key: cord-0261992-fzh949to authors: Huber, A.; Klug, S. J.; Abraham, A.; Westenberg, E.; Schmidt, V.; Winkler, A. S. title: Animals in higher education settings: Do animal-assisted interventions improve mental and cognitive health outcomes of students? A systematic review and meta-analysis date: 2022-04-16 journal: nan DOI: 10.1101/2022.04.11.22273607 sha: bee55a031f13888cc5270bc2de39beb40076ae48 doc_id: 261992 cord_uid: fzh949to Background: Due to the high burden of mental health issues among students at higher education institutions world-wide, animal-assisted interventions (AAIs) are being increasingly used to relieve student stress. The objective of this study was to systematically review of the effects of AAIs on the mental and cognitive health outcomes of higher education students. Methods: Randomized controlled trials using any unfamiliar animal as the sole intervention tool were included in the systematic review. Study quality was assessed using the Cochrane Risk-of-Bias tool. Where possible, effect sizes (Hedges g) were pooled for individual outcomes using random-effects meta-analyses. Albatross plots were used to supplement the data synthesis. Results: Of 2.401 identified studies, 35 were included. Almost all studies used dogs as the intervention animal. The quality of most included studies was rated as moderate. Studies showed an overall reduction of acute anxiety (g= -0.57 (95%CI -1.45;0.31)) and stress. For other mental outcomes, studies showed an overall small reduction of negative affect (g= -0.47 (95%CI -1.46;0.52)), chronic stress (g= -0.23 (95%CI -0.57;0.11)) and depression, as well as small increases in arousal, happiness and positive affect (g= 0.06 (95%CI -0.78;0.90)). Studies showed no effect on heart rate and heart rate variability, a small reduction in salivary cortisol and mixed effects on blood pressure. No effect on cognitive outcomes was found. Conclusion: Overall, evidence suggests that AAIs are effective at improving mental, but not physiological or cognitive outcomes of students. Strong methodological heterogeneity between studies limited the ability to draw clear conclusions. Introduction education institutions [29, 30] . To confidently implement AAIs in higher education settings, a 98 comprehensive overview of the current state of research and good evidence on the effects of 99 AAIs on the mental and cognitive outcomes of students is needed. 100 The objective of this systematic review was therefore to estimate the effects of AAIs 101 implemented in higher education settings on (1) the mental health outcomes and (2) the 102 cognitive outcomes of students. This review also aims to contribute evidence to the "shared 103 medicines and interventions" subgroup of The Lancet One Health Commission. only randomized controlled trials (RCTs) that were published in a peer-reviewed journal 133 were included in this review. Studies were included if they assessed the effect of an 134 intervention using a living animal that was unfamiliar to participants as the sole intervention 135 tool, for any mental health or cognitive outcome of higher education students. Mental health 136 outcomes were considered those that describe a person's emotional or psychological state 137 [33], for example through self-perceived assessments of stress, anxiety or depression. We 138 also included physiological outcome measures that reliably correlate with acute stress, such 139 as blood pressure (BP), heart rate (HR) or cortisol levels [34] . By contrast, we considered 140 cognitive outcomes those that describe a person's cognitive functioning [35] , for example 141 7 through assessments of intelligence, concentration or attention. Specifically in the higher 142 education context, we also considered cognitive outcomes to include academic outcomes 143 such as test performance. Details on the eligibility criteria can be found in S1 Table, while 144 details on the search strategy can be found in S2 File and S2 Table. 145 146 Study selection 147 The selection process was conducted in two steps, using Covidence [36] . First, two 148 independent reviewers (AH and EW) screened articles by title and abstract and voted on 149 eligibility. Potential disagreements were resolved through regular discussions. Second, the 150 full text of remaining articles was evaluated by both reviewers (AH and EW). If articles 151 could not be found, the corresponding author was contacted. If there was no response within 152 two weeks, the articles were excluded. Articles both reviewers agreed upon were included in 153 the systematic review. 154 155 Quality assessment 156 Only quantitative outcomes that were assessed by at least three studies and could thus 157 be meaningfully combined in a quantitative synthesis were included in the quality assessment 158 process. The risk of bias of the included studies was assessed independently by two reviewers 159 (AH and EW), using the Cochrane Risk-of-Bias tool for Randomized Trials 2 (RoB 2) [37] . 160 The version for individually randomized, parallel-group trials as well as the version for 161 crossover trials were used [38, 39] . 162 163 Data extraction 164 . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) To be included in a meta-analysis, studies needed to supply an effect size (Hedges' g) 195 of the post-test difference in mental health or cognitive outcomes between an intervention 196 group and a control group, and had to be of good quality (rated as "low risk" or "some 197 concerns" by the RoB 2). In addition, studies had to use comparable intervention and control 198 conditions. Interventions generally fell into two categories: (1) interventions that allowed 199 participants to freely interact with animals and their handlers (active intervention), and (2) 200 interventions where an animal was present while participants' primary focus was on a task 201 (passive intervention). These tasks typically aimed to increase the stress levels of participants 202 (stressors), such as timed math tasks. Interventions were additionally categorized based on 203 the animal species used in the intervention condition. Control conditions broadly fell into 204 four categories: (1) control groups that replaced the presence of an animal with a human 205 (active human control), (2) control groups that replaced the presence of the animal with a 206 different animal, a toy animal, or pictures/videos of an animal (active animal control), (3) 207 control groups with an active component that was not a human or a different animal like yoga 208 (active other control), and (4) control groups without any active component (no-treatment 209 control). Meta-analyses were conducted for all outcomes where at least three studies reported 210 an effect size, were of good quality, and used comparable intervention and control conditions. 211 Due to the small number of studies included in each meta-analysis, it was not possible to 212 conduct moderator analyses. 213 214 . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) The copyright holder for this preprint this version posted April 16, 2022. ; https://doi.org/10.1101/2022.04.11.22273607 doi: medRxiv preprint For eligible outcomes, meta-analyses were conducted using RStudio Version 1.3.959 215 [40] . Summary effect sizes as well as the corresponding 95% confidence interval (CI) were 216 calculated using a random-effects model, and visualized using forest plots. The heterogeneity 217 between included studies was assessed using the Q and I 2 statistics. If Hedges' g and its 218 standard error (SE) was not reported in the original study, it was computed in RStudio 219 Version 1.3.959, using the package "esc" [41] . Details of the conducted calculations can be 220 found in S4 Table. Funnel plots were used to explore publication bias, and Egger's test for 221 funnel plot asymmetry was conducted. Effect size contours were calculated based on the standardized mean difference (SMD). 231 Contours corresponded to the effect sizes 0.2 (small effect), 0.5 (medium effect) and 0.8 232 (large effect). Since all included studies were randomized, an equal group size was assumed. 233 As suggested by Harrison 35. 268 Common reasons for study exclusion can be found in the PRISMA flow chart (Fig 1) . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) The copyright holder for this preprint this version posted April 16, 2022. ; 279 An overview of the most important extracted data items and study results can be 280 found in the data extraction table (Table 1) . Information on additional important study 281 characteristics can be found in S5 Table. In general, most studies had more female than male 282 participants, and participants were mostly of "typical" undergraduate age (mean 20. CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 16, 2022. ; is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 16, 2022. 306 d Effect sizes were described as "null", indicating no effect of the intervention on the corresponding outcome, if the p-value corresponding to the effect size was non-significant and the effect size was very small (less 307 than 0.2). If the effect size was above 0.2, the direction of effect was specified even if the associated p-value was non-significant. 308 e p-value calculated by AH. . It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 16, 2022. , and no studies were 320 classed as "low risk". Common limitations included not reporting the method of allocation 321 sequence generation or allocation sequence concealment. Additionally, blinding of 322 participants and study personnel to a participants' allocated condition was generally not 323 possible due to the animal presence, although some studies tried to conceal the true study 324 purpose from participants. Nonetheless, in most studies, both participants and study personnel 325 were probably aware of their assigned condition, which may have affected self-reported 326 outcomes. Finally, none of the included crossover RCTs gave information about potential 327 carryover effects. An overview of quality assessment results for RCTs and crossover RCTs 328 can be found in S6 and S7 Figs. Quality assessment results at the individual outcome level 329 can be found in S6 and S7 Tables. 330 331 332 333 . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 16, 2022. ; found an improvement in test anxiety, attitude and study motivation [46] ( Table 1) . 350 351 Quantitative synthesis 352 The following outcomes were included in the quantitative synthesis: acute self-353 perceived stress, chronic self-perceived stress, negative affect, acute anxiety, arousal, chronic 354 depression, happiness, positive affect, BP, HR, HRV, salivary cortisol, and performance on a 355 memory task. Of these, meta-analyses were conducted for chronic self-perceived stress, 356 negative affect, acute anxiety, positive affect and BP. All studies included in the meta-357 analyses used an active intervention condition, a dog as the intervention animal and a no-358 . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. p=0.006), indicating a medium-sized negative effect of the intervention (Fig 2) . This result 367 was mirrored by the albatross plot, where most studies clustered around the 0.5 to the 0.8 368 negative effect size contours (Fig 3) . Acute self-perceived stress was reported by seven 369 studies. Although not combinable in a meta-analysis, the albatross plot demonstrated that 370 included studies showed a reduction of self-perceived stress with a medium to large effect 371 size, with most results clustering around the 0.5 to the 0.8 negative effect size contours of the 372 albatross plot (Fig 4) . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 16, 2022. ; Negative affect was reported by 6 studies, of which 4 studies were combined in a 383 meta-analysis [53,57,62,64]. The pooled Hedges' g was -0.47 (95% CI -1.46, 0.52; Q=15.3, 384 I^2=80.4%, p=0.016), indicating a small-to medium-sized negative effect of the intervention 385 ( Fig 5) . The albatross plot showed that while some studies showed a reduction of negative 386 affect, other studies showed no effect (Fig 6) . The tendency for some studies to show the expected effect while other studies showed 395 no effect was also observed for the remaining mental health outcomes. Accordingly, a small 396 negative effect of the intervention was observed for chronic self-perceived stress (pooled 397 Hedges' g: -0.23 (95% CI -0.57, 0.11; heterogeneity: Q=1.44, I^2=0%, p=0.49) and chronic 398 depression, and a small positive effect was observed for positive affect (pooled Hedges' g: 399 0.06 (95% CI -0.78, 0.90; heterogeneity: Q=3.97, I^2=49.6%, p=0.138), arousal and 400 happiness. Forest plots and albatross plots for these outcomes can be found in S8 -S14 Figs. 401 402 Among the physiological outcomes, salivary cortisol was the only outcome to 403 demonstrate the expected direction of effect. Salivary cortisol was reported by four studies. 404 Although not combinable in a meta-analysis, included studies showed a small to medium 405 negative effect on cortisol, with most results falling between the 0.3 and 0.8 effect size 406 contours of the albatross plot. In contrast, among the 8 studies assessing HR, most included 407 . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 16, 2022. ; studies showed no effect on HR, with most results clustered around the middle of the 408 albatross plot (Fig 7) . This trend was mirrored by the studies assessing HRV. Additionally, the forest plot showed a very high, statistically significant level of 417 heterogeneity between the included studies (Q=45.5, I^2=95.6%, p<0.0001). These levels of 418 heterogeneity were significantly higher than for any other meta-analysis conducted. 419 Accordingly, it was deemed inappropriate to statistically combine BP outcomes, and no 420 pooled effect size was calculated. This strong heterogeneity was mirrored in the albatross 421 plot, where results were spread out throughout the plot. Forest plots and albatross plots for 422 physiological outcomes can be found in S15 -S18 Figs. 423 The only cognitive outcome included in the quantitative synthesis was performance 425 on a memory task, reported by six studies. Overall, included studies suggested a very small 426 negative effect of the intervention on memory task performance, with most results clustering 427 around the 0.2 effect size contour of the albatross plot. The albatross plot can be found in S19 428 CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 16, 2022. ; The funnel plot showed no evidence of publication bias, as confirmed by Egger's 432 regression test for funnel plot asymmetry (z= -1.74, p=0.081). The funnel plot can be found 433 in S20 Fig. 434 Discussion 435 Summary of findings 436 The aim of this systematic review and meta-analysis was to assess the effect of AAIs 437 implemented in higher education settings on the mental and cognitive outcomes of students. While the overall direction of effect of the included mental health outcomes was beneficial as 454 expected, some studies reporting on mental health outcomes showed no effect of the 455 . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 16, 2022. ; intervention. Since formal moderator analyses were not possible in this review, we cannot say 456 with certainty which, if any study characteristics are associated with this. The comparatively 457 smaller effect sizes of chronic stress and depression, both assessed with instruments designed 458 to detect changes in the mental state over longer periods of time, may point to limited long-459 term effects of AAIs, as suggested in previous literature [77] [78] [79] . is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 16, 2022. ; effect of AAIs on BP has been reported in other systematic reviews, even though the overall 481 trend seems to be that BP decreases post-AAI [5, 8] . One possible explanation for the large 482 discrepancies between BP results in this review and past reviews could be the poor reliability 483 of BP as an outcome measure. Indeed, a study by Kelsey et Interestingly, most included studies showed no effect of the intervention on HR or 492 HRV. This is different from findings of other reviews, which have found an overall reduction 493 of HR after an AAI in a variety of populations [5, 82] . It is possible that AAIs may have less 494 of an effect on physiological outcomes in a young, healthy population. Indeed, while Nimer 495 & Lundahl found a significant improvement of physiological outcomes after an AAI, 496 moderator analyses revealed that populations with disabilities showed significantly larger 497 improvements than healthy populations did [16] . Additionally, it is possible that differences 498 in effects between studies are again associated with intervention design: Most studies that 499 assessed HR and HRV included a stressor in their intervention, thus likely triggering an acute 500 stress response among participants. It is well established that, in response to an acute stressor, 501 HR increases while HRV decreases [83]. Accordingly, it is possible that in studies with a 502 stressor, the potential effect of an AAI on these physiological outcomes was not strong 503 enough to compete with or alter the effects of the acute stress response. More studies without 504 . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 16, 2022. an incorporated stressor would be needed to judge the effects of AAIs on the physiological 505 outcomes of students in a non-stressful situation. 506 507 508 Cognitive outcomes 509 The studies included in this review showed no effect on the intervention on cognitive 510 outcomes. This is an interesting finding, especially considering that past systematic reviews 511 assessing the impact of AAIs on cognitive outcomes of children have found that the presence 512 of animals to helps to create a productive learning environment [8, 84] . Although these 513 systematic reviews point out that there is little evidence that AAIs directly improve academic 514 performance, they have nevertheless been shown to improve related cognitive outcomes like 515 concentration, motivation, attention and social functioning [8, 84] . However, Banks et al. 516 hypothesized that while the presence of an animal may be beneficial for children, whose 517 cognitive functions are still developing, there is less of an impact on these outcomes among 518 higher education students, who are already at their peak of cognitive functioning [53] . The 519 primary benefits of AAIs for this population therefore seem to be affective, not cognitive. later, showing that this increase in RCT availability is quite a recent development. This is an 526 encouraging finding, signaling the strong interest in this field from the scientific community. 527 . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 16, 2022. ; The quality of the RCTs included in this review was also judged to be satisfactory by the 528 RoB2. 529 530 Nevertheless, some characteristics shared by the included studies may limit the 531 generalizability of the results found in this review. First, participants in included studies were 532 overwhelmingly female. This may be attributable to an increased interest in AAIs among 533 females, as most studies recruited participants via self-selection, or to recruitment from 534 traditionally majority-female degree programs, such as psychology or nursing (150,151) . 535 Since previous research has shown differences between males and females in, for example, 536 responses to stressors, it is possible that the results may not be generalizable to both male and 537 female students (152,153). Second, although the search strategy was designed to find 538 publications using any intervention animal, almost all included studies used dogs. This may 539 be due to the popularity of dogs as companion animals and the feelings of empathy and 540 companionship associated with them, making them a popular choice for AAIs [85] . 541 Additionally, dogs may have been the easiest option logistically since some studies 542 cooperated with established university-based AAI programs that were already using dogs 543 is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 16, 2022. ; The strength of this review lies in the use of the albatross plots to enrich the 551 quantitative data synthesis, as well as the inclusion of RCTs only. Nonetheless some 552 important limitations remain. 553 First, the strong methodological heterogeneity severely limited the comparability of 554 included studies, as has been the case with many other reviews in the AAI field [5,6,13]. The 555 heterogeneity also limited the number of studies included in the individual meta-analyses and 556 limited our ability to conduct moderator analyses. This heterogeneity is at least partly 557 attributable to the broadly defined eligibility criteria used in this review. Kazdin et al. have 558 remarked that such broad eligibility criteria, where inclusion is based on the presence of an 559 animal in the intervention as opposed to the proposed mechanism of the intervention, is one 560 of the reasons for the methodological heterogeneity in most reviews in the AAI field [86] . 561 This lack of a guiding theoretical framework in most reviews is exacerbated by the lack of an 562 unanimously accepted theory on the mechanism of AAI effectiveness in the field [87]. In 563 order to limit this issue in future research, systematic reviews should settle on a specific 564 theoretical framework to guide their eligibility criteria in order to include only logically 565 comparable studies [86] . 566 Second, the albatross plots in this review were explicitly meant to allow a more 567 inclusive overview of available data than what was available based on meta-analyses alone 568 and were not meant to generate a usable summary statistic. The effect size contours 569 superimposed on the plot are only approximations of the actual effect size (100). While they 570 allow a visual interpretation of the general trend of the included studies in terms of effect size 571 and direction, they are not exact and are not to be interpreted as such (100). 572 573 . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) The copyright holder for this preprint this version posted April 16, 2022. ; If possible, future reviews in this field could conduct moderator analyses to assess 575 whether any study characteristics have an influence on study results, while future studies 576 could focus on comparing different aspects of AAIs, perhaps by using multiple intervention 577 conditions. For example, studies could explore whether incorporating a stressor in the study 578 design or conducting an AAI in either a group or an individual setting influences the effect of 579 AAIs on health outcomes. 580 Additionally, while a recent review suggested that AAI participation has no adverse 581 effects for participating animals, research is limited and results remain conflicting [88] . 582 There is even less research on potential benefits of AAI participation for animals [88] . 583 Interestingly, research has suggested that following stress, trauma or abuse, animals can 584 exhibit behavior similar to symptoms of human mental disorders such as depression or post-585 traumatic stress disorder [89, 90] . Taking this into account, it is essential that the physical and 586 mental health of animals participating in AAIs is protected. In the best case, AAIs should be 587 mutually beneficial to animals and humans, thus making them a truly shared intervention in 588 the spirit of One Health. 589 590 One of the goals of this review was to provide an evidence base that administrators at 591 higher education institutions can use to decide whether to implement AAIs at their own 592 campus. Despite the methodological limitations listed above, this review shows that AAIs 593 can be effective in improving student mental health, especially acute feelings of anxiety and 594 stress. Taking into consideration the high burden of mental health issues among students at 595 higher education institutions, along with the unprecedented stress caused by the COVID-19 596 pandemic, higher education institutions will likely be facing an increasing demand for mental 597 health support [29, 91, 92] . Due to their low cost, easy scalability and high popularity, AAIs 598 present a good option for higher education institutions to improve student mental health [26] . 599 . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) The copyright holder for this preprint this version posted April 16, 2022. ; This opportunity could be taken up particularly by universities outside of the US and Canada, 600 where AAI programs are still rare. It has to be kept in mind, however, that while stress 601 reduction efforts can certainly help, more structural changes should be implemented, which 602 aim to reduce academic, social and financial pressures that impact students' mental health. 603 These could include, for example, an increased mental health budget at higher education 604 institutions, reduced tuition fees and a mandatory salary for student internships [21, 93, 94] . The proximal origin of 638 SARS-CoV-2 Reconnecting for our future: The Lancet 640 One Health Commission. The Lancet Animal-assisted interventions: Definitions American Veterinary 642 Medical Association Current Status of Animal-Assisted Interventions in Scientific 645 Literature: A Critical Comment on Their Internal Validity. 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