Symptoms of Malignant Fungating Wounds and Functional Performance among Patients with Advanced Cancer: An Integrative Review from 2000 to 2019

Abstract

Introduction:

Malignant fungating wounds (MFWs), non-healing wounds caused by aggressive proliferation of malignant tumors, afflict 5%–14.5% of patients with advanced cancer. We conducted an integrative review to evaluate the level of evidence of peer-reviewed literature published from 2000 to 2019 on symptoms of MFWs, and the impact of the symptoms on functional performance among patients with advanced cancer.

Methods:

Four electronic databases were searched and 1506 articles were retrieved. A total of 1056 abstracts were screened for relevance and a full review of the 26 articles was performed. A total of 12 articles met inclusion criteria. An established quality assessment tool was used to rate the quality of the included studies.

Results:

The overall quality of the included 12 studies was adequate. This integrative review of the literature provided strong evidence that patients with MFWs suffered multiple symptoms, including pain, odor, exudate, bleeding, pruritus, perceived wound status, perceived bulk effect and lymphedema. Quantitative research was not able to capture the occurrence and characteristics of all the identified symptoms. There was a lack of quantitative research on the impact of MFWs and symptoms on patients' functional performance. Yet, qualitative studies provided vivid description of how the symptoms negatively affected patients' functional performance. Future research should develop a clinical tool that enables the comprehensive assessment of symptoms of MFWs. Well-designed quantitative research is needed to delineate the impact of symptoms of MFWs on patients' functional performance to ensure quality palliative care.

Introduction

Malignant Fungating Wounds (MFWs) generally occur during the last 6–12 months of life among patients with advanced cancer,^1,2 that is, when no medical or surgical intervention can control tumor growth.^3–5 MFWs are non-healing wounds due to aggressive proliferation and infiltration of malignant tumors into the skin, blood and lymph vessels, leading to widespread tissue damage, hypoxia, necrosis, as well as sustained polymicrobial proliferation and fungating ulceration of the wound.⁶ MFWs disproportionately affect older adults and women with MFWs of the breast as the most prevalent (66%), followed by head and neck (24%), then groin, genitals and back (3%) with all other sites accounting for the remaining 8%.^7,8 Given the incurable nature of MFWs and severity and numerous symptoms associated with these complex wounds, palliative care is imperative for this population to prevent and relieve suffering through comprehensive assessment and treatment of symptoms of MFWS, preservation and/or restoration of functional performance, and treatment of psychosocial and spiritual distress.^12,13

The unique symptom experience of each patient with MFWs can be subjectively reported or objectively measured through the symptom characteristics of timing, intensity, quality, and, distress.^14–18 Patients with MFWs may suffer cancer-related symptoms due to the cancer itself or cancer treatment, such as fatigue or cancer-related bone pain, as well as side effects from palliative therapies (e.g., palliative radiation or chemotherapy).^6,11,13

However, the symptoms and symptom characteristics specifically attributed to the MFWs (wound pain, malodor, bleeding) are unique to this population.^6,13 Research has shown symptoms can negatively impact individual's functional performance in the physical, psychological, social, occupational, and spiritual domains.^19–22 Clinicians and researchers have been aware that symptoms associated with MFWs have a detrimental effect on patients' functions, and negatively impact psychosocial well-being (e.g., positive emotions like hope, and life satisfaction).^5,6,9,11

Since 2000, more research has documented symptoms associated with MFWs (e.g., pain, malodor, exudate, bleeding, and pruritus) among patients with MFWs.^{8–11,23–25} This has made it possible to explore the relationships between symptoms of MFWs and the impact on functional performance through systematically reviewing the existing literature.

The purpose of this article is to evaluate the level of evidence of peer-reviewed literature published from 2000 to 2019 on symptoms of MFWs, and the impact of the symptoms on functional performance among patients with advanced cancer. Specifically, this review aimed to answer the following questions: (1) What were the symptoms of MFWs? (2) What were the symptom characteristics of MFW symptoms? (3) What was the impact of symptoms of MFWs on patients' functional performance?

Methods

Preparation for the search

To prepare for the review, a thorough literature search and review was accomplished to generate key search words or terms based on the concept of MFWs, symptoms, functional performance and quality of life (QOL). Subsequently, additional search terms were identified using the MeSH (Medical Subject Heading) database. To ensure the reliability, thoroughness, and accuracy of key searching terms, we had multiple consultations with the health librarian.^27,28

The key terms used for this systematic review included: “malignant fungating wound or malignancy or neoplasm or wound and symptoms, quality of life, psychosocial, functional performance, pain or bleeding or pruritus or odor or exudate or bulk effect or lymphedema, depression or anxiety or embarrassment or sexuality or social isolation or stigma.” Using various combinations of the key terms, the following databases were searched: the Excerpta Medical Database (EMBASE), PubMed, the Cumulative Index for Nursing and Allied Health Literature (CINAHL), and Cochrane Library.

Before the integrative review, we defined key concepts based on extensive review of the literature. Symptoms were defined as subjectively perceived indicators of abnormal biological or physiological changes that may or may not be observed or measured objectively.^14–17 We defined physiologic bulk effect as a sign of objective, measurable protrusion of the wound and wound dressing beneath a person's clothing or over exposed skin from side and frontal views.²² While the symptom of perceived bulk effect is the patient's subjective interpretation of how noticeable the protrusion is and the degree to which patients perceive it alters their appearance and causes distress.^9,13 Physiologic wound status is the objective, measurable dimensions and characteristics of the wound (e.g., tissue type, wound edges, presence of infection), while perceived wound status is the patient's perceived meaning of the wound's appearance.^9,13,22

Functional performance was defined as the ability to perform activities to meet basic needs, fulfill usual roles, and maintain health and well-being.²² The impact of symptoms on functional performance of patients with MFWs was operationalized in this review as statistically significant associations between symptoms and functional performance items measured in quantitative studies.^16,17,22

Inclusion and exclusion criteria

Inclusion criteria for this review were: (1) quantitative and qualitative research on symptoms related to MFWs, and (2) quantitative and qualitative research on functional performance among patients with MFWs. Excluded articles were: (1) any research that focused on other types of wounds, such as pressure ulcers, venous ulcers, and Marjolin's ulcers, (2) any research that focused on microbiome or interventional research, including invasive or topical therapies, (3) individual case studies, and (4) unpublished dissertations and abstracts.²⁶

Data extraction

In total, 1506 articles were retrieved by applying the key terms to the four databased, after removal of 450 duplicates, 1, 056 articles remained. Inclusion and exclusion criteria were applied to the 1056 articles through a review of the abstracts, 26 articles were deemed relevant. Upon a full-text review of the 26 articles, only 12 articles met inclusion criteria, resulting in five quantitative and seven qualitative studies for this review (Fig. 1).

FIG. 1.

Literature search flow chart. Symptoms of malignant fungating wounds and their impact on functional performance of patients with advanced cancer: an integrative review from 2000 to 2019.

An adapted quality assessment tool using a 14-item index was used to evaluate the quality of the 5 quantitative and 7 qualitative studies identified.^27,28 For this integrative review, studies that received an affirmative score of at least 10 out of 14 were considered to have adequate quality.^27,28 All 12 articles were deemed adequate and included in this review (Table 1).

Table 1.

Results of Quality Assessment Scores

Quality assessment criteria	Qualitative (n = 7), n	Quantitative (n = 5), n	Total (n = 12), n
Explicit and soundness of literature review	7	5	12
Clear aims and objectives	7	5	12
Clear description of setting	7	5	12
Clear description of sample	7	5	12
Appropriate sampling procedure	5	3	8
Clear description of data collection	7	5	12
Clear description of data analysis	7	5	12
Evidence of critical reflection (qualitative study)	7	—	7
Provision of recruitment data	1	2	3
Provision of attrition data	1	1	2
Provision of psychometric properties of measurement instruments (quantitative study)	—	3	3
Appropriate statistical analysis (quantitative study)	—	5	5
Findings reported for each outcome	7	5	12
Description of validity/reliability of results	5	5	10
Sufficient original data (qualitative study)	6	—	6
Provision of strengths and limitations of the study	6	5	11
Total score [mean (range; SD)]	11.14 (10–12; +0.89)	12.2 (12–13; +0.45)	11.58 (10–13; +0.9)

SD, standard deviation.

Data analysis

Detailed critical appraisal of each included article was performed using an adaptation of the Critical Appraisal Skills Programme (CASP) method.^28,29 Using the CASP method, we accomplished data analysis (Table 2).^26,30 After completing the evaluation of the 12 articles by the authors, the authors achieved consensus by discussing the results and resolving any discrepancies. A metasynthesis was conducted for the qualitative studies to identify emerging themes regarding the symptoms of MFWs and functional performance as well as descriptors for symptom characteristics (Tables 3–5).^26,30

Table 2.

Quantitative Studies of Symptoms of Malignant Fungating Wounds

Author and study origin	Aim and design	Sample	Physical and psychosocial symptom(s) evaluated	Psychometric tool(s) and statistical analysis	Key results		Studystrengths	Studyweaknesses	QS
Author and study origin	Aim and design	Sample	Physical and psychosocial symptom(s) evaluated	Psychometric tool(s) and statistical analysis	Symptoms	Functional performance impairment by symptom	Studystrengths	Studyweaknesses	QS
Maida et al.³⁵ Study origin: Canada	Aim: Accurately quantify the prevalence of malignant wounds and wound symptoms in cancer patients at baseline and the relationship between wounds and descriptive data. Design: Prospective, descriptive sequential case series	Sample: n = 67 (33 females, 34 males/MFW point prevalence 14.2%) Mean age (range): 72.3 (60–84.6) years Stage of cancer: NR Baseline performance status: PPSv2 51.7% Prevalence of MFW: Breast cancer (47.1%), head and neck (46.7%), primary skin (39.1%), GU/GYN (2.8%) Location (raw data): Breast 16, GI 15, lung 12, head and neck 7, skin 9, GU/GYN 2, other 6 Ave wounds per patient: 1.4 Wound classification: 33% nodules and induration, 55% fungating, 9.4% malignant ulcers, 2.6% others (zosteriform and mixed) Duration of MFW: NR Systemic anti-microbial inter-vention: NR Antineoplastic intervention: NR Topical intervention: NR	Physical symptom(s) evaluated: Pain Malodor Exudates Bleeding Mass effect (Bulk effect) Pruritus Crusting Psychosocial symptom(s) evaluated: Esthetic distress (social isolation, embarrassment)	Psychometric tool(s): None, all symptoms tallied. Symptom prevalence: total number and % Reliability and validity: Not applicable Statistical analysis: Descriptive statistics: continuous (age, PPSv2): t-test, categorical (gender, race): chi-squared with continuity correction Prevalence by diagnosis: chi-squared with continuity correction Symptom burden per site: total number of symptoms at the site divided by the number of wounds at the site	Overall 67.7% of MFWs were associated with at least 1 symptom, 21.9% with 2 or more, 11.5% with 3 or more Symptom prevalence: Symptom free (32.3%) Pain (30.2%) Mass effect (17.7%) Esthetic distress (16.7%) Exudate (14.6%) Odor (10.4%) Pruritus (5.2%) Bleeding (4.2%) Pain of mixed etiology was the most common symptom Symptom burden per anatomical site (symptoms per wound): GU/GYN: 2.2 Abdomen: 1.2 Spinal: 1.1 Chest/breast: 0.9 Head/neck: 0.7 Psychosocial Esthetic distress and odor led to embarrassment and isolation Bleeding led to fear of “bleeding to death”	Bulk effect: 24% had reduced mobility and technical difficulty with clothing	Adequate sample size Confirmed previous prevalence data Palliative performance status reported	Sampling procedure unclear No discussion of recruitment or attrition data Stage of cancer, anti-neoplastic and treatment information not reported QOL not measured Wound status not reported Magnitude of symptoms (severity) not reported Reporting of symptom effects on functional performance limited	12
Lo et al.³⁶ Study origin: Taiwan	Aim: Describe the relationship between symptoms and QOL in patients with MFW (symptom burden and demographic and wound-related status related to QOL). Design: Descriptive cross-sectional multi-center survey	Sample: n = 70 (47 males, 23 females) Mean age (range): 52.1 (29–82) years Stage of cancer: NR Baseline performance status: NR Prevalence of MFW: NR Location of MFW: Breast 13, head and neck 50, other 7 Wound classification: NR Duration of MFW: mean (range) = 8.49 (1.3–45.53) months	Physical symptom(s) evaluated: Pain Malodor Exudates Bleeding Wound status (edema, tissue type, size) Psychosocial symptom(s) evaluated: MQOL-TW: 13 items under 3 domains: Psycho-logical well-being (4) Existential well-being (6) Support issues (3) MFWAT-P: social issues (4) Psycho-logical issues (4)	Symptom measurement: MFWAT: MFWAT-P (subjective perception of patient with a MFW) scale of 0–200: higher scores indicating more serious level of patient's experience with the MFW. MFWAT-N (objective assessment of MFW) Reliability and validity: Whole questionnaire: Cronbach's alpha = 0.82, internal consistency coefficients for subscales = 0.82–0.90	Physical: Variables negatively correlated with QOL: MFWAT-N (r = −0.321, p = 0.015), pain issues (r = −0.265, p = 0.046), wound symptoms (r = −0.275, p = 0.038), bleeding (r = −0.280, p = 0.035), malodor (r = −0.293, p = 0.027) Psychosocial:	Not assessed	First reliable QOL study in patients with MFWs Rigorous study design	McGill QOL-TW (Taiwanese) was specifically designed for this study and needs further testing MFWAT has not undergone full reliability and validity testing Cross-sectional design (longitudinal needed) Small sample size Study didn't fully control for extraneous variables	13
		Systemic anti-microbial inter-vention:NRAntineoplasticintervention:46Topical intervention:Modern dressing 12, wet to-dry 37, herbal 6, other 3		Quality of life:MQOL-TW:Scale of 0–150: higher scores indicating better QOL.Reliability and validity:Whole questionnaire:Cronbach's alpha = 0.90, internal consistency coefficients for subscales = 0.75–0.95Statistical analysis:SPSS version 15.0 descriptive: percentages, means (range) or SD, relationship: Pearson's coefficient, multiple regression (p values of <0.05)	MFWAT-P:Total: mean = 102.98 (SD 37.66)Highest score = psychological issues domain (average score 25.71)QOL:McGill QOL:Total: mean = 77 (SD 31.39) SIS: mean = 6 (SD 2.63)Highest score = support issues domain (77.20)Variables negatively correlated with QOL:MFWAT-P (r = −0.277, p = 0.049), social issues (r = −0.268, p = 0.044)
Tamai et al.³²Study origin:Japan	Aim:Describe the morphologic characteristics of MAD in MFWs and link morphological characteristics of MAD to related factors.Design:Mixed methods qualitative descriptive study (morpho-qualitative analysis) with a cross-sectional study	Sample:n = 24 femalesMean age (range):62.0 (36–81) yearsStage of cancer:NRLocation of MFW:Breast: 24Duration of MFW:mean (range) = 14.5 (1–87) monthsAntimicrobialintervention:NRAntineoplasticintervention:NRTopical intervention:23	Physical symptom(s) evaluated:Wound statusExudatesPsychosocial symptom(s) evaluated:Not included	Performance status:ECOG PS: Ando et al. (2001)Reliability and validity:ECOG score, kappa0, 0.551, 0.482, 0.313, 0.434, 0.33Whole questionnaire:Cronbach's alpha = 0.82, internal consistency coefficients for subscales = 0.82–0.90Cronbach's alpha = 0.962, CVI Section I: 0.94CVI Section II: 0.62CVI Section III: 0.83MWAT-RBWATStatistical analysis:SAS version 9.2Median (range) or %, Spearman's correlation coefficient, Mann–Whitney U test (p values of <0.05)	Necrotic tissue type more severe in MAD than non-MAD group (χ² = 5.22, p = 0.048)Moderate or greater amount of exudate found in MAD than non-MAD group (χ² = 4.41, p = 0.066)Wound leakage more frequent in MAD than non-MAD group (χ² = 4.41, p = 0.066)	Not assessed	Revealed the prevalence and morphoqualitative characteristics of MAD in MFWs of the breast	Small sample sizePossible biasNo discussion of recruitment or attrition dataHistopathological observation in the diagnosis of MAD not practical	12
Tamai et al.³³Study origin:Japan	Aim:Examine the quality and intensity of malignant wound pain and to determine the association between wound status and pain in the patients with MFWs.Design:Cross-sectional, correlational study	Sample:n = 22 femalesMedian age (range):61.5 (36–81) yearsStage of cancer:NRLocation of MFW:Breast: 22, sternum 15, axilla 3, brachial region 4Duration of MFW:Mean (range): NRAntimicrobial intervention:SSD 9, metronidazole 13 (systemic NR)Antineoplastic intervention:22	Physical symptom(s) or characteristics R/T MASD:PainPsychosocial symptom(s):Not included	ECOG PS: Ando et al. (2001)ECOG score, kappa0, 0.551, 0.482, 0.313, 0.434, 0.33BWAT: Bates-Jensen et al. (1992)DESIGN-R: Sanada et al. (2004)SF-MPQStatistical analysis:SAS version 9.2 median (range) or %, Spearman's correlation coefficient (p values of <0.05)	Wound size:Median (range): 13.0 (0.18–151.1) cm²Pain:77.3% c/o painWound area, exudate, analgesic drugs didn't correlate with SF-MPQ scoreBWAT edges score positively correlated with sensory score (r = 0.465, p = 0.029) and present pain index (r = 0.476, p = 0.025)		First study to examine the quantitative and qualitative relationship between MFW status and wound pain in breast cancer patients	DESIGN-R tool not validated in MFWsSmall sample sizeNo discussion of recruitment or attrition dataGeneralization limited	12 (80%)
Fromantin et al.³¹Study origin:France	Aim:To evaluate the use of various local care procedures and characteristics of malignant wounds.Design:Prospective cohort study	Sample:With MFWsn = 32 femalesMean age (range):60 (30–96) yearsStage of cancer:NRLocation of MFW:Breast: 32Duration of MFW:Mean (range): 13 (1–64)Modern dressing:Multiple de-pendent on protocol: Alginate, Hydrofiber, Hydrocellular, InterfaceAntimicrobial intervention:NR (systemic NR)Antineoplastic intervention:22	Malignant wound care protocol:Infection (systemic), cleaning, local infection or suspicion of biofilm, pain, bleeding, odor, exudate, necrosis, fixation	Physical symptoms evaluated:Wound sizeBleedingMalodorExudationWound painPsychosocial symptoms evaluated:None	Exudate increased significantly with >4 different bacteria (p = 0.007) and at least 1 anaerobe (p = 0.05)Odor presence increased significantly when anaerobic bacteria are present (p = 0.050) and >10⁵/g bacteriaBleeding at dressing changes related to easily ruptured budding cellsPain symptoms did not change significantly over the course of the study		Evaluated bleeding as variable (few studies include)Attrition data provided	Small sample sizeOrdinal scales for odor, exudates, symptom control not validatedRecruitment data not providedFixed evaluation period-a longitudinal study of greater length may have been different	12

BWAT, Bates-Jensen Wound Assessment Tool; CVI; ECOG PS, Eastern Cooperative Oncology Group performance status; GU/GYN, genitourinary/gynecologic; MAD, moisture-associated dermatitis; MASD, moisture-associated skin damage; MFW, malignant fungating wounds; MFWAT, Malignant Fungating Wound Assessment Tool; MQOL-TW, McGill QOL questionnaire Taiwanese version; MWAT-R, Malignant Wound Assessment Tool for Research; NR, not recorded; QOL, quality of life; QS, quality score; RT, retention time; SF-MPQ, Short form McGill Pain Questionnaire; SSD, silver sulfadiazine.

Table 3.

Qualitative Studies of Symptoms of Malignant Fungating Wounds

Author and study origin	Aim and qualitative method	Sample (gender/age/stage of cancer/location of MFW/duration of MFW/antimicrobial intervention/anti-neoplastic intervention)	Symptom(s) identified	Emerging themes	Study strengths	Study weaknesses	QS
Lund-Nielsen et al.³⁷Study origin:Denmark	Aim:To investigate the way MFWs affect femininity, sexuality and daily life in women with progressive breast cancer.Qualitative method:Mixed methods study: exploratory semi-structured interviews (before and after the prospective intervention study)	Sample:n = 12 femalesMedian age (range):69 (57–85) yearsStage of cancer:Stage IV cancer 12Location of MFW:Breast: 9 (L), 3 (R)Duration of MFW:Median (range): 1.8 (0.1–4) yearsAntimicrobialintervention:NRAntineoplastic intervention:9	Symptoms:MalodorExudatesBulk effect (dressings)	Malodor and exudates reduce femininity and socializationMalodor, exudates, and dressing bulk-effect changed participants body image (low self-esteem) when they couldn't wear the clothes they wanted resulting in social isolationMalodor and exudates have a negative impact on sex lifeThe ability to wear a bra and feminine clothes is associated with femininity and identity and can increase the desire to socializeControlling symptoms strengthens femininity, renews desire for physical contact and sexual activity and prevents social isolationSymptom control made women feel the desire for intimacy, they felt safe and self-confident, which gave them a sense of freedom	Unique knowledge and insights into effects wound care interventions can have on attitudes, processes and experiences of patients with MFWsProvides new insights into the tabooed and overlooked experiences of patients with MFWs	Small sample sizeSampling procedure unclearInherent limitations from qualitative research design	9
Piggin and Jones³⁸Study origin:United Kingdom	Aims:Illuminate the nature, meaning and significance of living with a MFW through the description and interpretation of patient experiences.To allow the deeper meaning of living with a MFW, to fall within the clinicians reach and enable the facilitation of more empathetic approaches to care.Qualitative method:Heideggerian hermeneutic phenomenology	Sample:n = 5 femalesMedian age (range):NRStage of Cancer:NRLocation of MFW:NRDuration of MFW:NRAntimicrobialintervention:NRAntineoplasticintervention:NRConfidentiality sited	Symptoms:Wound appearanceMalodor	The MFW visibility provoked feared that it mirrored what was occurring internally and was a sign of mortalityMFWs and lack of control of symptoms resulted in an over-whelming sense of vulnerability, of living within a body that cannot be trustedWound appearance and malodor interfered with their family roleUncontrolled symptoms altered self-image and resulted in blame and guilt and self-imposed social isolationParticipants were still striving to be normal, yet felt different	Highlighted the importance of wound care on day-to-day livingImportance of adopting the phrase used by the patient to describe their woundHighlights the need to focus on subjective meaning of a visibly changing wound rather than objective measurements	Small sample sizeNo men (inclusion would have yielded richer textInterrater reliability not includedNo provision of recruitment or attrition dataInherent limitations from qualitative research design	10
Lo et al.³⁶Study origin:Taiwan	Aim:To explore the experience of cancer patients living with MFWs.Qualitative method:Grounded theory	Sample:n = 10 (6 females, 4 men)Mean age (range):54 (42–72) yearsStage of cancer:NRLocation of MFW:NRDuration of MFW:Median (range) = 9.86 (3–24) monthsAntimicrobialintervention:NRAntineoplastic intervention:NR	Symptoms:MalodorPainBleedingExudatePruritus	MFW, malodor and exudates caused embarrassment, a loss of femininity, sexuality, intimacy, and attractivenessBleeding and the MFW were visible sign of advanced disease, taking away the hope of recoveryWound appearance, odor, and exudates caused revulsion and shock leading to spoiled identity, relationship strain and self-imposed isolationLack of wound care guidance was stressful, time-consuming and led to uncontrollable and unpredictable symptoms and decreased QOL as the MFW became the center of their livesExpert helped participants live positively with the wound and improved QOL	Raises aware-ness of impact on daily living, the patients point of view, what specialist nurses can do to promote QOL, and the need for comprehensive assessment and training programsThe appropriate dressing can decrease symptoms	Small sample sizeData collection performed in only one settingOnly one cultural perspectiveNo provision of recruitment or attrition dataInherent limitations from qualitative research design	12
Alexander⁴²Study origin:Australia	Aim:To address the gap in knowledge (nonphysical issues associated with MFWs and how they might be addressed) by investigating the lived experience of malignant wounds from the perspectives of those living with it.Qualitative method:Hermeneutic phenomenology	Sample:n = 3 (2 females, 1 male)Mean age (range):71 (56–87) yearsStage of cancer:NRLocation of MFW:2 breast, 1 facial/scalpDuration of MFW:NRAntimicrobialintervention:NRAntineoplastic intervention:NR	Symptoms:MalodorPain	Advanced symptoms altered relationships with themselves and others, with little input into their new existence causing loss, confusion and disbeliefMalodor was the worst aspect of MFWs, and led to shame, embarrassment, depression, anxiety, frustration, and angerMFWs and malodor left care-givers with vivid memories for decadesWound appearance and pain signified the end of their lives causing fearPatients hoped for a peaceful and pain-free death, or a cure	First to explore the experiences of patients, caregivers and nurses, many new themes	Small sample sizeNo provision of attrition data and unclear recruitment dataInherent limitations from qualitative research design	12
Lund-Nielsen et al.³⁹Study origin:Denmark	Aim:To describe the experience of health care avoidance in women with advanced breast cancer who have developed malignant wounds.Qualitative method:Descriptive phenomenology	Sample:n = 17 femalesMedian age (range):69 (47–90) yearsStage of cancer:Stage IV breast cancerLocation of MFW:BreastDuration of MFW:Median (range) = 24 (3–84) monthsAntimicrobialintervention:NRAntineoplastic intervention:NR	Symptoms:MalodorPainBleedingExudatesPruritus	Participants felt disbelief: alone, with overwhelming responsibility and lack of resourcesWound appearance, odor, exudates led to shame, embarrassment, and blameMFW meant they surpassed any medical help one could receive, felt trapped and dissociated themselves from their bodiesTheir secrecy led to loneliness, depression, and hopelessnessOnce they sought professional help they felt full sharing of responsibility and total relief	Give support to find new positive reinforcementHealth care Team must pay special attention to these women neededResults transferable on a conceptual and theoretical level	Sampling procedure was unclearNo provision of recruitment or attrition dataInherent limitations from qualitative research design	11
Probst et al⁴⁰Study origin:Switzerland	Aim:To explore how women living at home with a MFW cope with such wounds.Qualitative method:Hermeneutic phenomenology	Sample:n = 9 femalesMean age (range):60 (40–76) yearsStage of cancer:Stage IV breast cancer 9Location of MFW:BreastDuration of MFW:Median (range) = >6 months (range NR)Antimicrobial intervention:NRAntineoplastic intervention:NR	Symptoms:MalodorPainBleedingExudatePruritusLymphedema	Malodor, pain, exudates, bleeding, and lymphedema led to embarrassment, shame, uncertainty and frustrationBleeding was unpredictable and uncontrolledAdvanced symptoms were labor intensive, consumed timePoorly managed pain decreased QOLSelf-perception changed with feelings of vulnerability, guilt, loss of normalcyKnowing how to care for wound returned a sense of normalcy	Uniquely describes how difficult it is to live and cope with a MFW	No provision of recruitment or attrition dataNo provision of strengths and limitations of the studyInherent limitations from qualitative research designSample limited to nine Caucasian women from the German part of Switzerland	11
Probst et al⁴¹Study origin:Switzerland	Aim:To understand the lived experiences of patients with a malignant fungating breast wound and their informal carers.Qualitative method:Hermeneutic phenomenology	Sample:n = 9 femalesMean age (range):60 (40–76) yearsStage of cancer:Stage IV breast cancerLocation of MFW:BreastDuration of MFW:Median (range) = >6 months (NR)Antimicrobial intervention:NRAntineoplastic intervention:NR	Symptoms:MalodorPainBleedingExudatePruritus	Malodor, pain, exudates, and bleeding led to embarrassment, shame, and isolationChanges in body image caused loss of femininity, loss of attractiveness, loss of sexuality leading to strategies to disguise their cancerVisualization of the MFW was a constant reminder of cancer with no hope for recoveryUncontrolled symptoms were unpredictable and contributed to isolation	Contributes to the under-standing that losing control over the body meant losing control over themselves and their lives	No provision of recruitment or attrition dataNo discussion of biasWeak ethics discussionNo provision of strengths and limitations of the studyInherent limitation from qualitative research design	11

Table 4.

Malignant Fungating Wound Symptom Descriptions by Patients from Qualitative Studies

Symptoms specific to MFWs	Selected descriptions	Number of articles with item
Pain^36–41	“My sleep and rest always break off because of slight to mild shooting and stabbing pain”³⁶	6
	“I only eat soft cold noodles and bread, because those can decrease my mouth wound pain”³⁶
	“Before I met the wound specialist I usually experienced moderate to strong pain even though I took analgesics”³⁶
	“I suffered so much from it. It was like someone stabbing your breast with a stick”⁴⁰
	“Sometimes I nearly burst because of this terrible pain. It was really terrible. I would cry.”⁴¹
Pruritus⁴¹	“…I tell you I would scratch night and day.”⁴¹	1
Exudate^36–41	“I cannot have a bra on or nice clothes. I am constantly afraid of seepage, and it (the wound) smells now”³⁷	5
	“I don't miss it (sex) because I know it will not be a pleasant experience, with the wound seeping like it does”³⁷
	“It was festering like a running nose”⁴⁰
	“I had to redo my dressing nearly every four hours because it was leaking”⁴⁰
	“Well, if it was festering…I had to change it over and over again. Yes, sometimes five to six times a day”⁴¹
Bleeding^{36,38,39–41}	“I always suffer from bleeding after a change of dressing or slight exercise…”³⁷	5
	“I first sought medical assistance for the wound when I couldn't stop the bleeding”³⁹
	“…I was sitting in the office with a client…lucky that I was wearing a jacket, because my bra and my blouse were again full of blood”⁴⁰
	“…because of the wound I could no longer go to the sauna.”⁴⁰
	“…happened so often. …you never knew if it would ooze or not”⁴¹
Odor^{36,38,40–42}	“Now, I am very ashamed and lose self-confidence, due to the malodour”³⁶	5
	“Mine has got a smell I know never goes away…”³⁸
	^“You cannot describe this smell. It is awful.”⁴⁰“You might compare it with the smell of a piece of rotting meat.”⁴⁰
	“That was very stressful for me especially when someone told me I stank”⁴⁰
	“…definitely the consciousness and the smell…the fact that everyone
	“Opening the front door I smelt a putrescent odour.”⁴¹
	“associates it like bad hygiene…”⁴²
	“…it was putrid, absolutely putrid, this smell would just knock the socks off you and it was just rotting flesh…”⁴²
	“It's got like that-that smell of death to it…”⁴²
Wound status^36,38,41	“…a lot of white coloured tissue? Is it slough? Is it…a sign of cancer cell spread?”³⁶	3
	“…it (wound) doesn't ever feel, or look, or smell good, neither does it make me feel good…”³⁸
	“But it gets bigger and bigger and I cannot wear a bra anymore.”⁴¹
Bulk effect of wounds or dressings³⁷	“When we have to go out, I can never have decent clothes on, so I decline many invitations”³⁷	1
Lymphedema⁴¹	“The problem is my swollen arm as well as the wound. I just want my free mobility back. I think I'd feel more normal then.”⁴¹	1

Table 5.

Qualitative Themes: Symptoms and Symptom Characteristics

Symptoms and symptom characteristics	Themes: symptoms and symptom characteristics	Sub-themes	Article(s)
MFW symptom occurrence in patients with advanced cancer	Multiple MFW symptoms usually occurred concurrently	Pain, malodor, exudate, bleeding, pruritus, perceived wound status, perceived bulk effect, and lymphedema were described by patients.	Alexander⁴²; Lo et al.³⁶; Lund-Nielsen et al.³⁷; Lund-Nielsen et al.³⁹; Piggins and Jones³⁸; Probst et al.⁴⁰; Probst, et al.⁴¹
MFW symptom occurrence in patients with advanced cancer	Multiple MFW symptoms usually occurred concurrently	Multiple MFW symptoms occurred concurrently and were described in vivid detail by patients and caregivers, at times years later.
MFW symptom timing in patients with advanced cancer	MFW symptoms were intermittent, unpredictable, and demanded constant caregiver attention	Symptoms such as bleeding and exudates were unpredictable and difficult to control.	Alexander⁴²; Lo et al.³⁶; Lund-Nielsen et al.³⁵; Lund-Nielsen³⁹; Piggins and Jones³⁸; Probst et al.⁴⁰; Probst et al.⁴¹
		The unpredictability of advanced symptoms threatened normalcy and led to anxiety and isolation.
		Lack of specialist-level wound care guidance resulted in suboptimal wound care that contributed to unpredictable symptoms.
		The lives of patients and their caregivers centered on symptom control and masking of symptoms.
MFW symptom severity in patients with advanced cancer	Symptom severity and control could either be a detriment to, or improve, psychological well-being and QOL	Pain was the most prevalent symptom, most often described as moderate to severe.	Lo et al.³⁶; Lund-Nielsen et al.³⁷; Lund-Nielsen et al.³⁹; Piggins and Jones³⁸; Probst et al.⁴⁰; Probst et al.⁴¹
		Lack of specialist-level wound care guidance resulted in suboptimal wound care that contributed to uncontrolled, increasingly severe symptoms.
		Lack of specialist-level wound care guidance necessitated self-reliance and creativity in symptom control by patients which improved self-confidence.
		Specialist-level wound care and appropriate wound care and symptom control restored normalcy and improved self-confidence, body image, socialization and QOL.
MFW symptom quality in patients with advanced cancer	MFW symptoms of perceived wound status (appearance) and perceived bulk effect resulted in impaired psycho-logical well-being and QOL	MFWs are visible signs of terminal disease and constant reminders of impending death, leading to fear.	Lo et al.³⁶; Lund-Nielsen et al.³⁷; Lund-Nielsen et al.³⁹; Probst et al.⁴⁰; Probst et al.⁴¹
MFW symptom quality in patients with advanced cancer		Bulk effect and wound status of MFWs impede clothing choices and women's body image and confidence.
MFW symptom distress in patients with advanced cancer	MFW symptoms resulted in suffering and poor QOL	Malodor was the most distressing symptom for patients and families, evoking vivid, deleterious memories by caregivers decades later.	Alexander⁴²; Lo et al.³⁶; Lund-Nielsen et al.³⁷; Lund-Nielsen et al.³⁹; Piggins and Jones³⁸; Probst et al.⁴⁰; Probst et al.⁴¹
		Lack of knowledge and pain-specific education led to suboptimal pain control by patients, caregivers and providers and increased distress.
		Malodor, exudates, lymphedema, wound appearance, and bleeding lead to embarrassment, shame, isolation and diminish QOL.
		Changes in body image caused loss of femininity, loss of attractiveness, and loss of sexuality.
		MFWs and symptoms contributed to role changes and relationship strain.
		The MFW appearance was a constant reminder of terminal cancer and impending death.
		Lack of specialist-level wound care guidance resulted in suboptimal wound care that was stressful, time-consuming, and forced patients to engage in ineffective and at times harmful self-management practices.

Results

Quality of the included studies

The overall quality of the 12 studies was adequate (mean = 11.58 ± 0.9, range from 10 to 13). The total population of all quantitative studies was 215 (mean = 43 ± 23.6, range from 22 to 70) and qualitative studies 65 (mean = 9.28 ± 4.5, range from 3 to 17). Detailed information regarding the quality of studies are presented in Table 1.

Sample characteristics

Consistent with the incidence of MFWs, this review also found that majority of study samples were women, older adults, and MFWs of the breast. The majority of the 215 participants in the quantitative studies were women (n = 135) and older adults (age >50 years). Three quantitative studies exclusively had women with breast MFWs,^32–34 one had a predominance of male subjects with MFWs of the head and neck,³⁵ and one study had an equal number of male (n = 34) and female (n = 33) participants with mixed MFW etiologies.³⁶ None of the studies included MFWs from genitourinary cancers. The 7 qualitative studies included 65 participants. The majority of participants were older female (92%), and 94% of participants had MFWs of the breast.^37–42

Symptoms of MFWs

Quantitative studies investigated symptoms related to MFWs in terms of symptom occurrence or prevalence of pain, malodor, exudate, bleeding, pruritus, and perceived bulk effect; yet no research investigate symptom occurrence of perceived wound status or lymphedema.^31,33,35,41 One qualitative study identified lymphedema and four qualitative studies perceived wound status (wound appearance) as distressing symptoms related to MFWs.^{36–38,41,42} None of the studies captured all eight reported symptoms of MFWs.

Symptom characteristics of MFWs

While quantitative research did not fully capture the characteristics of symptoms of MFWs, qualitative research provided rich descriptions of symptom characteristics (Table 4) in terms of timing, intensity, quality, and distress (Table 5).

Pain

Pain was the most frequently occurred symptom in patients with MFWs, ranging from 31.3% to 77.3%.^33,35 Pain occurrence was examined in terms of temporal characteristics: pain occurred in association with dressing changes; pain occurred either with (cyclic) or between (chronic) wound care or dressing changes.³⁴ Two studies found significant temporal associations between cyclic pain and wound care: fewer wound dressing changes were correlated with lower pain scores ([r = −0.274, p = 0.043];³⁴ [r = −0.428, p = 0.047]³³). Pain duration was measured in two studies.^33,34 One study found continuous pain in 40.9% of patients with MFWs of the breast.³³

Pain control was measured on an ordinal scale in only one study and found partially controlled to non-controlled pain ranged from 30% to 10%.³¹ Three different psychometric instruments were used to measure pain severity (intensity); the Verbal Rating Scale (none, slight, moderate, strong, intense),³¹ the Short Form-McGill Pain Questionnaire (SF-MPQ),³³ and the Malignant Fungating Wound Assessment Tool (MFWAT-P).³⁴ Pain intensity ranged from mild (50%–56%), to moderate (12%–27.3%), to severe (7%–19%).^31,33 Pain quality was measured in two quantitative studies utilizing the instrument of SF-MPQ and MFWAT-P and the most commonly occurring descriptors were “throbbing,” “shooting,” and “stabbing.”^33,34 Qualitative studies described pain quality as “stabbing,” “shooting,” and “bursting,” with intensity ranging from mild to severe (“terrible”).^36,40,41

Malodor

Malodor occurred in 11.9% of patients with MFWs.³¹ Malodor intensity ranged from slight (27%–50%), to moderate (25%–34%), to intense (0%–8%).³⁵ Qualitative studies described the quality of malodor as “garbage,” “rotting flesh,” “putrid,” and “moldy.”^36,41,42 Participants in one study likened the smell of the MFWs to a “cadaver.”⁴¹ Malodor is pervasive, caregivers recall altering their breathing patterns to avoid the smell and having vivid memories decades later.⁴²

Exudate

Exudate occurrence was 17.9% in patients with MFWs,³⁵ and exudate intensity ranged from slight (16%–31%), to moderate (61%–75%), to intense (8%–12%).³¹ Quality of exudates ranged from serous to purulent,^32,35 and amounts from small to moderate or large,^32,35 with the latter variable significantly associated with periwound moisture-associated skin damage (χ² = 4.41, p = 0.066).³² Five qualitative studies identified exudate as one of the most challenging and distressing symptoms to manage.^{36,37,39–41} Four qualitative studies described the feelings of shame and embarrassment due to exudate in patients with MFWs.^36,39,40,42 The negative emotions elicited by exudate undermined self-confidence and contributed to social isolation.^36,39,40,42

Bleeding

The occurrence of bleeding was 6% among patients with MFWs.³⁵ Intensity of spontaneous bleeding ranged from slight (3%–8%), to moderate (5%–10%), to intense (0%–11%).³¹ Intensity of induced bleeding ranged from slight (47%–60%), to moderate (12%–24%), to intense (0%–6%).³¹ Four qualitative studies described challenging personal accounts of bleeding associated with MFWs.^36,38–40 One woman recalled spontaneous bleeding during a work meeting, necessitating an impromptu clothing change.⁴⁰ Another spoke of bleeding after each dressing change and with “slight exercise,” necessitating constant dressing changes.³⁶ Bleeding led to uncertainty, lack of confidence, lack of control, avoidance of favorite pastimes, social isolation and feelings of impending death.^36,38–40

Pruritis

One quantitative study identified the prevalence of pruritus as 5.2%.³⁵ Pruritus intensity and quality was not investigated in quantitative studies, yet qualitative studies described pruritus as being extremely distressful, “…I can tell you I would scratch day and night.”⁴⁰

Perceived bulk effect and wound status

Only one quantitative study reported that 24% of patients with MFWs had perceived bulk effect that elicited negative emotions.³⁵ Five qualitative studies found that perceived wound status as a body disfigurement from the MFWs negatively impacted body image and self-esteem,^{36–38,41,42} leading to grief and loss of normalcy.^37,42 Three qualitative studies found that perceived bulk effect and wound status had a negative impact on femininity and sexuality.^36,37,40 Women reported a change in their body image (low self-esteem) and an inability to wear feminine clothes and a bra due to the bulk effect of dressings, leading to social avoidance.^37,40 Five studies found MFW appearance was a constant reminder of advanced and incurable disease, robbing patients of hope^{36,38,40–42} “…this wound looks as if death is more and more near me. I can't escape….”³⁶

Lymphedema

None of the quantitative studies identified lymphedema as a symptom of MFWs nor recorded its prevalence, intensity, or quality. One qualitative study described the distressful experience of a woman with a breast MFW and lymphedema.⁴¹ Lymphedema is known to have negative psychological and social impact on patients.²⁷ The participant with upper extremity lymphedema reported a sense of compromised normalcy, forcing her into isolation.⁴¹

Impact of symptoms on overall QOL and functional performance

Only one quantitative study examined the relationship between symptoms of MFWs assessed by the MFWAT and overall QOL measured by the McGill QOL questionnaire, however subscales were not reported.³⁴ This study found that number of symptoms per patient (r = −0.479, p = 0.049), pain (r = −0.479, p < 0.001), malodor (r = −0.293, p = 0.014), and bleeding (r = −0.280, p = 0.035) were correlated with poor overall QOL.³⁴ Several qualitative studies reported that malodor was the most distressing symptom to patients and caregivers.^{36,38,39,40,41,42}

None of the quantitative studies specifically investigated the impact of MFWs or symptoms of MFWs on functional performance, including dimensions of physical mobility, activities of daily living, participation in social activities. Qualitative studies provided rich data describing the devastating impact symptoms of MFWs on physical mobility, ability to perform activities of daily living, social interactions, and ability to work and participate in usual pastimes.^36–42 Table 6 summarizes the themes related to symptoms of MFWs and adverse impact of the symptoms on functional performance in the physical, social, occupational and psychological domains.

Table 6.

Qualitative Themes: Impact of Malignant Fungating Wound Symptoms on Functional Performance

Symptom impact on functional performance	Symptom(s)	Themes: functional performance impairment	Patient quotes	Article(s)
Physical:Impaired mobility and impaired activities of daily living	Pain, exudate, physiologic wound status, physiologic bulk effect, pruritus, lymphedema	MFW physiologic wound status (size, location), pain, and physiologic bulk effect limited movement of joints and extremities.Lymphedema associated with a breast MFW impaired upper extremity mobility.MFW physiologic wound status (size, location), pain, and exudate impaired ADLs; eating, bathing and dressing.	“I just want my free mobility back. I think I'd feel more normal then”	Probst et al.⁴⁰
			“I only eat soft cool noodles and bread, because those can decrease my mouth wound pain”	Lo et al.³⁶
			“Terrible…showering him all the time…it was a full-time job…”“But it gets bigger and bigger and I cannot wear a bra anymore”	Alexander⁴²; Probst et al.⁴⁰; Probst et al.⁴¹
			“My sleep and rest always break off because of slight to mild shooting and stabbing pain”	Alexander⁴²; Lo et al.³⁶
Social:Impaired interactions with family and members of the community	Pain, malodor, exudate, bleeding, perceived wound status	MFW perceived wound status (appearance), malodor, exudate, and bleeding limited interactions with family and community resulting in social isolation.	“I had to keep away from all those whom I cared about. I had to build a wall around myself…”“I didn't want them to see. I felt like a hunted animal”	Alexander⁴²; Lo et al.³⁶; Lund-Nielsen et al.³⁷; Lund-Nielsen et al.³⁹; Piggins and Jones³⁸; Probst et al.⁴⁰; Probst et al.⁴¹
Occupational:Impaired job-related task performance	Exudate, bleeding	Unpredictability of symptoms at work, such as bleeding and exudates, interfered with occupational tasks.Excessive caregiver burden led to an inability of caregivers to work.	“…sitting in the office with a client, yes, and I was lucky that I was wearing a jacket, because my bra and blouse were again full of blood”	Lund-Nielsen et al.³⁹; Probst et al.⁴⁰; Probst et al.⁴¹
Psychological:Impaired participation in pastimes, hobbies, and sharing personal concerns	Pain, malodor, exudate, bleeding, perceived wound status	MFW perceived wound status (appearance), pain, malodor, exudate, and bleeding interfered with pastimes, hobbies and sharing personal concerns with spouses and, family and friends.	“Yes because of the wound I could no longer go to the sauna”“…I worry about bleeding and leakage…I don't travel anymore”	Lo et al.³⁶; Lund-Nielsen et al.³⁹; Piggins and Jones³⁸; Probst et al.⁴⁰; Probst et al.⁴¹

ADLs, activities of daily living.

Discussion

This integrative review of the literature provided strong evidence that patients with MFWs suffered multiple symptoms, such as pain, odor, exudate, bleeding, pruritus, perceived wound status, perceived bulk effect and lymphedema. The major limitation of the quantitative studies was that none of the symptom measures used was able to capture the occurrence and characteristics of the totality of the identified symptoms of MFWs. The occurrence of perceived wound status and lymphedema as well as the intensity of pruritus, perceived bulk effect, perceived wound status, and lymphedema were not evaluated. Future research should focus on developing a clinical measure that is able to capture all the identified symptoms of MFWs as well as to assess that characteristics of the symptoms in terms of quality, intensity and duration. Interestingly, both quantitative and qualitative studies provided rich descriptors of pain, including nociceptive and neuropathic descriptors, to describe pain quality, such as “throbbing,” “shooting,” “stabbing,” and “bursting.” ^{33–34,36,40–41} This may indicate that pain related to MFWs has a mixed etiology. Future research should investigate the etiology of pain related to MFWs.

Qualitative studies have described intense, negative psychological effects from symptoms of MFWs, including; feelings of shame and embarrassment,^{8, 36,37,41} negative body image and self-esteem,^{8,36,37,38,40} and loss of femininity and sexuality.^36,37,40 These negative emotions undermined self-confidence, invoked anxiety and depression, and contributed to social isolation.^36,37,38,41 However, while qualitative studies did provide vivid descriptions regarding the negative impact of symptoms of MFWs on patients' functional performance and psychological well-being, this integrative review revealed a lack quantitative examination on the impact of symptoms of MFWs on functional performance or psychological symptoms.^31–35 Such significant gaps have impeded our understanding of symptoms of MFWs on functional performance impairment and QOL to ensure quality palliative care.

Strengths of the review and limitations of current literature

The strength of this literature review is its focus on the symptoms of MFWs in patients with advanced cancer and its quality review process.^27,28 Additionally, to limit selection bias, a broad inclusion criteria was established, and a variety of search strategies incorporating multiple data bases was utilized.²⁶

This review revealed that a variety of instruments were used to measure the symptoms and symptom characteristics associated with MFWs, however none of the tools was able to capture the full spectrum of symptoms identified in the literature.^31–35 There was an absence of quantitative research examining the impact of symptoms of MFWs on functional performance to ensure quality of palliative care for this population.^31–35

Limitations of the review

The heterogeneity of using different tools to assess MFWs and symptoms in the included quantitative studies limited the ability of the review for a formal meta-analysis. Additionally, the overwhelming majority of female participants, older adults, and participants with MFWs of the breast made generalizability of review findings to other populations impractical.

Conclusion

This review provided strong evidence that patients with MFWs suffer many symptoms, including, pain, malodor, exudate, bleeding, pruritus, perceived wound status, perceived bulk effect and lymphedema. Qualitative studies provided vivid description of the impact of symptoms on patients' functional performance. Methodologically rigorous quantitative studies are needed to comprehensively examine the symptoms of MFWs in terms of symptom occurrence, characteristics, and impact on functional performance. Development of a psychometric tool that is able comprehensively measures MFWs symptom occurrence, characteristics, and impact on functional performance is needed to assist researchers and clinicians to ensure quality palliative care among patients with advanced cancer.

Footnotes

Funding Information

Thank you to the American Cancer Society (ACS) DSCN-18-214-01-SCN.

Author Disclosure Statement

No competing financial interests exist.

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