Korean J Intern Med The Korean Journal of Internal Medicine 1226-3303 2005-6648 Korean Association of Internal Medicine 10.3904/kjim.2024.213 kjim-2024-213 Original Article Infectious diseases Clinical approach to sexually transmitted infections and pelvic inflammatory disease in women with acute pyelonephritis KimMi-Hee 1 AhnHyojin 2 KangSoyeon 3 LeeAhra 3 http://orcid.org/0000-0002-7603-5520 WieSeong-Heon 1 Division of Infectious Diseases, Department of Internal Medicine, St. Vincent’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea Division of Infectious Diseases Department of Internal Medicine, Daejeon St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea Department of Obstetrics and Gynecology, St. Vincent’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea Correspondence to: Seong-Heon Wie, M.D., Ph.D., Division of Infectious Diseases, Department of Internal Medicine, St. Vincent’s Hospital, College of Medicine, The Catholic University of Korea, 93 Jungbu-daero, Paldal-gu, Suwon 16247, Korea, Tel: +82-31-881-8851, Fax: +82-31-254-8898, E-mail: wiesh@catholic.ac.kr, https://orcid.org/0000-0002-7603-5520 5 2025 30 04 2025 40 3 482 490 13 06 2024 1 09 2024 7 10 2024 Copyright © 2025 The Korean Association of Internal Medicine 2025 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original work is properly cited. Background/Aims

This study aimed to investigate co-occurrence and clinical characteristics of sexually transmitted infections (STIs) and pelvic inflammatory disease (PID) in women hospitalized for acute pyelonephritis (APN).

 Methods

This single-center retrospective study reviewed medical records of inpatients with APN from January 2019 to February 2023 and identified records of 142 patients who were referred to a gynecologist to evaluate gynecological diseases including STIs.

 Results

Of the 142 patients, 47 were tested positive for sexually transmitted pathogens in nucleic acid amplification testing, confirming the presence of STIs. In patients with APN, those with STIs were more likely to have lower abdominal pain or cervical motion tenderness (CMT) on pelvic examination and leukocytosis (> 14.5 × 109/L) than those without STIs. Of the 93 patients who underwent pelvic examination, 34 had CMT with one or more of additional criteria for the clinical diagnosis of PID, such as abnormal vaginal discharge and leukorrhea confirmed by microscopic examination, which could be clinically diagnosed as PID.

 Conclusions

In sexually active women with APN, it is important to evaluate the possibility of STIs and PID, considering several risk factors such as lower abdominal pain, abnormal vaginal discharge, CMT, and leukocytosis.

 Pyelonephritis Pelvic inflammatory disease Sexually transmitted infection Graphical abstract

INTRODUCTION

Urinary tract infections (UTIs) are common bacterial infections that are more prevalent in women than in men. UTIs frequently coexist with sexually transmitted infections (STIs) in sexually active patients [1–3]. Notably, previous studies [3–7] have found that 10–50% of women with UTIs have STIs. UTIs and STIs share similar risk factors (such as sexual intercourse) with similar symptoms, including dysuria and lower abdominal pain. Therefore, it is challenging to distinguish STIs from UTIs. STIs are often ignored or underdiagnosed. Thus, they continue to spread in an undertreated state. The Centers for Disease Control and Prevention (CDC) estimated that approximately 26 million new cases of STIs occurred in the United States in 2018, with a total of 68 million infections. The economic burden of STIs is considerable. Annual direct medical costs of new infections alone totaled approximately $16 billion in the United States [8,9]. STIs can lead to severe clinical sequelae, including pelvic inflammatory disease (PID), infertility, cervical cancer, and chronic pelvic pain [7].

Therefore, early diagnosis and treatment of STIs are important and a more proactive approach to screening and evaluation is necessary in patients with UTIs.

PID is a syndrome characterized by inflammatory processes, including endometritis, salpingitis, tubo-ovarian abscess, and pelvic peritonitis. PID can be caused by vaginal flora, respiratory or enteric pathogens, and STIs, leading to infertility, ectopic pregnancy, and chronic pelvic pain, similar to effects of STIs. Symptoms and signs of PID, such as fever and abdominal pain, are similar to those of upper UTIs, such as acute pyelonephritis (APN). However, investigations on the association between APN and PID are limited [10–12].

Thus, this study aimed to investigate co-occurrence and clinical characteristics of STIs and PID in women hospitalized for APN.

 METHODS Study design

This retrospective study included patients hospitalized for nonobstructive APN at St. Vincent’s Hospital of the Catholic University in Suwon, Korea, from January 2019 to February 2023. The study protocol was approved by the Institutional Review Board (IRB) of St. Vincent’s Hospital of the Catholic University (IRB reference number: VC23RISI0205). This study was conducted in accordance with the tenets of the Declaration of Helsinki. The IRB waived the requirement for written informed consent because of its retrospective design.

 Patient population and definitions

Women aged at least 18 years with the potential for sexual activity who were admitted to St. Vincent’s Hospital with non-obstructive APN were included in this study. Criteria for diagnosing APN were: fever ≥ 38.5°C or the presence of fever or chills 24 hours before admission and the presence of at least one of the following: (1) flank pain; (2) costovertebral angle tenderness on physical examination; (3) at least one new or worsening symptom of lower UTI (dysuria, urgency, frequency, sense of residual urine, and suprapubic pain); and (4) pyuria (≥ 10 white blood cells [WBCs] per high-power field [hpf]) [13,14]. STI was diagnosed with nucleic acid amplification tests (NAATs) for six vaginal pathogens: Chlamydia trachomatis, Mycoplasma genitalium, Mycoplasma hominis, Ureaplasma urealyticum, Trichomonas vaginalis, and Neisseria gonorrhoeae. PID diagnosis required at least one of the minimum clinical criteria of CDC, including cervical motion tenderness (CMT), uterine tenderness, and adnexal tenderness on pelvic examination. Additional criteria to increase the specificity of diagnosis included the following: (1) tympanic temperature ≥ 38.3°C; (2) abnormal cervical mucopurulent discharge or cervical friability; (3) leukorrhea confirmed by microscopic examination (≥ 10 WBC/hpf in vaginal fluid); (4) elevated erythrocyte sedimentation rate; (5) elevated C-reactive protein level; and (6) laboratory documentation of cervical infection with N. gonorrhoeae or C. trachomatis [12,15]. Therefore, PID was diagnosed with CMT on pelvic examination and at least one of the additional criteria in this study.

 Data collection

We retrospectively collected data on baseline demographic characteristics, underlying diseases, and clinical signs and symptoms, including urinary and genital tract symptoms, physical examination findings, history of UTI or PID, laboratory findings, microbiological data, and time to defervescence. Results of abdominal computed tomography (CT) scans were collected for all patients. Vaginal swabs were obtained during gynecological consultations for saline microscopy, NAATs, and culture.

 Statistical methods

Categorical variables were summarized using frequencies and percentages. Continuous variables were summarized using the Mann–Whitney U-test. Chi-square test or Fisher’s exact test was performed to compare categorical data between groups. Logistic regression was used to assess risk factors for STIs. In addition, multivariable logistic regression analysis was performed to identify independent risk factors for STIs and PID in patients with APN. Statistical significance was set at p < 0.05. R version 4.2.2 (R Core Team, 2022) was used for all statistical analyses.

 RESULTS Clinical characteristics

A total of 841 patients hospitalized for APN between January 2019 and February 2023 were identified. Patients were referred for gynecological consultation for various reasons, including complaints of vaginal discomfort, such as vaginal discharge and itching, detection of gynecological abnormalities on abdominal CT, and issues related to menstruation or menopause. A total of 142 patients underwent evaluations by a gynecologist for possibility of STIs and PID. The gynecologist performed a pelvic examination and a vaginal swab test, including Gram staining, culture, and NAATs, to evaluate genital tract infections. Abdominal CT scan results for 142 patients revealed no cause of fever other than UTI. HIV and syphilis screenings were negative for all participants. Among 142 patients, 47 (33.1%) had an STI identified using NAATs, which could detect six vaginal pathogens: C. trachomatis, M. genitalium, M. hominis, U. urealyticum, T. vaginalis, and N. gonorrhoeae.

 Comparison of clinical features and laboratory results between STI-positive and -negative groups

In the comparison between STI-positive and STI-negative groups, the proportion of neuropsychiatric diseases was significantly higher in the STI-positive group (10.6% [5/47] vs. 2.1% [2/95]; odds ratio [OR], 5.5; p = 0.040) (Table 1). In the medical record review, records of lower abdominal tenderness and CMT were available for 89 and 93 patients, respectively. The number of patients with either lower abdominal tenderness or CMT was significantly higher in the STI-positive group than in the STI-negative group (71.4% [30/42] vs. 37.0% [30/81]; OR, 4.3; p < 0.001). Multiple logistic regression analysis showed that lower abdominal pain, CMT, and leukocytosis (> 14.5 × 109/L) were associated with positive NAAT results for sexually transmitted pathogens. Lower abdominal pain was identified as the most significant risk factor for STIs (OR, 8.1; 95% confidence interval [CI], 1.32–49.48) (Table 2).

 Clinical significance of CMT in APN patients

Patients with APN were divided into two groups based on the presence or absence of CMT on pelvic examination. PID could be clinically diagnosed in patients with CMT and one or more additional criteria according to clinical criteria of the CDC [15]. All 34 patients with CMT in this study met one or more of the additional criteria for clinical diagnosis of PID [12,15]. Therefore, among the 93 patients who underwent pelvic examinations in this study, all 34 patients exhibiting CMT were clinically diagnosed with PID (34/93, 36.6%). Most (30/34, 88.2%) of these 34 patients clinically diagnosed with PID exhibited one or both of the important components of the additional criteria: the presence of abnormal vaginal discharge and leukorrhea confirmed by microscopic examination (WBC ≥ 10/hpf in vaginal fluid). Among the 34 patients clinically diagnosed with PID, the proportion of patients with STIs was 44.1% (15/34), which was higher than that in patients without PID (25.4% [15/59]; OR, 2.3, p = 0.063). Multivariable logistic regression analysis showed that the presence of STIs indicated by positive NAAT results and abnormal vaginal discharge was significantly associated with PID. Moreover, a short defervescence time (≤ 2 days), long hospitalization period (≥ 10 days), and age < 40 years were risk factors for PID (Table 3).

 Distribution of six sexually transmitted pathogens in the STI-positive group of patients

Among the six sexually transmitted pathogens, U. urealyticum was the most prevalent (20%, 29/142), followed by M. hominis (15%, 21/142), C. trachomatis (6%, 8/142), M. genitalium (2%, 3/142), and T. vaginalis (2%, 3/142). N. gonorrhoeae was not detected in the present study. The proportion of patients with co-infections involving two or more pathogens was 27.7% (13/47) (Table 4).

 Comparison of clinical characteristics and outcomes by patient group with specific sexually transmitted pathogen

Table 5 shows baseline demographics, clinical characteristics, and laboratory results for patients infected with specific sexually transmitted pathogens. Of patients with five sexually transmitted pathogens, all patients with CMT met one or more of the additional criteria for clinical diagnosis of PID. Proportions of patients clinically diagnosed with PID were 50.0% (1/2), 0.0% (0/0), 66.7% (4/6), 42.9% (6/14), and 0.0% (0/1) for C. trachomatis, M. genitalium, M. hominis, U. urealyticum, and T. vaginalis, respectively (Table 5).

 DISCUSSION

Previous studies have investigated coinfection with STIs in women with UTI, with reported prevalence of coinfection in the range of 10% to 50% [3,5,6,16]. In this study, 33.1% (47/142) of patients with APN had concurrent STIs. APN with STIs was independently associated with lower abdominal pain, leukocytosis, and CMT. Of these three risk factors, lower abdominal pain was most strongly associated with STIs. Therefore, it is essential to inquire about the presence of lower abdominal pain in patients with APN to screen for STIs.

PID, a severe complication of STIs, shares overlapping clinical features with APN including fever and abdominal pain. This is attributable to ascending infections originating in the lower urinary and genital tract. However, investigations on the association between APN and PID are limited.

The prevalence of PID has been shown to be 10–14% among women of reproductive-age [17]. In the present study, the prevalence of PID, defined by the presence of CMT was estimated to be 36.6% (34/93), which was approximately twice as high as those reported in previous studies of patients without APN. In this study, a significant majority (85.3%, 29/34) of patients with APN with clinically diagnosed PID reported abnormal vaginal discharge. This proportion was notably higher than the 56% reported in a study by Mitchell and Prabhu [12], which focused on patients with endometritis and salpingitis. Furthermore, the prevalence of leukorrhea in patients with APN who were clinically diagnosed with PID was also higher in this study than that in the study by Mitchell and Prabhu [12] (41% vs. 22%). Such a high prevalence of symptoms and signs related to the genital tract observed in this study suggests that the prevalence of PID is high in APN patients.

In this study, the presence of STIs was significantly associated with PID. The OR determined by multivariable logistic regression analysis was 3.7. Previous studies have reported that N. gonorrhoeae and C. trachomatis are primary causes of PID. However, N. gonorrhoeae was not detected in the present study and C. trachomatis was present in only 6% of PID cases. Recent studies have reported a declining trend in the prevalence of N. gonorrhoeae. Non-chlamydial and non-gonococcal causes of PID have been reported to account for 9–23% of cases. Normal vaginal flora, including facultative anaerobes and enteric gram-negative rods, bacterial vaginosis-associated pathogens, and microorganisms such as M. genitalium, M. hominis, U. urealyticum, and T. vaginalis, can also cause PID [10,15]. Therefore, the presence of STIs such as M. genitalium, M. hominis, U. urealyticum, and T. vaginalis in this study appears to have a significant relationship with PID. The lower urinary tract and vagina can share urogenital microbiome. Microorganisms associated with PID encompass not only STIs, but also enteric bacteria. However, it remains unclear whether these latter entities are causative agents of PID or they were merely from an represent opportunistic growth owing to alterations in the microbiome of the upper genital tract. Nevertheless, recent studies have considered these important PID markers [11,18]. In this study, the higher prevalence of PID than the prevalence of STIs among patients with APN could be related to the microbiome in the urogenital tract.

In NAAT results of this study, the most common pathogen was U. urealyticum, which could colonize the genital tract. It is also considered an opportunistic pathogen that can cause gynecological diseases such as preterm delivery, infertility, and spontaneous abortion [19–22]. The colonization rate of U. urealyticum in the vagina ranges from 7% to 42% [23]. In this study, the proportion of U. urealyticum was 20% and the prevalence of PID in patients with APN infected with Ureaplasma urealyticum was found to be high at 44.4% (8/18). Previous studies did not provide clear evidence that U. urealyticum could cause PID. However, a previous study by Lee et al. [24] has reported that the most frequently identified pathogen is U. ureaplasma in patients with PID or Fitz-Hugh-Curtis Syndrome, accounting for 63.6% (42/66) of cases. In the present study, the prevalence of PID in patients with APN with a single U. ureaplasma infection was also high (42.9%). These results suggest that U. ureaplasma might be an important marker for PID. Therefore, if U. ureaplasma is detected in the vaginal fluid of sexually active patients with APN, the possibility of PID should be evaluated.

C. trachomatis is one of the most common STI pathogens worldwide. It can cause endometritis, PID, ectopic pregnancy, and infertility. A study conducted by Rowley et al. [25] has estimated that the global prevalence of C. trachomatis infection in women ranges from 1.5% to 7.0%, similar to the prevalence of 5.6% (8/142) found in the present study. Furthermore, 3 (60.0%) of 5 APN patients with C. trachomatis infection were clinically diagnosed with PID, presenting with CMT. In this study, the median age of patients with C. trachomatis infection was lower than that of patients infected with other pathogens. Therefore, young women with APN should be evaluated for C. trachomatis infection and PID, considering associated complications such as ectopic pregnancy and infertility.

This study has several limitations due to its retrospective design and characteristics of STIs. First, sexually transmitted pathogens identified in this study were detected in vaginal fluid samples rather than in samples collected from the upper genital tract. Therefore, the causative agent of PID could not be confirmed. However, PID is one of the severe complications of STI. A previous study has reported that the prevalence of PID among women with STIs is 94% [10]. Therefore, it is likely that STIs identified in this study are closely related to the etiology of PID. The presence of PID without detectable STIs in this study might warrant consideration of their relationships with other undetected pathogens. Further research on this aspect is necessary. Second, PID diagnosis was based on the minimum clinical criteria recommended by the CDC. Although this approach has a high sensitivity to include as many people at risk of PID as possible, it has the limitation of a low specificity. To histologically or microbiologically confirm PID, invasive procedures are necessary. However, they can lead to delays in the diagnosis and treatment of PID, increasing the burden of the disease [10]. Consequently, PID diagnosis usually relies on CDC clinical criteria. However, further histological and microbiological studies are required to better understand the pathogenesis of PID in patients with APN. Third, the 142 participants in this study were suspected of having an STI or PID. They subsequently underwent a pelvic examination or vaginal swab test by gynecologists. This could introduce a selection bias. The high prevalence of STIs or PID observed in this study might be associated with this bias. Further research is needed to more accurately determine the prevalence of STIs or PID in patients with APN.

In conclusion, it is essential to screen for concurrent STIs or PID based on clinical findings, such as abdominal pain or vaginal symptoms, when managing APN in women with potential sexual activity.

 KEY MESSAGE

1. It is necessary to screen for concurrent STIs or PID for patients with APN.

2. Lower abdominal pain in patients with APN was most strongly associated with STIs.

3. U. urealyticum was the most common NAAT result in this study. It might be an important marker for PID.

CRedit authorship contributions

Mi-Hee Kim: conceptualization, methodology, investigation, data curation, formal analysis, validation, writing - original draft, writing - review & editing, visualization; Hyojin Ahn: methodology, investigation, data curation; Soyeon Kang: methodology, investigation, data curation; Ahra Lee: methodology, investigation, data curation; Seong-Heon Wie: conceptualization, methodology, validation, writing - review & editing, supervision, funding acquisition

Conflicts of interest

The authors disclose no conflicts.

Funding

We thank the Research Institute of Medical Science at St. Vincent’s Hospital for providing financial support (SVHR-2020-06).

 REFERENCES Kim B Myung R Kim J Lee MJ Pai H Descriptive epidemiology of acute pyelonephritis in Korea, 2010–2014: population-based study J Korean Med Sci 2018 33 e310 Czajkowski K Broś-Konopielko M Teliga-Czajkowska J Urinary tract infection in women Prz Menopauzalny 2021 20 40 47 Berg E Benson DM Haraszkiewicz P Grieb J McDonald J High prevalence of sexually transmitted diseases in women with urinary infections Acad Emerg Med 1996 3 1030 1034 Moore EE Hawes SE Scholes D Boyko EJ Hughes JP Fihn SD Sexual intercourse and risk of symptomatic urinary tract infection in post-menopausal women J Gen Intern Med 2008 23 595 599 Tomas ME Getman D Donskey CJ Hecker MT Overdiagnosis of urinary tract infection and underdiagnosis of sexually transmitted infection in adult women presenting to an emergency department J Clin Microbiol 2015 53 2686 2692 Shapiro T Dalton M Hammock J Lavery R Matjucha J Salo DF The prevalence of urinary tract infections and sexually transmitted disease in women with symptoms of a simple urinary tract infection stratified by low colony count criteria Acad Emerg Med 2005 12 38 44 Behzadi P Behzadi E Pawlak-Adamska EA Urinary tract infections (UTIs) or genital tract infections (GTIs)? It’s the diagnostics that count GMS Hyg Infect Control 2019 14 Doc14 Kreisel KM Spicknall IH Gargano JW Sexually transmitted infections among US women and men: prevalence and incidence estimates, 2018 Sex Transm Dis 2021 48 208 214 Weinstock HS Kreisel KM Spicknall IH Chesson HW Miller WC STI prevalence, incidence, and costs in the United States: new estimates, new approach Sex Transm Dis 2021 48 207 Hillier SL Bernstein KT Aral S A review of the challenges and complexities in the diagnosis, etiology, epidemiology, and pathogenesis of pelvic inflammatory disease J Infect Dis 2021 224 12 Suppl 2 S23 S28 Mitchell CM Anyalechi GE Cohen CR Haggerty CL Manhart LE Hillier SL Etiology and diagnosis of pelvic inflammatory disease: looking beyond gonorrhea and chlamydia J Infect Dis 2021 224 12 Suppl 2 S29 S35 Mitchell C Prabhu M Pelvic inflammatory disease: current concepts in pathogenesis, diagnosis and treatment Infect Dis Clin North Am 2013 27 793 809 Wie SH Ki M Kim J Clinical characteristics predicting early clinical failure after 72 h of antibiotic treatment in women with community-onset acute pyelonephritis: a prospective multicentre study Clin Microbiol Infect 2014 20 O721 O729 Park JH Wee JH Choi SP Park KN Serum procalcitonin level for the prediction of severity in women with acute pyelonephritis in the ED: value of procalcitonin in acute pyelonephritis Am J Emerg Med 2013 31 1092 1097 Workowski KA Bachmann LH Chan PA Sexually transmitted infections treatment guidelines, 2021 MMWR Recomm Rep 2021 70 1 187 Huppert JS Biro F Lan D Mortensen JE Reed J Slap GB Urinary symptoms in adolescent females: STI or UTI? J Adolesc Health 2007 40 418 424 Yudin MH Hillier SL Wiesenfeld HC Krohn MA Amortegui AA Sweet RL Vaginal polymorphonuclear leukocytes and bacterial vaginosis as markers for histologic endometritis among women without symptoms of pelvic inflammatory disease Am J Obstet Gynecol 2003 188 318 323 Komesu YM Dinwiddie DL Richter HE Defining the relationship between vaginal and urinary microbiomes Am J Obstet Gynecol 2020 222 154e1 154.e10 Sprong KE Mabenge M Wright CA Govender S Ureaplasma species and preterm birth: current perspectives Crit Rev Microbiol 2020 46 169 181 Zhu CT Hu ZY Dong CL Zhang CS Wan MZ Ling Y Investigation of Ureaplasma urealyticum biovars and their relationship with antimicrobial resistance Indian J Med Microbiol 2011 29 288 292 Kokkayil P Dhawan B Ureaplasma: current perspectives Indian J Med Microbiol 2015 33 205 214 Rumyantseva T Khayrullina G Guschin A Donders G Prevalence of Ureaplasma spp. and Mycoplasma hominis in healthy women and patients with flora alterations Diagn Microbiol Infect Dis 2019 93 227 231 Kletzel HH Rotem R Barg M Michaeli J Reichman O Ureaplasma urealyticum: the role as a pathogen in women’s health, a systematic review Curr Infect Dis Rep 2018 20 33 Lee GH Kim HJ Park CH Frequency of N. gonorrheaee, C. trachomatis, U. urealyticum and M. hominis in pelvic inflammatory disease and Fitz-Hugh-Curtis syndrome Infect Chemother 2012 44 362 366 Rowley J Vander Hoorn S Korenromp E Chlamydia, gonorrhoea, trichomoniasis and syphilis: global prevalence and incidence estimates, 2016 Bull World Health Organ 2019 97 548 562 Figure and Tables

Comparison of demographic features between STI-positive and -negative groups

Variable NAAT Negative (n = 95) NAAT Positive (n = 47) OR (95% CI) p value
Age (yr) 36 (26–48.5) 38 (23.5–50) 0.591
Demographic feature
 < 30 35 (36.8) 19 (40.4) 1.2 (0.57–2.38) 0.679
 30–39 18 (18.9) 7 (14.9) 0.8 (0.29–1.94) 0.551
 40–49 20 (21.1) 7 (14.9) 0.7 (0.26–1.68) 0.379
 50–59 14 (14.7) 13 (27.7) 2.2 (0.94–5.20) 0.065
 ≥ 60 8 (8.4) 1 (2.1) 0.2 (0.03–1.95) 0.272
Comorbidities
 DM 13 (13.7) 5 (10.6) 0.8 (0.25–2.25) 0.608
 HTN 14 (14.7) 6 (12.8) 0.9 (0.30–2.37) 0.751
 Cancer 6 (6.3) 0 (0.0)
 Thyroid disease 7 (7.4) 2 (4.3) 0.6 (0.11–2.80) 0.718
 Autoimmune disease 2 (2.1) 4 (8.5) 4.3 (0.76–24.53) 0.093
 Neuropsychiatric disease 2 (2.1) 5 (10.6) 5.5 (1.03–29.70) 0.040
 Gynecologic disease 4 (4.2) 2 (4.3) 1.0 (0.18–5.73) > 0.999
 Urologic disease 5 (5.3) 3 (6.4) 1.2 (0.28–5.37) > 0.999
 PID history 7 (7.4) 2 (4.3) 0.6 (0.11–2.80) 0.718
 UTI history 26 (27.4) 15 (31.9) 1.2 (0.58–2.66) 0.574

Values are presented as median (interquartile range) or number (%).

STI, sexually transmitted infection; NAAT, nucleic acid amplification test; OR, odds ratio; CI, confidence interval; DM, diabetes mellitus; HTN, hypertension; PID, pelvic inflammatory disease; UTI, urinary tract infection.

Comparison of clinical features and laboratory results between STI-positive and STI-negative groups

Variable NAAT Negative (n = 95) NAAT Positive (n = 47) Univariable Multivariable
OR (95% CI) p value OR (95% CI) p value
Clinical features
 Body temperature ≥ 39°C 43 (45.3) 15 (31.9) 0.6 (0.27–1.18) 0.128
 Defervescent time ≤ 4 days 78/92 (84.8) 43/47 (91.5) 1.9 (0.60–6.23) 0.301
 Bacteremia 10/94 (10.6) 6/47 (12.8) 1.2 (0.42–3.615) 0.707
 Hospitalization period > 7 days 70 (73.7) 32 (68.1) 0.8 (0.36–1.64) 0.485
 Symptoms of UTI 50 (52.6) 29 (61.7) 1.5 (0.71–2.96) 0.306
 Flank pain 70 (73.7) 36 (76.6) 1.2 (0.52–2.64) 0.707
 CVA tenderness 86 (90.5) 43 (91.5) 1.1 (0.33–3.86) 1.000
 Lower abdominal pain 50 (52.6) 31 (66.0) 1.7 (0.84–3.60) 0.131 8.1 (1.32–49.48) 0.024
 LAT 17/56 (30.4) 18/33 (54.5) 2.8 (1.13–6.71) 0.024 1.4 (0.31–6.12) 0.670
 CMT 19/63 (30.2) 15/30 (50.0) 2.3 (0.95–5.67) 0.063 5.4 (1.28–22.53) 0.022
 LAT or CMT 30/81 (37.0) 30/42 (71.4) 4.3 (1.90–9.53) < 0.001
 Abnormal vaginal discharge 60 (63.2) 29 (61.7) 0.9 (0.46–1.93) 0.866 0.3 (0.05–1.22) 0.086
Laboratory value
 WBC > 14.5 × 109/L 24 (25.3) 21 (44.7) 2.4 (1.12–5.00) 0.019 5.2 (1.08–24.79) 0.040
 ESR > 34 mm/h 68/93 (73.1) 29/46 (63.0) 0.6 (0.30–1.33) 0.224
 CRP > 4 mg/dL 80 (84.2) 32 (68.1) 0.4 (0.18–0.91) 0.027 0.8 (0.16–3.90) 0.779

Values are presented as number (%).

STI, sexually transmitted infection; NAAT, nucleic acid amplification test; OR, odds ratio; CI, confidence interval; UTI, urinary tract infection; CVA, costovertebral angle; LAT, lower abdominal tenderness; CMT, cervical motion tenderness; WBC, white blood cell; ESR, erythrocyte sedimentation rate; CRP, C-reactive protein.

Comparison of clinical features and laboratory results between APN patients with and without PID

Variable PID (−)(n = 59) PID (+)(n = 34) Univariable Multivariable
OR (95% CI) p value OR (95% CI) p value
Demographic feature
 Age < 40 yr 30 (50.8) 25 (73.5) 2.7 (1.07–6.72) 0.032 4.8 (1.41–16.14) 0.012
Clinical features
 Body temperature > 38.3°C 36 (61.0) 25 (73.5) 1.8 (0.70–4.47) 0.221
 Defervescence time ≤ 2 days 20/58 (34.5) 18/33 (54.5) 2.3 (0.95–5.46) 0.062 3.3 (1.14–9.60) 0.027
 Hospitalization period ≥ 10 days 20 (33.9) 13 (38.2) 1.2 (0.50–2.90) 0.637 4.0 (1.09–14.69) 0.037
 Symptoms of UTI 37 (62.7) 18 (52.9) 0.7 (0.28–1.57) 0.356
 Flank pain 44 (74.6) 24 (70.6) 0.8 (0.32–2.10) 0.676
 CVA tenderness 53 (89.8) 30 (88.2) 0.9 (0.22–3.25) 1.000
 Lower abdominal pain 32 (54.2) 22 (64.7) 1.6 (0.65–3.69) 0.325 0.6 (0.18–1.68) 0.293
 Lower abdominal tenderness 13/38 (34.2) 9/21 (42.9) 1.4 (0.48–4.31) 0.511
 Abnormal vaginal discharge 35 (59.3) 29 (85.3) 4.0 (1.35–11.73) 0.009 6.2 (1.68–22.69) 0.006
 Abnormal vaginal discharge or Leukorrheaa) 43 (72.9) 30 (88.2) 2.8 (0.85–9.18) 0.116
Laboratory results
 Positive NAAT for STI 15 (25.4) 15 (44.1) 2.3 (0.95–5.67) 0.063 3.7 (1.20–11.25) 0.022
 Leukorrheaa) 23 (39.0) 14 (41.2) 1.1 (0.45–2.52) 0.886
 WBC > 15.0 ×109/L 15 (25.4) 13 (38.2) 1.8 (0.73–4.50) 0.195
 ESR > 70 mm/h 16/57 (28.1) 4/34 (11.8) 0.3 (0.10–1.13) 0.115
 CRP > 5 mg/dL 47 (79.7) 21 (61.8) 0.4 (0.16–1.05) 0.061

Values are presented as number (%).

APN, acute pyelonephritis; PID, pelvic inflammatory disease; OR, odds ratio; CI, confidence interval; UTI, urinary tract infection; CVA, costovertebral angle; NAAT, nucleic acid amplification test; STI, sexually transmitted infection; WBC, white blood cell; ESR, erythrocyte sedimentation rate; CRP, C-reactive protein; hpf, high-power field.

Leukorrhea was defined as WBC count ≥ 10/hpf in the vaginal fluid on microscopic examination.

Distribution of five sexually transmitted pathogens

Variable Value (n = 142)
Single 34 (23.9)
 CT 2 (5.9)
 MG 1 (2.9)
 MH 9 (26.5)
 UU 21 (61.8)
 TV 1 (2.9)
Multiple 13 (9.2)
 CT + MH 5 (38.5)
 CT + UU 1 (7.7)
 MG + MH + UU 1 (7.7)
 MG + MH + UU + TV 1 (7.7)
 MH + UU + TV 1 (7.7)
 MH + UU 4 (30.8)

CT, Chlamydia trachomatis; MG, Mycoplasma genitalium; MH, Mycoplasma hominis; UU, Ureaplasma urealyticum; TV, Trichomonas vaginalis.

Comparison of clinical characteristics for diagnosing PID among patients with five sexually transmitted pathogens

Variable Chlamydia trachomatis Mycoplasma genitalium Mycoplasma hominis Ureaplasma urealyticum Trichomonas vaginalis
Total 8 (5.6) 3 (2.1) 21 (14.8) 29 (20.4) 3 (2.1)
Demographic feature
 Age (yr) 24.5 (21.3–25.0) 44 (33.5–48.5) 38 (25.0–51.0) 38 (23.0–51.0) 53 (52.3–53.0)
Clinical features
 Patients with UTI symptoms 5 (62.5) 3 (100.0) 14 (66.7) 17 (58.6) 2 (66.7)
 Lower abdominal pain 4 (50.0) 2 (66.7) 13 (61.9) 19 (65.5) 2 (66.7)
 CMT 3/5 (60.0) 1/1 (100.0) 8/13 (61.5) 8/18 (44.4) 0/1 (0.0)
 LAT 1/5 (20.0) 1/3 (33.3) 9/18 (50.0) 11/19 (57.9) 0/1 (0.0)
 CMT or LAT 4/6 (66.7) 2/3 (66.7) 15/19 (78.9) 17/25 (68.0) 0/2 (0.0)
 Renal abscess 3 (37.5) 3 (100.0) 9 (42.9) 7 (24.1) 1 (33.3)
Additional criteria of the clinical diagnosis for PIDa)
 Patients with BT > 38.3°C 8 (100.0) 2 (66.7) 17 (81.0) 18 (62.1) 2 (66.7)
 Abnormal vaginal discharge 4 (50.0) 2 (66.7) 13 (61.9) 17 (58.6) 2 (66.7)
 Leukorrheab) 5 (62.5) 2 (66.7) 7 (33.3) 10 (34.5) 1 (33.3)
 ESR > 15 mm/h 7 (87.5) 3 (100.0) 20 (95.2) 25/28 (89.3) 3 (100.0)
 CRP > 0.5 mg/dL 8 (100.0) 3 (100.0) 20 (95.2) 29 (100.0) 3 (100.0)
Clinical diagnosis for PIDa) in patients with single infection
 CMT in patients with single infection 1/2 (50.0) 0/0 (0.0) 4/6 (66.7) 6/14 (42.9) 0/1 (0.0)

Values are presented as number (%) or median (interquartile range).

PID, pelvic inflammatory disease; UTI, urinary tract infection; CMT, cervical motion tenderness; LAT, Lower abdominal tenderness; BT, body temperature; ESR, erythrocyte sedimentation rate; CRP, C-reactive protein; CDC, Centers for Disease Control and Prevention; hpf, high-power field.

In the CDC’s sexually transmitted infection treatment guidelines 2021, additional criteria for the clinical diagnosis of PID included a tympanic temperature of ≥ 38.3°C, abnormal cervical mucopurulent discharge or cervical friability, presence of abundant numbers of white blood cell on saline microscopy of vaginal fluid, elevated erythrocyte sedimentation rate, elevated CRP, and laboratory documentation of cervical infection with Neisseria gonorrhoeae or Chlamydia trachomatis [15].

Leukorrhea was defined as a WBC count ≥ 10/hpf in the vaginal fluid on microscopic examination.