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Impact of Depression on Experimental Pain Perception: A Systematic Review of the Literature with Meta-Analysis

From the Department of Psychiatry (C.D.) and School of Nursing (L.M.), Manchester University, Manchester, United Kingdom; and Stepping Hill Hospital (S.D.), Stockport, United Kingdom.

Address reprint requests to: Chris Dickens, PhD, Department of Psychiatry, Rawnsley Building, Manchester Royal Infirmary, Oxford Road, Manchester M13 9WL, United Kingdom. Email: c.dickens{at}man.ac.uk

	ABSTRACT

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION ACKNOWLEDGMENTS REFERENCES

 
OBJECTIVE: This systematic review and meta-analysis was performed to examine the impact of depression on the perception of experimental pain stimuli.

METHODS: CD-ROM databases and bibliographies were searched to identify studies comparing the psychophysical responses to experimental pain stimuli of depressed subjects with that of healthy controls. Effect sizes (Cohen’s d) and probabilities were combined across studies; positive effect sizes indicated higher thresholds in depressed groups.

RESULTS: Six methodologically rigorous, independent studies were found comparing psychophysical responses to experimental pain stimuli in depressed subjects and healthy controls. Pain perception threshold was higher in depressed subjects (6 studies, d = 0.38, p = .001). This finding was not the result of publication bias. Absolute sensory perception threshold was much higher in depressed subjects (2 studies, d = 0.68, p = .002), though the findings for pain tolerance (2 studies) were too heterogeneous to enable us to combine results.

CONCLUSIONS: Depressed subjects are less likely to perceive a sensory stimulus as being painful compared with nondepressed controls. The influence of depression on attention to the pain stimulus may account for this effect. More studies are required to enable us to determine the impact of depression on absolute sensory perception threshold and pain tolerance. Furthermore, more studies would enable the examination of depression on the perception of different modalities.

Key Words: pain • depression • pain threshold • pain tolerance • meta-analysis • systematic review

	INTRODUCTION

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Considerable previous research has investigated the impact of depression on pain experience. Depression increases the risk of first-onset pain (1) and increases the risk of the development of chronic pain complaints over time (2–4). Among pain sufferers, depression is associated with greater pain intensity (5–11) and unpleasantness (12, 13), more bodily pain sites, and a higher degree of pain-related disability (7, 14). Overall, the weight of evidence seems to indicate that depressed subjects are more vulnerable to developing pain and, once pain has developed, have a broader spectrum of more negative experiences and outcomes.

Many theories have developed to explain why this might be so. Psychodynamic theories, where pain is a defense against unresolved emotional conflict, and pain-prone disorder, which suggests chronic pain in the absence of obvious cause is a variant of depression, lack empirical support (15). More recent biobehavioral models suggest that pain and depression may be associated through 1) certain individuals having trait susceptibility to dysphoric mood and dysphoric physical symptoms (including pain) and 2) depression being associated with maladaptive responses to pain (14).

Few studies have actually examined the effects of depression on pain perception. Early psychophysical experiments on depressed subjects indicated that pain perception thresholds were increased in depressed subjects, suggesting that depressed subjects were less sensitive to pain (16, 17). However, the use of poorly standardized methods of pain stimulation and the absence of healthy control subjects threaten the reliability of these findings. Later studies have used more highly standardized pain stimuli but have produced widely discrepant findings. Some studies indicate that depressed subjects have reduced pain perception thresholds and tolerances whereas others indicate that depressed subjects have higher pain perception thresholds and tolerances (18).

Methodological differences between studies are likely to account for variability in findings. A number of studies have examined the impact of low mood induced in otherwise healthy subjects (as opposed to naturally occurring depression) using psychological techniques (19–21). Other studies have examined subjects with naturally occurring depression but have failed to exclude subjects taking antidepressant medication or those experiencing clinical pain symptoms at the time of the experimental pain induction (22–25). Both of these characteristics are common in depressed patients and both are likely to influence responses to experimental pain in that group of subjects (23, 25–28). Speed of response to an experimental stimulus may be slowed in severely depressed patients, so psychophysical paradigms where time to response is important may influence the apparent pain perception thresholds in depressed subjects. Other differences between study methodologies such as stimulus modality (eg, heat, cold, pressure, electrical stimuli) and variations in mean age and sex mix are likely to contribute to variability in results in an unpredictable way. Consequently, distilling study findings into a coherent understanding of the effects of depression on pain experience is difficult.

To clarify the effects of depression on perception of experimental pain stimuli we have performed a systematic review of the literature with meta-analysis. Specifically this review aimed to answer the following questions:

1. Does depression increase or decrease pain perception threshold, absolute sensory threshold, or pain tolerance?
   
2. What are the magnitudes of these effects?
   

	METHODS

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Minimum Criteria for Study Inclusion
Studies were selected for this meta-analysis only if they included 1) a group of subjects with naturally occurring (ie, not induced) depression diagnosed using standardized criteria (by standardized interview or cutoff on a standardized questionnaire); 2) a healthy, nondepressed, control group; 3) all subjects were free from medication (particularly analgesics and antidepressants) at the time pain sensitivity was assessed; 4) at least 10 subjects in each of the depressed and nondepressed groups; 5) a standardized method to determine pain perception threshold (level at which stimuli are first perceived as painful), absolute sensory threshold (level at which stimulus is first perceived), or pain tolerance (minimum level at which pain is not tolerated) that enabled groups to be compared.

Identification of Relevant Papers
Electronic literature searches were performed on MEDLINE (1966 to present), EMBASE (1980 to present), and PsycINFO (1984 to present). Medical Subject Headings (MeSH) were used to identify all papers indexed as having content relevant to "Depression" and "Pain" (including "Pain measurement," "Pain threshold," and "Sensory thresholds"). The last search of the CD-ROM databases was performed on September 1, 2000. Reference lists from identified papers and from reviews in the area were searched by hand. Details of papers identified as relevant to this meta-analysis were used to search the Social Sciences Citations Index to identify subsequent papers that had referenced these useful papers. In addition, the authors of any paper identified as being useful to this meta-analysis were asked for details of any further studies of which they were aware (published or unpublished).

Data Extraction
Standardized data extraction sheets were designed and piloted for the purposes of this systematic review and meta-analysis. Relevant papers were first inspected and data were extracted by a single researcher (C.D. or S.D.). Means and standard deviations of the sensory perception thresholds, pain perception threshold, and tolerance scores for the depressed subjects and control groups were recorded using standardized data extraction sheets. Details of demographic characteristics, methods of assessing depression, and techniques used to determine sensory thresholds were recorded. Sensitivity of psychophysical techniques to speed of response was also recorded.

Reliability of data extraction was checked on a sub-sample of four study reports. Using the standardized data extraction sheets, another researcher (L.M.), blind to the data previously extracted, repeated the data extraction process on this subgroup of study reports. Accuracy of the data extraction procedure was determined by comparing data collected in the original extraction to that extracted by the blinded researcher and was found to be highly accurate, with complete concordance in 114 of 120 (95%) checked data points.

Meta-Analytic Techniques
Effect sizes (Cohen’s d) were generated for pain perception threshold, absolute sensory perception threshold, and pain tolerance from each study where adequate data were available, along with the 95% confidence intervals (29). For the purposes of this review, positive effect sizes indicate that sensory threshold was greater in the depressed group than in the control group, ie, that depressed subjects were less sensitive to experimental stimuli. Negative effect sizes indicate the opposite. In addition, effect sizes were classified according to the criteria of Cohen as small (d = 0.1), medium (d = 0.3), or large (d = 0.5) (30).

Tests of Homogeneity of Effects
The homogeneity of effects from individual studies was assessed by calculating the Q-statistic which was assumed to follow a ² distribution with k-1 degrees of freedom (where k = number of studies combined) (29).

Combination (Pooling) of Effect Sizes
Where appropriate, effect sizes for pain perception threshold from individual studies were pooled using the inverse variance method (29). This method of combining effect sizes calculates a weighted mean from individual studies, where the weight applied to each effect is the reciprocal of its squared standard errors. An overall test statistic (z) was calculated for the combined effect comparing depressed and nondepressed groups (29).

The Q-statistic can be used to estimate the between-study variance in a random effect analysis. In this study, the Q-statistic gave a negative estimate of the between-study variance. Inasmuch as, when this occurs, the fixed and random effect estimates are equal, the result of fixed effects methods only have been presented.

Assessing Publication Bias
The robustness of the meta-analyses to publication bias was determined constructing a funnel plot (sample size vs. effect size). In addition, to investigate statistically whether the magnitude of the effect was associated with the number of subjects studied, which may occur as the result of publication bias, a weighted regression analysis was performed using effect size as the dependent variable and sample size as the independent variable, weighting for the reciprocal of the pooled variance for each study (31).

The above calculations were performed using Microsoft Excel 97 (Microsoft Corporation, Redmond, WA) and StatsDirects version 1.9.14 (CamCode, Ashwell, UK).

	RESULTS

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In total, 84 studies were identified by electronic searches, hand searching of bibliographies, and contacting authors and were reviewed in detail. From these 84, studies were rejected for the following reasons: inadequate/no experimental data (N = 20); responses to experimental pain stimuli not assessed (N = 12); subject characteristics not meeting criteria (less than 10 subjects in subjects per group, not depressed by standardized criteria or no healthy controls) (N = 35); induced low mood (N = 4); and not medication free (N = 5).

Eight studies were found to meet the criteria for inclusion and contained sufficient data to be included in the meta-analysis. Among the eight study reports identified as useful to this meta-analysis, three reports presented data on the same or highly related subject (32–34). To avoid these highly related samples introducing too great an influence on the results of this meta-analysis, a single effect size generated from the first published report only (33) was used in the meta-analysis. Thus, six independent studies were identified by the systematic review and included in this meta-analysis.

Important methodological characteristics of the studies included in this review, along with effect sizes and 95% confidence intervals can be seen in Table 1.

In two of the six studies, psychophysical techniques were independent of time to response (18, 33) The remaining four studies had identified sensory threshold using techniques that were time dependent; two studies identified self-reported thresholds by timed exposure to a constant stimulus (35, 36), one study identified self-reported thresholds in response to a stimulus of gradually increasing intensity (37), and one study used both of these methods (38).

In three studies, reports confirm that subjects were free from physical complaints that might influence sensory responses, eg, peripheral neuropathies, upper limb trauma, etc. (18, 35). The remaining three studies make no report of the presence of absence of comorbid illness (36, 37, 39) and none of the six studies report whether depressed patients had any clinical pain not attributable to a diagnosed medical complaint.

Pain Perception Threshold
All six studies compared depressed and nondepressed subjects with regards to pain perception thresholds. Effect sizes ranged from very small (d = -0.01) to very large (d = 0.70). Five of the six studies showed a positive effect, indicating that depressed subjects had higher pain perception thresholds, ie, were less sensitive to experimental pain stimuli, than the healthy controls. The effect sizes for pain perception tolerance were not heterogeneous (Q = 3.02, df = 5, p = .70).

The effect sizes (and 95% confidence intervals) for pain perception thresholds along with the pooled effect are shown graphically in Fig 1. The pooled effect was moderate in magnitude (pooled Cohen’s d = 0.38) and highly significant [p (one-sided) = .001]. This indicated that depressed subjects had significantly higher pain perception thresholds than nondepressed, ie, were less sensitive to experimental pain stimuli.

View larger version (16K): [in this window] [in a new window]   Fig. 1. 95% CI = 95% confidence interval. Positive effects indicate that pain perception thresholds are greater in depressed subjects, ie, depressed subjects are less sensitive to experimental pain stimuli. Negative effects indicate that depressed subjects have lower pain perception thresholds. Each rectangle represents one of the studies included in the meta-analysis; the line in the center of the rectangle represents the effect size, the size of the central diamond represents the sample size, and the right and left extremes of the rectangles represent the 95% confidence intervals.

View larger version (12K): [in this window] [in a new window]   Fig. 2. *Weighted with the inverse of the variance for each study.

Pain Tolerance
A further two of the six studies examined pain tolerance in depressed and nondepressed subjects. The effects were highly heterogeneous, however [effect size (d) = -0.88 and d = 0.57; Q = 6.9; df = 1; p = .009] and therefore were not combined.

	DISCUSSION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION ACKNOWLEDGMENTS REFERENCES

 
Our main result indicates that depressed subjects had higher pain perception thresholds, (ie, reported onset of pain at greater stimulus intensities) in response to experimental pain stimuli, than nondepressed controls. The effect sizes of the studies reviewed were not heterogeneous and combined to give an effect which was moderate in magnitude and highly significant (d = 0.38, p = .001). There was no asymmetry in the funnel plot and no association between effect sizes and sizes of sample, which indicates that our finding was unlikely to have resulted from publication bias.

Only two studies had investigated the impact of depression on absolute sensory perception threshold, resulting in a very large, highly significant combined effect (d = 0.68, p = .002). This indicates that depressed subjects had higher sensory perception thresholds, ie, were less sensitive to stimuli overall compared with nondepressed subjects. The very small number of studies means that this result should be viewed with extreme caution as it is likely to be very sensitive to the methodological idiosyncrasies of the studies involved and the effects of publication bias.

The results of the two studies that had examined pain tolerance were very mixed and no conclusions can be drawn with regards to the influence of depression on pain tolerance.

This is the first review in this area that has been systematic in nature. Considerable efforts were spent identifying all studies containing data that were relevant to our aims. We imposed stringent methodological criteria to minimize the extent to which the results of the studies included were contaminated or obscured by, what we considered were, methodological shortcomings. Though these stringent criteria resulted in relatively few studies being included in the final meta-analysis, we believe that the combination of the studies with the most robust methodologies (by our criteria) increases the reliability of our finding that depressed subjects had higher pain perception thresholds. Regrettably, too few studies were identified to allow us to examine whether depression had different effects on pain stimuli of different modalities. Similarly, too few studies had examined the influence of depression on absolute sensory perception threshold and pain tolerance to enable any firm conclusions to be drawn with regards to these thresholds.

There are a number of methodological limitations in the studies included in this review that may have influenced the findings and thus merit discussion. First, four of the six studies used psychophysical techniques in which a delayed response to the sensory stimulus may have spuriously increased pain perception thresholds. Because slowing of psychomotor functioning is a feature of moderate to severe depression, this effect may have inflated our results. Inspection of the Forrest plot of effect sizes, however, shows clearly that those studies sensitive to reaction time did not have larger effect sizes than those which were insensitive to response time. It is thus highly unlikely that our results were significantly influenced by depressed subjects having slowed responses though this possibility should be considered when future studies are designed.

Second, there was, in general, inadequate reporting of the presence of comorbid physical illnesses in the subjects studied. Three studies excluded subjects with localized physical problems that might affect sensation, such as peripheral neuropathy, and three made no mention of such problems. Inasmuch as these local physical problems might result in reduced sensitivity (anesthesia) or increased sensitivity (hyperesthesia, allodynia) of the stimulus area, such problems might influence results. Once again examination of the Forrest plot does not show that those excluding local problems gave consistently different effect sizes from those that did not. More importantly, however, no studies commented on whether the depressed subjects were experiencing clinical pain (medically explained or otherwise). Such pain is commonly experienced in depressed subjects (over 50% in some studies) and some inquiries should have been made because comorbid pain might influence perception of experimental pain (40, 41). The nature of this potential influence is unclear, however. Though coexistent pain of defined physical origin could be expected to raise pain thresholds, it is not obvious whether medically unexplained (ie, somatized) pain would increase or decrease pain thresholds. Future studies should consider comorbid symptoms more thoroughly.

At first sight, our findings may seem counterintuitive. The large number of studies demonstrating positive correlations between pain and depression (5–11) would suggest that pain thresholds are reduced in depression. However, these latter studies have used subjects with chronic pain. Chronic pain results in reorganization of pain pathways so that both central and peripheral nociceptive processing is enhanced (42, 43). This process might be further enhanced by the presence of depressed mood (44). Furthermore, there are problems comparing studies using experimental pain stimuli with those using clinical pain (whether acute or chronic). Not only are the different contexts likely to influence how an individual perceives pain but also a number of secondary pathophysiological changes associated with the clinical pain, which may increase or decrease pain perception and which are less likely to be active in the experimental condition. Thus such extrapolation should be done only with caution.

Our findings are consistent with current models for the role of attention in pain processing. These state that pain competes for limited attentional resources with other environmental stimuli (45). The extent to which pain demands attention is partly related to its intensity. Thus the attentional impairment to environmental stimuli seen in depression (46) may be sufficient to reduce the perception of low intensity stimuli, such as those around absolute sensory perception or pain perception thresholds. By this reasoning we would expect depression to have a much smaller effect of perception of pain stimuli at or around maximum tolerance levels, though this could not be assessed in our review.

Our main finding, that depressed subjects have greater pain perception thresholds than nondepressed, did not occur as the result of publication bias. However, the number of studies was few and the tests used would be expected to have low power to detect publication bias under such circumstances. For this reason our results must be interpreted cautiously. More studies are required, controlling carefully for differences between groups apart from the presence of depression and excluding subjects with other comorbid problems that might influence pain responses. Consideration should be given to the use of psychophysical techniques that are not sensitive to speed of response, which will simplify the interpretation of results. Further studies are required using different stimulus modalities to determine whether depression has a similar effect on the perception of stimuli of all modalities.

	ACKNOWLEDGMENTS

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The authors thank the following authors who responded to requests for additional information on their studies: Georg Adler, Leslie Carter, Judi Ganchrow, Stephan Lautenbacher, Dan McNeil, and Glenn Pancyr. The authors also thank Dr. Chris Roberts, Senior Lecturer in the Department of Biostatistics, Manchester University for his advice on meta-analysis.

Received for publication November 14, 2001.

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