Lung cancer awareness and palliative care interventions implemented in Africa: A systematic scoping review’

Background: Lung cancer is the most common cancer and of cancer-related (LMICs), lung cancer is often diagnosed at a late stage due to poor public knowledge and awareness of the signs and symptoms of lung cancer. It is believed that increasing the awareness about lung cancer is key to reducing the diagnosis and treatment delays. Early implementation of palliative care has also been reported to improve a patient’s quality of life, symptom burden, and even survival. The aim of this paper was to map evidence on lung cancer awareness and palliative care interventions implemented in Africa. Methods: A scoping review was performed following the method of Arksey and O’Malley. Systematic searches were performed using EBSCOhost platform. A keyword search from the following electronic databases were conducted: PubMed/MEDLINE, Google Scholar, Science Direct, World Health Organization (WHO) library, and grey literature. The screening was guided by the inclusion and exclusion criteria. The quality of the included studies was determined by Mixed Method Appraisal Tool (MMAT). A thematic content analysis was used to present the narrative account of the reviews, and NVivo version 11 was employed to extract themes from all included studies. Results: A total of 2886 articles were screened, and 236 met the eligibility criteria. Furthermore, 167 articles were also excluded following abstract screening. Sixty-nine (69) articles were selected for full-article screening by two researchers with 9 being selected for independent detailed data extraction for this synthesis. These studies were also subjected to methodological quality assessment. Of the nine included studies, eight studies described at least one lung cancer warning signs and symptoms, while one study described the effectiveness of palliative care for lung cancer. Eight articles recognized the level of lung cancer knowledge, risk factors and awareness of warning signs and symptoms in LMICs, mostly Africa and Asia. Conclusions: Most of the participants were aware of tobacco use as a risk factor for lung cancer, but the majority still had limited knowledge on the other pre-disposing risk factors. There is limited evidence on the palliative treatment of symptoms, and majority of patients continued to suffer from

3 uncontrolled symptoms and unmet needs. Therefore, the urgent need for timely access to palliative care to be introduced from diagnosis to end of life to improve the quality of life of the lung cancer patients and their families.

Background
Cancer is an emerging healthcare problem in Africa and is the second leading cause of death after cardiovascular diseases worldwide (1). Globally, more than 20 million new cancer cases are projected for 2025 compared to an estimated 14.1 million and 17.5 million new cancer cases in 2012 and 2015 respectively (1)(2)(3)(4). In low and middle-income countries, lung cancer is often diagnosed at a late stage due to poor public knowledge and awareness of its signs and symptoms (5,6). Lung cancer is the most common cancer and cause of cancer-related deaths, responsible for nearly one in five deaths across the globe (7,8). In 2008, about 715,000 new cancer cases and 542,000 cancer deaths occurred in Africa (9). These numbers are expected to double in the next 20 years due to the aging and population growth, as well as the changes in lifestyle factors. These lifestyle factors are associated with urbanization and economic development of risk factors, such as smoking, obesity, physical inactivity and dietary patterns (4,9,10). It is believed that increasing the awareness about lung cancer is key to reducing the diagnosis and treatment delays (10). Evidence suggests that a significant portion of the increase in cancer is due to several factors, including poor awareness of the signs, symptoms, and risk factors for cancer; poor availability of tests or screening programs; and limited access to standard treatment (5,10,11). People may delay help-seeking due to poor knowledge of lung cancer symptoms (12,13), or wait until the disease advances to a terminal stage (14,15). Lack of public awareness of lung cancer and recognition of what to do when symptoms develop contribute to this delay (16,17). Early recognition by patients about the signs and symptoms of lung cancer depends on their level of awareness (4). The World Health Organization (WHO) defines palliative care as: "an approach that improves the quality of life of patients and their families facing the problems associated with life-threatening illness, through the prevention and relief of suffering by means of early identification and impeccable assessment and treatment of pain and other problems, physical, psychosocial, and spiritual" (18). Palliative care is focused on providing relief from the 4 symptoms and stress of a life-threatening illness such as lung cancer and improving quality of life for both the patient and the family. Early implementation of palliative care has been reported to improve a patient's quality of life, symptom burden, and even survival (19,20). Seventy percent of lung cancer deaths worldwide are due to tobacco use, with smokers being twenty times more likely to die from lung cancer than their non-smoking counterparts (21,22).
In Africa, cancer is predicted to have more than 85% increase by 2030, hence Morhason-Bello et al. (23) and Stefan et al. (24) have proposed various interventions, including cancer awareness, advocacy, research, workforce, care, training and funding to avert this situation (24). Poor awareness of cancer symptom is likely to contribute to patient delays in presenting to medical professionals (14,25), and in turn contribute to later stage diagnosis (25). A systematic review by Austoker et al (26) found limited evidence of the effectiveness of community-level interventions to promote cancer awareness. Over 90% of patients with lung cancer are symptomatic at the time of diagnosis and experience two to three symptoms on average (27,28). Cough is the most common presenting symptom and has been noted to be a good prognostic indicator (14,17,27). It has also been shown that many patients will visit their general practitioner (GP) on more than one occasion before further investigation or onward referral (27). The World Health Organisation (WHO) expects the burden of cancer in Africa to grow rapidly in the coming years and for incidence to exceed 1 million per year by 2030, if the situation is not averted (29). There is little evidence on lung cancer awareness and palliative care interventions implemented in Africa. The findings of this systematic scoping review will better our understanding of the lung cancer awareness and palliative care interventions implemented in Africa, expose knowledge gaps and stimulate research to fill in the gaps. Thus, the purpose of this systematic scoping review is to map the available evidence on the lung cancer awareness and palliative care interventions implemented in Africa.

Methods
This study was conducted through a systematic scoping review. This approach is particularly appropriate when the main sources and types of available evidence are complex or have not previously been comprehensively reviewed (30). This review included a quality assessment as 5 recommended by Levac et al (31) and was guided by the 5-step methodological framework outlined by Arksey and O'Malley (32). These steps consist of: (1) identifying the research question; (2) identifying the relevant studies; (3) study selection and eligibility; (4) charting the data, and (5) collating, summarizing and reporting the results.

Identifying the research question.
Our research question was "what evidence exist on the lung cancer awareness and palliative care interventions implemented in Africa?".
Research sub-question is as follows: What awareness programmes and early diagnostic interventions are implemented in Africa for lung cancer?
What are the palliative care interventions implemented in Africa for lung cancer?

Identifying relevant studies.
To identify relevant studies, we performed a systematic scoping review including all study designs

Study selection and eligibility.
Following title screening from the above-mentioned databases, articles with relevant study titles for this research were uploaded on the Endnote X7 software. Search results from different electronic 6 databases were combined in a single EndNote library. Studies which did not address the research question and the duplicates of the same records were then excluded. Abstract and full articles were screened from the included studies by two independent reviewers (UIN and MO). An abstract screening form with questions was developed based on the review eligibility criteria. Discrepancies between reviewers at abstract and full article stages was resolved by involving a third screener. The relevant studies were identified with guidance from the inclusion and exclusion criteria which was formulated according to the research questions.

Inclusion criteria
For studies to be included they had to meet the following criteria: Articles published in English.
Published from 2008 to present.
All study designs with relevant interventions.
Studies focusing on lung cancer awareness and or palliative care interventions in adults.

Research focusing on lung cancer awareness interventions implemented in Low and Middle-Income
Countries (LMICs) and whose conclusions and discussions demonstrate transferable findings to African settings.

Exclusion criteria
Studies with the following characteristics were excluded: Articles published in other languages other than English Studies published before 2008.
Articles focusing on lung cancer awareness interventions implemented in High income countries.
Studies focusing on lung cancer awareness and palliative care interventions in children.
Data on the study setting and the key findings described in each article were recorded and organized into different themes using NVivo 11. Information from the selected studies was sorted and organized into the following categories: author and year, country of origin, aim, study population, study design, study setting, and most relevant findings.

5.
Collating, summarising and reporting the results.
In the process of collating and summarizing the findings, the extracted evidence was repeatedly reviewed. Results were summarized to present an overview of the current evidence on lung cancer 7 awareness and palliative care interventions implemented in sub-Saharan Africa. We performed a thematic content analysis of the themes to identify further contextual factors (e.g. knowledge about lung cancer and awareness on risk factors, signs and symptoms for lung cancer, awareness interventions, palliative care interventions etc).

Quality assessment
Mixed Method Quality Appraisal Tool (MMAT) Version 2011 (33) , was used for quality assessment of included studies for the purpose of evaluating the risk of bias. Two reviewers (UIN and MO) independently assessed the quality of evidence of the studies included. The studies were assessed in the following domains: the appropriateness of aim of study, adequacy and methodology, study design, data collection, study selection, data analysis, presentation of findings, author's discussions and conclusions. An overall quality percentage score for each of the included studies was calculated and scores interpreted as low quality (˂50%), average quality (51-75%), and high quality (76-100%).

Screening results
After the title screening and deletion of duplicates, this scoping review found 236 eligible studies from a total of 2886 articles. A total of 167 articles were also excluded following abstract screening. Sixtynine (69) articles were selected for full-article screening by two researchers with 9 being selected for independent detailed data extraction for this synthesis. These studies were also subjected to methodological quality assessment. Cohen's kappa coefficient (κ) statistic using Stata 13.0SE (Stata corp. College station, Texas, USA) was used to measure inter-rater agreement between reviewers

Characteristics of included studies
All included studies were conducted in LMICs and published between 2008 and 2018. The total sample 8 size from primary studies was 3563 participants. Six studies showed majority of the participants to be males (19,(36)(37)(38)(39)(40) , two studies had a slight female preponderance (41,42), while one study (20) was a literature review . Of the nine studies included, 6 were cross-sectional studies (36-39, 41, 42), one was a pre-test and post-test study design (40), one was a prospective study (19) and one was a literature review (20). Of the nine included studies, eight studies described at least one lung cancer warning signs and symptoms (19,(36)(37)(38)(39)(40)(41)(42), while one study described the effectiveness of palliative care for lung cancer (20). The participants from one study had a good knowledge about lung cancer

Knowledge about lung cancer
From the seven studies, participants from one study had a good knowledge about lung cancer (42), and another one had a moderate knowledge of lung cancer (39). In another study, knowledge about lung cancer varied widely, mainly by socio-demographic factors (37), whereas in other four studies, low levels of knowledge about lung cancer were revealed (36,38,40,41). A study conducted in Malaysia found that most of the students had a good knowledge about lung cancer (42). They also knew that not only males were affected by lung cancer (42), in contrast with a very poor knowledge of lung cancer demonstrated by more than half of the teachers in West Bengal. They mentioned that only males are affected by lung cancer, which is an incorrect information. Lung cancer can affect both males & females (39).

Awareness on risk factors, signs and symptoms for lung cancer
All the participants from the seven studies showed a good knowledge for lung cancer risk factors (36)(37)(38)(39)(40)(41)(42). Regarding lung cancer signs and symptoms, two studies had a good knowledge about the signs and symptoms for lung cancer (36,42), three studies showed poor knowledge for lung cancer (38,40,41), one had a very poor knowledge about lung cancer signs and symptoms (39) and one study was not specific on the participant's knowledge of the signs and symptoms for lung cancer (37). Regarding the knowledge about lung cancer and smoking, two studies showed that about 92% (39) and 91.3% (36) of the participants mentioned that cigarette smoking was the most common risk factor of lung cancer respectively. Chawla et al. (37) found that 100% of the males were aware that smoking is a primary risk factor for lung cancer. Three studies showed that the participants had a low awareness of the non-specific warning signs of lung cancer (38,40,41). A study conducted by Naskar et al. (39) in West Bengal showed that 92% of the participants reported that asbestos, ionizing radiation and other cancer-causing substances are some of risk factors of lung cancer (39). Another Malaysian study by Al-Naggar et al. (36) reported that 75.6% of the participants mentioned that occupational exposure was one of the risk factors of lung cancer (36).
A study by Zainuddin et al, conducted in Malaysia among undergraduate students showed that 43.5% of the students knew that exercise or physical activities may reduce the risk of getting lung cancer (42). This is contrary to the study conducted by Al-Naggar et al among secondary school male teachers in the same country, whereby the majority (83%) knew that exercise could reduce the risk factors of lung cancer (36).

Lung cancer awareness interventions
A study by Shankar et al (40), conducted a Pink Chain Campaign on lung cancer awareness in 2011 in various women colleges in India. The same questionnaire was used for a Pre-test and post-test related to lung cancer awareness programs at the end of interactive session, at 1 year and 6 months respectively (40). The campaign at pre-test awareness showed a significant increase in level of knowledge regarding lung cancer at 6 months and this was sustained at 1 year. At post-awareness after 1 year and 6 months, there was a significant change in alcohol and smoking habits (40). This shows the adoption of safe practices after an improved awareness about lung cancer. Magazines and newspapers were the primary source for information regarding risk factors, signs and symptoms of lung cancer in more than 60% of teachers whereas more than 30% teachers were educated by doctors (40).

Palliative care interventions
Palliative treatment options for lung cancer include chemotherapy, radiotherapy and supportive care (20). The Turkish study by Bulbul et al. (19), showed that, at least 50% of all lung cancer patients were using nonnarcotic analgesics either alone or in combination with narcotic analgesics for the relief of pain (19), 30.2% of the patients underwent palliative radiotherapy for bone metastasis (19).
This study also found that female patients were more likely to report higher levels of anxiety and depression than their male counterparts (19). A literature review by Li and Li (20) on the effectiveness of palliative care for non-small cell lung cancer showed that palliative care has been recommended as the standard of care for patients with advanced NSCLC based on the results of random clinical trials completed over the past several decades (20). A study showed that Home oxygen use, and bronchodilator use was higher among lung cancer patients, since 1/4 to 1/2 of lung cancer patients are reported to have chronic obstructive pulmonary disease (19).

Discussion
Mapping evidence on the lung cancer awareness and palliative care interventions implemented in Africa is of primary importance to inform recognition of lung cancer risk factors, signs and symptoms, particularly in LMICs. In this scoping review, we identified 9 articles published between 2008 and 2018. Eight articles recognized the level of lung cancer knowledge, risk factors and awareness of warning signs and symptoms in LMICs mostly Africa and Asia (19,(36)(37)(38)(39)(40)(41)(42). We found limited evidence to inform policy on individual or community level interventions to promote lung cancer awareness and 11 palliative care in LMICs. The major symptoms of lung cancer as reported by the included studies were chest pain, coughing out blood, appetite loss, pain, shortness of breath, repeated respiratory infection, depression and tiredness (36,(38)(39)(40)(41)(42). The reviewed studies all stated the importance in educating the public on how to know and recognize the risk factors and symptoms of lung cancer.
Available evidence from our reviewed studies suggest that most of the participants recognized tobacco use as the main risk factor for lung cancer and more than half believed that second-hand smoking and air-pollution were also risk factors for lung cancer (36)(37)(38)(39)(40)(41)(42). This may reflect the effectiveness of anti-smoking initiatives in educating the public on the harmful effects of cigarette smoke (41). There is a poor recognition of the early warning signs of lung cancer in LMICs, so there is urgent need for the public and health professionals to be aware of the signs and symptoms of lung cancer to avoid delays in timely diagnosis (43). Lung cancer preventive measures mentioned by the participants were smoking cessation, avoiding second-hand smoking, avoiding unnecessary x-ray image of the chest, banning smoking totally in public places as well as in institutions (36,39). A study stated that at least 50% of all lung cancer patients were using non-narcotic analgesics either alone or in combination with narcotic analgesics for pain relief (19), and there was a significant number of unmet needs reported by patients with lung cancer (19). Most patients reported continuing symptoms, and a significant number of patients with dyspnea and pain reported that they were not receiving treatment (19). There is need for early palliative care to provide relief from pain and other distressing symptoms and give the patients and their families the best possible quality of life. Some studies suggest that exercise or physical activities may reduce the risk of getting lung cancer (36,42

Conclusions
This systematic scoping review of literature highlighted the lung cancer awareness and palliative care interventions implemented in LMICs. We found some evidence on interventions delivered to individuals during a campaign which showed improvement in healthy practices related to smoking and alcohol consumption. Most of the participants were aware of tobacco use as a risk factor for lung cancer but majority still had limited knowledge on the other pre-disposing risk factors. From our studies, there was limited evidence on the palliative treatment of symptoms, and majority of patients continued to suffer from uncontrolled symptoms and unmet needs. Therefore, the urgent need for timely access to palliative care to be introduced from diagnosis to end of life to improve the quality of life of the lung cancer patients and their families. Health education activities against smoking should be implemented in schools, universities and the community and also awareness programmes and campaigns to increase lung cancer knowledge and warning signs.

Ethics approval and consent to participate
This article is part of a MMedSc thesis, which is being currently conducted in accordance with permission from the ethics committee of the University of KwaZulu-Natal (UKZN) 13 Humanities & Social Sciences Ethics Committee (HSSREC), under the protocol reference number HSS/0544/018M.

Consent for publication
Not applicable

Availability of data and materials
All data generated or analysed during this study are included in this published article and its supplementary information files.