Abstract
Background:
This study aimed to compare the effects of awareness and knowledge on demographic and clinical factors in patients with breast cancer-related lymphedema (BCRL) and gynecologic cancer-related lymphedema (GCRL) in the oncologic rehabilitation setting.
Methods and Results:
A total of 506 female patients with upper or lower extremity lymphedema, were evaluated for lymphedema education in their postoperative period. Only 74 survivors (25%) with BCRL and 34 survivors (16.83%) with GCRL reported that they had received information about lymphedema by physicians/primary health care providers. In breast cancer survivors, the time of diagnostic delay for lymphedema was shorter in the informed group (p < 0.001), and there was a higher rate of cellulite attacks in uninformed patients (p = 0.021). Duration between surgery and lymphedema was longer and duration of diagnostic delay for lymphedema was shorter in the informed group than uninformed group in gynecologic cancer survivors (p = 0.019, p < 0.001). There was a higher rate of cellulite history in the uninformed patients than informed patients in gynecologic cancer survivors (p < 0.001). In gynecologic cancer survivors who were educated about lymphedema were at an earlier stage than noneducated patients (p = 0.024).
Conclusion:
The rate of awareness about lymphedema among patients with a history of surgery for gynecologic malignancies is lower compared with those for breast cancer. In female cancer survivors, awareness and knowledge about lymphedema may lead to a later onset of lymphedema, lower lymphedema grades, and fewer infection.
Introduction
Gynecologic cancers affect 17% of the female population worldwide and 14% of the population throughout Europe. 1 According to the 2013 data of the Public Health Agency of Turkey, the most common type of cancer in women is breast cancer with a 24% incidence, followed by gynecologic [endometrial (10.1%), ovarian (5.9%), and cervical (4.2%)] cancers. 2
Lymphedema is defined as the accumulation of protein-rich fluid in the interstitial space and acquired functional impairment or absence of lymphatic flow and lymph nodes is held responsible for the pathophysiology of lymphedema. 3 Surgical procedures and chemotherapy and radiotherapy applications increase the possibility of developing lymphedema. 4 In particular, radiotherapy applied to the axillary or pelvic region and axillary, pelvic, and/or paraaortic lymph node dissection are considered as important risk factors for the development of secondary lymphedema due to female cancers. 4 The incidences of secondary lymphedema were reported to be 24%–56% for breast cancer, 23%–38% for endometrium cancer, 8.5%–22.5% for ovarian cancer, 13%–36% for cervical cancer, and 15.5%–61.2% for vulvar cancer.5,6
In gynecologic cancers, the survival and increased disease-free survival rates have been prolonged through early diagnosis and developments in treatment methods.5,7 However, this may also lead to the increased incidence of adverse effects secondary to treatment, such as lymphedema.3,7 If early diagnosis and appropriate treatment for lymphedema are not undertaken, the prognosis of lymphedema worsens, increasing the treatment cost and leading to functional impairment and psychologic problems, which, in turn, further deteriorates the patient's quality of life. 8 Providing the necessary information for the patients to take measures for the prevention of lymphedema is of great importance for both the patients and the success of the course of treatment. 8
Currently, a limited number of studies have been conducted that examine sources of awareness and knowledge in individuals with lymphedema.9–16 However, the majority of these studies have been mainly focused on lymphedema seen in breast cancer survivors.9–15 Only one study has reported the awareness and education among individuals in subsets of patients with secondary lymphedema other than breast cancer survivors. 16 This study aimed to determine the patients' awareness and education about lymphedema and compare the effects of awareness and education on demographic and clinical factors in patients with breast cancer-related lymphedema (BCRL) and gynecologic cancer-related lymphedema (GCRL) in the oncologic rehabilitation setting.
Materials and Methods
This retrospective study included patients who were diagnosed with BCRL or GCRL, which was assessed according to the criteria from the 2016 Consensus Document of the International Society of Lymphology in an oncologic rehabilitation unit between January 2018 and March 2020 (Ref. 3 ). All participants completed the informed consent form. The inclusion criteria were: having undergone surgery due to breast or gynecologic malignancies, being between 18 and 85 years of age, and having symptoms of lymphedema (sense of weight, discomfort, pain and/or swelling in unilateral or bilateral upper or lower extremities or the genital area). The exclusion criterion was having the presence of any mental or psychologic problem that might not be eligible for education. This study conformed to the principles of the Helsinki Declaration, and approval of the local Ethics Committee of the medical institution was obtained before the study.
The following parameters were recorded: age, body mass index, educational level, type of cancer, number of dissected lymph nodes, number of positive lymph nodes, application of chemotherapy or radiotherapy, duration of time after surgery, duration of lymphedema, duration between surgery and diagnosis of lymphedema (time from surgery to the diagnosis of lymphedema), duration of diagnostic delay for lymphedema (time from the development of clinical symptoms of lymphedema to the diagnosis of lymphedema), stage of lymphedema according to percentage of difference [minimal (>5% to <20% increase in limb volume), moderate (20%–40% increase), or severe (>40% increase)], history of cellulitis, presence of pain (visual analog scale [VAS]), and clinical findings. 3 Circumferential measurements depend on well-defined distances along the limb, but hand and foot volumes cannot be included. This method also provides information on the localization of these swelling. In our clinical practice, the circumferences of the limb are measured for every 4 cm along the limb from the wrist/ankle and upto the axilla/symphysis pubis and the volume is calculated according to the truncated formula in upper/lower extremity lymphedema (V = 1/3 × π × h × (r12+r22+r1 × r2).3,17
The patients were asked the following questions for awareness and knowledge about lymphedema at first visit at the oncologic rehabilitation unit for lymphedema. These questions created from lymphedema expert suggestions are as listed below. 18
(a) Have they been informed by a physician/primary health care provider about the possibility of developing lymphedema secondary to surgery or chemotherapy or radiotherapy during the course of cancer treatment in the preoperative, postoperative, or follow-up stages?
(b) Did a physician/primary health care provider talk about risk factors for lymphedema, life style changes, and early self-detection?
(c) Did a physician/primary health care provider tell the patient what to do to protect the patient from lymphedema?
(d) Did a physician/primary health care provider mention the early signs and symptoms of lymphedema (unilateral/ipsilateral aching, heaviness, tightness, fullness, or stiffness) that often precede visible swelling and should ask about clothing or jewelry becoming tighter or patient-perceived swelling.
(e) Did a physician/primary health care providers tell where and how patient may refer when lymphedema develops (a reliable specialist as a point of contact)?
(f) Did a physician/primary health care provider support what she told with visual material and gave patient a brochure about care, prevention, and exercises?
(g) Did a physician/primary health care provider answer the question when the patient asked about the things she did not understand during the interview?
(h) Were the information about lymphedema understandable?
If the patient answered “yes” to all of the questions, the authors included the patient in the educated patient group for lymphedema.
Statistical analysis
Statistical analysis was performed using the Statistical Package for the Social Sciences software (SPSS Version 23.0; IBM, Armonk, NY). The normality of distribution was evaluated using visual and statistical method of Kolmogorov–Smirnov. The comparison of groups, the independent samples t test (normal distribution), and the Mann–Whitney U test (non-normal distribution) were used for the quantitative data. The Pearson's chi-squared test was used to test the differences in rates. Significance was accepted as p < 0.05.
Results
The study included 370 female patients with BCRL with a mean age of 55.14 ± 12.60 (26–81) years and 236 female patients with GCRL with a mean age of 61.74 ± 9.08 (29–83) years. Thirty-four of the patients (16.83%) with GCRL reported that they had knowledge about lymphedema and/or that they had been given information about lymphedema by physicians/primary health care provider, while the remaining 202 patients (83.17%) were neither informed nor educated about lymphedema during the course of the gynecologic cancer treatment in the preoperative, postoperative, or follow-up stages. The demographic and clinical characteristics of the patients with GCRL grouped according to lymphedema awareness and knowledge are shown in Table 1.
The Demographic and Clinical Characteristics of Patients with Gynecologic Cancer-Related Lymphedema with Regard to Education for Lymphedema
Bold and italic indicates significiant values of p < 0.05.
p: Independent sample t test.
p: Pearson's chi-squared test.
p: Mann–Whitney U test.
BMI, body mass index; IQR, interquartile range; n, number of patients; SD, standard deviation; VAS, visual analog scale.
Seventy-four patients with BCRL (25%) stated that they had knowledge about lymphedema and/or that they had been given information about lymphedema by physicians/primary health care provider while the remaining 296 patients (75%) were neither informed nor educated about lymphedema during the course of the breast cancer treatment in the preoperative, postoperative, or follow-up stages. The demographic and clinical characteristics of the patients with BCRL grouped according to lymphedema awareness and knowledge are shown in Table 2.
The Demographic and Clinical Characteristics of Patients with Breast Cancer-Related Lymphedema with Regard to Education for Lymphedema
Bold and italic indicates significiant values of p < 0.05.
p: Independent sample t test.
p: Pearson's chi-squared test.
p: Mann–Whitney U test.
GCRL patients educated about lymphedema were at an earlier stage than noneducated patients (p = 0.024). In informed group of GCRL patients the duration between surgery and lymphedema was longer (p = 0.019). Duration of diagnostic delay for lymphedema was shorter in the informed GCRL patients' group (p < 0.001). The rates of cellulitis history and number of cellulite attacks of lower extremities were higher in uninformed GCRL patients (p < 0.001, p < 0.001) (Table 1). In GCRL patients there are no difference at the rates of pain and VAS scores in patients with pain between two groups.
In BCRL patients, there was no difference between the informed and uninformed patient groups in terms of the stage of lymphedema, duration of lymphedema, and the duration between surgery and lymphedema development (p > 0.005). The duration of diagnostic delay for lymphedema was shorter in the informed group than uninformed group of BCRL (p < 0.001). The number of cellulitis attacks and skin infections in affected side was higher in the informed group than un-informed group of BCRL (p = 0.021) (Table 2).
The comparison of the clinical and demographic data of BCRL and GCRL patients who had received information about lymphedema are shown in Table 3. Educated patients about GCRL were older than educated patients with BCRL (p = 0.036). The number of lymph nodes removed during the operation was statistically significantly lower in BCRL patients than in GCRL patients (p < 0.001). Duration of diagnostic delay for lymphedema was shorter in GCRL patients than in BCRL patients (p = 0.014) (Table 3).
Comparison of Clinical and Demographic Data of Upper and Lower Extremity Lymphedema Patients Educated for Lymphedema
Bold and italic indicates significiant values of p < 0.05.
p: Independent sample t test.
p: Pearson's chi-squared test.
p: Mann–Whitney U test.
Discussion
Although lymphedema patient information sources have previously been reported in several studies, the primary population of these studies were patients with BCRL.9–16 To the best of our knowledge, this study is the first to compare the effects of awareness and knowledge about lymphedema development on demographic and clinical factors in both BCRL and GCRL patients.
The results of this study indicate that knowledge and awareness about lymphedema among patients with GCRL was lower compared with those with BCRL. The study found that the time of diagnostic delay for lymphedema was shorter and the rates of cellulite history was lower in the informed groups among these female cancer survivors with both lower or upper extremity lymphedema. The informed group of GCRL patients had lower-stage lymphedema and earlier referral timing to lymphedema units than the uninformed group.
Studies evaluating lymphedema knowledge or awareness about BCRL reported that the level of knowledge was low.8,9–15,19,20 In a study conducted by Borman et al. from Turkey, it was emphasized that only 19% of the patients who developed lymphedema after breast cancer had knowledge and awareness about their condition. 10 In the present study, 25% of BCRL patients had knowledge and awareness about lymphedema. Both studies were conducted on patients of similar age at a similar and low educational level in the same country. Higher education level can positively affect patients' awareness of lymphedema. It was promising to see that within the 3 years between the two studies, the knowledge and awareness of patients had increased from 19% to 25% (Ref. 10 ). In addition, we found that only 16.83% of gynecologic oncology patients with lymphedema had knowledge and awareness about their condition. This rate being lower in GCRL patients than BCRL patients can be attributed to the older age of GCRL patients or different surgical specialties. In our study, although there was no difference in the formal education between the patients in the two groups, the decrease in the perception and attention of the elderly population can explain these findings. 21 Similarly, Kwan et al. showed that awareness among BCRL patients might be related to age. 11 Another explanation may be that since surgical procedures performed in gynecologic malignancies have a wide range, and therefore as one of the long-term complications, lymphedema may not be the first concern. We consider that it may be a good idea for patients scheduled for gynecologic malignancy surgery to be informed about lymphedema in the preoperative period as prehabilitation.
In a review by Keast et al. referring to both primary and secondary upper and lower extremity lymphedema cases, it was emphasized that in addition to the insufficient awareness of the patients, physicians/primary health care provider lacked knowledge and information concerning the etiology and management of this condition. 8 Tam et al. showed that lymphedema awareness was low among health care professionals who provided health services for breast cancer patients. 22 Therefore, we think that it is important to inform surgeons and nurses who play an active role in patient care in the postoperative period and other health care professionals in close dialog with the patient about lymphedema. We have recommended the physicians should discuss lymphedema prevention strategies and make suggestions that are supported with written materials to ensure that patients know which medical facility to attend if they think that they have lymphedema. In addition, the patient's encounter with other patients with lymphedema during his/her visit to oncologic rehabilitation unit may lead to a better understanding of the concept of lymphedema, previously unknown to him/her. Some previous studies reported that information provided by clinical staff or booklets/leaflets about lymphedema played an important role in minimizing the risk of this condition. 19 In a study by Fu et al., it was suggested that supporting lymphedema awareness with written materials strengthened patients' self-management of the condition. 9
In the present study, the duration of diagnostic delay for lymphedema in both upper and lower lymphedema were shorter in the informed group than others. Considering that there was no difference between the groups with and without lymphedema in terms of cancer and treatment details (cancer type, number of lymph nodes removed during the operation, number of positive lymph nodes, and presence of chemotherapy and radiotherapy), the difference between the lymphedema duration of the two groups can be attributed to the awareness and knowledge of the patients. We consider that informed patients are more likely to protect themselves against lymphedema, implement the recommended preventive strategies, and develop lymphedema later. Similarly, Sherman et al. mentioned that lymphedema awareness could minimize behaviors that increased the risk of lymphedema and emphasized the importance of patient education for the diagnosis and treatment of this condition. 23 As also suggested in previous publications, as the time spent as a lymphedema increases, the quality of life decreases, health-related cost increases, and labor force decreases.8,24
The shorter duration of diagnostic delay of lymphedema suggests that patients did not need to look for an appropriate health center for the diagnosis of their condition. In our study, the Informed groups rapidly presented to the oncologic rehabilitation unit because they had already been informed about what to do. Duration of diagnostic delay for lymphedema was shorter in GCRL patients than in BCRL patients in our study. It is also predictable that the diagnostic delay in GCRL patients could be less because of lower extremity lymphedema, which can be more severe at presentation, more symptomatic, and noticeable given the lower extremity use. Most common symptoms experienced by patients with lower extremity lymphedema are similar to upper extremity lymphedema symptoms; however, intensity and distress scores were higher in lower extremity lymphedema patients. 25
In the current study, the GCRL patients who were previously informed about lymphedema was at an earlier stage of the disease. Since educated patients are more aware of the subject and the possibility of lymphedema development, they recognize the signs of discomfort and minimal edema mostly seen in early stages of lymphedema; thus, these patients present to oncologic rehabilitation setting in the early period and receive an early diagnosis.20,26 In the treatment of lymphedema, one of the most important prognostic factors of response to treatment is the stage of lymphedema at the time of diagnosis.3,8,17 This study suggested that informing gynecologic cancer patients about lymphedema will contribute to their treatment in the event of possible lymphedema and facilitate the treatment process, and this can be considered as a positive prognostic factor for the treatment of this condition.
Cellulitis is a common condition in patients with lymphedema, especially in later stages. 27 To prevent cellulite, it is recommended to perform skin care properly and regularly and to protect the integrity of the skin. Cellulitis adversely affects the prognosis and disrupts treatment efficiency in patients with lymphedema. 28 In the current study, the number of cellulitis attacks was lower in the informed patients with both BCRL and GCRL compared with the uninformed patients. Ya-Chen et al., who followed up breast cancer patients for 2 years, reported that the development of lymphedema has increased the cost of treatment, and skin infections have a significant share in this cost. 29 In another study, it was shown that the number and severity of cellulitis history of lower extremity lymphedema were higher than upper extremity lymphedema, and infections increased the cost of treatment in lymphedema patients. 30 Also, patients with cellulitis need to take antibiotic treatment for a long time and sometimes require hospitalization.28,29 The results of our study revealed that the patients without any awareness concerning lymphedema were more likely to develop cellulitis. Cellulitis adversely affects the treatment, increases the cost of treatment, and may lead to an increase in the lymphedema stage of the patient or even trigger the development of lymphedema. 30 This study suggested that raising the awareness of patients with lymphedema to be more conscious about skin care and providing them with prevention strategies can protect this patient population from cellulitis.
This study has some limitations. First of all, retrospective study design is the main limitation. Second, the study only obtained perceived knowledge of lymphedema, rather than using any objective measurement of lymphedema knowledge. Third, the results of the study should be considered with respect to selection bias as the results are based only on the information sources reported by patients.
In conclusion, this study is the first to compare the effects of awareness and knowledge about lymphedema in BCRL and GCRL patients. According to the data of this study, only one in four patients with BCRL and one in six patients with GCRL had been made aware about lymphedema. Patients that do not receive any information about lymphedema are more likely, in the early period, to develop lymphedema after surgery. Since they have not taken the necessary precautions, they face complications, such as cellulitis. Providing oncologic surgery patients with adequate information on lymphedema or referring them to the oncologic rehabilitation unit to provide them with the necessary information can reduce the time it takes to make lymphedema diagnosis and facilitate patients' referral to an appropriate center when lymphedema develops. Physicians/primary health care providers must educate their patients about lymphedema at preoperative (prehabilitation) and postoperative rehabilitation visits. Lymphedema education and preventive measures should be included in patients' care plans for early diagnosis, and early referral to treatment.
Footnotes
Author Disclosure Statement
No competing financial interests exist.
Funding Information
The authors didn't receive any financial support for the research and/authorship of this article.
