Stressors, Stress Response, and Cancer Recurrence: A Systematic Review
Todd, Briana L. MA, MS; Moskowitz, Michal C. MS; Ottati, Alicia MA; Feuerstein, Michael PhD, MPH
Author Affiliations: Department of Medical and Clinical Psychology (Mss Todd, Moskowitz, Ottati, and Dr Feuerstein) and Department of Preventive Medicine and Biometrics (Dr Feuerstein), Uniformed Services University of the Health Sciences, Bethesda, Maryland.
The opinions and assertions contained herein are the private views of the authors and are not to be construed as being official or as reflecting the views of the Uniformed Services University of the Health Sciences or the Department of Defense.
The authors have no funding or conflicts of interest to disclose.
Correspondence: Michael Feuerstein, PhD, MPH, Department of Medical and Clinical Psychology and Preventive Medicine and Biometrics, Uniformed Services University of the Health Sciences, 4301 Jones Bridge Road, Bethesda, MD 20814 (firstname.lastname@example.org).
Accepted for publication January 23, 2013.
Background: Cancer survivors assume that stress plays an important role in cancer recurrence. However, the role of stress in the etiology of cancer recurrence remains unclear.
Objective: A systematic review examining the causal role of exposure to stressors and/or stress response and cancer recurrence was conducted.
Methods: The authors screened the scientific literature published from December 1979 through April 2012. Prospective studies and randomized control trials that examined the link between exposure to stressors and/or stress response and cancer recurrence were included in the review.
Results: Fifteen studies examined exposures to stressors (life event questionnaires) and/or multiple indices of the stress response (mood, anxiety, depression, biological, and immune measures). The relationships between stressors and/or stress response and recurrence were observed as no relationship (80%), positive relationship (33%), and inverse relationship (27%). One of 3 randomized control trials reported a positive relationship between stress reduction and reduced risk of recurrence.
Conclusions: The scientific literature to date indicates no clear evidence for a causal relationship between stress (measured as stressor exposure and/or stress response) and cancer recurrence. Although additional high-quality research is needed to provide a more definitive answer, the evidence to date does not support this hypothesis.
Implications for Practice: Although at present, there is no evidence indicating a causal relationship between stress and cancer recurrence, attending to the reduction in a cancer survivor’s stress response can improve emotional well-being and quality of life.
Even after completion of primary treatment, with tests indicating no evidence of disease, cancer survivors grapple with the prospect of a recurrence. In breast cancer survivors, for example, 5-year recurrence rates may range widely from less than 1% to greater than 55% depending on age at diagnosis, type of treatment received, and diagnostic variables such as stage, lymph node involvement, and hormone receptor status.1,2 Fear of recurrence is highly prevalent in cancer survivors, even several years after completion of primary treatment, and is associated with poorer quality of life and well-being.3,4 Several years after diagnosis, uncertainty about recurrence can be triggered by several factors, including environmental stimuli, physical symptoms, or hearing about someone else’s cancer.5
Nurses and other healthcare providers report being asked by patients about lifestyle factors that cause cancer and can prevent recurrence.6 Many cancer survivors assume that stress plays an important role in the risk of cancer recurrence.7–9 When asked about factors preventing recurrence, between 28% and 78% of breast and gynecological cancer survivors cited stress reduction as important.7–9 A link between stress and primary development of cancer also has caught the imagination of the public and has become a common belief.10 A study of testicular cancer survivors (N = 316) found that attributing one’s cancer to psychological stress, which was reported by 17% of the sample, was associated with higher fear of recurrence (odds ratio, 2.57; 95% confidence interval, 1.40–4.73).11
Before addressing the question of whether stress is linked to cancer recurrence, an examination of the term stress is warranted. There is no gold standard definition of stress in human health. Stress is often assessed and measured in 3 broad ways: environmental, psychological, and biological.12 Environmental assessments of stress measure factors outside of the individual, focusing instead on objective exposure to stressors, that is, life events that are commonly perceived as stressful.12 Such measurement may include the occurrence of acute stressors, such as death of a loved one, divorce, illness, or job loss,13 or the existence of recurrent or chronic stressors, such as work stress and marital discord.14 The psychological conceptualization of stress, in contrast, focuses on the individual’s subjective response to stress. Lazarus et al15,16 developed this conceptualization by proposing a cognitive model in which the individual perceives potentially stressful stimuli and determines whether they constitute a threat or challenge. Perception of threatening stimuli activates a stress response that often consists of emotional (eg, negative mood), behavioral (eg, sleep, drinking, smoking), and physiological changes. The physiological stress response entails activation of the hypothalamic-pituitary-adrenocortical (HPA) axis and sympathetic nervous system (SNS),12 which in turn modulate cellular immune responses such as natural killer cell activity.17 Biological measurements of stress may assess indicators of HPA or SNS activity (eg, cortisol, catecholamines) or immune activity that are modulated by the stress response.
A potential link between stress and cancer progression would be consistent with a biobehavioral conceptual model of cancer.17 The perception of stress activates the HPA axis and SNS, which can modulate cellular immune responses that can disrupt physiological processes in tumor surveillance and containment, which may in turn encourage tumor progression or recurrence.17 Exposure to stressors has long been hypothesized to play a role in the recurrence of tumor activity,18 and some investigators have proposed that exposure to psychological stressors plays a larger role in cancer recurrence than cancer incidence.17 However, the role of stressors in the etiology of cancer remains unclear.19 Numerous studies attempting to examine the link between stress and cancer onset have produced conflicting results.19–21
Nurses and other healthcare providers report some reluctance in advising patients about lifestyle factors associated with the prevention of recurrence, in part because of confusion about contradictory findings in the literature.6 Although the hypothetical link between stress and recurrence is one held by many cancer survivors and is biologically plausible, the evidence for such a causal relationship has not been previously systematically reviewed. It is unknown whether stress is indeed positively associated with higher risk of recurrence, or whether stress reduction reduces the risk of recurrence. The purpose of this article was to address the following question: Does stress—measured in environmental, psychological, and/or biological terms—predict the subsequent recurrence of cancer over time? To answer this question, the authors conducted a systematic review of prospective longitudinal human studies and randomized controlled trials measuring stress and recurrence.
Systematic Review Search Strategy
A literature search was conducted using the electronic databases PubMed, Embase, Web of Science, and Cochrane (Figure 1). Limits on the search included studies published until April 2012 (ie, no limits were placed on the start date of the search, and the earliest date captured was August 1974), studies in the English language, and studies on humans. For PubMed, the MeSH search terms included (neoplasm [majr]) AND (neoplasm recurrence, local OR recurrence) AND (anxiety OR depression OR stress, psychological OR life change events). For Embase, the Emtree search terms included (cancer recurrence [exp/mj]) AND (stress [exp] OR anxiety [exp] OR depression [exp]). When searching Cochrane, the keyword search terms included (cancer) AND (recurrence) AND (stress OR anxiety OR depression OR stressful life event). The search terms for Web of Science included cancer, recurrence, stress, stressful life events, anxiety, and depression.
To be included, studies were required to measure stress in at least 1 of 3 ways: (1) environmental exposure to stressors such as cumulative life events that require adaptation (eg, death of a spouse), (2) psychological stress response such as measures of depression, anxiety, or mood in general, and (3) biological measures of either (a) direct stress response, for example, cortisol as an indicator of HPA axis activation, or (b) immune markers that are downregulated by activation of the stress response (eg, natural killer cell activity). These various modes of stressor exposure and stress response measurement are frequently used in the stress and health literature. All studies were required to include cancer recurrence as an outcome measure.
Exclusion criteria were as follows: cancer recurrence not an outcome variable (ie, dependent variable), stressor exposure and/or stress response not an independent variable (ie, exposure), stressor exposure and/or stress response did not proceed recurrence (ie, did not show prospective relationship), cancer was not examined, metastatic cancer was solely examined, not original articles, or cross-sectional, retrospective, or case studies. Two reviewers independently searched the titles and abstracts of the search results. When abstracts were ambiguous about meeting the inclusion/exclusion criteria for this review, the reviewers read the full text of the articles to determine inclusion. A third reviewer settled any disagreements in inclusion or exclusion between the first 2 reviewers. Reference lists were also examined to identify further articles for inclusion. Of 990 articles (77 duplicate articles were removed), lack of agreement occurred between the 2 initial reviewers on 18 articles. The interrater agreement was 98.18% (972/990).
As Figure 1 indicates, of 1067 (990 when excluding duplicates) potential papers on stressor exposure and/or stress response and cancer recurrence, only 15 articles met the inclusion criteria.22–36 These studies are summarized in the Table. As the Table indicates, there were 2 studies published from the 1970 to 1989 period, followed by 5 in the decade between 1990 and 1999, 6 studies between 2000 and 2009, and 2 thus far since 2010. Three studies were randomized control trials (RCTs). However, 2 of these studies followed the same participants over time.22,23 Although we did not limit the review to any specific types of cancer, 12 of 15 studies researched breast cancer and 3 of 15 examined melanoma. One study included biological measures of stress response (ie, cortisol and catecholamines). Five studies assessed biological measures of immunological activity associated with stress response. Six of the articles used environmental measures of recent life events as the index of stressor exposure, and 13 used measures of the psychological response to stress (eg, distress, depressive symptoms, anxiety symptoms).
The findings related to stress and cancer recurrence are illustrated in Figure 2. As the figure indicates, most of the studies (12/15) reported finding no relationship between cancer recurrence and at least 1 measure of stress. Ten studies reported exclusively null or even inverse findings. Three studies reported at least 1 finding of an inverse relationship between stress and cancer recurrence (ie, higher stress predicted lower recurrence). One study exclusively reported an inverse relationship between stress and recurrence. Five of 15 studies reported a positive association between cancer recurrence and stress, of which only 2 studies exclusively reported a positive finding and 3 reported mixed findings. When considering the 9 studies (7 longitudinal trials and 2 RCTs) that included multiple dimensions of stress (ie, environmental, biological, and psychological), 3 studies indicated a positive relationship between stressor exposure and/or stress response and cancer recurrence. The data points in Figure 2 exceed 100% of the studies because certain studies had multiple findings.
Findings differed by the dimension of stress assessed in each study (environmental, psychological, and biological). None of the 5 studies using environmental measures of stressor exposure (acute stressful life events and/or chronic stressors) reported a positive relationship between stressor exposure and cancer recurrence. On the contrary, 1 study found a significant inverse relationship whereby greater exposure to stressful events predicted nonrecurrence.27 Of the 13 studies assessing psychological stress response, 4 reported at least 1 positive finding, 7 reported exclusively null findings, and 1 reported an inverse finding. Of the studies using a biological measure of immune function, 2 reported mixed findings (1 reported both inverse and null results and 1 reported both positive and null results) and 5 found no association between stressor exposure and/or stress response and cancer recurrence. Only 1 study used a biological correlate of the stress response (ie, cortisol, catecholamines), and it reported mixed null and positive findings.
The current study systematically reviewed literature investigating the link between stressor exposure and/or stress response and cancer recurrence published from December 1979 through April 2012. At this time, there is insufficient evidence to conclude that a causal relationship between stressor exposure and/or stress response and cancer recurrence exists. Most of the studies did not find a relationship between stressors/stress response and cancer recurrence. Many of these studies examined multiple measures of stressor exposure/responses, and these studies reported mixed findings (ie, lack of findings, positive findings, and/or inverse findings).
Considering the differences in findings for each dimension of stress (mostly null findings of a relationship between environmental stressor exposure and recurrence, mixed positive and null findings of an association between psychological stress response and recurrence, and very few studies relating biological stress response and recurrence), there is, at best, tentative evidence of a possible relationship between psychological stress response and recurrence. However, further research is needed before any definitive conclusions can be drawn. It is difficult to know whether null findings can be attributed to insufficient power, measurement error, or a true null relationship.
It is important when reviewing evidence for the hypothesis related to stress (stressor exposure and/or stress response) and cancer recurrence that we consider the criteria that have emerged as a framework for determining whether an exposure is likely to be a causal agent of a health outcome.37 When considering this set of criteria, it is also important to recognize that many chronic illnesses, including cancer, can have a multivariate set of risk factors.38 Although this review focuses on stressor exposure and/or stress response, the identification of only 1 risk factor for any single disease is highly unlikely. It is often the combination of risk factors that predicts a disease.39 However, even if a cause-and-effect relationship is observed in a prospective study, for an exposure to be considered a viable “risk factor,” a certain pattern of findings should be observed. This pattern of evidence can provide guidance for determining whether there is necessary and sufficient evidence to conclude that exposure to a stressor represents a risk factor with a certain value that predicts cancer recurrence.
The 9 criteria for determining that a certain independent variable (exposure) is a risk factor for a specific health outcome are as follows: (1) strength of the relationship (ie, value of the relative risk ratio); (2) consistency of the association in different locations by different researchers; (3) specificity of the risk factor’s association with the disease and not others; (4) temporal relationship of exposure followed by the health outcome; (5) dose-response relationship, where higher levels of the exposure are related to higher levels of the health outcome (disease); (6) plausibility, where an evidence-based biological pathway exists; (7) coherence, where experimental findings reflect epidemiological findings; (8) experimental confirmation, where change in the exposure results in change in the health outcome (disease) based on RCTs; and (9) consideration of alternate hypotheses.37
The literature reviewed in this article was not consistent in the strength or direction of the relationship. The specificity criteria may not be appropriate for all health outcomes (eg, chronic illness) as it is with infectious diseases that are often acute in nature. Stress has been reported as a casual factor of several types of illnesses (eg, certain cardiovascular diseases). Although all studies in the present review reported exposure before the potential outcome of recurrence (ie, prospective), the outcomes varied in direction. In addition, there is no evidence of a dose-response relationship between stress and cancer recurrence in humans. Currently, the strongest evidence that stressor exposure and/or stress response may be a causal agent in cancer onset or recurrence is based on biological plausibility.17
Our review identified 3 RCTs.22–24 Andersen and colleagues24 provided evidence that stress reduction lowers a breast cancer survivor’s risk for recurrence. However, Fawzy et al found that a psychosocial intervention aimed at reducing psychological distress (ie, stress response) did not affect malignant melanoma recurrence at 5 to 6 years23 or at 10 years22 after treatment. Although the effects may be cancer type specific, the Andersen et al study has met with concern over the analyses of results.40 There is very little consistent evidence from RCTs that can inform us of the causal effects of stress exposure on recurrence.
All prospective studies reviewed were characterized by several methodological limitations, including the lack of a consistent measure of stressor exposure and/or stress response and potentially inadequate power to detect differences given the small number of participants. The type of stressor exposure and/or stress response also varied by study, complicating the interpretation of the findings. The studies reviewed assessed only limited aspects of stress; however, stress is a multidimensional phenomenon that can be measured in a variety of ways. Moreover, cancer recurrence was not consistently operationally defined. Whereas some studies clearly defined recurrence,26–29 the majority lacked a specific definition.22–25,30–36 The underlying models of stress that were used by the investigators are not always explicit. This type of transparency would greatly help the reader better understand choice of measurement and should be included in the measurement sections of methods. Finally, all studies included in the review measured stress response or stressor exposure at 1 specific point in time, yet stress response and stressor exposure are dynamic and can change over time. In addition to the concerns with the individual studies listed previously, there are limitations of the current review that should also be considered. The selected studies were limited to English only. In addition, most of the articles in the review studied breast cancer survivors. Considering differences between the male and female physiological stress response,41 it is unknown how gender might affect the findings.
Although the finding of an inverse relationship between stress and recurrence is opposite to the original hypothesis, a plausible biological explanation for this observation has been proposed.42 Unlike chronic stressors, acute stressors trigger the body to redistribute immune cells such as leukocytes to organs and injured sites to prepare the body for potential injury or infection, thereby improving overall immune response.42,43
Future studies should include prospective designs that measure stressor exposure and/or stress response with valid and consistent instruments and that account for confounding variables (eg, time since initial diagnosis, stage of tumor, previous psychiatric history). Although this review was not designed to focus on any specific cancer site, the articles retrieved studied breast cancer and melanoma. Future studies need to focus on many types of cancers to determine whether there may be an interaction with cancer type, treatment exposures, stressors, stress response, and recurrence. Examining cancers that are hormonally mediated, such as prostate and endometrial cancers, or immune mediated, such as leukemia and lymphomas, may be more likely to reveal a link between stress and cancer recurrence because of the relationship among exposure to stressors, immune response, and cancer progression.18 Future research on stress and cancer recurrence should consider each of the criteria for an evidence-based risk factor.38
Although the current review did not find consistent evidence for the relationship between stressor exposure and/or stress response and cancer recurrence, this does not negate the relationship among stressor exposure and/or stress response and long-term and late effects that cancer survivors experience over time.44 For example, after exposure to a stressor, breast cancer survivors with persistent fatigue differ in cortisol response compared with breast cancer survivors without fatigue, indicating that exposure to stressors plays a role in fatigue.45 In the general population, excessive exposure to stressors has also been related to cognitive problems (eg, impaired memory), sleep disturbance, and poorer mental health (eg, mood and anxiety disorders).46
In response to cancer survivors who may be concerned that stress leads to cancer recurrence, nurses can reassure survivors that at this point, there is no conclusive evidence that exposure to stressors or stress response cause cancer recurrence. However, considering the preliminary evidence that psychological stress response may possibly be a risk factor for cancer recurrence, as well as evidence that excessive stress is deleterious for other health reasons, it is recommended that cancer survivors maintain a healthy level of stress in their lives. Nurses can advise patients to use empirically supported treatments to manage psychological stress. Interventions targeted at attenuating the stress response reduce some measures of symptom burden.
A systematic review of cognitive-behavioral therapy approaches indicated that these approaches were effective in reducing a cancer survivor’s anxiety, depression, and quality of life in the short run.47 In addition, results from another systematic review indicate that when yoga is used as an intervention for emotional and physical health, along with mindfulness-based stress reduction, moderate improvements in stress response levels, quality of life, and mood are observed in a heterogeneous sample of cancer patients and survivors.48
Despite the lack of conclusive evidence supporting a relationship between stressor exposure and/or stress responses with cancer recurrence, attending to the reduction in a cancer survivor’s stress response can improve emotional well-being and quality of life. Nurses can play a pivotal role in this endeavor by assessing survivor beliefs about causal associations between stressors or stress-reducing behaviors and risk of recurrence.8,9,11,49 Nurses can also offer guidance about coping with common stressors and posttreatment symptoms.50
High-quality evidence is needed to provide a more definitive answer to the question of the role of stressors and/or the stress response in cancer recurrence. The overall evidence to date does not provide support for this hypothesis. The use of various stress management approaches may be more appropriately targeted at symptom management rather that recurrence, although such a relationship was not addressed in the current review.
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Cancer survivors; Exposure; Neoplasm; Recurrence; Stress; Systematic review
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