Human Papillomavirus Types and Cervical Cancer Vaccine for Sudanese Women: A Review

Abstract

Cervical cancer is thought to result from different high-risk human papillomavirus (HPV) types. Although many studies have been conducted worldwide regarding HPV infection and its oncogenic properties, limited data are available on the incidence and genotype specific dissemination of HPV in Sudan. The purpose of this review article is to summarize the existing data regarding HPV genotypes in Sudan. To review the distribution of HPV infections, electronic databases (e.g. PubMed, and Google Scholar) were searched for peer reviewed articles in English. The study was performed between January and April of 2019 and comprises a review of six relevant articles that were published prior to 2013. Inclusion criteria included: availability of general population data, cytology and tissue results and the use of polymerase chain reaction (PCR) for HPV detection. The overall infection rate of high-risk HPVs DNA was 173/506 (34%) and within the tissues ranged between 93 and 94% (all the paraffin sections were cancer and precancerous cases). The HPV genotyping in cervical smears were found to range from 2.9% to 50.0%, with the most prevalent types of HPV being 16 (2.9-50.0%), 18 (0-3.4%), 58 (2.9%), and 42 (2.9%). Familiarity of the frequent high risk HPV genotypes found in Sudan, which had a high prevalence of cervical cancer, is essential in order to construct an applicable genotype of the virus in the HPV vaccine. The commercially available vaccines do not prevent infection of the HPV types not contained in the vaccine. Based on this literature, it is clear that the nine-valent HPV vaccine should be considered in Sudan.

Full text

European Journal of Preventive Medicine
2019; 7(6): 95-99
http://www.sciencepublishinggroup.com/j/ejpm
doi: 10.11648/j.ejpm.20190706.11
ISSN: 2330-8222 (Print); ISSN: 2330-8230 (Online)
Human Papillomavirus Types and Cervical Cancer Vaccine
for Sudanese Women: A Review
Magdi Mansour Salih
Department of Clinical Laboratory Sciences, Taif University, Taif, Kingdom of Saudi Arabia
Email address:
To cite this article:
Magdi Mansour Salih. Human Papillomavirus Types and Cervical Cancer Vaccine for Sudanese Women: A Review. European Journal of
Preventive Medicine. Vol. 7, No. 6, 2019, pp. 95-99. doi: 10.11648/j.ejpm.20190706.11
Received: September 30, 2019; Accepted: October 28, 2019; Published: October 31, 2019
Abstract:
Cervical cancer is thought to result from different high-risk human papillomavirus (HPV) types. Although many
studies have been conducted worldwide regarding HPV infection and its oncogenic properties, limited data are available on the
incidence and genotype specific dissemination of HPV in Sudan. The purpose of this review article is to summarize the existing
data regarding HPV genotypes in Sudan. To review the distribution of HPV infections, electronic databases (e.g. PubMed, and
Google Scholar) were searched for peer reviewed articles in English. The study was performed between January and April of
2019 and comprises a review of six relevant articles that were published prior to 2013. Inclusion criteria included: availability of
general population data, cytology and tissue results and the use of polymerase chain reaction (PCR) for HPV detection. The
overall infection rate of high-risk HPVs DNA was 173/506 (34%) and within the tissues ranged between 93 and 94% (all the
paraffin sections were cancer and precancerous cases). The HPV genotyping in cervical smears were found to range from 2.9% to
50.0%, with the most prevalent types of HPV being 16 (2.9-50.0%), 18 (0-3.4%), 58 (2.9%), and 42 (2.9%). Familiarity of the
frequent high risk HPV genotypes found in Sudan, which had a high prevalence of cervical cancer, is essential in order to
construct an applicable genotype of the virus in the HPV vaccine. The commercially available vaccines do not prevent infection
of the HPV types not contained in the vaccine. Based on this literature, it is clear that the nine-valent HPV vaccine should be
considered in Sudan.
Keywords:
Human Papilloma Virus Genotypes Vaccine, Cervical Cancer
1. Introduction
Cervical cancer is one of the most common diseases
worldwid e. The universal prevalence rate of cervical
cancer is approximately 11.7%. Among asymptomatic
women, the global cervical HPV prevalence rate is
estimated to be 10.4% and it differs across geographical
sectors, ranging from 6.2% in south-eastern Asia to 31.6%
in East Africa, out of which.
Sub-Saharan Africa was found to be the most affected
with the highest preponderance rates. In Sudan, cervical
cancers are the second most prevalent type of cancer; 90.9%
of cancers in Sudan are squamous cell carcinoma, 4.8% are
adenocarcinomas, and 4.3% are other epithelial tumors [1].
Viral infections comprise 15-20% of all human cancers and
the interaction between a given virus and its correlated
cancer ranges from 15-100% [2]. HPV may be co-infected
with the human immunodeficiency virus (HIV) and other
microorganisms. Co-infections, specifically HIV-HPV
infection cause higher HIV reduplication and condition
advancement through the activation of cellular mechanisms
in the immune system that make cells liable to HIV elevated
viral load amount [3]. Most cervical cancers (globally) are
due to the human papillomavirus (HPV) infection [4]; HPVs
are a large group of viruses, which consist of more than 180
different types, of which, 15 have high oncogenic equity [5].
Infection with HPV can lead to different types of disorders,
from benign lesions to cancer. HPV is a DNA virus from the
Papillomavirus family. The classification 'high-risk' and
'low-risk' are common and reveal the types that are
commonly found in cervical cancers, in contrast to the types
that are rarely or never appear in cervical cancers [6]. HPV18
was first described in 1984 by Boshart and his group [7] and
is known to be present in a higher proportion of cervical
adenocarcinomas than cervical squamous cell carcinomas
[8]. HPV is transmitted sexually, and causes a great health

96 Magdi Mansour Salih: Human Papillomavirus Types and Cervical Cancer Vaccine for Sudanese Women: A Review
burden in both men and women [9]. Following HPV
infection, seropositive men are at an increased risk for
developing penile and anal cancer; some studies showed
HIV-HPV seropositive individuals are 60% more likely
(than healthy individuals) to develop cancer [10].
Additionally, heterosexual HPV-seropositive can transmit
HPV into female partners, which increases the risk for
cervical cancer [11]. The International Agency for Research
on Cancer (IARC) working group classified HPV into 21
types (HPV 6, 11, 16, 18, 26, 31, 33, 35, 39, 45, 51, 52, 53,
56, 58, 59, 66, 68, 70, 73 and 82) that are most prevalent in
their association with cervical tumors [12]. However,
information regarding HPV infection epidemiology in Sudan
is scarce and scattered. Therefore, the purpose of this review
article is to summarize the existing data on HPV genotypes
in Sudan, provide clarity for future research directions, and
to enhance public awareness of HPV infection and
HPV-related diseases in Sudan.
2. Materials and Methods
2.1. Design
This study was conducted using a computerized systematic
search. The Literature search was performed through a
detailed survey of the issued peer reviewed articles on HPV
infection and cervical cancer in Sudan with publication dates
prior to April 20, 2019 using the following databases: PubMed,
Scopus, Web of Science and Google Scholar. The search was
completed without language limitation between January and
April of 2019. The keywords “HPV”, “Sudan”, “genotype”,
and “cervical cancer” were used in the search. This resulted in
six relevant articles. Abstracts from these six articles were
read to determine relevance to this review. Original articles
that were included in this review mentioned at least one
specific HPV-related test that was being evaluated. Data were
included from international journals and local, non-indexed
medical journals and the following inclusion criteria were
applied: cervical cytology and paraffin wax embedded tissue
results available, use of PCR for viral DNA detection and
genotyping. Exclusion criteria included articles that were
published before 1990 and articles that described the
contribution of HPV infection to oral and other types of cancer.
Morbidity was not included. The application of these
inclusion/exclusion criteria resulted in six relevant articles on
the topic of the review. Of the articles reviewed, one was a
report from local non-indexed journals that was published in
Egypt: Acad. Journal. Biological. Sciences. The link is
provided in the list of references. In general, the information
available on HPV prevalence in Sudan is very ambiguous and
it became obvious that further research studies are necessary
in this field.
2.2. Ethical Consideration
This article is based on published data, and hence, ethical
approval was not required.
3. Results
HPV Infection in Sudan - Prevalence and Type Distribution
There have been many studies worldwide regarding the
epidemiology of HPV infections and oncogenic properties that
result from different HPV genotypes. However, limited data
are available regarding HPV prevalence, incidence and
genotype specific dissemination in Africa, no data regarding
the epidemiology of HPV infections are available for the
Sudanese population. There are only a few articles in
reference to HPV infections in Sudan that have been published
in international peer reviewed journals, although there are
several articles in local medical journals. The first article in
Sudan that investigated HPV genotyping published in an
international journal presented the results of 135 patients in
the Omdurman Military Hospital [13], and were tested for
(beta)-globin using PCR, as described by Jacobs et al. [14],
and Human papilloma virus infections were analyzed using a
general primer GP5+/6+ mediated PCR enzyme
immune-assay (EIA), also described by Jacobs et al. [14]. of
these 135 smears, there were 60.7% ß. globin positive samples
indicating DNA integrity. HPV DNA was identified in three
samples (2.2%) by gel electrophoresis and was positive in four
samples (2.9%) as single and multiple infections by
PCR-ELISA. The high risk HPV types (16 and 58) were
identified in one sample as a mixed infection. The low risk
HPV types (40 and 42) were also found as a mixed infection in
another patient. HPV types 58 and 42 were identified in the
other two patients. They reported that the HPV genotypes
identified were not associated with cancer [13]. The search in
the international journals for HPV epidemiology has allowed
us to identify the largest study of HPV prevalence (400
samples), which was done in the Khartoum state [15]. The
study on HPV prevalence and distribution was performed by
analyzing prospective cervical smears taken from women
attending different hospitals in Khartoum State during the
period between July of 2008 and July of 2009. Isolated DNA
from cervical scrapes was subjected to PCR of each GP5
(sequence 5" to 3": TTT GTT ACT GTG GTA GAT ACT AC),
and GP6 (sequence 5" to 3": GAA AAA TAA ACT GTA AAT
CAT ATT C) primers using a PCR processor (PE9600;
PerkinElmer) [15]. HPV DNA was found in 144 samples
(36.0%) that showed a product that was typical in size (150
bp), as indicated by the standard DNA marker 5. HPV was
detected at a high ratio among patients with cervical
intraepithelial neoplasia 29/30 (96.7%). Although, that study
did not assess the different genotypes of HPV. Another study
used cervical smears to investigate 40 cases. HRHPV 16 and
18 were identified in 16/40 (40%) of the cervical tissues and of
these, 8/16 (50%) were positive for HPV 16, 6/16 (37.5%)
were positive for HR-HPV 18, and 2/16 (12.5%) were positive
for both HR-HPV subtypes. PCR was used for these
detections [16]. In 2013, Sahar studied human papilloma virus
infection among 106 cervical smears. HR-HPV DNA was
detected in 29/106 (27.4%) patients using in situ hybridization.
Using the GenPoint Kit (#K 0620; DAKO) according to the
manufacturer's instructions, the risk associated with high risk

European Journal of Preventive Medicine 2019; 7(6): 95-99 97
HPV infection was found to be statistically significant [17].
Ebba Abate genotyped the Human Papillomavirus in paraffin
embedded cervical tissue samples from women in Ethiopia
and Sudan, and included 86 paraffin embedded tissues. PCR
was used for DNA detection and 98% (85/86) of the samples
were positive for the housekeeping gene, Beta-globin.
Probable HR-HPV, the overall HPV DNA was 94% (80/85)
Include 17 different HPV genotypes [18]. Huda investigated
cervical and oral screening for HR-HPV types 16 and 18
among Sudanese women with cervical lesions. They detected
HPV DNA in 93.6% (73/78) of the cancer samples, sixty
tumor samples harbored HPV genotype 18. Single infection
with this genotype was found in 40 samples (51.3%), while
mixed infection was detected in 20 samples (25.6%). The
HPV genotype 16 was found in 33 tumor samples. Single
infection with this genotype appeared in 13 patients (16.7%),
while 20 samples (25.6%) had mixed infections [19].
4. Discussion
The HPV DNA in Sudan was detected in cervical smears
and tissue-based HPV genotyping studies of cervical cancer
681 (80.6%) and 164 (19.4%), respectively. Within the
cervical smears, the overall infection rate of high-risk HPVs
DNA was found to be 173/506 (34%) and within the tissues
ranging from 93% to 94% as all the paraffin sections were
cancer and precancerous cases. The HPV genotyping in
cervical smears were found to range from 2.9% to 50.0%, with
the most prevalent types of HPV being 16 (2.9-50.0%), 18
(0-3.4%), 58 (2.9%), and 42 (2.9%). The genotypes within the
paraffin section (with the most common HPV genotypes) were
16 (60.4%), and 18 (34.1%). High rates of HPV infection was
detected in premalignant conditions. This finding supports the
importance of early diagnosis and treatment that can be made
on the basis of cytology and confirmed with histopathology. In
addition, the results of these studies strengthen the need for the
detection of high risk HPV as a screening method for early
detection of precancerous stages. Human papillomavirus 16
was the most numerous genotypes identified from all the HPV
positive cervical smears and tissue sections. This genotype
was also the most persistent in all cancerous and precancerous
conditions. The prevalence of HPV 16 over the other
genotypes (among these studies) is in agreement with previous
reports from different geographical areas [20, 21, 22]. Few
studies have been conducted in Africa to assess the
distribution of HPV genotypes (HPV 58 was common in the
current studies). However, HPV 58 is considered a rare type,
and is not commonly reported in most of Europe. However, in
Africa, this type has been observed in the east, central, west
and in South Africa [23]. This finding could reflect
international differences in the distribution of HPV. A high
preponderance of high risks for HPV 16, 18 and 58 were
determined with the different samples. HPV 16, 18 and 58
were revealed in cervical smear and paraffin blocks 6.8.%
(12/175) vs. 42% (99/164), 3.4% (6/175) vs. 34.1% (56/164)
and 2.9% (4/135) vs. 15% (12/80) of all HPV positive samples,
respectively. Studies have shown that 58 was recorded as the
most common HPV genotype in Latin America, East Asia and
for Chinese women with cervical pathology [24]. The
prevalence of multiple infections reported in two studies that
were done on cervical smears and paraffin embedded tissue
blocks were found to be due to the high sensitivity of the
detection method used. One advantage of the probe based
assay is the possibility to easily discriminate heterogeneous
PCR groups, which cannot be differentiated by other
hybridization methods used for genotyping general PCR
products. This may indicate that the incidence of multiple
infections may be underestimated in many other studies.
However, the scheme with epidemiology of HPV and its
relation to cervical cancers in Sudan is not very clear. Recent
statistical data regarding cervical cancers epidemiology in
Sudan are unsettled. Cervical cancer is appraised to be second,
after breast cancer among Sudanese women, and a recent
survey from the National Health Laboratory in Sudan
illustrate that each year, around 833 Sudanese women are
analyzed with cervical cancer (estimated age standardized
incidence: 7.9 per 100,000 per year, supplementary, around
534 die from this disease [25]. Studies from Africa, Asia, and
South America revealed that the highest reported age
standardized incidence rate were found to be
17.9/100,000/year in Zimbabwe and the lowest is
0.11/100,000/year in China. The highest reported age
standardized mortality rate was found to be 16/100,000/year
in India in 2015, and the lowest: 1.8/100,000/year in Colombia
[26]. In comparison to the developed countries of Europe and
North America, where the age-standardized incidence of
cervical cancer is less than 9% [27], Sudan’s statistical data
reveals depressing indicators. This imbalance is attributed
primarily to the effective and successful implementation of
organized cervical cancer screening programs in developed
countries, which lead to early detection and appropriate
management of precancerous lesions [28].
5. Conclusion
Familiarity with the frequent high risk HPV genotypes
found in Sudan that have a high prevalence of cervical cancer
is essential in order to construct an applicable genotype of the
virus in the HPV vaccine. Presently, three prophylactic HPV
vaccines are commercially usable. Gardasil and Cervarix,
which is a bivalent vaccine accepted for the avoidance of
cervical cancer and precancerous lesions caused by HPV 16
and 18 in young females. Gardasil is a quadrivalent vaccine
anti-HPV types 6, 11, 16, and 18 [29], and the nine-valent
HPV vaccine developed recently to provide protection against
HPV types 6, 11, 16, and 18; and is already covered by the
Gardasil and the next five most common oncogenic types
associated with cervical cancer worldwide (types 31, 33, 45,
52, and 58) [30]. However, the current vaccines do not prevent
infection with the HPV types that are not contained in the
vaccine. Thus, the data of the present studies are crucial for the
confirmation of the most suitable vaccines in an area without
much information regarding the HPV disease, like Sudan.
From the review given here, it is clear that other HPV

98 Magdi Mansour Salih: Human Papillomavirus Types and Cervical Cancer Vaccine for Sudanese Women: A Review
genotypes like HPV 58 should be considered in Sudan. This
review provides useful information for future HPV
genotyping research and vaccinations for cervical cancer in
Sudan. But more importantly, this work reveals the substantial
need for further studies on cervical cancer and associated risk
factors in Sudan.
6. Limitations
Our study is limited to PubMed, Web of Science and
Google Scholar. Thus, it may not cover all the studies
conducted in this field; particularly those non-published data
or data published in non-indexed local journals, and open
access platforms not covered by Google Scholar, PubMed and
Scopus. Moreover, we did not assess the publication bias of
the articles, as it is not relevant in the context of cervical
cancer, HPV DNA or genotypes studies. It is possible that
there is considerable under reporting in HPV DNA,
genotyping or cervical cancer in our study, particularly since
the capacity for cancer diagnoses and data capture is limited in
Sudan.
Table 1. Studies on Cervical Human Papilloma Virus Genotypes Percentage and Detection Methods.
Study/ year Sample size Detection method used Types N (%)
(Salih et al., 2010) 135 Cervical smear PCR, There were 60.7% ß. globin
positive samples
HRHPV16 4/135 (2.9%) HRHPV58 4/135 (2.9%)
LRHPV40 2/135 (1.4%) LRHPV42 4/135 (2.9%)
(Elasbali et al., 2012
40 Cervical smear PCR HRHPV 16 8/16 (50%), HRHPV 18 6/16 (37.5%) Mixed 16,
18 2/16 (12.5%)
Mansour et al. 2013 400 Cervical smears PCR HR-HPV DNA 144/400 (36.0%)
Gafar et al., 2013 106 Cervical smears In Situ hybridization (ISH) techniques HR-HPV DNA 29/106 (27.3%)
Abate et al., 2013 86 paraffin embedded
PCR
98% (85/86) of sample were positive for
Housekeeping gene (b-globin)
Probable HR-HPV genotype.
HRHPV 16 66/80 (82.5%), HRHPV 18 16/80 (20.0%)
HRHPV 31 5/80 (6.2%) HRHPV 33 10/80 (12.5%) HRHPV
35 8/80 (10%) HRHPV 39 3/80 (3.7%)
HRHPV 45 14/80 (17.5%) HRHPV 52 2/80 (2.5%) HRHPV
53 5/80 (6.2%) HRHPV 58 12/80 (15%) HRHPV 59 1/80
(1.2%) HRHPV 68 8/80 (10%) HRHPV 39/68 2/80 (2.5%)
HRHPV 56/74 2/80 (2.5%) LRHPV 6 8/80 (10%) LRHPV
44 1/80 (1.2%) LRHPV 74 1/80 (1.2%)
(Eltahir, Elhassan
and Ibrahim, 2012 78 paraffin section PCR HRHPV16 33/78 (42. 3%). HRHPV18 40/78 (51.3%).
Type of specimen
Cervical smear HPV DNA 173/506 (34%) HRHPV16 69
(
8
.
16
%), HRHPV18 86 (
10
.
17
%), HRHPV58 4 (0.
47
%)
LRHPV40 2 (0.2
3
%) LRHPV42 4 (0.
47
%))
Cervical smear 681 (80.6%)
Paraffin section 164 (19.4%)
Total 845 (100%)
Abbreviation
HPV: Human papilloma virus. HR: High risks. LR: Low
risk. PCR: polymerase chain reaction. DNA:
Deoxyribonucleic acids. N: number.
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