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DEVELOPING COUNTRIES Johan Fagan, Clare Stannard, Sameera Dalvie

Developing countries constitute the majori- (Figure 3) 1. Even though developing

ty of the world’s landmass (Figure 1) and countries account for 67% of cancer-
are home to more than 50% of its people. related deaths, they account for only 5% of
cancer-related spending 1.

75% 72%
80% 64%
60% 46%
Figure 1: Developing (blue) vs. developed 0%
world (tan)

Cancer poses a major public health crisis

in the developing world. Developing coun-
tries accounted for >50% of newly diagno-
sed cancers in 2010; it is projected that this Figure 3: Case fatality from cancer
figure will increase to 70% by 2030 according to income levels of countries 1
(Figure 2) 1. This increasing percentage is
attributed to population growth, reduced Therefore it is apparent that it is essential
mortality from infectious diseases and an that innovation, expertise, resources, teach-
ageing society 1. ing and research be directed to addressing
cancer in the developing world if we are to
100% improve cancer outcomes globally. Given
the financial and infrastructural challenges,
80% 70% the cancer management also has to be
adapted to local constraints.
60% 56%
20% 15%
Rapid economic growth in developing
countries has been accompanied by life-
0% style changes associated with squamous
1970 2008 2030 cell cancer such as smoking, alcohol, and
Figure 2: Increasing percentage of global longevity. Two-thirds of oral and pharyn-
burden of cancer in the developing geal cancers (excluding nasopharynx)
countries 1 occur in developing countries 2. Figure 4
illustrates the significant geographical
There is a wide disparity in cancer-related variation for oral cancer; it is the most
fatality which is aligned with income common cancer in males in high-risk areas
levels, ranging from 75% in low income such as Sri Lanka, India, Pakistan and
countries, to 46% in high income countries Bangladesh where it accounts for up to
25% of all new cancers 2. The principal cervical lymph nodes may require orbital
causes of oral cancer are tobacco (smoked exenteration, parotidectomy, neck dissect-
or chewed) and betel quid 2. Cancer of the tion and orbital reconstructive procedures.
nasopharynx is also principally a develop- The association between HIV and mucosal
ing world problem where it is related to squamous cell carcinoma of the upper
Epstein Barr virus infection (Figure 5) 3,4,5. aerodigestive tract is less clear-cut 8.



One should guard against simply extra-

polating management protocols from deve-
loped world centres to head and neck
patients in developing countries.

1. Advanced cancers
Figure 4: Countries (brown) with high
incidence and mortality from oral cancer 2 Patients in developing countries are more
likely to present with advanced cancer 9, 10;
consequently treatment is mostly pallia-
tive 11. Even in a middle income country
like South Africa, 52% of patients under-
going total laryngectomy initially required
an emergency tracheostomy 12. Late pre-
sentation may be due to ignorance, pover-
ty, poor access to health services, and
patients consulting traditional healers and
using traditional medicines.

Figure 5: Nasopharyngeal carcinoma: The adverse consequences of delayed

Estimated age-standardised incidence presentation are compounded by long
rate/100,000; GLOBOCAN 2008 (IARC) 3 waiting lists for surgery and irradiation.
Frequently patients become inoperable
HIV is also associated with malignancies while awaiting surgery or radiation; this
of the head and neck. The prevalence of complicates initial patient selection and
HIV is highest in developing countries; treatment planning. Jensen et al (2007) re-
sub-Saharan Africa accounts for two thirds ported that one month’s delay was asso-
of HIV positive people 6. HIV is associated ciated with a 62% increase in tumour size,
with Kaposi’s sarcoma and non-Hodgkin’s 20% new nodal metastases, and that can-
(and Hodgkin’s) lymphoma; with Kaposi’s cers were upstaged (TNM) in 16% of pa-
sarcoma and lymphoma, surgery is restric- tients studied; mean tumour volume doub-
ted to obtaining a tissue biopsy. Squamous ling time was 3 months 13. Some institu-
cell carcinoma of the conjunctiva is also tions administer “holding chemotherapy”
associated with HIV 7. Patients with ad- (methotrexate or platinum-based drugs) in
vanced squamous cell carcinoma of the an attempt to slow tumour progression
conjunctiva and metastases to parotid and while patients await definitive treatment;

yet there is no evidence that this improves Do CD4 count and HIV status affect
outcomes. surgical outcomes? Even major surgery
does not depress CD4 counts 18, and HIV
2. Does HIV status matter? status per se does not increase the like-
lihood of early surgical complications 19. A
Do HIV +ve patients need to be managed depressed CD4 count (<100 cells/mm3) has
differently? One may need to consider the however been reported to be a predictor of
following questions when managing HIV postoperative sepsis 20, 21. Instituting anti-
+ve patients, especially when resources are retroviral therapy prior to surgery has the
limited: benefits of reducing the viral load of the
patient (viral exposure to surgical team),
Is radiotherapy accompanied by increased and increases patients’ CD4 counts.
mucosal and cutaneous toxicity in HIV
+ve patients? Although there are many It may be concluded that there is insuffi-
reports of radiotherapy-induced skin and cient evidence to modify treatment of
mucosal toxicity with Kaposi sarcoma, the “apparently healthy” HIV +ve patients
few reports of toxicity with other head and with head and neck cancer with CD4
neck malignancies indicate good tolerance counts of >350cells/mm3 16. There is also
to radiation +/- chemotherapy 14, 15, 16 little reason to routinely determine the HIV
status of healthy-looking head and neck
Should antiretroviral therapy be commen- cancer patients from an oncologic
ced to boost CD4 counts in immunocom- perspective alone; only when HIV infec-
promised patients prior to (chemo)radia- tion causes ill health and immunosuppress-
tion? Radiation can suppress CD4 counts. sion may HIV status preclude patients
Yet even though it may seem reasonable to from undergoing major surgery or chemo-
institute antiretroviral therapy to boost de- radiation.
pressed CD4 counts prior to radiation,
there are no controlled studies that address 3. How does one prioritise head and
this question. Although interactions be- neck cancer patients?
tween antiretroviral therapy and radiation
have not been well documented in the Deciding who or who not to treat when
literature, there is a theoretical concern the burden of cancer exceeds available
about the combination of the myelosup- treatment resources is perhaps the most
pressive effects of certain antiretroviral difficult task that oncologists and sur-
agents and myelosuppressive chemothera- geons in developing countries have to
peutic agents used with head and neck can- deal with. Arriving at a decision involves
cers such as platinum alkylators e.g. ethical and practical considerations such as
cisplatin and carboplatin. 16 tumour stage, prognosis, palliation vs.
cure, comorbidities, nutritional status, age,
What is the anticipated life expectancy of socioeconomic status, social support struc-
an HIV +ve patient? Adults that com- ture, distance from the closest treatment
mence antiretroviral therapy before CD4 centre, likelihood of regular follow-up,
counts drop to < 200 cells/mm3 have about parental status, employment status, and the
80% of normal life expectancy; even se- difficult ethical issue of possibly denying
verely ill HIV patients treated with antire- access to publicly funded treatment to
trovirals have at least an 80% chance of patients originating from a foreign country
surviving 2 years. 17 without adequate treatment facilities.

However, when access to surgery and and Zubizarreta et al (2004) reported a
radiotherapy are the principal treatment major restriction to access to radiotherapy
constraints, it is reasonable to prioritise in 16/18 South American countries due to
patients with the most curable (early insufficient numbers of specialists 23.
stage) malignancies, especially when ad-
juvant radiation is not available or will be Consequently most radiation services in
significantly delayed following resection the developing world are fairly basic and
of advanced malignancies. deliver mainly palliative care 9. Radiation
therapists also need to be cautious about
4. Radiotherapy extrapolating favourable treatment results
emanating from modern radiation thera-
Though central to treatment of head and py centres of excellence to situations whe-
neck cancer, radiotherapy is unavailable re reliance is placed on dated technology.
in much of the developing world. Abdel-
Wahab et al (2013) reported that only Patients that undergo radiation to the head
23/52 African countries had radiotherapy and neck require long term follow-up to
facilities, and that facilities were concen- detect and manage delayed radiotherapy-
trated in the southern and northern parts of related complications e.g. hypothyroidism
the continent (Figure 6); that brachythera- increases over time and is present in 25%
py resources were available in only 20 of patients at 5 years 24. Therefore reliabili-
countries; and that, because only 2% of ty for follow-up and the ability to monitor
African countries had modern imaging thyroid function and treat hypothyroidism
equipment and treatment planning systems, have to be considered when selecting
simple, curative treatment is generally patients for radiation.
based on two-dimensional imaging and
treatment planning 11. 5. Chemoradiation

In developed countries, chemoradiation

(mostly chemotherapy used concurrently
with radiotherapy / CCRT) is widely used
as an organ-sparing treatment strategy with
squamous cell carcinoma of the oral cavi-
ty, larynx, and oro-, hypo-, and naso-
pharynx. Compared to radiotherapy alone
it has an 8% advantage in terms of locore-
gional control and survival rates 25.

However, to achieve such favourable out-

comes, the “package of care” must inclu-
de modern, sophisticated imaging (CT,
MRI, PET) both for treatment planning
and follow-up, medical and intensive care
Figure 6: Radiation therapy services in support for chemotoxicity, PEG feeding,
Africa 11 and complex salvage surgery for persis-
tent cancer or for recurrence as well as
Tatsuzaki & Levin (2001) similarly repor- dental, speech, swallowing and audio-
ted significant unavailability of radiation logical rehabilitation. Salvage surgery re-
facilities in Asia and the Pacific regions 22; quires high levels of surgical expertise

including proficiency with free tissue care“ mentioned above should be availa-
transfer flaps. ble.

Because chemoradiation is expensive, 6. Altered fractionation

toxic 25 and complex treatment and requi-
res a “package of care” not available in Altered fractionation schedules also im-
many developing world centres, it has to prove locoregional control. Accelerated
be employed with great circumspection in radiotherapy is perhaps better suited to a
a developing world setting. developing world setting than chemora-
diation as it is cheaper and better tolerated.
Kumar et al reported a 14% mortality rate Overgaard et al reported that a 6-fractions-
during and within 30 days of treatment in per-week radiation schedule significantly
patients with advanced head and neck can- improved locoregional control for squa-
cer treated with concomitant boost radio- mous cell carcinoma of the larynx, pha-
therapy with concurrent weekly cisplatin at rynx and oral cavity when compared to
a tertiary hospital in India; the authors conventional schedules of 5-treatments-
attributed the high mortality to poor sup- per-week. Despite increased acute morbi-
port to deal with acute morbidity, poverty, dity, accelerated radiotherapy did not cause
malnutrition, illiteracy, and poor hygiene increased late morbidity and had the be-
and concluded that “on present evidence in nefit of reducing overall treatment by 1
the setting of a developing country, CCRT week 27. Concomitant boost radiotherapy
with concurrent cisplatin cannot be recom- with a 2nd daily fraction to the gross
mended as primary therapy in advanced tumour volume in the final 10 days of
head and neck cancers without formal treatment also reduces overall treatment
comparison with other treatment modali- time, thus reducing the chance of repopu-
ties” (Figure 7) 26. lation and improves local control 28.

However unless a radiation therapy depart-

ment already treats patients 6 days/week,
both the above schedules require reorgani-
sation to accommodate the 2nd daily frac-

7. Surgery

Surgery is often the only treatment availa-

ble because of inadequate radiotherapy and
chemoradiation facilities. Yet, surgeons in
developing countries frequently lack head
Figure 7: Locoregional Control (LRC) and and neck surgical training, and modern
Overall Survival (OS) 26 surgical technology (bipolar cautery, laser,
transoral robotic surgery, endoscopic sur-
Therefore, if chemoradiation is to be con- gery), frozen section, blood products, ade-
sidered, patients must be carefully selec- quate operating time, good anaesthesia and
ted to predict favourable outcomes by intensive care support are often lacking 29.
considering factors such as age, general
health, social support, immune (HIV) Surgeons in developing countries need to
status, tuberculosis, and the “package of keep abreast of and adapt modern surgical

principles and techniques to a lower tech-
nology type practice e.g. substitute trans-
oral microsurgery for early laryngeal can-
cer with laryngofissure and other open
partial laryngectomy procedures; ensure
wide tumour resection margins in the ab-
sence of frozen section control and post-
operative radiation therapy; liberally em-
ploy elective neck dissection in the absen-
ce of sophisticated imaging, and rely on a
range of pedicled rather than microvascu-
lar free tissue transfer flaps to reconstruct
surgical defects.

Figure 8: PET CT image of pulmonary TB:
Selecting appropriate treatment for head Roy M, Ellis S. Radiological diagnosis and follow-up of
pulmonary tuberculosis. Postgrad Med J 2010;86:663-74
and neck cancer patients in developing
countries is particularly challenging and
likelihood of regular follow-up; access to
involves complex, individualised decisions
drugs e.g. thyroid and calcium replace-
often without the benefit of special inves-
ment; nutritional status; social support; po-
tigations such as FNAC, CT, MRI, PET-
verty; comorbidities (often poorly treated
CT and HPV status.
or neglected) including HIV; cultural bias;
and the availability of surgical expertise,
Unlike the situation in well-resourced
radiation therapy and chemotherapy.
health systems, it may not always be
possible for treatment to be protocol-
Certain principles will now be highlighted
driven as the majority of patients are
that may be considered when designing
dependent on state run services with poor
management protocols in resource con-
health infrastructure and resources. For the
strained settings.
same reasons protocols designed for
developed world settings are not always
History: Consider cultural and religious
relevant; e.g. tuberculosis mimics metasta-
values of patients as these may affect man-
ses on PET scan, therefore limiting its uti-
agement. Inquire about risk factors inclu-
lity as a staging tool in societies where
ding betel nut, areca nut, reverse smoking,
tuberculosis is endemic (Figure 8).
chewing tobacco and comorbidities e.g.
Reliance therefore frequently is placed on
clinical acumen, experience, intuition and
Metastatic workup: When access to opera-
institutional bias, often in the absence of
ting time and adjuvant radiotherapy is limi-
scientific evidence to support clinical deci-
ted, one could argue in favour of employ-
sions. Investigations and treatment have to
ing CT (even if it is a limited and expen-
be tailored to the individual patient taking
sive resource) to rule out pulmonary me-
into account resource constraints relating
tastases that are not evident on CXR before
to e.g. CT, MRI, operating rooms, ICU,
(inappropriately) committing scarce surgi-
radiation facilities, and blood transfusions;
cal resources to advanced T and N stage
treatment delays (often many months);
cancers that have metastases.

N0 neck: It is reasonable to have a low Indications Ranking
threshold to electively treat the N0 neck by
means of a selective neck dissection in Primary tumour
cases of unreliable follow-up, lack of
specialised imaging (initially and for  Incomplete resection / +ve
follow-up), and delayed adjuvant radiation. margin / tumour peeled off
major structure e.g. carotid
Surgeons should have a low threshold to
convert a selective to a modified neck
 Tumour spillage
dissection when suspicious lymph nodes  PNI along major nerves e.g.
are encountered, especially in the absence VII, XII (macroscopic)
of postoperative radiation capability.  Invasion of bone marrow
 Advanced T stage
N+ neck: Even though lymphadenopathy  PNI along minor nerves
in patients from poorer communities may (microscopic)
result from untreated dental, oral and pha-  Close margins
ryngeal infections, HIV, or TB, palpable  Vascular and/or lymphatic
nodes within the expected lymphatic invasion
drainage area of a cancer should be treated  Invasive vs. pushing
with modified or radical neck dissection to margin/tumour islands
avoid undertreating a neck that harbours
metastases. Cervical metastases

Adjuvant irradiation: When the burden of  Extracapsular spread (ECS)

o Histological
disease outstrips a centre’s capacity to pro-
o Invading muscle/other
vide postoperative radiation to all deser- extranodal tissues
ving patients, an oncologist may have to o Attached to major struc-
make a call as to who are most likely to tures e.g. carotid artery
benefit. Even though studies do not rank o N3 node
accepted indications for postoperative ra-  Tumour spillage
diation, Table 1 is an attempted ranking  >3 nodes
(“thumb-suck”) of indications for adjuvant  <3 nodes
radiation (not to be cited). E.g. having >2
cervical metastases is generally considered
Table 1: Relative ranking of indications for
to be an indication for adjuvant radiation,
postoperative irradiation (A thumb-suck,
even though the evidence to support this
not to be cited)
threshold is tenuous; hence centres that
lack capacity to provide radiation to all de-
Reconstruction: Although excellent func-
serving patients could argue that this thres-
tional results can be achieved with micro-
hold be adjusted upwards so that patients
vascular free tissue transfer flaps 31, the
most likely to benefit e.g. with positive
surgery is time-consuming and requires
margins, extracapsular spread (ECS), and
specialised training. In the absence of mi-
large tumour volumes are not deprived of
crovascular free tissues transfer flaps, sur-
adjuvant radiation 30. A final (major) ca-
geons should become proficient at using a
veat relating to using histological criteria
range of pedicled flaps e.g. pectoralis
for adjuvant radiation is the inaccuracy of
major, buccinator, temporalis, nasolabial,
histopathological (under)reporting, espe-
buccal fat pad, deltopectoral, latissimus
cially of the presence of cervical micro-
dorsi and forehead flaps.
metastases and perineural invasion (PNI).

Oral cavity: When postoperative radiation shift with the realisation that HPV infec-
is unavailable, surgery for T1 and T2 can- tion is both an aetiologic and prognostic
cers should be prioritised, including can- factor for a subset of oropharyngeal squa-
cers that are T4 due to only limited bony mous cell carcinomas; the introduction of
invasion that can be resected by marginal transoral robotic surgery (TORS) to resect
or segmental mandibulectomy or by partial oropharyngeal tumours as well as attempts
maxillectomy. Cancers of the tongue and to reduce the morbidity of chemoradiation
floor of mouth that are palpable (likely to by accepting smaller resection margins
be >4mm thick) or are staged >T2 should when combined with postoperative radia-
undergo elective neck dissection due to the tion. However HPV testing, transoral robo-
likelihood of there being occult cervical tic surgery, and chemoradiation are gene-
metastases. Preserving oral function is rally not available in developing world
crucial; other than microvascular free centres; neither is the ability to deal with
transfer flaps, surgeons can employ pedic- adverse consequences of chemoradiation.
led flaps e.g. pectoralis major, buccinator, Surgical resection and/or radiation are
buccal fat pad, temporalis, nasolabial flaps. therefore the mainstay of treatment in
With inferior or total maxillectomy, one developing countries. Pedicled flaps used
must separate the oral cavity from the to reconstruct soft palate, lateral pharyn-
nose; if prosthetic appliances are not avai- geal wall or base of tongue include
lable, this can be achieved with temporalis pectoralis major, buccinator, buccal fat
muscle flaps. Without the facility to recon- pad, and temporalis flaps.
struct bone (e.g. free fibula flap), mandibu-
lar resection should not be extended be- Larynx and Hypopharynx: In developed
yond the midline so as to avoid the crip- world centres early cancers are commonly
pling and unsightly Andy Gump deformity excised with CO2 laser. Advanced cancers
(Figure 9). (dysfunctional larynx, cartilage invasion,
tracheostomy for stridor) are treated with
total laryngectomy. The remainder are of-
fered chemoradiation with surgery reser-
ved for salvage for persistent or recurrent
cancer. CO2 laser is generally not availa-
ble in developing world centres; chemora-
diation is expensive and the package of
care required to manage both acute and
late consequences and complications of
chemoradiation (dysphagia, PEG feeds,
cancer surveillance with MRI and PET
scans, complex salvage surgery, hypothy-
roidism, hypocalcaemia) is lacking. There-
fore such centres have to rely on open
approaches such as laryngofissure, vertical
partial, supraglottic, supracricoid and near-
total laryngectomy for smaller cancers, and
total laryngectomy for advanced cancers.
Figure 9: Andy Gump deformity When performing total laryngectomy the
surgeon should attempt to preserve both
Oropharynx: Management of cancers of thyroid lobes and the parathyroids to mini-
the oropharynx has undergone a paradigm mise the risks of hypothyroidism and hy-

poparathyroidism, particularly when thy- Brazilian study mastered oesophageal
roid and calcium monitoring and replace- speech 33. Another option is to use muco-
ment are difficult or impossible. With a sal shunts; however the surgery is techni-
dedicated speech therapy service, fistula cally difficult and can be used only in
(Figure 10) speech results can be achieved highly selected patients with good pulmo-
that match those of developed world nary function who can cope with aspiration
centres even with poor, illiterate patients . Because there is a severe shortage of
living long distances from treatment speech therapists in many developing
centres 32. Voice prostheses are however countries 28, 33 an electrolarynx is a reason-
expensive; hence the adoption of strategies able alternative to achieve post-laryngec-
such as using removable prostheses as tomy speech.
indwelling prostheses to reduce expense 32.
Heat moisture exchange (HME) devices Nasopharynx: Cancers of the nasopharynx
are used in developed world centres to occur mainly in the developing world
humidify and warm inspired air; however a (Figure 5). Chemoradiation is the mainstay
homemade cloth stoma cover/bib (Figure of treatment 34. However the supportive
11) is equally effective at a fraction of the care required for the extreme chemotoxi-
cost (Quail et al; unpublished study). city is not always available in developing
countries. Patients generally present with
advanced disease; in an unpublished study
conducted in Cape Town, South Africa,
50% of patients presented with Stage 4B
disease of which 28% did not complete
treatment for socioeconomic reasons
(Dalvie et al: unpublished data). Hence it
may be prudent to accept lower survival
using radiation alone, than to try to im-
prove survival with concurrent CTRT with
its attendant morbidity. Intensity modula-
ted radiotherapy (complex 3D conformal
radiotherapy) has a documented survival
Figure 10: Speaking valve
benefit and can improve quality of life due
to reduced xerostomia; however this
generally is not available in developing
countries 34.

Thyroid: Most thyroidectomies in deve-

loping countries are done by surgeons not
specialising in endocrine surgery. Bilateral
recurrent laryngeal nerve injury causing
airway compromise, or hypoparathyroid-
ism causing hypocalcaemia in situations
where monitoring serum calcium and treat-
ing hypocalcaemia with calcium and Vita-
Figure 11: Cheap homemade Bib min D are not possible may have fatal con-
sequences. Regardless of surgical exper-
Although oesophageal speech does not tise, complication rates rise with the extent
cost anything, only 27% of patients in a of resection. Subtotal thyroidectomy pre-

serves the blood supply to the parathyroid advice early when symptoms appear, edu-
glands and reduces the risk of hypocal- cating doctors and health care workers to
caemia. Thyroid lobectomy almost never recognise potential malignancies and to re-
causes significant hypoparathyroidism. fer patients early for appropriate manage-
Total thyroidectomy is however associated ment.
with both increased short- and long-term
morbidity relating to recurrent laryngeal
nerve paralysis and hypocalcaemia, parti- CONCLUDING REMARKS
cularly in an occasional thyroid surgeon’s
hands. In the absence of convincing evi- There needs to be a global effort to educate
dence that total thyroidectomy confers and train oncologists and surgeons to man-
survival benefit in favourable, differen- age head and neck cancer in developing
tiated thyroid cancer 35, 36 (especially when countries through residency programmes,
I131 therapy is not available), coupled with clinical fellowships and outreach projects.
the morbidity and mortality of total thy- These should focus on developing sus-
roidectomy where calcium monitoring and tainable head and neck cancer program-
replacement are suboptimal, the occasional mes, integrating them with existing local
thyroid surgeon practising in a developing services and focusing on teaching and
world centre may be wise to perform training. Open access to journals and text-
thyroid lobectomy or subtotal thyroidecto- books should be encouraged. In addition, a
my for such cases. multifaceted approach is required inclu-
ding lobbying international organisations,
governments and aid organisations to sup-
PREVENTION AND SCREENING port infrastructure development and re-
search, and for industry to provide appro-
Given the cancer tsunami that the develop- priate and affordable technology. In this
ping world is facing, and the late presen- way the developed world can make a
tations of patients with advanced disease, substantial difference to the outcome of the
prevention (education and anti-smoking enormous head and neck cancer burden in
campaigns) and screening would appear to the developing world.
be reasonable strategies to adopt. Yet a
Cochrane review reported that visual
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modified 09/26/2013. Available at:
(Accessed 19 October 2013)
The Open Access Atlas of Otolaryngology, Head &
Neck Operative Surgery by Johan Fagan (Editor) is licensed under a Creative
Commons Attribution - Non-Commercial 3.0 Unported

Chapter written: February 2014

Author and Editor

Johan Fagan MBChB, FCORL, MMed

Professor and Chairman
Division of Otolaryngology
University of Cape Town
Cape Town
South Africa