Could Nature Contribute to the Management of ADHD in Children? A Systematic Review

Attention-deficit/hyperactivity disorder (ADHD) is a common neurodevelopmental disorder that is typically managed with pharmacological and psychotherapeutic interventions. In the general population, exposure to nature has been found to have robust beneficial effects on cognitive performance, including attention. With inattention being a factor of the symptomatology of individuals with ADHD, this provides a rationale to investigate the potential benefits of exposure to nature for this population. Four electronic databases (PubMED, PsycINFO, Embase, and Web of Science) were searched for empirical studies investigating the effects of nature on ADHD prevalence and/or symptom severity in populations of school-aged children. Key characteristics, methodologies, and outcomes of included studies were extracted and evaluated. Out of the 458 studies identified, 7 met the inclusion criteria. Despite the large heterogeneity in methodological approaches, the included articles consistently reported that exposure to nature is associated with reduced ADHD diagnoses and symptom severity. Furthermore, when several covariates, such as age, gender, annual household income, parental income, and education level, as well as several pre-natal factors, were controlled for, the relationship between nature and ADHD remained significant. The reviewed literature provides strong support for the benefits of exposure to nature on ADHD in school-aged children.


Introduction
Attention-deficit/hyperactivity disorder (ADHD) is a common neurodevelopmental disorder often diagnosed in childhood.It is characterized according to the Diagnostic and Statistical Manual for Psychiatric Disorders, Fifth Edition [1] (DSM-5; American Psychiatric Association) by a persistent pattern of inattention and/or hyperactivity-impulsivity that interferes with functioning and is persistent across multiple settings.Systematic reviews and meta-analyses have suggested that the global prevalence of ADHD is between 2 and 7% [2], with 5% of individuals 18 years of age or younger meeting the DSM-5 or International Classification of Disease (ICD-10; World Health Organization; [3]) criteria [4].
While the causes of ADHD are still being investigated, it is understood that ADHD has clear neurobiological underpinnings and that the heritability of ADHD is substantial, with first-degree biological relatives of individuals with ADHD posing a significant risk factor for the development of the disorder [5][6][7].Additionally, several factors such as very low birth weight, maternal smoking during pregnancy, alcohol exposure in utero, and certain childhood temperaments have been associated with ADHD (DSM-5; [1]).

Current ADHD Treatment Options
Typically, the management of ADHD consists of pharmacological and nonpharmacological interventions [8].While there is support for the efficacy of pharmacological approaches [9], there are also disadvantages that come with this treatment approach for some patients, including negative side effects, little or no symptom reduction, or medication resistance [10].There is also scarce evidence surrounding the use of medications to treat ADHD in preschool-aged children; therefore, behavioral interventions are the first point of call for this age group [8,11].Non-pharmacological approaches such as dietary adjustments, behavioral interventions (e.g., parent training), and neurocognitive therapies have been found to have some efficacy in the treatment of ADHD in children and adolescents [12][13][14][15].However, evidence for the efficacy of these approaches is difficult to determine due to the broad scope of interventions and outcome measures used.The benefits of exposure to green spaces and nature seen in non-clinical populations has inspired an emergence of thought around how the physical environment could contribute to the management of ADHD in children and adolescents [16].

Benefits of Exposure to Nature
Exposure to nature has been found to have a positive impact on human health, wellbeing, and cognitive functioning [17][18][19][20][21].More specifically, green spaces have also been shown to have benefits for restoring attention in adult and child non-clinical populations [22,23].The Attention Restoration Theory (ART [24]) postulates that being immersed in nature actually restores cognitive functioning and increases attentional capacity.With one of the primary symptoms of ADHD being inattention, this theory is most relevant in relation to ADHD.This theory is based on the premise that there are two types of attention, direct/voluntary attention and involuntary attention [25].According to ART, natural environments assist in the recovery from the fatigue that occurs when using direct attention because they primarily draw on involuntary attention [24].ART also suggests that the use of involuntary attention allows a restoration of fatigued direct attention [24].While there is evidence to suggest that the exposure to nature supports attention restoration in adults (for example [26] Berman et al., 2008), few studies have explored this concept in children [23].It is important to note that ART primarily focuses on the exposure to nature, and it does not explicitly specify whether the type of activity performed in nature matters.

The Current Review
Despite there being evidence to suggest that there is a link between the exposure to nature and the restoration of attention [22,23,26], there has not yet been a systematic review of the literature investigating how this relationship might benefit individuals affected by ADHD.This review aims to address this by compiling, clarifying, and summarizing the existing evidence for the use of nature exposure in children and adolescents with ADHD and its effects on ADHD symptoms.

Materials and Methods
This systematic review followed the general principles published by the Preferred Reporting Items for Systematic reviews and Meta-Analyses statement guidelines (PRISMA; [27,28]) and sought to answer the following question: does exposure to nature have a beneficial effect on children with ADHD?

Literature Search
The following electronic databases were searched: PubMED, PsycINFO, Embase, and Web of Science.The following search terms were used, with appropriate Boolean operators and MeSH terms identified for each database: (Child*, Adolescent*, Student*), (ADHD, "attention deficit/hyperactivity disorder", "attention deficit hyperactivity disorder"), (greenspace, "green space", greenery, greenness, biophilia, "biophilic design", plant*, natural, nature).The search was limited to humans and articles in the English language.The last search was conducted on 31 March 2021.

Study Design
Studies of a quantitative nature were considered for this review, while studies with qualitative designs were excluded.The decision to exclude qualitative studies was made because the focus of this review was to analyze the empirical evidence of the effects that nature has on the symptoms of ADHD in children rather than understanding the perspectives and experience of children with ADHD.

Population
The population of participants included preschool-and school-aged children aged below 18 years with a formal diagnosis of ADHD.Each participant underwent a diagnosis by a qualified healthcare professional using recognized and standardized assessment procedures.

Exposure
Studies were included if they involved some type of exposure to nature (forests, parks, green spaces, gardens), and this was measured empirically either by objective measures (such as remote sensing measurements) or subjective measures (such as standardized questionnaires).

Outcome
Studies were included if they measured ADHD at a population level (such as diagnoses of prevalence) or at an individual level (measuring symptom severity).

Data Collection and Evaluation of Evidence
A meta-analysis was not possible due to the heterogeneity in methodological approaches and the diverse nature of the outcome measures used; therefore, descriptive synthesis was used.Relevant study characteristics, methodologies, and outcomes of the studies included in this review were identified, extracted manually, and compiled in a data extraction table (Table 1).Information that was extracted included the following: author(s), year of publication, country, study design, study population, sample size, exposure assessment, outcome assessment, confounding factors, and main results.This information was used to create a summary of the key characteristics, methodologies, and outcomes of the included studies.Children with ADHD concentrated better after a walk in the park than after a downtown walk (p = 0.0229, Cohen's d = 0.52) or the neighborhood walk (p = 0.0072, Cohen's d = 0.77).
The park setting was rated significantly higher than the other two settings on fun (t 13 = 2.39, p = 0.02) and marginally significantly higher on relaxing (t 14 = 1.42, p = 0.83).

Study Selection
Searching databases resulted in 996 studies (Figure 1).After the removal of 62 duplicates, the titles and abstracts of 934 papers were screened independently by two reviewers for eligibility.The information included in the titles and abstracts was considered based on the selection criteria to determine eligibility.If there was insufficient information in the title and abstract to determine clear eligibility, the full text was also screened.After screening based on titles and abstracts, 894 papers were deemed ineligible based on selection criteria.The full text of 40 articles was read to determine their eligibility, of which 7 articles were deemed eligible for inclusion.Of the articles that were read fully, 33 were excluded: 14 for ineligible study designs, 12 for the absence of a measure of nature, 5 for containing ineligible populations, and 2 for ineligible outcome measures.There was no disagreement among the two reviewers regarding study selection.

Study Selection
Searching databases resulted in 996 studies (Figure 1).After the removal of 62 duplicates, the titles and abstracts of 934 papers were screened independently by two reviewers for eligibility.The information included in the titles and abstracts was considered based on the selection criteria to determine eligibility.If there was insufficient information in the title and abstract to determine clear eligibility, the full text was also screened.After screening based on titles and abstracts, 894 papers were deemed ineligible based on selection criteria.The full text of 40 articles was read to determine their eligibility, of which 7 articles were deemed eligible for inclusion.Of the articles that were read fully, 33 were excluded: 14 for ineligible study designs, 12 for the absence of a measure of nature, 5 for containing ineligible populations, and 2 for ineligible outcome measures.There was no disagreement among the two reviewers regarding study selection.

Description of Articles
As presented in Table 1, the seven selected studies were conducted in different countries and varied considerably in study design and sample size.The majority of studies employed observational designs (five out of seven), while articles utilized experimen-tal or quasi-experimental designs (please refer to Table 1).The majority of the included articles relied on parents' self-reports with regard to ADHD diagnosis and symptoms.Four studies relied on parents to report that their child were formally diagnosed with ADHD by a physician, psychologist, pediatrician, or psychiatrist [29][30][31][32], and one study relied on parents' ratings of the frequency of symptoms to categorize children as having ADHD or not [33].More details on the parent-reported methods used in each study to determine ADHD classification can be found in Table 1.Two studies identified children with a diagnosis of ADHD from hospital records; pharmacy records containing two or more prescriptions for methylphenidate, hydrochloride, atomoxetine, or dexamfetamine sulfate [34]; and healthcare claim data [35].Only three articles conducted analyses to assess if there were differences in effects between the different subtypes of ADHD.Two of these did not find significant statistical differences [31,33], while the study by Faber Taylor and Kuo [30] found that, for children with hyperkinetic symptoms, only spaces that are both green and open lead to improvements in symptom severity.

Effects of Nature on ADHD
Despite there being differences in the design and methodology of the studies, the included articles generally reported favorable effects of nature on ADHD symptoms.Studies that categorized nature based on satellite imaging reported potentially protective and/or curative factors of higher vegetation density on ADHD [33][34][35], consistently reporting that areas with a higher density of green vegetation were associated with lower instances of ADHD symptoms.Markevych and colleagues [35] demonstrated a negative correlation between ADHD and green vegetation density, while Donovan and colleagues [34] found that children who resided in rural areas were less likely to develop ADHD.Two articles that classified natural settings as those with "big trees and grass" and "a lot of open grass" reported that children who spent time in these natural settings, as reported by their parents, had less severe symptoms of ADHD and better concentration capabilities than those who spent their time in indoor or built settings, according to their parents [30,31].Two studies that classified natural settings as "an urban park" and "an open spot in a nearby wooded area" found that children concentrated better when they were exposed to these natural settings compared to built settings and that children rated natural settings as more restorative, fun, and relaxing than the built settings [29,32].

Moderating and Confounding Variables
The included articles measured and analyzed fourteen potential moderating and/or confounding variables for their impact on the effect of nature on ADHD.Five articles included sex/gender in their analysis and all five found that there was no difference in the effect of nature on ADHD symptoms between males and females [30,31,[33][34][35].Four articles investigated the age of children as a potential moderating variable and found that there was no impact of age on the effects of nature on ADHD [31,[33][34][35].Annual household income was investigated by three articles and was found to have no impact on the effect of nature on ADHD [31,33,34].In one study, household income was found to be negatively correlated with the severity of ADHD symptoms (F (1, 386) = 4.75, p < 0.05), suggesting that children in wealthier households had milder symptoms [31].Parental education level was also measured and reported on by two studies that found it had no impact on the relationship between nature and ADHD symptoms [30,33].Yang and colleagues [33] found that the effects of nature on ADHD were not dependent on maternal smoking and alcohol consumption during pregnancy, preterm birth, birthweight, breastfeeding, or the number of siblings.Two studies did not report any investigation of confounding or moderating variables [29,32].

Discussion
ADHD is a neurodevelopmental disorder characterized by symptoms of inattention, hyperactivity, and impulsivity.Neurobiologically, ADHD has been associated with ab-normalities in brain structure and function, particularly in regions involved in executive function and attention regulation, such as the prefrontal cortex and the basal ganglia [36].Dopaminergic and noradrenergic systems, which are crucial for attention and behavioral control, are also often dysregulated in individuals with ADHD [37].Nature may influence these brain systems by providing a serene environment that reduces stress and cortisol levels, having the ability to positively affect the prefrontal cortex, which is involved in executive functions [38,39].
The reviewed literature suggests an overall favorable effect of exposure to nature on ADHD.There are, however, a variety of ways in which nature has been defined and measured in the literature, and it is useful to consider the strengths and limitations of these different approaches to help guide and refine the future research in this area.Three studies included in this review used large-scale satellite imaging to identify and classify nature based on the 'greenness' in the images [30,33,35].On the one hand, this approach has the advantage that it is objective and replicable; on the other hand, however, this analysis does not allow for a more fine-grained classification of different nature settings (e.g., large trees vs. small trees) and it ignores other aspects of nature, such as water, that are not green vegetation but may still have a beneficial effect for children with ADHD.In contrast to the satellite imaging approach, several other studies [29,31,32,34] employed a more descriptive and idiosyncratic approach to classify nature (e.g., "urban park"), which has the advantage of providing a finer-grained classification but somewhat lacks objectivity and comparability across different studies.
Furthermore, once nature has been classified, there is the question of how to quantify the exposure to it.At one end of the spectrum, there are satellite imaging studies [30,33,35], which defined exposure to nature according to the geographical location of the participants' home address.On the other end of the spectrum are studies that employed self-reports by either the researcher(s) [31,34] or parents [29,32] to quantify the exposure to nature.Weeland and colleagues [40] assessed the impacts of nature on primary school-aged children's' ability to self-regulate their emotions and found stronger positive effects when exposure was measured via parent reports than via an objective index, such as a normalized difference vegetation index.This could indicate that qualitative aspects of experiencing nature are more predictive than the quantity of vegetation.However, while self-reports provide a richer account of exposure to nature, they somewhat lack objectivity and comparability across different studies.Furthermore, in future investigations examining the impact of nature on ADHD, it is crucial to explore specific natural elements, such as bird songs and water, to thoroughly assess their therapeutic potential.
While the included studies demonstrated a clear positive effect of exposure to nature on ADHD symptoms in children, it is important to note that the reviewed studies were mostly observational.Moreover, they may not have yet captured the minimum level of exposure required to achieve an effect.A survey of the general adult population has shown that there is a dose-dependent effect for the duration spent in nature on the prevalence of depression [41].Many families may have difficulty accessing nature, and schools as well as other communities have typically limited resources.Therefore, it is important to establish a minimum intensity and duration of exposure to nature to provide an understanding with regard to the effects on ADHD symptomology that can be achieved, even with minimal interventions.Additionally, it would be useful to measure the longevity of these effects by using a longitudinal design, with follow-up measures.This would help inform real-world applications with regard to how often this intervention may need to be re-administered, if at all.It is also important to acknowledge that the reviewed studies do not allow for investigating how much the effects are caused by activities in nature or by nature alone, which is a topic that should be addressed by future research.
It Is also important to note that ADHD is a heterogeneous disorder with diverse expressions of symptom domains.Only three of the reviewed studies considered the effects of ADHD subtypes.Future studies should therefore evaluate the benefits of nature while considering the heterogeneity in the symptomology of this disorder.In this context, it is also relevant to highlight the new Research Domain Criteria (rDoC) framework of the USAbased National Institute of Mental Health, which focuses on investigating dimensional biological, physiological, and behavioral mental health factors instead of heterogenous symptom-based diagnostic categories [42].In line with this approach, it might be fruitful to analyze effects across a spectrum of psychological functioning, irrespective of boundaries for distinct ADHD subtypes [43].Moreover, only three out of the seven studies assessed the medication status of the participants.Among these, none analyzed medication as a moderating factor.Future studies should therefore address this gap by including medication status in their analyses to better understand its potential moderating effects.
Finally, in terms of limitations, this review was based on the analysis of only seven articles, which restricts the robustness of our conclusions.However, it remains crucial to summarize the available literature and identify areas for future research.

Conclusions
The exploration of how best to manage and treat ADHD in children is ongoing; therefore, the findings reviewed here about the benefits of nature regarding ADHD symptoms are relevant and encouraging.While further research should be conducted to support a causal effect and provide better insight into the mechanisms behind this, there is strong enough evidence to begin implementing this approach into practice for use alongside already established treatments for ADHD.One way this could be implemented is by incorporating nature into behavioral interventions by recommending an increase in exposure to nature as a method of management in itself, or by increasing the presence of nature in therapeutic spaces.In general, incorporating elements of nature in the design of built environments, such as indoor plants, water features, large windows with natural light, etc., would allow children who live in urban areas to receive the benefits of exposure to nature that they otherwise would not have.Using this in areas we know children with ADHD spend time, such as schools, homes, and therapy rooms, could be one way in which children with ADHD could be subjected to the benefits highlighted in this review.Exposure to nature should be embraced as an additional approach to managing ADHD in children and adolescents to complement and enhance the existing treatment approaches.Moreover, it should be implemented at an individual and wider community level to allow individuals with ADHD to experience the benefits of nature.