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. 2024 Dec 19;19(12):e0313841. doi: 10.1371/journal.pone.0313841

Application of clown care in hospitalized children: A scoping review

Guo Xin 1,#, Fu Yingping 1,#, Chen Yue 1,, Wu Jiaming 1,, Hu Xue 2,*
Editor: Cho Lee Wong3
PMCID: PMC11658477  PMID: 39700221

Abstract

Purpose

This study aims to provide healthcare providers with insights into relevant interventions by examining the timing, format, content, outcome measures, and effects of clown care interventions on hospitalized children.

Methods

This study utilized a scoping review methodology based on the framework by Arksey and O’Malley. The search for Chinese and English literature on the utilization of clown care for hospitalized children was conducted in databases including CNKI, VIP, Wanfang, China Biology Medicine Database, PubMed, Embase, Web of Science, CINAHL, and Cochrane Library. At the same time, the references and other grey literatures included in the paper were also manually searched. covering publications from inception to December 10, 2023. Screening of the literature was done based on predefined inclusion and exclusion criteria, with data extraction and synthesis carried out independently by two researchers.

Results

Out of 1084 articles screened, 18 were included. Clown care can be used with children who have burns, perioperative care, fracture rehabilitation, autism, puncture therapy, chemotherapy, respiratory pathologies and disabled children, according to a review of the literature. Clown care is feasible and available for these kids, and it has been shown to have favorable impacts. The main interventions used in clown care are guided imagery, cognitive coping, emotional reflection, distraction, and empowerment. Physical(reduced children’s pain levels), psychological(reduced anxiety, improved coping skills, quicker recovery), cognitive-behavioral(for example, the number of meaningful words that children with autism say in 10 minutes.), and other indications are the several types of clown care outcome indicators.

Conclusions

Clown care can lessen a hospitalized child’s pain, alleviate their worry, and divert their focus from illness and suffering. However, not all pediatric patients benefit from clown care. Every youngster is an independent individual with unique personality traits, and some may experience intense pain along with a terror of the clown role. Future research should concentrate on understanding the characteristics of hospitalized children to develop tailored clown care programs that can enhance clinical effectiveness.

Trial registration number

https://doi.org/10.17605/OSF.IO/B4KMV.

Introduction

Hospitalization can have adverse effects on an individual’s emotional, behavioral, cognitive, and educational development, particularly in children. [14] due to their limited cognitive abilities and unfamiliarity with the hospital environment. The youngster may not be able to handle the unpleasant hospital stay due to the underdeveloped brain and nervous system, the absence of a defined objective, and the agony brought on by the illness. The child’s surrounding environment is exceedingly sensitive, leading to feelings of fear when confronted with the sight of medical staff in white gowns. Additionally, prolonged exposure to an unfamiliar setting, along with continuous diagnostic and nursing interventions, gives rise to anxiety, depression, and other detrimental emotions. These feelings are expressed through behaviors such as crying and resistance, which negatively impact the child’s willingness to comply with medical directives and hinder the effective progression of clinical diagnosis and treatment.

At present, a variety of non-drug intervention methods are used to relieve children’s pain and anxiety associated with medical operations [5, 6], and among these methods, clown care has demonstrated a significant effect. Clown care, also known as clown therapy or medical clowning, has emerged as a popular non-pharmacological intervention in pediatric care, in recent years. Clown care is a non-drug intervention method based on therapeutic humor. It is mainly manifested in the following four aspects, from a physiological perspective, patients can release endorphins through humor and hearty laughter, thereby regulating and stimulating their immune response. Cognitively, clowns embody various roles that divert patients’ attention from their conditions, fostering imagination and facilitating self-expression. In terms of emotional well-being, patients are encouraged to substitute negative feelings with positive ones. Socially, clowns engage with patients to enhance interaction and connection. It is upon this foundation of humor theory that clown care is recognized for its valuable contributions within medical environments [7]. In the early 20th century, two clowns first appeared in a paediatric ward in London [8]. In the 1980s, Michael Christensen, a professional clown, founded the Clown Care Center in New York [9]. In the same year, Canadian child life expert Karen Ridd established the Clown Care Program at Winnipeg Hospital [10]. Since then, clown care has been formally integrated into the medical and nursing process. Hospital clowning continues to grow around the world. Numerous hospitals across the United States, Canada, Europe, Israel, Australia, South Africa, Asia, and South America presently implement clown intervention programs [11].

Research has demonstrated that therapeutic clowning can significantly alleviate anxiety and fear in hospitalized children, mitigate postoperative pain, and positively contribute to enhancing the health outcomes during children’s disease rehabilitation [4]. Nevertheless, clown therapy may not be appropriate for every hospitalized child. The age of participants was found to be a significant determinant in treatment adherence studies, according to a systematic review [12]. Adolescents may exhibit greater behavioral control and a tendency to conceal their emotions, whereas younger children are more likely to display emotional distress readily. Compared to younger children, teens may benefit less from clown care. An additional study [13] revealed that children’s distress was unaffected by their interactions with clowns. This inconsistency could be due to methodological reasons. Clown care programs are still in the early stages of development in China, primarily due to cultural differences [14], the Western archetype of clowns, characterized by red-nosed masks and outlandishly dramatic costumes costumes, may not be appropriate for Chinese medical facilities. Incorporating a traditional Chinese cartoon character, like the Monkey King, could resonate more positively with children in hospital settings. In contrast to other countries, the implementation of therapeutic clowning for hospitalized children in China has been limited in duration. The majority of "clown doctors" are volunteers, which results in a lack of an organized training framework. Additionally, there is no standardized procedure regarding the recruitment criteria, sources, conditions, training methodologies, content, or length of training for "clown doctors."

Many reviews have clarified the effectiveness of the application of clown care in pediatric patients, but there is a lack of comprehensive descriptions of the intervention timing, form and content of intervention, and outcome indicators of existing clown care. A scope review can summarize a range of documentary evidence to show the breadth and depth of a knowledge domain. Therefore, guided by the scope review report framework [15], this study summarized and analyzed the relevant literature in this field at home and abroad, and summarized the intervention timing, form and content of intervention, outcome indicators, and effects of clown care in hospitalized children, with a view to providing references for medical staff to carry out relevant research. This report follows the PRISMA-ScR checklist (S1 File).

Methods

This study follows the framework outlined by Arksey and O’Malley, which includes five essential stages: 1) Formulating the research question; 2) Identifying pertinent studies; 3) Selecting studies; 4) Organizing data, and; 5) Synthesizing, summarizing, and presenting findings.

Stage one: Formulating the research question

According to the principle of participants, concept, context, the study object is hospitalized children, the study concept is clown care, and the study context is the application of clown care in hospitalized children.

Finalizing research questions:

  • What are the advantages and limitations of clown care in the application of hospitalized children?

  • What are the factors influencing the application of clown care in hospitalized children?

  • How can existing programs and application modalities aid hospitalized children in adapting to their new environment and alleviating negative emotions?

Stage two: Identifying relevant studies

A systematic search was conducted across databases such as CNKI, VIP, Wanfang, China Biology Medicine Database, PubMed, Embase, Web of Science, CINAHL, and Cochrane Library, aligning with the identified research queries. The search was restricted to articles published up to December 10, 2023. A comprehensive search strategy combining controlled vocabulary and free-text terms with Boolean operators "AND" and "OR" was employed. The search strategy tested in PubMed is presented in Table 1 (S2 File). Prior to screening, systematic training exercises were conducted on researchers to ensure the consistency of the studies. When there are discrepancies between two individuals regarding the literature selection process, the viewpoint of a third researcher is sought to ensure that no essential literature is overlooked in the inclusion procedure. All related articles are managed using EndNote X9 Reference Manager, which also helps to identify duplicate entries.

Table 1. Pilot search in PubMed electronic database.

Date Keywords Search results
10/12/2023 #1Clown [Title/Abstract] OR medical clown [Title/Abstract] OR clown doctor [Title/Abstract] OR clown intervention [Title/Abstract] OR clown therapy [Title/Abstract] OR clown nurse [Title/Abstract]
#2child [Mesh Terms] OR children [Title/Abstract] OR pediatric [Title/Abstract] OR kids [Title/Abstract]
#3 #1AND#2
1084

Stage three: Study selection

Eligibility and inclusion criteria

Inclusion criteria.

  • (1)Participant (P)

    Hospitalized children<18 years of age, along with any accompanying family members;

  • (2)Interest of phenomena (I)

    Receiving hospital clowns intervention;

  • (3) Comparison (C)

    Compared receipt of hospital clowns to standard of care;

  • (4)Outcome (O)

    The application and effect evaluation of clown care in hospitalized children;

  • (5)Study design (S)

    Original research literature, encompassing qualitative studies, case-control studies, cohort studies, case studies, etc.

Exclusion criteria.

  1. Literature where the effect of clown care in combination with other interventions is challenging to quantify;

  2. Conference papers or incomplete texts with ambiguous or imprecise data;

  3. Duplicate publications;

  4. Literature not available in Chinese or English.

Selection process

To eliminate duplicates, all literature was imported into the EndNote X9 software. Two researchers trained in evidence-based practice independently screened titles and abstracts based on the inclusion and exclusion criteria. Full-text review was conducted for all potentially relevant articles. In case of disagreements, a third researcher reviewed the material and a consensus was reached. The screening process is depicted in S1 Fig.

Stage four: Charting the data

A form be developed in Excel for the data extraction and piloted to ensure its accuracy. After carefully reading the entire text, the first and second researchers collected all pertinent data from the included literature. The following information be included in the data extraction form: the study’s title, authors, nation, publishing date, kind of study, sample size, study population, intervention strategy, and outcome indicators. Once the data were plotted, the third researcher, through repeated reading and analysis of the included literature, checked the extracted data and results, and updated the extracted data as needed, so as to obtain all the data to make the study more complete and form the final results.

Stage five: Collating, summarizing and reporting results

The following be serve as the foundation for themes pertaining to the study objectives: (i)What types of illnesses does clown care predominantly address in pediatric inpatients?(ii) How is clown care applied in pediatric settings, and which patients benefit most? (iii) How does providing clown care to pediatric patients in hospitals affect their evaluation? This will function as a story with pertinent themes.

Results

Characteristics of the studies selected

An initial search yielded 1,082 articles. After deleting duplicate articles, 429 articles were obtained. Further reading of the titles and abstracts of these articles yielded 87 articles. Finally, after reading the full text, 16 articles were obtained after excluding those that did not meet the standard. 2 articles were obtained by other means. These articles were selected by excluding those that did not fit the content and topic of the study substances, as well as those that cannot be accessed in full text. Finally, a total of 18 articles were included. At least two reviewers screened each result by title and abstract, with disagreements resolved by discussion with the review team. The remaining full text papers were accessed and screened against the eligibility criteria, again by at least two reviewers with disagreements resolved by discussion. Among these, 13 were in English and 5 were in Chinese. The included studies originated from countries such as Italy [16, 17, 23, 25, 31], Israel [18, 30], Denmark [19], Brazil [29], Germany [24], the United States [20], Turkey [12], and China [21, 22, 26, 27, 28], Canada [32] are among the countries whose works were published between 2005 and 2023. Table 2 (S1 Table) displays the fundamental features of the included literatur.

Table 2. General characteristics of the included studies (n = 18).

Reference publication year Country Study Design population clowns practitioner Timing of intervention Forms of intervention conclusion mark
Ben-Pazi H, et al. [16] 2017 Italy Randomized controlled trial A Medical clowns puncture therapy Cognitive responses;
Empowerment;
Emotional reflection;
Felluga M, et al.[17] 2016 Italy quasi-randomized controlled trial A Medical clowns puncture therapy Cognitive responses;
Divert attention;
①②
Goldberg A, et al [18] 2014 Israel Randomized controlled tria A Medical clowns puncture therapy Divert attention ①②
Kristensen HN, et al. [19] 2018 Denmark Controlled clinical trial A Medical clowns puncture therapy Cognitive responses;
Divert attention;
Meiri N, et al.[20] 2015 United States Randomized controlled tria A Medical clowns puncture therapy Divert attention; ①②④
NingXuemei,et al. [21] 2023 China Randomized controlled tria A Medical clowns puncture therapy Divert attention ①②④
Yang Fan, et al.[22] 2022 China Randomized controlled tria A Medical clowns puncture therapy Cognitive responses;
Divert attention;
Guided imagery;
①④
Dionigi A, et al. [23] 2014 Italy Randomized controlled tria B Medical clowns perioperative period Divert attention;
Markova G,et al. [24] 2021 Germany Randomized controlled tria B Medical clowns perioperative period Guided imagery;
Divert attention;
Vagnoli L, et al. [25] 2005 Italy Randomized controlled tria B Medical clowns perioperative period Guided imagery;
Divert attention
Cheng Zongyan, et al. [26] 2019 China Randomized controlled tria B Medical clowns perioperative period Cognitive responses;
Divert attention;
Guided imagery;
①④
Yildirim M, et al. [12] 2018 Turkish Randomized controlled tria C Medical clowns dressing changes Guided imagery;
Emotional reflection;
Yan Guifan, et al. [27] 2023 China Randomized controlled tria C Medical clowns dressing changes Divert attention; ①④
Wan Lin, et al. [28] 2023 China Randomized controlled tria D Medical clowns Postoperative fracture and rehabilitation Divert attention;
Cognitive responses
①④
Lopes-Junior LC, et al [29] 2020 Brazil quasi-randomized controlled trial E volunteers Before and after chemotherapy Divert attention; ②④
Shefer S, et al. [30] 2019 Israel Controlled clinical trial F Medical clowns When treating autism Emotional reflection;
Cognitive responses
Bertini, et al. [31] 2011 Italy Randomized controlled tria G Medical clowns When the child was in the hospital room Divert attention
Shauna, et al.[32] 2011 Canada non-randomised controlled trials H Medical clowns When the child was in the hospital room Divert attention
Empowerment;

A children with puncture therapy, B children in perioperative period, C children with burns, D children after fracture surgery, E children with chemotherapy, F children with autism;G Children hospitalized for respiratory pathologies, H disabled children. ①physiological indicators, ②psychological indicators, ③ cognitive-behavioral indicators, ④other indicators.

Essential elements of clown care

Clown care clients and clown care practitioners

Clown care is utilized in various settings for hospitalized children, including puncture therapy [1622], perioperative [2326], burn treatment [12, 27], fracture rehabilitation [28], chemotherapy support [29], autism intervention [30], respiratory pathologies [31], and disabled children [32]. Evaluation of clown care often involves measuring parent satisfaction, caregiver anxiety levels, and caregiver trait anxiety in the context of hospitalized children [18, 2123, 25, 27, 28, 31]. The evaluation of caregiver satisfaction primarily involved the use of questionnaire surveys or follow-up assessments of healthcare personnel. This methodology allows for a swift and straightforward capture of the subjective experiences reported by the parents of hospitalized children, making it both practical and accessible. However, it is important to note that this approach may lack the precision and objectivity associated with standardized assessment scales.

Individuals responsible for designing and implementing clown care programs are referred to as clown care practitioners in this study. These practitioners primarily consist of medical clowns who have received training in sociology, psychology, pedagogy, acting, nursing, and healthcare [12, 1628, 30, 31, 32]. Additionally, clown care volunteers [29], including clown doctors, clown nurses, and professional medical clowns, are also included within this category. However, there are no uniform requirements for "clown doctors." Only the basic rules of public morality were laid down. For example, the physical health of each "clown doctor" must be ensured, and the clown doctor must comply with the relevant regulations and codes of conduct of the medical institution. Patients must be served impartially, regardless of their gender, age, beliefs, or illness. There is no uniform standard for the recruitment methods, sources, conditions, training methods, content, and duration of "clown doctors," which lacks standardization.

Timing of clown care intervention for hospitalized children

Among the sixteen studies compiled, seven studies [1622] discussed the application of clown care in puncture therapy, encompassing procedures like venepuncture, intravenous infusions, phlebotomy, botulinum toxin injections, and allergy prick testing conducted during the hospital stay. Four publications [2326] focused on the use of clown care in anesthesia for induction, postoperative care, and preoperative care in the perioperative period. Two studies [12, 27] examined discomfort related to burns on the body, emphasizing pre-procedure anxiety, discomfort during dressing changes, and post-procedural relaxation. Postoperative rehabilitation following a fracture was explored in one paper [28], covering both postoperative fracture management and rehabilitation. Another paper [29] discussed the application of clown care during chemotherapy sessions. Additionally, one study [30] investigated the provision of clown care to children with autism, focusing on the timing of interventions ten minutes before, during, and after the procedure. The last two articles introduced the application effect of clown care in hospitalized children with respiratory diseases [31] and disabled children [32], respectively.

Form and content of clown care

The elements of clown care can be encapsulated by terms such as "cognitive coping," "guided imagery," "distraction," "emotional reflection," and "empowerment." “Cognitive coping” [16, 17, 19, 22, 26, 28, 30] is designed to encourage pediatric patients to actively respond to the challenges brought by the disease and improve their self-cognitive ability. Studies [33] have shown that "medical clowns" improve their self-cognitive ability by guiding perioperative pediatric patients to "Give yourself a like" other positive behaviors to improve their self-cognition ability. "Guided imagery" [12, 16, 22, 2426, 29] entails using clowning to create positive memories and help children cope with pain by guiding them to imagine pleasant experiences. Divert attention" [12, 1729, 31, 32] pertains to the use of medical clowns who engage with children through enjoyable experiences designed to capture their attention. These interactions can be tailored to the child’s age and may include magic tricks, pantomime, storytelling, and music, among other forms of entertainment. For instance, adolescents might appreciate magic performances or juggling acts, while younger children may enjoy fairy tales or their favorite children’s songs. By providing customized entertainment programs aligned with the age and interests of hospitalized children, we can more effectively alleviate discomfort and anxiety during their stay, thereby diverting their attention from distressing circumstances. "Emotional reflection" [12, 16, 26, 30] involves adapting the clown’s performance to the child’s emotional cues, engaging with the child in a manner that resonates with their feelings, and encouraging the child to express themselves during the interaction. "Empowerment" [16, 32] involves the clown adjusting their actions based on the child’s input, fostering the child’s confidence and agency. By simulating medical procedures as a game, children gain a better understanding of the process, reducing anxiety and fear.

Outcome indicators and effects

The collection of 18 studies outlined five sets of outcome measures: behavioral, cognitive-behavioral, physical, and miscellaneous markers. Physiological indicators were reported in eleven studies [1622, 26, 27, 28, 31] focusing primarily on children’s pain levels (measured using various scales such as Pain Visual Analog Scale, Pain Ruler, Numeric Pain Rating Scale, Facial Expression Pain Inventory, FLACC Pain Assessment Scale, self-reported pain levels, modified Facial Pain Expression Scale known as Piggyback), children’s fatigue (assessed using Pediatric Quality of Life Scale, Child Multidimensional Fatigue Scale), duration of children’s crying, healing times for fractures (using Femadez-esteve scale), and improvement in joint function (measured with Flynn scale).Psychological markers were reported in eight studies [17, 18, 21, 2325, 29, 32] focusing on children’s positive emotions, caregiver anxiety levels (State-Trait Anxiety Inventory), children’s emotional states and anxiety levels (Modified Yale Preoperative Anxiety Scale), trait anxiety (Children’s State-Trait Anxiety Inventory), and psychological stress (Children’s Stress Inventory). This study’s seven included studies demonstrated that, when compared to conventional care, children and adolescents who had hospital clowns—whether or not a parent was present at the time of intervention—reported much less anxiety and improved psychological adjustment. Cognitive-behavioral indicators were discussed in three studies [12, 27, 30], highlighting metrics such as the number of meaningful words spoken in ten minutes, instances of social smiles (Autism Diagnostic Scale, Second Edition), interactions during a game of "catch," and compliance with medication regimens. Additional measures, including salivary cortisol levels, duration of child’s crying, amount of pain medication used within 24 hours post-surgery, success rate of medical procedures, and parental satisfaction (assessed through questionnaires), were detailed in nine studies [12, 2022, 2629, 31].

Discussion

Clown care interventions are varied, but programs lack individualization

The study findings suggest that while there exists a wide range of clown care interventions, the predominant approaches revolve around "cognitive coping," "guided imagery," "distraction," "emotional reflection," and "empowerment." Each patient is a unique individual with distinct characteristics. Clown phobia refers to the extreme aversion and distress experienced by individuals towards clown figures. A study of 95 patients with clown phobia found that clown phobia occurs in younger female children clownphobia were in female youngsters. Serious psychological discomfort, such as anxiety or panic attacks, as well as a decline in social function, can also contribute to the development of clownphobia. In a study involving 1160 children receiving clown care interventions, 14 of them exhibited fear or phobia towards medical clowns [33]. Fear of clowns can affect children at any age (range 1–15), any ethnicity, religion, or degree of illness. Further large scale studies are required to better understand this unique phenomenon of fear of clowns.

Theories of the aetiology of clown fear can be broadly split into three general categories: those relating to their physical appearance, those relating to their behaviour and those derived from learning and/or experience. Firstly, considering fear of clowns as deriving from aspects of physical appearance, Moore [34] suggests that coulrophobia may stem from the uncanny valley effect which describes the feelings of eeriness and repulsion triggered by near human-looking objects. With regard to clowns, the distortion of their facial features through makeup gives them a ‘near-human’ quality which may elicit the uncanny valley effect. Secondly, behavioural explanations of clown fear focus on the unpredictability of their behaviour. Clowns laughing at random intervals, as well as the nature of their performances emphasizing magic and trickery, may make the child feel uncomfortable or upset. Finally, the fear of clowning may stem from the negative portrayal of clowns in the media, as well as from negative experiences in the same year. Research indicates that symptoms of clown phobia can persist for up to 60 years [35]. Furthermore, a report on clinical characteristics from clown care indicated that 9.5% of patients experienced no notable enhancement in their fear of clowns, nor did they find alleviation from social or psychological issues. Children may lack the cognitive capacity, and their hospitalization can already induce significant stress. Incorrectly tailored clown care interventions based on the children’s individual traits could lead to lasting psychological harm and hinder the normal development of their psychological, physiological, and cognitive functions. To enhance the efficacy of clown care programs and tailor them more effectively, it is crucial to integrate the unique needs and characteristics of hospitalized children into these interventions. Clinical practitioners should assess high-risk children for clown phobia before implementing clown care to prevent potential harm and address underlying issues. Further research is needed to enhance the focus, effectiveness, and clinical relevance of clown care for hospitalized children. Currently, there is a lack of assessment tools specifically designed for pediatric clown care.

A lesser known study in clown care examines the effect on biochemical tests such as salivary cortisol concentration in hospitalized children

To effectively manage and alleviate the pain experienced by hospitalized children, it is essential to conduct a thorough and precise evaluation of their discomfort. As some hospitalized children may struggle to articulate their pain levels, healthcare professionals often rely on observational scales to assess pain based on the children’s behaviors, such as limb movements and facial expressions [36]. However, it has been suggested [37] that pain assessment tools focusing on behavioral and facial cues might be limited to subcortical somatic and autonomic motor pathways, which may not accurately capture a child’s pain experience. Cortisol, the primary stress hormone produced by the body, has emerged as a valuable objective marker for evaluating children’s discomfort and the effectiveness of treatments [38]. When the body encounters pain stimuli, it elicits a corresponding neuroendocrine stress response, leading to an elevation in cortisol levels. Morelius et al. [39] demonstrated that painful interventions, such as fundus examinations and heel blood draws, can elevate cortisol levels in neonates, while certain non-pharmacological interventions may mitigate these cortisol levels. Cortisol secretion exhibits a circadian rhythm. Human cortisol metabolism adheres to a 24-hour physiological cycle, peaking between 6:00 and 8:00 AM, followed by a gradual decline, with the lowest levels occurring from midnight to 2:00 AM the subsequent day. Ivars et al. [40] undertook a 12-month study measuring salivary cortisol in healthy full-term and preterm infants, revealing that the salivary cortisol rhythm is established during the neonatal phase (one month postpartum), characterized by higher levels in the morning compared to the evening, which then stabilize over time. To mitigate the effects of circadian rhythm, clinical sampling should be conducted at the time of maximum cortisol concentration. Cortisol levels can be measured through blood, saliva, and urine samples. Saliva samples are easy to collect and non-invasive, and salivary cortisol represents biologically active free cortisol [41], enhancing the precision of assessments. Among the 18 studies included in this investigation, only one [29] utilized salivary cortisol as an outcome measure to assess pain in children.

Currently, the utilization of salivary cortisol for assessing neonatal pain predominantly centers on planned pain responses. There is a scarcity of research investigating variations in salivary cortisol levels in newborns following non-pharmacological therapies. This gap is largely attributed to the intricate nature of endocrine dynamics, which may have interplay among different hormones. Research conducted by Pavlyshyn et al. [42]. indicates that interventions such as skin-to-skin contact can elevate oxytocin levels while concurrently diminishing salivary cortisol levels, thus enhancing stress responses in preterm infants. Both endorphins and oxytocin possess analgesic and pleasurable effects and serve as anti-stress hormones, whereas cortisol is regarded as the primary hormone associated with stress. Further research is necessary to delve deeper into the interactions between hormones, pain, and their underlying mechanisms. To provide scientific validation for the advancement of clown care programs that effectively alleviate pain, reduce physical and psychological distress, shorten hospital stays, and aid in recovery, integrating pain assessment scales with biochemical testing in future research and clinical applications can offer valuable insights.

Exploring cost-effective and convenient alternatives to on-site clown care provision

The implementation of clown care clinical activities for hospitalized children was carried out on-site in the 18 publications included in this study. The healthcare landscape is evolving, with increasing demands on healthcare professionals as societal advancements and healthcare models undergo updating and transformation [30]. Pediatric wards entail high-risk, high-intensity, and high-pressure medical work compared to other departments. Introducing clown care may add to the workload of medical professionals. Moreover, the intense stress of clinical work could potentially lead to professional burnout and impact clinical outcomes for children [43]. Conversely, establishing a clown care team requires a substantial number of healthcare experts; therefore, virtual reality can be leveraged to enhance clinical tasks related to clown care interventions [44]. This approach can aid in the efficient allocation of medical resources, potentially leading to a more equitable distribution of human resources among clinical healthcare specialists. In addition to alleviating the burden on medical staff and enhancing treatment adherence for hospitalized children, virtual reality (VR) technology presents itself as a cutting-edge, cost-effective, and practical means to deliver care to children in hospital settings. By integrating virtual reality technology with clown care, such as offering a virtual reality interactive platform featuring children’s favorite cartoons to aid in engagement, we can provide a more immersive and tailored care experience. The utilization of virtual reality technology in healthcare is expanding and has shown promise in various domains, including pain management [45], psychotherapy [46], and other areas. It is recommended that future research explores more affordable and convenient programs that leverage virtual reality technology to enhance care delivery.

Clown care should be culturally appropriate and localized

The traditional Western clown appearance, characterized by white faces, red noses, and black eyes, may not be suitable for hospitalized children in China and many other Eastern countries due to cultural differences, potentially causing fear instead of comfort. Chinese children in hospitals may not respond positively to clown care interventions that involve mime, puppetry, or similar performance-based techniques. While some studies have demonstrated the benefits of clown care in alleviating pain and anxiety in children from diverse cultural backgrounds [46], it is evident that children from varying cultural backgrounds may respond differently to the same clown care approaches, underscoring the influence of cultural values and backgrounds on the effectiveness of such interventions. Therefore, it is essential to carefully consider and incorporate the cultural values and norms of each nation when implementing clown care for hospitalized children from different cultural backgrounds. Developing a culturally localized clown care strategy specific to our country is imperative.

Limitations of the study

Acknowledging the constraints of a scoping review is crucial. To begin with, the process of selecting articles did not involve any quality criteria. While this is not a mandatory methodological requirement for conducting a scoping review, it does hinder the authors’ ability to evaluate the reliability and strength of the literature included, consequently impacting the confidence in the conclusions drawn from it. Additionally, the generalizability of the findings is restricted as we solely incorporated published works in both Chinese and English during the selection of literature for inclusion.

Implications

This study delved into the scope of clown care initiatives for pediatric patients in hospitals, systematically categorizing research subjects, practitioners, intervention modalities, content, and outcome measures associated with clown care. Despite the existence of diverse clown care interventions, they lacked personalization. Additionally, the utilization of physiological markers such as salivary cortisol was infrequent, with measures and questionnaires being the predominant assessment tools for evaluating the impact of clown care. In comparison to the observational evaluation of behaviors like facial expressions and body language, cortisol serves as the primary hormone indicative of stress in the body. Its collection method is straightforward and non-invasive, which can make the detection results more accurate. Given the cultural disparities between China and Western nations, it is essential for Chinese medical institutions to develop an optimal clown care implementation strategy for pediatric patients in China. This should be informed by insights gained from international clown care practices while being tailored to align with the unique social and cultural context of China. To establish a robust and scientifically grounded framework for the clinical advancement of high-quality clown care programs for hospitalized children, future research should explore the influence of various cultural backgrounds and values.

Limitations of the study

Acknowledging the constraints of a scoping review is crucial. To begin with, the process of selecting articles did not involve any quality criteria. While this is not a mandatory methodological requirement for conducting a scoping review, it does hinder the authors’ ability to evaluate the reliability and strength of the literature included, consequently impacting the confidence in the conclusions drawn from it. Additionally, the generalizability of the findings is restricted as we solely incorporated published works in both Chinese and English during the selection of literature for inclusion.

Supporting information

S1 File. PRISMA-ScR checklist.

(DOCX)

pone.0313841.s001.docx (59.8KB, docx)
S2 File. Search strategy.

(DOCX)

pone.0313841.s002.docx (14.5KB, docx)
S1 Fig. Flow chart of literature screening.

(JPG)

pone.0313841.s003.jpg (180.9KB, jpg)
S1 Table. General characteristics of the included studies.

(DOCX)

pone.0313841.s004.docx (23.1KB, docx)

Data Availability

All relevant data are within the manuscript and its Supporting information files.

Funding Statement

The author(s) received no specific funding for this work.

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Decision Letter 0

Cho Lee Wong

10 Oct 2024

PONE-D-24-35005Application of clown care in hospitalized children: A scoping reviewPLOS ONE

Dear Dr. Hu,

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Additional Editor Comments:

Thank you for the opportunity to read this manuscript. This topic touches on an important subject and is interesting.

However, a few comments for authors consideration:

Introduction:

- There are some reviews about medical clowning for sick children, how does this article differ from them?

- Why conduct a scoping review rather than other types of reviews?

Methods:

- For Eligibility criteria: Please state in PICOS.

- A similar meta-analysis review was conducted and completed in November 2019 and they yielded 14 studies. However, your review is a scoping review and should include more papers. Please revisit if you missed any potential research.

Discussion:

The discussion addresses the key points and limitations of the current study. However, it could be strengthened by 1) a more explicit comparison of the findings with the existing literature. 2) elaborate the implications for practice and policy; 3) provide more specific recommendations for future research.

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

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Reviewer #1: Yes

Reviewer #2: Yes

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

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Reviewer #1: Yes

Reviewer #2: Yes

**********

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Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Review Comments to the Author

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Reviewer #1: - On abstract please mention the time period

- C clearly state your research difference from other similar studies in 2023 and 2024(https://doi.org/10.1007%2Fs12519-023-00720-y, and https://doi.org/10.3389%2Ffped.2024.1324283)

Reviewer #2: Dear Authors,

Thank you for submitting your manuscript titled "Application of Clown Care in Hospitalized Children: A Scoping Review." The study presents valuable insights into the role of clown care interventions and is commendably structured. However, I believe there are several areas that could benefit from further enhancement. I encourage you to review the attached documents, which outline specific comments and suggestions. Addressing these points will significantly strengthen your manuscript.

Best regards,

**********

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Reviewer #1: Yes: Yideg Abinew

Reviewer #2: Yes: Seid Muhumed Abdilaahi, Departments of Pediatrics and Child Health Nursing, Jigjiga University, Jigjiga, Ethiopia

**********

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Attachment

Submitted filename: PONE-D-24-35005_reviewer.docx

pone.0313841.s005.docx (248.1KB, docx)
PLoS One. 2024 Dec 19;19(12):e0313841. doi: 10.1371/journal.pone.0313841.r002

Author response to Decision Letter 0


25 Oct 2024

Dear Editor and Reviewers:

Greetings!

First of all, on behalf of all the authors, please allow me to extend our sincerest thanks to you and the reviewers. We would like to thank you for taking the time out of your busy schedules to review our paper in detail and provide valuable comments and suggestions. We are fully aware of the importance of these comments in improving the quality of the paper and ensuring academic rigor.

After receiving the review comments, we immediately organized our team to conduct in-depth discussion and analysis, and revised and improved the paper in strict accordance with the reviewers' suggestions. Editorial comments are listed below in red font. Reviewer comments are in blue font, such as below, where specific questions are numbered. Our responses are given in black font. The following are our responses and explanations to the reviewers' comments:

1.Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming:

In order to comply with the strict formatting requirements of PLOS ONE, we have revised the formatting of the previous manuscript, which now conforms to PLOS ONE style, as described under "Revised Manuscript with Track Changes" and "Manuscript."

2.Please include captions for your Supporting Information files at the end of your manuscript, and update any in-text citations to match accordingly:

We have included the title of this research supporting information file at the end of the manuscript in strict accordance with the editor's request, and updated any textual citations accordingly,as described under "Revised Manuscript with Track Changes" and " Manuscript."

3.We note that your Data Availability Statement is currently as follows:”All relevant data are within the manuscript and its Supporting Information files.”Please confirm at this time whether or not your submission contains all raw data required to replicate the results of your study. Authors must share the “minimal data set” for their submission. PLOS ONE defines the minimal data set to consist of the data required to replicate all study findings reported in the article, as well as related metadata and methods:

In accordance with the requirements of PLOS ONE's Data Availability Statement and the recommendations of the editors, we have examined all of the raw data used in this study and assure you that our paper contains all of the raw data necessary to replicate the results of the study, as described in Table 1、Table 2 and Figure 1 of the manuscript and in the Supporting Information (S1 File、S2 File、S3 Fig、S4 Table.).

4.INTRODUCTION:There are some reviews about medical clowning for sick children, how does this article differ from them:

Thank you very much for your valuable comment. Based on your advice, we searched two other similar articles on clown care (https://doi.org/10.1007%2Fs12519-023-00720-y and https://doi.org/10.3389%2Ffped.2024.1324283). By carefully reading the full text, we have detailed the differences between the two articles and this study, as follows.

The purpose of article 1 (https://doi.org/10.1007%2Fs12519-023-00720-y) is to analyze the effects of clown care on hospitalized children. The findings suggest that clown care can reduce children's distress, relieve their anxiety, shorten their crying time, and raise caregivers' anxiety levels. However, some young children may be frightened by clowns and become tearful or anxious. The clown should be trained to notice and understand these children, and staff and parents should be consulted to help reduce anxiety until the particular child is satisfied with the clown. This is consistent with the results of this study. The purpose of article 2 (https://doi.org/10.3389%2Ffped.2024.1324283) was to evaluate the effectiveness of medical clowns in reducing pain and anxiety in hospitalized pediatric patients and their parents in different areas of medicine. The findings suggest that medical clowns have substantial positive and beneficial effects on reducing stress and anxiety in pediatric children and their families in a variety of settings, consistent with the findings of this study.

However, different from these two articles, the purpose of this study is to summarize the timing, form, and content of intervention, outcome indicators, and effects of clown care in hospitalized children. The first two articles only analyzed the application effect of clown care on hospitalized children but did not analyze the intervention timing, intervention form and content, and outcome indicators of clown care in different diseases. At the same time, the pain assessment in the above two articles may be limited to the pain assessment scale based on facial expression and behavior due to the incomplete literature included, while this study noted through literature analysis that the pain assessment tools based on facial expression and behavior may be limited to the measurement of subcortical body and autonomic motor pathways. This does not objectively diagnose the pain experience of the child. Cortisol is the main hormone in the body under stress, which can effectively detect pain in children , the research objects included in the first two articles are mostly children receiving invasive medical operations and surgeries, and this study also includes children with autism and children with cancer, so the research objects are more abundant, and the scope of clown care is wider.

In short, other articles on clown care mostly focused on analyzing the clinical application effect of clown care in hospitalized children. However, compared with other similar articles on clown care, this study not only analyzed the application effect of clown care but also fully analyzed and summarized its intervention timing, intervention form and content, and outcome indicators. In order to provide a reference for medical personnel to carry out relevant intervention.See "Manuscript with Track Changes" and "Manuscript".

5.INTRODUCTION:Why conduct a scoping review rather than other types of reviews:

We appreciate the editor's advice, which has been very helpful to us, and the following is what we added:

Many reviews have clarified the effectiveness of the application of clown care in pediatric patients, but there is a lack of comprehensive descriptions of the intervention timing, form and content of intervention, and outcome indicators of existing clown care. A scope review can summarize a range of documentary evidence to show the breadth and depth of a knowledge domain. Therefore, guided by the scope review report framework, this study summarized and analyzed the relevant literature in this field at home and abroad, and summarized the intervention timing, form and content of intervention, outcome indicators, and effects of clown care in hospitalized children, with a view to providing references for medical staff to carry out relevant research.

6.METHODS:For Eligibility criteria: Please state in PICOS:

Thank you very much for your valuable comment. Based on your advice, we changed the Eligibility criteria to PICOS format. Population (P): Hospitalized children < 18 years of age, along with any accompanying family members; Intervention (I): Receiving hospital clowns intervention; Comparison (C): Compared receipt of hospital clowns to standard of care; Outcome (O): The application and effect evaluation of clown care in hospitalized children; Study design (S): Original research literature, encompassing qualitative studies, case-control studies, cohort studies, case studies, etc. See the manuscript for details.

7.A similar meta-analysis review was conducted and completed in November 2019 and they yielded 14 studies. However, your review is a scoping review and should include more papers. Please revisit if you missed any potential research:

We strongly agree with the editor's view.In order to guarantee the scientific soundness and comprehensiveness of the scope review outcomes,we have strictly followed the editor's comments,and researched relevant studies on clown care and screened and read articles according to the inclusion and exclusion criteria in this paper. We have meticulously reviewed and incorporated several articles that are closely aligned with our research objectives and methodologies. We believe this will enhance the discourse and contextual framework of our study. Interestingly, we found two articles from other types of reviews, the last two papers in Table 2 ("Bertini et al[25], 2011"; "Shauna et al[26], 2011"). The research objects of these two articles have not been included in this study (the research objects are children hospitalized for respiratory pathologies and disabled children, respectively), and new information has been extracted from these two articles. For specifics, refer to the manuscript.We trust that the updated manuscript will fulfill your expectations.

8.METHODS:The discussion addresses the key points and limitations of the current study. However, it could be strengthened by 1) a more explicit comparison of the findings with the existing literature. 2) elaborate the implications for practice and policy; 3) provide more specific recommendations for future research:

We have meticulously updated the discussion section in strict alignment with the editor's recommendations and provided additional clarifications corresponding to each suggestion made by the editor. as described under "Revised Manuscript with Track Changes" and " Manuscript."

Reviewer 1:

Regarding Reviewer 1's comments, we are very grateful to the reviewer for taking the time to read our paper. We would like to thank you for your professional review work, constructive comments, and valuable suggestions on our manuscript. Your time and efforts are greatly appreciated. We have revised the manuscript according to your comments as listed in detail below.

1.Clearly state your research difference from other similar studies in 2023 and 2024(https://doi.org/10.1007%2Fs12519-023-00720-y, and https://doi.org/10.3389%2Ffped.2024.1324283):

Thank you very much for your valuable comment. Based on your advice,we have read both articles on clown care (https://doi.org/10.1007%2Fs12519-023-00720-y and https://doi.org/10.3389%2Ffped.2024.1324283). By carefully reading the full text, we have detailed the differences between the two articles and this study, as follows.

The purpose of article 1 (https://doi.org/10.1007%2Fs12519-023-00720-y) is to analyze the effects of clown care on hospitalized children. The findings suggest that clown care can reduce children's distress, relieve their anxiety, shorten their crying time, and raise caregivers' anxiety levels. However, some young children may be frightened by clowns and become tearful or anxious. The clown should be trained to notice and understand these children, and staff and parents should be consulted to help reduce anxiety until the particular child is satisfied with the clown. This is consistent with the results of this study. The purpose of article 2 (https://doi.org/10.3389%2Ffped.2024.1324283) was to evaluate the effectiveness of medical clowns in reducing pain and anxiety in hospitalized pediatric patients and their parents in different areas of medicine. The findings suggest that medical clowns have substantial positive and beneficial effects on reducing stress and anxiety in pediatric children and their families in a variety of settings, consistent with the findings of this study.

However, different from these two articles, the purpose of this study is to summarize the timing, form, and content of intervention, outcome indicators, and effects of clown care in hospitalized children. The first two articles only analyzed the application effect of clown care on hospitalized children but did not analyze the intervention timing, intervention form and content, and outcome indicators of clown care in different diseases. At the same time, the pain assessment in the above two articles may be limited to the pain assessment scale based on facial expression and behavior due to the incomplete literature included, while this study noted through literature analysis that the pain assessment tools based on facial expression and behavior may be limited to the measurement of subcortical body and autonomic motor pathways. This does not objectively diagnose the pain experience of the child. Cortisol is the main hormone in the body under stress, which can effectively detect pain in children , the research objects included in the first two articles are mostly children receiving invasive medical operations and surgeries, and this study also includes children with autism and children with cancer, so the research objects are more abundant, and the scope of clown care is wider.

In short, other articles on clown care mostly focused on analyzing the clinical application effect of clown care in hospitalized children. However, compared with other similar articles on clown care, this study not only analyzed the application effect of clown care but also fully analyzed and summarized its intervention timing, intervention form and content, and outcome indicators. In order to provide a reference for medical personnel to carry out relevant intervention.We also present the results of the analysis in the manuscript. See the manuscript for details.

Reviewer 2:

Regarding Reviewer 2's comments, we would like to thank the reviewer for taking the time to read our paper and for giving us the opportunity to revise it with many meaningful comments. We have carefully read Reviewer 2's comments and revised each of them in order to take this opportunity to improve the rigor and scientific quality of our paper, as shown in the following responses:

1.Please rephrase this as PLOS Guidelines using the format "Department, Institution, City, State, Country". Adjust font, line spacing and other formatting:

We've rephrased it as the PLOS Guidelines as "Department, Agency, City, State, country,"As follows: School of Nursing, Yunnan University of Chinese Medicine, Kunming, Yunnan, China; Pediatric, Yan'an Hospital Affiliated To Kunming Medical University, Kunming, Yunnan, China.

At the same time, we also reset the font, line spacing, and other formats in strict accordance with the reviewer's annotations and PLOS ONE requirements.

2.ABSTRACT:Please attempt to shorten abstract by following the PLOS guidelines:

Thanks to the reviewer's reminder, We have shortened the abstracts in strict accordance with the requirements of the PLOS guidelines.Please refer to the "Manuscript with Track Changes" and "Manuscript."

3.ABSTRACT:(“Research on the efficacy of clown care for hospitalized children has produced varying results, with differences in treatment duration and methods.” )This is an important point, but it lacks specificity. What kind of variability in the results has been observed (e.g., effectiveness across age groups or types of conditions)? Clarifying this would help the reader understand the motivation behind conducting a scoping review.

We sincerely appreciate the suggestions provided by the reviewer and have implemented changes based on their feedback. However, due to the constraints of the abstract, we will relocate the enhanced specific content to the introduction section, where it will be more detailed. Please refer to the "Manuscript with Track Changes" and "Manuscript."

4.ABSTRACT:(“A total of 16 articles were included”)The number of articles included in the review is mentioned, but there is no indication of the total number of articles screened or excluded. Including these numbers would provide a better sense of the comprehensiveness of the review process. For example: "Out of X articles screened, 16 were included.":

Thanks to the reviewers' comments, We've updated it to reflect the reviewers' feedback and now read, "Out of 1084 articles screened, 18were included."

5.ABSTRACT:(“Clown care can be used with children who have burns, perioperative care, fracture rehabilitation, autism, puncture therapy, and chemotherapy, according to a review of the literature.”) This sentence effectively summarizes the range of conditions where clown care is applied. However, the results could be enhanced by specifying which conditions showed the most positive outcomes or where clown care was less

Attachment

Submitted filename: Response to Reviewers.docx

pone.0313841.s006.docx (56.7KB, docx)

Decision Letter 1

Cho Lee Wong

29 Oct 2024

PONE-D-24-35005R1Application of clown care in hospitalized children: A scoping reviewPLOS ONE

Dear Dr. Hu,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

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Cho Lee Wong, PhD

Academic Editor

PLOS ONE

Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

Additional Editor Comments :

Dear Authors

Thank you for your revision. Please shorten your conclusion and place it under the heading "Implications."

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PLoS One. 2024 Dec 19;19(12):e0313841. doi: 10.1371/journal.pone.0313841.r004

Author response to Decision Letter 1


30 Oct 2024

Dear Editors:

Greetings!

First of all, on behalf of all the authors, please allow me to extend our sincerest thanks to you and the reviewers. We would like to thank you for taking the time out of your busy schedules to review our paper in detail and provide valuable comments and suggestions. We are fully aware of the importance of these comments in improving the quality of the paper and ensuring academic rigor.

After receiving the review comments, we immediately organized our team to conduct in-depth discussion and analysis, and revised and improved the paper in strict accordance with the editors' suggestions. Editorial comments are listed below in red font. such as below, where specific questions are numbered. Our responses are given in black font. The following are our responses and explanations to the editorss' comments:

1.Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice:

I sincerely appreciate your guidance. At the same time, we sincerely apologize for any inconvenience our errors may have caused you. After receiving your recommendation, we looked over the references right away and, per your request, deleted the ones that had been withdrawn and substituted the most recent ones. Again, I apologize. Please refer to the "Manuscript with Track Changes" and "Manuscript."

2.Thank you for your revision. Please shorten your conclusion and place it under the heading "Implications.":

I appreciate your suggestion very lot. In response to your suggestion, we have condensed the conclusion and placed it under "Implication".Please refer to the "Manuscript with Track Changes" and "Manuscript."

Once again, I would like to thank the editor and reviewers for their comments and giving me the opportunity to revise my paper. Through this thesis revision process, I deeply realized the shortcomings in our research and made comprehensive and in-depth improvements under your guidance. I believe that after these revisions, the quality of the thesis has been significantly improved and is more in line with the publication standards of PLOS ONE journals. Once again, I would like to thank you for your hard work and valuable comments and look forward to your further review and affirmation.

Attachment

Submitted filename: Response to Reviewers.docx

pone.0313841.s007.docx (13.3KB, docx)

Decision Letter 2

Cho Lee Wong

1 Nov 2024

Application of clown care in hospitalized children: A scoping review

PONE-D-24-35005R2

Dear Dr. Hu,

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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If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. 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.

Kind regards,

Cho Lee Wong, PhD

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Acceptance letter

Cho Lee Wong

26 Nov 2024

PONE-D-24-35005R2

PLOS ONE

Dear Dr. Xue,

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

At this stage, our production department will prepare your paper for publication. This includes ensuring the following:

* All references, tables, and figures are properly cited

* All relevant supporting information is included in the manuscript submission,

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If revisions are needed, the production department will contact you directly to resolve them. If no revisions are needed, you will receive an email when the publication date has been set. At this time, we do not offer pre-publication proofs to authors during production of the accepted work. Please keep in mind that we are working through a large volume of accepted articles, so please give us a few weeks to review your paper and let you know the next and final steps.

Lastly, 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 customercare@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. Cho Lee Wong

Academic Editor

PLOS ONE

Associated Data

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

    Supplementary Materials

    S1 File. PRISMA-ScR checklist.

    (DOCX)

    pone.0313841.s001.docx (59.8KB, docx)
    S2 File. Search strategy.

    (DOCX)

    pone.0313841.s002.docx (14.5KB, docx)
    S1 Fig. Flow chart of literature screening.

    (JPG)

    pone.0313841.s003.jpg (180.9KB, jpg)
    S1 Table. General characteristics of the included studies.

    (DOCX)

    pone.0313841.s004.docx (23.1KB, docx)
    Attachment

    Submitted filename: PONE-D-24-35005_reviewer.docx

    pone.0313841.s005.docx (248.1KB, docx)
    Attachment

    Submitted filename: Response to Reviewers.docx

    pone.0313841.s006.docx (56.7KB, docx)
    Attachment

    Submitted filename: Response to Reviewers.docx

    pone.0313841.s007.docx (13.3KB, docx)

    Data Availability Statement

    All relevant data are within the manuscript and its Supporting information files.


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