9% as homosexual and 3.8% preferred not to answer. The percentage of those identifying themselves as homosexual was significantly higher in men (14.6%) than in women (1.9%), whereas the percentage of women who identified themselves as bisexual was significantly higher (14.6% as compared to 11.4% among men). These last data are not shown.

Perceived mental health (Table 2)

Table 2. Percentages of DABE variables in men and women.

Men
DEPRESSION No/Minimal Mild Moderate Severe
1st 72,07 % 13,06 % 8,11 % 6,76 %
2nd 68,32 % 13,86 % 10,89 % 6,93 %
3rd 63,72 % 15,81 % 10,70 % 9,77 %
4th 60,48 % 16,67 % 12,38 % 10,48 %
5th 63,59 % 18,89 % 9,22 % 8,29 %
6th 72,09 % 10,85 % 8,53 % 8,53 %
Mean 66,36 % 15,15 % 10,04 % 8,45 %
Women
DEPRESSION No/Minimal Mild Moderate Severe
1st 63,23 % 15,57 % 12,46 % 8,74 %
2nd 53,85 % 18,46 % 14,23 % 13,46 %
3rd 51,84 % 19,12 % 17,28 % 11,76 %
4th 55,04 % 17,76 % 16,64 % 10,56 %
5th 58,75 % 19,48 % 11,87 % 9,89 %
6th 58,78 % 21,81 % 11,97 % 7,45 %
Mean 56,92 % 18,35 % 14,17 % 10,56 %
ANXIETY state All Men Women
1st 26,90 % 27,48 % 26,71 %
2nd 25,79 % 27,72 % 25,26 %
3rd 25,62 % 20,00 % 26,91 %
4th 22,71 % 23,33 % 22,40 %
5th 21,92 % 19,35 % 22,83 %
6th 24,56 % 23,26 % 25,27 %
Mean 24,71 % 23,51 % 25,01 %
ANXIETY trait All Men Women
1st 21,54 % 18,47 % 22,51 %
2nd 22,03 % 18,81 % 22,82 %
3rd 23,90 % 19,53 % 24,93 %
4th 20,21 % 16,19 % 21,76 %
5th 21,02 % 16,59 % 22,37 %
6th 19,30 % 13,18 % 21,28 %
Mean 21,53 % 17,41 % 22,74 %
BURNOUT All Men Women
1st 22,58 % 22,52 % 22,40 %
2nd 35,23 % 29,70 % 36,67 %
3rd 38,21 % 34,42 % 39,38 %
4th 39,60 % 36,67 % 40,48 %
5th 46,67 % 48,85 % 46,12 %
6th 44,83 % 40,31 % 46,28 %
Mean 36,77 % 35,06 % 37,22 %
EMPATHY All Men Women
1st 14,02 % 13,51 % 14,13 %
2nd 15,33 % 7,92 % 17,31 %
3rd 20,02 % 11,16 % 22,80 %
4th 19,98 % 12,86 % 22,56 %
5th 22,03 % 14,29 % 24,51 %
6th 26,12 % 23,26 % 27,66 %
Mean 18,85 % 13,22 % 20,61 %
  1. Depression: The mean value was 13.46 ± 10.61, with a 95% CI from 13.17 to 13.75. A total of 41% of students reported some symptoms of depression and the percentage of women was significantly higher (43.1%) than that of men (33.6%). Moreover, 17.6% were found to have mild depression, 13.2% moderate depression and 10.2% severe depression, with all percentages being higher among women. In relation to question 9 of Beck’s test (suicidal ideation), 89% claimed not to have had ideas about harming themselves, although the rest (11%) did acknowledge suicidal ideation to varying degrees.

  2. Anxiety: 24.7% of students had high anxiety at the time of the survey (state), while 21.5% had high levels of anxiety on a regular basis (trait). The percentage of women with trait anxiety was significantly higher than that of men. No significant differences were observed between students in different years of their degree course.

  3. Burnout: 36.8% of participants had high burnout, defined as high scores for two of its components (exhaustion and cynicism). No differences were observed between men and women. The percentage of high burnout increased progressively from 1st (23%) to 6th (45%) year.

  4. Empathy: The mean numerical value for this variable was 120.6 ± 11.8 points (maximum 140), with 18.8% of participants having high levels of empathy (>130). The percentage of women was significantly higher than that of men, and percentages increased progressively year by year (from 14% in the 1st to 26% in the 6th year of the course).

Bivariant analysis between mental variables (Table 3)

Table 3. Association between variables.

DEPRESSION HIGH ANXIETY STATE HIGH ANXIETY TRAIT HIGH BURNOUT HIGH EMPATHY
NO YES Chi2 p level NO YES Chi2 p level NO YES Chi2 p level NO YES Chi2 p level NO YES Chi2 p level
Depression Yes - - - 1623–41.3% 518–40.2% 0.469 1514–37.0% 627–55.8% 0.000 809–24.5% 1332–69.4% 0.000 1783–42.1% 358–36.4% 0.001
Anxiety (State) High 771–25.1% 518–24.2% 0.469 745–18.2% 544–48.4% 0.000 824–25.0% 465–24.2% 0.55 1047–24.7% 242–24.6% 0.94
Anxiety (Trait) High 496–16.1% 627–29.3% 0.000 579–14.7% 544–42.2% 0.000 614–18.6% 509–26,5% 0.000 910–21.5% 213–21.7% 0.907
Burnout High 586–19.1% 1332–62.2% 0.000 1453–37.0% 465–36.1% 0.55 1409–34.4% 509–45.3% 0.000 1561–36.9% 357–36.3% 0.743
Empathy Yes 625–20.3% 358–16.7% 0.001 741–18.9% 242–18.8% 0.94 770–18.8% 213–19.0% .907 626–19.0% 357–18.6% 0.743

Data are number and percentage.

Depression was significantly related to anxiety trait, burnout and empathy, so that individuals having signs of depression had greater levels of anxiety trait and burnout but lower empathy levels. Having anxiety state was related only to high anxiety trait. High anxiety trait was significantly associated with depression, anxiety state and burnout, thus individuals with high anxiety trait had greater levels of these three variables. Burnout was significantly associated with both depression and anxiety trait, whereas empathy was significantly related only to depression, so that high empathic individuals showed lower depression signs.

Potential risk predictors (Table 4)

Table 4. Predictive factors.

Frequency Percentage
Problems or difficulties encountered Academic time management 3938 75.5%
Academic performance 3250 62.3%
Physical health 2935 56.3%
Task organization 2535 48.6%
Money management 1759 33.7%
Family relationships 1596 30.6%
Colleagues relationships 1533 29.4%
Partner relationships 1207 23.1%
Death of a family member 846 16.2%
Tobacco abuse 361 6.9%
Teachers relationship 304 5.8%
Alcohol abuse 242 4.6%
List of events Serious illness or accident in someone close to me 1309 25.1%
Economic problems 1131 21.7%
End of a stable love relationship 896 17.2%
Serious illness or accident of mine 506 9.7%
Abuse of other drugs 100 1.9%
Social support 1. How many people are you close enough to if you experience serious personal problems? >5 2122 40.7%
3–5 2079 39.9%
1 o 2 948 18.2%
None 67 1.3%
Social support 2. What is your interest and participation in your everyday experiences? Much 1963 37.6%
Something 1849 35.4%
I don’t know 868 16.6%
Little 483 9.3%
None 53 1.0%
Social support 3. How satisfied are you with the social activities you currently participate in? Much 1815 34.8%
Something 1878 36.0%
I don’t know 483 9.3%
Little 858 16.4%
None 182 3.5%
Social support 4, At this moment, how satisfied are you with the support you receive from your social relationships? Much 2407 46.1%
Something 1575 30.2%
I don’t know 493 9.5%
Little 601 11.5%
None 140 2.7%
Academic performance 1. Academic classification in relation to the effort made in the course Lower than the effort made 2528 48.5%
Concordant effort 2390 45.8%
Greater than the effort made 298 5.7%
Academic performance 2. Satisfaction with academic grades at this time Very much satisfied 493 9.5%
Satisfied 2214 42.4%
Little satisfied 1810 34.7%
No satisfied 699 13.4%
Academic performance 3. Level of satisfaction of your parents with your academic performance Very much satisfied 2422 46.4%
Satisfied 1915 36.7%
Little satisfied 638 12.2%
No satisfied 241 4.6%
Tobacco smoker Yes 407 7.8%
No 4392 84.2%
Ocassional 417 8.0%
Cannabis smoker No, never 3135 60.1%
I have tried 1782 34.2%
Ocassionally, < = 1 per week 227 4.4%
Habitually, 2 or more times per week 68 1.3%
Alcohol Never 829 15.9%
1 or less a month 1762 33.8%
2–4 a month 1984 38.0%
2 a week 526 10.1%
More than 3 a week 115 2.2%
Psychopharmaceuticals Yes 1063 20.4%
No 4153 79.6%
Tranquilizers / Anxiolytics 851 16.3%
Mood stabilizers 28 0.5%
Antidepressants 532 10.2%
Neuroleptics / antipsychotics 57 1.1%
Other 121 2.3%

The main problem or difficulty perceived by medical students was how to organize academic work (time management), with the percentage of women being significantly higher than that of men (77% vs. 70%). Academic performance problems varied across the years of the degree course, with peaks among students in their 2nd, 3rd and 4th years. In relation to events that had occurred over the past 6 months, 25% of participants mentioned someone important to them having had a serious illness or accident, with no differences observed in this sense between men and women. Moreover, 21.7% mentioned financial problems, 17% the end of a stable romantic relationship and 16% the death of a family member. Just under 10% mentioned having had a serious personal illness or accident (9.7%).

In relation to social support, almost 80% said they had more than 3 people they could count on if they had serious personal problems, with no differences being observed between men and women. The percentage of students with more than 5 people they could count on increased the further along on their degree course they were.

In terms of interest and participation in daily experiences, almost 10% claimed to have little or no interest, with this percentage being significantly lower among women. One fifth (20%) reported gaining little or no satisfaction from the social activities in which they participated and 13% reported receiving little or no support from their social relationships, with no differences being observed between men and women in these last two cases.

As for academic performance, almost 50% of students claimed to have grades that were lower than they had expected given the effort made, and considered themselves to be little or not at all satisfied with their current academic performance.

Drugs and substance abuse (Table 4)

Of the sample, 16% said they smoked, with this percentage being higher among men (20%) than among women (14%), and increasing as students progressed through their degree. As regards cannabis, 60% claimed never to have tried it and 1.3% said they used it habitually, with this percentage being higher among men than in women and also increasing over time (data not shown). Just over a tenth of all participants (12%) reported consuming alcohol two or more times per week, with this percentage again being higher among men (18%) than among women (10%). One fifth (20%) of participants reported taking psychotropic drugs, mainly anxiolytics (16.3%) and antidepressants (10.2%). Women took more psychotropic drugs (21%) than men (16%) and those in later years of the degree course took more than their counterparts in earlier ones, with the percentage increasing from 13% in the 1st to 23% in the 6th year of the course in relation to anxiolytics, and from 7% to 12% in relation to antidepressants.

Multivariable relationships between DABE variables and risk predictors

Tables 5 to 8 show the strength of association among the DABE variables and between them and the risk factors studied. Only factors found to be significant are included. In the case of depression (Table 5), low interest and participation in daily activities were the main risk factors (associated with a five-fold risk of having depressive symptoms, with a range of 3.8 to 6.8), followed by high burnout and physical health problems, to cite only the first three. The odds ratio for burnout (Table 6) again revealed an association with depression (odds ratio of 4), with academic performance problems and engaging in clinical rotations being the following two most important factors. The odds ratio values for anxiety (Table 7) indicated that both types, trait and state, were closely related to each other, as well as to working while studying and having financial problems. Finally, as shown in Table 8, empathy was closely associated with being a woman, engaging in clinical rotations and having a high level of social support.

Table 5. Risk factors for depression.

DEPRESSION P value Odds Ratio I.C. 95% for Odds Ratio
Lower Upper
Low interest and participation in daily activities <0.001 5.115 3.836 6.819
High Burnout <0.001 3.739 3.207 4.359
Physical health problems <0.001 2.673 2.292 3.116
Low satisfaction with academic grades <0.001 2.208 1.896 2.571
Take psychotropic drugs <0.001 2.185 1.819 2.624
Problems of relationship with colleagues <0.001 2.097 1.785 2.463
Academic performance problems <0.001 1.994 1.683 2.362
Problems of relationship with family <0.001 1.921 1.637 2.253
High Anxiety (Trait) <0.001 1.780 1.472 2.153
Problems of relationship with partner <0.001 1.767 1.485 2.102
Being woman <0.001 1.561 1.295 1.882
Academic homework organization problems <0.001 1.469 1.263 1.708
Homo-bisexual orientation <0.001 1.442 1.212 1.716
Habitual tobacco use 0.011 1.300 1.062 1.592
Academic work organization problems 0.024 1.241 1.029 1.496
Academic homework organization problems <0.001 1.469 1.263 1.708
4th-6th year 0.004 .797 .684 .928

Table 8. Risk factors for empathy.

EMPATHY P value Odds Ratio I.C. 95% for Odds Ratio
Lower Upper
Being woman <0.001 1.726 1.435 2.077
4th-6th year <0.001 1.503 1.306 1.730
High social support 3 <0.001 1.430 1.106 1.847

Table 6. Risk factors for burnout.

BURNOUT P value Odds Ratio I.C. 95% for Odds Ratio
Lower Upper
Depression symptoms <0.001 3.770 3.242 4.385
Problems of academic performance <0.001 2.163 1.851 2.528
4th-6th year <0.001 1.895 1.653 2.173
Academic satisfacción lower to effort <0.001 1.713 1.496 1.961
Low satisfaction with social activities <0.001 1.667 1.411 1.969
Taking psychopharmaceuticals <0.001 1.431 1.217 1.682
Academic homework organization problems <0.001 1.387 1.167 1.649
Physical health problems 0.001 1.292 1.117 1.494
Homo-bisexual orientation 0.004 1.259 1.078 1.469
High Anxiety (Trait) 0.034 1.206 1.014 1.435
Problems of relationship with family 0.026 1.181 1.020 1.366
Assistance to no compulsory activities >50% 0.001 0.785 0.682 0.904

Table 7. Risk factors for anxiety.

ANXIETY-STATE P value Odds Ratio I.C. 95% for Odds Ratio
Lower Upper
High Anxiety Trait <0.001 6.621 5.322 8.238
Work in addition to studying 0.002 1.540 1.166 2.033
Money management problems 0.026 1.290 1.031 1.614
4th-6th year 0.004 0.721 0.575 0.903
Low social support 3 <0.001 0.551 0.404 0.752
ANXIETY-TRAIT P value Odds Ratio I.C. 95% for Odds Ratio
Lower Upper
High Anxiety State <0.001 6.748 5.395 8.441
Depression symptoms <0.001 1.737 1.432 2.106

Discussion

In this study, which was carried out in 2020 in all 43 medical schools in Spain, we analyze the prevalence of depression, anxiety, empathy and burnout among medical students, in the first nationwide analysis of these mental health variables in this particular population. Although previous studies in this field have reported findings from some isolated university centers [36], ours is the first to offer global data from across the entire country. Moreover, the sample (5,216 participants) is large enough to endow the data presented here with a high degree of reliability, thereby enabling conclusions to be drawn. At present, the total number of university undergraduates studying medicine in Spain is close to 42,000, since around 7,000 freshmen began their studies in September 2019 [16]. This means that our sample represents around 12% of the total number of medical students in Spain. It is also important to highlight the fact that the survey, which was carried out at the beginning of the second semester, includes responses from students studying at all 43 medical schools operating at that time in Spain. We therefore believe that the number of participants may reflect the true situation of the problem in Spain medical training.

In relation to depression symptoms, the data indicate an overall prevalence of 41%, with the figure for moderate and severe depression being 23.4%. These findings are similar to those reported in the local studies cited above, being slightly lower than the figure reported for 4th year students at Catalonian medical schools (47%) [3] and practically identical to those found at the Universities of Murcia and Valencia [46]. In all these studies, as in the present work, depression was found to be more prevalent among women than among men. This is consistent also with the data reported in practically all international studies carried out on this topic [1]. Our results for depression symptoms are also consistent with those published recently in relation to some Italian medical schools, as well as with the findings of systematic reviews in both Europe and worldwide [1719]. We can therefore conclude that Spanish medical students behave similarly to their counterparts in other countries, indicating a certain degree of constancy in terms of problems or inductive factors throughout university centers worldwide. Our findings are also consistent with previous research reporting that the prevalence of depression symptoms is higher among medical students than in the general population, and also higher among women. For instance, in Spain, according to data from the 2017 National Health Survey [20], depression is more than twice as prevalent among women in the general population (9.2%) than among men (4%). In relation to the prevalence of depression symptoms among university students from disciplines other than medicine, the data are inconclusive [21], with percentages being either similar or lower [22]. Two of the most important factors associated with depression in our study were health issues and dissatisfaction with academic performance, which may well be the cause of the problem, while others such as lack of interest and participation in daily activities and consumption of psychotropic drugs may be its consequences.

One important finding in relation to the study of depression is the percentage of suicidal ideation found among Spanish medical students, in relation to which our results are consistent with those published previously [1, 36]. As stated earlier, around 10% of medical students admit to having engaged in suicidal ideation, a figure that indicates an urgent need to establish preventive measures and improve students’ access to advice, care and treatment to help them overcome this problem. Unfortunately, there are around 3,500 suicides every year in Spain (3,539 in 2018), of which 7% are young people between the ages of 15 and 29 [23]. However, no data is available on specific suicide rates among university students [24], although higher suicide rates have been reported among physicians than among the general population (1.3% as opposed to 0.8%) [25].

Regarding burnout, our data are consistent with those found among 3rd and 6th year medical students from a Spanish university [6], among which burnout risk was significantly more prevalent among 6th year students (37.5%) than among those in their 3rd year of training (14.8%), with no association being found between burnout and gender. In our study, burnout scores increased after the 1st year of the medical degree, with the highest scores being found in the 5th year. However, the means were very similar (around 35%), suggesting that the prevalence of burnout among medical students is fairly similar to that found among medical residents and practicing physicians [26, 27]. We identified several factors that may contribute to burnout among medical students, including curricular factors, personal life events, and the learning environment [14, 28, 29]; and burnout in turn may have serious consequences, leading to unprofessional conduct, increased risk of suicidal ideation, and serious thoughts of dropping out of medical school. However, some authors have suggested that burnout among medical students may be reversible, with 26% of sufferers recovering within a year [28]. We therefore believe it is vital to identify and treat students suffering from this syndrome before they begin their medical residencies.

In relation to empathy, the scores obtained by our sample were at the upper end of the scale [12, 15] and the mean value observed is consistent with that reported by previous studies both in Spain and abroad [15, 3033], and even slightly higher than in some. As stated in the Results section, women scored higher than men, as did those engaging in clinical rotations and those with strong social support, as indeed has been reported previously by other authors [34, 35]. It therefore appears that empathy levels increase over time and specially when students enter into contact with patients during their clinical rotations [36, 37].

The anxiety levels found in our study are consistent with the values reported previously [7, 11] among medical students, and are higher than in the general population in both categories or scales (trait and state). Furthermore, the greater prevalence of trait anxiety among women observed in our results has been also reported previously [11, 38, 39]. In relation to risk factors, the two categories were closely related to each other, and state anxiety particularly was very frequent among students who worked while studying, as well as among those experiencing financial difficulties. Finally, although no statistical differences were observed between students on different years of the degree course, those engaging in clinical rotations did seem to be somewhat protected against state anxiety, probably because they were better able to cope with medical school activities.

Strengths and limitations

The nationwide nature of the study design is a factor that speaks to the generalizability of our results; however, although the number of responses was high, not all the results will be applicable to each and every university, since the response rate varied widely across centers (from 0.2% to 5.8% of the total number of responses). The use of a self-administered instrument rather than structured clinical interviews may also be a limitation, since although used in many studies, depression scores may not accurately reflect the severity of depression. However, since it was not possible to perform a clinical evaluation of all medical students in Spain, we believe that the approach adopted provides a clear picture of something that is often commented on by students themselves, and which may lead to stigmatization [40]. It is also possible that students who were especially sensitive to these issues or were aware of having these problems were more predisposed to complete the survey than others. The moment at which surveys are launched may also be a confounding factor. We therefore decided to start the survey at the beginning of the second semester (which usually commences during the last week of January in most Spanish universities), once all the first semester examinations had finished and students had no responsibilities other than attending theoretical classes or practical and hospital rotations. Also, we only captured individual constructs, whereas institutional constructs that may also contribute were not analysed. Finally, it is important to emphasize that the instruments used in the present study are not diagnostic but of a screening nature. Finally, the sampling procedure was non probabilistic, since participation was offered to everyone but only those who wanted participated.

Conclusions

In the present study, we report the prevalence of depression, anxiety, burnout and empathy among students from all the medical schools in Spain. The results, which are similar to those already published in relation to other countries, provide a clear picture of the mental disorders affecting Spanish medical students. Medicine is an extremely demanding degree and it is important that universities and medical schools view this study as an opportunity to ensure conditions that help minimize mental health problems among their students. Some of the factors underlying these problems can be prevented by, among other things, creating an environment in which mental health is openly discussed and guidance is provided. Other factors need to be treated medically, and medical schools and universities should therefore provide support to students in need through the medical services available within their institutions.

Acknowledgments

The authors wish to thank the following students for helping them with the survey: Sònia Serrabou Pradas, Universidad Autónoma de Barcelona; Jorge Monzón Moya, Universidad de Alcalá de Henares; Lucía Martín López, Universidad Autónoma de Madrid; Ignacio Coll Orduña; Universidad Alfonso X El Sabio; Alba Arbués Martí, Universidad de Barcelona- Bellvitge; Mar Niella Bellot, Universidad de Barcelona-Clinic; María Sasía, Universidad de Cantabria; Ángel Francisco Serrano Andrades, Universidad de Cádiz; Ander Santiago Gómez, Universidad CEU Cardenal Herrera–Castelló; Sara Ivars Bernal, Universidad CEU Cardenal Herrera- Valencia; Laura Sindín, Universidad San Pablo C.E.U.; Juan Fco Vázquez Rodríguez, Universidad de Castilla La Mancha-Ciudad Real; Beatriz Jarabo Tévar, Universidad de Castilla La Mancha-Albacete; Jorge Mesa Guadalupe, Universidad Complutense de Madrid; Jesús Canales Fernández, Universidad de Córdoba; Alba María Torrat Novés, Universidad Católica de Valencia S. Vicente M.; Maria Molina Guerrero, Universidad de Girona; Alysson Micolta, Universidad Europea de Madrid; Clara Hoyas Sánchez, Universidad de Extremadura; Daniela Rocca Flores, Universidad Francisco de Vitoria; Araceli Jiménez Lara, Universidad de Granada; Yeray Damas Pons, Universitat de las Illes Balears; Marc Vallés Alabart, Universidad Internacional de Cataluña; Chourok Aknin, Universitat Jaume I de Castellón; Iriana Rodríguez Hernández, Universidad La Laguna; Rosa Maria Navarro Lopez, Universidad de Murcia; Yosef Benzaquen Aserraf, Universidad de Málaga; Laura Sánchez Sánchez, Universidad Miguel Hernández de Elche; Alberto Lorenzo Longedo, Universidad de Oviedo; Patricia Capdevila, Universitat Pompeu Fabra; Rodrigo Guitian Montes, Universidad del País Vasco; Lucas Antigono, Universidad Rey Juan Carlos; Bruno Fernández Cuevas, Universidad de Sevilla; Gloria Corbacho Hernández, Universidad de Salamanca; Candela Fernández Reino, Universidad de Santiago de Compostela; Jesús Andicoberry López, Universitat de València; Mateo Jiménez García, Universidad de Valladolid; Ana García Blasco, Universidad de Zaragoza; Mar García Bellas, Universidad las Palmas de Gran Canaria; Jose Carte García, Universidad de Navarra.

We also thank Diana Draper for correcting the english manuscript.

Data Availability

The data underlying the results presented in the study are available at the following repository of the Universidad de Murcia. https://digitum.um.es/digitum/handle/10201/112325.

Funding Statement

The authors received no specific funding for this work.

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Decision Letter 0

Kamran Sattar

5 Aug 2021

PONE-D-21-11578

Depression, Anxiety, Burnout and Empathy among Spanish Medical Students

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Reviewer #1: The manuscript offers an overview on medical students mental health in Spain. The strength of the study was the national scale study. However, I feel that the manuscript need to be improved based on the following comments before it is ready for publication.

This manuscript would need a native speaker proofreading to increase the readability of the findings. There is a glaring grammatical and spelling (eg: PubMed) errors throughout the manuscript.

Abstract:

Need to include study objective and some general methodology before jumping to results. Worthwhile to include the tools in the abstract so that readers can grasp whether the depression/anxiety prevalence was more of positive symptoms or diagnosis.

Introduction:

1. The introduction focused only on depression while the constructs measured also include burnout, anxiety and empathy. Hence, authors could incorporate this flow in the introduction

Introduction on burnout, depression and anxiety and some overview in general population - High prevalence of burnout, depression and anxiety - why it is more pronounced among medical students - the impact of these mental health problems if not addressed (including empathy) - why empathy is important in medical training - lack of studies looking into this in Spanish context

2. A search in Pubmed (October 6, 2020) revealed 859 articles featuring the Spanish word for "depression" and 517 featuring the Spanish term for “medical students". The union of the two terms returned no records at all.

(From my search, it seems there is such study (PMID: 32920780). Hence, this paragraph should be updated.

3. Some introduction on medical training and the structure in Spain is necessary since this is a national scale study. It would help readers to understand which are pre and clinical year students.

Methods:

1. First para: Need to include population size or estimate to give some picture to readers.

2. Each instruments need to be introduced separately in individual paragraph for a better flow- purpose of the instrument (screening or diagnosis), whether it was administered in English or Spanish version, validation in Spanish or medical students context, with reliability mentioned - scores calculation (whether there is dichotomous classification or measured as continuous variable). Note that validation must be mentioned specifically for the instruments (eg. CBI) rather than the construct (eg. Burnout)

3. Some explanation is needed to help readers in the difference of anxiety state vs trait

4. What is p75?

5. Statistical analysis - more details are needed what are the independent variables included for each logistic regression analyses? How was the independent variables selected for the multivariable model? (Some study used cutoff of p-value more than 0.2 for each univariate analysis run)

Results

1. "Cronbach's alpha coefficients were 0.923 (Beck's test), 0.703 (Maslach), 0.809 (Jefferson), 0.378 (state anxiety) and 0.365 (trait anxiety)." - I think this is not necessary as validation should be done in a separate cohort rather than the actual sample.

2. Table 1 - Percentage (%) should be in form of 22.9 rather than 22,9.

3. Table 1 - Age should be excluded and just mentioned in the paragraph in form of mean and standard deviation.

4. Second para: Authors refer this para as Table 1 but it seems there were 6 subgroup analyses that were not in Table 1. These subgroup analyses were mentioned selectively rather than comprehensively. Hence, authors should rethink whether this subgroup analysis need a separate table.

5. I suggest that Figure 1 to Figure 5 is changed into Table. It is difficult to read the result precisely from the bar chart.

6. "Percentage of depression was also significantly higher among 2nd, 3rd, and 4th year students, with those in their 1st and 6th years scoring lowest in this sense (Figure 2)" - How did authors came to this statement. Was one-way ANOVA conducted to ascertain this? - This comment also applies to paragraph on anxiety, burnout and empathy.

7. There was untranslated Spanish words in Table 3.

8. Drugs and substance abuse: "... with this percentage again being significantly higher among men.." - Authors must be careful when saying significantly unless there was t test or anova done to ascertain the association.

9. Multivariate relationships between DABE variables and risk predictors - Multivariable instead of multivariate

10. Table 4-7 (Inferior superior should be named as lower and upper)

11. p value of 0.000 should be written as p-value < 0.001

Discussion

1. "We therefore believe that the results offer an accurate and highly relevant overview of the mental health of medical students in our country" - I think this is overinflation of the study, plus it is a non-probability sampling. A better way to say this is - the number of participants may reflect the true situation of the problem in Spain medical training.

2. Second para is misleading as BDI is a screening tool rather than diagnostic. Hence the overall prevalence is more of depression symptoms rather than depression.

3. Second para - last 2 sentences were repetitive of result section. This should be discussed, compared or contrast rather than being repeated.

4. "... suggesting that the prevalence of burnout among medical students is fairly similar to that found among medical residents and practicing physicians (27)." reference given was studies on medical students. Hence a proper citation is needed.

5. Last para: The second last sentence was also repeating the result. Some critical discussion is desirable. Why anxiety trait and state could be highly correlated? What could this mean to educators or medical training.

6. Last sentence: Maybe this can help authors to expand the discussion https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6696211/

Strengths and limitations.

1. Need to emphasis the instruments are screening rather than diagnostic.

2. Other limitations have to be discussed - non probability sampling

2. Only captured more of individual constructs. Institutional constructs that may contribute to DABE were not captured

Conclusion only emphasized on high prevalence of DAB. No mention of empathy which was part of the study objective.

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PLoS One. 2021 Dec 2;16(12):e0260359. doi: 10.1371/journal.pone.0260359.r003

Author response to Decision Letter 0


21 Oct 2021

Answers marked in red in the Response To Reviewers document.

Reviewer #1: The manuscript offers an overview on medical students mental health in Spain. The strength of the study was the national scale study. However, I feel that the manuscript need to be improved based on the following comments before it is ready for publication.

This manuscript would need a native speaker proofreading to increase the readability of the findings. There is a glaring grammatical and spelling (eg: PubMed) errors throughout the manuscript. We are sorry, the manuscript was revised by a native professional but probably the last additions to the manuscript included some errors. Ms. Diana Draper has revised it again.

Abstract:

Need to include study objective and some general methodology before jumping to results. Worthwhile to include the tools in the abstract so that readers can grasp whether the depression/anxiety prevalence was more of positive symptoms or diagnosis. We agree with the reviewer, and we have included two paragraphs dealing with the objective and the methods employed.

Introduction:

1. The introduction focused only on depression while the constructs measured also include burnout, anxiety and empathy. Hence, authors could incorporate this flow in the introduction. Again, we agree. We have included a new paragraph in the introduction.

Introduction on burnout, depression and anxiety and some overview in general population - High prevalence of burnout, depression and anxiety - why it is more pronounced among medical students - the impact of these mental health problems if not addressed (including empathy) - why empathy is important in medical training - lack of studies looking into this in Spanish context

2. A search in Pubmed (October 6, 2020) revealed 859 articles featuring the Spanish word for "depression" and 517 featuring the Spanish term for “medical students". The union of the two terms returned no records at all.

(From my search, it seems there is such study (PMID: 32920780). Hence, this paragraph should be updated. Yes, the reviewer is right, the article was referenced in our list, but it did not appear in our search then. This spanish journal probably was not indexed immediately.

3. Some introduction on medical training and the structure in Spain is necessary since this is a national scale study. It would help readers to understand which are pre and clinical year students. Ok, we agree and a paragraph has been included in the introduction.

Methods:

1. First para: Need to include population size or estimate to give some picture to readers. Ok, the population number was included originally in the first paragraph of Discussion. This has been also included now in the first paragraph of Methods.

2. Each instruments need to be introduced separately in individual paragraph for a better flow- purpose of the instrument (screening or diagnosis), whether it was administered in English or Spanish version, validation in Spanish or medical students context, with reliability mentioned - scores calculation (whether there is dichotomous classification or measured as continuous variable). Note that validation must be mentioned specifically for the instruments (eg. CBI) rather than the construct (eg. Burnout) We agree, all the instruments ar enow in separate paragraphs.

3. Some explanation is needed to help readers in the difference of anxiety state vs trait. Ok, a new paragraph has been inserted in Methods.

4. What is p75? It is the 75th percentile or third quartile (Q3). This has been included in the revised manuscript.

5. Statistical analysis - more details are needed what are the independent variables included for each logistic regression analyses? How was the independent variables selected for the multivariable model? (Some study used cutoff of p-value more than 0.2 for each univariate analysis run). All the variables (except depression, burnout, anxiety and empathy that were the dependent variables) were the independent variables and we only selected those that gave a significant p value (less than 0.05) in the previous bivariate tests. This has been also added to the paragraph.

Results

1. "Cronbach's alpha coefficients were 0.923 (Beck's test), 0.703 (Maslach), 0.809 (Jefferson), 0.378 (state anxiety) and 0.365 (trait anxiety)." - I think this is not necessary as validation should be done in a separate cohort rather than the actual sample. Yes, we removed this paragraph.

2. Table 1 - Percentage (%) should be in form of 22.9 rather than 22,9. We are sorry, we have corrected it.

3. Table 1 - Age should be excluded and just mentioned in the paragraph in form of mean and standard deviation. Yes, we have included these numbers.

4. Second para: Authors refer this para as Table 1 but it seems there were 6 subgroup analyses that were not in Table 1. These subgroup analyses were mentioned selectively rather than comprehensively. Hence, authors should rethink whether this subgroup analysis need a separate table. The reviewer is right. We added these”subgroups” comments in order to give some more information. Since there are so many tables, we have decided to add the sentence ”data not shown”. We hope you agree, but if necessary we will add these new tables.

5. I suggest that Figure 1 to Figure 5 is changed into Table. It is difficult to read the result precisely from the bar chart. We agree with the reviewer and all these figures have been changed to a table, new table 2.

6. "Percentage of depression was also significantly higher among 2nd, 3rd, and 4th year students, with those in their 1st and 6th years scoring lowest in this sense (Figure 2)" - How did authors came to this statement. Was one-way ANOVA conducted to ascertain this? - This comment also applies to paragraph on anxiety, burnout and empathy. The term significantly was used only when the chi square p level was lower than 0.05. Then, the rest of sentences just tell the values that are lower and greater, but ANOVA was not performed to obtain significance among them. We have corrected all these sentences to indicate only when there are significant differences.

7. There was untranslated Spanish words in Table 3. We are sorry, we have corrected it.

8. Drugs and substance abuse: "... with this percentage again being significantly higher among men.." - Authors must be careful when saying significantly unless there was t test or anova done to ascertain the association. Yes, answered in point 6 above.

9. Multivariate relationships between DABE variables and risk predictors - Multivariable instead of multivariate. Ok, we have corrected it.

10. Table 4-7 (Inferior superior should be named as lower and upper). Ok, we have corrected it.

11. p value of 0.000 should be written as p-value < 0.001. Ok, we have corrected it.

Discussion

1. "We therefore believe that the results offer an accurate and highly relevant overview of the mental health of medical students in our country" - I think this is overinflation of the study, plus it is a non-probability sampling. A better way to say this is - the number of participants may reflect the true situation of the problem in Spain medical training. Yes, the reviewer is right. We have changed it in the last lines of the first para of Discussion.

2. Second para is misleading as BDI is a screening tool rather than diagnostic. Hence the overall prevalence is more of depression symptoms rather than depression. Yes, the reviewer is right. We have included the term symptoms in several places in the paragraph.

3. Second para - last 2 sentences were repetitive of result section. This should be discussed, compared or contrast rather than being repeated. The reviewer is right and we have eliminated it.

4. "... suggesting that the prevalence of burnout among medical students is fairly similar to that found among medical residents and practicing physicians (27)." reference given was studies on medical students. Hence a proper citation is needed. Our error, reference should be number 26.

5. Last para: The second last sentence was also repeating the result. Some critical discussion is desirable. Why anxiety trait and state could be highly correlated? What could this mean to educators or medical training. Regarding the correlation between both anxiety state and trait, it is question that still remains unanswered. According to an early formulation, anxiety is a unidimensional construct including both state and trait anxiety, considered to be different sides of the same coin. However, other authors suggested trait and state anxiety to be separate multidimensional constructs.

6. Last sentence: Maybe this can help authors to expand the discussion https://www.ncbi.nlm.nih.gov/ Thank you very much, it is a quite good paper. We have referenced it (new ref. 40) and added a sentence to the last paragraph.

Strengths and limitations.

1. Need to emphasis the instruments are screening rather than diagnostic. Yes, we have added it.

2. Other limitations have to be discussed - non probability sampling. Yes, we also added it.

2. Only captured more of individual constructs. Institutional constructs that may contribute to DABE were not captured. The reviewer is right, we have included a paragraph about it.

Conclusion only emphasized on high prevalence of DAB. No mention of empathy which was part of the study objective. The reviewer is right, we have included a paragraph on empathy.

Attachment

Submitted filename: Response to reviewers.docx

Decision Letter 1

Kamran Sattar

9 Nov 2021

Depression, Anxiety, Burnout and Empathy among Spanish Medical Students

PONE-D-21-11578R1

Dear Dr. Garcia-Estañ,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

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Kind regards,

Kamran Sattar

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Acceptance letter

Kamran Sattar

17 Nov 2021

PONE-D-21-11578R1

Depression, Anxiety, Burnout and Empathy among Spanish Medical Students

Dear Dr. García-Estañ:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

If we can help with anything else, please email us at plosone@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Kamran Sattar

Academic Editor

PLOS ONE

Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    Attachment

    Submitted filename: Rebuttal letter.docx

    Attachment

    Submitted filename: Response to reviewers.docx

    Data Availability Statement

    The data underlying the results presented in the study are available at the following repository of the Universidad de Murcia. https://digitum.um.es/digitum/handle/10201/112325.


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