Abstract
Background
Mycoplasma hominis, Ureaplasma parvum, and Ureaplasma urealyticum are commensal bacteria that are associated with colonization and infection of the urogenital tract. However, colonization of the respiratory tract by these microorganisms in adults has not been fully investigated.
Methods
Urine and respiratory tract samples (sputum, tracheal aspirates, and bronchoalveolar lavage) of patients aged 20−80 years were analyzed to detect the presence of M. hominis, U. parvum, and U. urealyticum using a conventional PCR method. The samples were submitted to the microbiological clinical laboratory of Hiroshima University Hospital from December 1, 2021 to May 31, 2022.
Results
In total, 334 urine and 238 respiratory tract samples were analyzed. The overall detection rates of M. hominis, U. parvum, and U. urealyticum were 2.9%, 1.7%, and 2.3% in male urine; 7.0%, 13.8%, and 1.9% in female urine; 2.2%, 0%, and 2.2% in male respiratory tract; and 0%, 2.0%, and 0% in female respiratory tract, respectively. In urine samples, the detection rates of M. hominis, U. parvum, and U. urealyticum were significantly higher (p < 0.001) for women (29/159; 18.2%) than for men (10/175; 5.7%); however, in respiratory tract samples, the detection rates were not significantly different (p = 0.70) between women (2/101; 2.0%) and men (5/137; 3.7%). Further, both the urine and respiratory samples of 83 patients were analyzed. Three male samples were positive for M. hominis or U. urealyticum, and M. hominis and U. urealyticum were matched in both the urine and respiratory tract samples: M. hominis (n = 1), U. urealyticum (n = 1), M. hominis + U. urealyticum (n = 1).
Conclusion
M. hominis, U. parvum, and U. urealyticum were detected in the respiratory tract of not only the young patients, but also of patients aged 50−60 years. Further studies are required to understand the relationship of these microorganisms in urogenital and respiratory tract samples with extra-genital infections.
Keywords: Respiratory tract, Colonization, Mycoplasma, Ureaplasma, PCR
Highlights
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The detection rates of Mycoplasma hominis, Ureaplasma parvum, and Ureaplasma urealyticum were investigated.
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The detection rates of these organisms in urine was significantly higher than in respiratory tract samples.
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These organisms were detected in the respiratory tract samples of young patients as well as patients aged 50–60 years.
1. Introduction
Mycoplasma hominis, Ureaplasma parvum, and Ureaplasma urealyticum are commensal bacteria that colonize the urogenital tract and typically cause urogenital infections [1]. M. hominis and Ureaplasma spp. can also rarely cause extra-urogenital infections, including mediastinitis, post-transplantation infections, and septic arthritis, particularly in postoperative and immunocompromised patients [[2], [3], [4], [5], [6], [7]]. In addition, a recent systematic review and meta-analysis showed a higher incidence and significantly increased risk of hyperammonemia syndrome among immunocompromised patients with Ureaplasma spp. infection, particularly in lung transplant recipients [8]. However, the sources of extra-urogenital infections of M. hominis and Ureaplasma spp. are not fully understood. It has been hypothesized that invasive medical procedures, such as urinary catheterization, lead to bloodstream invasions of M. hominis and seeding of the surgical site [9]. Additionally, recent reports have suggested donor-derived M. hominis or Ureaplasma spp. infections in lung transplant recipients [[10], [11], [12]]. A few reports have shown that M. hominis and Ureaplasma spp. were isolated from tracheal aspirates and bronchoalveolar lavage (BAL) specimens, suggesting that M. hominis and Ureaplasma spp. colonize the respiratory tract in adults [11,[13], [14], [15]]. Therefore, colonization of the respiratory tract with M. hominis and Ureaplasma spp. also may be associated with extra-urogenital infections caused by these microorganisms. However, the prevalence of detection of M. hominis and Ureaplasma spp. in the respiratory tract of adults remains unclear. Therefore, the aim of this study was to investigate the detection rate of M. hominis, U. parvum, and U. urealyticum in the urine and respiratory tract samples of patients who were not suspected to have sexually transmitted diseases (STDs).
2. Materials and methods
2.1. Study design
We examined the residual urine and respiratory tract samples (sputum, tracheal aspirates, and BAL samples) submitted to the microbiological clinical laboratory of Hiroshima University Hospital from December 1, 2021 to May 31, 2022. These samples were collected from patients aged 20–80 years with suspected urinary or respiratory tract infections. Patients who were administered antimicrobial agents that may be effective against Mycoplasma spp. and Ureaplasma spp. in the last 4 weeks, including macrolides, clindamycin, tetracyclines, and quinolones, were excluded. In addition, samples from patients who were suspected to have STDs, such as those with urethral or vaginal discharge, urethral irritation, and itching of genital lesions, were excluded. Demographic and clinical data including co-morbidities of the patients were obtained from medical records.
2.2. PCR analysis
Urine samples were centrifuged at 13,000×g for 10 min and 400 μL of the sediment was used for DNA extraction. The respiratory tract samples were homogenized with 100 μL to an equal volume of a mucolytic agent, Sputazyme (Kyokuto Pharmaceuticals Industrial Co., Ltd., Tokyo, Japan), depending on the viscosity of the samples, followed by centrifugation at 13,000×g for 10 min (400 μL of the sediment was used for DNA extraction). DNA was extracted using the automatic extraction system magLEAD® with magLEAD® Dx SV reagent (Precision System Science Co., Ltd., Chiba, Japan) in accordance with the manufacturer's instructions. The polymerase chain reaction (PCR) for M. hominis targeting 16s rRNA gene was performed at the following conditions: 2 min at 95 °C, 30 cycles consisting of 1 min at 95 °C, 1 min at 60 °C, and 1 min at 72 °C, with a final extension step of 5 min at 72 °C, using the following PCR primers: (RNAH1, 5′ -CAATGGCTAATGCCGGATACGC-3′; RNAH2, 5′-GGTACCGTCAGTCTGCAAT-3′) [16]. The length of the M. hominis PCR product was 334 bp. The PCR for U. parvum was performed at the following conditions: 2 min at 95 °C, 30 cycles consisting of 1 min at 95 °C, 1 min at 55 °C, and 1 min at 72 °C, with a final extension step of 5 min at 72 °C, using the following PCR primers: (UMS-57, 5′ -CAAATCTTAGTGTTCATATTTTTTAC-3′; UMA-222, 5′- GTAAGTGCAGCATTAAAT TCAATG-3′) [17]. The length of the U. parvum PCR product was 327 bp. The PCR for U. urealyticum was performed at the same conditions as U. parvum using the following PCR primers: (UMS-170, 5′ - GTATTTGCAATCTTTATATGTTTTCG-3′; UMA-263, 5′- TTTGTTGTTGCGTTTTCTG-3′) [17]. The length of the U. urealyticum PCR product was 476 bp. The amplified fragments were analyzed on 2% (w/v) agarose gels containing ethidium bromide and visualized using a UV-transilluminator. Samples were diluted (1:10) to reduce the background noise of the host DNA.
2.3. Ethics
The study protocol was approved by the Ethical Committee for Epidemiology of Hiroshima University (no. E−2133). The requirement for obtaining written informed consent was waived due to the observational study protocol and the fact that only residual samples were examined.
2.4. Statistics
Continuous variables were analyzed using the Wilcoxon rank-sum test. Categorical variables were analyzed using the χ2 test or Fisher's exact test for small samples. All statistical analyses were performed using JMP 16.0 (SAS Institute Inc., Cary, NC, USA). Statistical significance was set at p < 0.05.
3. Results
A total of 334 urine samples and 238 respiratory tract samples (145 sputum samples, 91 tracheal aspirates, and 2 BAL samples) were examined. Table 1 and Fig. 1 show the detection rates of M. hominis, U. parvum, and U. urealyticum in urine and respiratory tract samples. The table in Additional file 1 presents the age-wise distribution of prevalence of these microorganisms in various samples. Five tracheal aspirates from males and two sputum samples from females were positive for M. hominis, U. parvum or U. urealyticum. Table 2 show the demographic and clinical characteristics of patients with and without M. hominis and Ureaplasma spp. in their urine or respiratory tract samples.
Table 1.
Prevalence of Mycoplasma hominis and Ureaplasmaspp. detection in urine and respiratory tract samples.
| Samples | Variable | n, (%) |
|---|---|---|
| Urine samples from male patients (n = 175) | Overall prevalence (single + multiple colonization) | |
| Mycoplasma hominis | 5 (2.9) | |
| Ureaplasma parvum | 3 (1.7) | |
| Ureaplasma urealyticum | 4 (2.3) | |
| Double colonization | ||
| Mycoplasma hominis + Ureaplasma parvum | 2 (1.1) | |
| Urine samples from female patients (n = 159) | Overall prevalence (single + multiple colonization) | |
| Mycoplasma hominis | 9 (7.0) | |
| Ureaplasma parvum | 22 (13.8) | |
| Ureaplasma urealyticum | 3 (1.9) | |
| Double colonization | ||
| Mycoplasma hominis + Ureaplasma parvum | 4 (2.5) | |
| Mycoplasma hominis + Ureaplasma urealyticum | 1 (0.6) | |
| Respiratory tract samples from male patients (n = 137) | Overall prevalence (single + multiple colonization) | |
| Mycoplasma hominis | 3 (2.2) | |
| Ureaplasma parvum | 0 (0) | |
| Ureaplasma urealyticum | 3 (2.2) | |
| Double colonization | ||
| Mycoplasma hominis + Ureaplasma urealyticum | 1 (0.7) | |
| Respiratory tract samples from female patients (n = 101) | Overall prevalence (single + multiple colonization) | |
| Mycoplasma hominis | 0 (0) | |
| Ureaplasma parvum | 2 (2.0) | |
| Ureaplasma urealyticum | 0 (0) |
Fig. 1.
Prevalence of Mycoplasma hominis and Ureaplasmaspp. colonization in urine and respiratory tract samples (a) Urine samples from male patients. (b) Urine samples from female patients. (c) Respiratory tract samples from male patients. (d) Respiratory tract samples from female patients.
Table 2.
Demographic and clinical characteristics of patients with and without M. hominis and Ureaplasma spp. in their urine or respiratory tract samples.
| (a) Urine samples | |||
|---|---|---|---|
| Patient characteristics | Patients with M. homnis or/and Ureaplasma spp. in their urine samples (n = 39) | Patients without M. homnis or/and Ureaplasma spp. in their urine samples (n = 295) | P value |
| Age (years), median (range) | 32 (20–74) | 59 (19–89) | <0.001 |
| Sex, number, (%) | |||
| Male | 10 (25.6) | 165 (55.9) | <0.001 |
| Female | 29 (74.4) | 130 (44.1) | |
| Co-morbidity | |||
| Malignancies | 3 (7.7) | 100 (33.9) | <0.001 |
| Solid organ malignancy | 3 (7.7) | 86 (29.2) | 0.0034 |
| Hematologic malignancy | 0 (0) | 15 (5.1) | 0.23 |
| Diabetes mellitus | 2 (5.1) | 40 (13.6) | 0.20 |
| Liver cirrhosis | 0 (0) | 8 (2.7) | 0.60 |
| History of organ transplantation | 2 (5.1) | 19 (6.4) | 1.0 |
| Steroid or/and immunosuppressant use | 10 (25.6) | 57 (19.3) | 0.35 |
| (b) Respiratory tract samples | |||
|---|---|---|---|
| Patient characteristics | Patients with M. homnis or/and Ureaplasma spp. in their respiratory tract samples (n = 7) | Patients without M. homnis or/and Ureaplasma spp. in their respiratory tract samples (n = 231) | P value |
| Age (years), median (range) | 43 (33–67) | 67 (19–82) | 0.012 |
| Sex, number, (%) | |||
| Male | 5 (71.4) | 132 (57.1) | 0.70 |
| Female | 2 (28.6) | 99 (42.9) | |
| Co-morbidity | |||
| Malignancy | 2 (28.6) | 78 (33.7) | 1.0 |
| Solid organ malignancy | 2 (28.6) | 61 (26.4) | 1.0 |
| Hematologic malignancy | 0 (0) | 17 (7.4) | 1.0 |
| Diabetes mellitus | 0 (0) | 21 (9.1) | 1.0 |
| Liver cirrhosis | 0 (0) | 4 (1.7) | 1.0 |
| History of organ transplantation | 0 (0) | 4 (1.7) | 1.0 |
| Steroid or/and immunosuppressant use | 0 (0) | 34 (14.7) | 0.60 |
In each of urine and respiratory tract samples, patients with M. hominis, U. parvum, or U. urealyticum were significantly younger than patients without these organisms (p < 0.001, p = 0.012). In urine samples, the detection rates of M. hominis, U. parvum, and U. urealyticum were significantly higher for women than men (p < 0.001). In contrast, no significant difference was observed in the detection rates of M. hominis, U. parvum, and U. urealyticum in women and men respiratory samples (p = 0.70). In urine samples, patients with M. hominis, U. parvum, and U. urealyticum were significantly less likely to have an underlying solid organ malignancy compared to patients without these organisms (p = 0.003).
For total samples, the detection rates of M. hominis, U. parvum, and U. urealyticum were significantly higher for urine samples than for respiratory tract samples (p < 0.001, 39/334 [11.7%] vs. 7/238 [2.9%], respectively). Among samples collected from females, the detection rates of M. hominis, U. parvum, and U. urealyticum were significantly higher for urine samples than for respiratory tract samples (p < 0.001, 29/159 [18.2%] vs. 2/101 [2.0%]). In contrast, among male samples, the detection rates of the three microorganisms were not significantly different between urine and respiratory tract samples (p = 0.43 10/175 [5.7%] vs. 5/137 [3.6%], respectively).
Eighty-two patients were evaluated for both the urine and respiratory tract samples (male, n = 55; female, n = 27). Three male samples were positive for M. hominis or Ureaplasma spp., while none of the female samples were positive. Among the three positive samples, M. hominis and U. urealyticum were matched in both the urine and respiratory tract samples: M. hominis (n = 1), U. urealyticum (n = 1), M. hominis + U. urealyticum (n = 1). One female respiratory tract sample tested positive for U. parvum. However, urine samples from this patient have not yet been investigated.
4. Discussion
This study showed that the respiratory tract samples from patients aged 20–80 years were positive for M. hominis (n = 3, 1.3%), U. parvum (n = 2, 0.8%), and U. urealyticum (n = 3, 1.3%). Unlike previous studies involving lung transplant patients [8,11,15], the present study showed that M. hominis and Ureaplasma spp. were detected in the respiratory tract of not only young patients but also patients aged 50–60 years. Although M. hominis was not detected in respiratory tract samples of female patients, the detection rate of M. hominis in the respiratory tract was consistent with that of previous reports, which suggested that M hominis can be found in the respiratory secretions of 1–3% of healthy adults [18]. Recent reports showed the detection rate of M. hominis and Ureaplasma spp. in respiratory tract samples of lung transplant recipients and donors was 10.2–14.3% [11,15,19], which were higher than that of this study. This result may be associated with the fact that the patient population of our study was older than that of previous reports.
In our study, among the urine samples of male patients aged 20−30 years, the detection rates of M. hominis, U. parvum, and U. urealyticum were 6.7%, 2.2%, and 6.7%, respectively. Kawaguchi et al. reported that M. hominis, U. parvum, and U. urealyticum were detected in 10.9%, 6.5%, and 12.3% of male patients with urethritis (n = 141, mean age 37.6 years), whereas these species were detected in 2.0%, 4.7%, and 2.7% of the urine samples from the control groups (n = 154, mean age 39.0 years), respectively [20]. The detection rate of these organisms in male urine samples in the present study was similar to that in this previous report [20]. In addition, in our study, the prevalence of colonization by these organisms in the male patients aged 50−60 years was similar to those of 20–30 years. Reports on patients with symptoms of urogenital tract infection showed that the positive rates of M. hominis and U. urealyticum were the highest among the 55–59 [21] and >65 years age groups [22] in clinical specimens collected from male patients. However, these results may be associated with the small sample size in this age group.
Among female urine samples, the highest prevalence of M. hominis, U. parvum, and U. urealyticum was among the patients in the 30–39 years age group (43.4%), followed by the 20 years age group (40.8%), while a substantial drop in prevalence was observed in patients older than 50 years. U. parvum was the most frequently detected species in this study. These results were consistent with previous reports [23,24].
Among the 82 patients who were evaluated for both the urine and respiratory tract samples, three male samples were positive for M. hominis or Ureaplasma spp., and no female samples were positive. Interestingly, among the three patients, the detection results for M. hominis and Ureaplasma spp. were matched in both the urine and respiratory tract samples: M. hominis (n = 1), U. urealyticum (n = 1), M. hominis + U. urealyticum (n = 1). The same species of M. hominis and Ureaplasma spp. may colonize the urogenital tract, oral cavity, and respiratory tract, perhaps from sexual contact with their partners. A previous study showed that among sexually active Japanese male patients who attended the STD outpatient clinic (mean age, 34.4 years), the detection rates of M. hominis and Ureaplasma spp. were 10.3% and 16.0% in oral and 6.3% and 19.2% in urine samples, respectively [25]. This study showed that there were no significant differences in the detection rates of M. hominis and Ureaplasma spp. in males between the oral cavity and urine samples, suggesting that genital Mycoplasma spp. and Ureaplasma spp. could colonize the male oral cavity. Therefore, further studies are required to assess the prevalence of M. hominis and Ureaplasma spp. colonization in the urinary tract, oral cavity, and respiratory tract.
In this study, risk factors of detection of M. hominis, U. parvum, and U. urealyticum in urine samples were younger age, female, and not having the co-morbidity of solid organ malignancy. Not having the co-morbidity of solid organ malignancy may also be associated with a younger age. In contrast, a risk factor of detection of these microorganisms in respiratory tract samples was only younger age. Previous reports on lung transplantation suggest that the detection of M. hominis or Ureaplasma spp. in the respiratory tract was associated with sexually active young males [11,15,19]. This may be related to the fact that these pathogens frequently colonize the female urogenital tract, and it was hypothesized that M. hominis and Ureaplasma spp. colonizing the oral cavity, perhaps from sexual contact with their partners, were introduced into the respiratory tract during aspiration [11]. In this study, no significant difference was observed in the detection rates of these microorganisms in male and female respiratory tract samples. In addition, although U. parvum was the most frequently detected species in female urine samples, it was not detected in the respiratory tract samples of male patients. These results may be associated with the fact that the sample size of respiratory tract specimens of patients in the age group 20−30 years were limited as samples from this age group were submitted less frequently.
Our study has several limitations. First, this was a single-center study with a small sample size and the results may not be generalized to other centers or countries. Second, we did not investigate the sexual activity of patients; therefore, the relationship between sexual activity and the detection rates of these microorganisms in the urine and respiratory tract samples could not be examined. Third, culturing and determination of antimicrobial susceptibilities for M. hominis and Ureaplasma spp. were not performed. Therefore, we could not investigate the antimicrobial resistance of these organisms. Fourth, we investigated not only tracheal aspirates and BAL samples but also sputum specimens; therefore, the results of this study may have been influenced by the oral colonization of M. hominis, U. parvum, and U. urealyticum. Further, the respiratory tract samples of patients in the 20–40 years age group were less because we only collected the residual samples.
In conclusion, we demonstrated a significantly higher detection rate of M. hominis, U. parvum, and U. urealyticum in urine samples than in respiratory tract samples. We also showed that these microorganisms were detected in the respiratory tract samples of young patients as well as patients aged 50−60 years. In addition, we demonstrated that the same species of M. hominis, Ureaplasma spp. can be detected from urine and respiratory tract of the same patient. Further studies are required to understand the relationship of M. hominis, U. parvum, and U. urealyticum detection in urogenital and respiratory tract samples with extra-genital infections caused by these microorganisms.
Author contribution statement
Kayoko Tadera; Hiroki Kitagawa: Conceived and designed the experiments; Performed the experiments; Analyzed and interpreted the data; Wrote the paper.
Hiroyuki Kitano; Toshinori Hara; Seiya Kashiyama: Performed the experiments; Analyzed and interpreted the data.
Toshihito Nomura; Keitaro Omori; Norifumi Shigemoto; Michiya Yokozaki; Hiroki Ohge: Contributed reagents, materials, analysis tools or data.
Funding statement
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Data availability statement
Data included in article/supp. material/referenced in article.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
None.
Footnotes
Supplementary data to this article can be found online at https://doi.org/10.1016/j.heliyon.2023.e14543.
Appendix A. Supplementary data
The following is the Supplementary data to this article:
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