The importance of the exposome and allostatic load in the planetary health paradigm

The importance of the exposome and allostatic load in the planetary health paradigm In 1980, Jonas Salk (1914–1995) encouraged professionals in anthropology and related disciplines to consider the interconnections between “planetary health,” sociocultural changes associated with technological advances, and the biology of human health. The concept of planetary health emphasizes that human health is intricately connected to the health of natural systems within the Earth’s biosphere; experts in physiological anthropology have illuminated some of the mechanisms by which experiences in natural environments (or the built environment) can promote or detract from health. For example, shinrin-yoku and related research (which first emerged from Japan in the 1990s) helped set in motion international studies that have since examined physiological responses to time spent in natural and/or urban environments. However, in order to advance such findings into planetary health discourse, it will be necessary to further understand how these biological responses (inflammation and the collective of allostatic load) are connected to psychological constructs such as nature relatedness, and pro-social/ environmental attitudes and behaviors. The exposome refers to total environmental exposures—detrimental and beneficial—that can help predict biological responses of the organism to environment over time. Advances in “omics” techniques—metagenomics, proteomics, metabolomics—and systems biology are allowing researchers to gain unprecedented insight into the physiological ramifications of human behavior. Objective markers of stress physiology and microbiome research may help illuminate the personal, public, and planetary health consequences of “extinction of experience.” At the same time, planetary health as an emerging multidisciplinary concept will be strengthened by input from the perspectives of physiological anthropology. Keywords: Allostatic load, Exposome, Nature relatedness, Health disparities, Ecology, Non-communicable diseases, Dysbiosis, Natural environments Background In the quote above, found within a nearly 40-year-old medical anthropology textbook, Jonas Salk introduces “Sophisticated technology, intended to advantages for the term “planetary health” into multidisciplinary re- humankind, sometimes has had unforeseen adverse search. Although best known for developing the vaccine effects on human health...[environmental degradation] that helped to eradicate polio, Salk spent large portions threatens human and planetary health. The latter of his scientific career championing the idea that human must also be added to the consideration of biological health is dependent upon biodiversity and healthy eco- and sociocultural influences on health throughout the systems. Moreover, he argued that the human body was human life span” [1]. an extension of the functioning whole of the external en- vironments—including its biodiversity, social policies, Jonas Salk, MD, 1980 and cultural practices: “We must see ourselves as part of the ecosystem. Where we were once a product of evolu- tion, we are now part of the process” [2]. In underscor- * Correspondence: aclnd@cfs-fm.org ing planetary health in medical anthropology, Salk was In-VIVO Global Initiative, Research Group of the Worldwide Universities Network (WUN), 6010 Park Ave, Suite #4081, West New York, NJ 07093, USA referring to the health of the Earth’s natural systems as Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Logan et al. Journal of Physiological Anthropology (2018) 37:15 Page 2 of 10 an upstream driver of human health and vitality. He em- an environment formerly rich in biodiversity), and thus, phasized the need to study the interconnected biological a “baseline” awareness of the health of nature by succes- (hence, physiological), social, and cultural aspects of sive generations is reset in a way that underestimates the health from the planetary health perspective. full extent of degradation. While the term planetary health has since been used Next, we focus on the exposome and recent findings in by many different scientific, health, and environmental the science of allostatic load, underscoring how the total advocacy groups—each generally referring to the health lived experience of individuals—including missed oppor- of ecosystems within the biosphere [3]—the 2015 Lancet tunities and experiences—influences health at the personal, Commission on Planetary Health report formally defined public, and planetary scales. Alterations in biological re- the planetary health paradigm as “the health of human sponses to the modern environment—immune and ner- civilization and the state of the natural systems on which vous system functioning in particular—can drive low-grade it depends” [4]. Put simply, there is no human health inflammation which, in turn, can compromise mental without planetary health. Of high-level relevance to health. However, under the rubric of “extinction of experi- physiological anthropology, the Lancet Commission on ence,” the extent to which humans in westernized and in- Planetary Health report also emphasizes integration of dustrialized nations are aware of connections between biological, social, and cultural aspects of health in the health of self and biodiversity may be increasingly obscured. modern environment. Further, the report “accepts the Thus, it is our contention that progress toward the goals of complexity and non-linearity of the dynamics of natural planetary health is predicated upon a greater understanding systems” and underscores the need to study potential of how collected experiences in the natural environment in- health benefits derived from the maintenance and res- fluence physiology and behavior (Fig. 1). toration of natural systems. Physiological anthropology will play an important role Extinction of experience in the emergent planetary health paradigm; indeed, for the last several decades, physiological anthropology has “I would like to say”. been a leading contributor in understanding the physio- logical consequences of modern pressures placed upon Coyote is forever. humans. Specifically, physiological anthropology has fo- cused on the ways in which the modern environment— Inside you. with its high technology, dominance of ultra-processed foods, and diminished human contact with biodiver- “But it’s not true”. sity—can impact upon normal physiological functioning; understanding the gulf between the psychological and Gary Snyder, “The Call of the Wild”, 1974 physiological requirements of individuals—and the (in)- ability of the modern environment to help fulfill those Salk maintained that scientists should look toward the needs—is central to the aims of physiological anthropol- arts and humanities in order to identify fundamental ogy [5]. Since biological responses are a product of our questions worthy of scientific pursuit [6]. In this context, ancestral past, signs of metabolic dysregulation can un- veil an evolutionary mismatch that otherwise contributes to a global epidemic of NCDs. Roadmap to the current review Here in our narrative review and commentary, we illus- trate the importance of physiological anthropology in the context of planetary health. In order to emphasize this connection, we first discuss “extinction of experi- ence” with nature, a term which loosely describes the loss of experiential contact with biodiversity and natural environments. The term is related to other theories and phrases such as “shifting baseline syndrome” and “envir- onmental generational amnesia” which propose that in- dividuals gauge their perceptions (of, for example, Fig. 1 How does accumulated experience (or lack thereof) in the biodiversity losses or environmental degradation) from modern environment influence human physiology and help their own experiences in the surrounding environment; illuminate the links between personal, public, and planetary health? it is difficult to truly appreciate “what once was” (that is, Logan et al. Journal of Physiological Anthropology (2018) 37:15 Page 3 of 10 we highlight the work of scholar, environmentalist, and that declines in local biodiversity and environmental deg- Pulitzer-prize-winning poet Gary Snyder; greatly influ- radation are associated with greater time spent indoors enced by his many years living in Japan, studying the [19]; since lack of time spent outdoors is associated with rich biodiversity of the land, Snyder’s versification chronic disease [20], this could present a double burden through the 1950s–1960s celebrated the ways in which of increased risk of NCDs and decreased the awareness of our ancestral experience in natural environments could further threats to local and global biodiversity. The best reassert itself (in the form of vitality and joy) when evidence of extinction of experience has emerged from primed. This, according to Snyder, was most obvious Japanese research; using a range of 21 different neighbor- when an individual was once again immersed in nature hood flowering plants as a measure of interaction with [7]. However, in his later Pulitzer-winning book Turtle visible aspects of biodiversity, researchers have shown an Island (1974), Snyder expressed concern about the age-related, cross-generational decline in childhood trans-generational loss of experience with nature, and experiences with nature [21]. International research the subsequent ability of nature’s deep (albeit hidden) demonstrates that such neighborhood changes may be resonance—the coyote as a metaphor—to survive in compounded by cultural changes in media representations post-modern humans [8, 9]. of biodiversity which focus only on a miniscule sliver of Several years later, scientist Robert Pyle coined a term for well-known species [22–24]. this hypothesis—“extinction of experience.” Writing in Extinction of experience is, of course, worrisome from a Horticulture (1978), Pyle stated that the disappearance of conservation perspective; the ability to develop an emo- neighborhood biodiversity was a threat to the “collective tional connection with the natural world (measurable with psyche” and that its represented “the loss of opportunities - the psychological construct of nature-relatedness [25])— the extinction of experience”; in particular, Pyle was con- and subsequently develop pro-environmental attitudes cerned about vanishing opportunities for children, “the and behaviors—is dependent upon experience [26]. Na- ones whose sensibilities must be touched by the magic re- ture relatedness (see also nature connectivity, nature con- action with wildlife if biologists, conservationists and con- nectedness) allows researchers to determine individual cerned citizens are not to become endangered themselves. levels of awareness of, and fascination with, the natural What is the extinction the condor to a child who has never world; nature relatedness also captures the degree to seen a wren?” [10]. The concept of extinction of experience which subjects in research studies have an interest in mak- has been expanded upon, but the primary theme remains ing contact with nature. From the planetary health per- the same—loss of direct, personal, cognitive-emotional con- spective, nature relatedness is positively associated with tact with wildlife and elements of the natural world could empathy, pro-environmental attitudes, and humanitarian- lead to disaffection, apathy, and irresponsibility in behaviors ism (and negatively with materialism) [27–29]. However, toward the environment [11, 12]. nature relatedness is also highly relevant to physiological At the same time, a related hypothesis was expanding; anthropology, and human biology in general, because a the hygiene hypothesis and its variants proposed that substantial body of research has linked appreciation of diminishing early life exposures to microbes—due to a (and relatedness to) the natural environment with general more “sanitized” environment, antibiotic use, smaller fam- health and mental wellbeing [30, 31]. ily sizes, and lower exposure to bacteria in foods and the Sitting in parallel to research on the psychology of na- overall environment—could compromise normal training ture relatedness—unintegrated into the planetary health of the immune system. The recent biodiversity hypothesis paradigm—is a growing body of in vivo research involving updates and unifies this proposal by emphasizing that bio- physiological endpoints which demonstrate that time diversity losses at the neighborhood scale could translate spent in natural environments might be protective against into loss of contact with microbiotic diversity. Specifically, allostatic load (described in more detail shortly). While “biodiversity loss leads to reduced interaction between en- there are now many studies in this realm, it is perhaps best vironmental and human microbiotas. This in turn may exemplified by shinrin-yoku (now generally referred to in lead to immune dysfunction and impaired tolerance Japanese studies as simply “forest medicine” or “forest mechanisms in humans” [13, 14]. However, research in therapy”)research; shinrin-yoku loosely translates from the more biologically oriented biodiversity hypothesis and Japanese as forest-air bathing or “absorbing the forest air” the more psychologically oriented extinction of experience and places emphasis on the entire forest experience hypothesis has largely remained separated in silos. wherein the individual tales in all the “components emit- In the twenty-first century, there have been several stud- ted from the forest” [32]. Studies under the rubric of shin- ies which support the idea that adults and children in rin-yoku have shown that spending time in a forest westernized, industrial, and technologically mature na- environment can beneficially influence stress physiology, tions are spending more time indoors [15, 16] and less markers of inflammation, immune defenses, blood pres- time in natural environments [17, 18]. There are also hints sure, and heart rate variability [33–40]. Logan et al. Journal of Physiological Anthropology (2018) 37:15 Page 4 of 10 To appreciate the contribution of shinrin-yoku and re- It is our contention that an “exposome perspective” will lated research, consider that a 2018 systematic review help break down silos and incorporate the ongoing work identified a total of 43 studies which measured physio- of physiological anthropology into planetary health. The logical and psychological stress responses to outdoor en- exposome refers to the science of accumulated “expo- vironments—nearly half of the studies were conducted sures” (meaning both emotional experiences and physical/ in Japan [41]. Although limited by small sample sizes, sensory exposures) over time. As we explain below, this these and other studies with physiological endpoints view emphasizes that genes alone cannot explain health provide potential mechanistic pathways (e.g., immune disparities and underscores that each individual exposure activation, oxidative stress, blood pressure, cortisol re- (e.g., airborne particulate matter or fast-food, beneficial sponse) for the associative links between green space microbes, or phytoncides) does not occur independent of and health in large epidemiological studies [42]. More- the total environment. Moreover, from the physiological over, these studies can be viewed in the context of stud- perspective, the most direct path to understanding the ies which link markers of biodiversity with mental and connections between personal and planetary health—gains physical health [43, 44]. On the other hand, relatively and losses from extinction of certain experiences and the rapid environmental degradation and/or visible losses in birth and flourishing of others—may be to examine allo- species (e.g., the loss of millions of ash trees due to the static load (the physiology associated with the “wear and invasive emerald ash borer) are linked to declines in tear” of stress). We will elaborate on this shortly. physical and mental health [45–47]. Extinction of experience research also forces questions Exposome concerning shifting cultural norms and time use; in other words, if time spent in outdoors in nature is being “Human biology should be primarily concerned with displaced, then how specifically is that time displaced? the responses that the body and the mind make to the These are connected conversations. For example, excess surroundings and ways of life…little effort has been screen time and problematic smartphone use is linked made to develop methods for investigating with lower levels of personal nature relatedness [48]. It scientifically the interrelatedness of things. is also important to point out that “extinction of experi- Epidemiological evidence leaves no doubt that many ence” is not exclusive to psychological losses in contact chronic and degenerative disorders which constitute with biodiversity (or even biodiversity per se); it could be the most difficult and costly medical problems of our argued that for children in westernized nations, the loss societies have their origin in the surroundings and in of whole plant foods (relatively unprocessed, high in the ways of life rather than in the genetic constitution fiber) in the dietary and the massive encroachment of of the patient. But little is known of these the “invasive species” known as ultra-processed foods environmental determinants of disease” [54]. (which now dominate the nutritional landscape, like weeds, displacing nutrient-dense foods) is also an extinc- Rene J. Dubos, PhD, 1969 tion of experience [49]. Moreover, from the biological perspective, urbanization and loss of contact with bio- While he did not coin the term “exposome,” micro- diversity [50]—as well as related changes to contact with biologist and environmentalist Rene Dubos (1901–1982) diversity of the microbiome [51, 52]—could be viewed as urged scientists to study the response of the “total or- an “immunological extinction of experience.” ganism to the total environment” [55]; Dubos, of course, Since the health benefits derived from experiences in not only celebrated the value of single-variable studies natural environments may be determined by baseline na- but also warned of their limitations in the context of ture relatedness [53], researchers will need to examine chronic diseases, environmental degradations, and the the physiological consequences of the interplay between complexities of the human condition [56, 57]. Today, the presence (use) of certain technologies and the ab- the total accumulated environmental exposures (both sence (disuse) of natural environments and biodiversity. detrimental and beneficial) that can help predict the bio- Thus, the challenge for physiological anthropology in logical responses of the “total organism to the total en- the context of planetary health is to help bridge the vironment” over time are referred to as the exposome knowledge gaps between three large, research-based [58]. The temporal aspect of exposome science is im- silos—that is, (1) the psychological and cognitive aspects portant because the physiological responses of the hu- of nature relatedness and the loss of experience, (2) the man organism are a product of accumulated experiences physiological pathways involved in the risk of NCDs, and may differ across time depending on shifting envir- and (3) the ways in which human health and wellbeing onmental variables. The interpretation of stress physi- are, emotionally and biologically, predicated upon bio- ology in the here-and-now requires an understanding of diversity and the health of the Earth’s natural systems. the interplay between time scales of stress, including but Logan et al. Journal of Physiological Anthropology (2018) 37:15 Page 5 of 10 not limited to early life stress, acute and chronic Allostatic load stressors, experience of daily hassles, and the aggregate Human responsiveness to environmental threats has of life events [59]. been shaped by experience over millennia. In particular, The term exposome is now an essential feature of the an elegant and active process of allostasis—the normal planetary health discourse because it helps to demonstrate initiation, orchestration, and termination of neuroendo- why genome-wide association studies cannot explain the crine, metabolic, autonomic, and immune “mediators”— reasons for health disparities; it also helps us understand helps ensure a physiological state which supports sur- why NCDs are increasing over time and in non-random vival. Acutely, these multisystem physiological responses ways. In particular, the burden of NCDs, especially in to stress are, under normal circumstances, effectively ini- westernized nations, is most often shouldered by disad- tiated, maintained, and extinguished without harm. vantaged populations [58]. Furthermore, the exposome However, with repetitive and/or prolonged stimulation view of total health encompasses the World Health Orga- in the modern environment, these compensatory physio- nization’s interpretation of the word health; that is, not logical responses can lead to metabolic disturbances and simply the absence of specific disease criteria, but rather cellular damage. The collective toll of this physiological the fulfillment of human potential. Although genetics wear and tear—including the associated consequences of matter, health includes a state of complete physical, men- unhealthy lifestyle choices which compound the physio- tal, and social wellbeing—it is not a genetic trait. logical dysregulation—is known as allostatic load [64]. Rather, the study of physiology related to health promo- Over time, the combined disturbances of allostatic load tion and/or risk is better understood when it is placed into leads to allostatic overload and contribute to altered be- the context of the total exposures experienced by havior and disease risk [65]. humans—some positive, some negative—and their interac- Epidemiological research indicates that links between tions with genes over time [60]. From a life-course perspec- lower socioeconomic position and disease mortality are tive, exposome science emphasizes that certain windows of mediated by allostatic load [66]. In other words, socio- vulnerability (for disease risk) and opportunity (for health economic advantage is associated with lower allostatic promotion) are especially important [61]. In the context of load, which is in turn link to lowered risk of mortality. physiological anthropology, thismeansthat socioeconomic Such findings are supported by volumes of research indi- advantage or disadvantage can produce differing biological cating that disadvantage is accompanied by chronic psy- responses to specific “beneficial” or “detrimental” expo- chosocial stress and daily hassles, lower optimism (an sures—e.g., spending time in nature or consuming a asset in physical and mental health), and significantly fast-food meal—depending on many other background higher biomarkers of metabolic dysregulation, inflamma- variables. tion, and oxidative stress [67–74]. Indeed, within The interplay of these potentially beneficial and detri- westernized-industrialized nations, allostatic load ap- mental experiences is central to the concept of resili- pears to bear witness to the ways in which socioeco- ency; as researchers explore how and why positive nomic disadvantage “gets under the skin” and “into the adaptation and outcomes occur in the face of adversities, gut,” ultimately decreasing longevity [66, 75]. and why certain individuals (who score high on validated These links with socioeconomic disadvantage have resiliency scores) seem protected against the negative been found at the individual and neighborhood levels; health-related consequences of adverse events, it will be for example, allostatic load persists in low-income necessary to tease apart the ways in which resiliency is neighborhoods even after adjusting for individual-level built in the first place [62]. The available evidence allows income. Beyond income, anxious arousal is linked to for the hypothesis that exposure to elements of natural allostatic load, as well as other lifestyle factors such environments—e.g., microbial—can play a role in resili- as fast-food consumption, exercise habits, and smok- ency. Indeed, early-life exposure to diverse microbes ing [76]; moreover, neighborhood-level income is as- found in natural environments is part of the normal sociated with better physical and mental health over “training” of the immune system, and it may decrease time [77]. Since allostatic load transcends purely gen- vulnerability to later life stress-associated disorders; for etic influences [78], it reinforces the exposome per- example, researchers have found that urban upbringing spective and underscores the need to consider the without pets (vs. rural upbringing around animals) is as- context in which exposures are experienced. More- sociated with compromised resolution of systemic im- over, it also allows for the introduction of epigenetic mune activation (low-grade inflammation) following an research and opportunities to determine how expo- experimenter-induced social stress [63]. To further ap- sures (age, diet, physical activity, time in nature, posi- preciate the saliency of how accumulated experiences in- tive and/or negative emotions, and accumulated fluence physiology in the total environment, we can look experiences) modify DNA methylation, which in turn, to research on allostatic load. alters gene expression [79]. Logan et al. Journal of Physiological Anthropology (2018) 37:15 Page 6 of 10 Putting it all together, future directions non-harmful microbes that may influence health and be- The biological underpinnings of the exposome perspec- havior [97–100]. However, these studies are missing key tive indicate that the extent to which an organism can bits of information; how do measurements on the psycho- buffer against the detrimental physiological conse- logical construct of nature relatedness—and responses re- quences of particular exposures will determine the risk lated to extinction of experience at the neighborhood of NCDs [58]. Hence, it is essential to understand how level—match up with the objective markers of allostatic certain psychological “assets”—such as nature related- load, epigenetics and the microbiome? Does the ness, positive emotions, mindfulness, and optimism—are age-related decline in direct experiences with neighbor- accumulated and employed to act as physiological hood biodiversity manifest physiologically (allostatic load), buffers in the modern environment. The available re- and if so, are there connections between allostatic load search, outlined above, suggests that scientists need to and nature relatedness? look more closely at the total lived experience of individ- These are essential questions for the planetary health uals, and the total environment which surrounds them. paradigm. So far, the research focus on the human From the planetary health perspective, this means look- emotional connections to nature/local lands in the con- ing at the presence (or absence) of natural environments text of planetary health (exemplified by content within and specific features of the built environment that might the aforementioned and highly cited Lancet Commis- offset (or contribute to) allostatic load. sion on Planetary Health report) has been on the real Looking at research from the exposome perspective al- and potential mental health consequences of environ- lows researchers to consider the “big picture” and intercon- mental degradation. Although there is good research on nectivity of humankind’s most pressing problems. For the psychological aspects of pro-environmental and example, living closer to green space and having greater ac- pro-social beliefs and behaviors, its place in the dis- cess to safe, local parks, and open space is associated with course of planetary health is minimal. Moreover, the health in general and mental health in particular [80]. How- wealth of information gathered in the field of physio- ever, the presence of green space may be a surrogate marker logical anthropology (and related disciplines) on differ- for healthier dietary habits, lower density of fast-food out- ential physiological responses to natural and built lets, and better access to healthy foods [81–83]. environments (e.g., shinrin-yoku,forest bathing re- Consider also the psychological asset of optimism search) has not penetrated the planetary health dis- which we have alluded to several times; optimism is gen- course. In addition to nature relatedness, the inclusion erally defined as positive outcome expectancy for future of other psychological constructs in the literature, espe- events across life domains. Optimism has been linked to cially those investigating place attachment measure- lower body mass index and lower rates of chronic dis- ments (e.g., topophilia scales) [101, 102], will help ease and all-cause mortality [84–88]. In the physiological provide a better understanding of how physiological realm, optimism is linked to optimal metabolic markers endpoints might match individual and community-level of cardiovascular health, lower inflammatory cytokine emotional connections to the land. and C-reactive protein levels, and lower inflammatory We suspect that the absence of cohort studies which sim- response to experimental stress [89–91]. Research sug- ultaneously measure deep aspects of socioeconomic histor- gests that optimism is only about 25% heritable, leaving ies, allostatic load (and other objective markers such as the plenty of room for the influence of the total lived experi- microbiome), residential proximity to “assets” (green space) ence over time; indeed, higher levels of optimism are as- and “liabilities” (clustering of fast-food outlets), along with sociated with socioeconomic advantage [92, 93]. Since measures of positive psychology/nature-relatedness/envir- optimism is malleable [94], experts in physiological an- onmental attitudes is a barrier to multidisciplinary break- thropology might query on biological links between opti- throughs in planetary health. Available research indicates mism, nature relatedness, and extinction of experience. that the loss of experience (especially immunological) can For example, higher levels of optimism are associated shape acute biological responses in context over time; as we with protection against the detrimental effects of envir- have pointed out previously, these are intertwined with in- onmental toxins (this appears to operate through epi- come, education, race, immigrant status/segregation, social genetic mechanisms) [95]. cohesion, evaluations of neighborhood esthetic quality, and/ Scientists are beginning to tie these strands together; for or aspects of neighborhood safety (both real and perceived) example, researchers have found that close residential [103]. While constituents of a diet which simultaneously proximity to vegetated land cover is associated with lower promotes human and planetary health is generally agreed allostatic load and depression [96]. In addition, researchers upon [104–106], less is known concerning the ways in have begun to establish links between residential (or which nature relatedness, optimism, and pro-environmental school) proximity and green vegetation—and degrees of attitudes/behaviors and allostatic load intersect with adher- neighborhood urbanization—with exposure to diverse, ence to such a diet. Logan et al. Journal of Physiological Anthropology (2018) 37:15 Page 7 of 10 Macro-scale, multi-factorial, multi-indicator consider- Conclusion ations such as the exposome, allostatic load, and planetary Scientifically, the grand challenges of our time—environ- health present enormous challenges; it is easy to criticize mental degradation, a global non-communicable disease such efforts because they include an essentially unlimited (NCD) epidemic, gross biodiversity losses, climate array of variables. While single-variable studies remain es- change, health and other socioeconomic inequalities— sential to scientific knowledge, large cohort studies are are adisciplinary. In other words, these challenges are enjoying remarkable advances in “omics” research; clinic- overlapping, and their causative complexities suggests ally meaningful data sets are emerging from the analysis that they will not be solved by linear research which of functional proteins (proteomics), metabolites (metabo- otherwise remains in silos. The extinction of experience lomics), gene expression (epigenomics, transcriptomics), perspective suggests that each generation may accept the and genetic influences on specific drugs or nutrients inherited state of their environment with a greater sense (pharmacogenomics) [107]. For example, large datasets in of “normalcy”; while experts in biodiversity conservation the area of the microbiome have provided clinically rele- have a keen interest in extinction of experience research, vant information which may predict an individual’s a greater understanding of its physiological underpin- physiological responses to foods [108]. Thus, the ability of nings seem necessary. researchers to match environmental attitudes, nature re- In our narrative review and commentary, we have latedness, and other psychological indicators (based on ex- pointed to research on extinction of experience, nature re- perience or lack thereof) with important aspects of latedness, and the science of allostatic load to argue for a physiology at the individual and community-level is on stronger presence of physiological anthropology in the the horizon [58]. planetary health paradigm. Over time, the burdensome bio- As researchers begin to incorporate research on expo- logical consequences of detrimental exposures (and absence sures and experiences into the planetary health perspec- of beneficial exposures and psychological assets) will press tive—including studies on physiological endpoints, upon those with higher allostatic load, translating into a resiliency, and allostatic load—we will also learn more biologically corrosive allostatic overload. While physio- concerning realistic expectations concerning the role of logical anthropology has made tremendous contributions natural environments and health outcomes; access to to the understanding of mechanisms that help explain the green space is important, but there are many factors that ways in which experience in natural environments (or ex- push health inequalities and social injustices, including posure to individual constituent parts of nature) promote those that may have far more corrosive effects on health. health, many gaps remain. In particular, a more persuasive We may have unwittingly given the impression that the argument for the connections between personal, public, health implications of experiences, exposures, and allo- and planetary health could be made via more detailed static load are linear—that is, where more of a certain understanding of the biological pathways between nature sort of experience/exposure is better or the more of an- relatedness, changing levels of local biodiversity, and allo- other sort of experience or load is worse. These are not static load. aggregate responses with a universal dose-response rela- The prospect of personalized medicine test results tionship; indeed, researchers are already discovering that (based on physiological responses and large datasets) the potential benefits of nature are not found along a may provide much-needed incentives to motivate indi- neat continuum of benefit [109, 110]. viduals to change lifestyle behaviors that are in the inter- Finally, this entire conversation can be viewed through est of personal and planetary health. The challenge is to an evolutionary lens. What we need to eat—as opposed illuminate the direct links between elements of natural to the ultra-processed foods that surround us—is what environments with measurable parameters of human we are adapted to eat. The exercise we need is obviously health; having “lab results” in hand may help individuals, part-and-parcel of the physical activity to which we are communities, clinicians, and policy-makers to under- adapted; corals and mussels need not count steps! So, stand the direct lines between personal, public, and too, our requirements for the natural settings to which planetary health. In the meantime, the available evidence we are adapted can be viewed, scientifically, from the which supports the biodiversity hypothesis is not calling evolutionary perspective and can help guide future re- for a “back to nature” movement, but rather stepping search questions. It allows us to ask “why do we humans “forward with nature” in the urbanized environment. need nature to be whole?” in modernity. The answer is With the momentum initiated by the 2015 Lancet Com- blowing in the wind, complete with microbes, natural mission on Planetary Health report (now cited over 300 light, and phytoncides, because we are adapted to it as a times on Google Scholar), the counsel of Jonas Salk to part of us, and us as a part of it—for all the same rea- bring planetary health into alignment with the biological sons we need to breathe the atmosphere native to the and socio-cultural objectives of anthropology seems wise. planet that generated us. At the same time, the multidisciplinary effort of planetary Logan et al. Journal of Physiological Anthropology (2018) 37:15 Page 8 of 10 health (adisciplinary in nature, planetary health cannot be 7. Yamazato K. Seeking a fulcrum: Gary Snyder and Japan (1956-1975). Davis: University of California Press; 1987. viewed as a single discipline) should draw upon the ex- 8. Snyder G. Turtle Island. 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The importance of the exposome and allostatic load in the planetary health paradigm

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Abstract

In 1980, Jonas Salk (1914–1995) encouraged professionals in anthropology and related disciplines to consider the interconnections between “planetary health,” sociocultural changes associated with technological advances, and the biology of human health. The concept of planetary health emphasizes that human health is intricately connected to the health of natural systems within the Earth’s biosphere; experts in physiological anthropology have illuminated some of the mechanisms by which experiences in natural environments (or the built environment) can promote or detract from health. For example, shinrin-yoku and related research (which first emerged from Japan in the 1990s) helped set in motion international studies that have since examined physiological responses to time spent in natural and/or urban environments. However, in order to advance such findings into planetary health discourse, it will be necessary to further understand how these biological responses (inflammation and the collective of allostatic load) are connected to psychological constructs such as nature relatedness, and pro-social/ environmental attitudes and behaviors. The exposome refers to total environmental exposures—detrimental and beneficial—that can help predict biological responses of the organism to environment over time. Advances in “omics” techniques—metagenomics, proteomics, metabolomics—and systems biology are allowing researchers to gain unprecedented insight into the physiological ramifications of human behavior. Objective markers of stress physiology and microbiome research may help illuminate the personal, public, and planetary health consequences of “extinction of experience.” At the same time, planetary health as an emerging multidisciplinary concept will be strengthened by input from the perspectives of physiological anthropology. Keywords: Allostatic load, Exposome, Nature relatedness, Health disparities, Ecology, Non-communicable diseases, Dysbiosis, Natural environments Background In the quote above, found within a nearly 40-year-old medical anthropology textbook, Jonas Salk introduces “Sophisticated technology, intended to advantages for the term “planetary health” into multidisciplinary re- humankind, sometimes has had unforeseen adverse search. Although best known for developing the vaccine effects on human health...[environmental degradation] that helped to eradicate polio, Salk spent large portions threatens human and planetary health. The latter of his scientific career championing the idea that human must also be added to the consideration of biological health is dependent upon biodiversity and healthy eco- and sociocultural influences on health throughout the systems. Moreover, he argued that the human body was human life span” [1]. an extension of the functioning whole of the external en- vironments—including its biodiversity, social policies, Jonas Salk, MD, 1980 and cultural practices: “We must see ourselves as part of the ecosystem. Where we were once a product of evolu- tion, we are now part of the process” [2]. In underscor- * Correspondence: aclnd@cfs-fm.org ing planetary health in medical anthropology, Salk was In-VIVO Global Initiative, Research Group of the Worldwide Universities Network (WUN), 6010 Park Ave, Suite #4081, West New York, NJ 07093, USA referring to the health of the Earth’s natural systems as Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Logan et al. Journal of Physiological Anthropology (2018) 37:15 Page 2 of 10 an upstream driver of human health and vitality. He em- an environment formerly rich in biodiversity), and thus, phasized the need to study the interconnected biological a “baseline” awareness of the health of nature by succes- (hence, physiological), social, and cultural aspects of sive generations is reset in a way that underestimates the health from the planetary health perspective. full extent of degradation. While the term planetary health has since been used Next, we focus on the exposome and recent findings in by many different scientific, health, and environmental the science of allostatic load, underscoring how the total advocacy groups—each generally referring to the health lived experience of individuals—including missed oppor- of ecosystems within the biosphere [3]—the 2015 Lancet tunities and experiences—influences health at the personal, Commission on Planetary Health report formally defined public, and planetary scales. Alterations in biological re- the planetary health paradigm as “the health of human sponses to the modern environment—immune and ner- civilization and the state of the natural systems on which vous system functioning in particular—can drive low-grade it depends” [4]. Put simply, there is no human health inflammation which, in turn, can compromise mental without planetary health. Of high-level relevance to health. However, under the rubric of “extinction of experi- physiological anthropology, the Lancet Commission on ence,” the extent to which humans in westernized and in- Planetary Health report also emphasizes integration of dustrialized nations are aware of connections between biological, social, and cultural aspects of health in the health of self and biodiversity may be increasingly obscured. modern environment. Further, the report “accepts the Thus, it is our contention that progress toward the goals of complexity and non-linearity of the dynamics of natural planetary health is predicated upon a greater understanding systems” and underscores the need to study potential of how collected experiences in the natural environment in- health benefits derived from the maintenance and res- fluence physiology and behavior (Fig. 1). toration of natural systems. Physiological anthropology will play an important role Extinction of experience in the emergent planetary health paradigm; indeed, for the last several decades, physiological anthropology has “I would like to say”. been a leading contributor in understanding the physio- logical consequences of modern pressures placed upon Coyote is forever. humans. Specifically, physiological anthropology has fo- cused on the ways in which the modern environment— Inside you. with its high technology, dominance of ultra-processed foods, and diminished human contact with biodiver- “But it’s not true”. sity—can impact upon normal physiological functioning; understanding the gulf between the psychological and Gary Snyder, “The Call of the Wild”, 1974 physiological requirements of individuals—and the (in)- ability of the modern environment to help fulfill those Salk maintained that scientists should look toward the needs—is central to the aims of physiological anthropol- arts and humanities in order to identify fundamental ogy [5]. Since biological responses are a product of our questions worthy of scientific pursuit [6]. In this context, ancestral past, signs of metabolic dysregulation can un- veil an evolutionary mismatch that otherwise contributes to a global epidemic of NCDs. Roadmap to the current review Here in our narrative review and commentary, we illus- trate the importance of physiological anthropology in the context of planetary health. In order to emphasize this connection, we first discuss “extinction of experi- ence” with nature, a term which loosely describes the loss of experiential contact with biodiversity and natural environments. The term is related to other theories and phrases such as “shifting baseline syndrome” and “envir- onmental generational amnesia” which propose that in- dividuals gauge their perceptions (of, for example, Fig. 1 How does accumulated experience (or lack thereof) in the biodiversity losses or environmental degradation) from modern environment influence human physiology and help their own experiences in the surrounding environment; illuminate the links between personal, public, and planetary health? it is difficult to truly appreciate “what once was” (that is, Logan et al. Journal of Physiological Anthropology (2018) 37:15 Page 3 of 10 we highlight the work of scholar, environmentalist, and that declines in local biodiversity and environmental deg- Pulitzer-prize-winning poet Gary Snyder; greatly influ- radation are associated with greater time spent indoors enced by his many years living in Japan, studying the [19]; since lack of time spent outdoors is associated with rich biodiversity of the land, Snyder’s versification chronic disease [20], this could present a double burden through the 1950s–1960s celebrated the ways in which of increased risk of NCDs and decreased the awareness of our ancestral experience in natural environments could further threats to local and global biodiversity. The best reassert itself (in the form of vitality and joy) when evidence of extinction of experience has emerged from primed. This, according to Snyder, was most obvious Japanese research; using a range of 21 different neighbor- when an individual was once again immersed in nature hood flowering plants as a measure of interaction with [7]. However, in his later Pulitzer-winning book Turtle visible aspects of biodiversity, researchers have shown an Island (1974), Snyder expressed concern about the age-related, cross-generational decline in childhood trans-generational loss of experience with nature, and experiences with nature [21]. International research the subsequent ability of nature’s deep (albeit hidden) demonstrates that such neighborhood changes may be resonance—the coyote as a metaphor—to survive in compounded by cultural changes in media representations post-modern humans [8, 9]. of biodiversity which focus only on a miniscule sliver of Several years later, scientist Robert Pyle coined a term for well-known species [22–24]. this hypothesis—“extinction of experience.” Writing in Extinction of experience is, of course, worrisome from a Horticulture (1978), Pyle stated that the disappearance of conservation perspective; the ability to develop an emo- neighborhood biodiversity was a threat to the “collective tional connection with the natural world (measurable with psyche” and that its represented “the loss of opportunities - the psychological construct of nature-relatedness [25])— the extinction of experience”; in particular, Pyle was con- and subsequently develop pro-environmental attitudes cerned about vanishing opportunities for children, “the and behaviors—is dependent upon experience [26]. Na- ones whose sensibilities must be touched by the magic re- ture relatedness (see also nature connectivity, nature con- action with wildlife if biologists, conservationists and con- nectedness) allows researchers to determine individual cerned citizens are not to become endangered themselves. levels of awareness of, and fascination with, the natural What is the extinction the condor to a child who has never world; nature relatedness also captures the degree to seen a wren?” [10]. The concept of extinction of experience which subjects in research studies have an interest in mak- has been expanded upon, but the primary theme remains ing contact with nature. From the planetary health per- the same—loss of direct, personal, cognitive-emotional con- spective, nature relatedness is positively associated with tact with wildlife and elements of the natural world could empathy, pro-environmental attitudes, and humanitarian- lead to disaffection, apathy, and irresponsibility in behaviors ism (and negatively with materialism) [27–29]. However, toward the environment [11, 12]. nature relatedness is also highly relevant to physiological At the same time, a related hypothesis was expanding; anthropology, and human biology in general, because a the hygiene hypothesis and its variants proposed that substantial body of research has linked appreciation of diminishing early life exposures to microbes—due to a (and relatedness to) the natural environment with general more “sanitized” environment, antibiotic use, smaller fam- health and mental wellbeing [30, 31]. ily sizes, and lower exposure to bacteria in foods and the Sitting in parallel to research on the psychology of na- overall environment—could compromise normal training ture relatedness—unintegrated into the planetary health of the immune system. The recent biodiversity hypothesis paradigm—is a growing body of in vivo research involving updates and unifies this proposal by emphasizing that bio- physiological endpoints which demonstrate that time diversity losses at the neighborhood scale could translate spent in natural environments might be protective against into loss of contact with microbiotic diversity. Specifically, allostatic load (described in more detail shortly). While “biodiversity loss leads to reduced interaction between en- there are now many studies in this realm, it is perhaps best vironmental and human microbiotas. This in turn may exemplified by shinrin-yoku (now generally referred to in lead to immune dysfunction and impaired tolerance Japanese studies as simply “forest medicine” or “forest mechanisms in humans” [13, 14]. However, research in therapy”)research; shinrin-yoku loosely translates from the more biologically oriented biodiversity hypothesis and Japanese as forest-air bathing or “absorbing the forest air” the more psychologically oriented extinction of experience and places emphasis on the entire forest experience hypothesis has largely remained separated in silos. wherein the individual tales in all the “components emit- In the twenty-first century, there have been several stud- ted from the forest” [32]. Studies under the rubric of shin- ies which support the idea that adults and children in rin-yoku have shown that spending time in a forest westernized, industrial, and technologically mature na- environment can beneficially influence stress physiology, tions are spending more time indoors [15, 16] and less markers of inflammation, immune defenses, blood pres- time in natural environments [17, 18]. There are also hints sure, and heart rate variability [33–40]. Logan et al. Journal of Physiological Anthropology (2018) 37:15 Page 4 of 10 To appreciate the contribution of shinrin-yoku and re- It is our contention that an “exposome perspective” will lated research, consider that a 2018 systematic review help break down silos and incorporate the ongoing work identified a total of 43 studies which measured physio- of physiological anthropology into planetary health. The logical and psychological stress responses to outdoor en- exposome refers to the science of accumulated “expo- vironments—nearly half of the studies were conducted sures” (meaning both emotional experiences and physical/ in Japan [41]. Although limited by small sample sizes, sensory exposures) over time. As we explain below, this these and other studies with physiological endpoints view emphasizes that genes alone cannot explain health provide potential mechanistic pathways (e.g., immune disparities and underscores that each individual exposure activation, oxidative stress, blood pressure, cortisol re- (e.g., airborne particulate matter or fast-food, beneficial sponse) for the associative links between green space microbes, or phytoncides) does not occur independent of and health in large epidemiological studies [42]. More- the total environment. Moreover, from the physiological over, these studies can be viewed in the context of stud- perspective, the most direct path to understanding the ies which link markers of biodiversity with mental and connections between personal and planetary health—gains physical health [43, 44]. On the other hand, relatively and losses from extinction of certain experiences and the rapid environmental degradation and/or visible losses in birth and flourishing of others—may be to examine allo- species (e.g., the loss of millions of ash trees due to the static load (the physiology associated with the “wear and invasive emerald ash borer) are linked to declines in tear” of stress). We will elaborate on this shortly. physical and mental health [45–47]. Extinction of experience research also forces questions Exposome concerning shifting cultural norms and time use; in other words, if time spent in outdoors in nature is being “Human biology should be primarily concerned with displaced, then how specifically is that time displaced? the responses that the body and the mind make to the These are connected conversations. For example, excess surroundings and ways of life…little effort has been screen time and problematic smartphone use is linked made to develop methods for investigating with lower levels of personal nature relatedness [48]. It scientifically the interrelatedness of things. is also important to point out that “extinction of experi- Epidemiological evidence leaves no doubt that many ence” is not exclusive to psychological losses in contact chronic and degenerative disorders which constitute with biodiversity (or even biodiversity per se); it could be the most difficult and costly medical problems of our argued that for children in westernized nations, the loss societies have their origin in the surroundings and in of whole plant foods (relatively unprocessed, high in the ways of life rather than in the genetic constitution fiber) in the dietary and the massive encroachment of of the patient. But little is known of these the “invasive species” known as ultra-processed foods environmental determinants of disease” [54]. (which now dominate the nutritional landscape, like weeds, displacing nutrient-dense foods) is also an extinc- Rene J. Dubos, PhD, 1969 tion of experience [49]. Moreover, from the biological perspective, urbanization and loss of contact with bio- While he did not coin the term “exposome,” micro- diversity [50]—as well as related changes to contact with biologist and environmentalist Rene Dubos (1901–1982) diversity of the microbiome [51, 52]—could be viewed as urged scientists to study the response of the “total or- an “immunological extinction of experience.” ganism to the total environment” [55]; Dubos, of course, Since the health benefits derived from experiences in not only celebrated the value of single-variable studies natural environments may be determined by baseline na- but also warned of their limitations in the context of ture relatedness [53], researchers will need to examine chronic diseases, environmental degradations, and the the physiological consequences of the interplay between complexities of the human condition [56, 57]. Today, the presence (use) of certain technologies and the ab- the total accumulated environmental exposures (both sence (disuse) of natural environments and biodiversity. detrimental and beneficial) that can help predict the bio- Thus, the challenge for physiological anthropology in logical responses of the “total organism to the total en- the context of planetary health is to help bridge the vironment” over time are referred to as the exposome knowledge gaps between three large, research-based [58]. The temporal aspect of exposome science is im- silos—that is, (1) the psychological and cognitive aspects portant because the physiological responses of the hu- of nature relatedness and the loss of experience, (2) the man organism are a product of accumulated experiences physiological pathways involved in the risk of NCDs, and may differ across time depending on shifting envir- and (3) the ways in which human health and wellbeing onmental variables. The interpretation of stress physi- are, emotionally and biologically, predicated upon bio- ology in the here-and-now requires an understanding of diversity and the health of the Earth’s natural systems. the interplay between time scales of stress, including but Logan et al. Journal of Physiological Anthropology (2018) 37:15 Page 5 of 10 not limited to early life stress, acute and chronic Allostatic load stressors, experience of daily hassles, and the aggregate Human responsiveness to environmental threats has of life events [59]. been shaped by experience over millennia. In particular, The term exposome is now an essential feature of the an elegant and active process of allostasis—the normal planetary health discourse because it helps to demonstrate initiation, orchestration, and termination of neuroendo- why genome-wide association studies cannot explain the crine, metabolic, autonomic, and immune “mediators”— reasons for health disparities; it also helps us understand helps ensure a physiological state which supports sur- why NCDs are increasing over time and in non-random vival. Acutely, these multisystem physiological responses ways. In particular, the burden of NCDs, especially in to stress are, under normal circumstances, effectively ini- westernized nations, is most often shouldered by disad- tiated, maintained, and extinguished without harm. vantaged populations [58]. Furthermore, the exposome However, with repetitive and/or prolonged stimulation view of total health encompasses the World Health Orga- in the modern environment, these compensatory physio- nization’s interpretation of the word health; that is, not logical responses can lead to metabolic disturbances and simply the absence of specific disease criteria, but rather cellular damage. The collective toll of this physiological the fulfillment of human potential. Although genetics wear and tear—including the associated consequences of matter, health includes a state of complete physical, men- unhealthy lifestyle choices which compound the physio- tal, and social wellbeing—it is not a genetic trait. logical dysregulation—is known as allostatic load [64]. Rather, the study of physiology related to health promo- Over time, the combined disturbances of allostatic load tion and/or risk is better understood when it is placed into leads to allostatic overload and contribute to altered be- the context of the total exposures experienced by havior and disease risk [65]. humans—some positive, some negative—and their interac- Epidemiological research indicates that links between tions with genes over time [60]. From a life-course perspec- lower socioeconomic position and disease mortality are tive, exposome science emphasizes that certain windows of mediated by allostatic load [66]. In other words, socio- vulnerability (for disease risk) and opportunity (for health economic advantage is associated with lower allostatic promotion) are especially important [61]. In the context of load, which is in turn link to lowered risk of mortality. physiological anthropology, thismeansthat socioeconomic Such findings are supported by volumes of research indi- advantage or disadvantage can produce differing biological cating that disadvantage is accompanied by chronic psy- responses to specific “beneficial” or “detrimental” expo- chosocial stress and daily hassles, lower optimism (an sures—e.g., spending time in nature or consuming a asset in physical and mental health), and significantly fast-food meal—depending on many other background higher biomarkers of metabolic dysregulation, inflamma- variables. tion, and oxidative stress [67–74]. Indeed, within The interplay of these potentially beneficial and detri- westernized-industrialized nations, allostatic load ap- mental experiences is central to the concept of resili- pears to bear witness to the ways in which socioeco- ency; as researchers explore how and why positive nomic disadvantage “gets under the skin” and “into the adaptation and outcomes occur in the face of adversities, gut,” ultimately decreasing longevity [66, 75]. and why certain individuals (who score high on validated These links with socioeconomic disadvantage have resiliency scores) seem protected against the negative been found at the individual and neighborhood levels; health-related consequences of adverse events, it will be for example, allostatic load persists in low-income necessary to tease apart the ways in which resiliency is neighborhoods even after adjusting for individual-level built in the first place [62]. The available evidence allows income. Beyond income, anxious arousal is linked to for the hypothesis that exposure to elements of natural allostatic load, as well as other lifestyle factors such environments—e.g., microbial—can play a role in resili- as fast-food consumption, exercise habits, and smok- ency. Indeed, early-life exposure to diverse microbes ing [76]; moreover, neighborhood-level income is as- found in natural environments is part of the normal sociated with better physical and mental health over “training” of the immune system, and it may decrease time [77]. Since allostatic load transcends purely gen- vulnerability to later life stress-associated disorders; for etic influences [78], it reinforces the exposome per- example, researchers have found that urban upbringing spective and underscores the need to consider the without pets (vs. rural upbringing around animals) is as- context in which exposures are experienced. More- sociated with compromised resolution of systemic im- over, it also allows for the introduction of epigenetic mune activation (low-grade inflammation) following an research and opportunities to determine how expo- experimenter-induced social stress [63]. To further ap- sures (age, diet, physical activity, time in nature, posi- preciate the saliency of how accumulated experiences in- tive and/or negative emotions, and accumulated fluence physiology in the total environment, we can look experiences) modify DNA methylation, which in turn, to research on allostatic load. alters gene expression [79]. Logan et al. Journal of Physiological Anthropology (2018) 37:15 Page 6 of 10 Putting it all together, future directions non-harmful microbes that may influence health and be- The biological underpinnings of the exposome perspec- havior [97–100]. However, these studies are missing key tive indicate that the extent to which an organism can bits of information; how do measurements on the psycho- buffer against the detrimental physiological conse- logical construct of nature relatedness—and responses re- quences of particular exposures will determine the risk lated to extinction of experience at the neighborhood of NCDs [58]. Hence, it is essential to understand how level—match up with the objective markers of allostatic certain psychological “assets”—such as nature related- load, epigenetics and the microbiome? Does the ness, positive emotions, mindfulness, and optimism—are age-related decline in direct experiences with neighbor- accumulated and employed to act as physiological hood biodiversity manifest physiologically (allostatic load), buffers in the modern environment. The available re- and if so, are there connections between allostatic load search, outlined above, suggests that scientists need to and nature relatedness? look more closely at the total lived experience of individ- These are essential questions for the planetary health uals, and the total environment which surrounds them. paradigm. So far, the research focus on the human From the planetary health perspective, this means look- emotional connections to nature/local lands in the con- ing at the presence (or absence) of natural environments text of planetary health (exemplified by content within and specific features of the built environment that might the aforementioned and highly cited Lancet Commis- offset (or contribute to) allostatic load. sion on Planetary Health report) has been on the real Looking at research from the exposome perspective al- and potential mental health consequences of environ- lows researchers to consider the “big picture” and intercon- mental degradation. Although there is good research on nectivity of humankind’s most pressing problems. For the psychological aspects of pro-environmental and example, living closer to green space and having greater ac- pro-social beliefs and behaviors, its place in the dis- cess to safe, local parks, and open space is associated with course of planetary health is minimal. Moreover, the health in general and mental health in particular [80]. How- wealth of information gathered in the field of physio- ever, the presence of green space may be a surrogate marker logical anthropology (and related disciplines) on differ- for healthier dietary habits, lower density of fast-food out- ential physiological responses to natural and built lets, and better access to healthy foods [81–83]. environments (e.g., shinrin-yoku,forest bathing re- Consider also the psychological asset of optimism search) has not penetrated the planetary health dis- which we have alluded to several times; optimism is gen- course. In addition to nature relatedness, the inclusion erally defined as positive outcome expectancy for future of other psychological constructs in the literature, espe- events across life domains. Optimism has been linked to cially those investigating place attachment measure- lower body mass index and lower rates of chronic dis- ments (e.g., topophilia scales) [101, 102], will help ease and all-cause mortality [84–88]. In the physiological provide a better understanding of how physiological realm, optimism is linked to optimal metabolic markers endpoints might match individual and community-level of cardiovascular health, lower inflammatory cytokine emotional connections to the land. and C-reactive protein levels, and lower inflammatory We suspect that the absence of cohort studies which sim- response to experimental stress [89–91]. Research sug- ultaneously measure deep aspects of socioeconomic histor- gests that optimism is only about 25% heritable, leaving ies, allostatic load (and other objective markers such as the plenty of room for the influence of the total lived experi- microbiome), residential proximity to “assets” (green space) ence over time; indeed, higher levels of optimism are as- and “liabilities” (clustering of fast-food outlets), along with sociated with socioeconomic advantage [92, 93]. Since measures of positive psychology/nature-relatedness/envir- optimism is malleable [94], experts in physiological an- onmental attitudes is a barrier to multidisciplinary break- thropology might query on biological links between opti- throughs in planetary health. Available research indicates mism, nature relatedness, and extinction of experience. that the loss of experience (especially immunological) can For example, higher levels of optimism are associated shape acute biological responses in context over time; as we with protection against the detrimental effects of envir- have pointed out previously, these are intertwined with in- onmental toxins (this appears to operate through epi- come, education, race, immigrant status/segregation, social genetic mechanisms) [95]. cohesion, evaluations of neighborhood esthetic quality, and/ Scientists are beginning to tie these strands together; for or aspects of neighborhood safety (both real and perceived) example, researchers have found that close residential [103]. While constituents of a diet which simultaneously proximity to vegetated land cover is associated with lower promotes human and planetary health is generally agreed allostatic load and depression [96]. In addition, researchers upon [104–106], less is known concerning the ways in have begun to establish links between residential (or which nature relatedness, optimism, and pro-environmental school) proximity and green vegetation—and degrees of attitudes/behaviors and allostatic load intersect with adher- neighborhood urbanization—with exposure to diverse, ence to such a diet. Logan et al. Journal of Physiological Anthropology (2018) 37:15 Page 7 of 10 Macro-scale, multi-factorial, multi-indicator consider- Conclusion ations such as the exposome, allostatic load, and planetary Scientifically, the grand challenges of our time—environ- health present enormous challenges; it is easy to criticize mental degradation, a global non-communicable disease such efforts because they include an essentially unlimited (NCD) epidemic, gross biodiversity losses, climate array of variables. While single-variable studies remain es- change, health and other socioeconomic inequalities— sential to scientific knowledge, large cohort studies are are adisciplinary. In other words, these challenges are enjoying remarkable advances in “omics” research; clinic- overlapping, and their causative complexities suggests ally meaningful data sets are emerging from the analysis that they will not be solved by linear research which of functional proteins (proteomics), metabolites (metabo- otherwise remains in silos. The extinction of experience lomics), gene expression (epigenomics, transcriptomics), perspective suggests that each generation may accept the and genetic influences on specific drugs or nutrients inherited state of their environment with a greater sense (pharmacogenomics) [107]. For example, large datasets in of “normalcy”; while experts in biodiversity conservation the area of the microbiome have provided clinically rele- have a keen interest in extinction of experience research, vant information which may predict an individual’s a greater understanding of its physiological underpin- physiological responses to foods [108]. Thus, the ability of nings seem necessary. researchers to match environmental attitudes, nature re- In our narrative review and commentary, we have latedness, and other psychological indicators (based on ex- pointed to research on extinction of experience, nature re- perience or lack thereof) with important aspects of latedness, and the science of allostatic load to argue for a physiology at the individual and community-level is on stronger presence of physiological anthropology in the the horizon [58]. planetary health paradigm. Over time, the burdensome bio- As researchers begin to incorporate research on expo- logical consequences of detrimental exposures (and absence sures and experiences into the planetary health perspec- of beneficial exposures and psychological assets) will press tive—including studies on physiological endpoints, upon those with higher allostatic load, translating into a resiliency, and allostatic load—we will also learn more biologically corrosive allostatic overload. While physio- concerning realistic expectations concerning the role of logical anthropology has made tremendous contributions natural environments and health outcomes; access to to the understanding of mechanisms that help explain the green space is important, but there are many factors that ways in which experience in natural environments (or ex- push health inequalities and social injustices, including posure to individual constituent parts of nature) promote those that may have far more corrosive effects on health. health, many gaps remain. In particular, a more persuasive We may have unwittingly given the impression that the argument for the connections between personal, public, health implications of experiences, exposures, and allo- and planetary health could be made via more detailed static load are linear—that is, where more of a certain understanding of the biological pathways between nature sort of experience/exposure is better or the more of an- relatedness, changing levels of local biodiversity, and allo- other sort of experience or load is worse. These are not static load. aggregate responses with a universal dose-response rela- The prospect of personalized medicine test results tionship; indeed, researchers are already discovering that (based on physiological responses and large datasets) the potential benefits of nature are not found along a may provide much-needed incentives to motivate indi- neat continuum of benefit [109, 110]. viduals to change lifestyle behaviors that are in the inter- Finally, this entire conversation can be viewed through est of personal and planetary health. The challenge is to an evolutionary lens. What we need to eat—as opposed illuminate the direct links between elements of natural to the ultra-processed foods that surround us—is what environments with measurable parameters of human we are adapted to eat. The exercise we need is obviously health; having “lab results” in hand may help individuals, part-and-parcel of the physical activity to which we are communities, clinicians, and policy-makers to under- adapted; corals and mussels need not count steps! So, stand the direct lines between personal, public, and too, our requirements for the natural settings to which planetary health. In the meantime, the available evidence we are adapted can be viewed, scientifically, from the which supports the biodiversity hypothesis is not calling evolutionary perspective and can help guide future re- for a “back to nature” movement, but rather stepping search questions. It allows us to ask “why do we humans “forward with nature” in the urbanized environment. need nature to be whole?” in modernity. The answer is With the momentum initiated by the 2015 Lancet Com- blowing in the wind, complete with microbes, natural mission on Planetary Health report (now cited over 300 light, and phytoncides, because we are adapted to it as a times on Google Scholar), the counsel of Jonas Salk to part of us, and us as a part of it—for all the same rea- bring planetary health into alignment with the biological sons we need to breathe the atmosphere native to the and socio-cultural objectives of anthropology seems wise. planet that generated us. At the same time, the multidisciplinary effort of planetary Logan et al. Journal of Physiological Anthropology (2018) 37:15 Page 8 of 10 health (adisciplinary in nature, planetary health cannot be 7. Yamazato K. Seeking a fulcrum: Gary Snyder and Japan (1956-1975). Davis: University of California Press; 1987. viewed as a single discipline) should draw upon the ex- 8. Snyder G. Turtle Island. 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The World Allergy Organization journal. 2013;6(1):3. Abbreviation 14. Ruokolainen L, Lehtimäki J, Karkman A, Haahtela T, von Hertzen L, Fyhrquist NCDs : Non-communicable diseases N. Holistic view on health: two protective layers of biodiversity. Ann Zool Fenn. 2017;54:39–49. Authors’ contributions 15. Matz CJ, Stieb DM, Davis K, Egyed M, Rose A, Chou B, Brion O. Effects of SLP developed the commentary, project oversight, research analysis, and age, season, gender and urban-rural status on time-activity: approved the final manuscript. TH assisted with research interpretation CanadianHuman Activity Pattern Survey 2 (CHAPS 2). Int J Environ Res and input of early origins, life-course perspectives. ACL provided the Public Health. 2014;11(2):2108–24. research analysis and developed the manuscript draft. DLK is responsible 16. Clements R. An investigation of the status of outdoor play. Contemp Issues for the commentary oversight, research interpretation, critical review of Early Child. 2004;5:68–80. manuscript, and input of public health perspectives. All authors read and 17. Soga M, Gaston KJ. Extinction of experience: the loss of human-nature approved the final manuscript. interactions. Front Ecol Environ. 2016;14(2):94–101. 18. Pergams ORW, Zaradic PA. Evidence for a fundamental and pervasive shift Ethics approval and consent to participate away from nature-based recreation. P Natl Acad Sci USA. 2008;105(7):2295–300. Not applicable 19. Jones BA. Work more and play less? Time use impacts of changing ecosystem services: the case of the invasive emerald ash borer. Ecol Econ. 2016;124:49–58. Competing interests 20. Beyer KMM, Szabo A, Hoormann K, Stolley M. Time spent outdoors, activity SLP reports the following: Scientific Advisory Board and speakers fees levels, and chronic disease among American adults. 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Journal of Physiological AnthropologySpringer Journals

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