Surapaneni M, Uprety D.

Lung cancer management in low and middle-income

countries - current challenges and potential solutions. IJCCD. 2023;3(1).
doi:10.53876/001c.73042

Review Article

Lung cancer management in low and middle-income countries -

current challenges and potential solutions
Malini Surapaneni, MD1, Dipesh Uprety, MD, FACP1
1 Department of Hematology-Oncology, Karmanos Cancer Institute, Detroit, MI, USA
Keywords: “Lung Cancer”, “low-income”, “middle-income”, “country”
https://doi.org/10.53876/001c.73042

International Journal of Cancer Care and Delivery

Vol. 3, Issue 1, 2023

Lung cancer is the second-most prevalent cancer and, the most common cause of
cancer-related mortality throughout the world. Evidence-based strategies to decrease its
incidence and mortality are being implemented in different parts of the world. Smoking
cessation policies are being actively publicized to decrease the incidence of tobacco
related cancers including lung cancer. Screening program for early detection of localized
lung cancer which can then be targeted by a multimodality approach utilizing surgery,
radiation, chemoimmunotherapy to achieve cure is now becoming the standard in several
high-income countries. Precision medicine in lung cancer is booming with metastatic
non-curative cancers targeted with small molecule tyrosine kinase inhibitors. However,
these advancements are not available all around the world. Inequalities exist in the
management of lung cancer, mostly driven by the economic differences between the
countries. Raising awareness to these international barriers is pivotal for improving lung
cancer related incidence and mortality.

throughs have been made. However, lung cancer remains

Take home message
• Almost 60% of lung cancer incidence
throughout the world is seen in the low- and
middle-income countries.
• Several disparities exist in the screening, di-
agnostics, and management of lung cancer in
the low- and middle-income countries when
compared to the high-income countries.
• Limited resources, economic restrictions, and
lack of accessibility are the major causes for
the differences seen in the management of
lung cancer in the low- and middle-income
countries.
• Understanding the local limitations and im-
plementing innovative strategies to overcome
these problems can help bridge the worldwide
gap seen in the management of lung cancer.
1. INTRODUCTION
The field of thoracic oncology witnessed immense growth
in the last two decades. From the development of effective
lung cancer screening guidelines which aim for an early di-
agnosis of asymptomatic and non-metastatic lung cancers
to the advent of immunotherapy and targetable tyrosine ki-
nase inhibitors which aim to improve the quality of life and
survival in metastatic lung cancer patients, several break-
the most common cause of cancer-related mortality despite
all the advances, accounting for about 1.8 million deaths
worldwide in 2020.1 Several inequalities exist in managing
lung cancer worldwide, which ultimately contribute to the
disparities in its incidence and mortality burden. One com-
monly encountered reason for these inequalities is the so-
cio-economic variations in the different parts of the world.
The World Bank list of economies divides the countries
into four sub-groups based on their Gross National Income
(GNI) per capita- low income, lower-middle income, upper-
middle income, and high income. Among the low- and mid-
dle-income countries, the age-standardized incidence and
mortality are highest in Micronesia (36.4% and 34.9%, re-
spectively) and Eastern Asian countries (34.4% and 28.1%,
respectively), while its lowest in the Western-African re-
gion (2.2% and 2.1% respectively). Overall, about 60% of
the world’s lung cancer incidence is attributed to low- and
middle-income countries, with the majority noted in the
Asian continent.1 Hence, recognizing the challenges faced
by the patients and physicians in these countries is essen-
tial to improve the global outcomes of lung cancer.
2. HEALTHCARE SYSTEM
Healthcare is divided into public and private sectors in
most low- and middle-income countries. The government
primarily sponsors public sector hospitals/universities, and
they provide care to the patients at a low cost; however,
most advanced diagnostics, procedures, and novel medica-
tions might not be readily available in these hospitals due
 Lung cancer management in low and middle-income countries - current challenges and potential solutions
to their cost limitations. The private sector hospitals tend
to have an underlying for-profit motive. Though they have
more access to the newer products, their use in public is
limited to high-income or privately insured patients. Ex-
cept for some upper-middle-income countries like China
and Mexico, and a few lower-middle-income countries like
Vietnam, most of the low-and middle-income regions do
not have comprehensive nationally funded public health
insurance programs that are able to cover the expensive
testing and treatment required for lung cancer. Thus, pa-
tients must rely on private insurance or out-of-pocket pay-
ments which leads to financial toxicity.
3. SMOKING CESSATION
Tobacco use is suspected to have killed 8 million people in
2019 and is the most common risk factor for lung cancer
worldwide.2,3 The tobacco cessation efforts by WHO (FCTC,
NCD-GAP, MPOWER, and ENDS) have been instrumental
in controlling the tobacco epidemic. The fourth edition of
the WHO global report on the trends in the prevalence of
tobacco use reported a global decline in tobacco use from
32.7% in 2000 to 22.3% in 2020.4 Lower-middle income
groups had the highest drop in tobacco use (44% in 2000 to
24% in 2020), while the upper-middle income had the low-
est and slowest drop (28% in 2000 to 24% in 2020). How-
ever, some of South-East Asian and Middle Eastern coun-
tries like Myanmar, Indonesia, and Lebanon still have a
tobacco use prevalence as high as 50%.4 Primary and sec-
ondary smoking abstinence has been shown to be asso-
ciated with improved survival outcomes.5 In the National
Lung Cancer Screening trial, there was a 20% reduction
in cancer-related mortality with 7-year smoking cessation.6
Despite the awareness and the evidence, there are about
49 countries that currently do not have a single national
control measure, and a majority of them belong to low-
and middle-income countries. In addition to cigarette use,
other causes of nicotine exposure commonly encountered
in low- and middle-income countries include second-hand
tobacco smoke and the use of non-cigarette nicotine prod-
ucts like beedi, toombak.2,7 These products are generally
cheaper and cause higher nicotine exposure.8
The incidence of lung cancer in non-smokers is increas-
ing globally. Majority of the Asian women with lung cancer
are non-smokers. Some of the risk factors for lung cancer
that have been proposed in this population are outdoor air
pollution, environmental exposures (arsenic, asbestos), ge-
netic factors, benign pulmonary conditions (pulmonary fi-
brosis) etc.9 In rural areas of India, indoor air pollutants
like smoke from coal stoves and cooking oil have been at-
tributed to lung cancer as well.10 Further case-control stud-
ies to help establish a definite causal relationship with
these non-smoking factors is essential.
4. LUNG CANCER SCREENING
Wilson and Jungner laid down ten principles for disease
screening in 1968, which are still used while deciding on
screening recommendations for cancers.11 Lung cancer bi-
International Journal of Cancer Care and Delivery
ology and epidemiology make it a disease that would highly
benefit from screening. The United States National Lung
Screening Trial (NLST) and the Dutch-Belgian NEderlands
Leuvens Screening Onderzoek12 trial both demonstrated a
significant reduction in lung cancer-related mortality with
the use of annual low-dose CT screening in high-risk in-
dividuals.13,14 United States Preventive Service Task Force
(USPSTF) currently recommends LDCT for lung cancer
screening in high-risk patients in the United States of
America.15
The majority of the low- and middle-income countries
with a high incidence of lung cancer, like India, Bangladesh,
and Vietnam currently do not have screening guidelines
established for lung cancer. In most low- and middle-in-
come countries, nearly 80% of lung cancers are diagnosed
as stage III or IV. Mortality in lung cancer is stage-depen-
dent, with stage IV having the worst outcomes.16 Hence,
early detection of lung cancer with the help of screening
modalities can help decrease mortality. However, in practi-
cality, several barriers exist for an effective implementation
of lung cancer screening. A high prevalence of pulmonary
infections like tuberculosis results in a high false positive
rate.17 A positive screening test must be followed with sev-
eral invasive and non-invasive interventions to ultimately
lead to an accurate diagnosis. The imaging and interven-
tional modalities needed for lung cancer screening can add
to the already existing financial and infrastructure burden
in the low- and middle-income healthcare systems.17
5. MANAGEMENT OF NON-METASTATIC LUNG
CANCER
The goal of treatment for non-metastatic lung cancer is the
cure, primarily obtained with surgery or with definitive ra-
diation in patients who are not surgical candidates. Adju-
vant systemic therapy is added to stage II and III lung can-
cers to improve the cure and survival rates.15
Surgery: Anatomic surgical resection (lobectomy and
sometimes pneumonectomy) is the most common surgical
procedure that is performed for an early-stage lung cancer
with curative intent. The lung resection surgery can be per-
formed via open thoracotomy, video-assisted thoracoscopic
surgery (VATS) or robotic-assisted thoracoscopic surgery.18,
19 While VATS and RATS are associated with faster recovery
and lesser post-operative complications, there is no dif-
ference in cancer related survival outcomes compared to
open thoracotomy.20 When surgical resection is indicated,
open thoracotomy is the most commonly used approach in
most low- and middle-income countries.21 VATS is being
increasingly used in countries like Brazil and Vietnam.22,
23 RATS is less commonly available in most of these coun-
tries except for China, where robotic technology is rapidly
advancing.24,25 In countries with a high incidence of pul-
monary infections, like India and Nepal, there is a concern
for increased lung fibrosis and pleural adhesions making
minimally invasive surgical resection less feasible.26 The
availability of skilled surgical oncologists or thoracic sur-
geons and post-operative rehabilitation resources differ
widely throughout the world. The disparities in resource
2
 Lung cancer management in low and middle-income countries - current challenges and potential solutions
availability results in lower surgical resection rates; how-
ever, the overall post-operative outcomes are similar to
high-income countries.27
Radiotherapy (RT): For stages I and II non-small cell
lung cancer (NSCLC), definitive RT is used in patients who
are not surgical candidates. In inoperable stage III tumors,
it is used along with chemotherapy (concurrent or sequen-
tial). In stage IV lung cancer, it is used for treatment of
brain metastasis or oligo-progression or symptomatic dis-
ease. In limited-stage small-cell lung cancer (SCLC), pro-
phylactic cranial radiation is given following concurrent
chemoradiation to the chest.15 Hence, radiotherapy is a vi-
tal part of treatment for all stages of lung cancer man-
agement. The availability of radiotherapy equipment and
techniques is variable in each country. In general, there
is a paucity of RT availability in low- and middle-income
countries. For example, India has radiotherapy equipment
to serve only half of its current population.28 Furthermore,
only bigger cities within each country have established ra-
diotherapy centers, making it difficult for the rural popu-
lation to use them. Additionally, patients have a high wait
time to receive RT due to limited availability. For instance,
the average wait time for radiotherapy in Brazil is about 3-4
months.22 This can often result in the progression of the
disease from a curative to non-curative stage or can cause
the development of symptomatic metastasis intra- and ex-
tra-cranially.
6. MANAGEMENT OF METASTATIC LUNG
CANCER
Metastatic lung cancer is treated primarily with systemic
agents to help improve quality of life, progression-free sur-
vival, and overall survival. The goal of treatment is pal-
liative and not curative. Hence, it remains the most com-
mon cause of lung cancer-related mortality worldwide, with
an average 5- year survival of 5-7% in the United States
of America.29 The systemic treatment in lung cancer un-
derwent radical progress in the last decade with the dawn
of immunotherapy and targetable tyrosine kinase inhibitors
which are now readily available for patients in the high-
income countries like the North American and European
countries. However, most of the major clinical trials that led
to the approval of these agents (especially immunotherapy
trials) had minimal to no accrual from the low- and middle-
income countries located in the Middle East, South Asia,
and North and South African regions. This lack of inclusiv-
ity precipitates a lack of awareness, availability, and acces-
sibility which along with the high economic burden results
in lower utilization of these novel agents in low- and mid-
dle-income countries.
Tyrosine Kinase Inhibitors (TKI): Understanding the
oncogenic drivers and targeting them with small molecule
TKI revolutionized the management of non-small cell lung
cancer (NSCLC). However, TKI use in most low- and middle-
income countries is limited due to the lack of comprehen-
sive molecular testing, lack of access to several TKIs, and
the cost of the medication. It is thought that less than 50%
of patients with NSCLC throughout the world receive mol-
International Journal of Cancer Care and Delivery
ecular testing,30 and the most commonly cited reasons for
under testing are lack of availability/access and the cost. In
Brazil, EGFR evaluation is estimated to be used in only half
of the metastatic NSCLC due to the lack of advanced diag-
nostics.22,31 In Nepal, the samples for comprehensive test-
ing are sent to India and are generally associated with high
expenses.26 Like testing, there is also a stark difference
in the availability of TKIs between high-income and low-
income countries. Currently, several TKIs targeting EGRF,
ALK, ROS, NTRK, BRAF, MET, RET, and most recently,
KRAS G12C are approved and available in the USA and Eu-
rope. Out of all these mutations, EGFR is the most com-
monly encountered targetable mutation in NSCLC, with
prevalence much higher in the East Asian population (EGFR
mutation is noted in about 15% of NSCLC patients in the
USA while it’s frequency can be as high as 60% in East Asian
countries).32 China is one of the few Asian countries in
the upper-middle income group that actively participated
in several TKI studies and currently has access to multi-
ple TKIs targeting EGFR mutation, including Osimertinib.33
However, the same cannot be said about the rest of South-
East Asian countries. In Malaysia and Vietnam, Erlotinib
and Gefitinib are the only available EGFR-TKIs in the public
sector with reduced costs and national reimbursements.
The rest of the EGFR TKIs must be fully paid for by the
patients. The out-of-pocket monthly cost of Osimertinib is
about 2000$ in Malaysia and 8000$ in India/Brazil.34 A sim-
ilar trend is seen with TKIs targeting mutations other than
EGFR, with monthly costs ranging from 2000$ to 10,000$.28
Hence, their use is limited as a second-line treatment for
affluent patient populations in the tertiary healthcare sys-
tems.23,35
Immunotherapy (IO): In the non-oncogene-addicted
metastatic NSCLCs, an addition of immunotherapy signif-
icantly improved response rates and survival outcomes
when compared with standard chemotherapy.36‑39 Simi-
larly, in small cell lung cancer (SCLC), an addition of im-
munotherapy to chemotherapy improved OS and PFS ir-
respective of PDL1 immunohistochemistry.40,41
Immunotherapy is also responsible for producing a durable
clinical benefit.18,42 Currently, atezolizumab and durval-
umab (PDL-1 inhibitors) are FDA approved for metastatic
SCLC and, atezolizumab, pembrolizumab, cemiplimab (PD1
inhibitors) and nivolumab/ipilimumab (PD-1/CTLA4 in-
hibitor combination) are approved for metastatic NSCLC.15
Immunotherapy is also recommended in non-metastatic
NSCLC. Durvalumab significantly improved survival in
stage III NSCLC when given following chemoradiation.43
Atezolizumab in the adjuvant setting improved disease-
free survival for PDL-1 positive resectable stage II and IIIA
NSCLC.44 Additionally, neoadjuvant nivolumab in combi-
nation with chemotherapy has been shown to improve
pathological complete response rates in resectable stage I
to IIIA NSCLC.
Despite the ever-increasing evidence and indications for
immunotherapy in high-income countries, their availability
and utilization in low- and middle-income countries con-
tinue to remain low. Sudan does not have access to any im-
munotherapy agents or PDL-1 testing.45 In South Africa, no
3
 Lung cancer management in low and middle-income countries - current challenges and potential solutions
checkpoint inhibitors are available for first-line treatment
and Pembrolizumab is the only available IO in the second-
line setting.21 In India, IOs are sold as branded medications
and have an average cost of 2000-4000$ per vial, which sig-
nificantly restricts their use (especially in the first-line set-
ting).28 Similar trends of restricting IO use to second-line
setting are seen in most low- and middle-income countries
in the Middle Eastern, North African (MENA), and South-
east Asian regions due to a financial burden. Owing to the
lack of widespread global accessibility due to its cost, im-
munotherapy was not included in the essential medicine
list by WHO.46
Chemotherapy: Due to the cost and unavailability of
most TKIs and IOs, platinum-based doublet chemotherapy
remains the standard of care for first-line treatment of
metastatic NSCLC and SCLC in low- and middle-income
countries. In patients with NSCLC who have a driver mu-
tation, every attempt is made to get cost-effective access
to TKIs. In scenarios when the TKIs are unavailable or
not affordable, chemotherapy is given in the first-line set-
ting. There is not much discrepancy in the availability of
most first- and second-line chemotherapy agents except for
Pemetrexed which has limited availability in countries like
South Africa and Malaysia.
SUMMARY AND PERSPECTIVE
In summary, every single aspect of lung cancer manage-
ment, from epidemiologic risk mitigation to the availability
of palliative treatment, is strongly influenced by the re-
sources available in a country. These differences in the re-
sources are often attributed to the financial burden of treat-
ments, lack of accessibility and lack of awareness. Some of
the potential solutions are:
1. Lung cancer prevention and screening: Implementing
tobacco control policies like nicotine-replacement
therapies, smoking-related cancer awareness cam-
paigns and a nationwide ban on tobacco use in the
public places can help decrease the prevalence of lung
cancer. Use of plain packaging and graphic pictorial
warnings on nicotine products has been shown to de-
crease their attractiveness especially to young popu-
lation47,48 and hence, wider implementation of these
measures as suggested by WHO can help with smok-
ing cessation. New Zealand recently announced na-
tional plans to ban tobacco products for anyone born
after 2008. Similar age-based restrictions on nicotine
use can target the youth and decrease the incidence
of tobacco use. Hiking the prices of tobacco products
can decrease their use as well. In addition to smoking
cessation, starting a screening program can help re-
duce the long-term cancer-related mortality. Socio-
economic burden is the biggest challenge in provid-
ing appropriate screening in the low- and
middle-income countries, however, cultural concerns
and fear of radiation exposure can also rarely lead
to its underutilization.12 Hence, investigating to un-
derstand the local population’s outlook towards lung
cancer screening and raising awareness utilizing na-
International Journal of Cancer Care and Delivery
tional media can help deploy a successful screening
program. Though these measures can increase the
immediate cost of healthcare, focusing on lung can-
cer prevention and early detection can be cost-effec-
tive for a nation in the long run.
2. Clinical trials: There is an abundance of lung cancer
patients in low- and middle-income countries who fit
the general inclusion criteria noted in most lung can-
cer clinical trials. However, their inclusion in most
trials is dismal. Through clinical trials, patients can
get access to molecular testing and novel treatments
like TKIs and CPIs at minimal to no cost.
3. National health insurance coverage: The population
within each country is divided into multiple tiers
based on individual income. Patients from high-in-
come families can afford out-of-pocket payments or
private insurance. On the other hand, patients from
low-income households can rarely afford cancer
treatments without almost bankrupting their fami-
lies. Hence, having a nationally funded health in-
surance that works towards providing basic medical
care including coverage to the well-acknowledged di-
agnostics and cancer treatments can result in uni-
form oncologic care. In addition to national provi-
sions, state-based monetary help and hospital-based
medical coverage for cancer patients as seen in cer-
tain states/hospitals of India can bridge the economic
gap often seen in cancer care.
4. National cancer/disease registries: A national cancer
registry can provide information on the most preva-
lent cancers and their mortality in each country. This
can further help concentrate funds and resources on
the cancer types that are adding the most social and
economic burden on the country and its population.
International investigators can also use this registry
while considering clinical trial accrual.
5. National guidelines for management: Several low-
and middle-income countries like Sudan, Nepal, and
Georgia do not have national consensus guidelines
for managing lung cancer and rely on National Com-
prehensive Cancer Network (NCCN) and the Euro-
pean Society for Medical Oncology (ESMO) guide-
lines. NCCN has harmonized guidelines for countries
in the Sub-Saharan Africa, the Middle East, North
Africa, and the Caribbean regions.49,50 However,
there are no international guidelines that are focused
on managing cancer for patients from South Asia,
South-East Asia, Pacific Islands, and Latin America,
which also have several low- and middle-income
countries. Establishing national guidelines for man-
aging lung cancer can help provide uniform care to
patients within each country. Once these guidelines
are made publicly available throughout the country,
then, the insurance providers (both public and private
ones) can be petitioned to provide sufficient coverage
to the appropriate guideline-based treatments.
6. Teleoncology: Utilization of digital technologies like
Telemedicine became essential during the pandemic
era. In the low- and middle-income countries where
4
 Lung cancer management in low and middle-income countries - current challenges and potential solutions

Figure 1. Age-standardized incidence and mortality rates of lung cancer; source WHO 2020 data

the majority of the burden falls on the tertiary care

hospitals, appropriate use of Teleoncology can reduce
CONFLICT OF INTEREST
delay in oncologic care by triaging patients for
screening, lab tests or invasive diagnostics.51 It can None.
also help in patient counseling and surveillance.52
7. Cost of the medication: The most encountered barrier FUNDING INFORMATION
to appropriate treatment in low- and middle-income
countries is the cost of the treatment. Increasing the N/A
availability of bio-equivalent drugs can help decrease
their expense. TKIs like gefitinib and alectinib are ETHICAL STATEMENTS
available as generic agents in India, which decreased
the cost of the medication by almost half for the N/A
consumers. Doing the same for several TKIs and im-
munotherapy can help increase their affordability. ACKNOWLEDGEMENT
Another important potential solution is the use of
None
lower doses of therapeutic agents, especially im-
munotherapy to help mitigate their financial toxicity.
AUTHOR CONTRIBUTIONS
A recent phase III trial from India showed improved
survival in Head and Neck cancer with a combination i. All authors: conception and design
of Nivolumab given at 6% of the recommended dose ii. All authors: data collection and assembly
along with metronomic doses of chemotherapy iii. All authors: data analysis, manuscript writing
drugs.53 The possibility of ultra-low doses of anti-
cancer drugs providing similar efficacy in Lung cancer All authors have approved the manuscript
needs to be further explored as it can help signifi-
cantly decrease the total cost of the treatment.

International Journal of Cancer Care and Delivery 5

 Lung cancer management in low and middle-income countries - current challenges and potential solutions

Figure 2. Summary of potential strategies to improve cancer-related treatment access and outcome

Submitted: January 08, 2023 PST, Accepted: February 19, 2023

PST

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International Journal of Cancer Care and Delivery 6

 Lung cancer management in low and middle-income countries - current challenges and potential solutions
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