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The relationship between malignant wound status and pain in breast cancer patients
European Journal of Oncology Nursing 24 (2016) 8e12
Contents lists available at ScienceDirect
European Journal of Oncology Nursing journal homepage: www.elsevier.com/locate/ejon
The relationship between malignant wound status and pain in breast cancer patients Nao Tamai a, Yuko Mugita a, Mari Ikeda b, Hiromi Sanada a, * a Department of Gerontological Nursing/Wound Care Management, Division of Health Sciences and Nursing, Graduate School of Medicine, The University of Tokyo, 113-0033, 7-3-1 Hongo, Bunkyo-ku, Tokyo, Japan b Department of Nursing Administration and Advanced Clinical Nursing, Division of Health Sciences and Nursing, Graduate School of Medicine, The University of Tokyo, 113-0033, 7-3-1 Hongo, Bunkyo-ku, Tokyo, Japan
a r t i c l e i n f o
a b s t r a c t
Article history: Received 10 August 2015 Received in revised form 15 May 2016 Accepted 23 May 2016
Purpose: Skin metastasis is one of the most frequent metastases in breast cancer patients. Patients with malignant wounds experience numerous symptoms, including serious wound pain. However, the features of pain related to malignant wounds have not been investigated. Nurses can experience a dilemma when treating these patients due to a lack of knowledge of the pain. The aims of this study were to examine the quality and intensity of malignant wound pain and to determine the association between wound status and pain in the patients with malignant wounds. Methods: Cross-sectional study was conducted. Participants were recruited from a breast centre based in a general hospital. We collected the patients’ demographic and wound management data and assessed wound condition. Patients evaluated wound pain intensity and quality over the preceding week using the short-form McGill Pain Questionnaire (SF-MPQ). The association between SF-MPQ results, wound condition, and the time interval for wound care was evaluated using the Spearman’s correlation coefficient. The protocol was approved by the Ethical Committee of the each facilities. Results: The median age of the 22 enrolled patients was 61.5 years, and the median time after diagnosis of malignant wound was 15.5 months. Overall, 77.3% of patients complained of pain. Malignant wound pain significantly correlated with the degradation of wound edges, granulation tissue, and the time interval for wound care. Conclusion: We consider that it is necessary to provide pain-control care focused on the wound edge and granulation tissue of malignant wounds through the assessment of malignant wound pain and condition. © 2016 Published by Elsevier Ltd.
Keywords: Exudate Granulation tissue Malignant fungating wound Short-form McGill pain questionnaire Wound care
1. Introduction Breast cancer incidence increases annually worldwide, and it is a primary cancer among women (Ito et al., 2009). Breast cancer may metastasise to the lung, liver, bone, brain, and skin, with especially high rates of metastasis to skin sites (Elder et al., 2006). These skin metastases are called malignant wounds. Malignant wounds can be caused by direct invasion of the skin by cancer or by metastasis to the skin. These wounds have both ulcerative or fungating features. Patients with malignant wounds can develop numerous symptoms, including pain, exudate, infection, odour, and bleeding, which cause psychological distress (Gibson and Green, 2013; Maida et al.,
* Corresponding author. E-mail address: [email protected] (H. Sanada). http://dx.doi.org/10.1016/j.ejon.2016.05.004 1462-3889/© 2016 Published by Elsevier Ltd.
2009; Merz et al., 2001; Naylor, 2002; Probst et al., 2009; Schulz et al., 2002). Therefore, comprehensive palliative care to control these symptoms is needed for patients with malignant wounds, from treatment, follow-up care, and end-of-life care. Probst et al. reported that 50% of patients with malignant wounds needed to manage their pain. The causes of pain in breast cancer patients with malignant wounds were assumed to be the progression of cancer, infection, and peri-wound dermatitis caused by wound exudate. However, the features of pain related to malignant wounds in breast cancer patients have not been investigated. Nurses can experience a dilemma when treating these patients due to a lack of knowledge of the pain, thereby potentially providing insufficient management of wounds. Recently, a short form of the McGill Pain Questionnaire (SF-MPQ) has been used to evaluate various types of pain. A Japanese version of the SF-MPQ is available (Yamaguchi et al., 2007). It is a self-report questionnaire
N. Tamai et al. / European Journal of Oncology Nursing 24 (2016) 8e12
consisting of three major dimensions e sensory, affective, and total descriptors. Because the SF-MPQ provides qualitative and quantitative information, it may help nurses to understand more fully the quality and/or intensity of the malignant wound pain in breast cancer patients (Lo et al., 2012). The aims of this study were to examine the quality and intensity of pain and to determine the association between wound status and pain in breast cancer patients with malignant wounds. 2. Methods 2.1. Study design and participants A cross-sectional study was conducted. Participants were recruited from the outpatient department of a breast centre based in a general hospital in Japan between February 2010 and June 2011. Inclusion criteria were participants over 18 years of age presenting with a breast malignant wound. Patients with breast malignant wounds were diagnosed by the criteria of the hospital, which were (i) skin invasion near the breast cancer site or (ii) pathology reports from a breast tissue sample (oestrogen receptor, progesterone receptor, and human epidermal growth factor receptor type 2 [HER2] proteins). Exclusion criteria were participants in critical condition, as determined by physicians. Patients received standard wound management by nurses certified in wound, ostomy, and continence nursing or cancer pain management nursing in the hospital. The protocol was approved by the local Ethical Committees of our institution and an affiliated hospital. Written informed consent was obtained from all the participants. 2.2. Data collection Demographic characteristics were collected from medical records by the lead researcher and included the following: age, hormone receptors, HER2 proteins status, time after diagnosis of breast cancer, time after diagnosis of malignant wound, location of malignant wounds, metastatic site, treatments, administration of analgesic drugs, wound management, performance status, and comorbidity. Performance status by Eastern Cooperative Oncology Group as rated from 0 to 4, with 0 denoting perfect health and 4 indicated patients who were bedbound (Ando et al., 2001; Oken et al., 1982). The patients provided malignant wound care on an outpatient basis. During wound care, the lead researcher assessed the wound and the condition of the surrounding skin by visual inspection and palpation (pressing down with a finger and pinching of tissues), using the Bates-Jensen wound assessment tool (BWAT) and DESIGN (Bates-Jensen et al., 1992; Sussman and Bates-Jensen, 2007). BWAT evaluates 13 wound characteristics, including wound size, depth, edges, undermining, necrotic tissue type and amount, exudate type and amount, skin colour surrounding the wound, peripheral tissue oedema and induration, granulation tissue, and epithelialization, with a numerical rating scale. Induration is abnormal firmness of peri-wound. A high score indicates a severe condition. The reliability and validity of this tool have been verified (Bates-Jensen et al., 1992). DESIGN is a tool for scoring the severity of wounds, including pressure ulcers. It was developed by the Scientific Education Committee of the Japanese Society of Pressure Ulcers in 2002. DESIGN consists of seven components: depth, exudate, size, inflammation/infection, granulation tissue, necrotic tissue, and pockets (undermining). The total score is calculated, and a high score indicates greater severity. The reliability and validity of DESIGN have been shown (Sanada et al., 2004). The BWAT total score was positively correlated with DESIGN-R total score (r ¼ 0.89, P < 0.0001). In this study, the inter-rater reliability of BWAT score
9
was evaluated with separate raters (a plastic surgeon, a wound care nurse, and the lead researcher). The raters were assessed by calculating the rate of agreement on scores for photographs of malignant wounds (k ¼ 0.72e0.91 for each item). During wound care, digital photographs of the wound and periwound skin were taken with a digital camera (COOLPIX, NIKON, Tokyo, Japan). Wound size on the digital photograph was measured three times using the ImageJ software program (National Institutes of Health, Maryland, USA), and the median value was used for analysis. We interviewed patients about wound management (time interval to exchange dressings) related to wound pain. After wound care by the lead researcher, the patients answered the questionnaire related to their wound pain intensity and quality using the SF-MPQ. The SF-MPQ is the most widely used tool for assessing pain experience. Participants evaluated the SF-MPQ by rating the intensity and quality to which they experienced the average wound pain in the past week. The main component of the SF-MPQ consists of 15 descriptors (11 sensory and 4 affective) rated on a 4-point intensity scale (0 ¼ “none” to 3 ¼ “severe”). The SFMPQ also includes a 6-point present pain index (PPI) and a visual analogue scale (VAS), which measure overall pain intensity as a single dimension (Melzack, 1987). The reliability and validity of SFMPQ Japanese version have been shown (Yamaguchi et al., 2007). 2.3. Statistical analysis Data are presented as the median (range) or the number with percentage (%). The strength of the association between SF-MPQ and the wound area, the BWAT score, and time interval of wound care was evaluated using the Spearman correlation coefficient. A P value of <0.05 was considered to be statistically significant. Statistical analyses were conducted using Statistical Analysis System Ver. 9.2 (SAS Institute Inc., Cary, NC, USA). 3. Results 3.1. Patient characteristics Twenty-seven patients were recruited. Of these, three refused to participate and one was excluded because the wound was no longer present at the time of data collection. One patient fell ill during treatment and dropped out. As a result, our final assessment included 22 participants. The median age of the 22 patients was 61.5 (36e81) years, and the median time after diagnosis of malignant wound was 15.5 (1e87) months. The breast was the most common site of malignant wounds (68.2% of all cases). Nine patients had used nonsteroidal anti-inflammatory drugs and seven patients had taken opioids for pain regularly. For wound care, the malignant wounds of 18 patients were managed with gauze dressing and treated with sulfadiazine silver-containing cream (n ¼ 9) or metronidazole cream (n ¼ 13) (Table 1). 3.2. Malignant wound status and pain The median wound size was 13.0 (0.18e151.1) cm2. The patients had wounds of various sizes and status. The wounds produced a large amount of purulent exudates (Table 2). Overall, 77.3% of patients complained of pain. Fifty percent of these patients complained mild pain and 27.3% of them complained moderate pain. Of these, 40.9% experienced continuous throbbing pain that should be under control in the past week. On the other hand, 27.2e31.8% of patients had tender or aching pain in their malignant wounds. Table 3 shows the pain characteristics of malignant wounds based on SF-MPQ results. Regarding wound status, the wound area did not correlate with
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N. Tamai et al. / European Journal of Oncology Nursing 24 (2016) 8e12
Table 1 Patient characteristics (n ¼ 22). Median (range), n (%) Age (years) Time after diagnosis of breast cancer (months) Time after diagnosis of malignant wound (months) Location of malignant wounds
Metastatic sitea
Treatmentsa
Analgesic drugsa Wound-dressing materials Ointmentsa Performance status
Comorbidity
Breast Sternal region Axilla Brachial region Lung Liver Bone Brain Hormone therapy Chemotherapy Molecular-targeted therapy Radiation therapy Opioid NSAIDS Gauze dressing Absorbent pad Sulfadiazine silver-containing cream Metronidazole cream Completely active Restricted for physically strenuous activity Ambulatory and capable of self-care Capable of only limited self-care Hypertension Diabetes Hyperthyroidism Gynecological disorder
61.5 59.5 15.5 15 3 3 1 10 5 11 0 6 16 7 0 7 9 18 4 9 13 3 13 5 1 4 2 3 3
(36e81) (3e161) (1e087) (68.2) (13.6) (13.6) (04.6) (45.5) (22.7) (50.0) (00.0) (27.3) (72.7) (31.8) (00.0) (31.8) (40.9) (81.8) (18.2) (40.9) (59.1) (13.6) (59.1) (22.7) (04.6) (18.2) (09.1) (13.6) (13.6)
NSAIDS: nonsteroidal anti-inflammatory drugs. a Multiple answers.
Table 2 Malignant wound status in breast cancer patients (n ¼ 22). Median (range) 2
Wound area (cm ) BWAT (score)
Size Depth Edges Undermining Necrotic tissue type Necrotic tissue amount Exudate type Exudate amount Skin colour surrounding skin Peripheral tissue oedema Peripheral tissue induration Granulation tissue Epithelialization
13.0 3 3 3 1 2 3 5 4 4 2 2 3 5
(0.18e151.1) (1e5) (2e4) (1e4) (1e3) (1e4) (1e5) (2e5) (2e5) (1e5) (1e4) (1e5) (1e5) (3e5)
BWAT: Bates-Jensen wound assessment tool.
SF-MPQ score. However, the score of edges based on BWAT was positively correlated with the sensory score (r ¼ 0.465, P ¼ 0.029) and present pain index (r ¼ 0.476, P ¼ 0.025). The score of granulation tissue based on BWAT was positively correlated with the sensory score (r ¼ 0.474, P ¼ 0.026) and present pain index (r ¼ 0.548, P ¼ 0.008). The time interval of wound care was negatively correlated with the sensory score (r ¼ 0.506, P ¼ 0.016) and present pain index (r ¼ 0.428, P ¼ 0.047) (Table 4). Other items, including amount of wound exudate or use of analgesic drugs, did not correlate with SF-MPQ score.
4. Discussion This is the first study to our knowledge to examine quantitatively and qualitatively the relationship between malignant wound
status and wound pain in breast cancer patients with malignant wounds. This study reported that 77.3% of patients complained of pain, and 51.9% of these used analgesics. The present results indicate a greater necessity for pain management than that reported previously (50% of patients by Probst et al.). We characterized “throbbing” or “tender” pain in breast cancer patients with malignant wounds. These pain were different from literature reporting chronic wound pain or postsurgical pain. Regarding wound pain after mastectomy, Bruce et al., (2004) reported that at least 30% of patients complained of “aching”, “shooting”, “annoying”, and “numb” pain. Pain from a body organ or wound infection is described especially as throbbing. The patients may have throbbing pain in their malignant wounds by tissue damage to the breast. Many patients with malignant wounds have experienced various
N. Tamai et al. / European Journal of Oncology Nursing 24 (2016) 8e12
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Table 3 Characteristics of pain in malignant wounds (n ¼ 22). Short-form McGill pain questionnaire (multiple answer)
n (%)
Throbbing Shooting Stabbing Sharp Cramping Gnawing Hot-Burning Aching Heavy Tender Splitting Tiring-Exhausting Sickening Fearful Punishing-Cruel
9 5 5 3 2 4 4 6 5 7 2 3 1 1 2
McGill pain score
(40.9) (22.7) (22.7) (13.6) (9.1) (18.2) (18.2) (27.2) (22.7) (31.8) (9.1) (13.6) (4.5) (4.5) (9.1)
Mild
Moderate
8 4 4 2 2 4 3 5 5 4 2 3 1 1 2
1 1 1 1 0 0 1 1 0 3 0 0 0 0 0
(36.4) (18.2) (18.2) (9.1) (9.1) (18.2) (13.7) (22.7) (22.7) (18.2) (9.1) (13.6) (4.5) (4.5) (9.1)
(4.5) (4.5) (4.5) (4.5) (0.0) (0.0) (4.5) (4.5) (0.0) (13.6) (0.0) (0.0) (0.0) (0.0) (0.0)
Table 4 Association between malignant wound status and wound pain. SF-MPQ Sensory
Wound area (cm2) BWAT Size Depth Edges Undermining Necrotic tissue type Necrotic tissue amount Exudate type Exudate amount Skin colour surrounding skin Peripheral tissue oedema Peripheral tissue induration Granulation tissue Epithelialization Time interval of wound care (hour)
Affective
Present pain index (PPIVAS)
r
P
r
P
r
P
0.232 0.295 0.293 0.465 0.105 0.212 0.044 0.082 0.256 0.170 0.333 0.198 0.474 0.220 0.506
0.299 0.183 0.186 0.029* 0.643 0.343 0.846 0.718 0.250 0.451 0.130 0.378 0.026* 0.324 0.016*
0.196 0.278 0.155 0.309 0.102 0.138 0.089 0.043 0.088 0.273 0.183 0.212 0.181 0.186 0.214
0.382 0.211 0.492 0.162 0.650 0.540 0.693 0.850 0.698 0.219 0.414 0.344 0.421 0.407 0.340
0.085 0.128 0.349 0.476 0.087 0.281 0.191 0.131 0.149 0.206 0.109 0.222 0.548 0.354 0.428
0.707 0.571 0.112 0.025* 0.701 0.205 0.394 0.561 0.508 0.359 0.629 0.321 0.008* 0.106 0.047*
BWAT: Bates-Jensen Wound Assessment Tool. SF-MPQ: Short form McGill pain questionnaire. *: p < 0.05.
types and intensities of wound pain and should provide the appropriate pain or infection control. Our previous study reported about 30% patients with malignant wounds were actually infected with anaerobic or intestinal bacteria (Tamai et al., 2015). In the report, 30% infection was determined using swab culture technique. To prevent pain caused by wound infection, we think that pain control such as not only dressings but also management of infection. Although we hypothesized that the size of a malignant wound would be correlated with wound pain intensity, our study did not support this hypothesis. The degradation of wound edges and granulation tissue were correlated with sensory pain and present pain index. These findings suggest that the peripheral nerve fibres in superficial intradermal wound edges are rolled towards the wound bed or infiltrated by cancer. Thus, granulation tissue reported in this study may have been cancerous tissue, rather than granulation tissue observed in normal wound healing. Therefore, regardless of wound size, providers should focus on wound edges for assessing malignant wound pain and provide specific wound care for wound edges, including non-invasive dressing, to decrease wound pain and maintain the patients’ quality of life (Woo and Sibbald, 2010). In this study, we cannot deny the possibility of the effect to wound pain by gauze dressings. However, there was not
the relationship between wound pain and ointment in this study. The time interval for wound care was correlated with pain intensity, although our results could not explain the causal relationship between the term of wound dressing change and pain intensity. We cannot identify whether to change their dressings frequently due to severe wound pain or to produce wound pain due to dressing change frequently. This challenge is one that will have to be addressed in future research. “Pain” is a most subjective experience, and expression of pain varies widely. The SF-MPQ is one of the common widely used instruments in many languages and countries to evaluate pain multilaterally. This questionnaire may be a useful tool for patients with malignant wounds because clinician can understand the characteristics of malignant wound pain, thereby reducing their burden properly. A limitation of our study is that the sample population was small and generalization was restricted. Further prospective investigations would be useful to examine the effects of earlier interventions for wound pain. 5. Conclusion We clarified in this study that about 80% of patients with breast
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N. Tamai et al. / European Journal of Oncology Nursing 24 (2016) 8e12
malignant wounds complained of pain, and their pain was poorly controlled. Malignant wound pain significantly correlated with the degradation of wound edges, granulation tissue, and time interval for wound care. It is necessary to provide especially pain control focused on the wound edge or granulation tissue. Conflict of interest statement None. References Ando, M., Ando, Y., Hasegawa, Y., Shimokata, K., Minami, H., Wakai, K., Ohno, Y., Sakai, S., 2001. Prognostic value of performance status assessed by patients themselves, nurses, and oncologists in advanced non-small cell lung cancer. Br. J. Cancer 85, 1634e1639. Bates-Jensen, B.M., Vredevoe, D.L., Brecht, M.L., 1992. Validity and reliability of the pressure sore status tool. Decubitus 5, 20e28. Bruce, J., Poobalan, A.S., Smith, W.C., Chambers, W.A., 2004. Quantitative assessment of chronic postsurgical pain using the McGill pain questionnaire. Clin. J. Pain 20, 70e75. Elder, E.E., Kennedy, C.W., Gluch, L., Carmalt, H.L., Janu, N.C., Joseph, M.G., Donellan, M.J., Molland, J.G., Gillett, D.J., 2006. Patterns of breast cancer relapse. Eur. J. Surg. Oncol. 32, 922e927. Gibson, S., Green, J., 2013. Review of patients’ experiences with fungating wounds and associated quality of life. J. Wound Care 22, 265e275. Ito, Y., Ioka, A., Tanaka, M., Nakayama, T., Tsukuma, H., 2009. Trends in cancer incidence and mortality in Osaka, Japan: evaluation of cancer control activities. Cancer Sci. 100, 2390e2395.
Lo, S., Hayter, M., Hu, W., 2012. Symptom burden and quality of life in patients with malignant fungating wounds. J. Adv. Nurs. 68, 1312e1321. Maida, V., Ennis, M., Kuziemsky, C., Trozzolo, L., 2009. Symptoms associated with malignant wounds: a prospective case series. J. Pain Symptom. Manage 37, 206e211. Melzack, R., 1987. The short-form McGill pain questionnaire. Pain 30, 191e197. Merz, T., Klein, C., Uebach, B., Kern, M., Ostgathe, C., Bükki, J., 2001. Fungating wounds - multidimensional challenge in palliative care. Breast Care (Basel) 6, 21e24. Naylor, W., 2002. Malignant wounds: aetiology and principles of management. Nurs. Stand 16, 45e53 quiz 54, 56. Oken, M.M., Creech, R.H., Tormey, D.C., Horton, J., Davis, T.E., McFadden, E.T., Carbone, P.P., 1982. Toxicity and response criteria of the eastern cooperative oncology group. Am. J. Clin. Oncol. 5, 649e655. Probst, S., Arber, A., Faithfull, S., 2009. Malignant fungating wounds: a survey of nurses’ clinical practice in Switzerland. Eur. J. Oncol. Nurs. 13, 295e298. Sanada, H., Moriguchi, T., Miyachi, Y., Ohura, T., Nakajo, T., Tokunaga, K., Fukui, M., Sugama, J., Kitagawa, A., 2004. Reliability and validity of design, a tool that classifies pressure ulcer severity and monitors healing. J. Wound Care 13, 13e18. Schulz, V., Triska, O.H., Tonkin, K., 2002. Malignant wounds: caregiver-determined clinical problems. J. Pain Symptom Manage 24, 572e577. Sussman, C., Bates-Jensen, B.M., 2007. Wound Care: a Collaborative Practice Manual. Wolters Kluwer Health/Lippincott Williams & Wilkins, Baltimore. Tamai, N., Akase, T., Minematsu, T., Higashi, K., Toida, T., Igarashi, K., Sanada, H., 2015. Association between components of exudates and periwound moistureassociated dermatitis in breast cancer patients with malignant fungating wounds. Biol. Res. Nurs. 18, 199e206. Woo, K., Sibbald, R., 2010. Local wound care for malignant and palliative wounds. Adv. skin wound care 23, 417e428, 429-430. Yamaguchi, M., Kumano, H., Yamauchi, Y., Kadota, Y., Iseki, M., 2007. The development of a Japanese version of the short-form McGill pain questionnaire. J. Jpn. Soc. Pain Clin. 14, 9e14 (Article in Japanese).
Contents lists available at ScienceDirect
European Journal of Oncology Nursing journal homepage: www.elsevier.com/locate/ejon
The relationship between malignant wound status and pain in breast cancer patients Nao Tamai a, Yuko Mugita a, Mari Ikeda b, Hiromi Sanada a, * a Department of Gerontological Nursing/Wound Care Management, Division of Health Sciences and Nursing, Graduate School of Medicine, The University of Tokyo, 113-0033, 7-3-1 Hongo, Bunkyo-ku, Tokyo, Japan b Department of Nursing Administration and Advanced Clinical Nursing, Division of Health Sciences and Nursing, Graduate School of Medicine, The University of Tokyo, 113-0033, 7-3-1 Hongo, Bunkyo-ku, Tokyo, Japan
a r t i c l e i n f o
a b s t r a c t
Article history: Received 10 August 2015 Received in revised form 15 May 2016 Accepted 23 May 2016
Purpose: Skin metastasis is one of the most frequent metastases in breast cancer patients. Patients with malignant wounds experience numerous symptoms, including serious wound pain. However, the features of pain related to malignant wounds have not been investigated. Nurses can experience a dilemma when treating these patients due to a lack of knowledge of the pain. The aims of this study were to examine the quality and intensity of malignant wound pain and to determine the association between wound status and pain in the patients with malignant wounds. Methods: Cross-sectional study was conducted. Participants were recruited from a breast centre based in a general hospital. We collected the patients’ demographic and wound management data and assessed wound condition. Patients evaluated wound pain intensity and quality over the preceding week using the short-form McGill Pain Questionnaire (SF-MPQ). The association between SF-MPQ results, wound condition, and the time interval for wound care was evaluated using the Spearman’s correlation coefficient. The protocol was approved by the Ethical Committee of the each facilities. Results: The median age of the 22 enrolled patients was 61.5 years, and the median time after diagnosis of malignant wound was 15.5 months. Overall, 77.3% of patients complained of pain. Malignant wound pain significantly correlated with the degradation of wound edges, granulation tissue, and the time interval for wound care. Conclusion: We consider that it is necessary to provide pain-control care focused on the wound edge and granulation tissue of malignant wounds through the assessment of malignant wound pain and condition. © 2016 Published by Elsevier Ltd.
Keywords: Exudate Granulation tissue Malignant fungating wound Short-form McGill pain questionnaire Wound care
1. Introduction Breast cancer incidence increases annually worldwide, and it is a primary cancer among women (Ito et al., 2009). Breast cancer may metastasise to the lung, liver, bone, brain, and skin, with especially high rates of metastasis to skin sites (Elder et al., 2006). These skin metastases are called malignant wounds. Malignant wounds can be caused by direct invasion of the skin by cancer or by metastasis to the skin. These wounds have both ulcerative or fungating features. Patients with malignant wounds can develop numerous symptoms, including pain, exudate, infection, odour, and bleeding, which cause psychological distress (Gibson and Green, 2013; Maida et al.,
* Corresponding author. E-mail address: [email protected] (H. Sanada). http://dx.doi.org/10.1016/j.ejon.2016.05.004 1462-3889/© 2016 Published by Elsevier Ltd.
2009; Merz et al., 2001; Naylor, 2002; Probst et al., 2009; Schulz et al., 2002). Therefore, comprehensive palliative care to control these symptoms is needed for patients with malignant wounds, from treatment, follow-up care, and end-of-life care. Probst et al. reported that 50% of patients with malignant wounds needed to manage their pain. The causes of pain in breast cancer patients with malignant wounds were assumed to be the progression of cancer, infection, and peri-wound dermatitis caused by wound exudate. However, the features of pain related to malignant wounds in breast cancer patients have not been investigated. Nurses can experience a dilemma when treating these patients due to a lack of knowledge of the pain, thereby potentially providing insufficient management of wounds. Recently, a short form of the McGill Pain Questionnaire (SF-MPQ) has been used to evaluate various types of pain. A Japanese version of the SF-MPQ is available (Yamaguchi et al., 2007). It is a self-report questionnaire
N. Tamai et al. / European Journal of Oncology Nursing 24 (2016) 8e12
consisting of three major dimensions e sensory, affective, and total descriptors. Because the SF-MPQ provides qualitative and quantitative information, it may help nurses to understand more fully the quality and/or intensity of the malignant wound pain in breast cancer patients (Lo et al., 2012). The aims of this study were to examine the quality and intensity of pain and to determine the association between wound status and pain in breast cancer patients with malignant wounds. 2. Methods 2.1. Study design and participants A cross-sectional study was conducted. Participants were recruited from the outpatient department of a breast centre based in a general hospital in Japan between February 2010 and June 2011. Inclusion criteria were participants over 18 years of age presenting with a breast malignant wound. Patients with breast malignant wounds were diagnosed by the criteria of the hospital, which were (i) skin invasion near the breast cancer site or (ii) pathology reports from a breast tissue sample (oestrogen receptor, progesterone receptor, and human epidermal growth factor receptor type 2 [HER2] proteins). Exclusion criteria were participants in critical condition, as determined by physicians. Patients received standard wound management by nurses certified in wound, ostomy, and continence nursing or cancer pain management nursing in the hospital. The protocol was approved by the local Ethical Committees of our institution and an affiliated hospital. Written informed consent was obtained from all the participants. 2.2. Data collection Demographic characteristics were collected from medical records by the lead researcher and included the following: age, hormone receptors, HER2 proteins status, time after diagnosis of breast cancer, time after diagnosis of malignant wound, location of malignant wounds, metastatic site, treatments, administration of analgesic drugs, wound management, performance status, and comorbidity. Performance status by Eastern Cooperative Oncology Group as rated from 0 to 4, with 0 denoting perfect health and 4 indicated patients who were bedbound (Ando et al., 2001; Oken et al., 1982). The patients provided malignant wound care on an outpatient basis. During wound care, the lead researcher assessed the wound and the condition of the surrounding skin by visual inspection and palpation (pressing down with a finger and pinching of tissues), using the Bates-Jensen wound assessment tool (BWAT) and DESIGN (Bates-Jensen et al., 1992; Sussman and Bates-Jensen, 2007). BWAT evaluates 13 wound characteristics, including wound size, depth, edges, undermining, necrotic tissue type and amount, exudate type and amount, skin colour surrounding the wound, peripheral tissue oedema and induration, granulation tissue, and epithelialization, with a numerical rating scale. Induration is abnormal firmness of peri-wound. A high score indicates a severe condition. The reliability and validity of this tool have been verified (Bates-Jensen et al., 1992). DESIGN is a tool for scoring the severity of wounds, including pressure ulcers. It was developed by the Scientific Education Committee of the Japanese Society of Pressure Ulcers in 2002. DESIGN consists of seven components: depth, exudate, size, inflammation/infection, granulation tissue, necrotic tissue, and pockets (undermining). The total score is calculated, and a high score indicates greater severity. The reliability and validity of DESIGN have been shown (Sanada et al., 2004). The BWAT total score was positively correlated with DESIGN-R total score (r ¼ 0.89, P < 0.0001). In this study, the inter-rater reliability of BWAT score
9
was evaluated with separate raters (a plastic surgeon, a wound care nurse, and the lead researcher). The raters were assessed by calculating the rate of agreement on scores for photographs of malignant wounds (k ¼ 0.72e0.91 for each item). During wound care, digital photographs of the wound and periwound skin were taken with a digital camera (COOLPIX, NIKON, Tokyo, Japan). Wound size on the digital photograph was measured three times using the ImageJ software program (National Institutes of Health, Maryland, USA), and the median value was used for analysis. We interviewed patients about wound management (time interval to exchange dressings) related to wound pain. After wound care by the lead researcher, the patients answered the questionnaire related to their wound pain intensity and quality using the SF-MPQ. The SF-MPQ is the most widely used tool for assessing pain experience. Participants evaluated the SF-MPQ by rating the intensity and quality to which they experienced the average wound pain in the past week. The main component of the SF-MPQ consists of 15 descriptors (11 sensory and 4 affective) rated on a 4-point intensity scale (0 ¼ “none” to 3 ¼ “severe”). The SFMPQ also includes a 6-point present pain index (PPI) and a visual analogue scale (VAS), which measure overall pain intensity as a single dimension (Melzack, 1987). The reliability and validity of SFMPQ Japanese version have been shown (Yamaguchi et al., 2007). 2.3. Statistical analysis Data are presented as the median (range) or the number with percentage (%). The strength of the association between SF-MPQ and the wound area, the BWAT score, and time interval of wound care was evaluated using the Spearman correlation coefficient. A P value of <0.05 was considered to be statistically significant. Statistical analyses were conducted using Statistical Analysis System Ver. 9.2 (SAS Institute Inc., Cary, NC, USA). 3. Results 3.1. Patient characteristics Twenty-seven patients were recruited. Of these, three refused to participate and one was excluded because the wound was no longer present at the time of data collection. One patient fell ill during treatment and dropped out. As a result, our final assessment included 22 participants. The median age of the 22 patients was 61.5 (36e81) years, and the median time after diagnosis of malignant wound was 15.5 (1e87) months. The breast was the most common site of malignant wounds (68.2% of all cases). Nine patients had used nonsteroidal anti-inflammatory drugs and seven patients had taken opioids for pain regularly. For wound care, the malignant wounds of 18 patients were managed with gauze dressing and treated with sulfadiazine silver-containing cream (n ¼ 9) or metronidazole cream (n ¼ 13) (Table 1). 3.2. Malignant wound status and pain The median wound size was 13.0 (0.18e151.1) cm2. The patients had wounds of various sizes and status. The wounds produced a large amount of purulent exudates (Table 2). Overall, 77.3% of patients complained of pain. Fifty percent of these patients complained mild pain and 27.3% of them complained moderate pain. Of these, 40.9% experienced continuous throbbing pain that should be under control in the past week. On the other hand, 27.2e31.8% of patients had tender or aching pain in their malignant wounds. Table 3 shows the pain characteristics of malignant wounds based on SF-MPQ results. Regarding wound status, the wound area did not correlate with
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N. Tamai et al. / European Journal of Oncology Nursing 24 (2016) 8e12
Table 1 Patient characteristics (n ¼ 22). Median (range), n (%) Age (years) Time after diagnosis of breast cancer (months) Time after diagnosis of malignant wound (months) Location of malignant wounds
Metastatic sitea
Treatmentsa
Analgesic drugsa Wound-dressing materials Ointmentsa Performance status
Comorbidity
Breast Sternal region Axilla Brachial region Lung Liver Bone Brain Hormone therapy Chemotherapy Molecular-targeted therapy Radiation therapy Opioid NSAIDS Gauze dressing Absorbent pad Sulfadiazine silver-containing cream Metronidazole cream Completely active Restricted for physically strenuous activity Ambulatory and capable of self-care Capable of only limited self-care Hypertension Diabetes Hyperthyroidism Gynecological disorder
61.5 59.5 15.5 15 3 3 1 10 5 11 0 6 16 7 0 7 9 18 4 9 13 3 13 5 1 4 2 3 3
(36e81) (3e161) (1e087) (68.2) (13.6) (13.6) (04.6) (45.5) (22.7) (50.0) (00.0) (27.3) (72.7) (31.8) (00.0) (31.8) (40.9) (81.8) (18.2) (40.9) (59.1) (13.6) (59.1) (22.7) (04.6) (18.2) (09.1) (13.6) (13.6)
NSAIDS: nonsteroidal anti-inflammatory drugs. a Multiple answers.
Table 2 Malignant wound status in breast cancer patients (n ¼ 22). Median (range) 2
Wound area (cm ) BWAT (score)
Size Depth Edges Undermining Necrotic tissue type Necrotic tissue amount Exudate type Exudate amount Skin colour surrounding skin Peripheral tissue oedema Peripheral tissue induration Granulation tissue Epithelialization
13.0 3 3 3 1 2 3 5 4 4 2 2 3 5
(0.18e151.1) (1e5) (2e4) (1e4) (1e3) (1e4) (1e5) (2e5) (2e5) (1e5) (1e4) (1e5) (1e5) (3e5)
BWAT: Bates-Jensen wound assessment tool.
SF-MPQ score. However, the score of edges based on BWAT was positively correlated with the sensory score (r ¼ 0.465, P ¼ 0.029) and present pain index (r ¼ 0.476, P ¼ 0.025). The score of granulation tissue based on BWAT was positively correlated with the sensory score (r ¼ 0.474, P ¼ 0.026) and present pain index (r ¼ 0.548, P ¼ 0.008). The time interval of wound care was negatively correlated with the sensory score (r ¼ 0.506, P ¼ 0.016) and present pain index (r ¼ 0.428, P ¼ 0.047) (Table 4). Other items, including amount of wound exudate or use of analgesic drugs, did not correlate with SF-MPQ score.
4. Discussion This is the first study to our knowledge to examine quantitatively and qualitatively the relationship between malignant wound
status and wound pain in breast cancer patients with malignant wounds. This study reported that 77.3% of patients complained of pain, and 51.9% of these used analgesics. The present results indicate a greater necessity for pain management than that reported previously (50% of patients by Probst et al.). We characterized “throbbing” or “tender” pain in breast cancer patients with malignant wounds. These pain were different from literature reporting chronic wound pain or postsurgical pain. Regarding wound pain after mastectomy, Bruce et al., (2004) reported that at least 30% of patients complained of “aching”, “shooting”, “annoying”, and “numb” pain. Pain from a body organ or wound infection is described especially as throbbing. The patients may have throbbing pain in their malignant wounds by tissue damage to the breast. Many patients with malignant wounds have experienced various
N. Tamai et al. / European Journal of Oncology Nursing 24 (2016) 8e12
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Table 3 Characteristics of pain in malignant wounds (n ¼ 22). Short-form McGill pain questionnaire (multiple answer)
n (%)
Throbbing Shooting Stabbing Sharp Cramping Gnawing Hot-Burning Aching Heavy Tender Splitting Tiring-Exhausting Sickening Fearful Punishing-Cruel
9 5 5 3 2 4 4 6 5 7 2 3 1 1 2
McGill pain score
(40.9) (22.7) (22.7) (13.6) (9.1) (18.2) (18.2) (27.2) (22.7) (31.8) (9.1) (13.6) (4.5) (4.5) (9.1)
Mild
Moderate
8 4 4 2 2 4 3 5 5 4 2 3 1 1 2
1 1 1 1 0 0 1 1 0 3 0 0 0 0 0
(36.4) (18.2) (18.2) (9.1) (9.1) (18.2) (13.7) (22.7) (22.7) (18.2) (9.1) (13.6) (4.5) (4.5) (9.1)
(4.5) (4.5) (4.5) (4.5) (0.0) (0.0) (4.5) (4.5) (0.0) (13.6) (0.0) (0.0) (0.0) (0.0) (0.0)
Table 4 Association between malignant wound status and wound pain. SF-MPQ Sensory
Wound area (cm2) BWAT Size Depth Edges Undermining Necrotic tissue type Necrotic tissue amount Exudate type Exudate amount Skin colour surrounding skin Peripheral tissue oedema Peripheral tissue induration Granulation tissue Epithelialization Time interval of wound care (hour)
Affective
Present pain index (PPIVAS)
r
P
r
P
r
P
0.232 0.295 0.293 0.465 0.105 0.212 0.044 0.082 0.256 0.170 0.333 0.198 0.474 0.220 0.506
0.299 0.183 0.186 0.029* 0.643 0.343 0.846 0.718 0.250 0.451 0.130 0.378 0.026* 0.324 0.016*
0.196 0.278 0.155 0.309 0.102 0.138 0.089 0.043 0.088 0.273 0.183 0.212 0.181 0.186 0.214
0.382 0.211 0.492 0.162 0.650 0.540 0.693 0.850 0.698 0.219 0.414 0.344 0.421 0.407 0.340
0.085 0.128 0.349 0.476 0.087 0.281 0.191 0.131 0.149 0.206 0.109 0.222 0.548 0.354 0.428
0.707 0.571 0.112 0.025* 0.701 0.205 0.394 0.561 0.508 0.359 0.629 0.321 0.008* 0.106 0.047*
BWAT: Bates-Jensen Wound Assessment Tool. SF-MPQ: Short form McGill pain questionnaire. *: p < 0.05.
types and intensities of wound pain and should provide the appropriate pain or infection control. Our previous study reported about 30% patients with malignant wounds were actually infected with anaerobic or intestinal bacteria (Tamai et al., 2015). In the report, 30% infection was determined using swab culture technique. To prevent pain caused by wound infection, we think that pain control such as not only dressings but also management of infection. Although we hypothesized that the size of a malignant wound would be correlated with wound pain intensity, our study did not support this hypothesis. The degradation of wound edges and granulation tissue were correlated with sensory pain and present pain index. These findings suggest that the peripheral nerve fibres in superficial intradermal wound edges are rolled towards the wound bed or infiltrated by cancer. Thus, granulation tissue reported in this study may have been cancerous tissue, rather than granulation tissue observed in normal wound healing. Therefore, regardless of wound size, providers should focus on wound edges for assessing malignant wound pain and provide specific wound care for wound edges, including non-invasive dressing, to decrease wound pain and maintain the patients’ quality of life (Woo and Sibbald, 2010). In this study, we cannot deny the possibility of the effect to wound pain by gauze dressings. However, there was not
the relationship between wound pain and ointment in this study. The time interval for wound care was correlated with pain intensity, although our results could not explain the causal relationship between the term of wound dressing change and pain intensity. We cannot identify whether to change their dressings frequently due to severe wound pain or to produce wound pain due to dressing change frequently. This challenge is one that will have to be addressed in future research. “Pain” is a most subjective experience, and expression of pain varies widely. The SF-MPQ is one of the common widely used instruments in many languages and countries to evaluate pain multilaterally. This questionnaire may be a useful tool for patients with malignant wounds because clinician can understand the characteristics of malignant wound pain, thereby reducing their burden properly. A limitation of our study is that the sample population was small and generalization was restricted. Further prospective investigations would be useful to examine the effects of earlier interventions for wound pain. 5. Conclusion We clarified in this study that about 80% of patients with breast
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malignant wounds complained of pain, and their pain was poorly controlled. Malignant wound pain significantly correlated with the degradation of wound edges, granulation tissue, and time interval for wound care. It is necessary to provide especially pain control focused on the wound edge or granulation tissue. Conflict of interest statement None. References Ando, M., Ando, Y., Hasegawa, Y., Shimokata, K., Minami, H., Wakai, K., Ohno, Y., Sakai, S., 2001. Prognostic value of performance status assessed by patients themselves, nurses, and oncologists in advanced non-small cell lung cancer. Br. J. Cancer 85, 1634e1639. Bates-Jensen, B.M., Vredevoe, D.L., Brecht, M.L., 1992. Validity and reliability of the pressure sore status tool. Decubitus 5, 20e28. Bruce, J., Poobalan, A.S., Smith, W.C., Chambers, W.A., 2004. Quantitative assessment of chronic postsurgical pain using the McGill pain questionnaire. Clin. J. Pain 20, 70e75. Elder, E.E., Kennedy, C.W., Gluch, L., Carmalt, H.L., Janu, N.C., Joseph, M.G., Donellan, M.J., Molland, J.G., Gillett, D.J., 2006. Patterns of breast cancer relapse. Eur. J. Surg. Oncol. 32, 922e927. Gibson, S., Green, J., 2013. Review of patients’ experiences with fungating wounds and associated quality of life. J. Wound Care 22, 265e275. Ito, Y., Ioka, A., Tanaka, M., Nakayama, T., Tsukuma, H., 2009. Trends in cancer incidence and mortality in Osaka, Japan: evaluation of cancer control activities. Cancer Sci. 100, 2390e2395.
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