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Introduction
Dyspepsia, which by definition is the presence of one or more of
the symptoms of epigastric pain, bloating, post-prandial full-
ness, early satiation, and retrosternal pain [1], is estimated to
affect up to 50 % of individuals globally [2] with an estimated
higher prevalence in low and middle income countries, particu-
larly Africa with the highest prevalence of uninvestigated dys-
pepsia [3]. In one community study conducted in rural Uganda,
more than 50% of the respondents reported having had symp-
toms of dyspepsia [4]. The majority of dyspepsia in Africa is un-
investigated with patients often treated symptomatically. This
creates a challenge as treatable diseases including malignan-
cies are often missed only to present in very advanced stages.
Thepaucityofinformationondyspepsiainsub-SaharanAfrica
(SSA) also affects development of clinical and policy strategies
of mitigating causes including cancer of the stomach which is
the most prevalent gastrointestinal malignancy in SSA. SSA is
projected to have a more than 73% increase in gastrointestinal
cancers by 2030, way more than the 59% global estimate [5].
With uninvestigated dyspepsia masking this growing burden,
there is a need to fully understand the characteristics of dys-
High rates of gastroesophageal cancers in patients with dyspepsia
undergoing upper gastrointestinal endoscopy in Uganda
Authors
Ronald Mbiine1, Cephas Nakanwagi2, Olivia Kituuka1
Institutions
1 Department of Surgery, Makerere University College of
Health Sciences, Kampala, Uganda
2 Endoscopy Unit, Mulago National Referral Hospital,
Kampala, Uganda
submitted 20.1.2021
accepted after revision 12.3.2021
Bibliography
Endosc Int Open 2021; 09: E997–E1000
DOI 10.1055/a-1480-7231
ISSN 2364-3722
© 2021. The Author(s).
This is an open acce ss article published by Thie me under the terms of the C reative
Commons Attribut ion-NonDerivative-NonCommercial License, permitting copying
and reproducti on so long as the original work is given appropriate credit . Contents
may not be used for comme rcial purposes, or adapted, remixed , transformed or
built upon. (http s://creativecommons.org/licens es/by-nc-nd/4.0/)
Georg Thieme Verlag KG, Rüdigerstraße 14,
70469 Stuttgart, Germany
Corresponding author
Ronald Mbiine, P.O. Box 7072 Mulago Hill Road, Kampala,
Uganda
mbiineron@gmail.com
ABSTRACT
Background and study aims Dyspepsia is the most com-
mon presenting symptom in the gastrointestinal clinic of
Mulago National Referral hospital. The etiology is essential-
ly not fully described in our patient population. This study
was therefore conducted to establish the causes of dyspep-
sia based on endoscopic diagnosis among patients with
dyspepsia seeking care at the National Referral hospital of
Uganda.
Patients and methods This retrospective study conduct-
ed in the endoscopy unit of Mulago hospital reviewed 356
patient endoscopy reports spanning January 2018 to July
2020 with a focus on those with a referral indication of dys-
pepsia. Age and sex were the independent variables of in-
terest while the endoscopy findings as reported by the
endoscopist were the outcome variable of interest.
Results Of the 356 endoscopy reports reviewed, 159 met
the inclusion criterion of dyspepsia as the indication. Parti-
cipant mean age was 47.7 years (±16.53) with the majority
(25.79 %) in the fifth decade while the male to female ratio
was 1. The majority of patients had organic dyspepsia
(90.57 %) while the commonest finding was gastritis 69
(43.4 %). Gastroesophageal cancers represented (18)
11.32% of all findings. There was a positive association be-
tween age > 50 years with gastroesophageal cancers
(7.639) as well as age <50 years and functional dyspepsia
(2.794); however, all these were not statistically significant
(P= 0.006 and (P= 0.095, respectively).
Conclusions Organic/structural dyspepsia comprises over
90 % of investigated dyspepsia with 11 % comprising cancer
among patients seeking endoscopy at the National Referral
Hospital of Uganda.
Original article
Mbiine Ronald et al. High rates of …Endosc Int Open 2021; 09: E997–E1000 | © 2021. T he Author(s). E997
Article published online: 2021-06-17
peptic symptoms in our population seeking care for dyspepsia.
In one study in western Uganda, the majority of dyspeptic pa-
tients had gastritis [6] while in a study done in Kenya a signifi-
cant majority had functional dyspepsia [7], contrasting with a
study in Nigeria where only 8% of the participants had func-
tional dyspepsia [8]. Other studies conducted in Uganda are
representative of specific regions [9] and therefore non-gener-
alizable. This variability in findings, therefore, warrants a char-
acterization of dyspepsia in Uganda at a national referral center
that receives a more diverse patient population from all regions
in Uganda. This research, therefore, characterizes the etiology
of dyspepsia as seen on upper gastrointestinal endoscopy of pa-
tients seeking care at the National Referral Hospital of Uganda.
Patients and methods
This was a retrospective study conducted in the Endoscopy Unit
of Mulago National Referral Hospital of Uganda. This hospital
has a bed capacity 1500 at any given time and has 100% occu-
pancy consisting of primarily referrals from other hospitals
around the country. The gastrointestinal outpatient clinics
comprise one medical and one surgical outpatient unit, which
are attended by patients referred from other hospitals with an
average attendance of 2500 to 3000 patients per year. It is from
this population that patients referred for upper gastrointestinal
endoscopy are sent to the endoscopy unit. The endoscopy unit
also directly receives referrals from other hospitals in the re-
gion.
Despite receiving patients from all over the country, the ma-
jority of patients seeking care at the endoscopy unit are from
the surrounding central region of Uganda. Endoscopy services
are provided by experienced physicians and surgeons in the
unit and the diagnoses made are based on their observation of
the clinical characteristics of the disease entity. Where neces-
sary, biopsies are performed on suspicious tissues for further
evaluation. For gastritis, “endoscopic gastritis,”which refers to
the diagnosis of gastritis based on observations seen on endos-
copy, was the primary method of diagnosis and in severe forms,
biopsy with histological diagnosis of gastritis would be per-
formed. Diagnosis of gastritis is occasionally further classified
into superficial, hemorrhagic, erosive, atrophic, and metaplas-
tic.
Endoscopy reports of all patients that underwent an upper
gastrointestinal endoscopy procedure between January 2019
and January 2020 were reviewed. The referring doctor’sdiag-
nosis or reason for recommending an endoscopy as written on
thereferralnotewasreviewedforinclusioninthestudy.
Inclusion criteria
Referral reports with the diagnosis or reason for referral regis-
tered as either dyspepsia or uninvestigated dyspepsia by the re-
ferring doctor were included in the study. For referral notes that
had a different diagnosis besides dyspepsia, the diagnosis or
reason for referral was compared to the definition of dyspepsia
based on the ROME IV criteria [10] of having any of the follow-
ing: epigastric pain, epigastric fullness, early satiety, or burning
epigastric pain. When the referral reason or diagnosis met the
ROME IV criteria, the patient was included in the study. Reports
whose reason for referral was reported that did not meet the in-
clusion criteria, including some listed as dysphagia, odynopha-
gia, gastrointestinal bleeding, or screening endoscopy, all were
excluded from the study. For referral notes in which more than
one reason was included, such as dysphagia with dyspepsia,
these were also included as long as the indication of dyspepsia
was included in the referral note/endoscopy request. The en-
doscopies were performed by qualified endoscopists in the
unit.
The primary outcome variable of interest was the endo-
scopic diagnosis as reported on the endoscopy report by the
endoscopist. The findings were classified as organic/structural
if a physical lesion was observed on endoscopy while the pres-
ence of normal findings was classified as functional dyspepsia.
Other variables included the participant demographics includ-
ing the age, sex, tribe, and region.
Variables were captured in an Epi-data database and later
exported to Stata 16 software for analysis. Statistical analysis
took on a descriptive approach. All variables were categorical
and therefore described using proportions along with their per-
centages.
Results
In total, 356 patient endoscopy reports were evaluated and of
these, 159 met the inclusion criteria.
The male to female ratio of the study population was one
while the mean age was 47.70 years (±16.53) with the majority
(25.79 %) in the fifth decade of life (▶Table 1). On the primary
outcome variables of the endoscopic diagnosis, 90.57% of pa-
tients had organic dyspepsia, meaning that there was a diagno-
sis of a structural disease while 9.43% of the participants had
normal findings despite the dyspeptic symptoms (▶Table2), a
condition referred to as functional dyspepsia.
The most common findings on endoscopy were gastritis fol-
lowed by gastroesophageal reflux disease. Gastroesophageal
▶Table1 Participant demographic characteristics.
Parameter Frequency Percentage or ± SD
Age
< 30 29 18.24
31–40 27 16.98
41–50 28 17.61
51–60 41 25.79
60–70 17 10.69
> 70 17 10.69
Mean age 47.698 ± 16.53
Sex
Male 79 49.69
Female 80 50.31
E998 Mbiine Ronald et al. High rates of …Endosc Int Open 2021; 09: E997–E1000 | © 2021. The Author(s).
Original article
cancers (gastric and esophageal cancer) comprised 11.32% of
all diagnoses (▶Table 3). Of the 18 patients who had a diagno-
sis of gastrointestinal cancer, 61% had gastric cancer while the
rest had esophageal cancer (▶Table 4).
On evaluation for the association between the two indepen-
dent variables of age and sex with the primary outcome vari-
able, age was stratified into two categories: <50 years and > 50
years. We found no associationbetween age and gastritis with a
chi square coefficient of 0.612 while the presence of gastro-
esophageal cancers was strongly associated with age >50 years
with a positive coefficient of 7.639 (P=0.006) while that of
functional dyspepsia was 2.794 (P= 0.095). However, these
variables were not statistically significant in our study popula-
tion. In regard to the location of the cancer, there was no asso-
ciation with age or sex. Similarly, there was no association be-
tween sex and the overall endoscopy diagnosis.
Discussion
We conducted this study with the intention of describing
endoscopy findings among patients who underwent upper gas-
trointestinal endoscopy for dyspepsia as it is the most common
presenting symptom and indication for upper gastrointestinal
endoscopy at the Gastrointestinal Surgery Clinic in Mulago Na-
tional Referral hospital in Uganda.
We found that the majority of patients who presented for
upper gastrointestinal endoscopy were aged 51 to 60 years. In
Uganda, it is recommended but not mandatory that the pres-
ence of dyspeptic symptoms should be investigated with
endoscopy in patients aged >50 years. The public health train-
ing and awareness campaigns about gastric cancer could ex-
plain the higher proportion in this age group. Globally screen-
ing for gastroesophageal cancers is recommended in dyspeptic
patients aged > 40 years [11, 12] and this is in keeping with our
findings.
Our study reveals a very high prevalence of organic dyspep-
sia of > 90 % which could imply that by the nature of our study
setting being a national referral hospital, the most severe and
persistent symptomatic patients could possibly be the ones
seeking care at the national referral hospital, and hence, likely
to have more organic causes. This, therefore, is a potential
source of bias. Second the majority of referrals often come
late, due to either financial constraints associated with the pro-
cedure or perceptions such as disease progression after biopsy.
All these could explain the high rate of organic dyspeptic find-
ings being representative of late presentation. However, when
the prevalence of organic dyspepsia among patients with dys-
pepsia is compared with studies conducted in the African re-
gion, there is a striking similarity. In Kenya, the prevalence was
slightly lower at 8 % [7], implying a 92 % prevalence of organic
dyspepsia. while in a similar study in Ibadan, Nigeria, the prev-
alence of functional dyspepsia among dyspeptic patients was
lower at 6% [13], implying a prevalence of organic dyspepsia
of 94 %. Overall, the global prevalence of functional dyspepsia
is approximately 11 % to 29.2 % [3]. Our findings along with the
studies in SSA demonstrate that the majority of dyspepsia is
duetoanorganiccause.
The finding that gastritis was the most prevalent condition in
our study population was not surprising as it is similar to the de-
scribed findings in other regions of Uganda [6] and
SSA [14, 15]. Not surprisingly, there was no association be-
tween the age and sex in gastritis or any other endoscopic find-
ings among the study population.
Gastroesophageal cancer presentation, especially in early
stages, mimics any other benign causes of dyspepsia [16],
hence increasing the likelihood of missed early diagnosis [17]
in patients with dyspepsia. In our study population, the preval-
▶Table2 Endoscopic findings.
Diagnosis Frequency Percentage
Normal findings 15 9.43
Gastritis 69 43.4
Gastric ulcers 3 1.89
Duodenal ulcers 5 3.14
Hiatal hernia 4 2.52
GERD 31 19.5
Gastric cancer 11 6.92
Esophageal cancer 7 4.40
Esophagitis 2 1.26
Others 12 7.55
GERD, gastroesophageal reflux disease.
▶Table3 Dyspepsia classification.
Dyspepsia classification Frequency Percentage
Functional dyspepsia 15 9.43
Organic dyspepsia 144 90.57
▶Table4 Location of gastroesophageal malignancies.
Tumor type and location Frequency (N) Percentage (%)
Esophagus (7)
Proximal third 1 5.56
Mid third 5 27.78
Distal third 1 5. 56
Stomach (11)
Upper stomach (cardia and
upper body)
3 16.67
Middle stomach (angle,
middle body)
3 16.67
Lower stomach (lower body,
antrum, pylorus)
5 27.78
Mbiine Ronald et al. High rates of …Endosc Int Open 2021; 09: E997–E1000 | © 2021. The Author( s). E999
ence of gastroesophageal cancers among patients with dyspep-
sia was rather strikingly high at 11.32% when compared to lar-
ger studies in Hong Kong [18] and Canada [19], in which the
prevalence was less than 1%. However, it should be noted that
the above studies had a significantly larger sample size. Never-
theless, these findings raise a red flag for a potentially higher
prevalence of gastroesophageal malignancies among dyspeptic
patients in Uganda. This further emphasizes the need for more
purposeful investigation for gastroesophageal malignancies in
patients in SSA who present with dyspepsia, especially in the
fourth decades and above.
Its projected that SSA will have the highest burden of gastro-
esophageal cancers globally by 2030 [5] and this is a red flag
our results seem to agree with. Typically esophageal cancer
presents with dysphagia and patients with dysphagia were ex-
cluded; however, it’s important to recognize that dyspepsia,
especially retrosternal pain, may point towards early esopha-
geal cancer, hence requiring early screening [20].
Conclusions
More than 90% of dyspepsia in patients seeking care in Mulago
hospital is associated with a structural/organic lesion, including
gastritis, among other causes. There is a higher prevalence of
gastroesophageal cancer among patients with dyspepsia who
are aged >50 years. We recommend that patients aged >50
years who have dyspepsia that has not been investigated under-
take a mandatory endoscopic evaluation as the likelihood of
having a gastroesophageal malignancy in this population is
very high.
Acknowledgements
The authors thank the wonderful staff of the Endoscopy Unit of
Mulago National Referral Hospital.
Competing interests
The authors declare that they have no conflict of interest.
References
[1] Ford AC, Bercik P, Morgan DG et al. The Rome III criteria for the diag-
nosis of functional dyspepsia in secondary care are not superior to
previous definitions. Gastroenterology 2014; 146: 932–940; quiz
e914–935
[2] Talley NJ, Zinsmeister AR, Schleck CD et al. Dyspepsia and dyspepsia
subgroups: a population-based study. Gastroenterology 1992; 102:
1259–1268
[3] Mahadeva S, Goh K-L. Epidemiology of functional dyspepsia: a global
perspective. World J Gastroenterol 2006; 12: 2661–2666
[4] Lee YJ, Adusumilli G, Kyakulaga F et al. Survey on the prevalence of
dyspepsia and practices of dyspepsia management in rural Eastern
Uganda. Heliyon 2019; 5: e01644
[5] Singh P, Irabor D, Adedeji O. Gastrointestinal cancers in Sub-Saharan
Africa.Adedeji O. Cancer in Sub-Saharan Africa: Current Practice and
Future. 1. Aufl. UK: Springer International Publishing; 2017:
doi:10.1007/978-3-319-52554-9_9
[6] Obayo S, Muzoora C, Ocama P et al. Upper gastrointestinal diseases in
patients for endoscopy in South-Western Uganda. Afr Health Sci
2015; 15: 959–966
[7] Yuo PO, Some FF, Kiplagat J. Upper gastrointestinal endoscopy find-
ings in patients referred with upper gastrointestinal symptoms in El-
doret, Kenya: A retrospective review. East African Med J 2014; 91:
267–273
[8] Onyekwere CA, Hameed H, Anomneze EE et al. Upper gastrointestinal
endoscopy findings in Nigerians: a review of 170 cases in Lagos. Ni-
gerian Postgrad Med J 2008; 15: 126–129
[9] Ogwang M. Dyspepsia: endoscopy findings in Uganda. Tropical Doc-
tor 2003; 33: 175–177
[10] Stanghellini V. Functional dyspepsia and irritable bowel syndrome:
beyond Rome IV. Digest Dis 2017; 35: 14–17
[11] Choi KS, Suh M. Screening for gastric cancer: the usefulness of
endoscopy. Clin Endosc 2014; 47: 490–496
[12] Liou JM, Lin JT, Wang HP et al. The optimal age threshold for screening
upper endoscopy for uninvestigated dyspepsia inTaiwan, an area with
a higher prevalence of gastric cancer in young adults. Gastrointest
Endosc 2005; 61: 819–825
[13] Olokoba AB, Salawu FK, Vickola JA. Functional dyspepsia in Yola, Ni-
geria. Res J Health Sci 2015: 3
[14] Ayana SM, Swai B, Maro VP. Upper gastrointestinal endoscopic find-
ings and prevalence of Helicobacter pylori infection among adult pa-
tients with dyspepsia in northern Tanzania. Tanzania J Health Res
2014: 16
[15] Agyei-Nkansah A, Duah A, Alfonso M. Indications and findings of up-
per gastrointestinal endoscopy in patients presenting to a District
Hospital, Ghana. Pan Afr Med J 2019; 34: 82–82
[16] McColl KEL, Kidd J, Gillen D. Gastric cancer in patients with benign
dyspepsia. Gut 2000; 47: 741
[17] Schmidt N, Peitz U, Lippert H et al. Missing gastric cancer in dyspep-
sia. Aliment Pharmacol Therapeut 2005; 21: 813–820
[18] Sung JJ, Lao WC, Lai MS et al. Incidence of gastroesophageal malig-
nancy in patients with dyspepsia in Hong Kong: implications for
screening strategies. Gastrointest Endosc 2001; 54: 454–458
[19] Breslin NP, Thomson ABR, Bailey RJ et al. Gastric cancer and other
endoscopic diagnoses in patients with benign dyspepsia. Gut 2000;
46: 93
[20] Bird-Lieberman EL, Fitzgerald RC. Early diagnosis of oesophageal
cancer. Br J Cancer 2009; 101: 1–6
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