Eligible caregivers were required to be (1) related to patients who had been histologically-diagnosed with either non-small cell or small cell lung cancer (2) over 18 years of age, (3 )able to communicate in either Hindi or English, and (4) unpaid for their services. At the time of caregiver assessment, patients were either being evaluated for treatment or were actively undergoing cycles of cytotoxic chemotherapy. Attempts were undertaken to survey caregivers who were primarily assisting patients at home.

A Hindi-version of the Caregiver Quality of Life Cancer (CQOLC) index was administered to all eligible caregivers. The CQOLC index is a 35-item assessment comprising 4 major subdomains [9][10]. These subdomains include burden (10 items), disruptiveness (7 items), positive adaptation (7 items), and financial concerns (3 items). The index also includes 8 additional items that are not associated with any of the major subdomains. Caregivers respond to each item using a Likert scale ranging from 0 to 4, with 4 indicating that an individual item resonates strongly with the caregiver. Responses for 27 items contribute as positive additions to the caregiver’s overall score while 8 responses contribute as scoring deductions. Higher scores indicate worse QOL among caregivers.

Eligible caregivers were ushered to a private setting during a scheduled appointment for their respective patients. A copy of the Hindi-version of the CQOLC index was provided by a trained researcher. Assistance was offered to partially-illiterate caregivers during the completion of the surveys. Unanswered items were scored as “zero”. Surveys with more than 7 unfilled responses (>20%) were excluded from analysis. Attempts to obtain demographic data were undertaken at the time of caregiver assessment.

Microsoft Excel version 2016 was used to analyze the data. Descriptive statistics were calculated to evaluate baseline demographics of the included caregivers. Continuous demographic variables were converted to categorical variables based on the computed means and medians. Two-tailed t-tests or one-factor analysis of variance (ANOVA) were conducted to examine associations between demographic categorical variables and mean CQOLC index scores. Standard deviations were calculated with each mean score. Statistical significance was confirmed for p < 0.05. As arbitrarily defined by previous work, a clinically meaningful difference (CMD) required subgroup scores to differ by 0.5 standard deviations in magnitude [2]. The mean index scores for each subdomain were computed individually, and these scores were compared using ANOVA.

Investigations that either detailed QOL solely among lower-income caregivers for cancer patients or reported the association between QOL and socioeconomic status were selected. Selected studies were required to (1) be published articles, (2) assess QOL by administering a standardized survey to cancer caregivers, (3) query caregivers over 18 years of age, (4) and evaluate QOL among caregivers within 6 months of cancer treatment for their respective patients. Studies that combined the results of caregivers and cancer patients were excluded.

Studies were grouped based on geographical location. The methodology and results from each selected study were reviewed in detail. The differences in QOL assessment scores between lower-income caregivers and caregivers with more financial flexibility were extracted. The QOL among lower-income caregivers from different regions of the world were compared.

The National Heart, Lung, and Blood Institute’s Quality Assessment Tool for Observational Cohort and Cross-Sectional Studies was used to assess quality for each selected publication [12]. This 14-item quality assessment tool evaluates study methodology and population sample for bias. Studies were rated as “good”, “fair”, and “poor” following review.

In total, the survey data from 89 eligible caregivers were analyzed. All 89 caregivers provided their age, sex, relation to patient, and duration of care. A lesser number of caregivers provided their income, education, and living background. The mean age +/- standard deviation was 37.8 +/- 9.2 years while the median annual income per capita was 175,000 Rs. ($2516.67 US). The demographics of included caregivers are described in Table 1.

One study conducted in Europe and 3 studies conducted in North America were identified by systematic review [13][16][18][19]. In the Netherlands, Nijboer et al. administered the Caregiver Reaction Assessment (CRA) scale at three-month intervals to caregivers for colorectal cancer patients undergoing treatment at 1 of 10 regional centers m [18]. Caregivers of lower socioeconomic status reported greater variability among changes in their financial problems, schedules, and self-esteem over time. No large differences in effect size were identified among caregivers of varying socioeconomic groups. In Canada, Duggleby et al. evaluated hope, grief, and mental and physical health among rural female caregivers of stage IV cancer patients [13]. The annual combined income was less than CAD $29,999.00 for 31.9% of patients. Based on responses to the Short Form Health Survey Version 2 (SF12v2), the mental and physical subscores for rural female caregivers were near the 25^th percentile of the general US population. The authors did not report associations between QOL and varying levels of socioeconomic status. In the U.S.A., Goldstein et al. found no differences in ZBI scores based on household income among caregivers of terminally-ill cancer patients admitted to an inpatient hospice facility in Connecticut [16]. Rather, increasing burden was observed for younger caregivers and those sharing limited social networks. Oberst et al. assessed caregivers of patients undergoing radiotherapy in the Midwest region of the U.S.A. using the Appraisal of Caregiving Scale (ACS) [19]. Worse scores were observed within the threat subdomain of the ACS for caregivers of lower socioeconomic status. Otherwise, the authors identified no differences in the harm/loss, challenge, and benign subdomains of the ACS based on socioeconomic status.

In summation, the available evidence suggests that lower-income caregivers of cancer patients in North America and Europe do not clearly share substantially worse QOL compared to caregivers of higher socioeconomic status. We believe lower-income caregivers within these countries may not experience worse QOL for two reasons. First, access to cancer care is more widespread for patients in the developed world. Consequently, quality of care may be reasonably equitable among rich and poor, thereby mitigating feelings of frustration among lower-income caregivers. Second, palliative care services are more available to lower-income patients in North America and Europe [24][25]. The burden of responding to emergent symptoms is often reduced with the aid of medical management directed towards improving QOL.

Three studies completed in the Middle East, 3 studies completed in South or East Asia, and 1 study completed in Nigeria were identified by systematic review [14][15][17][20][21][22][23]. Hacialioglu et al. used the World Health Organization Quality of Life-Short Form, Turkish Version (WHOQOL – BREF TF) to evaluate QOL among family caregivers of Turkish patients actively undergoing chemotherapy [17]. Over half (57.5%) of caregivers were described as lower-income though the authors did not report their actual earnings. The authors observed worse psychological, environment, and national subscores among lower-income caregivers. No differences were observed among varying levels of education. In Iran, Soleimani et al. used the Quality of Life (Family Version) scale to evaluate outcomes among caregivers for cancer patients undergoing treatment planning [20]. A significant population (30.9%) of caregivers earned income within the poverty range for Iran. Though no differences in QOL were observed between levels of income, caregivers who relied on financial support from other family relatives reported worse QOL compared to those who were financially-independent. Similarly, Vahidi et al. reported that caregivers in Iran who have financial stress share worse ZBI scores than those who have more financial flexibility [21].

Both selected studies that were conducted in East Asia reported worse QOL among lower-income caregivers [15][22]. Yang et al. assessed depressive symptoms by administering the Center for Epidemiologic Studies Depressive Scale (CES-D) to caregivers for patients actively receiving chemotherapy for breast cancer, lung cancer, gynecologic cancer, or leukemia [22]. Caregivers who earned less than 800 Yuan ($116.46 US) monthly shared the highest depressive scores. Similarly, Yoon et al. found greater burden among lower-income South Korean caregivers for terminally-ill cancer patients by administering the CRA [15]. Caregivers who earned less than 2,000,000 KRW ($1790.75 US) monthly shared worse scores for all 4 subdomains of the CRA compared to those who earned more than 2,000,000 KRW monthly. In India, Lukhmana et al. compared ZBI scores among cancer caregivers of varying employment status [14]. Worse ZBI scores were observed for unemployed caregivers and caregivers with professions that required less education. The authors did not compare ZBI scores based on household income. Lastly, Yusuf et al. assessed burden among caregivers of Nigerian patients using the General Self-Efficacy Scale (GSES) and ZBI [23]. The mean annual income of the included subjects was equivalent to $2616.00 US. The authors observed no differences in assessment scores between employed and unemployed caregivers; however, caregivers who received financial support from family relatives were found to have better QOL with both assessments compared to those who received no support.

Overall, the above studies reflect that lower-income caregivers in Asia and the Middle-East face a greater decline in QOL compared to those with more financial flexibility. The specific components of QOL that suffered most were difficult to identify because of a wide array of standardized assessments used by the selected studies. Nonetheless, 4 studies indicated that lower-income caregivers residing in Asia or the Middle-East commonly struggle with increasing burden [14][15][21][23]. These findings are in accord with the results of our single-institutional study. Among African caregivers, limited data is currently available to determine the association between QOL and socioeconomic status.

The most salient finding from our cross-sectional study and systematic review is that caregivers of lower socioeconomic status in the developing world are at high-risk for a reduction in QOL. The burden associated with cancer caregiving is predominantly overwhelming. Clinicians who care for lower-income cancer patients, particularly in the Middle East and Asia, should be wary of the toll absorbed by the patients’ caregivers. QOL among lower-income caregivers is more likely to deteriorate as the duration of providing aid to cancer patients extends.

Moderate success has been observed for interventions designed to improve caregiver QOL regardless of socioeconomic status [26]. Implementing these interventions, which often include counseling, exercise sessions, and/or interactive discussions, may be difficult in lower-income regions because of limited available resources. Consequently, we recommend two approaches to alleviate caregiver burden. First, educating and empowering relatives at the time of diagnosis to proportionally share the responsibility of caring for a lower-income cancer patient may be a resourceful method to maintain a balanced QOL for all involved. Second, since palliative care specialists are often not available, implementing departmental prescription protocols could help manage the cumbersome symptoms of advanced cancer that unfortunately arise and burden both patients and caregivers [27]. Such approaches may not carry significant financial costs but could prove significantly beneficial to lower-income cancer caregivers.