The barriers to initiating lung cancer care in low-and middle-income countries

Lung cancer in low-and middle-income countries is the leading and the second leading cause of cancer deaths in males and females, respectively. This, in part, is due to late presentation of patients in health facilities and late diagnosis, thereby compromising the effectiveness of treatment and resulting in poor treatment outcomes. Investigating patients’ late presentation to health facilities and late diagnosis, as barriers to achieving good treatment outcomes, is an important step towards improving the existing pathways of care. Therefore, the aim of this paper is to critically review the published and unpublished literature, including government reports on lung cancer care, with regards to the barriers to patient access, referral, diagnosis and treatment in low-and middle-income countries. The emphasis is on access point and the primary care continuum. This review has been packaged into themes in order to efficiently inform researchers and cancer health professionals, on the existing gaps necessary for developing appropriate intervention strategies and policy guidelines. This review has revealed that the timeous and correct diagnosis of lung cancer enables lung specialists to engage on options for improved patient care. Currently, there are variations in lung cancer management in low-and middle-income countries. Many of the factors impacting on health care outcomes are a function of patient circumstances and/or understanding, leading to delays in presentation to health facilities. Factors pertaining to individual patient circumstances are further compounded by inefficiencies within the health care system. Therefore, limited health system capacities and competing health priorities in these settings require action.


Introduction
Cancer morbidity and mortality is increasingly becoming a major public health problem and it is the second leading cause of death worldwide [1]. While the overall incidence of cancer is lower in lowand middle-income countries (LMICs) compared with high-income countries (HICs), total cancer-related mortality is significantly higher in LMICs [2]. Approximately, 8 million new cancers were detected in the less developed regions of the world in 2012, and 5.3 million of them died of the disease [3]. Survival from cancer is strongly associated with geography, and patients in LMICs perform worse than those living in upper middle-income and HICs [4]. Therefore, almost 70% of all cancer deaths occur in LMICs [5]. The World Health Organisation's (WHO) projections indicate that global annual estimates will increase to 29.5 million new cancer diagnoses and 16.5 million cancer-related deaths, by the year 2040 [2,6,7], unless drastic interventions are implemented. In both sexes combined, lung cancer is the most commonly diagnosed cancer (11.6% of the total cases) and the leading cause of cancer death (18.4% of the total cancer deaths), closely followed by female breast cancer (11.6%), prostate cancer (7.1%), and colorectal cancer (6.1%) [6]. Lung cancer mortality is high among men, and most deaths occur in LMICs of Eastern Europe, Western Asia, Northern Africa, Eastern and South-Eastern Asia [8]. Highest lung cancer incidence was reported in South Korea China, Turkey, Singapore and Philippines [9,10]. An estimated 774,323 new cases were reported in China with a mortality of 690,567 people where China accounted for almost half of the total cases of lung cancer worldwide [11]. In Africa, lung cancer is the fourth most common cancer among men with approximately 39,300 and 37,700 new lung cancer cases and annual mortality, respectively [11,12].
In 2017, only 26% of low-income countries reported having pathology services available in the public sector [13], in contrast to more than 90% of HICs reporting the availability of treatment services [13].
Effective pathways of care in the management of cancers, including lung cancer, is key to achieving quality outcomes and comfort of knowing that patients are receiving the best care [14]. However, in LMICs, studies have reported several barriers to achieving optimal health outcomes enjoyed by the HICs [3,[15][16][17][18][19][20][21][22][23]. In addition, sociocultural and economic difficulties, weak health systems and poor knowledge deter many in LMICs from accessing appropriate cancer care services [16, [24][25][26][27][28][29]. While these challenges are substantial, they are not insurmountable, but the starting point is recognizing the magnitude of the problem [25]. Lung cancer patients in LMICs are bearing the effect of, not only the disease, but also the health systems. Raising awareness of risk factors and screening services for cancer in the population, especially lung cancer, along with improved access and quality of health care are key to enhancing the chances of cure and survival [27]. Accordingly, the aim of this review was to identify and assess gaps in the optimal management of lung cancer in LMICs, with a view to highlight key factors hindering the delivery of best practice for lung cancer care. This review was achieved through identifying and synthesizing the best available documented evidence on the effectiveness of lung cancer management to inform decisionmakers and stakeholders on the magnitude of the problem.

Methods
This review was conducted through a thematic analysis of the literature on the cancer care. The review is conceptual and focuses on the patterns of issues captured in research papers and other documents included in this review. The approach used in this review borrowed from the phenomenology design, which is best suited for exploring the lived experiences of people experiencing a particular phenomenon [17]. In this case, the research phenomenon was barriers to cancer care using a case study of lung cancer and the unit of analysis was research reports rather than the direct individuals who experienced the phenomenon. As a result, other studies using the same phenomenon, but different case study were included. The review was primarily focused on identifying the barriers to lung cancer patient access, investigations and referral points in LMICs. A wide variety of studies were reviewed including; qualitative, mixed method, literature reviews, government reports and research articles in order to understand the essence of phenomenon as seen through the eyes of the patients and healthcare workers and as documented by researchers who investigated the phenomenon.
With regards to timeliness, it is incumbent upon the patient to seek care and the health care system's ability to timeously provide health care as soon as the need is recognized.
Studies show that cancer has led to a high health burden in the public sector where the management of lung cancer has been associated or reportedly having poor health outcomes in LMICs [6, 9-12, 14, 38-40]. In many cases, however, the varying health outcomes are symptoms of differences in the quality of care; including, timing of diagnosis, type of diagnostic methods used, disease staging, initiation and type of treatment [14, [38][39][40].
Recognising, analysing and reporting these barriers are precursors to quality improvement and the design and evaluation of effective corrective interventions to existing processes of lung cancer care [41].
In the following sections the presentation is divided in three superordinate themes, namely; (I) the patient interval, (II) cultural and societal differences, and (III) the health services context. These themes describe different aspects or intervals where the barriers are resulting from. The first describes the barriers to care from the symptom knowledge and/or onset within the patient's interval. The following theme appreciates the diverse communities in these countries and therefore, describes the barriers to timely care resulting smoking and banning asbestos should be clear [26].
Socio economic status and place of residence: it is evident that poverty is a major problem in LMICs and it is closely linked to ill-health, limited access to health services, as well as lack of opportunity to lead a healthy life [52]. According to Jobson, societal poverty may impede their capacity to seek healthcare, even when the needs are obvious, and services are available [27,52]. In some of the LMICs, health services and health costs have risen considerably, creating a health divide between the rich and the poor, where those who can afford receive good quality care and those who cannot afford are excluded [53,54]. For most people without access to health, there is a terrible paradox: "poverty exacerbates poor health while poor health makes it harder to get out of poverty" [54]. Socio-economic status (SES) largely determines a person's place of residence and access to health care [55]. People who have higher incomes and health insurance are more likely to get tests that can detect lung cancer early and get the right treatment [32,36]. Living in rural areas is associated with timely and comprehensive care and support [27,32,47]. In the case of KwaZulu-Natal, for example, all three public hospitals with oncology units are located in two cities, namely: Durban and Pietermaritzburg [27]. The burden of travel from a patient's residence to healthcare providers is an important issue. The necessity for repeated visits for lung cancer diagnosis and treatment on an outpatient or an inpatient basis makes distance an issue with which the patient with cancer must manage during the care course [27,32].

CULTURAL AND SOCIETAL DIFFERENCES
Alternative medicine and illness representation: there is a conventional view that cancer evokes great anxiety and fear in the patient and significant others. Significant others always have "why" questions [42], but all scientific explanations answer the question "how", but not "why". It is the quest to find answers to "why" question that people consult sangomas, prophets and other health providers [42]. As a result, healthcare professionals grapple with meeting the expectations of diverse communities, with different cultural, religious, social and political beliefs. Culture has an influence on one's attitudes and beliefs, in turn affecting one's understanding of health, disease and cure [55,56]. Illness representations may be a barrier to early diagnosis of lung cancer and adhering to treatment.
Illness representations refer to a person's beliefs and expectations about their illness [57]; for example, the cause of the cancer and these beliefs influence responses to illness and health care. Healthcare professionals must be sensitive to various cultural issues to avoid cultural blindness. A book written from a South African perspective by a team of oncology specialists concludes that healthcare professionals need an in-depth understanding of the patients' cultural and religious beliefs [42]. It is only with this knowledge and understanding that they can truly communicate with and assist the sufferers [42]. Stigmatisation: stigma is relationship and context-specific where a specific attribute is associated with a negative evaluation that may lead to negative treatment or discrimination and self-fulfilling prophecies, stereotype activation, and identity threat. With lung cancer, health-related stigma is closely connected to beliefs about lung cancer causation and prognosis [58]. The association between lung cancer and smoking results in perception that lung cancer is selfinflicted, and affected patients have themselves to blame, thereby delaying treatment-seeking or even disclosing their condition to significant others [59]. Health professional behaviours were also described as blocking support of lung cancer patients, through the delay in offering appropriate referral points, due to, among other things, poor knowledge about lung cancer [25,27,31,39,42]. The psychological impact of having lung cancer include feelings of guilt and depression, which has reportedly been the same for both smokers and never smokers [59]. Promotion of right to health can potentially affect patients' health-seeking behaviour and the provision of treatment options by health providers.

HEALTH SERVICES CONTEXT
Screening services: this literature review found that early detection of cancer has held great promise and intuitive appeal in the medical community for well over a century. "Delayed presentation for cancer is the norm in many LMICs and within low-resource or geographically remote regions in upper-middle-income countries. This delay exists for a variety of structural, equity, and socio-cultural reasons" [36].
Early diagnosis might also be achieved through the provision of screening services at easy to access settings [23,36,46]. Screening involves looking for cancer before a person has any symptoms and the aim is to prevent cancer deaths and improve quality of life by finding cancers early and by effectively treating them [35]. Lung cancer in LMICs lack effective screening tools for early disease detection [27]. Implementation of lung cancer screening is challenging; therefore, organized lung cancer screening is practically non-existent in LMICs [8]. Lung cancer screening is largely restricted to HICs in spite of high prevalence of lung cancer cases even in LMICs [8,35,36]. These countries have a very high incidence of pulmonary tuberculosis and other chest infections [60][61][62]. Therefore, misdiagnosis is a major concern [8, 17, 26, 27, 34-36, 60, 62], which necessitates the need for screening services at primary level healthcare in these settings.  [8,21,27,28,37,40,63]. financial support [26]. In short, improved access and quality of healthcare remain important and all healthcare professionals must accept that a multi-disciplinary team is required to approach the patient, family and the management of lung cancer.

What is known about this topic
• Patients' late presentation to health facilities, are largely due to low suspicion index of lung cancer from the health professionals and patients alike; • Reported variations in lung cancer care management and achievement of optimal health outcomes in HICs, are currently not applicable to LMICs; • Cancer morbidity and mortality are becoming a major public health problem with a very high percentage of all cancer deaths occurring in LMICs.

What this study adds
• It identifies and synthesizes the best available documented evidence on access barriers to lung cancer care in LMICs, which cause delays in presentation, diagnosis and treatment of lung cancer; • It highlights the difference in cancer care between HICs and LMICs, which are the health systems and socioeconomic issues leading to lung cancer patients in LMICs performing worse than those living in HICs; • It strengthens the need and importance of organising and implementing lung cancer screening services in LMICs, which are currently non-existent.