Research ArticleClinical Studies
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Brief Pain Inventory (BPI) Pain Survey Versus Cysteine Protease Caspase-1 (Casp1) Blood Levels Following Midline Laparotomy: A Prospective Randomized Study of Patients With Benign Disease and Patients With Cancer

MAARET ESKELINEN, TUOMAS SELANDER, IINA SAIMANEN, JUKKA PULKKINEN, ESA HÄMÄLÄINEN and MATTI ESKELINEN
Anticancer Research August 2024, 44 (8) 3463-3471; DOI: https://doi.org/10.21873/anticanres.17166

Abstract

Background/Aim: There is lack of studies assessing the correlation between pain scales and acute phase immune response (APR) following surgery. The purpose of this work was to assess the correlation between cysteine protease caspase-1 (Casp1) blood levels and two pain scales in a cohort of 56 midline laparotomy (MLa) patients and to assess their link with other cytokines (CYTs). Patients and Methods: Blood levels of Casp1 and other CYTs (IL-18, IL-18BP, IL-1ra, IL-6, IL-8, IL-10, IL-1β) were measured before operation and following surgery in patients with MLa. Pain levels were assessed using the Numerical Rating Scale (NRS) and Brief Pain Inventory (BPI) scale, both preoperatively and postoperatively. Results: Casp1 blood levels showed an increasing trend at postoperative day 1 (POP1) and this increase was almost significant in a linear mixed effect model (LME) analysis (p=0.06). Additionally, Casp1 blood levels were higher in patients with cancer than those with benign disease and correlated with IL-18 blood levels (r=0.24, p=0.007). Furthermore, Casp1 blood levels correlated with BPIsev (severity) score values in MLa patients (r=−0.49, p=0.048). A significant correlation was also observed between Casp1 blood levels and NRS scores in patients with MLa. Conclusion: This is the first report to evaluate two pain surveys (NRS and BPI) in MLa patients in relation to blood levels of Casp1 and eight CYTs. This analysis is important in confirming the significant correlation between NRS and BPI pain scales and Casp1 blood levels. Our study is also the first to demonstrate that adequate postoperative analgesia in patients with MLa provides better functional ability and improved patient satisfaction.

Key Words:

The lack of measures has delayed the progress in the management of pain in patients following surgery. In the absence of objective measures, the doctors must depend on the patient to supply key information on the quality and severity of the pain. The patient’s self-report or patient-reported outcome measure (PROM) is the most accurate and reliable evidence of the intensity of pain, and this holds true for patients of all ages, regardless of communication or cognitive deficits (1-7). However, physicians commonly question the reported severity and rely on their own estimates or use rating scales of pain; the Numerical Rating Scale (NRS), the Visual Analogue Scale (VAS), and the Verbal Rating Scale (VRS) (8-11). The NRS, VAS and VRS give reliable results of pain intensity, however, they are insufficient to consider patients functional capacity versus pain (8-11). Because pain is strongly linked to reduced function, interventions should relieve pain and improve function and patient quality of life (QoL). The Brief Pain Inventory (BPI) is a PROM tool for capturing both the intensity of a patient’s pain as well as the amount of interference in daily life caused by pain (12-27). Kuosmanen et al. (17) investigated the rectus sheath block (RSB) analgesia following midline laparotomy (MLa) in patients with benign disease (BE) and cancer (CA). The BPI survey was conducted preoperatively and postoperatively. The patients in the repeated-dose (ReD) RSB analgesia group had lower BPI severity (BPIsev) score and BPI interference (BPIint) score values postoperatively compared to the three other groups separately. Also, the time effect in a linear mixed effect (LME) model in BPIint score values was statistically significant, which means that in the ReD group preoperative BPIsev and BPIint score values were significantly higher than the BPI values following surgery. Authors concluded that adequate analgesia (AnGe) yields better functional ability and better patient satisfaction following MLa. Since the grade of pain, satisfaction to surgery (SFS) and the effect of AnGe differ among patients, it has been suggested that acute phase immune response (APR) would influence pain scores (28-37). However, there is lack of studies assessing the role of pain scales in APR. The purpose of this work was to investigate a cysteine protease Casp1 blood levels in a cohort of 56 MLa patients and to assess their link with other cytokines (CYTs) and BPI and NRS pain scales.

Patients and Methods

The study was approved by the Local Ethical Board of Eastern Finland Hospital Area, Kuopio, Finland (DNRO 120/2011, November 11, 2011), registered in the EudraCT database (EudraCT number 2011-005136-25) and in the ClinicalTrials.gov database (ClinicalTrials.gov Identifier: NCT02869841). Detailed description of the protocol is shown in reports by Purdy et al. (28, 29) and in Figure 1.

Figure 1.
Figure 1.

Study flowchart.

Sample collection and methods. The blood samples were obtained before surgery (PRE), immediately after surgery (postoperative sample one; POP1) and 24 h post-operatively (POP2), and centrifuged at 1,000 × g (2,900 rpm) for 15 min. The Casp1 assay was performed using ELISA kit obtained from Thermo Fisher Scientific (Carlsbad, CA, USA). The manufacturer’s intra-assay and the inter-assay coefficient of variations (CVs) for Casp1 were <10% and 12%, respectively. The CYTs assays were performed using specific enzyme-linked immune absorbent assay (ELISA) methods from R&D Systems (Minneapolis, MN, USA). The lower limit (LL) of the detection and LL of the quantification for the blood high-sensitivity C-reactive protein (hs-CRP) were 0.15 mg/l and 0.30 mg/l, respectively. The intra-assay and the inter-assay CVs for hs-CRP were <1.6% and 2.1-8.6%, respectively. The hs-CRP and CYT assays were detailed in previous reports by Purdy et al. (28, 29).

Interpretation of pain and satisfaction scoring. The scoring of pain and satisfaction in MidLa patients is performed as follows: The satisfaction of the patients at 24 h following MidLa (SFS24; 0=fully unsatisfied; 10=fully satisfied), were filed on a 11-point NRS. The overall pain at rest (NRSr) and the pain under 2 kg pressure to the wound area (NRSp) were filed on an 11-point NRS (0=no pain; 10=most pain). The BPI survey contains eleven main domains (general activity, mood, walking, standing, sitting, clothing, lifting, work, relations with others, sleep, enjoyment of life) including four questions related to pain severity (BPIsev) and seven questions related to pain interference (BPIint) and each BPI item yields a score of zero and ten and the test with eleven variables ranges from zero and 110. Detailed description of the BPI scoring is shown in the report by Kuosmanen et al. (17).

Statistical analysis. Baseline demographic characteristics are presented in Table I as means with standard deviations or with frequencies. The baseline group comparisons were executed using independent samples t-test and chi-square test or Fishers exact test. The blood levels of Casp1 and CYTs in Table II and Table III are shown as median levels with interquartile ranges as distributions were right-skewed. Group differences were tested using the Mann–Whitney U-test, while alterations between time points were tested using the Wilcoxon signed rank test. A linear mixed effect model (LME) was employed to test group differences at various time points and to examine the overall group-by-time effect. In the LME analysis the hs-CRP and CYT levels were log transformed. Pearson’s method was used to test for correlation between Casp1 concentrations versus CYT and NRS and BPI values. Data were analyzed using the IBM SPSS statistical software (IBM SPSS Statistics for Windows, version 26.0, IBM Corporation, Armonk, NY, USA).

View this table:
Table I.

The clinical data of the four study groups.

Results

NRS and BPI in different study groups. Preoperatively, 56 patients were randomized into the MLa study. However, according to the study protocol, blood sampling for the PRE, POP1, and POP2 time points was completed for 44 (Figure 1). The final study cohort of 44 patients included 15 BE patients, and 29 CA patients (Table I). Table I shows patient pain and satisfaction, assessed using the NRS pain scale, as well as BPIint and BPIsev pain scores between the study groups. No statistically significant differences were detected in the NRS, BPIint, and BPIsev values between the control group and the three RSB analgesia groups preoperatively and post-surgery (Table I). However, in MLa patients, the RSB analgesia improved clearly the SFS24 levels as follows; control group, single dose (SiD) group, repeated dose (ReD) group, and continuous dose (CoD) group (8; 9; 9.5 and 10, respectively, p=0.001, Table I).

Correlation between Casp1 and hs-CRP as well as other CYTs. MLa patients in the control group and CoD group had higher Casp1 blood levels preoperatively compared to those in the SiD and ReD groups (median Casp1; 3.02 and 1.95 versus 0.41 and 0.85, respectively, Table II). In addition, the MLa patients in the ReD and CoD groups had a trend for higher Casp1 blood levels postoperatively compared to patients in the control and SiD groups (POP1 elevation of Casp1; 0.93 and 0.0 versus 2.11 and 1.40, respectively, Table II). However, there were no significant differences regarding other CYTs and hs-CRP blood levels between the control group and SiD, ReD, and CoD groups (Table II). The POP alteration of CYT and hs-CRP blood levels are shown in Table III. In all MLa patients, Casp1 blood levels had a trend for increase at POP1 and this increase was almost significant in the LME analysis (p=0.06, Table III). In contrast, IL-18 and IL-18BP blood levels decreased at POP1 and the POP drop between the PRE and the POP1 levels in the IL-18 and IL-18BP levels was clearly significantly different (p<0.001). However, IL-18 and IL-18BP blood levels increased at POP2 with a significant time effect in the LME model (p<0.001). The PRE, POP1, and POP2 Casp1 blood levels were higher in patients with CA versus patients with BE disease (1.02/2.81/2.39 versus 0.41/0.41/0.41, Table IV). The Casp1 levels were correlated significantly with IL-18 blood levels in MLa patients (r=0.24, p=0.007) (Figure 2).

View this table:
Table II.

The median (interquartile range) hs-CRP and cytokine concentrations are shown before (PRE), immediately after (postoperative sample one, POP1) and 24 hours after (POP2) surgery.

View this table:
Table III.

The median (interquartile range) hs-CRP and cytokine levels before (PRE), immediately (postoperative sample one, POP1), and 24 hours post-surgery (POP2) in all study patients.

View this table:
Table IV.

The median (interquartile range) hsCRP and cytokine levels before (PRE), immediately (postoperative sample one, POP1) and 24 hours post-surgery (POP2) in patients with benign diseases (N=15) and in those with cancer (n=29).

Figure 2.
Figure 2.

Scatter plot of caspase 1 blood levels versus IL-18 blood levels (r=0.24, p=0.007).

Correlation between Casp1 and BPI as well as NRS. A significant correlation was observed between Casp1 blood levels (POP2) versus BPIsev (at one year) values in this study cohort (r=−0.49, p=0.048) (Figure 3). However, there were no significant differences between POP1/Casp1 and POP3/Casp1 blood levels and BPIsev values (r=−0.43, p=0.077 and r=−0.3, p=0.228), respectively. A significant correlation was observed between PRE/Casp1 and PRE+POP1+POP2/Casp1 blood levels versus NRSp scores in MLa patients (r=−0.43, p=0.013 and r=−0.33, p=0.01). Moreover, there were no differences in Casp1 blood levels compared to SFS24, NRSr and BPIint scores in MidLa patients.

Figure 3.
Figure 3.

Scatter plot of caspase1 blood levels immediately after surgery versus brief pain inventory severity score levels one year postoperatively (r=−0.49, p=0.048).

Discussion

The pain management links with QoL issues, such as anxiety, depression, and other psychiatric symptoms (37-44) and the clinician must depend on the patient to supply key information of the pain. In the absence of objective measures, PROMs are the most accurate and reliable measures of pain and its intensity, and this holds true for patients of all ages, regardless of communication or cognitive deficits (1-7). The PROMs can be divided in two groups: i) unidimensional (UniD) and ii) multidimensional (MultiD) pain intensity scales. The UniD group includes the NRS, VAS and VRS scales, which give reliable results of pain intensity, but are insufficient to consider patient functional capacity versus pain. Recognizing that impairment of function is central to comprehensive pain assessment, the BPI was designed to measure two parameters; the subjective intensity of pain and the impairment caused by pain. The BPI scale, which belong to the MultiD group of PROMs has been validated and tested globally, is sensitive to alterations in pain and straightforward and most patients are able to complete the BPI questionnaire (12-27). Therefore, the BPI is an easy measure of pain intensity and the extent to which pain interferes with patient life. Using BPI, patients rate their worst, least, average, and current pain intensity and also consider the degree to which pain interferes with domains of functioning; general activity, mood, walking ability, normal work, relations with other persons, sleep, and enjoyment of life on a scale of 0 to 10. Since the grade of pain, SFS and the effect of AnGe differs among patients, it has been suggested that APR would influence pain scores (8-11). This hypothesis relies on the suggestion that the APR could activate the opioid receptors (OpRes). Therefore, the biomarkers of opioid treatment have been assessed to document the potency of AnGe (45-47).

Mystakidou et al. (17) translated and validated BPI in 220 patients with cancer in Areteion hospital in Athens, Greece. The cancer patients completed the Greek BPI (G-BPI) questionnaires, and the pain management index (PMI) was also calculated to document the adequacy of pain treatment. Authors concluded that the assessment of pain severity using the G-BPI could enhance AnGe treatment of patients with cancer. In their study, 67% of patients with cancer (147/220) reported severe pain, and of these only 14% (21/147) received aggressive AnGe treatment with opioids and 22% (33/147) received ‘weak’ (no opioids) AnGe treatment. Although the patients with cancer in the Mystakidou et al. (17) study had quite high BPIsev score values only 14% of the patients had received opioid treatment. The authors suggested that this might be due to the Greek common sense judgment on the use of opioids as addictive drugs or as a result of doctors not informing their cancer patients in their study cohort on the necessity of the Ange treatment with opioids (17, 48).

Klepstad et al. (18) investigated Norwegian patients with cancer and their BPI showed adequate psychometric properties but was different from other published reports with regard to low compliance to complete the BPI survey. In total, 78% of their patients with cancer (235/300) were able to complete the BPI questionnaire and 35% (82/235) of the completed questionnaires had one or more missing items. The authors concluded that further research is needed to enhance compliance to answer BPI pain questionnaires and to establish routines for analysis of missing values in PROMs.

Kuosmanen et al. (17) investigated the RSB analgesia in MLa patients. The BPI survey for 56 MLa patients was conducted preoperatively and postoperatively. The patients in the ReD group had lower BPIsev and BPIint score values post-surgery compared to the three other groups. The LME model time effect analysis in BPIint score values was significant, which indicates that in the ReD group PRE BPIsev and BPIint score values were higher than these BPI values following surgery. The authors concluded that adequate analgesia provides better functional ability and better satisfaction in MLa patients. However, there is no data available of BPI and NRS pain scales versus APR in their study.

The BPI has originally developed for the assessment of cancer-related pain and later extended its use for the nonmalignant pain population. BPI has also been translated to many different languages and used throughout the world for pain assessment. Therefore, BPI provides an important and widely used diagnostic tool for treating patient pain (12-27). Tan et al. (19) assessed the BPI in 440 patients with chronic pain. This study is important, because the BPI was used primarily to assess patients with cancer-related pain and there are no previous studies on patients with benign disease-related pain. Authors concluded that BPI scale could be used also to assess pain in patients with benign disease and this provides an important tool for the doctors managing chronic pain.

Gjeilo et al. (20) validated and investigated BPI in cardiac surgery patients six months following surgery. Their study showed good reliability and validity of the BPIsev and BPIint scales. In addition, the study also demonstrated high responsiveness of the BPI scale in detecting change in pain over time. The number of missing items often is used to evaluate the reliability of a questionnaire and, at baseline, there were slightly more missing items among the questions in the BPIint (17% missing) than in the BPIsev (11% missing) scale.

The purpose of this work was to investigate Casp1 blood levels in a cohort of 56 MLa patients and to assess their link with the levels of other CYTs and BPI and NRS pain scores. The present results show that Casp1 blood levels correlated with BPI and NRS pain scores. However, there were no significant differences between the Casp1 blood levels and the SFS levels, the NRS pain scores at rest, the NRS pain scores when moving/coughing or the NRS pain scores at discharge.

Conclusion

Since the effect of AnGe differs among patients post-surgery, it has been suggested that APR would enhance pain and interact with pain scores (8-11). Recent studies report also that the pro-inflammatory CYT IL-18 could participate in the APR process and enhance pain (35-37). Also, the inhibition of IL-18 action by IL-18BP (binding protein) seems to be involved in the occurrence of pain (36-37). However, the blood levels of CYTs are rarely correlated with pain scales following MLa. Therefore, the primary target of this investigation was to assess the blood levels of eight CYTs and hs-CRP in a cohort of 56 MLa patients in correlation with NRS and BPI pain scales. This is the first report to evaluate two pain scales in MLa patients with comparison to blood levels of Casp1 and other CYTs. This analysis is important in confirming the significant correlation in two pain surveys (NRS and BPI) versus Casp1 blood levels indicating that APR and pain are correlated in MLa patients. Our study is also the first to demonstrate that sufficient postoperative analgesia in MLa patients provides better functional ability and better patient satisfaction.

Acknowledgements

The study was funded by the North Savo Regional Fund (Pohjois-Savon Maakuntarahasto).

Footnotes

  • Authors’ Contributions

    All Authors contributed to the collection and analysis of data, drafting and revising the manuscript, and read and approved the final article.

  • Conflicts of Interest

    The Authors have no conflicts of interest or financial ties to disclose in relation to this study.

  • Received June 10, 2024.
  • Revision received June 24, 2024.
  • Accepted June 25, 2024.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY-NC-ND) 4.0 international license (https://creativecommons.org/licenses/by-nc-nd/4.0).

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Brief Pain Inventory (BPI) Pain Survey Versus Cysteine Protease Caspase-1 (Casp1) Blood Levels Following Midline Laparotomy: A Prospective Randomized Study of Patients With Benign Disease and Patients With Cancer
MAARET ESKELINEN, TUOMAS SELANDER, IINA SAIMANEN, JUKKA PULKKINEN, ESA HÄMÄLÄINEN, MATTI ESKELINEN
Anticancer Research Aug 2024, 44 (8) 3463-3471; DOI: 10.21873/anticanres.17166
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