Keywords: CKD, renal protection, risk factors
Abstract
Key Points
Adaptive coping behaviors are associated with lower odds of incident CKD.
Coping behaviors could represent a target to prevent CKD.
Background
How someone copes may alter the trajectory of their kidney function. We aimed to evaluate whether coping behaviors were associated with incident CKD or rapid kidney function decline.
Methods
We used data from the Healthy Aging in Neighborhoods of Diversity across the Life Span study (Baltimore, MD) for this longitudinal analysis. Adaptive and maladaptive coping behavioral constructs were measured using the Brief COPE Inventory at visit 1. We used multiple logistic regression to assess the odds of incident CKD and rapid kidney function decline per point increase in coping scales and adjusted for baseline demographics and clinical variables.
Results
Of 1935 participants, mean age was 48 years, 44% were male, 56% were Black persons, and baseline mean (SD) eGFR was 91 (16) ml/min per 1.73 m2. After a median of 8.2 years, 113 participants developed incident CKD and 341 had rapid kidney function decline. Compared with those who reported they usually did not use adaptive coping behaviors at all (such as emotional support), those with the highest use of adaptive coping had lower odds of incident CKD. Every 1-unit increase in adaptive coping corresponded with a 2% lower adjusted odds of incident CKD (odds ratio, 0.98; 95% confidence interval, 0.95 to 0.99). There was no association between maladaptive coping behaviors and incident CKD. Coping behaviors were not associated with rapid kidney function decline.
Conclusions
Adaptive coping behaviors were associated with lower odds of incident CKD and could represent a target to facilitate CKD prevention. The role of medical care in this association is an area worthy of further investigation.
Introduction
A diagnosis of kidney disease carries notable challenges for individuals. Kidney disease is associated with a high medication burden, frequent appointments, nuanced dietary restrictions, and financial resource strain.1–3 There is a high burden of emotional distress among people with kidney disease and limited therapeutic success of antidepressant medications.2,3 To prevent kidney disease from developing and progressing, individuals must be active participants in their medical care, advocate for themselves, and manage comorbidities. Existing literature suggests that how individuals cope with challenges may make them more or less likely to engage in care and manage comorbidities, potentially altering the trajectory of their kidney function.4–11
Coping has been defined as constantly changing cognitive, behavioral, and emotional efforts to manage particular external and/or internal demands that are appraised as taxing or exceeding the resources of a person.12–15 Typical responses to stressful events vary across populations and cultures. However, certain coping tendencies are believed to promote resolution of conflict and greater adaptation than others. Adaptive coping behaviors involve active ways to deal with stressful events, including problem solving, reframing the meaning of the problem, seeking information, or turning to instrumental or religious support.12 Maladaptive coping behaviors promote feelings of helplessness, reliance on others to resolve the stressful event, or result in avoidance, withdrawal, or wishful thinking, although these strategies sometimes develop as a way to survive uncontrollable stressors.12 It is unknown whether coping behaviors are associated with the development of CKD or disease progression.
We aimed to evaluate whether coping behaviors were prospectively associated with incident CKD or rapid kidney function decline among community-dwelling adults with normal kidney function. We hypothesized that greater use of adaptive coping behaviors would be associated with lower odds of incident CKD and rapid kidney function decline and that greater use of maladaptive coping behaviors would be associated with higher odds of incident CKD and rapid kidney function decline.
Methods
Healthy Aging in Neighborhoods of Diversity across the Life Span Study
We analyzed data from the National Institute on Aging, Healthy Aging in Neighborhoods of Diversity across the Life Span (HANDLS) study, which has been described in detail.16 HANDLS is a population-based cohort study examining the interaction of race and socioeconomic status on the development of health disparities among historically minoritized populations and people with lower socioeconomic status. The cohort includes 3720 Black and White community-dwelling individuals aged 30–64 years sampled from 13 neighborhoods in both low and high socioeconomic strata (self-reported household income <125% and ≥125% of 2004 Federal Poverty Guidelines) in Baltimore, Maryland. Participant enrollment occurred between August 2004 and November 2008, with the plan for 20 years of five triennial study visits. Each participant provided informed consent and was compensated monetarily, and the National Institute of Environmental Health Sciences, National Institute of Health, approved the study protocol. Data from HANDLS visits 1 (August 2004–March 2009), 3 (June 2009–July 2013), and 4 (September 2013–September 2017) were used for this study.
Study Sample
Participants were excluded from this study if they did not complete their baseline medical examination (n=1066), if they were missing the Brief COPE Inventory (n=568), or if they had prevalent eGFR <60 ml/min per 1.73 m2 (n=151) at visit 1 (Figure 1). The final study sample included 1935 participants, and the analytic samples with complete cases for the incident CKD and rapid decline analyses were 1552 and 1147, respectively.
Figure 1.
Study flow diagram. We defined incident CKD as the first occurrence of eGFR <60 ml/min per 1.73 m2 and ≥25% decline in eGFR at study visits 3 or 4 in relation to visit 1 and rapid decline as eGFR loss of >3 ml/min per 1.73 m2 per year between study visits 3 and 4. The rapid kidney function decline analytic sample was smaller because there were fewer participants who had eGFR data from both visits 3 and 4. HANDLS, Healthy Aging in Neighborhoods of Diversity across the Life Span.
Measurement of Coping Behaviors
Coping behaviors were measured using the Brief COPE Inventory14,17–20 as part of the audio computer-assisted self-interview questionnaires on the mobile research vehicles (Figure 2). The Brief COPE Inventory included 28 items, with 14 subscales and two items per subscale. It assessed tendencies to use positive reinterpretation, active coping, use of humor, acceptance, planning, religious coping, use of instrumental support, use of emotional support, behavioral disengagement, self-distraction, focus on venting of emotions, self-blame, denial, and substance use. Inventory questions were modified to assess what participants usually do when confronted with a stressful event by adding the word “usually” to responses. All statements began with “When I am confronted with a difficult or stressful event.” Responses were scored as 1: “I usually do not do this at all,” 2: “I usually do this a little bit,” 3: “I usually do this a medium amount,” or 4: “I usually do this a lot.”
Figure 2.
Subscales of the Brief COPE Inventory.
On the basis of existing literature, we categorized the subscales into two groupings: adaptive coping and maladaptive coping.21 Adaptive coping consisted of eight subscales: positive reinterpretation, active coping, humor, acceptance, planning, religious coping, use of instrumental support, and use of emotional support. Maladaptive coping consisted of six subscales: behavioral disengagement, self-distraction, focus on venting of emotions, self-blame, denial, and substance use. Adaptive and maladaptive coping were both analyzed as continuous variables reflecting the sum of constituent subscales. Adaptive coping can range from 16 to 64, and maladaptive coping can range from 12 to 48, with higher values reflecting higher self-reported use of the behaviors within that grouping.
Measurement of Outcomes
Primary outcomes were incident CKD and rapid kidney function decline. We included both outcomes to determine whether the relation between coping behaviors and kidney disease development differed from the relation with kidney disease progression. Incident CKD was defined as first occurrence of eGFR <60 ml/min per 1.73 m2 and ≥25% decline in eGFR at study visits 3 or 4 in relation to visit 1.22,23 Rapid kidney function decline was defined as eGFR loss of >3 ml/min per 1.73 m2 per year between study visits 3 and 4.23,24 Both outcomes were analyzed as dichotomous variables (yes/no). We used the creatinine-based CKD Epidemiology Collaboration 2021 equation to calculate eGFR.25
Fasting blood samples were obtained during study visit medical assessments. Serum creatinine was measured at Quest Diagnostics Inc. by isotype dilution mass spectrometry (Olympus America Inc., Melville, NY) and standardized to the reference laboratory at the Cleveland Clinic.
Measurement of Covariables
Sex at birth, self-identified Black or White race, and household income above or below 125% of the federal poverty level were ascertained at enrollment. Depressive symptoms were measured using the twenty-item Center for Epidemiologic Studies Depression (CES-D)26,27 during visit 1, which ranged from 0 to 30, and higher values indicated higher depressive symptoms. Total CES-D was analyzed as a categorical variable (low: <10, moderate: 10–20, or severe: ≥21).17,28–30 Hypertension status was defined as (yes/no) self-report of hypertension, measured BP >140/90 mm Hg, or prescription of antihypertensive medications at visit 1. Diabetes status was defined as (yes/no) self-report of diabetes, fasting glucose ≥126 mg/dl, prescription of diabetes medications, or serum hemoglobin A1c ≥6.5% at visit 1. Urine samples were obtained during study visit medical assessments. Urine albumin-to-creatinine ratio measurement was performed at Quest Diagnostics Inc. using an immunoturbidimetric assay (Kamiya Biomedical Co., Seattle, WA).
Statistical Analyses
We described participants' characteristics using proportions for categorical variables and means (SD) or medians (interquartile range) for continuous variables. We evaluated frequencies of each coping behavior.
We used multiple logistic regression to assess whether adaptive and maladaptive coping at visit 1 were associated with kidney outcomes at visits 3 and 4. For each outcome, we fit regression models with two levels of adjusters in addition to coping variables. In conjunction with existing literature and our conceptual framework, we chose the models with the greatest parsimony and least amount of missing data. The first model adjusted for age, race, sex at birth, poverty status, and visit 1 eGFR; the second model additionally adjusted for visit 1 hypertension and diabetes status to account for the potential effect of comorbidities on coping and outcomes. As a post hoc exploratory analysis, for scales found to be significantly associated with outcomes, we used multiple logistic regression to assess whether individual behaviors were associated with the outcome.
To explore whether relations between coping and outcomes vary in the setting of different levels of depressive symptoms, we evaluated for effect modification by depressive symptoms by including interaction terms for adaptive coping×CES-D and maladaptive coping×CES-D. To explore whether coping behaviors drive the previously documented associations between depression and kidney outcomes, we used the mediation package in R to evaluate for mediation of depressive symptoms at visit 1 and outcomes at visits 3 and 4 by coping behaviors at visit 1.31–33
Follow-up time was dictated by data availability. We accounted for time by adjusting for visit 1 eGFR. Differential time to follow-up between study visits was accounted for by adjusting for the time difference between visit 1 and visit 4. The mean imputation was used for participants missing visit 4. All analyses were performed using R Statistical Software (version 4.1.2; R Core Team 2021). A P value ≤ 0.05 was considered statistically significant.
Results
Primary Analysis
Among 1935 individuals in the study population, mean (SD) age was 48 (9.1) years, 847 (43.8%) were male, 1080 (55.8%) were Black persons, mean (SD) baseline eGFR was 91.4 (15.5) ml/min per 1.73 m2, and mean (SD) baseline urine albumin-to-creatinine ratio was 26.1 (144.5) mg/g (Table 1). The median (interquartile range) adaptive and maladaptive coping was 43 (36–49) and 23 (19–27), respectively. Active coping, planning, acceptance, and religious coping behaviors were common (Supplemental Figure 1). HANDLS participants who were excluded for missing the Brief COPE Inventory did not differ substantially from those included in this study (Supplemental Table 1).
Table 1.
Study sample characteristics
Characteristic | Total N=1935 |
---|---|
Age, mean (SD) yr | 48 (9.1) |
Sex, N (%) | |
Women | 1088 (56.2) |
Men | 847 (43.8) |
Race, N (%) | |
White | 855 (44.2) |
Black | 1080 (55.8) |
Income <125% Federal poverty level, N (%) | |
Above | 1140 (58.9) |
Below | 795 (41.1) |
Adaptive coping, mean (SD) | 42.5 (9.2) |
Maladaptive coping, mean (SD) | 23.5 (5.9) |
Baseline eGFR, mean (SD) ml/min per 1.73 m2 | 91.4 (15.5) |
Baseline urine albumin/creatinine ratio, mean (SD) mg/g | 26.1 (144.5) |
Hypertension, N (%) | |
No | 1104 (57.8) |
Yes | 807 (42.2) |
Missing | 24 (1.2) |
Diabetes, N (%) | |
No diabetes | 1262 (66.2) |
Prediabetes | 350 (18.4) |
Diabetes | 294 (15.4) |
Missing | 29 (1.5) |
Depressive Symptoms, N (%) | |
Low (CES-D <10) | 779 (40.3) |
Moderate (CES-D 10–20) | 575 (29.7) |
Severe (CES-D ≥21) | 549 (28.4) |
Missing | 32 (1.7) |
Health insurance | |
No | 621 (33) |
Yes | 1260 (67) |
Postponed seeking healthcare in the last 12 mo | |
Needed but did not postpone | 858 (45.6) |
Yes | 639 (34) |
Did not need health care | 384 (20.4) |
Missing | 54 (2.8) |
CES-D, Center for Epidemiologic Study Depression.
There were 1935 individuals in the study sample. Among those, only complete cases were included in the analytic samples. There were 1552 participants in the incident CKD sample and 1147 participants in the rapid kidney function decline analysis.
We followed participants for a median of 8.2 years. There were 1552 participants with complete information in the incident CKD analytic sample, of whom 113 (7.2%) developed CKD. For every one-point increase in adaptive coping, the odds of incident CKD decreased by 2% (adjusted odds ratio [OR], 0.98; 95% confidence interval [CI], 0.96 to 0.999) (Figure 3, Table 2). For example, compared with those with the lowest score on the adaptive coping scale (score=16), those with the highest reported use of adaptive coping behaviors (score=64) had 96% lower odds of incident CKD. The use of positive reinterpretation and religious coping were independently associated with reduced odds of incident CKD (Supplemental Table 2). Maladaptive coping was not significantly associated with incident CKD (adjusted OR, 1.02; 95% CI, 0.98 to 1.05 for every one-point increase in maladaptive coping).
Figure 3.
Relationship of coping behaviors with incident CKD (eGFR <60 ml/min per 1.73 m2 and ≥25% decline at study visits 3 or 4 in relation to visit 1) and rapid kidney function decline (eGFR loss of >3 ml/min per 1.73 m2 per year). P values correspond with associations between one-point increase in coping scales and outcomes.
Table 2.
Association between coping behaviors, incident CKD and rapid kidney function decline
Analysis | OR (95% CI) of the Outcome per One-Point Increase in Coping Scale | |
---|---|---|
Model 1 | Model 2 | |
Incident CKDa (n=1552; events=113) | ||
Adaptiveb | 0.98 (0.95 to 1.00) | 0.98 (0.96 to 0.999) |
Maladaptiveb | 1.02 (0.98 to 1.05) | 1.02 (0.98 to 1.05) |
Rapid kidney function declinea (n=1147; events=341) | ||
Adaptive | 0.99 (0.98 to 1.01) | 0.99 (0.98 to 1.01) |
Maladaptive | 1.00 (0.97 to 1.02) | 1.00 (0.98 to 1.02) |
Model 1: adaptive and maladaptive coping+adjustment for age, differential time to follow-up, sex, race, baseline eGFR, and poverty status.
Model 2: model 1+adjustment for baseline hypertension and diabetes status.
OR, odds ratio; CI, confidence interval.
Incident CKD was defined as eGFR <60 ml/min per 1.73 m2 and ≥25% decline at study visits 3 or 4 in relation to visit 1; rapid kidney function decline was defined as eGFR loss of >3 ml/min per 1.73 m2 per year.
Adaptive and maladaptive coping were analyzed as continuous variables reflecting the sum of constituent subscales. Adaptive coping ranged from 16 to 64, and maladaptive coping ranged from 12 to 48, with higher values reflecting higher self-reported use of the behaviors within that factor. Adaptive coping consisted of eight subscales: positive reinterpretation, active coping, humor, acceptance, planning, religious coping, use of instrumental support, and use of emotional support. Maladaptive coping consisted of six subscales: behavioral disengagement, self-distraction, focus on venting of emotions, self-blame, denial, and substance use.
There were 1147 participants with complete information in the rapid kidney function decline analytic sample, of whom 341 (29.7%) experienced the outcome. Adaptive coping was not associated with rapid kidney function decline (adjusted OR, 0.99; 95% CI, 0.98 to 1.01 for every one-point increase in adaptive coping). Maladaptive coping was not associated with rapid kidney function decline (adjusted OR, 1.00; 95% CI, 0.98 to 1.02 for every one-point increase in maladaptive coping).
Exploratory Analyses
The relationships between coping behaviors and incident CKD were not modified by depressive symptoms (P interaction 0.52 for adaptive coping; P interaction 0.99 for maladaptive coping). The relationships between coping behaviors and rapid kidney function decline were not modified by depressive symptoms (P interaction 0.32 for adaptive coping; P interaction 1.00 for maladaptive coping). We did not find an association between depressive symptoms at visit 1 and outcomes, so formal evaluation for mediation by coping behaviors was not performed.
Discussion
In this prospective cohort study of urban-dwelling adults with normal baseline kidney function, higher self-reported use of adaptive coping was associated with lower odds of incident CKD, but not rapid kidney function decline. Maladaptive coping behaviors were not associated with incident CKD or rapid kidney function decline.
To the best of our knowledge, this study was among the first to evaluate the relationship between multiple coping behaviors, incident CKD, and rapid kidney function decline. Our findings are similar to past studies that have highlighted the positive effect of religion, social support, and other coping tendencies on kidney outcomes.34,35 For example, in a study that included 76,443 adults with low socioeconomic status, Black persons who reported high spirituality had reduced kidney failure risk after multivariate adjustment.36 Among people with kidney disease, coping behaviors have been found to affect mental wellbeing, symptoms, and overall quality of life.37–39 For example, individuals on dialysis who deal with stress through avoidance strategies (focus on work or distractions to not think about stress) tend to find their illness more intrusive and have lower quality of life.4
Emotional distress is common among people with kidney disease, and hospitalizations due to anxiety, depression, and substance abuse are 1.5–3 times more common than individuals with other chronic diseases.40 We found that associations between coping and outcomes did not differ according to severity of depressive symptoms. We did not find an association between depressive symptoms and outcomes, unlike past studies,29 and therefore did not assess for mediation by coping behaviors. Our study may have been underpowered to evaluate the nuanced relationships between coping, depression, and kidney disease or an association between maladaptive coping behaviors and outcomes, and future larger studies are needed.
Adaptive coping behaviors may be linked to kidney disease via development and control of comorbidities and health promoting behaviors. People with higher use of adaptive behaviors might be more consistent with their self-care, play a more active role in managing their medical conditions, or minimize disruptions in health and medical care when they encounter stressful life events. Adaptive coping may also affect health through neurohormonal mechanisms. Stress is postulated to enhance sympathetic nervous system activity, the renin–angiotensin–aldosterone system, inflammatory cytokines, the hypothalamic–pituitary–adrenal axis, and endothelin-A.41–46 By mitigating stress, adaptive coping behaviors might lower levels of hypertension, diabetes, obesity, and vascular disease, all risk factors for kidney disease. Age, sex, and socioeconomic status may be associated with the use of adaptive behaviors, although studies on predictors of various coping behaviors are mixed.20,34,35 Additional studies that examine whether coping behaviors influence care processes, such as being seen by a specialist and obtaining control of blood pressure and glycemia, are needed.
Inquiring about coping and encouraging the use of adaptive coping behaviors could be incorporated into clinical practice, which may promote CKD prevention by optimizing management of comorbidities. Providing individuals and their family members with opportunities to become kidney disease advocates could facilitate positive reinterpretation and the opportunity to make sense of their diagnosis (i.e., “I developed kidney disease, so I can help others and raise awareness”).47 Motivational interviewing is a communication style that helps people resolve ambivalent feelings and find internal motivation and can be used to encourage acceptance and positive reinterpretation.48 Giving patients the tools they need to properly manage their disease and feel in control and facilitating positive psychological strategies might facilitate active coping and planning. For example, meditation and mindfulness have been associated with reduction in blood pressure and stress.49,50
Inquiring about faith and religious preferences and whether patients would like to involve religious leaders could facilitate religious coping. The use of instrumental and emotional support could be encouraged by including family members or their support system when making decisions about clinical care, or disease-specific support groups could be offered to strengthen patients' connections and sense of belonging.51 Trauma-informed care is a standardized approach to deliver sensitive care to people who have experienced a variety of traumatic experiences, including illness-related trauma, which is sensitive and avoids retraumatization and should be considered in all medical settings to facilitate a trusting and supportive relationship with health care staff.52,53
Strengths of this study include the prospective design and identification of a novel risk factor for kidney disease among people with normal kidney function.
Some limitations bear mention. We categorized behaviors as adaptive or maladaptive to be consistent with other studies that used the Brief COPE Inventory. Whether one coping behavior, or a combination, produces a superior outcome likely depends on the individual, the stressor, and the context, and it is difficult to capture the nuanced effects of each unique behavior.12 We analyzed behaviors as continuous variables to avoid assigning arbitrary cutoffs, with higher values reflecting higher self-reported use of the behaviors within each grouping. The exact amount of adaptive coping needed to make a difference clinically is difficult to discern. We evaluated how someone usually copes, but whether these behaviors are functionally the same in the short term is unclear. By using a single baseline assessment of coping behaviors, we were unable to capture how participants' coping changed over time. Additional studies on specific behaviors, their frequency of use, how they change over time, their meaning in an individual's life, and relation with kidney disease are needed.
Those who completed the baseline medical examination or Brief COPE Inventory as part of HANDLS might have been more engaged in this study and introduce selection bias if their distribution of coping behaviors differed from those who did not complete the Brief COPE Inventory. Our findings may not be generalizable to nonurban populations or populations with different ethnic compositions, given cultural nuances in coping behaviors.
In conclusion, we found that higher self-reported use of adaptive coping was associated with lower odds of incident CKD. Our work highlights a potential target for kidney disease prevention. Longitudinal studies that apply qualitative methods and studies using larger cohorts are needed to delineate the mechanisms underlying coping and the development of CKD.
Supplementary Material
Disclosures
D.C. Crews reports the following: Consultancy: Yale New Haven Health Services Corporation Center for Outcomes Research and Evaluation (CORE); Research Funding: Baxter International; Somatus, Inc.; Honoraria: Maze Therapeutics; Advisory or Leadership Role: Editorial Board—Journal of Renal Nutrition, Clinical Journal of the American Society of Nephrology, Journal of the American Society of Nephrology; Associate Editor, Kidney360; Co-Chair, Bayer HealthCare Pharmaceuticals Inc. Patient and Physician Advisory Board Steering Committee for Disparities in CKD Project; Advisory Group, Health Equity Collaborative, Partner Research for Equitable System Transformation after COVID-19 (PRESTA), Optum Labs; and Other Interests or Relationships: Board of Directors, National Kidney Foundation of Maryland/Delaware; Nephrology Board, American Board of Internal Medicine; Council of Subspecialist Societies, American College of Physicians; Executive Councilor, American Society of Nephrology. T.K. Novick reports the following: Consultancy: Cricket Health. P.J. Rathouz reports the following: Consultancy: Consultant for Sunovion Pharmaceuticals, unrelated to this work presented here. All remaining authors have nothing to disclose.
Funding
This work is supported by the Intramural Research Program of the National Institute on Aging, National Institutes of Health (AG000513). Dr. T.K. Novick is supported by the National Institute of Diabetes and Digestive and Kidney Diseases grant K23DK127153. Dr. D.C. Crews is supported by grant K24HL148181 from the National Heart, Lung and Blood Institute/NIH.
Author Contributions
Conceptualization: Deidra C. Crews, Michele K. Evans, Marie Kuczmarski, Tessa K. Novick, Paul J. Rathouz.
Data curation: Tessa K. Novick, Alan B. Zonderman.
Formal analysis: James Custer, Tessa K. Novick, Paul J. Rathouz.
Investigation: Deidra C. Crews, Tessa K. Novick.
Methodology: Deidra C. Crews, Tessa K. Novick.
Project administration: Tessa K. Novick.
Resources: Alan B. Zonderman.
Supervision: Deidra C. Crews.
Writing – original draft: Tessa K. Novick.
Writing – review & editing: Deidra C. Crews, Michele K. Evans, Melissa Hladek, Marie Kuczmarski, Tessa K. Novick, Paul J. Rathouz, Alan B. Zonderman.
Supplemental Material
This article contains the following supplemental material online at http://links.lww.com/KN9/A373.
Supplemental Figure 1. Frequency of individual coping behavior.
Supplemental Table 1. Comparison of HANDLs participants who were included versus those who were excluded due to missing the Brief COPE Inventory.
Supplemental Table 2. Association between Adaptive Coping subscales and Incident CKD.
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