Abstract
Objective
Pelvic inflammatory disease (PID) is an infection of female reproductive organs mainly in sexually active patients, which can cause serious complications throughout life. We aimed to analyze the risk factors and differences in sexually transmitted infections (STIs) between adolescents and adult PID patients.
Materials and methods
We conducted a retrospective study based on descriptive and statistical analyses of the clinical records of patients with PID treated with antibiotics between January 2013 and December 2023 at Busan Paik Hospital. In this study, we analyzed the clinical characteristics of patients and the types of cultured bacteria in vaginal discharge, as well as their association with STIs according to age.
Results
Three hundred patients required hospitalization and treatment with antibiotics. Thirty-nine (13.0 %) were adolescent patients, and 261 (87 %) were adult patients. Infections of Chlamydia trachomatis , Neisseria gonorrhoeae , Mycoplasma genitalium , Mycoplasma hominis , Ureaplasma urealyticum, and Trichomonas vaginalis were more prevalent in adolescents than in adult patients ( P < 0.001, 0.001, 0.013, <0.001, 0.004 and 0.010, respectively) . Although Lactobacillus spp . was predominant among the cultured strains in both adolescents and adults, it was detected in 29.6 % of adolescent patients and 48.4 % of adults; its detection rates were relatively lower among adolescents ( P = 0.071). Among adolescents, 30.6 % were smokers, while 13.3 % were smokers among adult patients. Although there was a higher prevalence of smoking among adolescents, the statistical analysis did not show a significant difference in smoking prevalence between adolescents and adults ( P = 0.08).
Conclusion
In this study, adolescents with PID exhibited a higher prevalence of STIs compared to adults. Additionally, One-third of these adolescents were smokers and did not use barrier protection. PID in adolescents has distinct risk factors, causative bacteria, and clinical features compared to adults. Hence, it is crucial to develop effective strategies for treating and preventing STIs in this population.
Introduction
Pelvic inflammatory disease (PID) is the inflammation of the upper genital tract, including the uterus, fallopian tubes, and ovaries. PID often results from an ascending infection that spreads to the lower genital tract. The primary cause of PID, which accounts for approximately 50 % of cases, is sexually transmitted infections (STIs), with Chlamydia trachomatis and Neisseria gonorrhoeae being the most common pathogens involved [ , ]. STIs like Chlamydia trichomatis and N. gonorrhoeae can disrupt the normal vaginal microbiota, leading to dysbiosis. This disruption is linked to an increased risk of further infections and complications [ , ].
PID occurs most frequently in women aged 15–25 years who are sexually active [ ]. Therefore, the Centers for Disease Control and Prevention (CDC) recommends that sexually active women aged <25 years undergo screening for Chlamydia and Gonorrhea [ ].
In South Korea, the average age at the initiation of sexual intercourse among teenagers is gradually decreasing. According to the Korean CDC (KCDC) [ ], the average age at the first sexual experience is 14.1 years, typically occurring within 3–4 years after menarche. The early onset of sexual activity is often associated with multiple sexual partners, which can lead to an increased risk of various sexual health conditions, including sexually related diseases [ ]. Risk factors for PID include being under 25 years old, having multiple sexual partners, engaging in unprotected sexual intercourse, initiating sexual activity at a young age (under 15 years), having a history of STIs or previous PID, smoking, and recent insertion of an intrauterine device (IUD) [ , ]. Therefore, teenagers who have sexual experience are exposed to a higher risk of PID. And PID can lead to significant long-term complications in young patients.
In this study, we aimed to analyze the frequency of occurrence in teenagers among PID patients and compare the differences between adolescents and adults by analyzing STIs and microbiota in PID patients. Furthermore, we intend to compare the clinical characteristics among patients to analyze more common risk factors in adolescents compared to adults and explore methods to prevent PID by eliminating these risk factors.
Methods and patients
Study population
We conducted a retrospective study based on descriptive and statistical analyses of the clinical records of patients with PID who were treated with antibiotics at the Department of Obstetrics and Gynecology, College of Medicine, Inje University Busan Paik Hospital, between January 2013 and December 2023. This study was approved by the Institutional Review Board of Busan Paik Hospital, Korea (IRB No. 2024-01-035).
PID was diagnosed based on clinical symptoms and gynecological examinations. The diagnostic criteria of PID were utilized by the CDC STD guideline [ ]. PID was diagnosed if a pelvic examination revealed any of the following three minimum clinical criteria: cervical motion tenderness, uterine tenderness, or adnexal tenderness. All patients were checked for body temperature and underwent vaginal examination to identify mucopurulent cervical discharge. We collected laboratory data on C-reactive protein, white blood cells, and laboratory documentation of cervical infection with N. gonorrhoeae or C. trachomatis, Mycoplasma genitalium, Trichomonas vaginalis, Mycoplasma hominis, and Ureaplasma urealyticum . The vaginal discharge culture results were also collected.
Data analysis
We analyzed the symptoms of patients who visited an emergency department (ED) or gynecological outpatient department (OPD). We also assessed the clinical characteristics related to PID risk factors, such as smoking, history of dilation and curettage (D&C), previous PID, IUD insertion, and Human papillomavirus (HPV) infection by age. We also estimated the proportion of PID diagnoses associated with STIs, such as N. gonorrhoeae or C. trachomatis, M. genitalium, T. vaginalis, M. hominis, and U. urealyticum according to age. In addition, we also calculated the proportion of microorganisms cultured from vaginal discharge by age.
Statistical analysis
Statistical analyses were performed using MedCalc version 14.8.1 software (Frank Schoonjans, Ghent University, Belgium). Categorical variables were compared using the chi-squared test or Fisher’s exact test. The mean, median, and standard deviation were calculated for continuous variables and compared using t-tests, the Mann–Whitney U test, and Pearson’s correlation coefficients. All tests were two-sided, and the level of significance was set at P < 0.05.
Results
Clinical characteristics and risk factors related to PID by age
Three hundred patients were enrolled in the study, and out of these patients, 13 % were adolescents. The age distribution among these patients was as follows: 39 (13.0 %) were in their teens, 132 (44.0 %) were in their twenties, 62 (20.7 %) were in their thirties, and 67 patients (22.3 %) were aged ≥40 ( Supplementary Fig. 1 ). The mean age of all patients was 30.1 ± 10.4 years. Specifically, adolescent patients had a mean age of 17.4 ± 1.4 years (age range, 14–19), and patients aged ≥20 years had a mean age of 32.0 ± 9.8 years (age range, 20–63) ( Table 1 ).
| All age | adolescents (%) | Adults (%) | P value | |
|---|---|---|---|---|
| Mean age (years) | 30.1 ± 10.4 | 17.4 ± 1.4 | 32.0 ± 9.8 | |
| Median age (years) | 27 (14–63) | 18 (14–19) | 29 (20–63) | |
| BMI (g/m 2 ) | 21.5 ± 3.4 | 20.9 ± 2.5 | 21.6 ± 3.4 | 0.030 |
| Fever (°C) | 0.410 | |||
| No | 38 (97.4) | 246 (94.3) | ||
| Yes | 1 (2.6) | 15 (5.7) | ||
| Gravida | <0.001 | |||
| No | 137 (46.1) | 30 (76.9) | 107 (41.5) | |
| Yes | 160 (53.9) | 9 (23.1) | 151 (58.5) | |
| Para | <0.001 | |||
| No | 181 (60.7) | 39 (100) | 142 (54.8) | |
| Yes | 117 (39.3) | 0 (0) | 117 (45.2) | |
| Smoking | 0.008 | |||
| No | 234 (84.5) | 25 (69.4) | 209 (86.7) | |
| Yes | 43 (15.5) | 11 (30.6) | 32 (13.3) | |
| Contraceptives use | 0.064 | |||
| No | 266 (88.7) | 38 (97.4) | 228 (87.4) | |
| Yes | 34 (11.3) | 1 (2.6) | 33 (12.6) | |
| IUD | 0.074 | |||
| No | 280 (93.3) | 39 (100) | 241 (92.3) | |
| Yes | 20 (6.7) | 0 (0) | 20 (7.7) | |
| History of D&C | 0.102 | |||
| No | 213 (71.5) | 30 (76.9) | 181 (69.9) | |
| Yes | 85 (28.5) | 9 (23.1) | 78 (30.1) | |
| History of PID | 0.152 | |||
| No | 261 (87.9) | 37 (94.9) | 224 (86.8) | |
| Yes | 36 (12.1) | 2 (5.1) | 34 (13.2) | |
| Admission route | 0.523 | |||
| ED | 218 (72.7) | 30 (76.9) | 188 (72.0) | |
| OPD | 82 (27.3) | 9 (23.1) | 73 (28.0) | |
a Yang WC, Kuo HT, Lin CH et al. Tympanic temperature versus temporal temperature in patients with pyrexia and chills. Medicine (Baltimore) 2016; 95 (44): e5267. https://doi.org/10.1097/md.0000000000005267 [published Online First: 2016/11/20].
Among all patients, 34 (11.4 %) used contraception. Of patients aged ≥20 years, 12.6 % utilized contraception; however, among adolescents, only one individual (2.6 %) used oral contraceptives. All of adults who used contraception, all of them opted for IUDs ( Table 1 ).
Thirty-six patients (12.1 %) had previously experienced PID, including two adolescents (5.1 %) and 34 patients aged ≥20 years (13.2 %). Eighty-five patients (28.5 %) underwent D&C to end a pregnancy, including nine adolescents (23.1 %) and 78 patients aged ≥20 years (30.1 %). There was no statistically significant difference in the history of D&C between adolescents and adults ( P = 0.102) ( Table 1 ).
Among the patients, 43 (15.5 %) were smokers, with 11 (30.6 %) among adolescents and 32 (13.3 %) among those aged ≥20 years, indicating a higher prevalence of smoking among adolescents but not a statistically significant difference in smoking prevalence between adolescents and adults ( P = 0.08). Notably, the average age of smoking initiation among smokers was 18.6 ± 5 years, with the youngest individual starting at 13 years old (range, 13–36 years) ( Table 1 ).
Analysis of STIs according to age
Specifically, in adolescents, there was a higher prevalence of C. trachomatis ( P < 0.001 ), N. gonorrhoeae ( P = 0.001), M. genitalium ( P = 0.013) , M. hominis ( P < 0.001 ), U. urealyticum ( P = 0.004), and T. vaginalis ( P = 0.010) infections compared to adult patients ( Table 2 ). As age decreased, the proportion of STIs caused by various pathogens, including C. trachomatis, N. gonorrhoeae, T. vaginalis, M. hominis, U. urealyticum, and HPV , tended to increase ( P = 0.001, 0.005, 0.041, <0.001, 0.002, and 0.002, respectively) ( Fig. 1 ).
