Professional Documents
Culture Documents
DOI: 10.1002/ejp.1411
ORIGINAL ARTICLE
1
Department of Neurophysiology,
Center of Biomedicine and Medical
Abstract
Technology Mannheim, Medical Faculty Background: Cutting is the most common method of non‐suicidal self‐injury (NSSI)
Mannheim, Ruprecht Karls‐University to reduce inner tension in patients with Borderline Personality Disorder (BPD). Aim
Heidelberg, Mannheim, Germany
2
of this study was to compare pain perception induced by an incision and by applica-
Department of Neurology, University of
Cologne, Cologne, Germany tion of a surrogate model for sharp mechanical pain (a non‐invasive “blade”) in BPD.
3
Department of Psychosomatic Medicine Methods: 22 female patients and 20 healthy controls (HC) received a small incision
and Psychotherapy, Central Institute of into the volar forearm, a 7s‐blade application on the same side, and non‐invasive pha-
Mental Health, Ruprecht Karls‐University
Heidelberg, Mannheim, Germany
sic stimuli (pinprick, blade, laser, tactile). Pain intensity as well as affective versus
4
Department of General, Visceral and sensory components were assessed.
Transplantation Surgery, University Results: Incision was rated similarly by both groups (BPD: 28.6 ± 5.5 vs. HC:
Hospital Heidelberg, Heidelberg, Germany
33.9 ± 6.6; mean maximum pain ± SEM; p > 0.8), without significant difference
Correspondence for “7‐s‐blade” (BPD: 18.1 ± 3.8 vs. HC: 25.3 ± 3.6; mean maximum pain ± SEM;
Ulf Baumgärtner, Department of p > 0.17) or between “7‐s‐blade” and incision (BPD: p > 0.12; HC: p > 0.84).
Neurophysiology, Center of Biomedicine
However, patients’ intensity ratings returned significantly faster to baseline after in-
and Medical Technology Mannheim
(CBTM), Medical Faculty Mannheim, cision (BPD: 38.9 ± 12.6 s vs. HC: 74.52 ± 11.5 s; p < 0.05), and patients evaluated
Ruprecht Karls‐University Heidelberg, “blade” and incision without any affective and with different sensory descriptors,
Mannheim, Germany
Email: ulf.baumgaertner@medma.uni-
indicating an altered evaluation of NSSI‐like stimulation with qualitative in addition
heidelberg.de to quantitative differences—especially for the sharp pain component.
Conclusions: The reduced perception of suprathreshold nociceptive stimuli is based
on a missing affective component and specific loss of the perception of “sharpness”
as part of the sensory component of pain. The results further demonstrate the useful-
ness of the “blade” for the perception of sharpness in patients.
Significance: Patients with Borderline Personality Disorder (BPD) who engage in
non‐suicidal self‐injury (NSSI) report less pain in response to phasic nociceptive
stimuli. In comparing an invasive pain stimulus to phasic nociceptive stimuli in BPD
patients, the “blade” as non‐invasive surrogate model for sharp mechanical pain in
psychiatric patients is used. In contrast to healthy volunteers, BPD patients do not
report significant affective ratings and specifically display a reduced sensory com-
ponent for sharpness.
1 | IN TRO D U C T ION Willis and colleagues were the first to use the “blade”
to explore the effect of tissue damage in BPD (Willis et al.,
Non‐suicidal self‐injury (NSSI)—the deliberate and direct 2017) in the context of stress reduction. After experimental
destruction of body tissue without suicidal intent—is fre- stress induction, BPD patients and controls received either an
quently encountered among healthy adolescents and psy- incision or the “blade” or a non‐nociceptive control stimulus
chiatric patients (e.g., in eating disorder and Borderline (sham). Shortly after the application, both painful stimula-
Personality Disorder (BPD); (Swannell, Martin, Page, tions led to a greater stress reduction measured by arousal
Hasking, & St John, 2014 ). Research on this topic has ratings than the sham stimulus in BPD, without significant
more than tripled during the early 2000s, attempting to un- difference between incision and “blade”, emphasizing the
derstand the motivation for as well as underlying pathol- importance of pain experience rather than tissue injury in
ogies of NSSI and to develop adequate therapies (Nock, early stress reduction.
2010). People with BPD struggle with aberrant impulse It is still unclear, if the pain sensation of a real cut as
control, emotion‐ and stress‐dysregulation (Leichsenring, well as of the blade stimulus is perceived differently in BPD
Leibing, Kruse, New, & Leweke, 2011; Lieb Zanarini, under normal conditions without specific stress induction.
Schmahl, Linehan, & Bohus, 2004), which in 69%–90% of We now examined the impact of tissue‐damage (“incision”)
female BPD‐patients result in NSSI (Zanarini et al., 2008), and application of the non‐invasive “blade” without specific
predominantly in the form of cutting or burning them- stress induction regarding temporal pain aspects as well as
selves (Kleindienst et al., 2008; Klonsky, 2007) with the subjective affective and sensory evaluations in detail in order
most commonly reported reasons: reducing aversive inner to investigate whether there are differences in its processing
tension or terminating negative emotions (Kleindienst within acute BPD patients and between patients and healthy
et al., 2008; Ludäscher et al., 2009). controls. It was undertaken according to the experimental
About 70%–80% to eighty percentage of BPD patients re- paradigm used for healthy participants before (Shabes et al.,
port little or no pain during acts of self‐injury (Leibenluft, 2016) to test the following hypotheses:
Gardner, & Cowdry, 1987; Shearer, 1994), and several stud-
ies revealed reduced pain sensitivity in BPD patients who per- 1. We expected the blade to be an adequate incision pain
form NSSI compared to healthy controls. BPD patients report surrogate model in borderline patients with respect to
less pain when exposed to non‐invasive thermal (Bekrater‐ intensity and quality.
Bodmann et al., 2015; Bohus et al., 2000; Russ et al., 1992; 2. Patients with BPD differ from their healthy counterparts
Schmahl et al., 2006, 2004), electrical (Ludäscher et al., in lower pain ratings for different pain modalities. We
2007), mechanical and chemical stimuli (Magerl, Burkart, expected to find reduced mechanical and thermal pain
Fernandez, Schmidt, & Treede, 2012) while their ability to ratings within the same sample of BPD which was pre-
discriminate intensity and localization of nociceptive stimuli viously reported for separate patient groups for pinpricks
was normal (Ludäscher et al., 2007; Schmahl et al., 2004). (Magerl et al., 2012) and laser (Schmahl et al., 2004).
However, investigations concerning invasive, tissue‐damag- 3. Patients perceive and describe pain differently from their
ing painful stimulation as used during NSSI, are sparse. healthy counterparts—especially with respect to the sharp
Reitz and colleagues (Reitz et al., 2015, 2012) first tested mechanical pain component, due to disturbances of affec-
an incision in BPD‐patients, according to the incision‐model tive and sensory processing with a) lower affective levels
of Kawamata established for research on mechanisms of and b) less perception of the “sharp” component in BPD.
postoperative pain (Kawamata et al., 2002). BPD‐patients
exhibited a significant decrease of aversive tension as well
as a decrease of amygdala activity after an incision—a lim-
bic structure important for emotion and stress regulation
2 | M ATERIAL S AND M ETHOD S
(LeDoux, 2000)—whereas amygdala activity increased over
time in the healthy control group.
2.1 | Participants
However, one methodological problem for further anal- After approval of the local Ethics Committee (No.
yses is the limitation to present a single incision stimulus 2011‐243N‐MA), the study was conducted in accordance
during fMRI, where repetitive stimulation is required to in- with the Declaration of Helsinki at the University Medical
crease signal strength for a more detailed examination of af- Centre Mannheim. Having received both verbal and writ-
fected neuronal pain circuitries in BPD. Therefore, Shabes et ten explanations of all tasks, volunteers gave written in-
al. (2016) established a non‐invasive surrogate model—the formed consent and received monetary compensation for
0.1 × 4 mm non‐penetrating “blade” with a force of 4096 participation.
mN—offering a repeatable application of an incision‐like The patients investigated in this study took part in a larger
pain stimulus (Shabes et al., 2016). research framework where patients were recruited through
SCHLOSS et al.
3
|
a central office of KFO 256. After the diagnostic procedure 14 sensory (e.g., stinging, burning) and 14 affective items
conducted by clinically experienced interviewers, all patients (e.g., cruel, miserable) (Geissner, 1996; Schilder et al.,
included met the criteria for BPD according to the Diagnostic 2014). In the SES, pain descriptors were weighed by ratings
and Statistical Manual of Mental Disorders (DSM, APA on a 0 to 3 ordinal scale (0 = does not apply, 1 = applies
2013) determined via the International Personality Disorder somewhat, 2 = applies mostly, 3 = applies fully). According
Examination (IPDE) (Loranger, 1999). A subsample of 22 to previous work, sensory scores can be grouped into “deep”
female patients with BPD (mean age 30.45 ± 10.54 SD) par- and superficial pain, which itself can be subclassified into
ticipated in this study and was compared to 20 female healthy “heat” (C‐fibre related quality) and “sharp” (A‐δ related
controls who underwent the same testing protocol as described quality) mechanical pain. Hansen et al. performed a factor
in “2.4 Experimental procedure” (Shabes et al., 2016) (com- analysis to elucidate meaningful sensory qualities by using
parison of healthy women to men; mean age 24.25 ± 4.68 the VARIMAX method. Hence, we used these three factors
SD). Eleven i.e., 50% of the BPD patients represent a sub- (thermal, sharp, deep) in order to categorize the relatively
sample of the patients with acute BPD who also took part in large number of items for simplification (Hansen, Klein,
the study of Wills et al. (2017). All experiments were held at Magerl, & Treede, 2007).
different dates. Considering the aspect of hypoalgesia during dissociative
NSSI including tissue‐damage within the preceding states in BPD, dissociation was checked via DSS‐4, a valid
6 months was reported by all BPD‐patients. Any healthy short instrument to assess dissociative experience during ex-
control subject with a life‐time‐event of NSSI was excluded periments (Stiglmayr, Schmahl, Bremner, Bohus, & Ebner‐
from this study. Further exclusion criteria included a lifetime Priemer, 2009).
diagnosis of schizophrenia, bipolar disorder type 1, current
substance abuse, neurologic diseases (i.e., epilepsy, multiple
sclerosis, brain tumors) or pre‐existing mild to severe pain T A B L E 1 Demographic data and psychiatric comorbidities. HC
syndromes. None of the participants took any analgesic med- data from Shabes et al. (2016)
ication two weeks prior to this study, also known that use of
potent analgesics might aggravate psychopathology in BPD Group BPD (n = 22) HC (n = 20)
(Thurauf & Washeim, 2000); as psychotropic drugs selective Age 30.45 ± 10.54 24.25 ± 4.68
serotonin reuptake inhibitors and tricyclic antidepressants Psychiatric comorbidities
were allowed because of the high prevalence of this medi- Mood disorder, current 9 (40.9%)
cation among BPD patients. For demographic and psycho- Mood disorder, lifetime 19 (86.4%)
pathological data, see Table 1. Substance abuse, lifetime 9 (40.9%)
Substance dependence, 8 (36.4%)
2.2 | Ratings and questionnaires lifetime
Anxiety disorder, current 8 (36.4%)
All stimuli were evaluated in terms of pain intensity via a
Anxiety disorder, life time 10 (45.5%)
numeric rating scale (NRS) and a visual analogue scale
Posttraumatic stress disorder, 7 (31.8%)
(VAS) which both ranged from 0 (= no pain at all) to 100
current
(= most intense pain imaginable). NRS was given verbally
Posttraumatic stress disorder, 10 (45.5%)
for every single stimulus, whereas the rating via VAS was
lifetime
executed electronically using a computer mouse for incision
Eating disorder, current 7 (31.8%)
and 7‐s‐blade application. The time course of VAS rating
was sampled at 10 Hz (Dapsys software provided by Brian Eating disorder, lifetime 10 (45.5%)
Turnquist). These VAS and NRS were pure “pain scales”, Medication
where “0” indicated either no perception at all or any per- None 11 (50%) 12 (60%)
ception that was not painful (warmth, touch), without anchor Selective serotonin reuptake 5 (23%)
points in order to have a pure rationale scale. inhibitors
To differentiate between the sensory‐discriminative Tricyclic antidepressants 1 (4.5%)
and affective‐evaluative components of pain, an extended Beta‐blocker 1 (4.5%)
version of the German Pain Perception Scale (Schmerz‐ Proton pump inhibitors 2 (9%)
Empfindungsskala, SES Geissner, 1995) was used, which Oral contraceptives 3 (14%) 6 (30%)
contains 4 additional sensory items (dull, pressing, pull-
Thyroid hormones 1 (4.5%) 2 (10%)
ing, pulsating) than the previous version with 24 descrip-
Phytopharmaca 1 (4.5%)
tors—derived from the McGill Pain Questionnaire (MPQ,
Melzack, 1975, 1987)—resulting in a list with an number of Asthma medication 1 (4.5%)
|
4 SCHLOSS et al.
Blunt pressure tactile stimuli (1 s) 1. Incision (1 s): As Shabes and colleagues found no dif-
Serving as control stimuli, five non‐noxious mechanical ferences of effects (order effect) when the incision was
stimuli with sphere‐shaped tips were used. They were con- executed before or after the remaining stimuli (Shabes
structed like the blades, with the same forces on different et al., 2016), incision in the present study was executed
contact areas: 50.3 mm2 (256 mN), 63.6 mm2 (512 mN), at the beginning of the experiment to the left volar
95.0 mm2 (1024 mN), 132.7 mm2 (2048 mN), and 201.1 forearm.
mm2 (4096 mN). 2. Pinpricks, blades, and spheres were applied manually,
perpendicular to the skin with variation of location to the
Laser heat stimuli (1 ms) right volar forearm for 1 s. These single modalities were
Using laser heat stimuli is the most validated method to ex- tested in separate blocks the order of which was balanced
plore the nociceptive system in selectively activating A‐δ and across subjects. Within each of these blocks, five intensi-
C‐fibres without exciting tactile receptors of the skin/ sen- ties (of the respective modality) were applied in pseudor-
sory cutaneous receptors (Bromm & Treede, 1991; Plaghki & andomized order (25 stimulations).
Mouraux, 2003) and have frequently been used in investigat- 3. After that, a block of 25 laser heat stimuli was applied in
ing pain perception in BPD (Ludäscher et al., 2009; Schmahl the same fashion again to the right volar forearm, for 1 ms.
et al., 2004). Therefore, we again stimulated with radiant 4. At the end, the application of the sharp mechanical pain
heat stimuli generated by a PC‐controlled infrared thulium‐ stimulus (blade, 4096 mN) for the duration of 7 s took
YAG laser (THEMIS, StarmedTec, Starnberg, Germany; place. It was presented to the same arm as the incision (left
wavelength 2 µm; pulse duration 1 ms). We used a paradigm volar forearm).
F I G U R E 2 Study design. First, an incision (1 s) was made into the left volar forearm followed by a balanced sequence of phasic (1 s),
mechanical and tactile stimuli to the right volar forearm. After that, a block of laser stimuli (1 msec) was applied, again to the right volar forearm.
At the end, an investigation with the blade (4096 mN, 7 s) was carried out to the left volar forearm. VAS = visual analogue scale (only during and
after incision and 7 s blade application), NRS = numeric rating scale; SES score (“Schmerz‐Empfindungsskala”) for each stimulus; I‐V = stimulus
intensities
|
6 SCHLOSS et al.
3.2.1 | Blade
Mean pain ratings across the entire time course of the
4096mN‐blade application until ratings returned to baseline
were lower in BPD (22.2 ± 5.3 SEM) than in the healthy
control group (32.5 ± 4.8 SEM; p < 0.05, d = 0.46; Figure
5a,b). Accordingly, evaluating the individual maximum pain
ratings, BPD patients reported significantly lower pain, with
23.1 ± 4.6 compared to 33. 9 ± 4.7 (HC; p < 0.05, d = 0.52).
Concentrating only on the first 7 s, where the actual blade‐ap-
plication took place, there was no significant difference be-
tween groups (mean maximum pain ratings: BPD 18.1 ± 3.8
and HC 25.3 ± 3.6; p = 0.17, d = 0.43; Figure 5b).
Although peak ratings of healthy subjects were higher, the
mean time course of both groups was similar without signif-
icant differences, both reached maximum pain after 5.3 (HC)
and 5.5 (BPD) seconds (mean) and reached baseline again
after 20–30 s.
3.2.2 | Incision
F I G U R E 4 (a) Description of the affective and sensory pain
There was no significant difference for incision between
components by means of the Pain Sensation Questionnaire (Schmerz‐
Empfindungsskala, SES) for incision and blade (7s) in BPD (n = 22)
groups (p > 0.6, d = 0.2), although nominally ratings
with significantly lower affective than sensory scores for both stimuli were slightly lower in BPD patients than in healthy sub-
(p < 0.05). *** p < 0.001. (b) SES pain ratings for the three sensory jects, with a mean maximum rating in the BPD group
submodalitites according to the factorial analyses from (Hansen et average across time of 28.6 ± 5.5 (mean ± SEM; on av-
al., 2007): “deep” pain and “superficial” pain consisting of the two erage 3.3 s after beginning of the incision; Figure 5c)
components “sharp” mechanical pain (A‐delta‐fiber related quality) compared to 33.9 ± 6.6 in the HC group, after 3.6 s on
and “heat” pain (C‐fiber related quality); from sensory pain descriptors average after incision‐start. As in both groups the interin-
form the Pain Sensation Questionnaire (Schmerz‐Empfindungsskala, dividual pain duration was highly variable, time courses
SES) scores for incision and blade (7 s) in BPD (n = 22). Blade evoked were roughly similar. While 3 healthy subjects rated up
a similar perception pattern as incision (sharp > thermal > deep), but to over 80/100 mm on the VAS scale and 2 of them even
with overall significantly higher values for incision. * =p < 0.05,
over 90, there was also only one BPD patient who reported
**=p < 0.01
a maximum pain sensation of 85. Further, only 2 healthy
participants gave ratings under 10, whereas there were 6 of
a similar descending order for both stimuli, with “sharp” as these in the BPD group. In addition, there was also no sig-
the highest scored modality, followed by thermal and deep nificant difference in the individual peak ratings of incision
(sharp > thermal > deep, Figure 4b). induced‐pain: 31.2 ± 5.5 (BPD) compared with 40.0 ± 6.7
The single SES description (raw) items again showed sim- (HC; p > 0.3, d = 0.32). We also found no significant dif-
ilar profiles for incision and blade (7 s) without any affective ferences in the early phases—0 to 30 s as well as 30 to
descriptor as statistically significant (Bonferroni‐correction). 60 s—but after a minute, in the time window 60 to 90 s,
For the sensory pain component, 4 sensory descriptors were healthy women gave significantly higher ratings than BPD
found to be statistically different from zero for incision (“cut- patients (p < 0.05, d = 0.69; Figure 5d). With a mean decay
ting”, “burning”, “stinging”, “pulling”) versus 2 for blade to half‐maximal pain of 33.0 ± 7.9 s, and finally to base-
(“stinging”, “pressing”), with differences between stimulus line after 74.5 ± 11.5 s in HC, BPD patients dropped sig-
modalities for “cutting”, “burning” and “throbbing” which nificantly faster to baseline again after less than a minute
|
8 SCHLOSS et al.
F I G U R E 5 (a) Mean time course of blade pain (7 s) in BPD patients (grey line; n = 22) versus healthy controls (black line; n = 20). (b) Mean
ratings for BPD patients and healthy controls and in the time windows 0 to 7 s ± SD. No significant difference between BPD and HC for both blade
pain and incision pain (p > 0.1 for blade; p > 0.7 for incision; unpaired student t test) and between incision and blade pain within each group (BPD:
p > 0.4; HC: p > 0.8; unpaired student t test). (c) Mean time course of incisional pain in BPD patients (grey line; n = 22) versus healthy controls
(black line; n = 20). (d) Mean ratings for BPD patients and healthy controls in the time windows 0 to 30, 30 to 60, 60 to 90, and 90 to 239 s ± SD.
Between 60 and 90 s, BPD patients gave significantly lower pain ratings (p < 0.05; unpaired student t test). HC data from Shabes et al. (2016)
F I G U R E 6 Comparison of stimulus‐
response functions for mechanical (left) and
laser heat (right) stimuli (all 1 s) between
BPD patients (n = 22) and healthy controls
(n = 20). In both groups, modality and
intensity affect pain rating significantly
(p ≤ 0.001). There was a significant main
effect of group for all modalities (p ≤ 0.001)
except for tactile spheres (p > 0.6). HC data
from Shabes et al. (2016)
with 38.9 ± 12 s (p < 0.05, d = 0.68) and showed a trend difference was found for modality as well as for intensity as
towards statistical significance of 16.0 ± 3.5 s for reaching main effect (p < 0.001, f2 = 0.24; with a significant interac-
half‐maximum pain (p < 0.06, d = 0.64). tion group X modality p < 0.001, F = 5.48; but no significant
Similar as for BPD patients, mean pain ratings during interaction group × intensity p = 0.47, F = 0.88). Borderline
the first 7 s in HC did not differ significantly between in- patients gave significantly lower pain ratings than healthy
cision and blade application (incision: 24.2 ± 4.4 vs. blade: controls for pinprick (p < 0.05, f2 = 2.1), 1s blade (p < 0.001,
25.3 ± 3.6, p > 0.8, d = 0.06; Figure 5b). f2 = 9.26) and laser (p < 0.01, f2 = 1.66) stimuli. In both
groups, spheres as control stimuli were similarly not evaluated
as painful (p > 0.6). There was no significant difference for
3.2.3 | Stimulus response functions for
the lowest two intensities of each modality between groups,
phasic stimuli
rated rather “tactile” than painful, whereas healthy controls
BPD patients tended to give overall lower pain ratings than showed significantly higher pain ratings for the higher third
their healthy counterparts (Figure 6): A significant group (only laser, p < 0.05, f2 = 0.03), the fourth and fifth (laser and
SCHLOSS et al.
|
9
blade, both p < 0.01, f2 = 0.05) intensity. In both groups, stim- counterparts (p < 0.01, d(incision) = 1.02, d(blade) = 1; Figure
ulus modality had a highly significant impact on pain intensity 7b).
(2‐way ANOVA modality: p < 0.001, f2 = 0.62; intensity: 1‐ For both groups, scores for the sensory pain compo-
factorial ANOVA, p < 0.001, f2 = 0.13; Figure 6). There was nent were significantly higher than for the affective pain
no significant difference within each group between ratings component, independent of the stimulus modality (in BPD:
for blade (1 s) and laser (HC p > 0.6; BPD p > 0.3). Using p < 0.001 for incision, blade and laser; p < 0.05 for pin-
the blade as a surrogate for incisional pain, it elicited 2 to 3 prick and sphere; in HC: p < 0.001 for incision, blade, pin-
times higher pain ratings than provoked through the other me- prick and laser; p < 0.05 for sphere; see Figure 8 depicting
chanical modalities in both groups. In summary, BPD patients the comparison of affective and sensory pain evaluation
reported less pain for pinprick, blade and laser stimuli. between the group of BPD patients and HC for incision,
blade, pinprick, laser and sphere (1 s).
3.3 | SES‐scores For the control stimulus (spheres), pinprick and laser, the
Stimulus modality influenced SES scores, consisting of sen- SES‐scoring pattern of the descriptors was similar between
sory and affective subscales, significantly (p < 0.001, f2 = groups. For pinpricks, in both groups the descriptor “sting-
0.24) and there were statistically significant differences be- ing” depicted pain sensation. For laser heat, 4 same sensory
tween groups (p < 0.05, f2 = 0.01) and between affective and descriptors were found in both groups (“burning”, “scald-
sensory scores (p < 0.001, f2 = 0.13; 3‐factorial ANOVA; ing”, “stinging” and “hot”) with one additional sensory item
main effects affective‐sensory, modality, group; Table 2). (“pulling”) in healthy controls and one additional affective
There was no statistically significant interaction between item (“agonizing”) in BPD, without significant difference.
group and modality (p > 0.1) or between group and affec- As expected, there were no descriptors found characterizing
tive‐sensory (p > 0.8), but between modality and affective‐ pain for our tactile control stimuli (spheres; see supplemen-
sensory (p < 0.001, f2 = 0.04). tary Figure S2 in the Supplement for detailed overview of the
Concentrating only on incision and phasic blade‐applica- comparison of affective and sensory pain descriptors form
tion (1 s), there were significant differences between groups the SES Pain Sensation Questionnaire scores between BPD
(2‐factorial ANOVA; main effects group, affective‐sensory; and HC).
p < 0.001, f2 = 0.05; Table 2). There was no significant dif-
ference between groups for incision SES scores (affective: 3.4 | Dissociation
p > 0.1, d = 0.44; sensory: p > 0.2, d = 0.37), however 1s
blade induced pain was scored lower in BPD than HC for both Patients did not dissociate during pain stimulation according to
modalities (affective: p < 0.05, d = 0.72; sensory: p < 0.05, DSS 4 questionnaire (score = 0.77 ± 0.35 [< 1.57 as score for
d = 0.66, Figure 7a). transition to dissociation] (Stiglmayr et al., 2009)).
Significant differences were found for several descriptors
as single items of the sub‐modalities affective/sensory for the
blade stimulus and incision: 7 descriptors (2 affective and 5
4 | DISCUSSION
sensory) characterized incisional pain in healthy subjects, This study is investigating incisional pain under standard-
whereas in BPD no affective and only 4 sensory descriptors ized experimental conditions in patients with acute BPD in
(“cutting”, “burning”, “stinging” and “pulling”) were found. comparison with the new sharp mechanical pain stimulus
The affective descriptor “agonizing” and the sensory descrip- “blade” and well‐established, experimental nociceptive and
tors “cutting” and “stinging” were rated significantly lower in tactile control stimuli with respect to time courses of pain
BPD (p(agonizing) < 0.005, d = 0.48; p(cutting, stinging) < 0.05 d(cut- perception as well as affective and sensory evaluation. For
ting) = 0.39, d(stinging) = 0.36). Similar different evaluations the whole duration of incisional and blade pain, ratings were
were also found for blade, where the same sensory descrip- lower in BPD than healthy controls, however there was no
tors “cutting” and “stinging” and additionally “piercing” and significant difference in the early (7 s) phase during stimulus
the affective depiction “dreadful” were rated significantly application. The same was true for the comparison between
lower in BPD (p < 0.05, d(stinging) = 0.31, d(piercing) = 0.32, “blade” and incision for both BPD and HC. Hence, in BPD
d(dreadful) = 0.39; for “cutting” p < 0.001, d = 0.58). tonic (7 s) blade stimulation induces comparable effects at
Single items were again grouped as three factors (ther- the initial time course of an incision. Stimulus‐response func-
mal, sharp, deep), according to (Hansen et al., 2007). In tion for both nociceptive mechanical and heat stimuli indi-
both groups, sensory SES scoring patterns for incision and cated reduced pain perception in comparison with HCs.
blade (1s) were similar (sharp > thermal > deep), whereas Overall, patients with BPD evaluated pain sensation as
both incision and blade (1s) were perceived significantly less unpleasant, and interestingly, the sensory component
less sharp in the BPD group compared to their healthy “sharp” in specific was rated less in BPD patients.
|
10 SCHLOSS et al.
T A B L E 2 SES‐scores: Main‐effects/
Least square
Interaction‐effects of 2‐/3‐factorial ANOVAs (3
In BPD Incision, blade 7 s means ± SEM df F P
way interactions not shown)
Modality 1 3.7 0.059
Incision 4.4 ± 0.5
blade 7sec 3.0 ± 0.5
Evaluation scores 1 36.5 <0.001
Sensory 5.9 ± 0.5
Affective 1.5 ± 0.5
Modality X sensory‐affective 1 1.6 0.205
In BPD Incision, blade 1 s
Modality 1 9.4 0.003
incision 4.4 ± 0.5
blade 1sec 2.3 ± 0.5
Evaluation scores 1 34.9 <0.001
Sensory 5.4 ± 0.5
Affective 1.3 ± 0.5
Modality X sensory‐affective 1 3.4 0.07
Both groups, incision, blade 1 s
Group 1 11.9 <0.001
BPD 3.3 ± 0.4
HC 5.4 ± 0.4
Evaluation scores 1 52.8 <0.001
Sensory 6.4 ± 0.4
Affective 2.2 ± 0.4
Group X sensory‐affective 1 0.1 0.738
Both groups, all stimuli
Group 1 7.8 0.006
BPD 2.8 ± 0.3
HC 3.9 ± 0.3
Modality 4 29.9 <0.001
incision 5.1 ± 0.4
blade 1 s 3.6 ± 0.4
pinprick 1 s 1.7 ± 0.4
laser 1 s 5.9 ± 0.4
sphere 1 s 0.2 ± 0.4
Evaluation scores 1 73.0 <0.001
Sensory 4.9 ± 0.3
Affective 1.7 ± 0.3
Group × modality 4 1.6 0.187
Group × sensory‐affective 1 0.7 0.824
Modality × sensory‐affective 4 6.6 <0.001
Note: Upper (first) panel: results of 2 way ANOVA for the comparison incision versus blade within
BPD patients with main factors modality (incision, 7 s blade) and SES (sensory, affective), and
interaction. Second panel: Same as upper (first) panel, however with modality and SES for the 1 s
blade stimulus (used in the stimulus‐response functions), Third panel: results of 2 way ANOVA
for the SES/ group comparison (modalities incision and 1 s blade pooled) with main factors group
(BPD, HC) and SES (sensory, affective) and interaction. Forth (lowest) panel: Results of 3‐way
ANOVA for groups, modalities, and SES with main factors group (BPD, HC), modality (5 modali-
ties) and SES (sensory, affective), and 3 1 × 1 interactions.
SCHLOSS et al.
|
11
F I G U R E 7 (a) Comparison of affective and sensory SES pain ratings for incision (left) and blade (1 s, right) between BPD patients
(n = 22) and healthy controls (n = 20). No significant difference for incision between groups, but for blade (1 s) for both affective and sensory
scores. * =p < 0.05. (b) Comparison of sensory SES pain ratings for the three factors (thermal, sharp and deep) (Hansen et al., 2007) for incision
(left) and blade (1 s, right) between BPD patients (n = 22) and healthy controls (n = 20). Both groups showed similar evaluation patterns
(sharp > thermal > deep). Descriptors depicting the “sharp” component were rated significantly less in the BPD group for both incision and blade
(1 s) than in the HC group. **=p < 0.01. HC data from Shabes et al. (2016)
|
12 SCHLOSS et al.
borderline personality disorder: Results from the thermal grill with borderline personality disorder using signal detection theory.
illusion. Pain, 156(10), 2084–2092. https ://doi.org/10.1097/j. Psychiatry Research, 70(3), 175–183.
pain.0000000000000275 Kleindienst, N., Bohus, M., Ludascher, P., Limberger, M. F., Kuenkele,
Bodnar, R. J., Kelly, D. D., Brutus, M., & Glusman, M. (1980). Stress‐in- K., Ebner‐Priemer, U. W., … Schmahl, C. (2008). Motives for non-
duced analgesia: Neural and hormonal determinants. Neuroscience suicidal self‐injury among women with borderline personality disor-
and Biobehavioral Reviews, 4(1), 87–100. der. The Journal of Nervous and Mental Disease, 196(3), 230–236.
Bohus, M., Limberger, M., Ebner, U., Glocker, F. X., Schwarz, B., https://doi.org/10.1097/NMD.0b013e3181663026
Wernz, M., & Lieb, K. (2000). Pain perception during self‐reported Kleinschnitz, C., Brinkhoff, J., Zelenka, M., Sommer, C., & Stoll, G.
distress and calmness in patients with borderline personality disorder (2004). The extent of cytokine induction in peripheral nerve le-
and self‐mutilating behavior. Psychiatry Research, 95(3), 251–260. sions depends on the mode of injury and NMDA receptor signal-
Bowler, J. O., Bartholomew, K. J., Kellar, I., Mackintosh, B., Hoppitt, L., ing. Journal of Neuroimmunology, 149(1–2), 77–83. https ://doi.
& Bayliss, A. P. (2017). Attentional bias modification for acute exper- org/10.1016/j.jneuroim.2003.12.013
imental pain: A randomized controlled trial of retraining early versus Klonsky, E. D. (2007). The functions of deliberate self‐injury: A review
later attention on pain severity, threshold and tolerance. European of the evidence. Clinical Psychology Review, 27(2), 226–239. https
Journal of Pain, 21(1), 112–124. https://doi.org/10.1002/ejp.908 ://doi.org/10.1016/j.cpr.2006.08.002
Brennan, T. J., Zahn, P. K., & Pogatzki‐Zahn, E. M. (2005). Mechanisms Kluetsch, R. C., Schmahl, C., Niedtfeld, I., Densmore, M., Calhoun, V.
of incisional pain. Anesthesiology Clinics of North America, 23(1), D., Daniels, J., … Lanius, R. A. (2012). Alterations in default mode
1–20. https://doi.org/10.1016/j.atc.2004.11.009 network connectivity during pain processing in borderline person-
Bromm, B., & Treede, R. D. (1991). Laser‐evoked cerebral potentials in ality disorder. Archives of General Psychiatry, 69(10), 993–1002.
the assessment of cutaneous pain sensitivity in normal subjects and https://doi.org/10.1001/archgenpsychiatry.2012.476
patients. Revue Neurologique, 147(10), 625–643. LeDoux, J. E. (2000). Emotion circuits in the brain. Annual Review
Desmond, J. E., & Glover, G. H. (2002). Estimating sample size in func- of Neuroscience, 23, 155–184. https ://doi.org/10.1146/annur
tional MRI (fMRI) neuroimaging studies: Statistical power analyses. ev.neuro.23.1.155
Journal of Neuroscience Methods, 118(2), 115–128. Leibenluft, E., Gardner, D. L., & Cowdry, R. W. (1987). Special feature the
Fißmer, I., Klein, T., Magerl, W., Treede, R. D., Zahn, P. K., & Pogatzki‐ inner experience of the borderline self‐mutilator. Journal of Personality
Zahn, E. M. (2011). Modality‐specific somatosensory changes in Disorders, 1(4), 317–324. https://doi.org/10.1521/pedi.1987.1.4.317
a human surrogate model of postoperative pain. Anesthesiology, Leichsenring, F., Leibing, E., Kruse, J., New, A. S., & Leweke, F.
115(2), 387–397. https://doi.org/10.1097/ALN.0b013e318219509e (2011). Borderline personality disorder. Lancet, 377(9759), 74–84.
Geis, C., Geuss, E., Sommer, C., Schmidt, H. H., & Kleinschnitz, C. (2017). https://doi.org/10.1016/S0140-6736(10)61422-5
NOX4 is an early initiator of neuropathic pain. Experimental Neurology, Leknes, S., & Tracey, I. (2008). A common neurobiology for pain and
288, 94–103. https://doi.org/10.1016/j.expneurol.2016.11.008 pleasure. Nature Reviews Neuroscience, 9(4), 314–320. https://doi.
Geissner, E. (1995). The Pain Perception Scale—A differentiated org/10.1038/nrn2333
and change‐sensitive scale for assessing chronic and acute pain. Lieb, K., Zanarini, M. C., Schmahl, C., Linehan, M. M., & Bohus, M.
Rehabilitation (Stuttg), 34(4), XXXV–XLIII. (2004). Borderline personality disorder. The Lancet, 364(9432),
Geissner, E. (1996). Die Schmerzempfindungs‐Skala : (SES); 453–461. https://doi.org/10.1016/s0140-6736(04)16770-6
Handanweisung. Göttingen; Bern; Toronto; Seattle: Hogrefe, Verl. Loranger, A. W. (1999). International Personality Disorder Examination
für Psychologie. (IPDE): DSMIV and ICD‐10 modules. Psychological Assessment
Hansen, N., Klein, T., Magerl, W., & Treede, R. D. (2007). Resources.
Psychophysical evidence for long‐term potentiation of C‐fiber Ludascher, P., Bohus, M., Lieb, K., Philipsen, A., Jochims, A., &
and Adelta‐fiber pathways in humans by analysis of pain descrip- Schmahl, C. (2007). Elevated pain thresholds correlate with dis-
tors. Journal of Neurophysiology, 97(3), 2559–2563. https://doi. sociation and aversive arousal in patients with borderline person-
org/10.1152/jn.01125.2006 ality disorder. Psychiatry Research, 149(1–3), 291–296. https://doi.
Hayasaka, S., Peiffer, A. M., Hugenschmidt, C. E., & Laurienti, P. J. org/10.1016/j.psychres.2005.04.009
(2007). Power and sample size calculation for neuroimaging studies Ludäscher, P., Greffrath, W., Schmahl, C., Kleindienst, N., Kraus, A.,
by non‐central random field theory. NeuroImage, 37(3), 721–730. Baumgartner, U., … Bohus, M. (2009). A cross‐sectional investigation of
https://doi.org/10.1016/j.neuroimage.2007.06.009 discontinuation of self‐injury and normalizing pain perception in patients
Iannetti, G. D., Zambreanu, L., Cruccu, G., & Tracey, I. (2005). with borderline personality disorder. Acta Psychiatrica Scandinavica,
Operculoinsular cortex encodes pain intensity at the earliest stages 120(1), 62–70. https://doi.org/10.1111/j.1600-0447.2008.01335.x
of cortical processing as indicated by amplitude of laser‐evoked Magerl, W., Burkart, D., Fernandez, A., Schmidt, L. G., & Treede, R.
potentials in humans. Neuroscience, 131(1), 199–208. https://doi. D. (2012). Persistent antinociception through repeated self‐injury
org/10.1016/j.neuroscience.2004.10.035 in patients with borderline personality disorder. Pain, 153(3), 575–
Kawamata, M., Takahashi, T., Kozuka, Y., Nawa, Y., Nishikawa, K., 584. https://doi.org/10.1016/j.pain.2011.11.021
Narimatsu, E., … Namiki, A. (2002). Experimental incision‐in- McCown, W., Galina, H., Johnson, J., DeSimone, P. A., & Posa, J.
duced pain in human skin: Effects of systemic lidocaine on flare (1993). Borderline personality disorder and laboratory‐induced
formation and hyperalgesia. Pain, 100(1–2), 77–89. cold pressor pain: Evidence of stress‐induced analgesia. Journal of
Kelly, D. D. (1982). The role of endorphins in stress‐induced analgesia. Psychopathology and Behavioral Assessment, 15(2), 87–95. https://
Annals of the New York Academy of Sciences, 398, 260–271. doi.org/10.1007/bf00960610
Kemperman, I., Russ, M. J., Clark, W. C., Kakuma, T., Zanine, E., McIver, T. A., Kornelsen, J., & Stroman, P. W. (2018). Diversity in the
& Harrison, K. (1997). Pain assessment in self‐injurious patients emotional modulation of pain perception: An account of individual
SCHLOSS et al.
15
|
variability. European Journal of Pain, 22(2), 319–332. https://doi. behavior. Journal of Personality Disorders, 26(4), 605–615. https://
org/10.1002/ejp.1122 doi.org/10.1521/pedi.2012.26.4.605
Melzack, R. (1975). The McGill Pain Questionnaire: Major properties Rolke, R., Baron, R., Maier, C., Tolle, T. R., Treede, R. D., Beyer, A., …
and scoring methods. Pain, 1(3), 277–299. Wasserka, B. (2006a). Quantitative sensory testing in the German
Melzack, R. (1987). The short‐form McGill Pain Questionnaire. Pain, Research Network on Neuropathic Pain (DFNS): Standardized
30(2), 191–197. protocol and reference values. Pain, 123(3), 231–243. https://doi.
Morewedge, C. K., Kassam, K. S., Hsee, C. K., & Caruso, E. M. (2009). org/10.1016/j.pain.2006.01.041
Duration sensitivity depends on stimulus familiarity. Journal of Rolke, R., Magerl, W., Campbell, K. A., Schalber, C., Caspari, S.,
Experimental Psychology: General, 138(2), 177–186. https://doi. Birklein, F., & Treede, R. D. (2006b). Quantitative sensory testing:
org/10.1037/a0015219 A comprehensive protocol for clinical trials. European Journal of
Mumford, J. A., & Nichols, T. E. (2008). Power calculation for group Pain, 10(1), 77–88. https://doi.org/10.1016/j.ejpain.2005.02.003
fMRI studies accounting for arbitrary design and temporal autocor- Russ, M. J., Roth, S. D., Lerman, A., Kakuma, T., Harrison, K.,
relation. NeuroImage, 39(1), 261–268. https ://doi.org/10.1016/j. Shindledecker, R. D., … Mattis, S. (1992). Pain perception in self‐
neuroimage.2007.07.061 injurious patients with borderline personality disorder. Biological
Naoum, J., Reitz, S., Krause‐Utz, A., Kleindienst, N., Willis, F., Kuniss, Psychiatry, 32(6), 501–511.
S., … Schmahl, C. (2016). The role of seeing blood in non‐suicidal Schilder, A., Hoheisel, U., Magerl, W., Benrath, J., Klein, T., & Treede,
self‐injury in female patients with borderline personality disorder. R. D. (2014). Sensory findings after stimulation of the thoraco-
Psychiatry Research, 246, 676–682. https://doi.org/10.1016/j.psych lumbar fascia with hypertonic saline suggest its contribution to
res.2016.10.066 low back pain. Pain, 155(2), 222–231. https ://doi.org/10.1016/j.
New, A. S., & Stanley, B. (2010). An opioid deficit in borderline per- pain.2013.09.025
sonality disorder: Self‐cutting, substance abuse, and social dysfunc- Schmahl, C., Bohus, M., Esposito, F., Treede, R. D., Di Salle, F.,
tion. American Journal of Psychiatry, 167(8), 882–885. https://doi. Greffrath, W., … Seifritz, E. (2006). Neural correlates of antino-
org/10.1176/appi.ajp.2010.10040634 ciception in borderline personality disorder. Archives of General
Niedtfeld, I., Schulze, L., Kirsch, P., Herpertz, S. C., Bohus, M., & Psychiatry, 63(6), 659–667. https
://doi.org/10.1001/archp
Schmahl, C. (2010). Affect regulation and pain in borderline per- syc.63.6.659
sonality disorder: A possible link to the understanding of self‐injury. Schmahl, C., Greffrath, W., Baumgartner, U., Schlereth, T., Magerl,
Biological Psychiatry, 68(4), 383–391. https ://doi.org/10.1016/j. W., Philipsen, A., … Treede, R. D. (2004). Differential nociceptive
biopsych.2010.04.015 deficits in patients with borderline personality disorder and self‐in-
Nock, M. K. (2010). Self‐injury. Annual Review of Clinical Psychology, jurious behavior: Laser‐evoked potentials, spatial discrimination of
6, 339–363. https://doi.org/10.1146/annurev.clinpsy.121208.131258 noxious stimuli, and pain ratings. Pain, 110(1–2), 470–479. https://
Pavony, M. T., & Lenzenweger, M. F. (2014). Somatosensory process- doi.org/10.1016/j.pain.2004.04.035
ing and borderline personality disorder: Pain perception and a signal Schulz, E., Tiemann, L., Schuster, T., Gross, J., & Ploner, M. (2011).
detection analysis of proprioception and exteroceptive sensitivity. Neurophysiological coding of traits and states in the perception of
Personal Disord, 5(2), 164–171. https://doi.org/10.1037/per0000017 pain. Cerebral Cortex, 21(10), 2408–2414. https://doi.org/10.1093/
Plaghki, L., & Mouraux, A. (2003). How do we selectively activate cercor/bhr027
skin nociceptors with a high power infrared laser? Physiology and Shabes, P., Schloss, N., Magerl, W., Schmahl, C., Treede, R. D., &
biophysics of laser stimulation. Neurophysiologie Clinique, 33(6), Baumgartner, U. (2016). A novel human surrogate model of non-
269–277. injurious sharp mechanical pain. Pain, 157(1), 214–224. https://doi.
Pogatzki‐Zahn, E. M., Wagner, C., Meinhardt‐Renner, A., Burgmer, M., org/10.1097/j.pain.0000000000000352
Beste, C., Zahn, P. K., & Pfleiderer, B. (2010). Coding of incisional Shearer, S. L. (1994). Phenomenology of self‐injury among inpatient
pain in the brain: A functional magnetic resonance imaging study women with borderline personality disorder. The Journal of Nervous
in human volunteers. Anesthesiology, 112(2), 406–417. https://doi. and Mental Disease, 182(9), 524–526.
org/10.1097/ALN.0b013e3181ca4c82 Slugg, R. M., Campbell, J. N., & Meyer, R. A. (2004). The population
Porges, S. W. (2007). The polyvagal perspective. Biological Psychology, response of A‐ and C‐fiber nociceptors in monkey encodes high‐in-
74(2), 116–143. https://doi.org/10.1016/j.biopsycho.2006.06.009 tensity mechanical stimuli. Journal of Neuroscience, 24(19), 4649–
Prossin, A. R., Love, T. M., Koeppe, R. A., Zubieta, J. K., & Silk, 4656. https://doi.org/10.1523/JNEUROSCI.0701-04.2004
K. R. (2010). Dysregulation of regional endogenous opioid Slugg, R. M., Meyer, R. A., & Campbell, J. N. (2000). Response of cuta-
function in borderline personality disorder. American Journal neous A‐ and C‐fiber nociceptors in the monkey to controlled‐force
of Psychiatry, 167(8), 925–933. https ://doi.org/10.1176/appi. stimuli. Journal of Neurophysiology, 83(4), 2179–2191.
ajp.2010.09091348 Sommer, C., & Kress, M. (2004). Recent findings on how proinflam-
Reitz, S., Kluetsch, R., Niedtfeld, I., Knorz, T., Lis, S., Paret, C., … matory cytokines cause pain: Peripheral mechanisms in inflamma-
Schmahl, C. (2015). Incision and stress regulation in borderline tory and neuropathic hyperalgesia. Neuroscience Letters, 361(1–3),
personality disorder: Neurobiological mechanisms of self‐injurious 184–187. https://doi.org/10.1016/j.neulet.2003.12.007
behaviour. British Journal of Psychiatry, 207(2), 165–172. https:// Stiglmayr, C. E., Grathwol, T., Linehan, M. M., Ihorst, G., Fahrenberg,
doi.org/10.1192/bjp.bp.114.153379 J., & Bohus, M. (2005). Aversive tension in patients with bor-
Reitz, S., Krause‐Utz, A., Pogatzki‐Zahn, E. M., Ebner‐Priemer, U., derline personality disorder: a computer-based controlled field
Bohus, M., & Schmahl, C. (2012). Stress regulation and incision study. Acta Psychiatr Scand, 111(5), 372–379. https ://doi.
in borderline personality disorder—A pilot study modeling cutting org/10.1111/j.1600-0447.2004.00466.x.
|
16 SCHLOSS et al.
Stiglmayr, C., Schmahl, C., Bremner, J. D., Bohus, M., & Ebner‐ Zanarini, M. C., Frankenburg, F. R., Reich, D. B., Fitzmaurice, G.,
Priemer, U. (2009). Development and psychometric characteristics Weinberg, I., & Gunderson, J. G. (2008). The 10‐year course of
of the DSS‐4 as a short instrument to assess dissociative experience physically self‐destructive acts reported by borderline patients and
during neuropsychological experiments. Psychopathology, 42(6), axis II comparison subjects. Acta Psychiatrica Scandinavica, 117(3),
370–374. https://doi.org/10.1159/000236908 177–184. https://doi.org/10.1111/j.1600-0447.2008.01155.x
Swannell, S. V., Martin, G. E., Page, A., Hasking, P., & St John, N. J. Zlotnick, C., Mattia, J. I., & Zimmerman, M. (1999). Clinical correlates
(2014). Prevalence of nonsuicidal self‐injury in nonclinical samples: of self‐mutilation in a sample of general psychiatric patients. The
Systematic review, meta‐analysis and meta‐regression. Suicide and Journal of Nervous and Mental Disease, 187(5), 296–301.
Lifethreatening Behavior, 44(3), 273–303. https://doi.org/10.1111/
sltb.12070
Thurauf, N. J., & Washeim, H. A. (2000). The effects of exogenous
analgesia in a patient with borderline personality disorder (BPD) SUPPORTING INFORMATION
and severe self‐injurious behaviour. European Journal of Pain, 4(1),
Additional supporting information may be found online in
107–109. https://doi.org/10.1053/eujp.2000.0161
Weinberg, A., Klonsky, E. D., & Hajcak, G. (2009). Autonomic impair-
the Supporting Information section at the end of the article.
ment in borderline personality disorder: A laboratory investigation.
Brain and Cognition, 71(3), 279–286. https ://doi.org/10.1016/j.
bandc.2009.07.014 How to cite this article: Schloss N, Shabes P, Kuniss
Willis, F., Kuniss, S., Kleindienst, N., Naoum, J., Reitz, S., Boll, S., S, et al. Differential perception of sharp pain in
… Schmahl, C. (2017). The role of nociceptive input and tissue patients with borderline personality disorder. Eur J
injury on stress regulation in borderline personality disorder. Pain. 2019;00:1–16. https://doi.org/10.1002/ejp.1411
Pain, 158(3), 479–487. https ://doi.org/10.1097/j.pain.00000
00000000787