Research Article | Volume: 8, Issue: 6, Nov-Dec, 2020

Prevalence and antimicrobial susceptibility profile of Mycoplasma hominis and Ureaplasma urealyticum in female population, Gabon

Mohamed Ag Baraïka Richard Onanga Berthold Bivigou-Mboumba Arsène Mabika-Mabika Ulrick Jolhy Bisvigou Fousseyni S. Touré Ndouo N. Coumba Touré Kane   

Open Access   

Published:  Nov 25, 2020

DOI: 10.7324/JABB.2020.80605
Abstract

Mycoplasma hominis and Ureaplasma urealyticum are microorganisms involved in many pathologies and intrauterine infections. Vaginal wall swabs were taken from 278 women for mycoplasma detection and to study the antimicrobial susceptibility using the Mycoplasma IST2 Kit (bioMérieux). We were able to document in 278 women enrolled in the study, 64.7% have infections caused by U. urealyticum, 22.7% by M. hominis, and 19.4 % of coinfections involving both germs. Such infections were observed in age groups between 18 and 42 years. Other socio-demographic characteristics studies have been conducted, which allowed to document that single women were the majority population with 68.7% against 16.5% who were living in couple. In response to our questionnaire, 131 single women enrolled in the study never protected themselves during sexual intercourse compared with 52.9% who reported using at least condom. A total of 260 (93.5%) of women reported having only one partner versus 6.5% having more. The study of strains susceptibility to antibiotics revealed a resistance of approximately 80% for macrolides and 100% for fluoroquinolones. All our isolated strains had a sensitivity of about 90% for Pristinamycin and 70% for Josamycin. This study shows that carriage of mycoplasma infection is high in female population in Franceville and vicinities, what should be an element of cautious use of antibiotic during probabilistic therapy treatment of mycoplasma.


Keyword:     Antimicrobial susceptibility Female population Mycoplasma hominis Ureaplasma urealyticum.


Citation:

Baraïka MA, Onanga R, Bivigou-Mboumba B, Mabika-Mabika A, Bisvigou UJ, Ndouo FS T, Kane NCT. Prevalence and antimicrobial susceptibility profile of Mycoplasma hominis and Ureaplasma urealyticum in female population, Gabon. J App Biol Biotech. 2020;8(6):28-32.

Copyright: Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike license.

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1. INTRODUCTION

Mycoplasma hominis and Ureaplasma urealyticum are microorganisms involved in many pathologies and intrauterine infections. They are generally associated with pyelonephritis, chorioamnionitis, pelvic inflammatory disease, endometritis, and other important complications such as prematurity, low-birth weight, spontaneous abortion, and infertility issues [1-5]. Pathologies due to such bacteria are often undiagnosed because of the non-specificity and poverty of their clinical presentations.

Such non-specificity problem has been increased ever since HIV pandemic emergence, which has complicated the germs diagnosis [6]. Mycoplasmas are also bacterial agents, of which several species are found in commensal state in humans they are responsible for respiratory, genital, and systemic infections in immunosuppressed individuals [7,8]. Urogenital colonization varies in the world between 20 and 30% for M. hominis and 60–80% for U. urealyticum [9]. Treatment of urogenital infections due to mycoplasmas is mainly based on cyclins (tetracyclines), macrolides, and quinolones [10].

In the number of quinolones, fluoroquinolones are attractive choices for treating genitourinary tract infections [11]. Biological data obtained in CIRMF Public Health Laboratory on ambulatory patients show a spread of Mycoplasma and Ureaplasma spp. infections in recent years, what is, furthermore, associated with antibiotic resistance. As a result, a better knowledge of the epidemiology of resistance to such antibiotics will, on the one hand, improve the therapeutic management of patients while reducing broad-spectrum antibiotics prescription and reduce the impact of such infection in the population, on the other hand. No study to date has considered looking into a comprehensive epidemiology and evaluation of mycoplasma resistance to antimicrobials in Gabon. The purpose of our study was on determining M. hominis and U. urealyticum strains prevalence in asymptomatic and assessing the resistance of such strains to some antibiotics.


2. MATERIALS AND METHODS

The study was conducted in Franceville at the International Center for Medical Research, (CIRMF). It was a cross-cutting and descriptive study, which was conducted over a period of 4 months on women living in Franceville and vicinities, which have been checked either during gynecological consultation or voluntarily come for mycoplasma bacteriological screening at the medical analysis laboratory of CIRMF. To be included in the study, women had to be at least 13 years old and sexually active. Their consent was to be sought before enrolling.

On inclusion in the study, a detailed medical history and clinical examination were performed for each woman. Such information was recorded on a patient card aimed at collecting first-hand socio-demographic, gestational, and behavioral data. Sampling was performed with a swab after a highlighting of cervix using speculum. In that process, leucorrhea losses were picked at endocervix level for the research of mycoplasma. Since such bacteria have high affinity for cells membranes and mucous, it was deemed important to vaginally scratch the mucosa to collect as many cells as possible for diagnosis and antimicrobial susceptibility testing.

The diagnosis was performed using Mycoplasma IST2 Kit (bioMérieux) in consonance with manufacturer’s instructions, specifically for urogenital mycoplasmas. This kit allows the culture, identification, indicative blood count, and determination the susceptibility of U. urealyticum and M. hominis to antibiotics. Mycoplasma IST2 principle combines a selective culture broth with a 22-well gallery. The broth is suitable for optimal growth of urogenital mycoplasmas.

The result has been interpreted according to the manufacturer’s recommendations (positive for identification), yellow to red color (positive for germ number ≥ 104 UFC/sample). The infection threshold for such microorganisms is set to a specific value greater than or equal to 104 ufc/ml, what enables to determine a colonization for a turn of <104 ufc/ml and an infection for a value greater than or equal to 104 ufc/ml. Wells were read in 24 and 40 h at 36 ± 2°C and the reading was valid if only the control was positive. As far as antibiotic susceptibility study was concerned, nine antibiotics molecules from Mycoplasma IST2 Kit identification gallery were tested. These molecules are Tetracycline, Doxycycline, Josamycin, Erythromycin, Azithromycin, Clarithromycin, Ofloxacin, Ciprofloxacin, and Pristinamycin. Such molecules belong, respectively, to the antibiotic families of Cyclins, Macrolides, Fluoroquinolones, and Streptogramines.

The data collected on information sheets were recorded in a database (MS Excel® spreadsheet). Data analysis was conducted using SPSS software, version 20. The value of P ? 0.05 was considered statistically significant.


3. RESULTS AND DISCUSSION

3.1. Results

For four months, we received 278 women aged 13 and over. This allowed us to isolate strains, 180 U. urealyticum 63 strains of M. hominis and 54 strains in coinfection all of them in infection situation. The study of socio-demographic, behavioral and gestational characteristics summarized in Table 1 allowed to argue that single women constituted the majority population with 68.7% compared with 16.5% living in couples. The 23–32 age groups were majority population avec 42.4%, followed by the 33–42 age groups, and accounting for 27% of the study population [Table 2]. In response to our questionnaire, 131 (47.1%) single women enrolled in the study never protected themselves during sex intercourses, compared with 147 (52.9%) who reported having used at least one condom. A total of 260 women, or 93.5% stated having one single partner versus 6.5% having more than two partners.

Table 1: Socio-demographic, behavioral and gestational data.

Socio-demographic behavioral and gestational dataFemale headcountPercentage
Marital status
 Married8731,3
 Single19168,7
 Total278100
Use of condoms
 No13147,1
 Yes14752,9
 Total278100
Number of partners
 One partner26093,5
 Several partners186,5
 Total278100
Pregnancies
 No24387,4
 Yes3512,6
 Total278100

Table 2: Prevalence of urogenital mycoplasmas by age group.

Age group (year)Ureaplasma sppM. hominis


Vaginal colonization (Uu<104 UFC/ml)Infection (Uu≥104 UFC/ml)Sterile cultureVaginal colonization l (Uu<104 UFC/ml)Infection (Uu≥104FC/ml)Sterile culture






n (%)n (%)n (%)n (%)n (%)n (%)
13–171 (5.0)2 (1.1)4 (5.1)1 (1.4)2 (3,2)4 (2.8)
18–228 (40.0)37 (20.6)5 (6.4)19 (26.8)18 (28.6)13 (9.0)
23–326 (30.0)73 (40.6)39 (50.0)23 (32.4)23 (36.5)72 (50.0)
33–424 (20.0)50 (27.8)21 (26.9)20 (28.2)17 (27.0)38 (26.4)
43–521 (5.0)18 (10.0)8 (10.3)8 (11.3)3 (4.8)16 (11.1)
53 et plus0 (0.0)0 (0.0)1 (1.3)0 (0.0)0 (0.0)1 (0.7)
Total20 (100)180 (100)78 (100)71 (100)63 (100)144 (100)

Mh: Mycoplasma hominis; Uu: Ureaplasma urealyticum; UFC: colony format unit; n: number of population.

Our study population consisted of 35 pregnant women or 12.6% of the study population. It has been observed that vaginal colonization or commensal portage by such microorganisms changed with age. Prevalence was high in the 18- to 42-year-old age groups with greater portage in the 23–32 year-old modal age group. Such germs were found in commensalism in our study population, respectively, at 7.2% for U. urealyticum and 25.5% for M. hominis [Table 2]. In our study, population investigations of urogenital mycoplasma infections showed 65% for U. urealyticum and 22.7% for M. hominis. Coinfection due to such germs (M. hominis and U. urealyticum) represented 19.4% in our study population; such infection was more involuted in age groups between 18 and 42 years.

M. hominis and/or U. urealyticum spp. isolation in infection situations in pregnant women was mostly found in the first and second pregnancy quarter. Infection by behavioral and gestational status is summarized in Table 3. The susceptibility of isolated mycoplasmas to antibiotics is summarized in Table 4. All strains isolated in infection showed relatively low resistance to Tetracycline, Josamycin, and Pristinamycin ranging from 2.8% to 29.6%. We observed 100% resistance, of U. urealyticum not only to Ciprofloxacin but also to M. hominis with Azithromycin, Clarithromycin, and Erythromycin. Strains found in coinfection showed a 100% resistance to ciprofloxacin, Azithromycin, Clarithromycin, and Erythromycin. In a particular way, all the U. urealyticum strains displayed high resistance to all the tested antibiotic molecules.

Table 3: Results of infectious status according to behavioral and gestational data.

Socio-demographic data behavioral and gestationalPresence status of germs

U. u Infection n (%)M. h Infection n (%)Co-Infection (Uu+Mh) n (%)
Use of condoms
 No100 (55.5)36 (57.1)23 (42.6)
 Yes80 (44.4)27 (42.8)31 (57.4)
 Total180 (100)63 (100)54 (100)
Number of partners
 One partner167 (92.8)59 (93.6)50 (92.6)
 Several partners13 (7.2)4 (6.3)4 (7.4)
 Total180 (100)63 (100)54(100)
Pregnancies
 No 161 (89.4)57 (90.5)50 (92.6)
 Yes19 (10.5)6 (9.5)4 (7.4)
 Total180 (100)63 (100)54 (100)

U.u: Ureaplasma urealyticum, M. h: Mycoplasma hominis, n: Number of population.

Table 4: The susceptibility of isolated mycoplasmas to antibiotics

Antibiotic families/MoleculesUrea plasma urealyticum strains (n=180)Mycoplasma hominis Strains (n=63)Coinfection (Uu+Mh) (n=54)



SusceptibleResistantSusceptibleResistantSusceptibleResistant






n%n%n%n%n%n%
Fluoroquinolones
 Ofloxacin52,817597,234,86095,211,95398,1
 Ciprofloxacin0--18010023,26196,80--54100
Cyclins
 Tetracycline13373,84726,13555,62844,42953,72546,3
 Doxycyclin16088,92011,15587,3812,74685,2814,8
Macrolides
 Azithromycin3519,414580,60--631000--54100
 Clarithromycin6133,911966,90--631000--54100
 Erythromycin3318,314781,70--631000--54100
 Josamycin 14781,73318,34774,61625,43870,41629,6
streptogramins
 Pristinamycine17597,25285993,746,35092,647,4

Uu: Ureaplasma urealyticum, Mh: Mycoplasma hominis, n: Number of population.


4. DISCUSSION

The study is the first of its kind to assess in a comprehensive manner the prevalence and antibiotic resistance profile of Mycoplasma strains (U. urealyticum and M. hominis) in Franceville, Gabon. The exclusion of women under childbearing age and the free availability of mycoplasma research examinations at the CIRMF Medical Analysis Laboratory allowed us to eliminate certain selection biases. We were able to document in 278 women enrolled in the study, 64.7% of infection caused by U. urealyticum, 22.7% by M. hominis, and 19.4% coinfection involving both germs (U. urealyticum and M. hominis). Infections alike were observed in age groups between 18 and 42 years. Carriage rate was more significant in such age groups. Carriage and infections caused of mycoplasma this kind may to be explained by this population’s sexual activity. In China, authors reported that 31.2% infections caused by U. urealyticum, 0.7% by M. hominis, and 1.9% coinfections due to the two bacterial germs were believed to be in a population of 6051 women over 4-year period [12].

In Serbia in 2010, it has been reported following a study comparing mycoplasma infections that the prevalence in a symptomatic and asymptomatic infections and coinfections rates in pregnant women population was variable [13]. Such difference observed in all the alike studies could be caused not only to the methodology but also to the epidemiological facies of different epidemiological zones.

Our outcomes show that the prevalence of Mycoplasma in Franceville is higher than that in Ouagadougou [14] and Bangui among a women population [15]. Such variation between Northern and Southern countries in terms of mycoplasma infection rate could be explained by the fact that the studies performed in northern countries focused on symptomatic populations, whereas the ones we performed focused on all women broadly speaking a broader comprehensive way focused on achieved in rates.

In all such studies infections and coinfections, distribution profile is the same decreasing order, dominated by U. urealyticum followed by M. hominis and finally coinfection caused to the two germs (U. urealyticum and M. hominis) [12,14-15]. The study of behavioral parameters allowed us to document that single women were the majority population. In response to our questionnaire, 131 single women enrolled in the study did not protect themselves during sexual intercourse that had no real influence on mycoplasma infection rates. Few authors having performed that mycoplasma studies have addressed behavioral parameters. In pregnant women, urogenital mycoplasmas often only bear witness to oestroprogestative impregnation in this particular population [16].

Mycoplasmas naturally resist to antibiotics that act on bacterial cell wall. This is because they do not have a wall. However, they are generally susceptible to antibiotics that inhibit bacterial proteins synthesis [11]. Of all the mycoplasma isolates tested, the overall resistance to fluoroquinolones ranged from 95.2% to 100% for Ciprofloxacin and Ofloxacin. For isolates of U. urealyticum and M. hominis, overall resistance rates for fluoroquinolones were, respectively, 96.8% and 100% for Ciprofloxacin and 95.2% and 97.2% for Ofloxacin. Such results are higher that, those reported in 2011 in a study which looked at determining the susceptibility of U. urealyticum and M. hominis strains to antibiotics in northeastern Romania. In the course of said study, a resistance was documented to Ciprofloxacin 75% and 53.7%, respectively, for M. hominis and U. urealyticum, against 30% and 16.13% for Ofloxacin in M. hominis and U. urealyticum strains [17].

The explanation for the high percentage of mycoplasma resistance to fluoroquinolones from strains isolated from human patients could not only cause to the frequency of such family of molecules prescription by prescribers in infection treatments but also caused to their mild side effects that could cause such molecules. Macrolide mycoplasmas resistance rates ranged from 69.9% to 100% for all test molecules (Erythromycin, Azithromycin, and Clarithromycin).

Studies achieved in New Guinea and Romania reported resistance rates of mycoplasma ranging from 33.33% to 97.8% for Erythromycin, confirming a high level of resistance to macrolides [17,18]. Such variable rates observed between the results of different studies for the same therapeutic molecules against mycoplasmas, could be due not only to the variability of isolates but also to the attitude of public as regard the therapeutic regimens given by the prescribers. However, mycoplasmas expressed a resistance to Josamycin ranging between 18.3% and 25.4%. Such levels are lower than those of the other molecules of the same family of macrolides. Cyclins resistant (Tetracycline and Doxycycline) was variable in the range of 26.1–44.4%. Such resistance rates are higher than those reported by some authors in New Guinea, Senegal, and Serbia [18-20].

Observed differences could be due to the use of molecules of this family since birth in some African populations. Some mycoplasmas acquire genetic resistance to Tetracycline through a Tet (M) mutation [7,21]. It would be interesting to study the prevalence of Tet (M) mutations, but also mutation genes to fluoroquinolones. In contrast to fluoroquinolones, macrolides, and cyclins, our isolates had a very low resistance to Pristinamycin in the range of 2.8–7.4%. This result shows the good activity of such a molecule on mycoplasma and is a significant a therapeutic agent for infections mainly caused by M. hominis and U. urealyticum. Studies on the identification of antibiotic resistance genes should be considered in Franceville, where the resistance of mycoplasma to certain antibiotic molecules reaches 100%. Such wide variability in antibiotic resistance profile tested has been reported by several authors throughout the world [22-24].


5. CONCLUSION

The results obtained in this study show that carriage of mycoplasma infection or colonization is high in the female population in Franceville. The treatment based on mycoplasmas probabilistic antibiotic therapy should focus on first-line use of Pristinamycin, followed by Cyclins, although somewhere, their effectiveness is probable on such mycoplasmas.


6. ACKNOWLEDGMENTS

Work was conducted at UARSP of CIRMF, Franceville, Gabon. We thank the sampling staff for their help in the collection of patient’s samples. This study was supported by CIRMF.


7. Conflicts of Interest

Authors declared that there are no conflicts of interest.


8. Financial Support and Sponsorship

None.

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16. Furr PM, Taylor-Robinson D. The effect of sex hormones on Mycoplasma genital infections. In: Stanek G, Cassell GH, Tully JG, Whitcomb RF, editors. Recent Advances in Mycoplasmology. Stuttgart: Fischer; 1990. p. 223-6.

17. Mihai M, Valentin N, Bogdan D, Carmen MC, Coralia B, Demetra S. Antibiotic susceptibility profiles of Mycoplasma hominis and Ureaplasma urealyticum isolated during a population-based study concerning women infertility in Northeast Romania. Braz J Microbiol 2011;42:256-60. [CrossRef]

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Reference

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2. Daxboeck F, Zitta S, Stadler M, Iro E, Krause R. Mycoplasma hominis and Ureaplasma urealyticum in patients with sterile pyuria. J Infect 2005;51:54-8. https://doi.org/10.1016/j.jinf.2004.06.010

3. Patai K, Szilagyi G, Hubay M, Szentmariay IF, Paulin F. Severe endometritis caused by genital Mycoplasmas after Caesarean section. J Med Microbiol 2005;54:1249-50. https://doi.org/10.1099/jmm.0.05457-0

4. Witt A, Berger A, Gruber CJ, Petricevic L, Apfalter P, Worda C, et al. Increased intrauterine frequency of Ureaplasma urealyticum in women with preterm labor and preterm premature rupture of the membranes and subsequent cesarean delivery. Am J Obstet Gynecol 2005;193:1663-9. https://doi.org/10.1016/j.ajog.2005.03.067

5. Pararas MV, Skevaki CL, Kafetzis DA. Preterm birth due to maternal infection: Causative pathogens and modes of prevention. Eur J Clin Microbiol Infect Dis 2006;25:562-9. https://doi.org/10.1007/s10096-006-0190-3

6. Goeman J, Meheus A, Piot P. The epidemiology of sexually transmitted diseases in developing countries in AIDS era. Ann Soc Belg Med Trop 1991;71:81-113.

7. Bébéar C. Infections humaines à mycoplasmes. Rev Francoph Lab 2007;37:63-9. https://doi.org/10.1016/S1773-035X(07)80131-6

8. Bébéar C. Mycoplasma et chlamydia. In: Nicolas JC, editor. Collection Medi Bio. Paris: Elsevie; 2002.

9. Clegg A, Passey M, Yoannes M, Michael A. High rates of genital Mycoplasma infection in the highlands of Papua New Guinea determined both by culture and by a commercial detection kit. J Clin Microbiol 1997;l35:197-200. https://doi.org/10.1128/JCM.35.1.197-200.1997

10. Waites KB, Katz B, Schelonka RL. Mycoplasmas and Ureaplasmas as neonatal pathogens. Clin Microbiol Rev 2005;18:757-89. https://doi.org/10.1128/CMR.18.4.757-789.2005

11. Taylor-Robinson D, Bebear C. Antibiotic susceptibilities ofMycoplasmas and treatment of mycoplasmal infections. J Antimicrob Chemother 1997;40:622-30. https://doi.org/10.1093/jac/40.5.622

12. Wang QY, Li RH, Zheng LQ, Shang XH. Prevalence and antimicrobial susceptibility of Ureaplasma urealyticum and Mycoplasma hominis in female outpatients, 2009-2013. J Microbiol Immunol Infect 2016;49:359-62. https://doi.org/10.1016/j.jmii.2014.06.007

13. Bayraktar RM, Ozerol IH, Gucluer N, Celik O. Prevalence and antibiotic susceptibility of Mycoplasma hominis and Ureaplasma urealyticum in pregnant women. Int J Infect Dis 2010;14:e90-5. https://doi.org/10.1016/j.ijid.2009.03.020

14. Djigma F, Ouedraogo C, Ouermi D, Bisseye C, Sagna T, Zeba M, et al. Co-infection of Mycoplasma hominis and Ureaplasma urealyticum in HIV-positive women in Ouagadougou. Science et technique, 2008;31:9-20.

15. Rapelanoro RF, Lepère P, Escarguel C, Lamarque P, Malvy D. Prevalence of urogenital Mycoplasma infection in HIV-infected women in Bangui (Central African Republic). Health Noteb1998;8:189-92.

16. Furr PM, Taylor-Robinson D. The effect of sex hormones on Mycoplasma genital infections. In: Stanek G, Cassell GH, Tully JG, Whitcomb RF, editors. Recent Advances in Mycoplasmology. Stuttgart: Fischer; 1990. p. 223-6.

17. Mihai M, Valentin N, Bogdan D, Carmen MC, Coralia B, Demetra S. Antibiotic susceptibility profiles of Mycoplasma hominis and Ureaplasma urealyticum isolated during a population-based study concerning women infertility in Northeast Romania. Braz J Microbiol 2011;42:256-60. https://doi.org/10.1590/S1517-83822011000100032

18. Alison C, Megan P, Mition Y, Audrey M. High rates of genital Mycoplasma infection in the highlands of papua new guinea determined both by culture and by a commercial detection kit. J Clin Microbiol 1997;35:197-200. https://doi.org/10.1128/JCM.35.1.197-200.1997

19. Sow A. I, Diallo Y, Diab El Hadi A, Samb A. In vitro sensitivity to antibiotics in 178 strains of genital Mycoplasma isolated from gynecology consultants in Dakar. Bull Soc Pathol Exot 2000;93:6-7.

20. Skiljevic D, Mirkov D, Vukicevic J. Prevalence and antibiotic susceptibility of Mycoplasma hominis and Ureaplasma urealyticum in genital samples collected over 6 years at a Serbian university hospital. Indian J Dermatol Venereol Leprol 2016;82:37-41. https://doi.org/10.4103/0378-6323.172903

21. Degrange S, Renaudin H, Charron A, Bébéar C, Bébéar CM. Tetracycline resistance in Ureaplasma spp. and Mycoplasma hominis: Prevalence in Bordeaux, France, from 1999 to 2002 and description of two tet(M)-positive isolates of Mycoplasma hominis susceptible to tetracycline. Antimicrob Agents Chemother 2008;2:742-4. https://doi.org/10.1128/AAC.00960-07

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