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

Introduction HIV and syphilis are major public health problems in Morocco. The region of Souss-Massa, south-west of the country, hold more than 24% of HIV seropositive cases registered in Morocco during 2009. The aim of this study is to evaluate the seroprevalence of syphilis among HIV seropositive patients in the region of Souss-Massa, south-west of Morocco. 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 The population studied involved 1381 males (49.18%) and 1427 females (50.82%) HIV seropositive patients. Among them, 481 patients 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 to 0.11%. Conclusion Even if the prevalence of HIV and syphilis is stable in the region of Souss-Massa, the prevalence of syphilis among HIV seropositive patients remained high and correlated positively with that of HIV infection. We did not find a significant difference between the genders, in relation to the prevalence of HIV and syphilis. We concluded that it was essential to continue monitoring the population, in order to improve the prevention and the access to the medical care in the south-west of Morocco.


Introduction
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][5][6]. This infection, might 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 a tertiary stage that leads to a disease of the central nervous system, called neurosyphilis [11]. Each stage of the disease is associated with particular symptoms [12]. The overall incidence of syphilis in the world have increased in recent years [13][14][15], partially due to its association with HIV infection [16]; in particular high-risk groups of the population, including drug users (IDUs), female sex workers (FSWs) and men who have sex with men (MSM) [17][18][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 showed that 24.6% of all HIV seropositive 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
Collecting data: the department of infectious disease of the regional Statistical analysis: the statistical analysis of the 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 infection and syphilis.
Ethical considerations: the data were collected in the hospital register, and the information obtained were kept confidential. The study was approved by the Department of Infectious Disease of the Regional Hospital in Agadir.

Results
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 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
The This incidence was higher than those previously reported in 2012 [17].
The highest number of new HIV cases was recorded in 2014 (Table 1) We noted a stable incidence of new cases of syphilis, 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), consistently with previous report carried out in Agadir and Marrakesh within groups of men who have sex with men [9]. By contrast, it was reported that the prevalence and incidence of active syphilis among women in Morocco was in decline between 1995-2016 [19]. In developing countries, prisons played an important role in HIV and STIs epidemics [29][30][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][35][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). The entire of the neurosyphilis cases (3 cases, registered during the year of 2015) were males. The prevalence of neurosyphilis was estimated to 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-tohigh-risk life style were males [10]. Indeed, 71% of all HIV infections among women were due to an infected spouse [26]. There was no significant difference between male and female groups, for HIV and syphilis prevalence (Table 3). This was probably due to the low rate

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
The authors declare no competing interests.

Acknowledgments
We are grateful to all who participated in this research.