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. Author manuscript; available in PMC: 2018 Nov 1.
Published in final edited form as: Brain Behav Immun. 2017 May 22;66:85–88. doi: 10.1016/j.bbi.2017.05.016

Inflammation and Attentional Bias in Breast Cancer Survivors

Chloe C Boyle 1, Patricia A Ganz 2,3, Kathleen M Van Dyk 2, Julienne E Bower 1,2,4
PMCID: PMC5920531  NIHMSID: NIHMS959834  PMID: 28546059

Abstract

Evidence suggests an association between inflammation and depression, although findings are mixed. Focusing on core processes in depression may clarify associated biological underpinnings. Negative cognitive bias is a key component of depression, but has not been examined in relation to inflammation. Thus, we tested the hypothesis that elevated inflammatory markers would be associated with negative attentional bias in a sample of 91 breast cancer survivors. Participants were drawn from a larger study and provided blood samples for assessment of peripheral markers of inflammation and completed questionnaires and neuropsychological testing. Attentional bias towards emotional stimuli was assessed with a dot-probe computer task using emotional (sad, happy, angry) and neutral faces. Circulating concentrations of C-reactive protein (CRP) were positively correlated with negative attentional bias (p = .03), such that women with higher CRP allocated greater attention towards sad faces. This association held when controlling for attention function and current depressive symptoms. While cross-sectional, results are consistent with research showing that inflammation heightens the salience of negative emotional stimuli, and identify a novel pathway through which inflammation may lead to depression.

Keywords: inflammation, C-reactive protein, depression, attentional bias

1. Introduction

A growing literature implicates inflammation in the pathogenesis of depression. Meta-analysis demonstrates that individuals with depression have elevated levels of inflammatory biomarkers1, and longitudinal studies have shown that elevations in inflammatory biomarkers predict the onset of depressive symptoms2. In experimental paradigms, inducing an inflammatory response through interferon-alpha treatment3, typhoid vaccine4, and endotoxin5 elicits sickness behavior, a constellation of symptoms that overlap with depression3. However, a number of inconsistencies have also been noted. Inflammation is neither a necessary component nor a sufficient cause of depression, and there is notable variability in whether an inflammatory stimulus elicits depressive symptoms6. Some studies suggest that depressive symptoms predict inflammation or fail to find any association7.

Such inconsistencies may arise from the heterogeneous nature of depression, which is characterized by a constellation of cognitive, affective, and somatic symptoms. As recently articulated by the NIMH Research Domain Criteria initiative, focusing on core processes in depression may help clarify its associated biological underpinnings8. One such process is attentional bias, which plays a critical role in cognitive theories of depression. Selective attention towards and difficulty disengaging from negative, and especially sad, stimuli is theorized to reinforce negative mood and contribute to the development and maintenance of depression9. Indeed, individuals with depression or elevated depressive symptoms demonstrate biases towards negative emotional information10. These biases predict increases in depressive symptom severity and are evident in individuals at high-risk for depression9. Training individuals to reduce negative attentional bias alleviates depressive symptoms9, suggesting attentional bias is not merely a symptom of depression but serves to initiate and sustain this disorder.

To date, no studies have examined whether inflammation is associated with attentional bias towards negative emotional stimuli. The current report focuses on breast cancer survivors, a population in which the inflammation-depression link is of particular importance. Depression is elevated in cancer survivors and associated with increased mortality, poorer adherence to medical treatment regimens, and impaired quality of life11. Chronic inflammation (particularly CRP and IL-612) contributes to the initiation and progression of cancer, and cancer treatment may further increase inflammation13. Behavioral comorbidities that arise in cancer patients have been partly attributed to inflammatory activity and described as sickness behaviors14; however, inflammation has been inconsistently linked with general measures of depressive symptoms in cancer survivors11,15.

The current study tested the hypothesis that elevated inflammation would be associated with attentional bias towards sad faces in breast cancer survivors using a dot probe task. This task is commonly used in the literature on depression, and assesses the relative allocation of attention towards emotional versus neutral stimuli. Because inflammation has been linked to both alterations in affect5 and neurocognitive performance and complaints16–18, we conducted analyses controlling for current mood and simple attention to identify whether any association between inflammation and attentional bias was driven by alterations in mood or in attention. In exploratory analyses, we examined links between inflammation and attentional bias for other emotional faces (happy and angry).

2. Methods

2.1. Participants

Participants were breast cancer survivors from a longitudinal study of cognitive functioning after treatment for breast cancer at the University of California, Los Angeles (UCLA) which enrolled patients from May 2007-March 201119. Criteria eligibility included: English language proficient, age 21–65 years, newly diagnosed with Stage 0-IIIA breast cancer, within 3 months of primary treatment (surgery, radiation, and/or chemotherapy), and not yet on endocrine therapy, if prescribed. Participants were ineligible if they had prior cancer diagnosis, current or past neurologic disorder, current major affective disorder, substance abuse/dependence, active autoimmune disorder or other disease involving the immune system. Details on participant screening, recruitment, and enrollment are reported in Ganz et al. (2013b). After approval by the UCLA IRB and with informed consent, data were collected in person at UCLA at study entry, 6 months, and 1 year18,19. In March 2013-July 2014, participants were invited to complete a final in-person assessment, which occurred between 3–7 years after study entry. At each assessment, participants provided morning or early afternoon blood samples prior to undergoing neuropsychological testing and completing questionnaires.

The parent study enrolled 191 women; 103 came in for the final in-person assessment, and 91 provided blood samples for assessment of inflammatory biomarkers and completed a computerized task to assess attentional bias towards emotional stimuli. These 91 women did not differ significantly from the full sample in terms of race, marital status, income, age, depressive symptoms, cancer treatment or time since last treatment (all p’s > .05).

2.2. Procedures

At the final in-person assessment, participants completed a 5-minute dot probe computer task after providing blood samples and prior to undergoing neuropsychological testing.

2.3. Demographic and treatment-related variables

Demographic information was obtained from self-report. Treatment-related information was obtained from medical record abstraction.

2.4. Attentional bias

Attentional bias was assessed using a dot-probe task, which is widely used in clinical and non-clinical populations9,20. In this task, a dot is presented on either the right or left side of a computer screen, and participants indicate which side of the screen the dot is on as quickly and accurately as possible by pressing the “j” or “f” key. Prior to presentation of the dot, two faces are flashed side-by-side. Each pair of faces consists of an individual portraying one neutral and one emotional (i.e., sad, happy, angry) expression. A total of 30 different emotional faces (10 sad, 10 happy, 10 angry) were paired with 30 corresponding neutral faces. Faces were drawn from the NimStim set of facial expressions21 and presented in color; half were male, half were female and each face pair was presented four times to accommodate all combinations of emotional face location and dot location, yielding 120 trials.

Each trial began with presentation of a centrally-positioned fixation cross for 500ms, followed by pairs of faces for 1000ms. A single red dot (2cm diameter) was presented on either the right or left hand side of the screen until the participant made her choice. Attentional bias scores for each emotion were calculated by subtracting average response times for congruent dot probes (replaced emotional faces) from the average response times for incongruent dot probes (replaced neutral faces). A score of 0 indicates no attentional bias, positive values indicate greater attention towards an emotional versus neutral face, and negative values indicate greater attention towards a neutral versus emotional face10. In the current study, attentional bias scores more than four standard deviations from the mean were removed as outliers (.3% of data) as were response latencies below 200ms (.1% of data) and above 2000ms (.98% of data). The task was programmed using DirectRT. Stimuli were presented on an 11.6” screen; each photograph was 12cm × 10cm.

2.5. Inflammation

Inflammation was assessed by measuring circulating levels of the pro-inflammatory cytokine IL-6 and the systemic inflammatory marker CRP1,12,13. Blood samples were collected by venipuncture into EDTA tubes, placed on ice, centrifuged for acquisition of plasma, and stored at 80°C for batch testing. CRP levels were determined by a high-sensitivity ELISA (Immundiagnostik; ALPCO Immunoassays, Salem, NH) per the manufacturer’s protocol but with an extended standard curve to a lower limit of detection of 0.2 mg/L. IL-6 levels were determined by high sensitivity ELISA (lower limit 0.2 pg/ml) (R&D Systems, Minneapolis, MN) per the manufacturer’s protocols. Samples were assayed in duplicate. Intra- and inter-assay precision of all tests was less than or equal to 10%.

2.6. Visual Attention

The Trail Making Test-A is a widely used, standardized measure of simple visual attention and psychomotor speed, used in several studies of breast cancer survivors and among the recommended tests in the cancer survivorship research community18,21. Participants are instructed to draw lines as quickly as possible sequentially connecting arrayed numbered items 1–25. Completion times were transformed into T-scores based on published age and education stratified normative data. The TMT-A was used to control for the influence of basic attentional function on the relationship between inflammation and attentional bias.

2.7. Questionnaires

Depressive symptoms were assessed with the Beck Depression Inventory-II23, a 21-item measure that assesses severity of depressive symptoms over the past 2 weeks. The BDI-II was used to control for the influence of current emotional state on the relationship between inflammation and bias.

2.8. Data Analysis

Multiple regression analyses were used to examine associations between CRP, IL-6, and attentional bias. Covariates included chemotherapy, radiation, use of anti-depressant/anti-inflammatory medications (yes/no), time since last treatment, age, and BMI, which may influence inflammation and/or attentional bias6,13,16. CRP and IL-6 were log-transformed prior to all analyses. Analyses were performed in Stata 13.1 (StataCorp, College Station, TX). Statistical significance was set at p < .05.

3. Results

Participants were on average 57 years old (SD=7.85; range=36 to 69 years) and 4.8 years post-diagnosis (SD=.67; range 3.6–6.8 years). Most of the women had Stage I (n=44; 48%) and II (n=27; 30%) breast cancer. Fifty women (55%) had received chemotherapy and 67(74%) had received radiation treatment; 16(18%) were on anti-inflammatory and 19(21%) were on antidepressant medications. CRP levels ranged from .2 to 11.9 mg/L (M=2.43, SD=2.72), and IL-6 levels ranged from .3 to 5.1 pg/L (M=1.25, SD=.92); both markers were low relative to population norms24,25. Average scores for depressive symptoms were low on the BDI-II (M=7.7, SD=7.03) with 79% in the minimal range, 13% in the mild range, and 8% in the moderate range. Compared to published normative data, nearly all participants performed within normal limits or better on TMT-A; only one participant’s performance fell in the impaired range. Response time on the dot probe task was comparable to that of individuals without cancer26. CRP was associated with depressive symptoms, (p=.03), but IL-6 was not (p=.15) (see Table 1).

Table 1.

Correlations for Study Variables

1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13.
1. Sad Bias
2. Happy Bias −.157
3. Angry Bias .097 −.132
4. CRP .224* −.152 −.064
5. IL6 .117 −.073 .011 .548***
6. BDI-II .047 −.077 .040 .227* .151
7. TMT-A .060 .072 .091 .016 −.056 −.091
8. Chemotherapy .068 −.065 .082 −.031 .032 −.003 −.018
9. Radiation −.039 −.169 −.047 .028 .049 −.034 −.061 .112
10. Time since last treatment .167 −.143 .006 .054 −.014 .158 .103 −.171 −.120
11. Age −.062 −.117 −.068 .009 .148 .042 −.297** −.266* .130 −.013
12. BMI .132 −.081 −.138 .516*** .482*** .172 .094 −.006 .043 .024 .093
13. Anti-inflammatory −.100 .085 −.263* −.035 −.034 −.126 −.085 −.042 .083 −.058 .154 .070
14. Anti-depressant .062 .129 −.112 .207 .184 .146 −.054 .091 −.058 .088 .166 .235* .111
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Note. CRP=C-reactive protein; IL-6=Interleukin-6; BDI-II=Beck Depression Inventory-II; TMT-A = Trail Making Test-A.

*

p<.05,

**

p<.01,

***

p<.001.

3.1. Inflammation and Attentional Bias

As hypothesized, circulating concentrations of CRP were positively correlated with sad attentional bias (p=.03), such that higher levels of CRP were associated with greater attention towards sad faces. This association remained significant in analyses that additionally controlled for demographic and treatment-related covariates, b=6.92, t(85)=2.11, p=.04, for depressive symptoms and TMT-A, b=7.1, t(83)=2.08, p=.04, and for medications, b=6.81, t(82)=1.99, p=.05, but not for BMI, b=6.31, t(81)=1.59, p=.12.

Exploratory analyses suggested that CRP was also associated with attentional bias away from happy faces, though this effect was not significant (p=.13). Controlling for demographic, treatment-related and medication covariates yielded a significant association between CRP and attentional bias away from happy faces, b=-5.69, t(82)=-2.02, p=.046, but this association was not significant when additionally controlling for depressive symptoms and TMT-A, b=-5.56, t(80)=-1.89, p=.062, or BMI, b=-5.35, t(81)=-1.79, p=.077. We found no association between CRP and angry bias, and IL-6 did not predict attentional bias in any model. Of note, no covariates, including BMI, depressive symptoms, and TMT-A, predicted attentional bias in any of the regression models.

4. Discussion

This study examined whether inflammation was associated with negative attentional bias, a fundamental psychological process that underlies depressive symptomology, in a sample of women with a history of breast cancer (approximately 5 years post-diagnosis). As hypothesized, CRP was positively associated with sad attentional bias, indicating that women with higher CRP also attended more to sad than neutral faces. This association was not evident with IL-6, but as a downstream marker of inflammation27, CRP may be a more stable indicator of chronic inflammation than IL-6.

Exploratory analyses revealed a trend for women with higher CRP to attend less to happy than neutral faces. This is consistent with the finding for sad faces, as avoidance of positive stimuli is also a feature of depressive symptomatology28. While there was no association between inflammation and angry faces, the stimuli in our study were presented for 1000ms, a relatively long exposure time that likely captures processes central to depression (like difficulty disengaging from negative stimuli or avoidance of positive stimuli28) rather than processes central to anxiety (like initial orientation towards threatening stimuli)9.

Sad attentional bias remained significant when controlling for current depressive symptoms, suggesting that the effects may be independent of state dysphoria. This is consistent with past research showing that attentional bias is not only a symptom of depression, but may also represent a more general tendency that increases risk for depression9. The association between CRP and sad bias also remained when controlling for basic attentional functioning, suggesting that it is the emotional component of sad attentional bias that is related to inflammatory processes. Of note, while this association was rendered marginal when BMI was accounted for, BMI itself was not related to sad attentional bias. This suggests that BMI may contribute to post-treatment inflammation, which then influences attentional bias.

Overall, these results identify attentional bias as a novel pathway through which inflammation may influence depression. This finding is directly relevant for breast cancer survivors, who are at elevated risk for depression and may be particularly sensitive to neural effects of inflammation29, and may also be evident outside of the cancer context. Indeed, our results are consistent with research showing that inflammation heightens the salience of negative emotional stimuli in healthy participants. For example, in comparison to placebo control, participants administered endotoxin demonstrate greater amygdala activation in response to negative feedback30 and fearful, but not happy, faces31. Following typhoid vaccine, healthy participants exhibit decrements in mood that are associated with greater reactivity to emotional faces (sad, angry, happy) in the subgenual anterior cingulate, an area associated with depression4. Additional work is needed to interrogate the relationship between inflammation and attentional bias in healthy participants, and in individuals at risk for depression due to medical conditions such as cancer or other risk factors.

This study is limited by its cross-sectional design. While our conceptual framework suggests inflammation contributes to sad attentional bias, it is also possible that greater negative attentional bias fosters higher levels of negative mood and stress, which in turn promotes systemic inflammation. The causal direction of this association should be addressed in experimental studies, which may benefit from inclusion of measures of attentional bias. Advancing our understanding of basic processes that contribute to the onset or maintenance of depressive symptoms has the potential to inform detection of vulnerable individuals and development of targeted treatment and prevention.

Acknowledgments

This research was supported by funding from the National Cancer Institute R01 CA 109650 and the Breast Cancer Research Foundation (to PAG) and the NIH/NIMH Predoctoral Fellowship 5T32MH015750-35 (CCB)

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