The Breast 23 (2014) 836e843

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Original article

Axillary web syndrome self-assessment questionnaire: Initial development and validation Luiz Felipe Nevola Teixeira a, *, Paolo Veronesi b, Visnu Lohsiriwat c, Alberto Luini b, Mario Casales Schorr d, Cristina Garusi e, Maria Claudia Simoncini a, Luis Otavio Zanatta Sarian f, Sara Gandini g, Fabio Sandrin a, Mario Rietjens e a

Physiotherapy Department, European Institute of Oncology, Via Ripamonti 435, 20141, Milan, Italy Breast Surgery Unit, European Institute of Oncology, Via Ripamonti 435, 20141, Milan, Italy Department of Surgery, Mahidol University School of Medicine, 2 Prannok Rd., Bangkoknoi, Bangkok, 10700, Thailand d Porto Alegre Federal Health Science University, Sarmento Leite St., 245, CEP 90050-170, Porto Alegre, Brazil e Plastic and Reconstructive Surgery Unit, European Institute of Oncology, Via Giusepe Ripamonti, 435, 20141, Milan, Italy f Medical Sciences Departament, University of Campinas, Zeferino Vaz St., Cidade Universitaria, Campinas, 13083-970, Brazil g Division of Epidemiology and Biostatistics, European Institute of Oncology, Via Ripamonti 435, 20141, Milan, Italy b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 8 February 2014 Received in revised form 20 May 2014 Accepted 5 September 2014 Available online 26 September 2014

Introduction: Despite the great strides made in medical knowledge, surgery still remains a necessary part of the breast cancer treatment. Surgical procedures still lead to post surgical sequelae. The axillary web syndrome (AWS) is one such sequela, which can lead to disability, reduced arm mobility and compromised quality of life. It is often unidentified and the literature regarding its assessment is limited. To improve diagnosis and patient education, the Screening Test AWS (ST-AWS) questionnaire was drafted and applied at the European Institute of Oncology (EIO). Materials and method: We prospectively recruited patients from October 2012 to December 2012. Patients who underwent sentinel lymph node biopsy and/or axillary dissection procedures were registered. Physical examination was set as a gold standard. Results: 88 patients completed the questionnaire. Among these, 32 patients had axillary web syndrome diagnosed, thus a 36% incidence. The questionnaire achieved a sensitivity of 94%, a specificity of 91%, a positive prevalence value (PPV) of 86%, a negative prevalence value (NPV) of 96% and an accuracy of 92%. Conclusion: Our questionnaire achieves high sensitivity and predictive values, and we would recommend it as a screening-tool for auto-diagnosis of the AWS. The main objective of the questionnaire is to enhance patient and therapist awareness of the problem, and prompt management to shorten the effects of this disability. Moreover, it may offer a tool to enhance body image acceptance after surgery. Further studies whereby the efficacy of the questionnaire is investigated in a larger, heterogeneous group and in different situations are warranted. © 2014 Elsevier Ltd. All rights reserved.

Keywords: Breast neoplasms Breast reconstruction Lymph node dissection Physiotherapy Rehabilitation

Introduction Despite advances in medical knowledge and technology, surgery remains a necessary procedure within the breast cancer treatment protocol [1e5]. Even with the employment of less aggressive techniques, surgery still leads to post-surgical sequelae and

* Corresponding author. Tel.: þ39 0257489747; fax: þ39 0257489208. E-mail addresses: [email protected], [email protected] (L.F. Nevola Teixeira). http://dx.doi.org/10.1016/j.breast.2014.09.001 0960-9776/© 2014 Elsevier Ltd. All rights reserved.

complications [3,6]. The axillary web syndrome (AWS) is one such sequela that can involve disability, reduced arm mobility and a decreased quality of life. It is often unidentified and the literature regarding its assessment and management consensus is limited [7e14]. Currently, there is no diagnostic tool such as a self-validated questionnaire to detect AWS, which may help the patient with immediate treatment. To improve diagnosis and patient education, a new questionnaire, the Screening Test AWS (ST-AWS) was designed and applied at the European Institute of Oncology (EIO), where patients performed a self-assessment to discover the presence of the syndrome.

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The objective of the study is to build and initiate a validation process of the questionnaire in order to provide an adjunct diagnostic tool which patients and therapists may find useful for selfassessment of the axillary web syndrome and for educating patients to seek help for their symptoms. Materials and method We prospectively recruited patients from October 2012 to December 2012. Patients who underwent ipsilateral sentinel lymph node biopsy and patients with axillary dissection procedures were both enrolled. The questionnaire was provided to the patients during the post-surgery examination after completion of an informed consent. From the 108 patients initially recruited, 20 patients were excluded because they did not sign the consent forms to participate in the study, were unable to answer the questionnaire independently or had undergone autologous flap reconstruction. The Local Ethical Committee approved the study and the patients gave their written informed written consent. Questionnaire development On the basis of clinical experience and analysis of the literature, we compiled an initial list of signs and symptoms associated with AWS. The questionnaire derived from this list, called ST-AWS1, included a series of 4 questions. This provisional questionnaire was used on patients in order to observe the feasibility of the questionnaire and assess whether patients were able to fill in the form and understand the questions. To improve the quality of the questionnaire and receive feedback and review from our target public we use the “Face validity” method [15], sending out educational information to patients and also to 50 experts in oncological area with instructions on how to answer the questions. The experts comprised nurses, plastic and breast surgeons, physiotherapists, biostatisticians and clinical oncologists. The critiques provided by this group enabled us to highlight points that needed to be changed in the questionnaire and develop a second version. Our operator checklist was approved for every face validity experts, so we chose to not do make any changes to it. We started an initial pilot trial with 35 patients who underwent axillary dissection or sentinel lymph node biopsy and were present in the physiotherapy clinic and in the post-surgery medication clinic. The patients were instructed to answer the questionnaire before the physical evaluation. After evaluating the patient, the therapist completed the checklist and finally the answers of both questionnaire and checklist were compared to assess whether or not axillary web syndrome was present, and the efficacy of the tool. Based on the responses, it was decided to make further changes to the questionnaire, indicating more clearly, by means of a drawing, the area of the body where the syndrome appears. We also include pictures showing how the syndrome visually looks like and figures showing how to perform the arm movement during the test. This led to the subsequent drafting of a third questionnaire, which was completed by 40 patients in a second pilot test. The results obtained in this phase were promising: the sensitivity of the test was 94.74% and specificity of 85% 3 false positives (7%), 1 false negative (2%), 18 patients diagnosed with AWS (45%), 17 patients diagnosed without AWS (43%) and 1 patient excluded because bleeding during the assessment (3%). However, it was decided to make further changes to the questionnaire and healthcare worker’ checklist in order to confirm and possibly further increase the sensitivity by more specific questions and representative images. A fifth question was added, in order to try to reduce the false positive results, which are usually masked by

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the swelling felling in the armpit or breast in patients who had undergone oncological breast surgery. ST-AWS questionnaire All patients had to complete the final questionnaire after medical examination. This consists of five questions about the perception of arm movement; feeling of tension; visual and tactile perception of the axillary web and edema sensation in the breast or armpit. Questions regarding range of motion, visual and tactile perception of the AWS, and feeling of tension of score one point in the case of positive response. The question regarding swelling sensation in the axilla has a reversed score, scoring one point in case of negative response. If the score was greater than three, this was considered indicative of the presence of the syndrome. A score of three were considered suspect, while less than three was considered not indicative of AWS. Every patient diagnosed with the axillary web syndrome received clear and precise indications to proceed with the treatment after final participation in our study (Figs. 1e4). Physiotherapy evaluation (gold standard) During the medical examination, the patients were evaluated by a physiotherapist (LFNT), as physical examination being considered as the only gold standard for AWS diagnosis [7].

Fig. 1. ST-AWS questionnaire page 1

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Fig. 2. ST-AWS questionnaire page 2

The same physiotherapist performed the evaluation during the study. Range of motion (ROM) of the operated side was compared with the contralateral arm ROM; the tactile and visual signs of the axillary web syndrome; subjective feeling of tension during the movement in the maximal range of motion; signs of swelling in the arm pit and any sensitivity loss or disturbances were evaluated and the answers were recorded by means of a physiotherapeutic check list. Information regarding patients and tumor characteristics, pre surgery and post surgery, were collected. Patient answers and therapist checklist results on AWS assessment were then registered, compared and input into a database by a second therapist. Statistical methods Sample-size calculations In order to validate the self-assessment questionnaire of AWS we recruited 88 patients. Sample-size estimation was conducted based on the results obtained in the pilot study. A sample size of 88 achieves 94% power to detect a difference (P0-PB) of 2% using a one-sided binomial test

[16e18]. The actual significance level achieved by this test is 5%. These results assume a baseline proportion (PB) of 95% and assume that the actual proportion (P1) is 99%. The maximum value that is still considered unimportant is 93%. PB is the baseline or standard value of the proportion. P0 is the smallest proportion, which is still considered equivalent to PB. P1 is the value of the proportion under the alternative hypothesis. Statistical analysis Descriptive characteristics of the patients, types of surgery, history of disease and cancer features are presented as frequencies by ASW status, assessed by the therapist. Concurrent validity was estimated from how well the participant's self-reported symptoms corresponded with those assessed by the therapist. Because the criterion variable of symptom was dichotomized (presence or absence), a logistic regression was used to model the ability of ST-AWS to predict symptom diagnosis. Odds ratio (OR), adjusted for confounders were calculated. The sensitivity and specificity was given on scale of 0e100%. The score of the questionnaire was also tested against the presence or absence of the corresponding symptom by the

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Fig. 3. ST-AWS questionnaire page 3

therapist. The ability of ST-AWS considered as a score to discriminate positive from negative diagnosis of a therapist was estimated with receiver operating characteristics (ROC) analysis. An area under the curve (AUC) with a value greater that 0.8 was considered a good predictive ability of the questionnaire. Results Eighty-eight patients completed the questionnaire and the physical examinations. Among them, 32 patients (36%) had a diagnosis of AWS. The median age was 51 years old (range of 22e78) (Flowchart). A history of previous surgery and history of shoulder joint morbidity, previous evaluated by an external observer, were not significantly associated with the incidence of axillary web syndrome. Educational level and age were also not significantly associated with AWS. On the other hand body mass index (BMI) was an important feature: patients with AWS are significantly thinner (p ¼ 0.006). Types of breast surgery (quadrantectomy or mastectomy) and axillary surgery (axillary dissection or sentinel lymph node biopsy) were not relevant for AWS

incidence. However AWS was more frequent in plastic surgery reconstruction patients (p ¼ 0.02) and they also more frequent have in patients with greater length in time of surgery (p ¼ 0.05). The lost of sensitivity in the arm or chest wall was also significantly more greatly associated with this syndrome (47% of patients with AWS had lost of sensibility versus 16% of ‘no AWS’; p ¼ 0.002) (Table 1). The questionnaire achieved a sensitivity of 94%, a specificity of 91%, a positive predictive value (PPV) of 86%, negative predicted value (NPV) of 96% and an accuracy of 92% (Table 2). The OR for the ST-AWS score was highly significant: OR ¼ 5.9 (95%CI: 3.0,11.6) and p < 0.000. The area under the curve was 0.95 (Fig. 5). Plastic surgery reconstruction, lost of sensitivity, cancer stage, age and education of the patients did not influence the answers of the questionnaire nor they influence between self-assessment and the therapist evaluation. Discussion Our questionnaire was designed to provide an easy tool for the patients self-assessment and self diagnoses of axillary web

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Fig. 4. ST-AWS questionnaire page 4

syndrome, providing education about signs and symptoms and reducing the time between the diagnoses and treatment, avoiding pain and change in motor patterns. The results in sensitivity (94%), specificity (91%) and accuracy (92%), show that the questionnaire can provide a sensitive tool to detect the syndrome. During our study, we found two false negative results from patients with no symptoms at all but with clinical signs of the syndrome. Even with a false result in the questionnaire, the asymptomatic patients did not have any pain or range of motion restrictions that could lead to articular and muscular problems. Such patients should be stimulated to move the arm in daily activities and be re-evaluated if any symptoms appear. The five false positive cases were found in patients with difficulties in the area of body image acceptance after surgery. The questionnaire encourages the patients to touch and look at the surgery site. Even so, should the problem persist, psychological help could minimize this problem, enhancing the quality of life of these patients [19]. We found that 34% of our sample suffered from axillary web syndrome after surgery, in which 63% of them had undergone

axillary dissection while 37% has undergone sentinel lymph node biopsy. These numbers are compatible with those found in the literature concerning the incidence, based on large populations [7,14]. The causes of axillary web syndrome are not yet completely explicable and the most accepted theory is based on a lymphothrombophlebitis of lymphatic and blood vessels during axillary dissection or sentinel lymph node biopsy. Recently, Rashtak et al. [12]. reported a histopathological findings of axillary cord after axillary furunculosis. The specific marker for lymphatic endothelium, D2-40, was found positive stained in the band of axillary cord. This findings support the theory that the etiology of the ‘cord’ is the lymphatic origin. Findings aimed at breast cancer patients are still warranted to determine the hypothesis accurately. Previous analyses confirmed our results on the association between BMI and AWS as seen in Bergman et al. [7] and Torres et al. [14] Slimmer patients are more frequently diagnosed with AWS since the cord is more readily observed when the underarm region does not have excessive fat tissue. We took this factor into consideration when developing our questionnaire, deciding upon

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Fig. 5. ROC Curve from the data Analyzed

issues that could lead to the syndrome being detected even in overweight patients, since clinical experience has shown us that in high body mass index patients the axillary web syndrome can prove difficult to assess. In the questionnaire, items pertaining to surgery, length of surgery and reconstruction had a significant statistical association with AWS. Once the reconstruction leads to a longer and more invasive surgery, these items could be correlated. The current articles in literature regarding axillary web syndrome did not included patients who underwent immediate reconstructive surgery [7,14]. The loss of sensitivity item could be an important factor in misdiagnosing the syndrome. This could be explained by intercostobrachial nerve injury during axillary surgery, which can lead to a loss of sensitivity or paresthesia in the arm and chest wall, which is immediately noticeable post-surgery. Patients who

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suffer from this injury tend to report a reduced sensitivity, especially in the medial internal part of the injured arm, leading to misinterpretation of proprioceptive stimuli in that area. Studies have indicated that the incidence of the deficit is high and the sequelae not permanent [20e22]. For these patients, an explanation by the therapist about the causes is important in reducing the patient's fears and insecurity. Patients diagnosed with or without loss of sensitivity and without AWS are also advised to repeat the questionnaire over the following six weeks, in order to respect the AWS insurgence period and enhance the diagnoses [23,24]. Fortunately neither loss of sensitivity, BMI, nor reconstruction surgery significantly affects the validity of the self-assessment. Axillary web syndrome therapeutic rehabilitative protocols are varied without international standardized protocol and mostly based in case reports. The wide range of therapeutic modalities can be varied from no treatment given, patient education, NSAIDs and analgesic local treatment, active and passive stretching, skin traction technique, hooking technique, and even some patients were offered radiation and surgical options in concomitant with rehabilitative protocols. At EIO, we are validating and setting a clinical trial in order to deliver a rehabilitative protocol for AWS treatment. Early diagnosis, which definitely leads to early rehabilitative therapy, plays an important role in prognosis and outcome of AWS treatment [7,14]. We acknowledge that there were some limitations in our study as it was an initial questionnaire validation. Although our group size is not sufficiently large to clarify the incidence of the syndrome, nevertheless the numbers were compatible with some of the studies conducted with large populations. The fact that the questionnaire was compiled by the patients simultaneously with the sign up for enrollment, in the presence of the researcher and waiting for the medical appointment lead us to believe that different results would be obtained if the patients had completed the questionnaire at home. Future studies assessing the efficacy of the questionnaire in larger groups and different groups of patients who have undergone oncological surgery are necessary. Conclusion Our questionnaire achieves high sensitivity and predictive values, and we recommend it as a screening tool for self-

Flowchart. Participants' progress through the phases of the study.

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Table 1 Patient characteristics, types of surgery and cancer features by AWS assessment of the therapist. Categories All Age* Educational level BMI

Previous articular problems Previous breast surgery Neoadjuvant treatment Time of surgery min.* Reconstruction Reconstruction type Time between surgery e visit Breast surgery Axillary surgery

Lymph nodes removed (BLS) n T stage

N stage

Sensitivity loss

25 Yes No Yes No Yes No 119 >119 Yes No Prothesys Expander 2 Tx Tis T0 T1 T2 T3 0 1 2 3 Yes No

AWS (%)

NO AWS (%)

32 19 13 28 4 5 22 5 1 31 2 30 2 30 12 20 25 7 10 14 16 16 25 7 20 12

(100%) (59) (41) (88) (12) (16) (68) (16) (3) (97) (6) (94) (6) (94) (37) (63) (78) (22) (42) (58) (50) (50) (78) (22) (63) (37)

56 24 32 42 14 0 32 24 1 55 6 50 8 48 33 23 29 27 14 14 28 28 34 22 29 27

(100%) (43) (57) (75) (25) (0) (57) (43) (2) (98) (11) (89) (15) (85) (59) (41) (52) (48) (50) (50) (50) (50) (61) (39) (52) (48)

8 4 0 3 1 8 17 3 9 15 2 6 15 17

(67) (33) (0) (9) (3) (25) (54) (9) (28) (47) (6) (19) (47) (53)

21 6 2 3 1 23 22 5 25 16 10 5 9 47

(78) (22) (4) (5) (2) (41) (39) (9) (45) (28) (18) (9) (16) (84)

p-Value*

0.14 0.16 0.006

0.69

0.25

Acknowledgments

0.05

The author would like to thank the Umberto Veronesi Foundation for the 2013 fellowship grant.

0.02 0.55

References

1.00 0.10 0.33

0.69 0.67

0.07

0.002

assessment of the axillary web syndrome. Nevertheless, the results of the ST-AWS should be confirmed by a physiotherapy examination. The main objective of the questionnaire is to enhance patient and therapist awareness about the problem, thereby leading to prompt management in order to shorten this disability. Moreover, it may offer a tool to improve education and body image acceptance after surgery. Further studies, for the reproducibility of the questionnaire in a bigger, heterogeneous group and in different post surgery situations are undoubtedly warranted.

Table 2 Comparing physical evaluation and axillary web syndrome and questionnaire answers.

Negative Positive Total

We report no conflict if interest, all authors of the manuscript and I have contributed significantly to and share in the responsibility for the release of any part or all of the material contained within the article noted above. All Authors stipulated that the material described in this paper is new, original and has not been submitted to another publication for concurrent consideration. We further attest that we have herein disclosed any and financial or other relationships which could be construed as a conflict of interests and that all sources of financial support for this study have been disclosed.

0.48

* Data in italics shows significance at 0.05 level.

Questionnaire

Conflict of interest statement

Physical evaluation (gold standard) Negative

Positive

Total

51 5 56

2 30 32

53 35 88

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Axillary web syndrome self-assessment questionnaire: Initial development and validation.

Despite the great strides made in medical knowledge, surgery still remains a necessary part of the breast cancer treatment. Surgical procedures still ...
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