The effect of social exclusion on pain perception and heart rate variability in healthy controls and somatoform pain patients

Fabrice Kleber; Andreas Reif; Moritz de Greck

doi:10.1515/sjpain-2024-0042

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The effect of social exclusion on pain perception and heart rate variability in healthy controls and somatoform pain patients

Fabrice Kleber , Andreas Reif und Moritz de Greck

Veröffentlicht/Copyright: 4. Dezember 2024

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Aus der Zeitschrift Scandinavian Journal of Pain Band 24 Heft 1

Abstract

Objectives

The overlapping neural networks of social and physical pain have been investigated intensively in recent years. It was postulated that triggering social pain might result in greater physical pain. Nonetheless, how this affects somatoform pain disorder has not yet been considered. Since an increased pain processing activity is reported in these patients, the investigation of social exclusion and its effect on this group seems interesting. Hence, the aim of this study was to compare the influence of social exclusion on healthy controls and patients with somatoform pain disorder.

Methods

Nineteen patients with somatoform pain disorder and 19 healthy controls were examined. Cyberball, a virtual ball-tossing paradigm, was used to experimentally induce social exclusion and inclusion. To measure effects on pain perception, pressure pain thresholds and heart rate variability (HRV) were recorded after each round of cyberball. Demographic data, pain medication, and potential psychosocial moderators were collected by questionnaires.

Results

After social exclusion, pressure pain thresholds were significantly reduced in healthy controls (p < 0.01) as well as somatoform pain patients (p < 0.05), while HRV increased only in patients with somatoform pain disorder (p < 0.05) indicating increased parasympathetic activity.

Conclusion

This study is the first to analyse the effects of social exclusion on pain perception in somatoform pain disorder. While the reduction in pressure pain thresholds is in line with the social pain literature, the effects on HRV could be interpreted as a form of pain regulation mechanism. However, further research is needed to investigate the role of parasympathetic activity in socially excluded somatoform pain patients.

Keywords: pain; pain perception; somatoform disorders; pain disorder; social exclusion; pain threshold

1 Introduction

Pain is defined as an unpleasant sensory and emotional experience typically caused by actual or potential tissue injury; however, a broad influence of psychosocial factors in the development of pain is generally accepted [1]. Based on that, the idea of a distinction between two kinds of pain developed. On the one hand, physical pain is triggered by tissue damage and represents the common understanding of the word pain [2]. On the other hand, the threatening loss of close relationships or social devaluations can provoke something called social pain [3]. Over the last two decades, the examination of social pain was an area of increasing research interest [4]. The overlap theory of physical and social pain proposes the existence of shared neural regions responsible for the processing of physical and social pain [2,5]. Although shared pathways in the brain for emotional and pain processing are not specifically connected to the idea of social pain, many studies have investigated the physical–social pain overlap [4]. The most important evidence is provided by neuroimaging studies, which identified the dorsal anterior cingulate cortex (ACC) and the anterior insula as key areas for the physical–social pain overlap [6,7]. It should be noted, that the modern view of how the brain works is moving away from specific mind–brain aspects. Rather, the focus is placed on closely connected neuronal networks that cannot simply be broken down into segregated parts [8,9]. Nevertheless, it was postulated against the background of overlapping neural processing of physical and social pain, that external factors which change the current state of one pain form should influence the other pain form in the same direction [2]. Hence, triggering social pain might result in greater physical pain. There is convincing evidence for this assumption [10–13]. However, some studies found contradictory results [11,14–16]. Besides research within the general population, the effect of social exclusion on pain perception was examined in different clinical samples [12,13,17–19].

Interestingly, an analysis based on patients with somatoform pain disorder, to the best of our knowledge, has not yet been conducted. Prolonged and recurrent pain is characterizing for patients with somatoform pain disorder. In general, pain in this disorder is not sufficiently explained by physiological reasons, which does not mean that it must be purely psychological in nature. However, patients mostly exhibit serious psychosocial stress factors and a long medical history [20]. Neurophysiological aspects seem to play an important part in the development of somatoform pain disorders as well. The circuit network model of somatosensory describes enhanced neuronal pain processing activity in the ACC and the insular cortex [21]. This fact is particularly interesting because parts of the ACC and the insula play a key role in terms of the physical–social pain overlap [6]. Another noteworthy fact is that patients with somatoform pain disorder are frequently stigmatized and devaluated by their social environment [22,23]. For example, pain patients without sufficient physical explanation are more often socially excluded than pain patients with an adequately diagnosed organic cause [24].

In recent years, heart rate variability (HRV) has become a well-established, non-subjective parameter in pain research [25]. It describes natural alterations in the time interval between consecutive heartbeats. HRV is regarded as a precise assessment of autonomic input to the heart and can display activity in the sympathetic as well as the parasympathetic branch of the autonomic nervous system [26]. More interestingly, brain areas like the ACC, the insula, and others participate in autonomic control. Since these systems are as well related to pain perception, HRV can be considered as a valid indicator of autonomic reactivity to painful stimulation [25,27–29].

As mentioned above, there is no study examining the effect of social exclusion on pain perception in somatoform pain patients. Considering the described neuronal changes in the ACC and the insular cortex, however, a strong reciprocal interference of social and physical pain seems most likely, especially in somatoform pain patients. This is of clinical relevance regarding the described stigmatization and social exclusion of somatoform pain patients. Consequently, the purpose of this study was to fill this gap in the current state of research.

2 Methods

2.1 Participants

To estimate the required sample size, an a priori power analysis with G*Power Version 3.1 was conducted [30]. It was based on a significant effect of social exclusion on pain ratings in patients with borderline personality disorder of η partial 2 = 0.188 [12]. Under the assumption of an error probability of α = 0.05 and a power of (1 – β) = 0.80, a required sample size of 19 participants per group was estimated. Somatoform pain patients were recruited from the Department of Psychiatry, Psychosomatic Medicine and Psychotherapy of the University Hospital Frankfurt. All patients were diagnosed by an experienced physician according to ICD-10, fulfilling the criteria for the diagnostic groups F45.40 (persistent somatoform pain disorder) and F45.41 (chronic pain disorder with somatic and psychological factors) [31]. Exclusion criteria were severe psychiatric disorders (e.g., acute suicidal tendencies, bipolar disorder, and schizophrenia) as well as physical problems which may interfere with pain perception (e.g., neuropathy, acute injury of the upper extremities, and Raynaud’s phenomenon) [15,29]. Written informed consent was obtained from all subjects before the study. Ethical approval was obtained from the ethics committee of the Medical School, Goethe University Frankfurt (No. 20-842). All procedures complied with the latest version of the Declaration of Helsinki [32].

2.2 Cyberball paradigm

The latest version of the cyberball paradigm was used to induce social inclusion and exclusion [33,34]. Subjects were informed that they will play a virtual ball-tossing game with two other players on the internet to bridge the time between the pain measurements. The players could select by a simple mouse-click which player would receive the next throw. Actually, the fellow players were simulated, and the course of play was predetermined. Every round consisted of 80 tosses [35]. In the inclusion condition the test persons received a well-balanced number of throws, whereas in the exclusion condition they were excluded after the tenth caught ball. The duration of each round was approximately 5 min.

2.3 Pressure pain threshold

To measure the effects of social inclusion and exclusion on pain perception pressure pain thresholds were determined as described elsewhere [36,14,11]. Therefore, a force gage (FDN 100, Wagner Instruments, Greenwich, USA) was used. It was vertically positioned on the thenar as well as a tender point 2 cm distal of the epicondylus lateralis humeri of the subjects’ right hand. The pressure was increased in steps of 5 N per second. Before testing, participants were familiarized with the pressure pain stimuli and briefed to say immediately “now” when they felt pain for the first time. The pressure pain threshold was determined by computing the mean of the measurements.

2.4 HRV

In addition, an electrocardiogram (ECG) was derived to detect the non-subjective HRV. Therefore, BrainVision Recorder, Version 1.24 (Brain Products GmbH, Gilching, Germany) was used. To avoid disturbances of the ECG measurement, two electrodes were placed on both sides in the subclavian region and one electrode in the neck [37]. The ECG was recorded while subjects were playing cyberball.

2.5 Questionnaires

The Screening for Somatoform Disorders (SOMS-2) was used to evaluate physical symptoms which are not based on organic causes. It consists of 68 items and includes questions about pain as well as gastrointestinal, cardiovascular, urogenital, and neurological complaints. This questionnaire offers the possibility to compute the somatization index ICD-10 by which a somatoform disorder can be diagnosed [38].

To assess clinical pain the Brief Pain Inventory (BPI) was utilized. It is composed of 11 items that can be assigned to two different domains. The pain severity domain rates pain at its worst, least, average, and the current pain. The pain interference domain quantifies how much pain interferes with seven daily activities (e.g., work, mood, relationships) [39].

The Pain Sensitivity Questionnaire (PSQ) describes 17 daily situations (e.g., burning the tongue on a very hot drink), that need to be rated in terms of painfulness. The PSQ total score can be calculated as the average rating on 14 of the 17 items [40,41].

2.6 Procedure

We implemented a 2 (somatoform pain patients vs healthy controls) × 2 (social inclusion vs social exclusion) mixed-model design. The subjects were told that they were taking part in an experiment on pain perception and that they would play a virtual ball-tossing game with two other players on the internet to bridge the time between the pain measurements. Subjects were familiarized with the pressure pain stimuli and the ECG electrodes were attached. The testing itself started with online questionnaires on demographic data, possible pain medication, the BPI, and the PSQ. Afterward, an induction of social inclusion or social exclusion with the cyberball paradigm took place. Meanwhile, an ECG was recorded. Immediately after that, pressure pain thresholds were measured. Then subjects completed the SOMS-2. Thereafter, a second induction of social inclusion or social exclusion, as well as another ECG and a pressure pain measurement took place. All participants were confronted, respectively, with one round of social inclusion and exclusion, only the experimental order was counterbalanced (inclusion–exclusion or exclusion–inclusion). Finally, a manipulation check was conducted. Subjects rated whether they believed that they had played with a real person during the cyberball paradigm. All participants were informed thoroughly about the actual research objectives after the experiment.

2.7 Data analysis

The HR (average heart rate) and the time domain HRV indices RMSSD (root mean square differences of successive heartbeat intervals) and pNN50 (percentage of successive intervals that differ by >50 ms) were calculated [42,43]. To analyse the ECG data, BrainVision Analyzer, Version 2.2 (Brain Products GmbH, Gilching, Germany) and ARTiiFACT Version 2.13 was utilized [44]. Movement artefacts and ectopic beats were excluded from the data. The provided algorithms for R-peak detection in the QRS complex were used. The results were verified by hand and adjusted where necessary.

Statistical analyses were conducted using SPSS Statistics Version 29.0 for Windows (IBM Corporation, Armonk, USA). Dependent sample t-tests were performed to examine the influence of social exclusion on pressure pain thresholds and HRV. Mixed-model ANOVAs were used to check for potential interaction effects.

3 Results

3.1 Participants characteristics

To analyse the patient and the control group, we conducted between-subjects comparisons. The results are displayed in Table 1. In total, 38 subjects were recruited for this study. There was no significant difference between the control and patient group concerning age and sex. Most of the pain patients fulfilled the diagnostic criteria for F45.41 (94.7%, n = 18) and only 5.3% (n = 1) were diagnosed with F45.40. Because of that, both diagnoses were combined and no subgroup analyses were conducted. In the patient group a wide variety of pain medications like non-opioid analgesics (89.5%, n = 17), opioids (15.8%, n = 3), psychotropic drugs (47.4%, n = 9), and antiepileptic drugs (26.3%, n = 5) were taken, while in healthy controls only non-opioid analgesics as on-demand medication were used (26.3%, n = 5). In somatoform pain patients there were significantly higher levels of somatoform symptoms measured by the somatization index ICD-10 of the SOMS-2. Regarding the specific painful body areas, most pain patients named joints (84.2%, n = 16), head/face (78.9%, n = 15), arms/legs (78.9%, n = 15), and the back (73.7%, n = 14). In the control group considerably fewer participants complained about pain in these body parts (joints: 21.1%, n = 4; head/face: 26.3%, n = 5; arms/legs: 10.5%, n = 2; back: 31.6%, n = 6). Somatoform pain patients also reported significantly higher pain severity and pain interference with daily activities measured by the BPI (e.g., work, mood, relationships), as well as greater pain sensitivity determined by the PSQ.

Table 1

Participant characteristics

	Healthy controls (n = 19)		Somatoform pain patients (n = 19)
	M	SD	M	SD	t	p
Age	40.21	17.17	44.84	11.43	0.98	0.33
SOMS-2 somatization index	1.42	1.43	6.84	3.44	6.50	<0.001**
BPI pain severity	0.78	0.94	4.89	2.45	6.83	<0.001**
BPI pain interference	0.32	0.59	5.57	2.45	9.08	<0.001**
PSQ total	3.56	1.49	5.61	2.77	2.84	0.007**
	Male	Female	Male	Female	χ²	p
Sex	5	14	2	17	1.58	0.21

Significant results are displayed in bold and marked as follows: **p < 0.01 (two-tailed).

3.2 Effects on pain and HRV

To investigate the influence of social exclusion on pain measurements and HRV, we carried out within-subjects comparisons. The results are presented in Table 2. In contrast to the inclusion condition, pressure pain thresholds were significantly lower after social exclusion in both healthy controls (t(18) = 3.40, p = 0.003) and somatoform pain patients (t(18) = 2.88, p = 0.010). However, mixed-model ANOVAs showed no substantial interaction between type of subject and the cyberball condition (F(1) = 0.03, p = 0.870; Figure 1), which means that the influence of social exclusion was not greater in somatoform pain patients than in healthy controls. With regard to HRV, RMSSD as a measure of the parasympathetic tone (t(18) = −2.54, p = 0.021; Figure 2) and pNN50 (t(18) = −2.97, p = 0.008; Figure 3) increased significantly in somatoform pain patients after social exclusion, while no effect was found in healthy controls. There was no effect of cyberball on the average heart rate in both groups. No moderating influence of pain medication, pain sensitivity (PSQ), pain severity and interference (BPI), or somatization tendency (SOMS-2) on the effect of social exclusion on pain perception was found.

Table 2

Effects of social inclusion and exclusion on healthy controls and somatoform pain patients

	Healthy controls (n = 19)						Somatoform pain patients (n = 19)
	Inclusion		Exclusion				Inclusion		Exclusion
	M	SD	M	SD	t(18)	p	M	SD	M	SD	t(18)	P
Pressure pain threshold (N)	33.42	10.28	29.08	10.20	3.40	0.003**	27.56	16.94	22.87	15.55	2.88	0.010*
Heart rate (bpm)	76.34	9.05	75.94	8.61	0.68	0.504	81.51	14.14	81.10	13.58	0.665	0.515
RMSSD (ms)	25.38	12.91	25.20	15.10	0.13	0.899	20.34	8.81	22.67	10.98	2.54	0.021*
pNN50 (%)	9.08	13.48	8.84	14.84	0.17	0.867	3.69	4.82	5.88	6.41	2.97	0.008**

Differences between groups were calculated by dependent sample t-tests. Significant results are displayed in bold and marked as follows: *p < 0.05 (two-tailed); **p < 0.01 (two-tailed). bpm, beats per minute; ms, milliseconds; N, newton; pNN50, percentage of successive R-R intervals that differ by >50 ms; RMSSD, root mean square differences of successive R-R intervals; SDNN, standard deviation of NN intervals.

Figure 1

Changes in the subjective pain measurement in dependence of the cyberball condition. Error bars represent 95% confidence intervals. Significant results are marked as follows: *p < 0.05 (two tailed); **p < 0.01 (two-tailed). N, newton.

Figure 2

Changes in the objective pain measurement in dependence of the cyberball condition. Error bars represent 95% confidence intervals. Significant results are marked as follows: *p < 0.05 (two-tailed); **p < 0.01 (two-tailed). ms, milliseconds; RMSSD, root mean square differences of successive R-R intervals.

Figure 3

Changes in the objective pain measurement in dependence of the cyberball condition. Error bars represent 95% confidence intervals. Significant results are marked as follows: *p < 0.05 (two-tailed); **p < 0.01 (two-tailed). pNN50, percentage of successive R-R intervals that differ by >50 ms.

4 Discussion

We aimed to compare the effect of social exclusion on pain perception in somatoform pain patients and healthy controls. Regarding pressure pain, social exclusion led to decreased pain thresholds in healthy subjects and somatoform pain patients, without a significant difference between both groups. This result is in line with studies finding greater pain perception after social exclusion in the general population as well as in different clinical samples [10–13]. However, contrary results must be acknowledged. Sometimes, socially excluded individuals experienced less pain, yet another study found greater pain sensitivity after social inclusion, and a recent work reported no effect of social in- or exclusion on pain ratings at all [11,14–16]. This clearly reflects the controversy and the need for an extensive theoretical framework, which integrates these research lines in the pain literature [45–47]. Furthermore, it would be equally helpful to establish a standardized pain measurement procedure in the social pain literature. This would significantly increase the comparability of studies and the informative value of the research area.

Regarding HRV, however, a substantial effect of social exclusion was only detected in somatoform pain patients. RMSSD and pNN50 increased in socially excluded pain patients suggesting a greater activation of parasympathetic nervous system. As already argued in the social pain literature, these findings might indicate an anticipatory regulation process to prevent possible social pain because similar parasympathetic activation patterns have been described for situations that require strong emotional regulation [48–51]. Regarding physical pain, a recent systematic review reported an association between better self-regulation capacities and higher parasympathetic activation [25]. Accordingly, when the parasympathetic element of HRV was high, most studies reported higher pain inhibition capacities (e.g., better management of painful situations) [52–54]. These results are in consonance with the Polyvagal Theory and the Neurovisceral Integration Model which both identify the autonomic nervous system and especially the parasympathetic branch as an important part in the adaptation to various types of stressors including pain [55,56].

Now it is controversial to postulate that somatoform pain patients could have better pain management capacities than the general population. Comparable with the trend of HRV results in this study, a meta-analysis of chronic pain patients showed a significantly reduced RMSSD in comparison to healthy controls, indicating a lower parasympathetic tone in general [57]. Because of the increased pain sensitivity in these patients, pain regulation mechanisms like the parasympathetic component of HRV still might be activated more often and earlier but starts from a lower initial level. This could be an explanation why in this study changes in HRV were only detected in socially excluded somatoform pain patients and not in healthy controls.

To the best of our knowledge, an analysis of social exclusion’s effect on pain perception on patients with somatoform pain disorder was not conducted so far. The current understanding of the functioning of the brain emphasizes the interaction of complex neuronal networks [8,9]. Nevertheless, in view of the neuronal changes in the ACC and the insular cortex, a considerable mutual impact of social and physical pain appears probable, especially in somatoform pain patients. Therefore, a strong influence of social pain on physical pain and vice versa seems very likely. Furthermore, the urgency of a better understanding of pain patients has become more and more clear as one in five US adults is suffering from chronic pain producing enormous healthcare costs and productivity losses [58]. Hopefully, this study provides a first step to examine the effect of social exclusion on pain perception in somatoform pain patients.

Possible limitations of this work should be considered in further research. This study lacks baseline and recovery data for pressure pain and HRV at the beginning and the end of the study. These measurements would have provided useful information and should be included in future studies. Furthermore, different pain modalities like mechanical, thermal, and electrical stimuli could be combined to achieve a broader understanding of the influence of social exclusion on pain perception. However, as described above, the establishment of a standardized pain measurement procedure in social pain studies would be preferable. A larger sample size and comparisons with other pain disorders, such as fibromyalgia, could increase the robustness and generalizability of the results in future studies. Lastly, the influence of different moderating variables like the mood state, social distress caused by the cyberball paradigm or comorbidities could be integrated in the statistical analyses.

From our point of view, it might be interesting to illuminate two research areas in the context of social pain and somatoform pain patients. First, a lot of chronic pain patients report stigmatization and bullying. This is of particular interest because in the framework of the physical–social pain overlap devaluations might provide an explanation for the maintenance of chronic pain. Future studies should address this issue. Second, the investigation of interventions with a positive effect on the parasympathetic component of HRV like breathing techniques or meditation could offer a possible therapeutical approach to achieve better pain management skills [59,60].

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Acknowledgements

The authors would like to thank Heike Althen, Maren Schmidt-Kassow, and Maurice Christian for their extensive technical support. They also thank all the participants for their time and effort in participating.

Research ethics: Research involving human subjects complied with all relevant national regulations, institutional policies and is in accordance with the tenets of the Helsinki Declaration (as amended in 2013) and has been approved by the ethics committee of the Medical School, Goethe University Frankfurt (No. 20-842).
Author contributions: The authors have accepted responsibility for the entire content of this manuscript and approved its submission. F.K. and M.d.G. researched the literature and conceived the study. All authors were involved in protocol development, gaining ethical approval, patient recruitment, and data analysis. F.K. wrote the first draft of the manuscript. All authors reviewed and edited the manuscript and approved the final version of the manuscript.
Competing interests: The authors state no conflict of interest.
Informed consent: Informed consent was obtained from all individuals included in this study, or their legal guardians or wards.
Research funding: None declared.
Supplementary materials: Data set. Social exclusion in somatoform pain patients. (xlsx)
Data availability: The raw data can be obtained on request from the corresponding author.
Artificial intelligence/machine learning tools: Not applicable.

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Received: 2024-05-27

Revised: 2024-10-06

Accepted: 2024-10-25

Published Online: 2024-12-04

This work is licensed under the Creative Commons Attribution 4.0 International License.

Supplementary material

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https://doi.org/10.1515/sjpain-2024-0042

Schlagwörter für diesen Artikel

pain; pain perception; somatoform disorders; pain disorder; social exclusion; pain threshold

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BY 4.0

The effect of social exclusion on pain perception and heart rate variability in healthy controls and somatoform pain patients

Artikel

Abstract

Objectives

Methods

Results

Conclusion

1 Introduction

2 Methods

2.1 Participants

2.2 Cyberball paradigm

2.3 Pressure pain threshold

2.4 HRV

2.5 Questionnaires

2.6 Procedure

2.7 Data analysis

3 Results

3.1 Participants characteristics

3.2 Effects on pain and HRV

4 Discussion

Acknowledgements

References

Zusatzmaterial

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Artikel in diesem Heft

Artikel in diesem Heft