Gynecologic infections seen in ThinPrep cytological test in Wuhan, China

Abstract

This study aimed to analyze the prevalence of bacterial, Candida, Trichomonas, and human papillomavirus (HPV) infections in ThinPrep cytological test (TCT) performed on women of Wuhan, China. ThinPrep smears were screened by two independent experienced pathologists and reported from 2008 to 2010. A total of 46 866 ThinPrep smears were studied, and smears with inflammation were analyzed. Of the 44 162 enrolled patients, inflammation changes were observed in 21 935 (49.7%) and specific infections in 6884 (31.4%). The infections detected were as follows: bacteria, 5663 (82.3%); Candida, 825 (12.0%); Trichomonas, 273 (4.0%); and HPV, 148 (2.1%). Significant changes were found in the prevalence of bacteria and Candida among women who underwent TCT before and after 2010. χ² revealed an increasing proportion of specific infections found in smears after 2010 (P=0.000). In conclusion, bacterial infection was the most detectable in the ThinPrep smears, followed by Candida and Trichomonas. The prevalence of infection identified by TCT was found to be similar in previous literature in China.

Keywords

ThinPrep cytological test / human papillomavirus / Candida infection / Trichomonas infection / bacterial infection

Introduction

ThinPrep cytological test (TCT) as a screening method has significantly decreased the incidence of cervical cancer [1]. Cytological results in TCT have a key function in the diagnosis of cervical lesions, so this procedure is routinely offered to women visiting hospitals as an opportunistic screening method. As an added advantage, diagnosis of microbial infection is performed in TCT [2,3]. Bacterial infection reportedly acts as a trigger co-factor in the carcinogenesis of cervical cancer [4]. China is currently facing a lifestyle change with modern trends [5]. However, TCT results about gynecologic infections have only been occasionally reported, and studies have mostly focused on human papillomavirus (HPV) detection [6,7]. This study was performed to determine the prevalence and the pattern of gynecologic infections, especially bacteria, Candida, Trichomonas and HPV, in a hospital setting and to identify the spectrum of these agents seen among women in Wuhan.

Materials and methods

This research constitutes a retrospective study reviewing previous TCT smears in Tongji Hospital and the Central Hospital of Wuhan satisfactory for cytological analysis between July 2008 and June 2010. The cytological reports were accomplished according to the modified Bethesda System (TBS) 2001. The specific infection included bacteria, Candida, Trichomonas, and HPV. The diagnosis of these infections was based on the typical cellular changes shown in Fig. 1. The non-specific infection consisted of benign and reactive cellular changes associated with inflammations.

Statistical analysis was performed using the statistical software package SPSS version 13.0 (SPSS, Chicago, IL). Categorical variables, such as bacterial, Trichomonas and Candida infection rates, among different years were compared using Chi-square test. A probability value of P<0.05 was considered statistically significant.

Results

Evaluation of inflammation by year

Among the 46 866 cases receiving TCT, 2688 cases were excluded due to incomplete data. Another 16 cases whose cytological results were atypical glandular cells or adenocarcinoma were also excluded. This screening process yielded 44 162 cases which were finally included in the statistical analysis. The mean age of the patients enrolled was 38.68 ± 10.00 years (aged 16 to 86), whereas the mean ages were 38.36 ± 9.98, 38.70 ± 9.92, and 38.97 ± 10.17 years in 2008, 2009, and 2010, respectively.

The proportions of ThinPrep smears with specific infections and non-specific inflammation were 31.4% and 68.6%, respectively. The proportion of specific infections increased from 23.9% in 2008 to 43.7% in 2010 (Table 1).

The distribution of specific infections is shown in Table 2. Among the 6884 ThinPrep smears with specific infections, bacterium was detected in 82.3% of smears, Candida in 12.0%, Trichomonas in 4.0%, and HPV in 2.1%. A total of 6869 patients exhibited multiple infections, whereas the other 15 patients had double infections. No triple infections were observed in our study. Nine cases of multiple infections were observed in 2009, followed by four in 2008, and two in 2010.

The prevalence changes in infectious agents over 3 years were analyzed by comparing the prevalence each year (Table 3). Observations showed an increase in the proportion of specific infections detected by TCT. Significant increase of prevalence was observed in bacterial and Candida infections by comparing the prevalence in 2009 to 2008 and 2010 to 2009 (P = 0.000 and P = 0.000 for bacterial infection, and P = 0.019 and P = 0.038 for Candida infection, respectively). The prevalence of Trichomonas and HPV infections increased in 2009 and remained unchanged in 2010 (P = 0.000 and P = 0.945 for Trichomonas infection, and P = 0.001 and P = 0.069 for HPV infection, respectively).

Evaluation of inflammation by age

The prevalence of specific infections in ThinPrep smears is shown in Table 4. Significant difference was found among different age groups in all infectious agents. The age group with highest prevalence was further analyzed by comparison with the rest of the patients. Therefore, women aged between 46 and 60 had higher prevalence of bacterial and Trichomonas infections than the other patients (P = 0.000 and P = 0.000, respectively), whereas women under the age of 30 had higher prevalence of Candida infection than women older than 30 (P = 0.000).

Discussion

Gynecologic infections are common around the world and have become major health concerns in China. Most studies in China focus on cytological results in ThinPrep smears using the revised 2001 Bethesda System [2]. However, none has analyzed the prevalence of infections in TCT, and only occasional reports show the prevalence of various infectious agents using conventional Pap smears at the community level [8-11].

The percentage of ThinPrep smears with inflammation in our research was 49.7%, whereas other studies from the Middle East have reported 34.8% to 79.9% [12-15]. Specific infectious agents were identified in 31.4% of our inflammatory cases, which is higher than that in the Muslim population. The most prevalent infections in our study were bacteria (12.8%), Candida (1.9%), and Trichomonas (0.6%). Other studies in China showed similar pattern, with bacterial infection being the most prevalent, followed by Candida (Table 5).

In our study, the prevalence of HPV infection remains unchanged (Table 3). A significant change in HPV infection was observed before and after 2010. Most studies focusing on HPV infection in China obtain their findings from biological results rather than morphology because the typical morphological changes are not recognized in all HPV infections, especially in early infections, which could cause certain missed diagnoses. Unfortunately, this retrospective analysis lacks the biological results of these ThinPrep smears because the biological test for HPV is not a routine part of TCT.

Bacterial infection was statistically significantly increased in women receiving TCT after 2010 in our study. Findings of other studies reporting on the prevalence of bacterial infection in China vary. Zhang et al. [9] showed that the bacterial infection in low-income women was 22.2%, a value much higher than that in medical staff. Therefore, living conditions might contribute to the inconsistency of results of bacterial infection. The prevalence of Candida and Trichomonas infection was 1.9% and 0.6%, respectively, which were lower than those in previous studies (Table 5). These results may be due to the difference in sample size and bias in enrollment.

Moreover, the peak ages of Trichomonas, bacterial, and Candida infections differed, but were relatively approximate in previous studies [16-22]. The occurrence of cervical inflammation was reportedly associated with microbial infection of genital tract and damage caused by physical and chemical factors. The inflammation resulting from chronic microbial infection can produce non-specific and protective anti-microbial oxidants, which can also be harmful to the host DNA, leading to the occurrence of cancer.

This retrospective study reports on the prevalence of specific infectious agents in ThinPrep smears in Wuhan. Cytological results may be a suitable screening method for infections; however, other definitive diagnostic methods cannot be replaced when available, especially for HPV detection.

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