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The Characteristics of Pain Tolerance in Patients Who Underwent Unilateral Breast Cancer Surgery: The Effect of Handedness and Surgical Site to Assess the Potential Musculoskeletal Symptoms and Function

Published:August 05, 2022DOI:https://doi.org/10.1016/j.clbc.2022.08.001

      Abstract

      Background

      Breast cancer survivors (BCS) usually experience musculoskeletal pain and strength imbalance between surgical and nonsurgical sites.

      Material and methods

      This study aimed to assess the effect of handedness and surgical site on pain tolerance and upper extremity strength in BCS. A total of 96 female BCS (Mean age and BMI: 51.06 ± 9.36 years and 27.77 ± 3.75 kg/m2) were included in this study. BCS were categorized as “DoS” or “NoS” whether they had surgery on their dominant or nondominant site, respectively. Socio-demographic data, upper extremity strength, pain tolerance, and pain-related function measurements were performed by simple form, manual muscle tester, pain algometer, and Disabilities of Arm, Shoulder, and Hand's (DASH) pain subscale, respectively.

      Results

      Pain tolerances were significantly lower in upper trapezius muscle region in the surgical site (t = -4,263, P < .001 and t = -2138, P = 0.037) while in the deltoid tuberosity, pain tolerance was significantly higher in surgical site (t = 2633, P = 0.011). Mean differences in strength in shoulder flexion and abduction were significantly lower in the DoS group compared to the NoS group (z = -3.166, P = .002 and z = -2.131, P = .033, respectively), whereas the pain subscale was significantly higher in the DoS (P = .013).

      Conclusion

      Pain tolerance decreased in the upper trapezius muscle region on the surgical site irrespective of the handedness. However, in deltoid tuberosity, the effect of handedness was remarkable. Exercise programs should focus to establish a strength balance in nondominant surgery BCS since strength imbalance might be more prominent to affect them to take part in activities in daily living.

      Keywords

      Introduction

      Breast cancer (BC) is the most common type of cancer among women. The reported incidence of BC reaches nearly 13% globally. Thanks to the advancements in BC treatment and early diagnosis, 5 years survival rate of BC is increased up to nearly 90%.

      Tan, P.H., et al., The 2019 World Health Organization classification of tumours of the breast. 2020.

      In parallel with this, Abraham et al
      • Abraham H.G.
      • Xia Y.
      • Mukherjee B.
      • Merajver S.D.
      Incidence and survival of inflammatory breast cancer between 1973 and 2015 in the SEER database.
      reported that a nearly 40% decrease in mortality is achieved between the ’80s and 2020 in BC. Due to the increased rate of survival, consequences related to the multimodal treatment of BC which might interfere with the functionality and participation of BC survivors take a great majority of interest to improve their activities of daily living and functionality. Researchers reported that 600 million dollars are spent annually associated with BC treatment side effects in which musculoskeletal problems take the lion's share.
      • Rashid N.
      • Koh H.A.
      • Baca H.C.
      • Lin K.J.
      • Malecha S.E.
      • Masaquel A.
      Economic burden related to chemotherapy-related adverse events in patients with metastatic breast cancer in an integrated health care system.
      Since BC treatment is composed of multimodal parameters, their side effects may affect one's functionality by deteriorating their activity and participation. Pain is the most frequent complaint in BC survivors not only during the therapy but also during the completion of initial treatment. Persistent pain is reported as affecting up to 60% of BC survivors.
      • Mejdahl M.K.
      • Andersen K.G.
      • Gärtner R.
      • Kroman N.
      • Kehlet H.
      • et al.
      Persistent pain and sensory disturbances after treatment for breast cancer: six year nationwide follow-up study.
      Studies indicated that pain can be last up to 5 years.
      • Ernst M.F.
      • Voogd A.C.
      • Balder W.
      • Klinkenbijl J.H.
      • Roukema J.A.
      Early and late morbidity associated with axillary levels I–III dissection in breast cancer.
      The burden of persistent pain after BC is also shown as compared to those with low back pain, arthritis, and other painful musculoskeletal problems.
      • Cohen S.P.
      • Vase L.
      • Hooten W.M.
      Chronic pain: an update on burden, best practices, and new advances.
      ,
      • De Groef A.
      • Meeus M.
      • Heathcote L.C.
      • et al.
      Treating persistent pain after breast cancer: practice gaps and future directions.
      Therefore, it is not surprising that physical, mental, and financial burdens and consequences of pain as well as their impact one's quality of life. Not only pain itself, but also other factors such as surgery, adjuvant therapies, and patient characteristics can exacerbate the perceived pain and functional limitation.
      • Hidding J.T.
      • Beurskens C.H.
      • van der Wees P.J.
      • van Laarhoven H.W.
      • Nijhuis-van der Sanden M.W.
      Treatment related impairments in arm and shoulder in patients with breast cancer: a systematic review.
      • Rasmussen G.
      • Madeleine P.
      • Arroyo-Morales M.
      • Voigt M.
      • Kristiansen M.
      Pain sensitivity and shoulder function among breast cancer survivors compared to matched controls: a case-control study.
      • Yang E.J.
      • Park W.B.
      • Seo K.S.
      • Kim S.W.
      • Heo C.Y.
      • Lim J.Y.
      Longitudinal change of treatment-related upper limb dysfunction and its impact on late dysfunction in breast cancer survivors: a prospective cohort study.
      For instance, upper body strength is known to be associated with functional use of the shoulder joint, therefore diminished scapula-humeral interaction might occur due to myofascial pain.
      • Rasmussen G.
      • Madeleine P.
      • Arroyo-Morales M.
      • Voigt M.
      • Kristiansen M.
      Pain sensitivity and shoulder function among breast cancer survivors compared to matched controls: a case-control study.
      In the literature, there are many studies exist investigating the pain parameters in BC survivors. To our knowledge, studies about the effect of surgical as well as dominant sites on function and pain tolerance are needed to enlighten and improve our practice related to BC pain. Since there has been no standard clinical guideline to manage BC pain,
      • De Groef A.
      • Meeus M.
      • Heathcote L.C.
      • et al.
      Treating persistent pain after breast cancer: practice gaps and future directions.
      therefore, we aimed to assess the pain threshold and tolerance of BC survivors specifically focusing on the upper extremity and upper back. As a secondary purpose, we also aimed to know upper extremity strength and pain-related function and their relationship with each other. Our hypothesis was patients who underwent surgery in their dominant site showed higher pain tolerance levels compared to those with nondominant site surgery.

      Methods

      Study Design

      This study was planned as a cross-sectional study. The nonprobability sampling method was used. This study was held between December 2019 and April 2021. All procedures and measurements were performed according to the 1964 Helsinki Declaration and ethical board approval was granted from the Ethical Board of Clinical Research Studies with protocol number 02/11092019. All participants were informed before the enrollment of this study and written informed consent was taken.

      Patients

      Patients who underwent unilateral breast cancer surgery were screened according to the predetermined inclusion and exclusion criteria. Aged over 18 years old, being a volunteer to participate and being a woman, having completed adjuvant therapies prior to participation, and having spent at least 6 months after surgery were set as inclusion criteria. Having active metastasis, bilateral breast surgery, having mental or cognitive disabilities, having orthopedic and/or neurological conditions, and having breast surgery due to aesthetic reasons were set as exclusion criteria.

      Assessment

      Demographic Data Form

      Patients’ clinical and demographic data were gathered via a simple assessment form in which their time and type of surgery, type of axillary procedure, as well as their age, body mass index, drugs, dominant side, etc. were questioned.

      Pain Threshold and Tolerance

      Patients’ pain threshold and tolerance level were measured via the digital algometer (Wagner Force One Model FDIX 50, Wagner Instruments, Greenwich, Conn) which has 1 cm2 round-tipped silicon rubber. Patients were requested to sit in an erect position with their palms over their knees. A soft pen was used to mark predetermined reference points for each side (Figure 1). The reference points were as follows: A1: C5-C6 zygapophyseal joint, A2: Upper Trapezius proximal site, A3: Upper Trapezius middle point, A4: Upper Trapezius lateral site, A5: 4 cm superior of the Tuberositas Deltoidea, A6: The dorsum of the webspace. Prior to the assessment of pain tolerance, pressure sense evaluation was performed as a pain threshold. They were informed and required to say “Yes and/or okay” as soon as they feel pain, immediately, the device recorded that pressure as kilogram-force (kgF). The algometer was applied perpendicular to each reference point. Since it was aimed to prevent incorrect results, the pressure was steadily increased by 1 unit increase for each second.
      • Ylinen J.
      • Nykänen M.
      • Kautiainen H.
      • Häkkinen A.
      Evaluation of repeatability of pressure algometry on the neck muscles for clinical use.
      All measurements were performed on both sides. The pain tolerance value was used for statistical analysis.
      Figure 1
      Figure 1Illustration of the predefined reference points of pain tolerance measurements.

      Manual Muscle Testing

      Shoulder abduction, flexion, and elbow flexion peak muscle force were assessed with a manual muscle dynamometer on both sides (Lafayette Manual Muscle Tester v.01165, Lafayette, USA). Briefly, patients were requested to sit in an erect position in a chair without arm support. Then, their arm was positioned before the measurement. They were required to resist to force applied to them by preserving their position. The force was applied to the distal arm, perpendicularly. Three seconds was set to measure the peak muscle force as newton (N). Three repetitions were performed for each movement on each side by integrating a 10-second resting interval. The mean peak force was calculated as N.
      • Beshay N.
      • Lam P.H.
      • Murrell G.A.
      Assessing the reliability of shoulder strength measurement: hand-held versus fixed dynamometry.

      Pain-Related Function

      Disabilities of arm, shoulder, and hand (DASH) questionnaire was shown as a reliable and valid tool to assess musculoskeletal symptoms of the upper extremity in different situations with a very good test-retest value ranging from 0.92 to 0.96.
      • Drummond A.S.
      • Sampaio R.F.
      • Mancini M.C.
      • Kirkwood R.N.
      • Stamm T.A.
      Linking the disabilities of arm, shoulder, and hand to the international classification of functioning, disability, and health.
      ,
      • Gummesson C.
      • Atroshi I.
      • Ekdahl C.
      The disabilities of the arm, shoulder and hand (DASH) outcome questionnaire: longitudinal construct validity and measuring self-rated health change after surgery.
      Since we aimed to assess pain and related function in this study, we chose to use specifically the DASH pain subscale (items 24-28) to assess the patient's reported upper extremity function associated with pain. Pain, the difficulty of movement, weakness, tingling, and pain during the function in the upper extremity were assessed within a 5-Likert type scale from “1: None” through “5: Extreme”. A higher score indicates worse symptoms or vice versa.
      • Beaton D.E.
      • Katz J.N.
      • Fossel A.H.
      • Wright J.G.
      • Tarasuk V.
      • Bombardier C.
      Measuring the whole or the parts?: validity, reliability, and responsiveness of the disabilities of the arm, shoulder and hand outcome measure in different regions of the upper extremity.
      ,
      • Harrington S.
      • Michener L.A.
      • Kendig T.
      • Miale S.
      • George S.Z.
      Patient-reported upper extremity outcome measures used in breast cancer survivors: a systematic review.

      Statistical Analysis

      The data of patients were shown as mean and standard deviation or number and percent according to the type of data whether continuous or categorical. Normality was assessed with KS-SW normality tests, skewness, and kurtosis. Paired t test was used to assess one's left or right side while an independent t test was used to assess different groups. In case of violated assumptions of normality, nonparametric versions of these tests were used. The alpha level of 0.05 is accepted as statistically significant. Statistical analyses were performed with IBM SPSS version 20.0 (IBM Corporation, Armonk, NY).

      Results

      A total of 96 female breast cancer survivors (BCS) (Mean age and BMI: 51.06 ± 9.36 years and 27.77 ± 3.75 kg/m2) completed all assessments and participated in this study. The right side was dominant for all participants. Fifty-one participants (53.1%) had right-side surgery. Sociodemographic and clinical characteristics of patients are shown in Table 1.
      Table 1Sociodemographic and Clinical Characteristics of Patients
      n = 96n%
      Occupational Status
       Active working1212.5
       Not working8487.5
      Marital Status
       Married8487.5
       Single1212.5
      Type of breast surgery
       Conservative6870.8
       MRM2829.2
      Axillary procedure
       ALND8083.3
       SLNB1616.7
      Chemotherapy
       Yes8285.4
       No1414.6
      Radiotherapy
       Yes9295.8
       No44.2
      Tamoxifen Use
       Yes4445.8
       No5254.2
      Aromatase Inhibitor Use
       Yes4344.8
       No5355.2
      Abbreviations: ALND = Axillary lymph node dissection; MRM = Modified radical mastectomy; SLNB = Sentinel lymph node biopsy.
      Participants who underwent surgery on their dominant side were categorized as “DoS” while who underwent surgery on their nondominant (left) side was categorized as “NoS”. Muscle strengths and pain tolerance were analyzed between the right and left sides within this group. In DoS, the rates of conservative surgery and axillary lymph node dissection (ALND) were 68.6% and 86.3%, respectively. In NoS, those rates were 73.3% and 80%, respectively. Type of surgery and axillary procedure were not found different between NoS and DoS (Chi-Square test, P > .05) as well as age and BMI (Independent samples t test, P > .05).
      The pain tolerance analysis showed that significant differences were obtained in A2, A3, and A5 reference points in the DoS group. In A2 and A3 reference points, pain tolerances were significantly lower in surgical site (t = -4,263, P < .001 and t = -2138, P = .037) while in A5 reference point, pain tolerance was significantly higher in surgical site (t = 2633, P = .011). In the NoS group, pain tolerance was found significantly lower in A3 and A5 reference points on the surgical site. Between-group comparisons (DoS vs. NoS) showed that pain tolerance of the right side was significantly lower in A1, A2 and A6 reference points in DoS group compared to the NoS group (t = -2128, P = .036, t =-2263, P = .026 and t =-2889, P = .005). The pain tolerance of the left side was significantly lower in A1, A4 and A6 reference points in DoS group compared to the NoS group (t = -1978, P = .048, t = -2039, P = .044 and t = -2260, P = .026). Within and between-group comparisons of pain tolerance are shown in Table 2.
      Table 2Within and Between-Group Comparisons Of Pain Tolerance Values of Patients in Predefined Reference Points in Patients With Dominant Side Surgery (DoS) and Those With Nondominant Side Surgery (NoS)
      DoSNoSBetween Groups
      n = 96Right X±SDLeft X±SDtPRight X ± SDLeft X ± SDtPRight t PLeft t P
      A1 (kgF)6.36 ± 2.316.30 ± 2.520,349.7297.43 ± 2.577.27 ± 2.570,692.493-2,128.036-1,978*.048*
      A2 (kgF)5.54 ± 2.276.01 ± 2.30-4,263<.0016.66 ± 2.546.62 ± 2.210,228.821-2,263.026-1,299.197
      A3 (kgF)5.68 ± 2.345.97 ± 2.13-2,138.0376.48 ± 2.266.18 ± 2.052,321.025-1,690.094-0,485.629
      A4 (kgF)5.58 ± 2.175.41 ± 1.981,235.2226.08 ± 2.226.23 ± 1.93-0,941.352-1,095.276-2,039.044
      A5 (kgF)5.32 ± 2.024.99 ± 1.852,633.0116.04 ± 1.855.60 ± 1.642,815.007-1,798.075-1,672.098
      A6 (kgF)5.31 ± 1.565.15 ± 1.721,231.2246.22 ± 1.495.97 ± 1.801,789.081-2,889.005-2,260.026
      Abbreviations: A1 = C5-C6 zygoapophyseal joint; A2 = Upper Trapezius proximal site; A3 = Upper Trapezius middle point; A4 = Upper Trapezius lateral site; A5 = 4 cm superior of the Tuberositas Deltoidea; A6 = The dorsum of the web space; DoS = Patients with dominant side surgery; kgF = kilogram force; NoS = Patients with nondominant side surgery; t = Paired and independent samples t test; X±SD = Mean and standard deviation. P < .05.
      In DoS, shoulder flexion, abduction, and elbow flexion muscle strength were not found different between surgical and nonsurgical sites (paired t test, P > .05). However, in the NoS group, shoulder flexion, abduction, and elbow flexion muscle strength were found significantly lower on the surgical site compared to the nonsurgical side (paired t test, P < .05). Between groups (DoS vs. NoS), shoulder flexion, abduction, and elbow flexion were analyzed separately in right and left sides. There was no significant difference in all muscle strengths (independent samples t test, P > .05) (Table 3).
      Table 3Comparisons of Muscle Strengths in Patients With Dominant Side Surgery (DoS) and Nondominant Side Surgery (NoS) Within and Between Groups
      DoS (n = 51)NoS (n = 45)Between Groups
      n = 96Right X ± SDLeft X ± SDtPRight X ± SDLeft X ± SDtPRight t PLeft t P
      Shoulder Flexion (N)100.59 ± 18.87100.91 ± 18.21-0,195.846104.22 ± 16.9698.57 ± 21.182,803.008-0.972.3340,574.567
      Shoulder Abduction (N)88.40 ± 18.1088.13 ± 16.050,883.88394.81 ± 20.5388.50 ± 18.553,122.003-1,598.114-0,101.920
      Elbow Flexion (N)112.85 ± 21.22111.73 ± 21.250,529.599116.74 ± 21.02111.44 ± 25.252,102.041-0,887.3780.059.953
      DoS = Patients with dominant side surgery; N = Newton; NoS = Patients with nondominant surgery; t = paired and independent samples t test; X±SD = Mean and standard deviation.
      The mean difference of strength between the right and left sides was calculated by subtracting the nondominant side's strength from the dominant side's strength. Mean difference in strength in shoulder flexion and abduction were found significantly lower in the DoS group compared to the NoS group (z = -3.166, P = .002 and z = -2.131, P = .033, respectively) while the mean difference in strength in elbow flexion did not significantly differ between right and left sides (z: -0.981, P = .327). Between-group comparisons of the mean difference in strength between the right and left sides are shown in Table 4.
      Table 4Comparison of Mean Difference of Muscle Strengths Between Patients With Dominant Side Surgery (Dos) and Nondominant Side Surgery (NoS)
      n = 96DoSNoSMedianIQR (25-75)zP
      Shoulder Flexion (N)38.6056.353.50-5.28/10.36-3.166.002
      Shoulder Abduction (N)41.3553.303.53-5.66/12.88-2.131.033
      Wrist Flexion (N)44.4049.903.87-5.33/13.30-0.981.327
      DoS = Patients with dominant side surgery; IQR = Interquartile range; N = Newton; NoS = Patients with nondominant side surgery; z = Mann-Whitney U test.
      DASH pain subscale was found significantly higher in patients who underwent surgery on their dominant side (DoS group) compared to patients who underwent surgery on their nondominant side (NoS group) (12.18 vs. 10, t = 2544, P = .013). Besides, the DASH pain subscale was found to be significantly correlated with both left and right sides’ shoulder flexion and abduction muscle strengths at a low to moderate level (ranged between r = -0.228 and r = -0.326, P < .05) while elbow flexion was not found significantly correlated with DASH pain subscale (P > .05).

      Discussion

      This study showed that patients who underwent breast cancer surgery on their dominant side show less imbalance in shoulder flexion and abduction strength between their upper extremities by a smaller decline in the surgical side's strength compared to patients who underwent breast cancer surgery on their nondominant side. Pain tolerance was also significantly decreased in the upper trapezius muscle region on the surgical side irrespective of the handedness. In addition, it was shown that patients who underwent breast cancer surgery on their dominant side experience more pain in the function compared to those with nondominant side surgery.
      Musculoskeletal pain contributes a considerable amount of pain associated with cancer treatment. Pain related to the musculoskeletal system is generally and specifically localized in the upper extremity and trunk in BC patients.
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      Pain in long-term breast cancer survivors: the role of body mass index, physical activity, and sedentary behavior.
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      Upper-extremity pain disorders in breast cancer.
      Recent studies stated that some mechanisms such as ALND and/or radiotherapy may play a role in central sensitization and therefore pain sensitivity might be increased.
      • Caro-Morán E.
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      Nerve pressure pain hypersensitivity and upper limb mechanosensitivity in breast cancer survivors: a case–control study.
      • Caro-Morán E.
      • Fernández-Lao C.
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      • antarero-Villanueva I.
      • Madeleine P.
      • Arroyo-Morales M.
      Pressure pain sensitivity maps of the neck-shoulder region in breast cancer survivors.
      • Fernandez-Lao C.
      • Cantarero-Villanueva I.
      • Fernández-de-Las-Peñas C.
      • Del-Moral-Avila R.
      • Arendt-Nielsen L.
      • Arroyo-Morales M.
      Myofascial trigger points in neck and shoulder muscles and widespread pressure pain hypersensitivtiy in patients with postmastectomy pain: evidence of peripheral and central sensitization.
      Myofascial trigger points cause dysfunction by creating motor, sensorial and autonomic changes in muscles, and the incidence of myofascial pain was reported between 21% and 45% after BC surgery.
      • Caro-Morán E.
      • Fernández-Lao C.
      • Diaz-Rodriguez L.
      • antarero-Villanueva I.
      • Madeleine P.
      • Arroyo-Morales M.
      Pressure pain sensitivity maps of the neck-shoulder region in breast cancer survivors.
      ,
      • Bron C.
      • Dommerholt J.D.
      Etiology of myofascial trigger points.
      Since the etiology of pain in cancer survivors can be multifactorial, thereby there has been no reported standard evaluation of the pain in cancer survivors. Decreased pain threshold and pain tolerance were reported along the trapezius muscle body in patients who underwent BC surgery compared to the healthy controls.
      • Caro-Morán E.
      • Fernández-Lao C.
      • Diaz-Rodriguez L.
      • antarero-Villanueva I.
      • Madeleine P.
      • Arroyo-Morales M.
      Pressure pain sensitivity maps of the neck-shoulder region in breast cancer survivors.
      In our study, there was no control group. However, we found significantly lower pain tolerance in the upper trapezius proximal and middle points on the surgical side compared to the contralateral side in patients who underwent surgery on their dominant side. In addition, the trapezius middle reference point was also found significantly lower in patients who underwent surgery on their nondominant side. Our findings are compatible with the literature findings. Dibai-Filho et al
      • Dibai-Filho A.V.
      • de Jesus Guirro R.R.
      • Ferreira V.T.K.
      • de Oliveira A.K.
      • de Almeida A.M.
      • de Oliveira Guirro E.C.
      Analysis of chronic myofascial pain in the upper trapezius muscle of breast cancer survivors and women with neck pain.
      reported an exaggerated pain intensity in the upper trapezius muscle in patients who underwent BC surgery compared to patients with chronic neck pain. We are of the opinion that the decreased pain tolerance of the trapezius muscle in patients who underwent BC surgery on their dominant side might be the presignal of the potential shoulder and neck pain. This hypothesis is supported by which is changed in pain pattern is shown as a primary reason for the musculoskeletal system.
      • Binderup A.T.
      • Arendt-Nielsen L.
      • Madeleine P.
      Pressure pain sensitivity maps of the neck-shoulder and the low back regions in men and women.
      Hübscher et al
      • Hübscher M.
      • Moloney N.
      • Leaver A.
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      • McAuley J.H.
      • Refshauge K.M.
      Relationship between quantitative sensory testing and pain or disability in people with spinal pain—a systematic review and meta-analysis.
      reported that the potential pain pattern might be the reason for not only the posture but also the nonspecific neck pain in the future.
      The pain tolerance at the deltoid tuberosity was significantly higher on the surgical site in patients who underwent surgery on their dominant side compared to their contralateral side. While in patients who underwent surgery on their nondominant side, pain tolerance of the same reference point was significantly lower at the surgical site. This result made us think that the pain sensitivity and tolerance did not decrease due to the more frequent use of the dominant extremity of patients in their daily lives despite the surgery, but the decrease in pain tolerance might be more pronounced in the case of the nondominant side involvement. We think that with these results the effects of handedness on pain sensitization and tolerance are shown. Nonetheless, it should also be noted that patients after BC surgery generally avoid using their affected extremities due to the fear of lymphedema and, a protective behavior might occur which affects upper extremities. This situation may change the pain perception and sensitivity in the affected region, especially in the trapezius and neck muscles. In this regard, there were no significant differences between the surgical and nonsurgical sides in zygapophyseal joint reference points for both patients who underwent surgery on their dominant side and who underwent surgery on their nondominant side. However, group comparisons showed significant differences in both dominant and nondominant sites separately. Patients who underwent surgery in their dominant site showed significantly lower pain tolerance in both extremities compared to patients who underwent surgery in their nondominant site in A1, A4, and A6 reference points. This result might help to show the marked potential effect of pain sensitization on pain tolerance regarding handedness. On the other hand, especially at the A6 point which is the farthest point of the surgery, is important to show the pain perception with the decreased pain tolerance in patients who underwent BC surgery on their dominant side. Our findings are parallel with the findings of Caro Moran et al
      • Caro-Morán E.
      • Fernández-Lao C.
      • Diaz-Rodriguez L.
      • antarero-Villanueva I.
      • Madeleine P.
      • Arroyo-Morales M.
      Pressure pain sensitivity maps of the neck-shoulder region in breast cancer survivors.
      whose findings also showed insignificant differences in the neck region while in reference points in the trapezius muscle, they also reported significant differences compared to affected and nonaffected sites. Fernandez Lao et al
      • Fernandez-Lao C.
      • Cantarero-Villanueva I.
      • Fernández-de-Las-Peñas C.
      • Del-Moral-Avila R.
      • Arendt-Nielsen L.
      • Arroyo-Morales M.
      Myofascial trigger points in neck and shoulder muscles and widespread pressure pain hypersensitivtiy in patients with postmastectomy pain: evidence of peripheral and central sensitization.
      also reported the bilaterally decreased pain thresholds in the reference points at the zygapophyseal joint in patients who underwent mastectomy compared to the healthy matches. Yet, their sample consisted of only patients with mastectomy.
      Patients who underwent BC surgery could experience a broad spectrum of musculoskeletal symptoms. It was reported that 62% of patients still experience surgery-related musculoskeletal symptoms 1 year later after completion of the primary treatment which is reported to be experienceable even 6 years later.
      • Schmitz K.H.
      • Prosnitz R.G.
      • Schwartz A.L.
      • Carver J.R.
      Prospective surveillance and management of cardiac toxicity and health in breast cancer survivors.
      Hidding et al
      • Hidding J.T.
      • Beurskens C.H.
      • van der Wees P.J.
      • van Laarhoven H.W.
      • Nijhuis-van der Sanden M.W.
      Treatment related impairments in arm and shoulder in patients with breast cancer: a systematic review.
      reported that one 1 in every 4 women faces muscle weakness in their affected shoulder. In our study, patients who underwent surgery on their dominant side showed no difference in muscle strength compared to their contralateral sides. This result can be interpreted as patients who use their dominant extremity in their daily life despite the surgery might have maintained their muscle strength. On the contrary, patients who underwent surgery on their nondominant side showed a significant decrease in muscle strength compared to their contralateral sides. However, it should be taken into account that patients who underwent surgery from their nondominant side may neglect to use their extremities more. Besides, patients who underwent surgery on their nondominant side may experience more problematic results, especially in functional movements that require bilateral participation during activity. Our findings are parallel with the literature findings. Merchant et al
      • Merchant C.
      • Chapman T.
      • Kilbreath S.
      • Refshauge K.
      • Krupa K.
      Decreased muscle strength following management of breast cancer.
      reported no significant difference in the strength of shoulder flexion in patients who underwent surgery on their dominant side. Hidding et al
      • Hidding J.T.
      • Beurskens C.H.
      • van der Wees P.J.
      • van Laarhoven H.W.
      • Nijhuis-van der Sanden M.W.
      Treatment related impairments in arm and shoulder in patients with breast cancer: a systematic review.
      reported the highest decrease in muscle strength to occur in the first year of the completion of the treatment. Yet roughly 20% of our sample were in the first year of the completion of primary treatment. Therefore, the insignificant difference in muscle strength between the extremities in patients who underwent surgery on their dominant side might be explained in this way. In addition, when the right and left sides were analyzed separately between DoS and NoS groups, there was no significant difference. We think when planning the physiotherapy program for patients who underwent surgery on the nondominant side, bilateral activities and exercises especially resistant strengthening exercises for the nondominant side should be used more intensively not only to prevent functional and activity limitations but also to improve clinical outcomes compared to patients who underwent surgery in their dominant side.
      This study has some strengths and limitations. Firstly, we did not evaluate the previous and/or active neck pain status of our patients with a scale or numeric rating scale compared to previous studies in the literature. In addition, we did not use a strict grid measure template to measure pressure pain tolerance in our patients nor did we perform a mapping of the distribution of pain. Since our sample consisted of the mostly homogenous Caucasian race, the generalizability of the results might be disputable. However, we determined our reference points based on the previous works. Relatively large sample size and detailed follow-up of patients within a multidisciplinary team approach for the inclusion process can be thought of as strengths. However, further studies should include functional and performance-based evaluations along with pressure pain measurements.

      Conclusion

      Not only regional but also widespread musculoskeletal pain in patients who underwent BC surgery is a common and debilitating problem among BC patients. To prevent musculoskeletal symptoms which could interfere with their activities in daily life as well as improve shoulder function, a detailed examination of the pain characteristics and pain perceptions of muscles in these patient cohorts might give a remarkable insight into the understanding of the basis of the problem. Our findings revealed that patients who underwent BC surgery in their dominant site should be assessed in detail regarding the potential nonspecific shoulder and neck pain compared to the patients who underwent BC surgery in their nondominant site. Whereas patient-specific strengthening exercise program in which bilateral participation activities should take part must be established in patients who underwent surgery in their nondominant site due to imbalance in shoulder muscle strength might be more prominent to affect them to take part in activities in daily living.

      Clinical Practice Points

      • What is already known about this subject?
      • Pain is a well-known consequence of breast cancer treatment. Breast cancer survivors suffer from pain not only during active treatment but also after the completion of primary treatment. Participation in daily living decreases due to pain during function. Musculoskeletal pain due to multimodal breast cancer treatment might build a basis for future nonspecific neck and upper back pain.
      • What are the new findings?
      • Though decreased pain tolerance of upper trapezius muscle in the surgical site is known, this study highlights the higher pain tolerance in the deltoid tuberosity region in the surgical site despite surgery. Breast cancer survivors who had surgery on their nondominant site experience more strength imbalance between their upper extremities.
      • How might it impact clinical practice in the foreseeable future?
      • Decreased pain tolerance in the upper trapezius region might be the preliminary base for nonspecific neck and upper back pain in breast cancer survivors. Examining the myofascial pain characteristics as early as possible might provide a preventive nature of diminished function in this patient cohort. In addition, breast cancer survivors who had surgery in their nondominant site should be followed and monitored closely to prevent strength imbalance due to bilateral participation of both extremities is needed in most daily functional activities.

      Author Contributions

      All authors contributed to the study's conception and design. Material preparation and data collection were performed by Alper Tuğral, Yeşim Bakar and Murat Akyol. Statistical analysis was performed by Alper Tuğral. The first draft of the manuscript was written by Alper Tuğral and Yeşim Bakar. All authors commented on previous versions of the manuscript and all authors read and approved the final manuscript.

      Acknowledgments

      The authors would like to thank patients who voluntarily participated in this study.

      Disclosure

      The authors declare that no funds, grants, or other support were received during the preparation of this manuscript. The authors declare that there is no conflict of interest.

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