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African Journal of Parasitology, Mycology and Entomology

(ISSN: 1987-1473) Open Access Journal
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Afr. J. Parasitol. Mycol. Entomol. , 2(1), 5; doi:10.35995/ajpme2010003

 
Trichomonas vaginalis and Mycoplasma co-infection among women received in a microbiology laboratory in Dakar
Mame C. Seck PharmD PhD 1,2,*, Papa A.T. Gueye PharmD 2, Cheikh Faye PharmD 2, Pasca E. Engo PharmD 2, Khadim Diongue PharmD PhD 1, Mouhamadou Ndiaye PharmD PhD 1, Aida S. Badiane PharmD PhD 1 and Daouda Ndiaye PharmD PhD 1
1
Service of Parasitology-Mycology, Faculty of Medicine, Pharmacy and Odontology, Cheikh Anta Diop University, BO 3005, Dakar, Senegal
2
Laboratory of Microbiology – Military Hospital of Ouakam, BO 28216, Dakar, Senegal
*
Corresponding author: mamecheikh.seck@ucad.edu.sn; Tel.: 00 221 77 44 03 600
How to Cite: Seck, M.C.; Gueye, P.A.T.; Faye, C.; Engo, P.E.; Diongue, K.; Ndiaye, M.; Badiane, A.S.; Ndiaye, D. Trichomonas vaginalis and Mycoplasma co-infection among women received in a microbiology laboratory in Dakar. Afr. J. Parasitol. Mycol. Entomol., 2024, 2(1): 5; doi:10.35995/ajpme2010005.
Received: 22 September 2023 / Accepted: 15 December 2023 / Published: 16 May 2024

Abstract

:
Introduction: Trichomonas vaginalis and Mycoplasma are common causes of sexually transmitted infections, but limited prevalence data are available in Senegal. This study aimed to determine the prevalence of T. vaginalis and genital mycoplasma infection among women in Dakar. Materials and Methods: A retrospective study was carried out between 2016 and 2021 among women referred to the microbiology laboratory of the Military Hospital of Ouakam for vaginal discharge. Mycoplasma was detected by a commercial Mycoplasma EIS Kit using the endocervical swab. A wet mount smear and Gram staining were performed to detect T. vaginalis. Results: We analyzed a group of 1889 women, ranging in age from 14 to 81, with a mean age of 32.5 years (+/− 8.3 years). Our findings showed that 18.5% (95% CI (16–20)) of the women were infected with Mycoplasma hominis, while 50.5% (95% CI (48–53)) had Ureaplasma urealyticum. Trichomonas vaginitis was found in 3.5% (95% CI (2.7–4.5)) of the women. Out of the 66 patients with trichomoniasis, 68.2% were also infected with Mycoplasma hominis and 36.4% with U. urealyticum. We also observed that 88% of the women with M. homininis infection had U. urealyticum. Conclusion: Our study revealed a significant co-infection rate between Trichomonas vaginalis and Mycoplasma. This highlights the need for systematic mycoplasma screening in patients with urogenital trichomoniasis.
Keywords:
Trichomonas vaginalis; Mycoplasma hominis; Ureaplasma urealitycum; women; Dakar

1. Introduction

Vulvovaginal symptoms are among the most common reasons for women attending a health facility. The symptoms of vaginal discharge that a woman may perceive as abnormal include vulval irritation and itching. More than 30 bacteria, viruses, and parasites are known to be sexually transmitted. The most frequently identified include Chlamydia trachomatis, Neisseria gonorrhoeae, Treponema pallidum, and Trichomonas vaginalis, with over 350 million infections yearly worldwide [1]. Urogenital trichomoniasis is the only parasitic STI recognized as the most common non-viral STI globally, with 250 million new cases annually [2]. The infection is usually asymptomatic in men, although it may be associated with urethral discharge or dysuria. However, clinical manifestations in women are more frequent, with various symptoms such as greenish-yellow leucorrhea, dysuria, and vaginal mucosa with hemorrhagic staining [3]. In addition, T. vaginalis infection can cause complications in pregnant women, such as the premature rupture of membranes, premature delivery with low birth weight, infertility, or cervical cancer [4]. The transmission of T. vaginalis is extremely heterogeneous and depends on several factors, including socioeconomic status, age, hygiene habits, sexual behavior, post-menstrual phase, and access to health care. In addition, association with other infectious agents of the urogenital tract, such as mycoplasma, is often reported [5,6]. Mycoplasmas (M. hominis and Ureaplasma spp.) are commensals of the lower urogenital tract. Colonization varies with age, race, socioeconomic status, sexual activity, and hormonal status, and increases during pregnancy [7]. Ureaplasma spp. can be found vaginally in 30% of women, while M. hominis is found in less than 10% and these infections can cause cervicitis, infertility, premature delivery, or spontaneous abortion in pregnant women [8]. These consequences justify preventing these infections, especially in women of childbearing age. In addition, studies have suggested a symbiotic relationship between T. vaginalis and Mycoplasma hominis, but the potential synergy between these two pathogens has yet to be evaluated under clinical conditions [9]. In Senegal, most patients with signs suggestive of STIs (urethral discharge and vaginal discharge syndromes) are often diagnosed presumptively using a syndromic approach. However, this approach may lack sensitivity and specificity in some settings and lead to the mismanagement of several conditions, including urogenital trichomoniasis and Mycoplasma infections [10]. In addition, biological confirmation of these infections remains poor in many health facilities due to a lack of appropriate laboratories [11]. This results in a lack of available data on the epidemiology of Mycoplasma spp. and T. vaginalis co-infection, particularly in at-risk populations such as women of childbearing age. In this context, we conducted this study at the Ouakam Military Hospital. The aim was to determine the characteristics of T. vaginalis and mycoplasma (M. hominis and U. urealyticum) co-infection among women referred to the microbiology laboratory.

2. Material and Methods

2.1. Study design

Over a period of six years, from January 2016 to December 2021, a retrospective descriptive study was carried out. The study included all women referred to the microbiology laboratory of the military hospital of Ouakam for vaginal discharge and a search for genital mycoplasma.
From each participant, two vaginal swabs were collected as the routine diagnostic procedure. To assess the prevalence of T. vaginalis infection, a wet mount smear was performed immediately as part of a routine diagnostic procedure for a motile parasite. The wet mount smear was examined using an optical microscope at ×40 to detect T. vaginalis and assess biological modifications such as the presence of epithelial cells, white blood cells, and red blood cells. T. vaginalis infection was considered based on a positive result from wet mount microscopy of motile trichomonad. The magnitude of white cells within the vaginal discharge was classified as follows: (i) rare: 1–5 cells/high-power field; (ii) moderate: 6–10 cells/high-power field; (iii) many: 11–20 cells/high-power field; and (iv) high: 21 cells and above/high-power field, as described elsewhere [8]. In addition, a Gram-stained smear was performed to characterize the vaginal flora using Nugent scoring [12]. Mycoplasma testing was performed using the Mycoplasma IES kit (Autobio Diagnostics Co., Ltd.; Zhengzhou-China) for urogenital mycoplasma according to the manufacturer's recommendations. The Mycoplasma kit is based on the reaction of cultivation and biochemistry. Urea can be decomposed by Urease for U.urealyticum and release NH3; arginine can be decomposed by arginase for M. hominis and release NH3. Then, NH3 causes an increased pH of the liquid medium. The corresponding color change of the indicator is used to judge the result. The separated cultivation, identification, and enumeration of U. urealyticum and M. hominis are completed simultaneously.

2.2. Statistical analysis

Statistical analyses were performed using R software (R- 4.3.2). Continuous variables were described as mean with standard deviation. Normally distributed variables were compared with a t-test. Categorical variables were presented as percent, and Fisher exact or chi-squared tests were used for proportional assessments. Univariate logistic regression analysis assessed the association between the related risk factors and positivity. Five age groups (years) were defined for analysis, i.e., <20, 20 to 30, 31 to 40, 41 to 50, and over 50. We accepted that a two-sided significance level was set at p ≤ 0.05 for all statistical tests.

3. Results

3.1. Characteristics of the study population and distribution of Trichomonas vaginalis infection

Over the course of the study period, 1889 patients were referred to the laboratory for vaginal discharge and genital mycoplasma testing. The mean age was 32.5 years ± 8.3. Within the study period, 2020 recorded the highest number of patients, at 18.5% (n = 355), while the lowest was noted in 2016, at 12.4% (n = 235). Out of all age groups, the 20–30-year-olds were the most frequent, accounting for 41.7% (n = 788). Vaginal flora type III was the most common, accounting for 44.8% (n = 847), followed by types IV and II with 35.5% and 19.4%, respectively. The number of white blood cells per high-power field was at the rare level, at 82% (Table 1). Out of 1889 patients, the prevalence of Trichomonas vaginalis infection was 3.5% (95% CI [2.7–4.5]). The highest frequency of infection was noted in 2016 at 4.7% and the lowest in 2021 at 2%. The difference was not statistically significant (p = 0.5). The frequency of T. vaginalis infection was highest in the 41-to-50-year-old age group, at 5.3%, while those over 50 years of age were the least affected, with a frequency of 2.4%. The difference was not statistically significant (p = 0.4). T. vaginalis infection was statistically associated with moderate WBC levels (p < 0.001) and with vaginal flora types III and IV (p = 0.048). The other characteristics of the distribution of T. vaginalis infection are detailed in Table 1.
Table
Table 1. Characteristics of the study population and Trichomonas vaginalis infection distribution.
Table 1. Characteristics of the study population and Trichomonas vaginalis infection distribution.
Characteristics of the Study Population Trichomonas vaginalis infection, N = 66Overall,
N = 1889
% [CI 95%]% [CI 95%]p-Value 1
Study period
201612 [11–14]4.7 [2.5–8.4]0.5235 (100%)
201717 [16–19]4.0 [2.2–6.8]329 (100%)
201815 [14–17]2.8 [1.3–5.6]289 (100%)
201918 [16–19]3.9 [2.2–6.8]331 (100%)
202019 [17–21]3.9 [2.3–6.7]355 (100%)
202119 [17–21]2.0 [0.88–4.3]350 (100%)
Age group (years)
< 204.8 [3.9–5.9]4.4 [1.4–11]0.491 (100%)
20–3042 [39–44]3.2 [2.1–4.7]788 (100%)
31–4036 [34–39]3.1 [2.0–4.7]687 (100%)
41–5015 [13–17]5.3 [3.1–8.8]281 (100%)
> 502.2 [1.6–3.0]2.4 [0.12–14]42 (100%)
Vaginal flora type
I0.3 [0.10–0.65]20.0 [1.1–70]0.0485 (100%)
II19 [18–21]1.9 [0.84–4.1]367 (100%)
III45 [43–47]3.4 [2.3–4.9]847 (100%)
IV35 [33–38]4.3 [3.0–6.2]670 (100%)
White blood cells/high power field
Rare82 [80–84]2.3 [1.7–3.2]<0.0011548 (100%)
Moderate17 [15–19]8.4 [5.7–12]320 (100%)
Many1.1 [0.71–1.7]14.3 [3.8–37]21 (100%)
1 Pearson’s chi-squared test; Fisher’s exact test.

3.2. Distribution of Ureaplasma urealyticum and Mycoplasma hominis infections

The overall prevalence of U. urealyticum was 50.5% (95% CI [48–53]). Within the study period, the frequency was the highest in 2018, at 55.9% (n = 171), and the lowest in 2016, at 33.2% (n = 78). The difference was statistically significant (p < 0.001). According to age group, patients aged between 21 and 30 were more affected, at 52.4%, followed by those under 20 and the 31–40 age group, at 51.6% and 49.2%, respectively. The difference was not statistically significant (p = 0.6). U. urealyticum prevalence was mainly associated with moderate WBC levels at 56.9% (p = 0.04), and vaginal flora types III and IV at 58.7% and 50.1%, respectively (p < 0.001). The prevalence of M. hominis infection was 18.2% (95% CI [16–20]). During the study period, the highest rate was observed in 2018, at 29.4% (n = 85), while 2019 had the lowest frequency at 13.6%. The difference was statistically significant (p < 0.001). Patients under 20 were the most affected, at 23.1%, while those over 41 were the least affected. This difference was not statistically significant (p = 0.7). M. hominis infection was mainly associated with many WBC levels at 28.6% (p = 0.02), and flora vaginal type IV in 25.8% (p < 0.001). Other characteristics of M. hominis and U. urealyticum infections are presented in Table 2.
Table
Table 2. Distribution of Ureaplasma urealyticum and Mycoplasma hominis infections.
Table 2. Distribution of Ureaplasma urealyticum and Mycoplasma hominis infections.
Overall,
N = 1889		Ureaplasma urealyticum,
Positive = 954		Mycoplasma hominis,
Positive = 343
% [95% CI]p-Value 1% [95% CI]p-Value 1
Study period
201623533.2 [27–40]<0.00115.7 [11–21]<0.001
201732947.7 [42–53]17.3% [13–22]
201828959.2 [53–65]29.4 [24–35]
201933155.9 [50–61]13.6 [10–18]
202035551.3 [46–57]19.7 [16–24]
202135051.7 [46–57]14.0 [11–18]
Age group (years)
<209151.6 [41–62]0.623.1 [15–33]0.7
20–3078852.4 [49–56]18.3 [16–21]
31–4068749.2 [45–53]18.0 [15–21]
41–5028148.8 [43–55]16.7 [13–22]
>504245.2 [30–61]16.7 [7.5–32]
Vaginal flora type
I540.0 [7.3–83]<0.0010.0 [0.00 – 54]<0.001
II36736.8 [32–42] 6.5 [4.3–9.7]
III84750.1 [47–53] 17.2 [13–23]
IV67058.7 [55–62] 25.8 [23–29]
White blood cells/high power field
Rare154849.2 [47–52]0.04317.1 [15–19]0.022
Moderate32056.9 [51–62]22.8 [18–28]
Many2147.6 [26–70]28.6 [12–52]
1 Pearson’s Chi-squared test, Fisher’s exact test.

3.3. Co-infection T. vaginalis and Mycoplasma

Among the 66 patients infected with T. vaginalis, co-infection with U. urealyticum and M. hominis was noted in 36.4% (n = 24) and 68.2% (n = 45), respectively. The difference was statistically significant (p < 0.001).

3.4. Co-infection between U. urealyticum and M. hominis

Of the 343 patients infected with M. hominis infection, 302 presented U. urealyticum infection simultaneously, resulting in an 88% co-infection rate. This difference was statistically significant (0.003).

4. Discussion

Our goal was to evaluate Mycoplasma spp. and Trichomonas vaginalis infections in women in Dakar. Patients aged 20–30 were the most represented, followed by those aged 31–40. One possible explanation is that hospital-based investigation of women presenting with STI clinical signs are likely to detect genital infections in women who are sexually active and of childbearing age.
Trichomoniasis, caused by T. vaginalis, is a widely prevalent sexually transmitted infection (STI) worldwide. However, its prevalence varies significantly in different countries [2,13]. Limited data are available in Senegal regarding the epidemiological profile of T. vaginalis infections. Our study found an overall frequency of 3.5%, consistent with previous research conducted in Dakar by Tine, who reported a frequency rate of 3.07% [14]. In addition, patients aged between 41 and 50 had the highest percentage of impact at 5.3%, though the difference was not statistically significant. In contrast, Tine et al.'s study showed that women under 25 were the most affected [14]. Reports from Egypt, Iran, and the USA indicate that urogenital trichomoniasis is prevalent among women aged 25 to 45 [15,16,17]. Urogenital trichomoniasis is more prevalent in sexually active age groups, which includes this age group, making them more exposed and more susceptible to infection [8,18]. Our study found a lower incidence of T. vaginalis infection than that reported in other countries. For instance, a prevalence of 9.5% was recorded in Zimbabwe [19]. Additionally, in many cities in Nigeria, frequencies of 18.66%, 24.1%, and 10.99% were reported in Zaria, Zos, and Maiduguri, respectively [20,21,22]. Differences in disease exposure or diagnostic methods could cause differences in frequency. In our study, only fresh direct examination and Gram-staining techniques were used, while it has been found that combining direct examination with culture is more effective for diagnosing urogenital trichomoniasis [23]. Previous studies have shown a strong link between urogenital trichomoniasis and low education, smoking, and sexual behavior [8,24]. However, our research did not collect any data on these variables.
T. vaginalis infection can cause non-specific biological changes, including significant inflammatory and cytolytic actions induced by the parasites. The severity of these pathogenic actions varies depending on the host and the strains of T. vaginalis [25,26]. Our research found that T. vaginalis infection caused a notable alteration in the vaginal flora, specifically of types III and IV. These findings align with previous longitudinal studies that indicate a higher likelihood of acquiring T. vaginalis in individuals with bacterial vaginosis [27,28].
According to our research, 50.5% of symptomatic patients had U. urealyticum, and 18.2% had M. hominis. The prevalence of most genital mycoplasma remained stable throughout the study. We could not compare our findings to previous studies on the trend of genital mycoplasma prevalence in symptomatic patients in Senegal during this period. Previously in Dakar, Tine et al. reported in their research, conducted at the Centre Hospitalier National et Universitaire de Fann, a similar prevalence of 54.9% for U. urealyticum. In comparison, the frequency of M. hominis infections was much higher at 57.4% [14]. Furthermore, according to several studies conducted in South Korea, the prevalence of U. urealyticum in symptomatic patients was higher than that of M. hominis. According to Moon et al., the prevalence of U. urealyticum and M. hominis was 21.3% and 2.9%, respectively [29], whereas it was 65.6% and 11.8% according to Kweon et al. [30], and 48.8% and 25.3% according to Jang et al. [31]. Similar values have been reported in Poland [32] and China [33]. The prevalence rates of M. hominis infection of 48%, 42.8%, 80%, and 70% have been reported in Cameroon, Korea, South Africa, and Papua New Guinea, respectively [34,35,36,37].
Our research indicates that M. hominis and U. urealyticum infections are more frequent in women under 40 years. However, the differences between age groups were not significant enough to draw a statistical conclusion. Tine et al. found a similar trend in their study, with the highest prevalence of STIs in patients under 45 [14]. One possible reason is that people within this age range tend to be sexually active and in their reproductive years, which may increase their susceptibility to such infections [8,18]. Furthermore, Mycoplasma caused significant biological changes, such as increased white blood cells observed on fresh examination. In addition, a significant association of these infections with type III or IV vaginal flora was noted. Indeed, Mycoplasma infections of the female urogenital tract are commonly associated with bacterial vaginosis [38,39], pelvic inflammatory disease, and cervicitis, which may result in increased white blood cell secretion [40].
As a dynamic environment, the female urogenital tract presents with a resident microflora of various species. The coexistence of other sexually transmitted microorganisms is quite common. It is due to several factors, such as a common route of transmission, the sexual behavior of the host, and the resident flora [41]. However, little attention has been paid to the presence of vaginal co-infections and their clinical and diagnostic implications. A symbiotic association between T. vaginalis and M. hominis, two microorganisms infecting the vaginal tract, has been demonstrated [37,42].
In our research, out of the 66 patients who had T. vaginalis infection, 45 patients had a co-infection with M. hominis, which is 68.2%. Additionally, it was observed that 88% of the cases had an association with U. urealyticum. The symbiotic relationship between T. vaginalis and Mycoplasma has been described in several studies [9,42]. It has been established that T. vaginalis can act as a niche and vector for transmitting M. hominis [43]. In addition, Mycoplasmas harbored by T. vaginalis have the privilege of evading the host immune response and enhancing the virulence of T. vaginalis [44]. This clinically significant symbiosis between these two obligate human microorganisms suggests that the routine screening of patients with T. vaginalis infection for mycoplasma is a better approach to optimize STI treatment practices [45]. In many cases, co-infection with Trichomonas and Mycoplasma may reduce susceptibility to antimicrobial agents, complicating the infection's eradication [37,43].
While this study provided relevant evidence on the association between T. vaginalis and mycoplasma, it has some limitations.
Firstly, laboratory tests included antimicrobial susceptibility testing; no follow-up assessment was performed after treatment. Further investigations would provide a better understanding of the effect of co-infection on treatment response in routine practice [46,47]. Secondly, the detection of T. vaginalis was based on fresh microscopic examination and staining as part of standard routine practice, and no additional investigations such as culture or PCR were performed. This may have led to an underestimation of its prevalence, as it is well established that culture in combination with direct microscopy is more sensitive to detection [48].

5. Conclusions

This study reveals that a higher percentage of the population was infected with U. urealyticum, while less than a quarter was infected with M. hominis. While the prevalence of T. vaginalis infection was low, an important co-infection with Mycoplasma spp. was observed. This emphasizes the importance of screening for mycoplasma in patients with urogenital trichomoniasis.

Author contributions

Conception, design of the study, and drafting of the article: M.C.S. Data collection: M.C.S.; P.A.T.G.; C.F. Data analysis: M.C.S.; P.E.E. Reviewing the article: K.D.; M.N.; A.S.B.; D.N. Final approval of the version to be submitted: All authors.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Ethical Statement

This study was a hospital-based research conducted in normal conditions under the Declaration of Helsinki. Ethical permission was obtained from the hospital authorities. Information collected during the study was analyzed using the participant's identification code to ensure confidentiality.

Data Availability

The datasets used and analyzed during the current study are available from the corresponding author upon reasonable request.

Acknowledgments

The authors would like to thank the participants in this study and all personnel of the microbiology unit of the military hospital of Ouakam Laboratory.

Conflicts of Interest

The authors declare that they have no competing interests.

References

  1. World Health Organization. Vaginal discharge syndrome. In Guidelines for the Management of Symptomatic Sexually Transmitted Infections; World Health Organization: Geneva, Switzerland, 2021; https://www.ncbi.nlm.nih.gov/books/NBK572663/.
  2. Menezes, C.B.; Frasson, A.P.; Tasca, T. Trichomoniasis—Are we giving the deserved attention to the most common non-viral sexually transmitted disease worldwide? Microb. Cell 2016, 3, 404–419. [Google Scholar] [CrossRef] [PubMed]
  3. Lis, R.; Rowhani-Rahbar, A.; Manhart, L.E. Mycoplasma genitalium infection and female reproductive tract disease: A meta-analysis. Clin. Infect. Dis. 2015, 61, 418–426. [Google Scholar] [CrossRef] [PubMed]
  4. Mabaso, N.; Abbai, N.S. A review on Trichomonas vaginalis infections in women from Africa. S. Afr. J. Infect. Dis. 2021, 36, 254. [Google Scholar] [CrossRef] [PubMed]
  5. Fichorova, R.N. Impact of T. Vaginalis Infection on Innate Immune Responses and Reproductive Outcome. J. Reprod. Immunol. 2009, 83, 185–189. [Google Scholar] [CrossRef] [PubMed]
  6. van der Colf, B.E.; Noden, B.H.; Wilkinson, R.; Chipare, I. Low seroprevalence of antibodies to Toxoplasma gondii in blood donors in central Namibia. S. Afr. J. Infect. Dis. 2014, 29, 101–104. [Google Scholar] [CrossRef]
  7. Matasariu, D.R.; Ursache, A.; Agache, A.; Mandici, C.E.; Boiculese, V.L.; Bujor, I.E.; Rudisteanu, D.; Dumitrascu, I.; Schaas, C.M. Genital infection with Ureaplasma urealyticum and its effect on pregnancy. Exp. Ther. Med. 2022, 23, 1–7. [Google Scholar] [CrossRef] [PubMed]
  8. Grama, D.F.; da Casarotti, L.S.; de Morato, M.G.V.A.; Silva, L.S.; Mendonça, D.F.; Limongi, J.E.; da Viana, J.C.; Cury, M.C. Prevalence of Trichomonas vaginalis and risk factors in women treated at public health units in Brazil: A transversal study. Trans. R. Soc. Trop. Med. Hyg. 2013, 107, 584–591. [Google Scholar] [CrossRef]
  9. Fiori, P.L.; Diaz, N.; Cocco, A.R.; Rappelli, P.; Dessì, D. Association of Trichomonas vaginalis with its symbiont Mycoplasma hominis synergistically upregulates the in vitro proinflammatory response of human monocytes. Sex. Transm. Infect. 2013, 89, 449–454. [Google Scholar] [CrossRef]
  10. Barry, M.S.; Ba Diallo, A.; Diadhiou, M.; Mall, I.; Gassama, O.; Ndiaye Guèye, M.D.; Covi-Alavo, S.; Gawa, E.; Ndao Fall, A.; Gaye Diallo, A.; et al. Accuracy of syndromic management in targeting vaginal and cervical infections among symptomatic women of reproductive age attending primary care clinics in Dakar, Senegal. Trop. Med. Int. Health 2018, 23, 541–548. [Google Scholar] [CrossRef] [PubMed]
  11. Vuylsteke, B. Current status of syndromic management of sexually transmitted infections in developing countries. Sex. Transm. Infect. 2004, 80, 333–334. [Google Scholar] [CrossRef]
  12. Nugent, R.P.; Krohn, M.A.; Hillier, S.L. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J. Clin. Microbiol. 1991, 29, 297–301. [Google Scholar] [CrossRef]
  13. Kissinger, P. Epidemiology and treatment of trichomoniasis. Curr. Infect. Dis. Rep. 2015, 17, 484. [Google Scholar] [CrossRef] [PubMed]
  14. Tine, R.C.; Dia, L.; Sylla, K.; Sow, D.; Lelo, S.; Ndour, C.T. Trichomonas vaginalis and Mycoplasma infections among women with vaginal discharge at Fann teaching hospital in Senegal. Trop. Parasitol. 2019, 9, 45–53. [Google Scholar] [CrossRef]
  15. Mahmoud, A.; Sherif, N.A.; Abdella, R.; El-Genedy, A.R.; El Kateb, A.Y.; Askalani, A.N. Prevalence of Trichomonas vaginalis infection among Egyptian women using culture and Latex agglutination: Cross-sectional study. BMC Womens Health 2015, 15, 7. [Google Scholar] [CrossRef]
  16. Azambakhtiar, A.; Nikmanesh, B.; Rezaeian, M.; Dashti, N.; Safari, F.; Zarebavani, M. The Prevalence of Trichomoniasis in Women Referred to Clinical Centers in South of Tehran, Iran during 2015–2016. Iran J. Parasitol. 2018, 13, 108–113. [Google Scholar] [PubMed]
  17. Sutton, M.; Sternberg, M.; Koumans, E.H.; McQuillan, G.; Berman, S.; Markowitz, L. The prevalence of Trichomonas vaginalis infection among reproductive-age women in the United States, 2001–2004. Clin. Infect. Dis. 2007, 45, 1319–1326. [Google Scholar] [CrossRef] [PubMed]
  18. Madhivanan, P.; Bartman, M.T.; Pasutti, L.; Krupp, K.; Arun, A.; Reingold, A.L.; Klausner, J.D. Prevalence of Trichomonas vaginalis infection among young reproductive age women in India: Implications for treatment and prevention. Sex. Health 2009, 6, 339–344. [Google Scholar] [CrossRef]
  19. Gregson, S.; Mason, P.R.; Garnett, G.P.; Zhuwau, T.; Nyamukapa, C.A.; Anderson, R.M.; Chandiwana, S.K. A rural HIV epidemic in Zimbabwe? Findings from a population-based survey. Int. J. STD AIDS 2001, 12, 189–196. [Google Scholar] [CrossRef]
  20. Jatau, E.D.; Olonitola, O.S.; Olayinka, A.T. Prevalence of Trichomonas Infection among Women Attending Antenatal Clinics in Zaria, Nigeria. Ann. Afr. Med. 2006, 5, 178–181. [Google Scholar]
  21. Mairiga, A.G.; Balla, H.J.; Ahmad, M.I. Prevalence of trichomonas vaginalis infections among antenatal clients in maiduguri Nigeria. Int. J. Biol. Med. Res. 2011, 2, 998–1002. [Google Scholar]
  22. Opara, K.N.; Udoidung, N.I.; Ukpong, I.G. Genitourinary schistosomiasis among pre-primary schoolchildren in a rural community within the Cross River Basin, Nigeria. J. Helminthol. 2007, 81, 393–397. [Google Scholar] [CrossRef] [PubMed]
  23. Fouts, A.C.; Kraus, S.J. Trichomonas vaginalis: Reevaluation of its clinical presentation and laboratory diagnosis. J. Infect. Dis. 1980, 141, 137–143. [Google Scholar] [CrossRef] [PubMed]
  24. Cotch, M.F.; Pastorek, J.G.; Nugent, R.P.; Yerg, D.E.; Martin, D.H.; Eschenbach, D.A. Demographic and behavioral predictors of Trichomonas vaginalis infection among pregnant women. The Vaginal Infections and Prematurity Study Group. Obstet. Gynecol. 1991, 78, 1087–1092. [Google Scholar] [PubMed]
  25. Pachano, T.; Nievas, Y.R.; Lizarraga, A.; Johnson, P.J.; Strobl-Mazzulla, P.H.; de Miguel, N. Epigenetics regulates transcription and pathogenesis in the parasite Trichomonas vaginalis. Cell Microbiol. 2017, 19, e12716. [Google Scholar] [CrossRef] [PubMed]
  26. Krieger, J.N.; Poisson, M.A.; Rein, M.F. Beta-hemolytic activity of Trichomonas vaginalis correlates with virulence. Infect. Immun. 1983, 41, 1291–1295. [Google Scholar] [CrossRef]
  27. Moodley, P.; Connolly, C.; Sturm, A.W. Interrelationships among human immunodeficiency virus type 1 infection, bacterial vaginosis, trichomoniasis, and the presence of yeasts. J. Infect. Dis. 2002, 185, 69–73. [Google Scholar] [CrossRef] [PubMed]
  28. Rathod, S.D.; Klausner, J.D.; Krupp, K.; Reingold, A.L.; Madhivanan, P. Epidemiologic features of Vulvovaginal Candidiasis among reproductive-age women in India. Infect. Dis. Obstet. Gynecol. 2012, 2012, 859071. [Google Scholar] [CrossRef] [PubMed]
  29. Moon, S.J.; Choi, J.-E.; Park, K.-I. Comparison of the Anyplex II STI-7 and Seeplex STD6 ACE Detection Kits for the Detection of Sexually Transmitted Infections. J. Lab. Med. Qual. Assur. 2013, 35, 87–92. [Google Scholar]
  30. Kweon, O.J.; Lim, Y.K.; Oh, S.M.; Kim, T.-H.; Choe, H.-S.; Lee, S.-J.; Cho, Y.-H.; Lee, M.-K. Prevalence and Antimicrobial Susceptibility of Mycoplasma hominis, Ureaplasma urealyticum and Ureaplasma parvum in Individuals with or without Symptoms of Genitourinary Infections. Lab. Med. Online 2016, 6, 79–87. [Google Scholar] [CrossRef]
  31. Jang, Y.-S.; Min, J.-W.; Kim, Y.-S. Positive culture rate and antimicrobial susceptibilities of Mycoplasma hominis and Ureaplasma urealyticum. Obstet. Gynecol. Sci. 2019, 62, 127–133. [Google Scholar] [CrossRef]
  32. Kasprzykowska, U.; Sobieszczańska, B.; Duda-Madej, A.; Secewicz, A.; Nowicka, J.; Gościniak, G. A twelve-year retrospective analysis of prevalence and antimicrobial susceptibility patterns of Ureaplasma spp. and Mycoplasma hominis in the province of Lower Silesia in Poland. Eur. J. Obstet. Gynecol. Reprod. Biol. 2018, 220, 44–49. [Google Scholar] [CrossRef] [PubMed]
  33. Wang, Q.-Y.; Li, R.-H.; Zheng, L.-Q.; Shang, X.-H. Prevalence and antimicrobial susceptibility of Ureaplasma urealyticum and Mycoplasma hominis in female outpatients, 2009–2013. J. Microbiol. Immunol. Infect. 2016, 49, 359–362. [Google Scholar] [CrossRef] [PubMed]
  34. Njunda, A.L.; Nsagha, D.S.; Assob, J.C.N.; Palle, J.N.; Kamga, H.L.; Nde, P.F.; Ntube, M.N.C.; Weledji, P.E. Genital mycoplasmas in women attending the Yaoundé University Teaching Hospital in Cameroon. J. Public. Health Afr. 2011, 2, e16. [Google Scholar] [CrossRef] [PubMed]
  35. Lee, Y.-S.; Kim, J.-Y.; Kim, J.C.; Park, W.H.; Choo, M.-S.; Lee, K.-S. Prevalence and treatment efficacy of genitourinary mycoplasmas in women with overactive bladder symptoms. Korean J. Urol. 2010, 51, 625–630. [Google Scholar] [CrossRef] [PubMed]
  36. Redelinghuys, M.J.; Ehlers, M.M.; Dreyer, A.W.; Lombaard, H.; Olorunju, S.A.S.; Kock, M.M. A cross-sectional study on the relationship of age, gestational age and HIV infection to bacterial vaginosis and genital mycoplasma infection. BMJ Open 2015, 5, e008530. [Google Scholar] [CrossRef] [PubMed]
  37. Rappelli, P.; Carta, F.; Delogu, G.; Addis, M.F.; Dessì, D.; Cappuccinelli, P.; Fiori, P.L. Mycoplasma hominis and Trichomonas vaginalis symbiosis: Multiplicity of infection and transmissibility of M. hominis to human cells. Arch. Microbiol. 2001, 175, 70–74. [Google Scholar] [CrossRef] [PubMed]
  38. Taylor-Robinson, D. Mollicutes in vaginal microbiology: Mycoplasma hominis, Ureaplasma urealyticum, Ureaplasma parvum and Mycoplasma genitalium. Res. Microbiol. 2017, 168, 875–881. [Google Scholar] [CrossRef] [PubMed]
  39. Larsen, B.; Hwang, J. Mycoplasma, Ureaplasma, and adverse pregnancy outcomes: A fresh look. Infect. Dis. Obstet. Gynecol. 2010, 2010, 521921. [Google Scholar] [CrossRef] [PubMed]
  40. Fettweis, J.M.; Serrano, M.G.; Huang, B.; Brooks, J.P.; Glascock, A.L.; Sheth, N.U.; Vaginal Microbiome Consortium; Strauss, J. F.; Jefferson, K.K.; Buck, G.A. An emerging mycoplasma associated with trichomoniasis, vaginal infection and disease. PLoS ONE 2014, 9, e110943. [Google Scholar] [CrossRef] [PubMed]
  41. Fortenberry, J.D.; Brizendine, E.J.; Katz, B.P.; Wools, K.K.; Blythe, M.J.; Orr, D.P. Subsequent sexually transmitted infections among adolescent women with genital infection due to Chlamydia trachomatis, Neisseria gonorrhoeae, or Trichomonas vaginalis. Sex. Transm. Dis. 1999, 26, 26–32. [Google Scholar] [CrossRef]
  42. Dessì, D.; Rappelli, P.; Diaz, N.; Cappuccinelli, P.; Fiori, P.L. Mycoplasma hominis and Trichomonas vaginalis: A unique case of symbiotic relationship between two obligate human parasites. Front. Biosci. 2006, 11, 2028–2034. [Google Scholar] [CrossRef] [PubMed]
  43. Ioannidis, A.; Papaioannou, P.; Magiorkinis, E.; Magana, M.; Ioannidou, V.; Tzanetou, K.; Burriel, A.R.; Tsironi, M.; Chatzipanagiotou, S. Detecting the Diversity of Mycoplasma and Ureaplasma Endosymbionts Hosted by Trichomonas vaginalis Isolates. Front. Microbiol. 2017, 8, 1188. [Google Scholar] [CrossRef] [PubMed]
  44. Dessì, D.; Delogu, G.; Emonte, E.; Catania, M.R.; Fiori, P.L.; Rappelli, P. Long-term survival and intracellular replication of Mycoplasma hominis in Trichomonas vaginalis cells: Potential role of the protozoon in transmitting bacterial infection. Infect. Immun. 2005, 73, 1180–1186. [Google Scholar] [CrossRef] [PubMed]
  45. Dessì, D.; Margarita, V.; Cocco, A.R.; Marongiu, A.; Fiori, P.L.; Rappelli, P. Trichomonas vaginalis and Mycoplasma hominis: New tales of two old friends. Parasitology 2019, 146, 1150–1155. [Google Scholar] [CrossRef] [PubMed]
  46. Adu-Sarkodie, Y. Comparison of latex agglutination, wet preparation, and culture for the detection of Trichomonas vaginalis. Sex. Transm. Infect. 2004, 80, 201–203. [Google Scholar] [CrossRef] [PubMed]
  47. Garber, G.E. The laboratory diagnosis of Trichomonas vaginalis. Can. J. Infect. Dis. Med. Microbiol. 2005, 16, 35–38. [Google Scholar] [CrossRef]
  48. Arbabi, M.; Delavari, M.; Fakhrieh-Kashan, Z.; Hooshyar, H. Review of Trichomonas vaginalis in Iran, Based on Epidemiological Situation. J. Reprod. Infertil. 2018, 19, 82–88. [Google Scholar]

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