Abstract
Objectives
The aims of this study were to investigate modifications in pain sensitivity after RYGB and to explore associations between pain sensitivity and weight loss, chronic abdominal pain, total body pain, anxiety, depression, and pain catastrophizing.
Methods
In total, 163 patients with obesity were examined with a cold pressor test for pain sensitivity before and two years after RYGB. Two aspects of pain sensitivity were registered: Pain intensity (numeric rating scale, range 0–10) and pain tolerance (seconds). Associations between pain sensitivity and the explanatory variables were assessed with linear regression.
Results
Two years after RYGB the pain intensity increased (mean ± SD 0.64 ± 1.9 score units, p<0.001). Pain tolerance decreased (7.2 ± 32.4 s, p=0.005). A larger reduction in body mass index was associated with increased pain intensity, β=−0.090 (95 % CI −0.15 to −0.031, p=0.003), and decreased pain tolerance β=1.1 (95 % CI 0.95 to 2.2, p=0.03). Before surgery, participants with chronic abdominal pain reported 1.2 ± 0.5 higher pain intensity (p=0.02) and had 19.2 ± 9.3 s lower pain tolerance (p=0.04) than those without abdominal pain. No differences in pain sensitivity were observed between participants who did or did not develop chronic abdominal pain after RYGB. Pain sensitivity was associated with symptoms of anxiety but not with pain catastrophizing, depression or bodily pain.
Conclusions
The pain sensitivity increased after RYGB and was associated with larger weight loss and anxiety symptoms. Changes in pain sensitivity were not associated with development of chronic abdominal pain after RYGB in our study.
Introduction
A linear relationship between obesity and pain has been suggested [1, 2]. Obesity is a risk factor for development of varying chronic pain symptoms [3, 4], and weight loss may reduce pain [5].
Roux-en-Y gastric bypass (RYGB) is a widely applied weight loss surgical procedure [6] enabling substantial and sustained weight loss, with improvement of obesity-related comorbidities and quality of life [7], [8], [9]. However, high rates of chronic abdominal pain symptoms have been reported by us and others after RYGB, posing a negative effect on outcome [10], [11], [12]. The etiology and physiology of these symptoms of pain are in part obscure, but psychological factors may be involved [10, 13]. Anxiety, depression, and pain catastrophizing interact with symptom perception and are proposed mediators of chronic pain [14], [15], [16]. We have previously demonstrated associations between anxiety and depression and symptom perception after RYGB [14].
Increased pain sensitivity is a risk factor for chronic pain [17]. Conflicting findings, however, are reported regarding pain sensitivity in individuals with obesity [18].
By use of cold pressor tests pain intensity and tolerance to cold stimulus can be quantified [19]. To our knowledge, changes in pain sensitivity assessed by response to cold stimuli after RYGB have not been explored.
The primary aim of this study was to investigate modifications in pain sensitivity after RYGB and secondly to explore associations between cold tolerance test scores with weight loss, chronic abdominal pain, total body pain, anxiety, depression, and pain catastrophizing.
Methods
Study design and setting
This is a substudy of a prospective cohort study including patients scheduled for RYGB at the Department of Morbid Obesity and Bariatric Surgery, Oslo University Hospital, a tertiary referral centre for treatment of obesity. Participants were recruited from February 2014 to June 2015 and a two-year follow-up was completed in June 2017.
Surgical procedure and study visits
Laparoscopic RYGB was performed in all patients [20]. Mesenteric defects were closed. Study visits including study questionnaires, demographics, medical history, current medications and anthropometric evaluations and a cold pressor test were performed preoperatively and two years after RYGB. Changes in the prevalence of abdominal pain and symptoms have been reported previously [12].
Out of 271 participants eligible for study enrollment 236 consented to study participation; 15 declined the cold pressor tests and technical problems prevented a correct test in another 24 participants at baseline, therefore, 197/236 patients (85 %) patients were included at baseline. At two years 172/197 participants (87 %) attended the follow-up. Two declined the cold pressor test and technical problems prevented a correct test for five participants. Thus, 163/197 (83 %) patients were included at two years.
Measures
Cold pressor test
Pain sensitivity was evaluated by submerging the dominant hand and wrist in circulating cold water as long as possible up to a maximum of 120 s. Two aspects of pain sensitivity are presented: Pain intensity and pain tolerance.
We used a refrigerated water circulator, Julabo FP40HE (Julabo Labortechnik GmbH, Germany), with calibrated water temperature of 2.0 °C and a flow rate of 22 L/min. During the stimulus, the participants rated their pain intensity on a numeric rating scale (NRS) every 10th second.
Cold pressor tolerance (pain tolerance) was assessed as seconds endured with the hand submerged in cold water. To compare our data to the general population we recorded how many participants endured the hand submerged in cold water for 106 s or longer [21].
Cold pressure pain intensity (pain intensity) was estimated as an overall pain intensity using a numeric rating scale (NRS) score as follows:
For participants with tolerance time <120 s, the missing ratings after hand withdrawal were set to NRS=10.
Single missing ratings were set as the mean NRS value of the preceding and the next values.
A mean NRS score over all time points was computed, as an index of the average pain intensity over the full 120-s time period.
Two subjects did not report pain intensity and four had insufficient data (>50 % missing time point values). For these participants only the cold pressor tolerance is reported.
Study questionnaires
Study questionnaires were distributed at baseline and follow-up. Screening for chronic abdominal pain was performed using a questionnaire with the inlet question, “Do you experience long-term or recurrent abdominal pain, lasting for more than 3 months?” [11, 13]. Total body pain was assessed with Brief Pain Inventory Question 3 “please rate your pain by circling the one number that best describes your pain at its worst in the last 24 h” [22]. The quality of life related to bodily pain was assessed with SF-36®2 [23]. Musculoskeletal pain was self-reported and recorded in a predefined case report form. Negative affect was recorded by using the Hospital Anxiety and Depression Scale (HADS) [24] and pain catastrophizing (prior to the cold pressor test) by the Pain Catastrophizing Scale [25].
Statistics
Normally distributed continuous variables are presented as mean and standard deviation (±SD) other variables are presented as median (range). Categorical data are presented as proportions (percentage). Cohen’s d (effect size evaluation) was calculated as the difference between two means divided by the standard deviation of the difference. Suggested cut‐off values for Cohen’s d, used cautiously, were: small 0.2, medium 0.5 and large 0.8 [26]. Linear regression was applied to assess associations between the cold pressor test and relevant variables, results are presented as regression coefficients (β) with 95 % CI.
Ethics
The study was conducted in accordance with the Declaration of Helsinki and was approved by the Regional Committee for Medical and Health Research Ethics South East Norway; 2013/1263. Written informed consent was obtained from all participants.
Results
The study population consisted of 163 patients, 123 women (75 %). Mean ± SD age was 43.7 ± 9.7 years. At baseline mean body weight was 125.7 ± 54 kg and body mass index (BMI) was 43.0 ± 4.4 kg/m2. At two years the participants had lost mean 39.2 ± 14.6 kg, and BMI had decreased with 13.5 ± 4.9 kg/m2. The percentage total weight loss (%TWL) was 31.1 ± 10.1 %.
Before and after RYGB the mean pain intensity scores were 7.4 ± 2.2, and 8.0 ± 2.0, respectively. The mean change was 0.64 ± 1.9, p<0.001. The mean pain tolerance scores were 70.5 ± 40.0 and 63.3 ± 41.0 s, respectively. The mean change was −7.2 ± 32.4 s, p=0.005 (Figure 1). The effect size was 0.3 for changes in pain intensity and 0.18 for pain tolerance. Pain tolerance time >106 s was achieved by 56 (34 %) before and 48 (29 %) after RYGB. We did not observe any gender or age differences in response to the cold pressor tests (data not shown).
Changes in pain sensitivity in 163 patients before to two years after Roux-en-Y gastric bypass by cold pressor tests. The mean change in pain intensity was 0.64 ± 1.9, p<0.001 and the mean change in pain tolerance was – 7.2 ± 32.4 s, p=0.005. Cold pressor pain intensity is reported as mean ± SE on numerical rating scores (NRS) (0=no pain and 10=worst possible pain). Cold pressor tolerance is reported as median ± SE time (seconds) with dominant hand and wrist submerged in water with temperature 2.0 °C.
Pain sensitivity and weight loss
We observed an association between changes in BMI and changes in pain intensity and pain tolerance, β=−0.09 (95 % CI −0.15 to −0.03, p=0.003) and β=1.1 (95 % CI 0.95 to 2.2, p=0.03), respectively. A similar association was observed between %TWL and changes in pain intensity and pain tolerance, β=3.04 (95 % CI 0.19 to 5.89, p=0.037) and β=−49.8 (95 % CI −101.5 to 1.9, p=0.059), respectively. Participants who lost more weight had a larger increase in pain intensity and larger decrease in pain tolerance.
Pain sensitivity and bodily pain
The prevalence of musculoskeletal pain was 77 (47 %) at baseline and 75 (46 %) after RYGB, p=0.08. The scores for bodily pain were 3 (0–10) at baseline and 2 (0–10) after RYGB, p=0.12. The quality of life related to bodily pain improved from, a mean score of 61.3 ± 27.2 to 67.5 ± 27.5 at two years, p=0.01. There was no significant association between neither pain sensitivity nor quality of life with bodily pain. Participants reporting musculoskeletal pain had comparable pain sensitivity trajectories to the remaining participants, at baseline and at follow-up (data not shown).
Pain sensitivity and chronic abdominal pain
Chronic abdominal pain was reported by 21 (13 %) of the participants at baseline and 43 (26 %) at follow-up, p=0.001 (Figure 2). Before RYGB, participants with chronic abdominal pain reported a mean 1.2 ± 0.5 higher pain intensity scores and 19.2 ± 9.3 s lower pain tolerance compared to patients not having abdominal pain. At follow-up participants with chronic abdominal pain reported comparable pain sensitivity to participants without chronic abdominal pain (Table 1).
Chronic abdominal pain before and two years after Roux-en-Y gastric bypass (RYGB). Patients who have answered the question about chronic abdominal pain both at the baseline visit and at the two-year follow-up visit are included in the figure. Chronic abdominal pain was reported by 21 participants at baseline and 42 at follow-up, p=0.001.
Pain sensitivity to cold pressor induced stimuli in subjects with and without chronic abdominal pain before and two years after Roux-en-Y gastric bypass.
| Before surgery | Chronic abdominal pain (n=21) | Without chronic abdominal pain (n=140) | Mean difference | p-Value |
|---|---|---|---|---|
| Pain intensity (n=157) | 8.4 ± 1.1 | 7.2 ± 2.3 | 1.2 ± 0.5 | 0.02 |
| Pain tolerance (n=161) | 53.9 ± 30.3 | 73.2 ± 40.8 | −19.2 ± 9.3 | 0.04 |
| Two years after surgery | Chronic abdominal pain (n=43) | Without chronic abdominal pain (n=116) | Mean difference | p-Value |
|---|---|---|---|---|
| Pain intensity (n=159) | 8.3 ± 1.7 | 8.0 ± 2.0 | 0.22 ± 0.35 | 0.52 |
| Pain tolerance (n=159) | 59.6 ± 35.9 | 64.7 ± 41.3 | −5.1 ± 7.1 | 0.48 |
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Data are presented as mean ± SD. The difference between patients with and without chronic abdominal pain is evaluated with independent sample t-test.
Table 2 shows pain sensitivity before RYGB in patients who did not have chronic abdominal pain at baseline, stratified by whether the patient developed chronic abdominal pain after RYGB. Table 3 shows the change in pain sensitivity stratified by whether the patient developed chronic abdominal pain after RYGB.
Pain sensitivity to cold pressor induced stimuli before Roux-en-Y gastric bypass (RYGB) in participants who did or did not develop chronic abdominal pain after RYGB.
| New-onset chronic abdominal pain after RYGB (n=32) | Without chronic abdominal pain before and after RYGB (n=104) | Mean difference | p-Value | |
|---|---|---|---|---|
| Pain intensity before RYGB (n=157) | 7.7 ± 1.9 | 7.1 ± 2.4 | 0.55 ± 0.46 | 0.23 |
| Pain tolerance before RYGB (n=161) | 69.2 ± 40.4 | 74.9 ± 41.1 | −5.8 ± 8.3 | 0.49 |
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Data are presented as mean ± SD. The difference between patients with and without chronic abdominal pain is examined with independent sample t-test.
Change in pain sensitivity to cold pressor induced stimuli after Roux-en-Y gastric bypass (RYGB) in participants who did or did not develop chronic abdominal pain after RYGB.
| New-onset chronic abdominal pain after RYGB (n=32) | Without chronic abdominal pain before and after RYGB (n=104) | Mean difference | p-Value | |
|---|---|---|---|---|
| Change in pain intensity (n=157) | 0.48 ± 1.6 | 0.79 ± 0.0 | −0.32 ± 0.40 | 0.43 |
| Change in pain tolerance (n=161) | −6.9 ± 37.7 | −9.5 ± 32.8 | 2.6 ± 6.9 | 0.70 |
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Data are presented as mean ± SD. The difference between patients with and without chronic abdominal pain is examined with independent sample t-test.
Pain sensitivity and anxiety
After RYGB, the mean score for anxiety symptoms increased from 4.1 ± 2.9 at baseline to 4.7 ± 4.3, p=0.06. Before RYGB higher pain intensity and lower pain tolerance were associated with higher score for anxiety symptoms, β=0.14 (95 % CI 0.02 to 0.26, p=0.02) and β=−3.1 (95 % CI −5.1 to −1.0, p=0.004), respectively. Similarly, we observed a positive association between anxiety symptoms and pain intensity, β=0.08 (95 % CI 0.01 to 0.15, p=0.03) and tolerance β=−1.5 (95 % CI −3.0 to −0.06, p=0.04) after RYGB.
Pain sensitivity and depression
The sum score for depression symptoms decreased from 3.0 ± 3.2 at baseline to 2.0 ± 2.9 after RYGB, p<0.001. We did not observe any association between the degree of depression symptoms and pain sensitivity before or after RYGB (data not shown).
Pain sensitivity and pain catastrophizing
The sum score for pain catastrophizing score was 11.4 ± 8.5 before and 11.9 ± 10.3 after RYGB, p=0.54. There was no association between pain catastrophizing and pain sensitivity before or after RYGB (data not shown). In subgroup analyses of participants with new onset of chronic abdominal pain after RYGB, a positive association between pain catastrophizing and pain intensity β=0.046 (95 % CI 0.002 to 0.09, p=0.04) was observed. This association was unchanged after adjustment for depression symptoms βadj=0.056 (95 % CI 0.01 to 0.11, p=0.03), but no longer significant after adjustment for symptoms of anxiety. We did not observe an association between pain catastrophizing and pain intensity in subjects with and without abdominal pain before RYGB.
Discussion and conclusions
Sensitivity to cold induced pain increased two years after RYGB. As subjects with high sensitivity to pain respond poorly to treatment for chronic pain [27] our findings may be clinically relevant. Participants who lost more weight had a larger increase in pain sensitivity. The findings contradict others reporting unchanged and decreased pain sensitivity 6 to 12 months after bariatric surgery [28, 29]. Our study sample is larger than reported in the few previous studies and includes participants with and without chronic pain conditions. Methodological variations including evaluations of pain and duration of follow-up may contribute to the divergent findings across studies: The first year after RYGB rapid weight loss, improvements in physical health and mobility and increased social acceptance may induce a state of euphoria [30] that affects early pain sensitivity measurements.
Higher pain expectancies increase pain sensitivity [31]. Increased pain sensitivity could thus be linked to expectations from the cold pressor test at follow-up and the participant may therefore be more sensitive to the cold induced pain. On the other hand, pain catastrophizing mediates the influence of pain expectancies on pain sensitivity [31]. We did not evaluate pain expectancy, but pain catastrophizing did not change after RYGB. The increase in pain sensitivity may thus be explained by other mechanisms than pain expectancy.
Based on the effect size evaluations the changes in cold pressure tolerance (small effect size) and in cold pressure intensity (small to medium effect size) indicate that modifications of pain sensitivity may not be a major clinical contributor for development of chronic pain after RYGB.
Obesity, gender and pain sensitivity
Interestingly, 34 % of the participants reached cold pressor tolerance time of 106 s or more before and 29 % after RYGB contrasting a Norwegian population-based study including 10,486 adults, where 68 % of the participants reached cold pressor tolerance time of 106 s or more [21]. The reported mean cold pressor pain intensity of 6.3 ± 2.6 in the population-based study may also be lower than our measurements of 7.4 ± 2.2 before RYGB (21). If weight loss per se improved pain sensitivity to cold induced pain, we would have expected an improved pain tolerance after RYGB. However, we observed the opposite. Women are reported to have higher pain sensitivity [32] and higher rates of chronic pain conditions compared to men [33], [34], [35], [36], including chronic abdominal pain after RYGB [11]. We did not observe any gender difference in pain sensitivity in our study.
Pain sensitivity and abdominal pain
In line with others, we observed that participants with chronic abdominal pain before RYGB had higher pain sensitivity than participants without chronic abdominal pain [17, 21, 37]. Several groups report increased pain sensitivity in subjects with post-surgical pain [38, 39]. We found that participants with chronic abdominal pain after RYGB had comparable pain sensitivity to those without. Our findings are in line with findings from the population based Norwegian Tromsø study [33].
We have previously shown that chronic abdominal pain before RYGB is associated with chronic abdominal pain after RYGB [13]. In the present study 48 % of participants with chronic abdominal pain before RYGB did still report chronic abdominal pain two years after surgery.
Symptoms of anxiety, pain catastrophizing and pain sensitivity
Symptoms of anxiety may increase after RYGB [40]. We found an association between symptoms of anxiety and pain sensitivity. Pain catastrophizing remained unchanged after RYGB and was not associated with pain sensitivity. This contradicts findings across different musculoskeletal conditions where high catastrophizing is related to higher pain sensitivity [41]. We noted that for participants with new-onset chronic abdominal pain after RYGB there was an association between a larger degree of pain catastrophizing and higher pain sensitivity, which might be mediated through increased anxiety symptoms. We did not observe any association between depressive symptoms and pain sensitivity to cold induced pain before or after RYGB, contradicting other studies [42].
Strengths and limitations
The large cohort, longitudinal design, low attrition rates and comprehensive evaluations are strengths of the study. The single center design strengthens internal validity but may restrict the generalizability of our findings. The use of standardized pain sensitivity evaluations and validated questionnaires are other strengths. The effect size considerations may better place our findings in a clinical context. However, the lack of a control group is a limitation. The results should be considered as hypothesis generating. The restricted number of participants in subgroup analyses may impose a risk of statistical type II errors.
Conclusions
Pain sensitivity increased two years after RYGB and was associated with larger weight loss and symptoms of anxiety. The increase in pain sensitivity did not seem to be a significant contributor to the development of symptoms of chronic abdominal pain after RYGB.
Highlights
Pain sensitivity increased two years after Roux-en-Y gastric bypass.
Larger weight loss and symptoms of anxiety were associated with larger increase in pain sensitivity.
Changes in pain sensitivity were not associated with development of symptoms of chronic abdominal pain.
Acknowledgments
We deeply appreciate the support from MD Monica Chahal-Kummen, Marianne Sæter and Irene Ruud Johannessen at the Department of Endocrinology, Morbid Obesity and Preventive Medicine, Oslo University Hospital, for their assistance in patient recruitment and questionnaire retrieval. We thank MD, PhD Kristin Engebretsen for the help with patient follow-up.
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Research funding: The first author (IKBH) has received a PhD grant from South-Eastern Norway Regional Health authority, project number 2014073. The project has received a financial grant from the Norwegian Gastroenterology Association.
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Author contributions: All authors have accepted responsibility for the entire content of this manuscript and approved its submission.
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Competing interests: Authors state no conflict of interest.
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Informed consent: Informed consent has been obtained from all individuals included in this study.
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Ethical approval: All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
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