1 Iva Grgić
2 Melita Rukavina
2 Olivera Petrak
1 Special Hospital for Medical Rehabilitation Krapinske Toplice, Krapinske Toplice, Croatia
2 University of Applied Health Sciences, Zagreb, Croatia
Article received: 04.01.2024.
Article accepted: 26.03.2024.
https://doi.org/10.24141/2/8/2/11
Author for correspondence:
Melita Rukavina
University of Applied Health Sciences Mlinarska 38, Zagreb, Croatia
E-mail: melita.rukavina@zvu.hr
Keywords: lymphedema, breast cancer, everyday activities, mental health
Breast cancer remains the most common malignant disease among women, accounting for 24% of all malignant diseases (1-3). In the Republic of Croa- tia, 2,500 women are diagnosed with breast cancer annually (4). The mortality rate is declining due to prevention, which raises awareness among women about self-examinations and regular check-ups, as well as aggressive and radical breast cancer treat- ments that often lead to arm lymphedema. In West- ern Europe, lymphedema primarily occurs because of breast cancer treatment. The first treatment choice for cancer is surgery, which largely depends on the size of the tumour and the breast itself. The most radical form of surgery is a mastectomy, where the breast and nipple are removed, although reconstruc- tion can be performed during the first operation or later. Segmentectomy or quadrantectomy is a breast- conserving surgery where only the tumour area is removed (5). However, since the breasts are rich in lymphatic vessels that extend to the axillary lymph nodes, cancerous cells may spread to that region. Therefore, axillary lymph node dissection is often performed, which can lead to arm lymphedema (4,6).
Lymph nodes play a crucial role in the biological fil- tration of the body, destroying harmful substances, regulating proteins in the lymph, and depositing harmful substances that cannot be eliminated (7). The lymphatic system also collects cerebrospinal fluid and has an immune function by destroying harmful substances through phagocytosis. Thus, the removal of lymph nodes from the axillary region can result in complications such as loss of sensation in the operated area, discomfort in the back of the arm, swelling in the axillary region immediately after sur- gery, and lymphedema. Lymphedema is defined as a chronic inflammatory lymphostatic disease caused by mechanical insufficiency. The increasing volume of lymph accumulating in the tissue, which the lym- phatic system cannot remove, creates a burden that results in edema. Damage to lymphatic vessels dis- rupts antigen transport, which can lead to infection.
The incidence of upper limb lymphedema is 17% and increases in the two years following the breast cancer diagnosis or surgery. However, it is highly variable, and the timing of lymphedema onset is un-
predictable. Lymphedema may develop immediately, a few days, months, or even years after surgery as a result of an external factor. Swelling in the axil- lary region may subside within days after surgery or become permanent (8). The incidence is four times higher in patients who had axillary lymph node dis- section compared to those who had sentinel lymph node biopsy (9-11). In addition to surgery, which is the most common cause of lymphedema, radiation therapy can damage part of the lymph nodes in the affected region, as can individual factors such as ex- cessive activity, inactivity, infection, injury, or weight gain (1).
The onset of lymphedema is characterized by a tight wristwatch or tight sleeve. Patients may complain of a feeling of heaviness and fullness in the affected region, stiffness in the upper limbs, and mild swelling that subsides. Dry skin can also be a significant is- sue, as it may lead to infections, requiring proper skin care. Patients also complain of pain and difficulty per- forming everyday activities, as well as challenges in finding appropriate clothing. Lymphedema also visu- ally deviates from the standard concept of beauty, which can negatively affect the psychological state of a person and may influence their social life (10).
Lymphedema can have various stages, ranging from the initial latent phase, where edema is not yet vis- ible, to the final stage, where atrophic changes to the skin occur, and the edema becomes irreversible (12).
Physical illnesses are often accompanied by unpleas- ant emotional states such as stress, anxiety, and de- pression, particularly when dealing with life-threat- ening diseases. Besides the threat to life, breast cancer treatment can provoke intense negative emo- tions in women, especially when it involves partial or complete removal of the breast, as breasts are associ- ated with motherhood and feminine beauty. If treat- ment includes chemotherapy, hair loss (alopecia) can occur, which many women also find difficult to cope with, in addition to the possible onset of lymphede- ma. Therefore, the diagnosis and treatment process bring a multitude of negative emotions that women must confront. The occurrence of lymphedema has a detrimental effect on performing everyday activi- ties, which can further negatively impact both physi- cal and mental health, leading to stress, anxiety, and even depression. Daily activities are crucial for every individual’s mental well-being. Patients who have un- dergone breast cancer surgery and have had axillary lymph node dissection are forced to adjust their daily
activities, and in some cases, avoid certain activities to prevent worsening of their arm condition. It is im- portant to educate patients to detect lymphedema as early as possible and to start rehabilitation to pre- vent lymphedema escalation (1), as well as to teach them how to live with lymphedema and adapt their everyday activities to this condition.
Avoiding injury in the lymphedema-affected area in- cludes avoiding injections, depilation, and any activi- ties that might worsen the condition. Heat, not only during the summer months, as well as steam from cooking and baking, can be harmful. For example, ironing can be risky due to the potential burns and strains on the arm. Patients with lymphedema should avoid wearing tight clothing and anything that might cut into the skin, as this restricts lymph flow. Pa- tients should be informed about precautionary meas- ures, including avoiding blood pressure measurement on the arm with lymphedema. Overexertion, such as household chores like window washing or gardening, should also be avoided. Patients need to be made aware of the benefits of regular exercise, maintain- ing a healthy body weight, and proper skin care (12). Shaving and depilation can damage the skin, so the use of depilatory creams is recommended. During cooking or baking, it is advisable to place a wet cloth on the arm, and if tingling occurs during activities, rest is required. Additionally, patients should be edu- cated about self-bandaging, which significantly eas- es the performance of daily activities (12).
To determine the perception of the impact of arm lymphedema on the performance of everyday ac- tivities and the mental health of women who devel- oped lymphedema due to breast cancer treatment. Additionally, the aim is to examine the correlation between these variables and different sociodemo- graphic characteristics, as well as certain aspects of the disease.
Table 1. Sociodemographic data of participants with arm lymphoedema (N=100) | ||
Frequency | ||
single | 6 | |
in a relationship | 5 | |
Marital status | married | 69 |
divorced | 15 | |
widowed | 5 | |
primary education education | 2 | |
Education | secondary education | 51 |
higher education | 21 | |
high education | 26 | |
village | 18 | |
Place of living | small town | 144 |
town | 68 | |
below average | 17 | |
Income | average | 72 |
above average | 11 | |
The sample in this research includes 100 participants who, after breast cancer treatment, were diagnosed with arm lymphedema. The average age of the par- ticipants is 52.3 years (SD=9.69), with the young- est participant being 31 years old and the oldest 74 years old. The sample consists of members of asso- ciations that gather women diagnosed with breast cancer which include: “Sve za nju” and “Nismo same” from Zagreb, “Caspera” from Split, and the “Nada” association from Rijeka. Table 1 shows the sociode- mographic data of the participants. The mentioned frequencies also represent percentages.
Two validated measuring instruments were used in this study: the Lymphedema Quality of Life Ques- tionnaire (LQOLQ) for the Upper Limb and the De- pression, Anxiety, and Stress Scale (DASS-21), along with additional questions about sociodemographic data and some aspects of the disease and the onset of lymphedema.
The Lymphoedema Quality of Life Questionnaire for the Upper Limb by Keeley et al., from 2010, was translated by the authors for the purposes of this study. The questionnaire contains 21 statements grouped into 4 domains: questions 1 (a-h), 2, and 3 relate to function (e.g., “How much does your swelling arm affect your daily activities such as work, house- work, or leisure and social activities?”), questions 4-8 pertain to appearance (e.g., “How much do you feel the swelling affects your appearance?”), questions 9-14 describe symptoms (e.g., “Have you had trou- ble sleeping?”), and questions 15-20 describe mood (e.g., “Have you felt worried?”). The overall quality of life is assessed by question 21. Participants rate on a 4-point scale how much lymphedema affects a par- ticular daily activity, where 1 means “not at all” and 4 means “a lot” (13). The total result is expressed as the average value of all statements within each sub- scale, with a higher score indicating a worse condi- tion. For overall quality of life, a lower score indicates lower quality, and it is rated on a scale from 0 (poor) to 10 (excellent).
The validation of this questionnaire was conducted by Wedina et al. (2019) on a Swedish sample. The research showed that the questionnaire is simple, clear, and not too long for use with patients with arm lymphedema, making it a useful tool in clinical prac- tice. The validity of the questionnaire was found to be high, and the perceived lymphedema was signifi- cant in the domains of function and appearance. The reliability of the questionnaire ranged from 0.53 to
0.87 (14). Pas et al. (2015) demonstrated good inter- nal consistency and reliability for the second part of this questionnaire, focused on the lower extremities, and a good correlation with the physical component of the SF-36 short form, indicating good validity (15). Borman et al. (2018) also found high reliability of the questionnaire on a Turkish population (16). This study also showed high reliability for all subscales: function (0.91), appearance (0.92), mood (0.91),
symptoms (0.92).
The Depression, Anxiety, and Stress Scale (DASS-21), by Lovibond and Lovibond (1995), with a Croatian adaptation by Jokić-Begić, Jakšić, Ivezić, and Sura- nyi (2012), was used to measure mental health. The DASS-21 assesses the frequency and intensity of negative emotions over the past week and con- tains 21 statements, with 7 statements in each of the three subscales (stress, anxiety, and depression). Each subscale is rated on a 4-point scale, where 0 means “does not apply to me at all,” and 3 means “ap- plies to me very much or most of the time” (17-19). The maximum score on each subscale is 42, and the scales are divided into categories: normal, mild, mod- erate, severe, and extremely severe. Each subscale has its critical value; for depression, a score above 9 is critical, for anxiety above 7, and for stress above
14. Scores below the critical value are considered
normal. According to Cronbach’s alpha, the reliabil- ity for depression is 0.90, for anxiety 0.89, and for stress 0.91, with the overall scale reliability being
0.96 (20-21).
The survey was conducted online from March to June 2023. The representatives of the associations for- warded the questionnaire to their members, who, after breast cancer treatment, were diagnosed with arm lymphedema, along with a request to partici- pate in the research. All participants voluntarily took part in the study. The survey was conducted anony- mously, and filling out the questionnaire took 10 to 15 minutes. Approval was obtained from the Ethics Committee of the University of Applied Health Sci- ences Zagreb, as well as consent from all associa- tions whose members participated in the research.
Descriptive and inferential statistical measures were used in data processing. The normality of distribution for nine quantitative variables (age and total scores on the subscales) was tested using the Kolmogorov- Smirnov test, which showed that the distributions of seven variables significantly deviated from normal. However, additional checks of skewness and kurtosis showed that skewness did not exceed recommend- ed values (22), as the highest skewness score was
-0.65, and the highest kurtosis was -1.361. There- fore, given the relatively large sample size, we de- cided to apply parametric statistical procedures.
The average time elapsed since the diagnosis of a breast cancer was 5.77 years, while the median was 4 years. The range of results was from 4 months to 25 years. Information related to arm lymphedema is shown in table 2. Frequencies also represent a per- centage since the number of participants is 100.
Lymphedema occurs on both left and right arm, and 9% of women have lymphedema on both arms. Most of the participants are involved in some form of therapeutic treatment for lymphedema. Relapse is not very frequent; it occurs in only 6% of the par- ticipants. The following is a presentation of the aver- age results of the quality of life subscales obtained by the LYMQOL questionnaire, as well as of mental health obtained by the DASS-21 questionnaire.
Table 2. Information on arm lymphedema | ||
frequency | ||
right | 95 | |
Dominant hand | ||
left | 5 | |
right | 46 | |
Arm with lymphedema | left | 45 |
both | 9 | |
yes | 72 | |
Therapy for lymphedema | ||
no | 28 | |
yes | 6 | |
Relapse | ||
no | 94 | |
From Table 3, we can conclude that the women’s function or daily life activities, appearance and mood are impaired to a lesser extent, while the symptoms are somewhat more present in the majority of the sample. The overall assessment of the quality of life is slightly above the theoretical average, which indi- cates moderate satisfaction (M=5.49; SD=2.12).
Arithmetic values for all three subscales of the DASS-21 questionnaire are higher than their critical values. In order to check what proportion of female re- spondents achieves high results on that questionnaire, Table 4 shows the distribution by categories from nor- mal to very serious for all subscales (in percentages).
Table 3. Average scores of subscales of the quality of life questionnaire (LYMQOL) and mental health (DASS-21) of women with arm lymphedema (N=100) | |||||
Questionnaire | Subscale | Mean | SD | Minimum | Maximum |
Function | 2.01 | 0.607 | 1 | 3.7 | |
Appearance | 2.21 | 0.808 | 1 | 4 | |
LYMQOL | Mood | 2.39 | 0.704 | 1 | 4 |
Symptoms | 2.62 | 0.775 | 1 | 4 | |
Quality of life | 5.49 | 2.12 | 0 | 10 | |
Stress | 22.56 | 10.847 | 0 | 42 | |
Depression | 16.92 | 12.386 | 0 | 42 | |
DASS-21 | |||||
Anxiety | 16.52 | 11.373 | 0 | 42 | |
Total | 56.00 | 32.345 | 0 | 122 | |
Table 4. Proportion of respondents by subscale categories of the DASS-21 questionnaire | |||
Stress | Anxiety | Depression | |
normal | 23 | 23 | 40 |
mild | 4 | 12 | 5 |
moderate | 20 | 9 | 10 |
severe | 42 | 11 | 11 |
extremely severe | 11 | 45 | 34 |
Almost half of the respondents have a severe to ex- tremely severe state of depression (45%), while in terms of stress, the proportion of women in these categories is 53%, and in terms of anxiety, even 56%. In order to check the relationship of certain sociodemographic variables with aspects of quality of life and mental health, additional analyses were conducted. We used the analysis of variance to check whether there are statistically significant differences regarding to women’s financial situation. There were 72 respondents in the group with below average in- comes, 11 female respondents with average, while the group with above average incomes included 17 women.
Significant differences were obtained for all three subscales of the DASS-21, and for the quality of life of the LYMQOL. Post hoc Scheffe test showed that for anxiety, depression, stress, and quality of life there is a difference between women with below-av- erage and above-average incomes; significances are
0.017 for stress, 0.025 for anxiety, 0.037 for depres- sion and 0.043 for quality of life. Respondents with below-average incomes have a lower stress, anxiety,
and depression, with stress also showing a differ- ence compared to women with average incomes. It is interesting that they are more satisfied with the quality of life than respondents with above-average incomes. Arithmetic means are shown in the Table 5. It should be kept in mind that these categories are not based on objective criteria given the fact that the participants assessed which category they belong to. Also, there is a considerable disproportion in the size of the comparison groups, so these findings should be taken with some caution. For place of living and marital status, no statistically significant differences were obtained in relation to the observed variables. Regarding the level of education, two low-educated participants were excluded from the comparison, and a significant difference was found only for the over- all quality of life (F=4.093; p=0.009): women with a higher education (M=6.23) are significantly more satisfied with the overall quality of life compared to those with secondary education (M=4.82).
The subscale mood is significantly related to age (r=- 0.329; p=0.001): older respondents rate their mood as better than younger respondents. Age is also statistically significantly related to depression (r=- 0.220; p=0.028), anxiety (r=-0.287; p=0.004) and stress (r=-0.247; p=0.013), but the correlations are low: older women show lower levels of depression, anxiety, and stress. All subscales of the DASS-21 questionnaire correlate with the subscales of the quality of life questionnaire in such a way that a more pronounced unpleasant emotional state is as- sociated with a worse status of various aspects of quality of life. The more pronounced the anxiety, the worse the function, symptoms and appearance of the women are. Overall quality of life is negatively related to stress (r=-0.489; p=0.00), anxiety (r=- 0.461; p=0.00) and depression (r=-0.485; p=0.00). Appearance is related to stress (r=0.495; p=0.00),
Table 5. Descriptive statistics and ANOVA results for subscales of depression, anxiety, stress, and quality of life regarding women’s financial status | ||||||||
Below average income | Average income | Above average income | ||||||
Mean | SD | Mean | SD | Mean | SD | F | p | |
Anxiety | 14.61 | 10.581 | 19.27 | 10.555 | 22.82 | 13.040 | 4.203 | 0.018 |
Depression | 14.83 | 11.461 | 20.73 | 13.864 | 23.29 | 13.171 | 4.024 | 0.021 |
Stress | 20.25 | 10.583 | 28.73 | 5.884 | 28.35 | 11.118 | 6.481 | 0.002 |
Quality of life | 5.78 | 2.118 | 5.36 | 2.111 | 4.35 | 1.835 | 3.271 | 0.042 |
anxiety (r=0.512; p=0.00) and depression (r=0.549; p=0.00): the more pronounced the women’s percep- tion that lymphedema affects their appearance, they experience unpleasant emotions to a greater extent. The correlation is also present in the function in re- lation to stress (r=0.542; p=0.00), anxiety (r=0.520; p=0.00) and depression (r=0.540; p=0.00).
In this research, we were interested in how women with arm lymphedema caused by breast cancer per- ceive the impact of lymphedema on their lives. The results of the quality of life questionnaire for wom- en with arm lymphedema indicate low to moderate impairment in daily life activities: appearance, and mood. Symptoms are somewhat more prevalent, but still moderate. The impact of lymphedema on func- tioning is relatively small, although, by comparing the average values with the results of other authors, we can conclude that our participants score higher on all subscales (23-25). Even among patients with the 2nd and 3rd stages of arm lymphedema, the average values usually range from 1.0 to 2.0, while among our participants, the average values on all subscales are above 2, with ranges going up to a maximum of
4. Authors do not find statistically significant differ- ences in certain aspects of quality of life regarding the stage of lymphedema, except in the appearance subscale, where participants with higher stages re- port more difficulties in body image, and higher av- erage values are obtained for these groups (2.6 and 2.2) (23, 24). The overall quality of life is average, indicating moderate satisfaction among participants, which is generally in line with the results of other authors (23, 24), while moderate to high satisfaction with overall quality of life and relatively low scores on other subscales were obtained in the Swedish sample (14).
In this study, we did not track changes during ther- apy; instead, participants assessed how much arm lymphedema affects them in performing certain daily activities using a questionnaire specifically focused on evaluating the quality of life in individuals with arm lymphedema.
The Lymphoedema Quality of Life Questionnaire included open-ended questions, which participants were not required to answer, concerning leisure ac- tivities that are limited or harder to perform due to the presence of lymphedema. A variety of responses were received. Most often, the limitations relate to sports activities, particularly cycling, hiking, walk- ing, and swimming. In addition, participants mention aesthetic concerns, specifically the reduced selec- tion of clothing available for various occasions due to the difference in arm circumference, and difficulties in being accepted in social situations where people stare at the arm, which can be very uncomfortable and can negatively affect mental health. Participants also noted limitations in everyday activities such as brushing hair, bathing, carrying items, and driving a car, along with getting tired quickly. Furthermore, summer months or higher temperatures exacerbate the swelling, increase the feeling of heaviness in the arm, and cause pain. Exposure to the sun can also worsen lymphedema. Beyond the limitations tied to daily and leisure activities, lymphedema can hinder reintegration into society. In Croatia, lymphedema is still not something that can be surgically corrected or concealed like breast reconstruction or the use of bras with inserts. This condition is visible to every- one, which, along with the difficulty of finding suit- able clothing, leads to stares from people and con- stant questioning. Society imposes norms and has certain expectations regarding female beauty, es- tablishing standards for what a woman should look. Departing from these standards may result in soci- etal rejection and a feeling of exclusion, regardless of age. Because of this, women with lymphedema often struggle with a lack of self-confidence and feelings of inferiority, viewing themselves through the lens of their impairment.
Bojinović-Rodić and colleagues highlighted a de- crease in arm mobility, or arm dysfunction, as a greater issue in terms of quality of life than the actu- al circumference of the lymphedema. Their research also showed that lymphedema has a greater impact on quality of life than on mental health (11), which somewhat differs from the results of our study. This is undoubtedly an interesting finding, although a sig- nificant impact on quality of life could become a ma- jor issue for the individual’s mental health over time.
Surprised looks, difficulty finding desired clothing, and constant questioning about what happened can lead to uncomfortable emotions, feelings of discom-
fort, and societal rejection. These attitudes create additional challenges for the social reintegration of women who have survived breast cancer, as visible lymphedema further complicates acceptance and so- cialization. It is not surprising, therefore, that a high percentage of participants in this study experience psychological difficulties: 42% of participants face a serious degree of stress, 45% deal with very severe anxiety, and 34% struggle with very serious depres- sion, which is certainly alarming and necessitates professional help. Although the correlations between symptoms, appearance, and function associated with lymphedema are statistically significantly linked to participants’ emotional difficulties, we presume that lymphedema is not the sole cause of their condition, as the primary illness itself, along with other dif- ficulties caused by various therapeutic procedures, probably disrupts women’s emotional stability. The findings confirm our assumptions regarding the par- ticipants’ emotional states. Even though the study lacks a control group or comparison with the general population, based on previous studies mentioned in the introduction, increased values are observed, lead- ing to the conclusion that a portion of participants has compromised mental health. These findings em- phasize the importance of professional psychological support in coping with lymphedema, as well as in fa- cilitating acceptance and life adjustments that would ease the return to daily and social activities, both of which are crucial for mental health.
Our results are in line with the findings of Morgan and colleagues (2005), who compared various stud- ies indicating poor psychological adjustment to lymphedema and difficulties in physical and social functioning. Higher anxiety and depression levels have also been observed in patients with lymphede- ma compared to those without it. However, it has also been demonstrated that a coordinated approach to care and treatment, as well as patient education, has a positive effect on improving quality of life and developing a positive self-image (26).
The age of the women proved to be significantly re- lated to their emotional state. Older women experi- ence less stress, anxiety, and depression and score better on the mood subscale. This finding can be explained by the fact that with age and experience, women learn different ways of coping with life’s problems, including illness. In our study, age is also significantly related to the time elapsed since the breast cancer diagnosis and given that unpleasant
emotions are certainly not caused only by lymphede- ma but also by the primary diagnosis, therapy-re- lated difficulties, and other challenges, this may be why age acts as a “protective” factor. A difference in quality of life was also observed in terms of finan- cial status: women with below-average incomes re- port lower levels of stress, anxiety, and depression, and they assess their quality of life more positively compared to women with above-average incomes, which was an unexpected finding. This result could be explained by the fact that women themselves de- termined their income category, which may not fully reflect their actual economic status. Another reason could be that women of higher socio-economic sta- tus may have higher expectations regarding their own quality of life and thus experience the decline in quality more dramatically than women of lower socio-economic status. However, this finding should be further verified in future studies.
We are aware of certain limitations of our study. For example, we were unable to consider some objective indicators of the state of lymphedema, such as the duration of the condition or the stage of lymphede- ma. Additionally, the self-assessment of participants’ income may not accurately reflect their actual eco- nomic status. Caution should also be exercised re- garding the critical values and categories set by the authors of the DASS-21 questionnaire, as they them- selves note that the DASS-21 does not have direct implications for placing respondents into discrete classification categories, such as those found in di- agnostic and statistical manuals for mental disorders (DSM, ICD), and the categories of serious and very serious do not necessarily indicate the clinical status of women.
Conclusion
The research was conducted on 100 participants, members of associations that gather women who have been diagnosed with lymphedema. The women rated their quality of life as moderate, and among the various aspects of life affected by lymphedema, symptoms were the most prominent, although the women reported only a moderate impact on their lives. The study shows that lymphedema is related to the mental health of women, particularly anxi- ety, where the highest percentage of women falls into the category of very severe anxiety, which is concerning and requires professional help. Everyday activities and leisure activities, such as cycling, are limited as they worsen the condition of lymphedema. These limitations contribute to the mental health outcomes of women with arm lymphedema.
This condition is complex and leaves a mark not only on the physical but also on the mental health of the individual, as demonstrated in the study. The involve- ment of various specialists in treatment is necessary to help and contribute to reducing the consequences of lymphedema.
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slobodnog vremena, a kao otežane najčešće navode sportove, vožnju bicikla, automobila, planinarenje, izlazak na sunce, općenito druženja, ali i samu nepre- dvidivost kako će ruka reagirati u određenim uvjetima.
Ključne riječi: limfedem, rak dojke, svakodnevne aktivno- sti, mentalno zdravlje
