Home | Volume 33 | Article number 252

Original article

The prevalence of syphilis in HIV-seropositive patients: a retrospective study at the regional hospital in Agadir, Morocco

The prevalence of syphilis in HIV-seropositive patients: a retrospective study at the regional hospital in Agadir, Morocco

Mohamed Bourouache1,&, Rachida Mimouni1, Mohamed Nejmeddine2, Smail Chadli3, Fatima Benlmeliani4, Jamila Sardi4, Mourad Malmoussi5, Zineb Ouagari5, Maryam El Basbassi4, Mohamed Aghrouch4


1Department of Biology, Faculty of Sciences, Ibn Zohr University, Agadir, Morocco, 2Infectious Diseases Group, Laboratory of Cell Biology and Molecular Genetics, Faculty of Sciences, Ibn Zohr University, Agadir, Morocco, 3Higher Institute for Nursing Professions and Health Techniques, Agadir, Morocco, 4Laboratory of Bio-Medical Analysis, Hassan II Regional Hospital, Agadir, Morocco, 5Department of Infectious Diseases, Hassan II Regional Hospital, Agadir, Morocco



&Corresponding author
Mohamed Bourouache, Department of Biology, Faculty of Sciences, Ibn Zohr University, Agadir, Morocco




Introduction: HIV and syphilis are major public health problems in Morocco. This southwestern part of Morocco accounted for 24% of the country's HIV registered cases in 2009. This study aims to evaluate the seroprevalence of syphilis among an HIV-positive population in the region of Souss-Massa.


Methods: to evaluate the seroprevalence of syphilis and neurosyphilis among HIV seropositive patients, we retrospectively investigated the medical records of HIV-infected patients attending the regional hospital located in the city of Agadir, during the period comprised between 2011 and 2016.


Results: a study population of 1381 males (49.18%) and 1427 females (50.82%) were found to be seropositive for HIV infection. Of these 2808 HIV seropositive patients, 481 were seropositive for syphilis and three cases were diagnosed with neurosyphilis. The sex ratio distribution was 243 male (52.71%) and 218 female (47.29%). The prevalence of syphilis among the studied population was estimated to 16.42% with a slight dominance in male (17.63%) compared to female (15.28%). By contrast, neurosyphilis was only detected in male patients, with a prevalence estimated at 0.11%.


Conclusion: although the prevalence of HIV and syphilis is stable in the Souss-Massa population, the prevalence of syphilis among HIV patients remained high and correlated positively with that of HIV infection. We did not find a significant difference between the genders in the prevalence of HIV and syphilis. We concluded that it was essential to continue monitoring the population, in order to improve the prevention and access to the medical care in the south-west of Morocco.



Introduction    Down

Syphilis is a sexually transmitted infection (STI), associated with the bacterium Treponema pallidum [1]. The vast majority of infections are sexually transmitted [2]. However, the infection might also be transmitted from an infected woman to her newborn child [3]. During pregnancy, the syphilis can lead to spontaneous abortion, congenital deformities, or severe neonatal disease [4-6]. This infection, which can cause long-term complications if not treated appropriately [7, 8], continues to be a major health concern in Morocco [9, 10]. The syphilis is a progressive disease, which could be classified according to the degree of severity; from primary stage, to the tertiary that leads to a disease of the central nervous system, called neurosyphilis [11]. Different signs and symptoms are associated with each stage [12]. The overall incidence of syphilis in the world have increased in recent years [13-15], partially due to its association with HIV infection [16]; Especially, in high-risk groups, including drug users (IDUs), female sex workers (FSWs) and men who have sex with men (MSM) [17-19]. The HIV is still a common causes of morbidity and mortality around the world, particularly in the developing countries [20, 21]. Interestingly, syphilis itself facilitates HIV infection in several ways and vice versa [22]. In 2009, an analysis of the medical records shows that 24.6% of all HIV cases registered in the country were from the region of Souss-Massa, in the south-west of Morocco [10]. Previous reports that evaluated the association between HIV and syphilis in Morocco focused mostly on some high risk groups; in particular, female sex workers and men who have sex with men [9, 23]. This led to an overestimation of the prevalence of syphilis in the general population of Souss-Massa. The aim of this study is to establish a more accurate assessment of the prevalence of syphilis in patients tested positive for HIV.



Methods Up    Down

Collecting data: the department of infectious disease of the regional hospital in Agadir covers all HIV patients from the whole region of Souss-Massa, Morocco. The medical records of HIV-infected patients, tested between 2011 and 2016, were examined for the presence of syphilis and neurosyphilis cases.


Screening for HIV: screening for HIV infection was performed according to the Moroccan Health Ministry recommendations (Figure 1). The diagnostic of HIV infection included a rapid test (Alere Determine®HIV-1/2, Alere Inc, Japan) white visual read; qualitative immunoassay for the detection of antibodies to HIV-1 and HIV-2; or the ELISA test (Murex®HIV Ag/Ab Combination, Dia-Sorin S.p.A, Saluggia, Italy). In addition, a confirmation test was performed using a Western blot test (MP Diagnostics (MPD) HIV BLOT 2.2, Japan). The interpretations of the tests were performed in accordance with the recommendations of the World Health Organization (WHO), based on the detection of two ENV bands, with or without GAG or POL bands.


Serological tests for the detection syphilis: the serological diagnosis of syphilis was based on a series of two types of serological tests. The first test was a non-treponemal antigen test (VDRL), used for the screening for syphilis in serum or cerebral spinal fluid. The Venereal Disease Research Laboratory test (VDRL; carbon antigen plasmatec laboratory products Ltd, Bridport, UK) allowed the detection of antibodies directed against non-treponemic antigens, called cardiolipins. The second test was a treponemal antigen test TPHA (treponema pallidum hemagglutination assay; immutrep® TPHA, Omega Diagnostics, UK). This test was based on an indirect hemagglutination assay for the detection and titration of antibodies against the causative agent of syphilis, treponema pallidum. The samples that were positive in both tests were then identified as seropositive for syphilis.


Statistical analysis: statistical analysis of data was performed using the R software, version 3.16. The results were summarized using descriptive statistics. The Welch two sample t-test was used to evaluate the differences between gender (male and female) for both HIV and syphilis prevalence. The Pearson´s correlation coefficient was used to assess the correlation between HIV and syphilis. The patients details obtained during the study were kept confidential.


Ethical considerations: as data were collected in patient's register, no informed consent was necessary. Patients informations obtained during the study were kept confidential. The study was approved by the Department of Infectious Disease of the Regional Hospital in Agadir.



Results Up    Down

A total of 2808 HIV seropositive patients were included in the present study. The calculated sex ratio was 0.97, for a gender distribution of 1381 males (49.18%) and 1427 females (50.82%). The average annual incidence of HIV infection between 2011 and 2016 was estimated to be about 468 ± 94.41 cases per year. The highest number of new cases was recorded in 2014, with 623 (22.19%) cases. By contrast, the lowest number of new cases was recorded in 2012 with 346 (12.32%) cases (Table 1). We did not detect a statistically significant difference between the male and female seropositive patients (p = 0.788). Among the 2808 HIV seropositive patients, 481 were tested positive for syphilis and 3 cases were diagnosed with neurosyphilis. Syphilis was therefore prevalent in 16.42% in this population, slightly more in males (17.63%) than in females (15.28%). However, this difference was not statistically significant (p = 0,492). The three cases of neurosyphilis detected were all males, placing the prevalence of neurosyphilis in the HIV seropositive patients around 0.11% (Table 2). Statistical analysis of the data showed a significant positive correlation between HIV and syphilis (r = 0.828; p = 0.042).



Discussion Up    Down

Souss Massa (SM) is home to 2,677 million inhabitants (according to the latest general population and housing census in 2014), many of whom live in Agadir the region's capital and largest city. The Infectiology Department of the Agadir Regional Hospital provides reception, medical care and drug distribution to almost all HIV and STIs patients in the region [24]. Like everywhere else in the world, in particular in Africa, the sexually transmitted infections (STIs) in Morocco constitute a public health burden. Around 400,000 new cases are registered through public health clinics every year, but the true burden is believed to be higher, as cases that are not symptomatic and not treated, or which are managed by private health providers or self-treated, are not reported [19]. We report on the seroprevalence of HIV, syphilis and neurosyphilis among the population in the region of Souss-Massa, than compared the results with previous data in the region of Souss-Massa as well as with recently reported data in other regions of Morocco. According to the Health Ministry Department, the region of Souss-Massa is the most affected regions by HIV/AIDS in Morocco. In 2009, this region recorded the highest prevalence of HIV/AIDS in the country (0.9%) [10]. Since then, few studies have been carried out in the area [9, 17, 21, 23-28]; most of them were especially focused on groups that carried a high-risk (female sex workers, men who have sex with men, drug users) [9, 17, 23]. These groups are the core drivers of the HIV epidemic in Morocco and elsewhere in the world, with heterosexual sex-worker networks being the largest of the three kinds of high-risk groups, followed by MSM, and then IDUs [10]. These studies might have overestimated the influence and the prevalence of HIV and STIs in the general population. The purpose of this study was to examine more accurately the prevalence of syphilis and neurosyphilis in HIV seropositive-patients of SM region for the last six years. New HIV infections were about 468 ± 94.4 cases per year. This incidence was higher than those previously reported in 2012 [17]. The highest number of new HIV cases was recorded in 2014 (Table 1). This might be due to the higher number of screening campaigns that took place in the country in recent years. Also, the higher awareness about the disease within the population probably resulted in the decline of stigma towards HIV carriers and some high-risk groups such as MSM and FSWS. In accordance with recent reports [17, 20, 25], the statistical analysis did not show a significant difference in prevalence between male and female populations (p = 0.224). This is contrast to previous studies in Morocco, as well as in most Arab countries, that often showed a gender dominance [10, 17, 21, 25].


We noted a stable incidence of new syphilis cases, despite the peak incidence in 2014. The prevalence of syphilis between 2011 and 2016 was estimated at 17.13% and did not appear to be affected by the genders (Table 3). This result is comparable to that found by Johnson et al 2013 [9]. By contrast, Bennani et al. 2017, reported a decline in the incidence and prevalence of active syphilis between 1995-2016 in Morocco [19]. In developing countries, prisons played an important role in HIV and STIs epidemics [29-31]. Prisoners represented a special high-risk group, due to high rates of injected drug users, unprotected sex and the use of non-sterile equipment for tattooing or for shaving [19, 32, 33]. Heijnen et al 2016, estimated 496,000 prisoners in MENA, with drug-related offences being a major cause for incarceration [33]. In Morocco, the prevalence of HIV among prisoners is between 0.4% to 0.8%, with higher prevalence in the regions of Souss-Massa-Draa and Marrakech Tensift Al Haouz [32]. But not enough data is available about prisoners in the Souss-Massa region [10, 32], which makes it difficult to assess the contribution of this group in HIV and STIs transmission. The rate of co-infection (Syphilis and HIV) is increasing in North Africa [34-36]; especially, in the group of MSM [37]. A recent report showed that co-infection with HIV and syphilis was estimated to 31.6% in Agadir and 56.4% in Marrakesh [9]. It is well known that the syphilis chancre creates an integument discontinuity, which facilitates the penetration of HIV into the organism [38]. The presence of the virus in the syphilitic ulcers was previously reported [39]. The immunodeficiency state induced by HIV infection [40] can also influence the clinical features and treatment outcome of the syphilis [41]. This was confirmed by the high positive correlation between HIV and syphilis in the MS population (r = 0.828 ; p = 0.042). All neurosyphilis cases (3 cases) were found in males during the year of 2015. The prevalence of neurosyphilis was estimated at 0.11%. This result was in agreement with those reported in 2016 by Fekih et al. [42]. The male correlation was probably due to the high frequency of chronic meningo encephalitis observed in men, which was 4-7 times more common in males than in females [43]. The men who have sex with men (MSM) showed the most exposure to syphilis [2, 14, 44]. Almost 90% of the Moroccan population that engages in intermediate-to-high-risk life style were males [10]. Indeed, 71% of all HIV infections among women are due to an infected spouse [26]. There was no significant difference between male and female groups, for HIV and syphilis prevalence (Table 3). This is probably due to the low rate of MSM in Agadir compared to Marrakech, and to the increased awareness of the general population about sexually transmitted infections (STI) and AIDS.



Conclusion Up    Down

Both HIV and syphilis infections reached alarming rates in the region of Souss-Massa in the south-west of Morocco. Despite the peak recorded in 2014, the prevalence of HIV appears to be stable. However, the prevalence of syphilis among HIV patients remained high, and following the same trend as HIV. In order to prevent or to anticipate any further change in the current situation, In order to prevent or to anticipate any further change in the current situation, it is important to keep a permanent scrutiny of the prevalence and incidence in the region of Souss-Massa. This will be essential to provide a better care and to put in place adapted strategies of prevention in Morocco, especially among the most vulnerable in the general population.

What is known about this topic

  • Since 2009, high HIV and syphilis prevalence was reported in the region of Souss-Massa, in Morocco;
  • HIV, STIs testing and counseling is a key strategy to reduce sexual risk-taking and control the burden of HIV infection;
  • In the region of Souss-Massa, MSM, FSW and prisoners constituted the main high-risk group carriers of HIV, syphilis and several sexually transmitted infections.

What this study adds

  • The prevalence of syphilis among HIV-infected patients were stable, over the years but remains very high;
  • There was a significant correlation between the prevalence of HIV and syphilis infections in the Souss-Massa population;
  • Significant efforts will be needed to reduce the prevalence of syphilis and HIV in this region.



Competing interests Up    Down

The authors declare no competing interests.



Authors’ contributions Up    Down

Mohamed Aghrouch and Mohamed Nejmeddine conceived of the study and participated in its design and coordination. Mourad Malmoussi, Zineb Ouagar and Maryam El Basbassi were involved in the data collection. Fatima Benlmeliani, Jamila Sardi contributed in interpretation of data. Mohamed Bourouache drafted the manuscript. Rachida Mimouni, Smail Chadli reviewed and finalized the version to be published. All authors read and approved the final manuscript.



Acknowledgments Up    Down

We are grateful to all who participated in this research.



Tables and figure Up    Down

Table 1: seroprevalence of HIV infection in Souss-Massa between 2011 and 2016

Table 2: seroprevalence of syphilis in the HIV seropositive patients between 2011 and 2016

Table 3: summary of the Welch two sample t-test

Figure 1: recommended laboratory HIV testing algorithm for serum or plasma specimens



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