Advances in Biocultural Approaches to Understanding Stress in Humans

Abstract

This paper outlines advances in biocultural approaches to anthropology by discussing anthropological approaches to understanding stress, how anthropologists have typically measured stress, and why it matters for anthropology and beyond. We discuss the application of common quantification techniques such as the Perceived Stress Scale (PSS) and biomarkers of psychosocial stress from abnormal hypothalamic–pituitary–adrenal (HPA) axis activity. We highlight case studies that demonstrate the utility of a biocultural approach to stress across a range of topics—(i) childhood effects, (ii) non-human animals, (iii) depression and anxiety, (iv) migration, and (v) religion—as well as the complexities in the relationship between perceived and biological stress. We conclude by highlighting several areas where we have seen significant advances and point to approaches in other disciplines that anthropology might incorporate to its benefit.

1. Introduction

In the 21st century, questions about human health and well-being are a driving focus for researchers across the natural and social sciences as well as the humanities. This shared interest has the potential for accelerated advances through interdisciplinary and transdisciplinary research. However, the enormity of the body of literature making up studies of human health and well-being can make it challenging to identify the priorities and strengths of individual disciplines, particularly for students and scholars reading across disciplinary boundaries. As such, this article seeks to provide a review of some of the key trends and future directions in the field of biocultural anthropology, particularly pertaining to the study of human stress. While a complete review of anthropological stress studies would be extensive and technical out of necessity, we aim instead to provide an overview of key concepts and case studies that may be of interest to those seeking to enter into this field.

Within the broader study of global human well-being, “stress” is a concept that has garnered much attention due to its serious long-term biological and psychological consequences. Since its conceptualization almost one hundred years ago [1], the various biological and psychological influences on stress have been explored extensively. While great advances have been made in elucidating the biological pathways that stress works through, it is only much more recently that social and cultural aspects of the stress response have been systematically evaluated. Psychologists and other social scientists have contributed greatly to articulating the importance of the social experience of stress, including arguing that stressful life events and illness episodes may be “mediated by a different biological process” (p. 131) than perceived stress or negative affect and stress [2]. Such claims draw attention to the importance of expanding the study of stress beyond the biological and into the social and psychological. Even when accounting for social factors, however, the field of stress research has consistently prioritized Western understandings of stress and well-being. Anthropological perspectives, particularly those found within biocultural anthropology, provide theoretical frameworks and methodological approaches that serve to push the study of stress beyond a Western perspective and consider biological and cultural stress processes simultaneously.

Biocultural anthropologists recognize that the stress one experiences is deeply cultural and biological in nature. Broadly, biocultural work aims to understand biological and evolutionary processes as well as the construction and workings of culture often in regards to health [2,3]. This extensive perspective persists because a “biocultural” framework is claimed by both biological and cultural anthropologists. However, it is this shared heritage from multiple subdisciplines of anthropology that make a biocultural approach to stress valuable far beyond anthropology. Its theoretical breadth provides biocultural anthropology with a unique flexibility in its approach to stress. As the two, sometimes disconnected, subdisciplines have reconned with similar questions over the last few decades, the merging of theoretical concepts has allowed biocultural anthropologists to argue that human “marginality and vulnerability, often framed as a result of stressful physical and biotic environments, were neither natural nor inevitable. Rather, the grinding poverty of structural violence, social and political inequalities, and the subjugation of groups in colonial and postcolonial political economies, created vulnerabilities” ([4], p. 3). Attention to environments and adaptation has long been the purview of biological anthropologists and has only more recently entered into cultural anthropological conversation. Conversely, the latter concepts expressed by Leatherman and Goodman [4], namely structural violence and postcolonial political economies, are at the forefront in corners of cultural anthropology. A similar sort of synergism continues to develop in the methodological orientation of biocultural anthropology [5,6] as genomics and biomarkers are triangulated with participant observation and interviews within and across studies. As these theories and methods come together, anthropologists can contribute new views on the human experience across time and space.

2. What Is Stress? [7,8,9]

Stress, a concept first used in physiological and biological research by Selye [1,10], is employed today to describe a wide range of conditions an individual may experience either physiologically or mentally. Although some argue that a lack of standardization and overapplication exist in how the term stress is applied [11,12,13], it is generally defined as a threat to and/or disruption of an organism’s capacity to sustain homeostasis (equilibrium in physiological functions) as a response to external and/or internal antagonistic stimuli (i.e., stressors [14,15,16]). Consequently, an organism’s ‘stress response’ is the physiological attempt to counteract this disruption and engage the processes of allostasis (re-establishment of homeostasis) via activation of the sympathetic adrenomedullary (SAM) system and the HPA axis (further described below [17,18]). Stressors derive from many different sources and can be psychosocial (e.g., discrimination, socioeconomic status), physical (e.g., oxidative, trauma, disease, nutrition) or environmental (e.g., heat or cold stress, disruptive environment) in nature.

2.1. Psychosocial Stress

Psychosocial stress refers to the various personal and socioenvironmental conditions that elicit a stress response due to having a psychological impact [19] and can include various factors such as emotional abuse, exposure to war and terrorism, racism, discrimination, social group and socioeconomic status, and family dynamics [14,20]. This type of stress represents a “ubiquitous phenomenon” in today’s society [18] and can impact anyone regardless of age, sex, economic status, and environmental conditions. Psychosocial stress also has another layer of impact than other forms of stressors since it can affect not only the main subject but also other individuals through observations or second-hand accounts due to experiencing cognitive and/or emotional empathy ([18], p. 2) An overview of the current state of psychosocial stress research indicates a significant focus on comparing either sex- [19] or age-specific [20] responses to both physical and psychological stressors. Psychosocial stress is often the stressor type used in stress studies under experimental conditions to trigger a stress response in order to assess an individual’s cortisol reaction [21,22]. Regarding the latter, for example, a recent study by Schnitzphan et al. [23] shows that although the stress experienced by young adults when the Trier Social Stress Test is administered directly impairs their potential memory capabilities, this impairment is not observed in their older counterparts under the same stress conditions.

2.2. Physical Stress

Physical stress can take the form of a more internal, biological phenomenon, such as oxidative stress or stress due to disease or nutritional deficiency or as external physical stress due to an individual undergoing physical abuse or trauma. Physical stress in the form of abuse, especially if suffered during childhood, can have long-lasting impacts and result in a disordered cortisol response in adulthood when faced with other types of stressors [24,25]. Much of the research conducted surrounding physical stress centers on trauma and abuse, with focus often placed on how these stressors affect child development, although attention has also been paid to the oxidative stress resulting from chronic health conditions such as hypertension [26]. Oxidative stress also involves factors that affect physiological oxidation, induced by physical exercise or infections [27].

2.3. Environmental Stress

Environmental stress involves a wide variety of external stressors or conditions (e.g., loud noises, unfamiliar surroundings, heat stress, cold stress, and altitude stress) that can have impacts at the local or global level [28,29]. Environmental stress on a local level can affect an individual and their cognitive and/or physical function depending on the stress intensity level of the environment and duration of exposure [29,30]. This type of stress can have a serious and immediate effect, with studies indicating that cognitive function can be severely impaired within a high-stress environment. Global-level environmental stress can have a more extensive, albeit gradual, impact than other types of stressors since it can affect entire ecosystems. For example, global-warming-induced heat stress at this scale can negatively affect both human and animal reproductive efficiency by raising body temperatures beyond their respective physiological homeothermic point [28]. This rise in body temperature can negatively affect fertilization and all stages of fetal development, with potential long-term effects including a decline in population density, a reduction in world-wide food supply due to livestock decreases, and even new evolutionary developments to adapt to this unprecedented form of stress.

2.4. Appraisal and Coping

Stressors are not static categories, and they often occur concurrently with potentially compounding effects (e.g., experiencing both physical and emotional abuse during the same period [20]). Additionally, a stressor for one individual may not, if at all, trigger the same stress response in another individual even with the same environmental conditions [13], a concept known as ‘appraisal’ [31]. Better defined as “the perception of the balance between demands and resources” ([28], p. 16), appraisal is divided into two processes: primary and secondary [32]. Primary appraisal process assesses whether the stressor or stimulus being experienced is an actual threat. If it is deemed a threat, the secondary process determines whether the individual experiencing it can handle it accordingly, thus initiating idiosyncratic coping behaviors and mechanisms [31,32].

Ultimately, stressors elicit different responses from different people, with individuals possessing different ways to cope with stress. Scholars began identifying this existence of differential stress responses in the late 1960s with foundational work by Lazarus and Folkman [32,33] exemplifying this research. This work expanded beyond the arguably more “simplistic” approaches towards coping and appraisal previously put forth by Selye [1,10] and Cannon [34]. Work by Travers et al. [35] highlights this phenomenon in a review of the relationship and impact of physical exercise and environmental stress on an individual. In brief, although whole-body systems can function to maintain homeostasis in a hot environment setting involving mitigated exercise efforts with low physiological impacts, the same environment combined with intense exercises results in severe physiological strain with impaired regulation of homeostasis.

2.5. Acute vs. Chronic Stress

An individual‘s stress response can be categorized as either an acute (immediate and short-term) or chronic (continuous and long-term) physiological reaction, with the former possessing the ability to transform into the latter due to either repetitive or constant stimulation [20]. For example, acute stress disorder (ASD) describes an immediate post-trauma response that can transform into post-traumatic stress disorder (PTSD) or other significant psychiatric disorders if symptoms persist beyond four weeks [36]. Although acute stress can be a physiologically necessary adaptive response, chronic stress can have extensive, adverse effects [21]. Exposure to acute or chronic stress can impact an individual‘s health beyond the primary stress response, with acute stress triggering certain health disorders (e.g., eczema, asthma, migraines, gastrointestinal issues, panic attacks) and chronic stress generating or exacerbating chronic health conditions (e.g., depression, anxiety, osteoporosis, obesity, hypertension [15].

Human research on acute versus chronic stress differs due to the nature of each type of response. Studies on acute stress tend to focus on an individual’s response to trauma and its short-term versus long-term health effects, particularly PTSD [36,37,38]. In contrast, chronic stress studies largely focus on its relationship with psychiatric disorders [39,40,41] as well as work-related chronic stress and its various negative health impacts [42,43,44,45,46].

Evidently, the various types of stressors and stress responses enveloped by the stress concept are complex and intricately linked with one another with both indirect and direct health consequences, thus demonstrating the nuanced relationship between health and stress.

3. Measuring How Humans Experience Stress

Biocultural approaches to understanding stress require systematic assessment of both the biological experiences and the sociocultural experiences of stress. A variety of survey instruments have been developed to measure the psychological or perceived experience of stress. Typically, these surveys employ a self-reported checklist or Likert scale to measure exposure to stressors, and they vary in the populations they are designed to study and in the time span upon which they are focused. Among the earliest attempts to gather systematic data on the experience of stressors was Adolph Meyer’s “Life Chart” method [47], which used an extensive semi-structured interview to create a graphical representation of both past and present experiences and to relate those experiences to existing difficulties. While admirable in its comprehensiveness, administering a Meyer-style “Life Chart” proved both time-consuming and labor-intensive. We discuss here the instruments that are currently widely used within anthropology, regardless of their disciplinary origins. Below, in Section 8, we draw the reader’s attention to instruments from other subdisciplines likely to be adopted by anthropologists. Among the most widely used of the attempts to create a more efficient measure of stressors is the Perceived Stress Scale (PSS) developed by Cohen et al. [48]. The PSS consists of 14 items, scored on a 0–4 Likert scale, and it asks only about experiences within the previous month. While it can therefore be administered efficiently, and in many modalities, it is not appropriate to all research agendas. The original PSS is often referred to as PSS-14 to indicate that it has 14 questions. Two other common versions of the PPS are PSS-10 and PSS-4 [49], which are even more efficiently administered, and the PSS has been translated into several languages [50,51,52,53,54].

It is widely recognized that childhood trauma and abuse can compromise adult mental and physical health. Consequently, there is significant interest in retrospective assessments of childhood experiences of stressors. The Childhood Trauma Questionnaire [55] is administered to adults and begins each of the 70 questions with “When I was growing up… ” and, like the PSS, requests a rating on a 5-point Likert self-reported scale. Likewise, the Adverse Childhood Experiences (ACEs) Study Questionnaire is a retrospective assessment of childhood-perceived stressors, asking specifically about 17 exposures during the first 18 years of life [56]. Rather than using the popular Likert scale, the ACE Questionnaire collects binary responses—either a participant self-reports that they were exposed to a specific adverse childhood experience, or they were not, and a “dose” is calculated by summing the affirmative responses. Survey instruments have also been developed to assess specific aspects of stress. The Asian American Racism-Related Stress Inventory (AARRSI) is a 29-item survey that uses a 5-point Likert scale and assesses participants’ self-reported experiences with socio-historical racism, general racism, and perpetual foreigner racism [57]. Likewise, the Index of Race-Related Stress [58,59] is a survey instrument designed to assess perceived daily hassles [32] and everyday racism [60,61].

While anthropologists have incorporated generalized scales, such as those mentioned above, to answer questions about health and well-being globally, one way in which they are assisting in revolutionizing the study of stress is through the adaptation and creation of scales appropriate for local contexts around the world. This is necessary for the advancement of stress research because many commonly used generalized scales were developed and tested for reliability in a Western context [62]. Western-generalized scales often fail to consider how stress is understood cross-culturally, from its sources to appropriate ways to cope with it. Anthropologists have proposed at least three approaches to local scale adaptation and creation. A first approach, which is utilized outside of anthropology as well, is a linguistic and cultural translation of an existing scale. This allows Western or general scales of stress and depression to be translated not just into new languages but to adjust scale prompts in a way that utilizes local terminology to describe stress. This approach allows existing, well-established scales to be applied across diverse linguistic contexts. However, anthropologists and other scholars researching cross-cultural perspectives on stress warn that “sheer focus on translation and terminology may limit the ability of the scale to understand and measure deeply rooted causes of stress that are culturally defined among distinct groups” ([61], p. 3). Anthropologists see great value in comparing perspectives and experiences with stress across groups, but they see local cultural conditions as an essential starting point for these comparisons.

To accomplish the goal of cross-cultural sensitivity in stress and well-being research, anthropologists have employed two alternate strategies for scale use. One increasingly popular approach is creating local scales. This is useful even within a Western context, where other more generalized scales could be chosen. Snipes et al. [63] demonstrate the necessity and utility of this approach in their research with Mexican farm workers in Washington, United States. Multiple perceived stress scales exist for measuring the experience of Latinos/Hispanics in the United States. Yet, these scales, according to Snipes and colleagues, fail to address some of the unique sources of psychological stress experienced by Mexican farm workers. They identified these unique stressors through qualitative methods standard to anthropology, such as focus groups and participant observation. After developing their scale for measuring Mexican farm worker-perceived stress, they compared the internal reliability of their scale with that of other standardized scales (which they administered to the same sample) and found their locally specific scale to have similar levels of reliability. In a similar approach, other anthropologists likewise developed scales based on local “idioms of distress” [64]. Idioms of distress, or culture-bound syndromes [65], are named conditions specific to a group or groups of people. Weaver and Kaiser [66] describe their approach to creating local mental health scales in India and Haiti. Key to their approach is a mixed methodology that relies on both traditional cultural anthropological methods such as ethnography coupled with statistical verification of the consistency and validity of their local scales. In the presentation of their data, they make a strong argument for the value of presenting their ethnographic findings alongside their survey scale findings. Cultural syndromes noted in the literature are often distress responses specific to a local context. Brooks [67] demonstrates this in his adaption of Rubel et al.’s [68] social stress gauge to the Peruvian Andes while also looking at the cultural syndrome of chucaque, a cultural syndrome not found widely in other areas. By not measuring “stress” based on Western assumptions, anthropologists have been able to draw much needed attention to broader understanding of human psychosocial and physiological well-being. These scales can more fully capture the varied causes and consequences of distress, both psychological as well as biological, across diverse populations. However, because of their intentionally localized nature, they can be difficult if not impossible to transpose onto another. Indeed, this would be contradictory to their very purpose.

A third approach to local scale creation attempts to bridge the two previously described techniques to allow for both uniquely local perspectives on well-being through the implementation of an approach that can be replicated across numerous local contexts. Snodgrass et al. [69] propose this approach through a case study of well-being and emotion in India. They argue that scale creation based on positive and negative emotions resolves many of the limitations presented by other methods of scale creation due to the universality of emotion, thus providing a way to account for both insider and outsider perspectives on well-being. This approach has great potential for future anthropological research endeavors.

Biocultural anthropologists are active in finding ways to connect broader research on stress with cross-cultural perspectives that exemplify the breadth of human experiences with well-being. Through the careful utilization of existing scales and the creation of new scales when needed, they are bridging the gap between domains of study that have long been held separate and have limited understandings of stress. Increasingly, a key consideration in measuring experiences of stress and cultural distress is incorporating measurements of biological stress responses. The following section provides a brief overview of one of the biological pathways that has garnered great attention from biocultural anthropologists and other scholars of stress: the hypothalamic–pituitary–adrenal axis.

4. The Hypothalamic–Pituitary–Adrenal (HPA) Axis

One of the most accessible biological systems involved in stress responses is the hypothalamic–pituitary–adrenal (HPA) axis. Measures of the HPA axis access illustrate (i) normal circadian functioning; (ii) normal acute stress functioning; and (iii) dysregulation and chronic stress.

4.1. Normal Circadian Functioning

The circadian rhythm system regulates hormone secretion throughout the body and is often discussed in reference to the fluctuations of hormone secretion during the body’s sleep/wake cycle [16,70]. Succinctly, the circadian rhythm is the regulation of a 24 h cycle of production and degradation of proteins [71]. The hypothalamic nucleus involved in regulating the body’s master clock is the suprachiasmatic nucleus (SCN) [16]. With the absence of light input, SCN neurons have an approximately 24 h cycle, which is modified by light input. However, disruptions to the SCN circadian rhythm can affect the cardiovascular system as well as sleep and energy balance, as sleep is an important influence on energy homeostasis [16,72,73].

The HPA axis is considered a representative model for circadian rhythms with modulation through negative feedback loops [74,75]. Cortisol is released in a clear pattern throughout the day based on circadian functioning. In a non-disrupted schedule, peak glucocorticoid levels are seen shortly after waking during early-morning hours and steadily decreases until the lowest point is seen around midnight [70,71]. Cortisol starts to increase with a peak at about 30 to 40 min post-waking and rises far more in this period than during the last hour prior to awakening [76]. This trend in cortisol rise and fall throughout a 24 h period is a relatively consistent display for non-ill individuals [70]. The peak of cortisol upon waking plays an important role in body synchronization [72]. Alterations and dysregulation of the HPA axis can be tied to both chronic and acute stressors, including chronic ill health [77,78,79,80,81]. Normal circadian functioning is imperative for positive biological health; whereas, disrupted functioning is related to negative effects.

4.2. Normal Acute Stress Functioning

Physical and psychological stressors can activate the HPA axis [82]. The HPA axis is an important part of the neuroendocrine system that maintains homeostasis and is essential in responding to stress to restore homeostasis [75]. The HPA axis may maintain homeostasis through a circadian release of glucocorticoids [72,83], while also being triggered by encountering a stressor. The intensity of the HPA axis response depends on the nature of the stressor.

When the brain recognizes acute stress, the HPA axis becomes triggered by the release of corticotropin-releasing hormone (CRH), further triggering secretion of adrenocorticotropic hormone (ACTH) by the anterior pituitary, which finally leads to the adrenal cortex releasing elevated levels of glucocorticoids [82,84]. Cortisol is the primary glucocorticoid in humans. In non-stressful periods, mineralocorticoid receptors and cortisol have a higher binding likelihood [74]. During periods of stress, however, when there is a spike in cortisol, it will bind to glucocorticoid receptors, which in turn suppress the stress response.

Regulation of cortisol is important due to the influences it has on different bodily functions including memory and learning as well as cardiovascular functions. Release of cortisol can take about 90 min to return to normal levels after the stress-induced increase, and the quick rise and fall is considered a healthy stress response [74,85]. While the stress response has nongenomic and genomic effects to assist in stress coping, excessive glucocorticoid exposure can become taxing on an individual with an understanding that it can assist in the development of certain disorders [74,86].

4.3. Dysregulation and Chronic Stress

As outlined above, the activation and then quiescence of the HPA axis is essential to the maintenance of homeostasis. When the stress response is chronically stimulated, the ability of the HPA axis and its associated systems to respond appropriately to stress challenges is compromised. The inappropriate response to stressors is termed dysregulation and can take the form of hyper- or hypo-reactivity. Hyper-reactivity results in circulating cortisol levels remaining high after a stressor is experienced because of reduced activity in the negative feedback regulatory system that would typically return cortisol levels to baseline [87,88]. Hypo-reactivity, also known as a blunted cortisol response, seems to have two etiologies—either there is upregulation in the negative feedback regulatory system resulting in a rapid return to baseline cortisol levels [88] or the pituitary gland is less responsive than typical to the presence of corticotropin-releasing hormone, resulting in less production of ACTH to simulate cortisol release by the adrenal cortex [89,90].

5. Measuring Hypothalamic–Adrenal Axis Activity

Cortisol permeates body tissues. It can therefore be assayed to measure levels of HPA axis activity. Different biological samples allow the assessment of HPA axis activity at different time scales, and there are practical advantages and disadvantages to each. The utilization of saliva, urine, and hair samples are considered reliable biomarkers for assessing HPA axis activity [91]. As cortisol can be found in many biological specimens, it is the most commonly analyzed biomarker of psychosocial stress [14].

5.1. Saliva

Saliva is the least intrusive sampling method of measuring HPA axis activity in the human body [92]. However, utilizing saliva does require participants to adhere to strict sampling instructions that could limit their eating or drinking habits. Saliva is a short-term biomarker for measuring HPA axis activity, providing levels anywhere from several minutes to hours after acute stress [91].

5.2. Urine

Urine as a sampling method is also non-invasive, but storage of urine over 24 h periods by participants can be unappealing and space-consuming. Measuring cortisol via urine however may be a better measure than other sampling options [93]. The 24 h urine samples are short-term biomarkers providing levels throughout an individual day. Multi-day levels can be achieved through daily collection over several days to weeks [91].

5.3. Blood

Using blood for HPA axis activity measurement is convenient in instances of in-/out-patient procedures, but innovations in storage and collection facilitate the collection of dried blood spots in diverse fieldwork settings [94]. Sampling blood for cortisol measurements may induce more stress in participants due to its invasive nature, which could potentially affect cortisol levels [95].

5.4. Fingernails

Utilization of fingernails for measuring HPA axis activity is a newer, lesser-known method, of which we have less knowledge of its reliability and validity [96]. Sampling fingernails is non-invasive and may provide a longer measurement of cortisol secretion than blood, urine, or saliva. Researchers hypothesize that fingernails could represent cortisol secretion from a 10-day period from several months prior using just a 1 mm sample. However, research has shown that certain drugs can show up in fingernails only shortly after ingestion, which suggests that cumulative secretion of cortisol may cover a longer timeframe up until the point of collection [96]. More research needs to be conducted to better understand the temporality of fingernail cortisol measures.

5.5. Hair

The method to extract cortisol from hair was developed around 20 years ago [97]. It is a non-invasive sampling method, as researchers only need about 1 to 10 cm of hair for analysis, and it can be stored at room temperature over long periods of time. Hair is also less likely to be affected by confounders, such as time of day, unlike blood, urine, or saliva [76]. Researchers may run into issues gathering hair samples as participants may have aesthetic concerns about hair sampling or simply not enough hair; although, in our experience, participants are often both willing to donate hair and interested in having their own results returned to them when the study is complete. Unlike other sampling methods, hair provides a long-term measurement of cortisol secretion of up to several months.

6. Case Studies in Stress and Its Consequences

The previous sections have outlined some foundational aspects of biocultural research in anthropology. The body of literature emerging from these key assumptions examines stress in various social contexts and continues to grow quickly. Here, we provide an overview of some of the topics to which biocultural anthropologists have contributed and found valuable for exploring the relationship between various stressors and their biopsychosocial consequences: (i) childhood effects, (ii) non-human animals, (iii) depression and anxiety, (iv) migration, and (v) religion.

6.1. Childhood Effects

As described above, children seem particularly vulnerable to dysregulation of the HPA axis in the face of chronic stress. When exposed to an experimental stressor (the Trier Social Stress Test, TSST), adult women who had suffered physical abuse during childhood and those who were victims of, or witnesses too, at least two episodes of violence showed lower HPA axis reactivity than controls. Likewise, adults with a history of moderate-to-severe childhood trauma and without symptoms of major depressive disorder or post-traumatic stress disorder (as defined in the DSM-IV) showed lower ACTH and cortisol reactivity in response to the TSST [98]. Non-exhaustively, the pattern has also been seen in healthy Dutch university students having suffered childhood trauma [25], Canadian adolescent girls in the care of child protection agencies [99], British 12-year-old children suffering bullying [100], and children in the care of the Children and Family Services in a large west coast city in the USA [101]. The nature of HPA axis dysregulation, however, is not universal. Higher HPA axis reactivity in response to the TSST has been found in Canadian adolescents and young adults with a mood disorder who suffered childhood abuse [102], in American women who suffered childhood physical or sexual abuse, a pattern that was exacerbated by existing symptoms of anxiety or depression [103], and in young children (ages 6 to 9) in the eastern US, who lived with their mothers but for whom Child Protective Service records documented neglect [104]. Intriguingly, Ouellet-Morin et al. [105] found that in a sample of 155 men, those with some experiences of childhood maltreatment showed blunted salivary cortisol responses, but those with high rates of childhood maltreatment showed elevated salivary cortisol responses. These data suggest that HPA axis dysregulation in the face of childhood maltreatment can vary markedly depending on the severity of the experiences endured.

6.2. Non-Human Animals

All mammals respond to stressors via the HPA axis. Consequently, biomarkers of stress can be assayed in non-human animals to assess the biological load of stress, in both the short term (e.g., in saliva) and long term (e.g., in hair), depending on the conditions under study. Analyses of cortisol in the hair of police horses working in Barcelona found that horses subject to relocation had higher levels of cortisol in their body hair than controls [106], even though the relocation was intended as a rest period. Similarly, in a three-way comparison, it was found that competition dogs exhibited higher levels of cortisol in body hair than either companion dogs or dogs that worked in a professional capacity for the police force or army [107]. Interestingly, the police horses exhibited higher hair cortisol levels in warmer months, but the dogs did so in cooler months. Primates too have been the subject of investigation. Except for infants and the eldest individuals in the communities, captive rhesus monkeys living in high-density environments exhibited higher levels of cortisol in hair than those living in low-density environments [108]. In the wild, olive baboons and hamadryas baboons have formed a hybrid population in Ethiopia. The hybrid monkeys exhibited higher levels of cortisol in their hair than either the olive or the hamadryas baboons [109]. The source of the elevated cortisol in the hybrid monkeys is not yet clear, but it is possible that the effect results from the genetics of hybridization rather than higher levels of experienced stress.

6.3. Depression and Anxiety

Prolonged exposure to excessive stress is a well-documented risk factor for the development of psychopathologies, including depression and anxiety. A mechanism through which chronic, severe stress results in psychiatric disorders is the dysregulation of the HPA axis [110]. Several studies have shown that patients with major depressive disorder exhibit higher levels of cortisol than healthy controls in both blood [111] and saliva [112] samples and that an uncommonly large cortisol awakening response (see above) predicts the onset of a major depressive episode, especially in recurrences [113,114,115].

6.4. Migration

Migration is a psychologically and biologically stressful social and physical phenomenon, making it an ideal area of research to which stress biomarkers can be applied. It has served as an important area of bioanthropological research since very early in anthropology’s history, dating back to Maurice Fishberg [116] and Franz Boas’ [117] studies on migrants in New York City. They both found that human biological plasticity was much greater than previously thought—both height [116,118] and cranial shape underwent significant, measurable differences between immigrants and their children born after migration. These studies challenged racialized views of migrants at the time. Today, research on migration continues to employ cutting-edge biological measurements to understand the intertwined social and biological experience of migration, including the complex interplay of stressors present before, during, and after migration. The current biocultural research on migrants reveals two important trends. First, multiple measures of stress are necessary to illuminate the complexity of the migrant experience. Second, this work is best conducted with attention to both biological factors as well as social factors.

Cross-disciplinary research on migration makes it increasingly clear that understanding migration stress requires multi-pronged approaches to avoid obscuring important variables. At the most basic level, this includes generalized self-reported distress scales, such as the PSS, CES-D and major life events scales, which are often common in migration health research [119]. Anthropologists contribute to the creation of group-specific migration perceived stress scales [63,120]. Scales have provided an excellent entrée into understanding the intricacies of migrant stress. To advance understandings of migrant stress, however, they are of most use when partnered with biological measurements such as blood pressure [121,122], Epstein–Barr virus antibodies [123], catecholamines [119], and glucocorticoids-like cortisol [124]. To try to capture a holistic perspective, a popular approach among migration researchers is the use of “allostatic load”, which is a score based on the amalgamation of measurements like systolic and diastolic blood pressure, waist-to-hip ratio, cholesterol, hemoglobin A1C levels, triglycerides, and C-reactive protein [125,126]. Yet, even with such a comprehensive measurement of biological factors, researchers are still finding contradictory results, with some finding a significant difference in allostatic load between migrants and non-migrants [125] and others finding no significant difference [126]. To date, there are very few agreements in the biological stress processes active in migration.

These results speak to the importance of social variables that must be further considered in studies of migration. Some of the variables that have been highlighted in research include self-reported gendered discrimination [123], adherence to locally held religious devotion ideals [120], and the presence or absence of local migrant enclaves [127]. Such social factors are often missing from studies outside of anthropology, which potentially adds to the confusion in migrant stress pathways. For example, in their measurements of hair cortisol concentrations (HCCs) of migrants and refugees, Mewes et al. [128] found that asylum seekers had higher HCCs than settled migrants, while Buchmuller et al. [129] found that asylum seekers had lower HCCs than migrants. The social variables uncovered in these studies, as well as many others yet to be identified, are likely the key to understanding stress processes active in migrant lives.

6.5. Religion

In the biocultural study of religion, progress is being made in understanding how biology functions both during religious ritual and the days following it. In work conducted by Lynn et al. [130] among American Apostolic Pentecostals, both the HPA and the sympathetic nervous system (SNS) were identified as being active. Salivary cortisol levels were lower on non-worship days than worship days, while salivary alpha-amylase levels were higher on non-worship days. Lynn et al. [131] propose multiple theories for this pattern. In a separate paper on this project, they extrapolate on the variable of glossolalia, the ritualistic speaking in tongues, when practitioners enter a dissociative state. They note that high levels of glossolalia correspond with elevations in salivary cortisol and alpha-amylase, but that high glossalists have lower stress (salivary cortisol) and arousal (alpha-amylase) loads on non-service days. This could mean that greater experience with ritualistic disassociation could contribute to reducing biological stress. Aside from social experience, socioeconomic status and better psychological health has been linked to better health outcomes from ritual [131]. Engaging in religious ritual has implications for biological and psychological stress levels, but the impacts are variable based on individual social position and ritual experience.

Aside from rituals, religious contexts also provide an opportunity to study belief/devotion and religious status. One approach to this work utilizes a cultural consensus and consonance framework [132], which measures the presence of shared cultural knowledge and individual adherence to it. Among migrants, consonance to local appropriate methods of devotion to the Virgin de Guadalupe was significantly associated with lower psychological stress levels (as measured using the 13-item Immigration Stressor Scale (ISS)) [120]. Dengah [133] found that religious consonance was a better predictor of psychological health than secular consonance for Brazilian Pentecostals. Working in a very different religious context, this time among college-aged American Latter-day Saints, Dengah et al. [134] found that women attempting to adhere to both local religious and local secular gender norms had elevated perceived stress levels on the Perceived Stress Scale (PSS). Thus, echoing the findings among migrants, synthesizing the results from biological, psychological, and social measures gives a clearer picture of the social and biological pathways that stress interacts with.

7. Complexities in Relationship between Perceived and Biological Stress

As demonstrated in the case studies above, the relationship between perceived and biological stress is complex and remains unclear. Continued research across these topics as well as many others will likely yet contribute to clarifying how perceived and biological stress interact. Applied broadly across social contexts, further studies that combine common psychological, self-reported stress measurements, such as the PSS or locally developed scales, with emerging biomarkers of stress, such as HCCs [48,135,136,137], will provide a viable way to further evaluate the relationship between perceived and biological stress and better understand the nuanced complexities involved.

One branch of study that is taking up this biocultural approach to tease apart the complex relationship between perceived and biological stress focuses on intergenerational trauma and impacts of perpetual sociocultural challenges—especially among minority populations [138]. Henley et al.’s [139] work is indicative of this with a study on the disparity between perceived and biological stress among a First Nations community in Canada, a group that has faced stressors in the form of adverse socioeconomic and environmental conditions, cultural oppression, high rates of chronic diseases, and intergenerational trauma spanning generations. Through comparison of the PSS and hair cortisol levels between First Nations and White participants, results showed that although the First Nations participants possessed higher physiological stress levels than the White participant group, the PSS scores between the two groups were not significantly different. This indicates that although the First Nations participants did not report having higher stress levels on a psychological level than their White counterparts, physiologically the negative impact of the chronic stresses they and their ancestors had endured was evident.

It is also worth noting the concept of resilience when discussing the potential disparities between perceived and biological stress. As Garcia-Leon et al. [87,122] defines it, resilience in this context is “the result of the adaptive response to a stressor that enables individuals to cope with a stressful circumstance”. It is further argued that this form of resilience is likely a determining factor in how perceived stress, the intensity and impact of a stressful situation, and even chronic stress manifest. In the case of the results of the Henley et al. [139] study, resilience in this sense may play a potentially significant role in blunting an individual’s psychological response to various psychosocial stressors despite physiological effects still occurring. This is a seemingly opposite effect from those who experience physical trauma as children, resulting in a diminished cortisol response to stress in adulthood (see [24,98,140]). However, it has been argued that intergenerational trauma may dispose individuals to further stressors as well as increase the level of their response both psychologically and physically [138], further highlighting the complexities in the relationship between perceived and biological stress.

8. Possible Future Directions

Anthropology’s potential to contribute to the complex questions now at the heart of stress research, such as explored in the previous section, will likely be influenced by its readiness to look to developments in other disciplines. Anthropology has long profited from adopting methodological and theoretical advances developed in allied disciplines. While a significant portion of the work described herein has a distinctly anthropological flavor, many of the approaches originated outside of anthropology. We therefore argue that anthropology is well-served when it carefully considers work beyond its disciplinary boundaries. We do not pretend to provide a comprehensive review of all disciplines with an interest in the relationships between stress and health but point to developments we think particularly interesting and likely to be of particular value to anthropologists as they pursue their own research agendas.

Sociologists have often focused on the social contexts and structures that impact the experience of stress. Drawing on insights from epidemiology, medical sociologists, in particular, have paid considerable attention to the ways in which large-scale phenomena, like the bureaucracy of healthcare systems or persistent structures of social class, impact people’s experiences of stress and result in health disparities. For example, Holst et al. [141] used a mixed-methods approach to demonstrate that, despite an established and functional governmentally provided social safety net, existing social class structures in Germany shaped the health and economic risks of the COVID-19 pandemic in different dimensions. They found that on average members of the independent economic classes, including business owners, consultants, and technical workers, such as engineers, experienced the pandemic most significantly as a financial threat, rather than a health threat. In contrast, people in occupations dominated by interpersonal interactions, like factory workers, teachers, childcare workers, and nurses, most frequently experienced the pandemic primarily as a threat to their health. Existing gendered social structures were also found to impact both economic and health risks, with service workers in female-dominated occupations and male workers at the lowest paid technical jobs both at especially high risk of health and economic risks.

Sociologists have generally employed methods familiar to anthropologists, including ethnographic work rooted in participant-observation and large-scale data collection through surveys. A set of methods central to sociological approaches that are seldom embraced by anthropologists involve the analyses of large databases that might have been developed for research purposes, but were not necessarily developed with their particular research questions in mind, such as social media data [142], healthcare usage statistics [143], or data from the National Historical Geographic Information System [144].

In contrast with sociology’s general focus on group-level phenomena, psychologists have paid particular attention to individual variation and the interactions between cognitive processes and measurable physiological responses. Psychological approaches to understanding stress responses have embraced the experimental in ways largely alien to anthropologists. A significant development in psychology, embraced also by many subdisciplines of public health, is the gathering of data using ecological momentary assessment (EMA). In a large scale, but otherwise fairly typical, example of an EMA, Gordon and Mendes [145] enrolled participants who completed an intake survey, calibrated blood pressure readings taken by the optical sensor on their phone using an external blood pressure cuff, and showed them how to download an EMA mobile application to their smartphones. Participants were then prompted three times per day for twenty-one days to complete a blood pressure reading, a survey about their experiences with stressors, the resources at their disposal to manage those stressors, and whether they had recently exercised. The study found that while indeed blood pressure responded significantly to the experience of stressors, the availability of coping resources was particularly important in predicting the degree of blood pressure increase. Interestingly, the concordance between reported stress and changes in blood pressure increased with increasing age of the participants.

While we are generally enthusiastic about the prospects of EMA-based research in anthropology, we are cautious about the demands placed on participants by these kinds of approaches. We note that Gordon and Mendes [145] enrolled more than 91,000 people in their study, but that by the time they had removed participants for non-compliance with data collection procedures, their sample size decreased to under 22,000 participants, despite the incentive that compliance was rewarded with entry into a lottery to win one of twenty new smartphones. By almost any anthropological standard, 22,000 people is an enormous sample size. However, most anthropological teams have neither the funding nor the labor to sustain a research program with a ~75% sample loss. Additionally, anthropologists will need to consider carefully whether there are characteristics of compliant participants that might differ significantly from those of non-compliant participants that could meaningfully skew the results.

Theoretical developments in psychology are also relevant to anthropologists interested in stress. A particularly salient example concerns theory initially developed more than 20 years ago that has undergone significant evolution since its inception and from which anthropology will continue to benefit. First published by Meyer [146] in 2003, Minority Stress Theory sought to explain the pathways to the substantial mental health burdens endured by members of sexual minority groups—gay men, lesbians, and bisexuals. The model distinguished general stress, as is experienced by any person, from the stress experienced as a result of living as a member of a stigmatized group, distal stressors originating outside the subject, and proximal stressors interior to the subject resulting from socialization in a prejudiced society. The focus of Minority Stress Theory has been expanded since its original conception to include gender minorities and the experiences of being repeatedly misgendered [147,148], and attention has been paid to measurable biological impacts of living with minority stress [149]. We expect that of particular interest to anthropologists, especially those with a focus on analyzing the impacts of personal networks, will be the work perofrmed to elucidate the patterns of minority stress contagion in couples [150,151].

9. Conclusions

Our review of concepts and advances in biocultural approaches to understanding stress in humans has highlighted three areas where anthropologists have made significant progress. The first is in terms of the adoption of quantitative instruments for measuring stress. These include the application of assessment of stress through interviews and measuring biomarkers of physiological stress as well as scale creation for both local and comparative contexts. Consequently, it is reasonable to foresee a time in the near future where there are large, rich biocultural databases on stress similar to those that curate genetic data (e.g., GenBank, run by the US National Institutes of Health and the European Molecular Biology Laboratory) that protect confidentiality while giving researchers a baseline with which to compare new results. Cross-cultural comparison is central to the anthropological project, and the development of such databases will significantly facilitate our ability to advance that project.

Second, the use of multiple measures of the experiences and consequences of stress (e.g., social, biological) across cultures helps anthropologists contribute to exposing the fundamental causal mechanisms of stress. We have seen this especially in terms of what we are learning more of about the complex interactions between common social phenomena (e.g., migration, religion) and the hypothalamic–pituitary–adrenal (HPA) axis. Consequently, we can hope to see medical interventions informed by cross-cultural comparative biocultural research.

Third, we are seeing advances in the scope and scale of our understanding of stress. For example, studies that include non-human animals expand upon stress within the larger social ecosystem in which humans operate. We are also seeing the timescale of studies expand from contemporary individuals and groups to across generations and even evolutionary time. As demonstrated by biocultural anthropology’s past, the discipline’s future advances will most likely stem from looking to the cutting-edge approaches of other disciplines while maintaining its commitment to attention to cultural diversity and variation. As a consequence, we are poised to unlock how stress has fundamentally shaped the human experience and what it is to be human.