Arab Journal of Gastroenterology 13 (2012) 174–177

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Arab Journal of Gastroenterology

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Gastroenterology in Arab Countries

Predominance of females with oesophageal cancer in Gezira, Central Sudan

Moawia Elbalal Mohammed a, Daffala O. Abuidris b, Elgaili M. Elgaili c, Nagla Gasmelseed d,⇑a Department of Medicine, Faculty of Medicine, University of Gezira, Wad Medani, Sudanb Department of Oncology, National Cancer Institute, University of Gezira, Wad Medani, Sudanc Department of Pathology, Faculty of Medicine, University of Gezira, Wad Medani, Sudand Department of Molecular Biology, National Cancer Institute, University of Gezira, Wad Medani, Sudan

a r t i c l e i n f o

Article history:Received 23 June 2011Accepted 29 June 2012

Keywords:Oesophageal carcinomaFemalesGezira stateSudan

1687-1979/$ - see front matter � 2012 Arab Journal ohttp://dx.doi.org/10.1016/j.ajg.2012.06.012

⇑ Corresponding author. Address: Department ofCancer Institute, University of Gezira, P.O. Box 20, Wa

E-mail address: nag_la@yahoo.com (N. Gasmelsee

a b s t r a c t

Background: The majority of oesophageal cancer cases occur in developing countries. Globally males pre-dominate.Objective: This study aims to review the clinical aspects of oesophageal carcinoma in Sudanese patientsreferred to endoscopy in Gezira, Central Sudan.Patients & method: Data were collected from patients who underwent endoscopy during the period from2005 to 2007 at The Gezira Centre for Gastroenterology Endoscopies and Laparoscopic Surgery. Demo-graphic and clinical data including; sex, age, locality of residence, clinical presentation, tumour siteand morphology were collected and analysed.Results: Seven hundred and two patients were consecutively referred to our centre for endoscopy. Sev-enty-three out of 702 patients (9.6%) referred for endoscopy proved to have oesophageal cancer. Fifty-fiveout of 73 patients (75.3%) were females generating a male to female ratio of 1:3.3. The mean age offemales was 52.75 ± 11.66 years and that of males was 66.11 ± 9.52. Sixteen (21.9%) patients came fromthe Managil; 14 (19.2%) from Hasaheesa and Rufaa; 14 (19.2%) from Blue Nile; 10 (13.7%) fromWadmedani (Central Sudan) and 19 (26%) from Elfaw and Kassala. In most cases (75.3%), the tumourswere located in the middle third of the oesophagus. 79.5% of the tumours were squamous cell type.Conclusion: Patients referred for endoscopy to The Gezira Centre for Gastroenterology, Endoscopies andLaparoscopic Surgery in Gezira revealed a greater proportion of women than of men diagnosed with thedisease (1:3.3). More studies are needed to investigate the epidemiology of this disease and to identifythe reason for the apparent gender uneven manifestation.

� 2012 Arab Journal of Gastroenterology. Published by Elsevier B.V. All rights reserved.

Introduction group for males was 50 years and females 48 years. The mean

Oesophageal cancer (OC) is a disease with a wide variation inoccurrence between countries and within ethnic and populationsof a country [1]. Cancer of the oesophagus is the ninth most com-mon cancer in the world, affecting more than 400,000 people [2].The highest incidence is reported in what is so-called the ‘‘Asianoesophageal cancer belt’’ stretching from Eastern Turkey throughnorth-eastern Iran, northern Afghanistan and southern Russia tonorthern China. South Africa is another common area for OC espe-cially among blacks [1,3]. The majority of cases occur in developingcountries and it is relatively uncommon in the United States [4,5].Treatment of cancer of the oesophagus is problematic and mortal-ity rates are very high with no cure in the majority of cases, onlypalliative care can be offered and mortality is almost 100% within6 months [6]. In Ethiopia, a retrospective study was done by Baneet al., they showed a male to female ratio of 1.5:1. The mean age

f Gastroenterology. Published by El

Molecular Biology, Nationald Medani, Sudan.

d).

duration of major presenting symptoms was 4–6 months in bothoesophageal and gastric cancers [7].

There are many histological types of OC. The most common his-tological type is squamous cell carcinoma (SCC). Another commonmorphology is adenocarcinoma (AC) which occurs more in thelower third and in the oesophageo-gastric junction (OGJ) [6].

Common risk factors for SCC include alcohol, tobacco, (smoke-less tobacco), hot beverages, achalasia, lyme and caustic fluidsingestion (cancer in the upper third) [8–10]. Gastro-oesophagealreflux disease and Barrett’s oesophagus are associated mainly withAC (cancer in the lower third) [11,12].

The objectives of this study are to review the clinical aspects ofoesophageal carcinoma in Sudanese patients with symptoms andseeking medical care in Gezira Central Sudan and to compare themwith the national and internationally published series.

Patients and methods

Wadmedani teaching hospital (WTH) and The Gezira Cen-tre for Gastroenterology, Endoscopies and Laparoscopic Surgery

sevier B.V. All rights reserved.

M.E. Mohammed et al. / Arab Journal of Gastroenterology 13 (2012) 174–177 175

(GCGELS), are located in Wadmendani the Capital of Gezira State,the Central of Sudan, with wide catchment area serving patientsfrom different states of the country. The Gezira Centre for Gastro-enterology, Endoscopies and Laparoscopic Surgery (GCGELS) wasestablished in 2003 and since then it has been doing a tremendouswork regarding flexible upper and lower endoscopies.

During the period from January 2005 to December 2006, a totalnumber of 702 patients were endoscopied at (GCGELS) and a verbalinformed consent was taken from each patient. Out of those, 73 pa-tients (9.6%) presenting with dysphagia, which showed a histolog-ically proven oesophageal carcinoma, were included in the study.Demographic data including; sex, age, locality, clinical presenta-tion, tumour site and morphology were analysed. All patientshad an oesophageal biopsy under 3 mg of intravenous midazolamusing a flexible video-endoscope, Evis Exera, Olympus type. Thefirst author performed all the procedures. Histopathology speci-mens were examined by the third author who had a good experi-ence in histopathology. Data were analysed statistically usingStatistical Package for Social Sciences (SPSS) version 16.

Fig. 1. Age range of the study subjects.

Table 2Age group of patients with oesophageal carcinoma.

Age range No. of patients Percent

21–30 2 2.731–40 13 17.841–50 13 17.851–60 23 31.561–70 16 21.971–80 5 6.881–90 1 1.4Total 73 100.0

Table 3Histopathology type according to gender.

Histopathology Gender Total

Male Female

SQ cell carcinoma 8 50 58Adenocarcinoma 10 5 15Total 18 55 73

Fisher exact test = (16.11 P value = 0.00).

Table 4Location of the tumour and histopathology of the study subjects (N = 73).

Histopathology Level OGD Total

Upper 3rd Middle 3rd Lower 3rd

Squamous cell carcinoma 12 40 6 58Adenocarcinoma in Barrett’s 0 0 4 4Adenocarcinoma 0 0 11 11Total 12 40 21 73

Results

A total number of 73 patients were diagnosed with OC and theirdemographic and clinical presentations are reviewed. The meanage of patients was 65 ± 12.52 (min 26 and max 85 years). Fifty-five patients (75.3%) were females. A male to female ratio was1:3. The females were predominating compared with other neigh-bouring countries as in Table 1. The mean age of females was52.75 ± 11.66 (min 26–max 75 years), while that of males was66.11 ± 9.52 (min 40–max 85 years). The males’ age range in pa-tients presenting with oesophageal carcinoma is shifting to theright of the graph with high frequency between 61 and 71 years,while the females’ graph is shifting to the left with more frequentages between 51 and 60 years with a significant difference, P value<0.05 (Fig. 1).

Twenty-eight patients (38.4%) were less than 50 years of ageand the majority of 45 patients (61.6%) were above 51 years.Regarding the different age group affected Table 2 shows.

Thirty-eight patients (52.1%) gave a history of 3 weeks to2 months of dysphagia for solids. Twenty-three patients (31.5%)had dysphagia for both solids and liquids for 1–3 months. The restof the study group suffered from symptoms ranging from foodregurgitation, bleeding to anorexia and weight loss. SCC is morefrequent in females 50/58 (86.2%), while AC is more frequentlyseen in males 10/15 (66.7%). as in Table 3.

In 40 patients (54.8.2%) the tumour was located in the middlethird, in 21 cases (28.8%) was located in the lower third, while inonly 12 patients (16.4%) the tumour was located in the upper thirdof the oesophagus (Table 4).

In 58 patients (79.5%) the tumour was squamous cell type withvarying degree of differentiation ranging from highly anaplastic tothe well differentiated keratinizing squamous cell carcinoma. In 11patients (15.11%) the tumour was adenocarcinoma and four pa-tients developed Barrett’s oesophagus as shown in Table 4.

Table 1Comparison between sex ratio in endemic and non-endemic regions and this study.

Country Male:female References

This study (Sudan) 1:3.3Ethiopia 1.5:1 Bane et al. (2009)Uganda 1.8:1 Ocama et al. (2008)South Africa 3:1 Stewart (2003)United States 3:1 Daly et al. (2000)

Discussion

This is the first study of its kind in the centre of Sudan evaluat-ing oesophageal cancer, by using flexible video-endoscopy. Themajor presenting symptoms common to all patients was dysphagiato food or drink of various degrees of severity and duration averag-ing 2–3 months. Peter et al. in a population-based study inDenmark reported dysphagia of the same period of 5 years and

176 M.E. Mohammed et al. / Arab Journal of Gastroenterology 13 (2012) 174–177

pain was noticed only among three patients [13]. Kenya and Asal[14] in an epidemiological study in the United States noticed thatcases with carcinoma and with pain as the first symptom soughtmedical advice late compared to cases with dysphagia, the lattergroup seeking medical advice earlier [14]. Although this study isnot population based and with a small number of patients, yet itshowed that women are significantly (P > 0.05) much more af-fected than men with a ratio of 3.3:1. This is consistent with Geziracancer registry, National Cancer Institute 2009 (NCI) [15] data re-cords, and not conforming with East and South Africa [6,7,16]and also data from USA [17]. This predominance of females maybe due to several factors. Although, pernicious anaemia is an estab-lished risk factor for stomach cancer, a link between perniciousanaemia and increased risk of OC was studied in Sweden [18]reporting a significant excess risk of OC in the presence of perni-cious anaemia. In Sudan pernicious anaemia was studied by Abu-Sin and Ahmed [19] in three affected patients and they found thatit is uncommon among the Sudanese. Previous studies have re-ported a high prevalence of anaemia and folate deficiency amongpregnant women in Gezira and Eastern Sudan [20–22]. Iron defi-ciency may play a role in the occurrence of OC in Gezira, an effectwhich may be exacerbated in women of reproductive age throughblood loss during menstruation and also through repeated preg-nancies (average fertility rates in Sudan are 4.6 children per wo-men). Other probable risk factor, is the smoke produced by theburning of acacia wood (Acacia nilotica), which is used for cos-metic purposes by married women who, practise this ritual fre-quently. It is unknown if inhalation of this smoke, usually donein an enclosed space and in close proximity to the burning source,has any role as a cancer causing agent. Acacia bark has been stud-ied, on the other hand, for its apparent anti-cancer properties[23,24] but never before, to our knowledge, through burning ofthe wood. Polycyclic aromatic hydrocarbons (PAH) are incompletecombustion by-products and have been pointed out as carcino-genic agents, in particular benzo[a]pyrene (B[a]P). A recent studyin Iran [25] has found significantly higher levels of B[a]P biomark-ers in non-tumoural oesophageal epithelium from patients withOC than from control subjects suggesting a role of PAH in OC gen-esis. Inhalation of the Acacia wood smoke could expose women toPAH. Whether protective, associated with increased risk of cancer.

Boulos et al., found that in a series of 135 Sudanese, studied dur-ing the period of 1965–1974, the incidence of OC is 1.4% of allmalignant tumours and they showed that OC affected both sexesequally [26]. The same result was found by Babiker et al. [16]. Re-cently Mudawi et al. in a prospective descriptive study of 114Sudanese patients presenting with dysphagia found that the maleto female ratio was 1:1.04 [27], this is more or less consistent withour finding in showing the female preponderance. Babiker et al.and Boulos et al. mentioned that the risk factor of OC may not bedue to alcohol consumption or tobacco (smokeless tobacco) usein females in spite of the equal ratio [16,26].

What is alarming in this study is that the Managil area in thewestern part of Gezira State is ranking as a second area for theOC following the eastern part of Gezira, this is consistent withthe cancer registry of the NCI. In a retrospective hospital basedstudy done by El Mustafa et al during 1995-1999 showed thatfemales were predominant [28]. The increased incidence amongfemales was also noticed by Chanvitan et al. in the lower subregion of south Thailand [29]. Females were found to be affectedat a younger age with a mean age of 52.75 ± 11.66. This is consis-tent with the group studied by El Mustafa et al. and Ahmed thatshowed patients with OC were found to be affected at a medianage of 48 years [30].

In Iran, South Africa, Middle East countries, United States andEastern Europe men are more affected than women [3,17,6,31–33]. In conclusion this study showed that oesophageal carcinoma

in Central Sudan occurs commonly among females, thus reasonsaccounting for the greater number of women among OC casesare unknown, and it is and important to address as they reportexposure to established risk factors significantly less often thanmen in the general population. Thus, we believe that additionalrisk factors, not documented to date, operate in this populationand possibly through lifestyle, occupational, reproductive or/andenvironmental factors that might be avoidable.

Conflicts of interest

The authors declared that there was no conflict of interest.

Acknowledgement

The authors are grateful to Professor Ahmed AbdallaMohamadani for reviewing the manuscript.

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