a b s t r a c t

Introduction: Tubo-ovarian abscess (TOA) is a rare but Serious condition that carries with it a high rate of morbid- ity and even mortality.

Objective: This review highlights the pearls and pitfalls of TOA, including diagnosis, Initial resuscitation, and man- agement in the emergency department (ED) based on current evidence.

Discussion: TOA is associated with pelvic inflammatory disease (PID) as well as intrauterine devices, uterine pro- cedures, multiple sexual partners, diabetes mellitus, and immunocompromised states. While usually arising from a gynecologic infection, TOA can be associated with a gastrointestinal source. History and physical examination are limited, demonstrating predominantly lower abdominal pain, but a minority of patients will present with vaginal symptoms. Half of patients will exhibit systemic illness to include fever, nausea, and vomiting. Laboratory evaluation may reveal elevations in white blood cell count and other inflammatory markers. Transvaginal ultra- sound and computed tomography (CT) may be utilized for diagnosis, though CT has higher sensitivity and can differentiate this disease from similarly presenting gastrointestinal pathology. Initial medical management in- cludes antibiotics. Surgical intervention is indicated in those who fail initial medical therapy, which is more likely in those with bilateral abscesses, large abscesses, and older patients.

Conclusions: An understanding of TOA can assist emergency clinicians in diagnosing and managing this poten- tially deadly disease.

Published by Elsevier Inc.

1. Introduction

This article series addresses high risk and low prevalence diseases that are encountered in the emergency department (ED). Much of the primary literature evaluating these conditions is not emergency medicine focused. By their very nature, many of these Disease states and clinical presentations have little useful evidence available to guide the emergency physician in diagnosis and management. The format of each article defines the disease or clinical presentation to be reviewed, provides an overview of the extent of what we cur- rently understand, and finally discusses pearls and pitfalls using a question and answer format. This article will discuss tubo-ovarian abscess (TOA). This condition’s low prevalence but high morbidity and mortality, as well as its variable atypical Patient presentations and challenging diagnosis, makes it a high risk and low prevalence disease.

* Corresponding author at: 3841 Roger Brooke Dr, Fort Sam Houston, TX 78234, USA.

E-mail address: [email protected] (B. Long).

• 1. Definition

TOA is an inflammatory infectious mass including the fallopian tube, ovary, and in severe cases, other pelvic organs such as the bowel and bladder [1-3]. This mass may present as a tubo-ovarian complex with agglutination of these structures or as a collection of pus. TOA most commonly results from ascending infection with sexually transmitted infection or vaginal flora, but it may also occur due to a secondary infec- tion from the gastrointestinal (GI) system or from another condition such as pelvic organ cancer [1-8].

The most common predisposing condition of TOA is pelvic inflam- matory disease (PID) in premenopausal patients, which occurred in 15-35% of PID cases before current diagnostic criteria and treatment with antibiotics [1,2,5,9-11]. In the current era with improved diagnosis and treatment of PID, the rate of TOA complicating PID approximates 2% [1-3,5-7]. In postmenopausal patients, there is a high rate of concurrent malignancy [12-15]. Ascending infection progresses to endothelial dam- age of the fallopian tube and edema of the infundibulum, leading to tubal blockage and development of pyosalpinx if left untreated. This progresses to further tissue invasion, destruction, edema, and finally tis- sue ischemia and necrosis, leading to coalescence of tissues and

https://doi.org/10.1016/j.ajem.2022.04.026 0735-6757/Published by Elsevier Inc.

development of TOA [2,3,5,6]. TOAs are typically polymicrobial, with similar bacteria to those present in uncomplicated PID; however, aero- bic, facultative, and anaerobic bacteria have been isolated from TOA [1-3,6,8]. Immunocompromised patients may experience TOA due to atypical organisms including Candida, Mycobacterium tuberculosis, Pasteurella, and Streptococcus pneumoniae [16-19].

There are few data regarding the incidence of TOA. Over 200,000 women are hospitalized annually for PID, and a significant number of these patients hospitalized for PID will be diagnosed with a TOA [8,20-22]. Women between the ages of 15-40 years are most commonly affected [6,8,21,23]. Unfortunately, if this condition is missed, the abscess can rupture, occurring in 15% of cases [21,23]. Sepsis can occur in 10-20% of patients with TOA, with mortality rates approaching 50% before the advent of current treatments [21,23-26]. Current mortal- ity rates with appropriate treatment approach 0%, but rupture is associ- ated with a mortality rate up to 4%, even with modern therapies [6,23,25,26]. Other complications include infertility and chronic pelvic pain [6,27-29].

1. Discussion
   1. Presentation

TOA is most commonly a complication of PID and may present with lower abdominal pain, chills, fever, and vaginal discharge [1-3,6,8,21]. The majority of patients are hemodynamically stable with no clear evi- dence of sepsis if the TOA has not ruptured; however, TOA should be suspected in those who are acutely ill, have significant abdominal or pelvic tenderness, have an adnexal mass present on examination, or who present after failed therapy for PID [1-3,6,8,21]. Patients can pres- ent acutely or with longer term symptoms. Rupture of the TOA may result in peritonitis and sepsis [1-3,6,26].

• 1. ED evaluation

Assessment in the ED setting includes pregnancy testing and evalu- ation for PID with testing for N. gonorrheae and Chlamydia trachomatis. complete blood cell count and inflammatory markers such as erythrocyte sedimentation rate and C-reactive protein (CRP) may assist [1-3,6,21,30-33]. In the setting of sepsis, a toxic-appearing patient, or suspected TOA rupture, blood cultures should be obtained [6]. If the clinician suspects TOA, imaging is warranted [2,3,6,34]. Ultra- sound (US) or computed tomography (CT) with contrast may be uti- lized for diagnosis [6,34]. US is often the first-line modality and may demonstrate complex multilocular masses disrupting normal adnexal

Fig. 1. Transvaginal US. The right adnexa contains a complex, predominantly cystic mass consistent with a TOA. Case courtesy of RMH Core Conditions, Radiopaedia.org, rID: 26157.

architecture (Fig. 1), though CT has greater sensitivity [2,3,6,34-36]. CT may demonstrate multilocular, rim-enhancing, thick-walled adnexal masses (Fig. 2) [27,28]. CT can also demonstrate signs of abscess rupture such as free abdominopelvic fluid [6,27,28].

• 1. ED management

In those who have evidence of sepsis or rupture, resuscitation and broad-spectrum antibiotics with obstetric/gynecology (OBGYN) consul- tation are recommended, as surgical intervention is necessary [1-3,6]. Surgical intervention is also commonly required if the abscess is over 7 cm in diameter [1-3,6,8,26,37]. Premenopausal patients who are he- modynamically stable with no evidence of rupture and Abscess size

<=7 cm in diameter respond to intravenous antibiotics alone in up to 70% of cases without need for image-guided drainage or surgery [2,6,38,39]. Once patients clinically improve, IV antibiotics are transi- tioned to per os (PO) for at least 14 days [2,6,37]. If patients do not im- prove with antibiotics but are not clinically declining, image-guided drainage can be utilized, but if clinical decline is present, surgical treat- ment is recommended [2,6,37]. For postmenopausal patients, surgical diagnosis and management with antibiotics are more commonly uti- lized due to the risk of concurrent gynecologic malignancy [12].

1. Pearls and pitfalls
   1. What risk factors are associated with TOA beyond PID?

While PID is the most common risk factor for TOAs, other factors in- clude the presence of intrauterine contraceptive devices, recent Uterine procedures such as hysteroscopy, multiple sexual partners, diabetes, and immunocompromised states including inflammatory bowel disease [2,3,6,35,40]. Other reports describe TOA after abdominal or pelvic sur- gery including total abdominal hysterectomy, endometrial ablation, Transvaginal ultrasonographic-guided oocyte retrieval and transcervical embryo transfer, and animal bites [6,41-46]. Patients with human im- munodeficiency virus (HIV) are more likely to develop TOA, compared to those without HIV [47,48]. Endometriosis is also associated with more severe PID and higher rates of TOA [6,49]. TOAs have been re- ported in females who are not sexually active, and while the source may not always be identified, it may arise from conditions affecting the GI or Genitourinary system (appendicitis, diverticulitis, or pyelone- phritis), or be associated with pelvic organ cancer [4,6,50,51]. Addition- ally, chronic bacterial infection may predispose patients to TOA, with documented TOAs secondary to Brucellosis, Salmonella typhi, and Burkholderia pseudomallei [52-55]. Postmenopausal patients with TOA have a high rate of associated malignancy [12-15].

• 1. What are the limitations of the history and examination?

History and examination findings in TOA can overlap with a myriad of other diagnoses. The majority of patients (89%) will present with lower abdominal pain. Fever occurs in 50-90% of patients, chills in 50%, nausea in 26%, vaginal discharge in 28%, and abnormal Vaginal bleeding in 21% [2,3,6,8]. Diarrhea can also occur. Fever is less likely in PID and suggests TOA [6]. In severe cases, ureteral obstruction may re- sult in hydronephrosis and flank or back pain. A TOA resulting in intes- tinal obstruction may present with abdominal distension and GI symptoms [56,57]. While most patients will present with lower abdom- inal pain, approximately a quarter will have genitourinary symptoms [6,8], making this diagnosis challenging based on historical factors.

Physical examination similarly lends limited information, though all patients should undergo examination including a speculum and biman- ual examination, which may display mucopurulent discharge or cervical motion tenderness, representative of underlying PID [2,3,6,8]. Bimanual examination with adnexal or uterine tenderness may suggest TOA [3,6]. However, in retrospective analysis of 93 patients with PID complicated

Fig. 2. A) CT axial slice demonstrating TOA. B) CT coronal slice demonstrating TOA. Extensive inflammatory change in the lower abdomen and pelvis, with an IUD in place. Mural thickening and enhancement of a tubular structure in the right adnexa, adjacent to a collection with enhancing margins, consistent with TOA. Case courtesy of Dr. Vikas Shah, Radiopaedia.org, rID: 54792.

by TOA, no specific physical examination factor, including peritoneal ir- ritation and abnormal vaginal discharge, was associated with poor clin- ical course on logistic regression analysis [58]. Congruent to vague symptoms, the examination in TOA can generate a wide differential, rendering it a challenging ED diagnosis requiring careful consideration.

• 1. What are limitations of Laboratory analysis?

Laboratory analysis in TOA can predict illness severity, though the associated markers are non-specific. The most commonly associated laboratory markers include elevated white blood cell count, ESR, and CRP [2,3,6,8]. Leukocytosis may be present but is non-specific with a re- ceiver operator curve of 0.58, demonstrating its limited utility [31]. However, elevated ESR and CRP possessed greater Diagnostic ability based on receiver operator curve analysis, 0.87 and 0.73, respectively. ESR with a threshold of 19.5 mm/h has a sensitivity and specificity of 79% and 83%, respectively, while a CRP threshold of 11.5 mg/L has a sen- sitivity and specificity of 72% and 63%, respectively [31]. These elevated inflammatory markers are predictive of more severe illness and longer hospital stay, though they are non-specific and will be elevated in many patients with an infection requiring admission [31]. Specifically, a CRP over 49.3 mg/L in a patient with PID suggests the presence of a TOA with a sensitivity of 85.4% and a specificity of 93.4% [33]. In evalu- ating other inflammatory markers, procalcitonin has limited utility in its diagnostic or prognostic value in TOA [59].

• 1. What imaging modalities may be used for diagnosis?

US or CT with contrast may be utilized for diagnosis of TOA [2,3,6,34]. US is not associated with radiation, while CT may add addi- tional value, especially in evaluating other pathologies with similar pre- sentations. Literature suggests transvaginal US may be more accurate than transabdominal US in identifying adnexal lesions and masses [60-62]. A cross sectional comparative study of 50 patients found transvaginal US compared to transabdominal US was superior in identi- fying cystic teratomas (100% vs. 40%), endometriomas (90% vs. 57.1%), hemorrhagic ovarian cysts (85.7% vs. 50%), hydrosalpinx(75% vs. 25%), pyosalpinx/tubo-ovarian mass(75% vs. 75%), and Ectopic pregnancy (100% vs. 77.7%) [60]. A second study found transvaginal US to be supe- rior to transabdominal US in 63% of cases [62]. Transvaginal US may demonstrate a complex adnexal structure with thick walls and internal

echogenicity representing purulent material and cellular debris [2,6,63]. Incomplete septae within the fallopian tubes is indicative of acute tubal inflammation, and thickened endosalpingeal folds may be present on US, known as the ‘cogwheel sign’ [64-66]. Additionally, complex free fluid may be present in the pouch of Douglas, and dirty shadowing may be seen which represents foci of air within the abscess [2,65,67]. However, Transvaginal ultrasound has a sensitivity ranging from 75 to 90% and is operator dependent, which may require further imaging if definitive diagnosis is not made on ultrasound [2,8,63-66].

Compared with US, CT with contrast demonstrates greater sensitiv- ity (78-100% for CT compared with 75-90% for US) [2,3,27,28,34,35,68]. If obtaining CT for suspected TOA, discussion with the radiologist is rec- ommended. Intravenous contrast is recommended, but the addition of oral contrast to improve sensitivity and specificity is controversial [27,28,34]. CT allows for visualization of both the salpinx as well as the ovaries in addition to the surrounding GI tract and can evaluate for other conditions. CT may demonstrate uniformly thickened and en- hanced abscess wall in 95% of cases, increased fluid density within the abscess in 95%, and multilocular fluid collection in 89% of cases [6,27,28]. CT can also demonstrate satellite lesions adjacent to the pri- mary abscess, anteriorly displaced round ligament, and peripherally en- hancing low-density pelvic masses [68]. Thickened, fluid-filled tubes consistent with pyosalpinx can be present in up to half of cases, as well as incomplete septae present in the fallopian tube [27,28]. CT can help differentiate TOA from periappendicular abscess, the latter of which is managed by percutaneous drainage with subsequent appen- dectomy [6,28,68]. Other CT findings include bowel wall thickening and infiltration of pelvic fat, while ascites is an uncommon finding [27,28,68].

MRI can be utilized, particularly in pregnant patients if US is incon- clusive or unavailable. A TOA will appear with low signal intensity on T1 weighted imaging and high signal intensity on T2 weighted imaging [6,29,69]. MRI has a sensitivity approaching 95% and specificity close to 81% for diagnosis [6,29,69], but this modality is not available in all ED settings.

• 1. What antibiotics should be utilized?

Parenteral antibiotics should be rapidly initiated to cover both sexu- ally transmitted infections including N. gonorrheae and Chlamydia trachomatis as well as polymicrobial GI bacteria including Escherichia

Table 1

antibiotic regimens for TOA [37].

Ceftriaxone 1 g daily + doxycycline 100 mg every 12 h + metronidazole 500 mg every 12 h

or

Cefotetan 2 g every 12 h + doxycycline 100 mg every 12 h or

Cefoxitin 2 g every 6 h + doxycycline 100 mg every 12 h or

Ampicillin-sulbactam 3 g every 6 h + doxycycline 100 mg every 12 h For those with severe cephalosporin allergy:

Clindamycin 900 mg every 8 h + gentamicin 2 mg/kg load then 1.5 mg/kg every 8 h

coli, Bacterioides fragilis, Prevotella, and anaerobic streptococci species [6,37]. Recommended antibiotic regimens are included in Table 1.

• 1. Which patient with TOA requires surgical intervention?

If TOA is diagnosed, consultation with the OBGYN specialist is rec- ommended. Drainage of an abscess without rupture can include lapa- rotomy, percutaneous drainage, or colpotomy incision [1-3,6,70]. However, rupture necessitates emergent operative management and can occur spontaneously into the bladder, colon, peritoneum, or rectum [1-3,6]. Rupture into the vaginal vault is rare.

Traditionally, unruptured TOAs were treated with IV antibiotics for the initial 72 h, but this may fail in 25-30% of cases [70-72]. In a Retro- spective analysis of 163 TOA patients, factors associated with failed medical management included larger abscess size, older age, parity, and initially elevated white blood cell count [1,2,71-75]. An additional study identified these factors as well as the presence of bilateral ab- scesses predicted increased rate of medical management failure [74]. Abscess features associated with need for surgical management include abscess diameter exceeding 5 cm and volume exceeding 40 cm³ based on one study [71]. Another study found abscesses larger than 7 cm are associated with need for surgical intervention, longer hospital stay, and increased complication rates [38].

A scoring system has been proposed to predict medical management failure, which incorporates temperature, CRP, and TOA diameter (Table 2) [76]. In this study including a total of 214 consecutive patients, a score >= 4 was predictive of the need for surgical or radiological inter- vention, with a sensitivity of 69%, specificity of 88%, and area under the curve of 0.859 [76]. However, further validation of this score is required before routine clinical use.

• 1. What are considerations if the patient is pregnant or has an intrauterine device?

TOA is rare is pregnancy, but it can lead to adverse outcomes includ- ing preterm labor, miscarriage, chorioamnionitis, and fetal or maternal death [6,77,78]. An appendiceal abscess is more common than TOA in pregnancy [6]. The approach to diagnosis and management is similar in pregnant and nonpregnant patients, though US or MRI are recom- mended if available. If these are non-diagnostic or unavailable, CT is rec- ommended. Consultation with the OBGYN specialist is necessary, as early delivery may be necessary, and surgical management is associated with greater risk to the fetus and mother [79].

Table 2

TOA predictive risk score for medical management failure [76].

Components	Points
	0	1	2	3
Temperature (?C) TOA size (cm) CRP (mg/L)	<37 <5.5 <250	>=37 but <38 >=5.5 but <8.5 –	>=38 but <38.5 >=8.5 but <10.5 >=250	>=38.5 >=10.5 –

Table 3

Summary of TOA pearls and pitfalls.

• • • Key risk factors to consider for TOA include PID, presence of IUD, multiple sexual partners, DM, and immunocompromised states.
    • History and physical examination are non-specific; TOA should be considered in the female patient with lower abdominal pain and fever/chills.
    • Elevations in CRP can be a predictor of more severe disease though elevations in inflammatory markers are non-specific.
    • US and CT can be used for diagnosis, though CT has higher sensitivity.
    • Management includes consultation with the OBGYN specialist and adminis- tration of parenteral antibiotics covering Sexually transmitted infections and polymicrobial gastrointestinal bacteria.
    • Factors associated with failed medical management include larger abscess size or bilateral abscesses, fever, older age, parity, and significantly elevated inflammatory markers on laboratory evaluation.

Intrauterine devices (IUD) are associated with risk of TOA [1-3,6]. If an IUD is present in the setting of TOA, removal by the OBGYN specialist is often performed, as removal is associated with improved Short-term outcomes [69]. However, removal must be balanced with the risk of pregnancy in patients who have had intercourse in the prior 5 days. Of note, there is an association between IUDs and Actinomyces [6,67,69]. Tubo-ovarian actinomycosis is associated with the formation of multi- ple abscesses, granulation tissue, and fibrosis [6,67,69]. This will demon- strate predominantly solid-appearing areas with Contrast enhancement on imaging, and the infection will respond to standard therapies [69].

Table 3 provides a summary of pearls and pitfalls in the evaluation and management of TOA.

1. Conclusions

TOA occurs as an inflammatory consequence of purulence within the tubo-ovarian complex. Most commonly a complication of PID, TOA can arise secondary to GI etiologies as well as systemic bacterial infections. Physical examination is non-specific, as most women display lower ab- dominal pain, but only a quarter will have vaginal discharge. Laboratory analysis may show elevated inflammatory markers though these are non-specific. Transvaginal US or CT may be utilized for diagnosis. In con- junction with gynecology consultation, prompt medical management should include a second or third generation cephalosporin with doxycy- cline plus metronidazole to target common sexually transmitted infec- tions and GI flora. Surgical intervention should be considered in those who have larger abscesses exceeding 5 cm, bilateral abscesses, older pa- tients, and those who fail medical management.

Credit authorship contribution statement

Rachel E. Bridwell: Writing – review & editing, Writing – original draft, Validation. Alex Koyfman: Supervision, Conceptualization. Brit Long: Writing – review & editing, Writing – original draft, Supervision, Conceptualization.

Declaration of Competing Interest

None.

Acknowledgements

BL, RE, and AK conceived the idea for this manuscript and contrib- uted substantially to the writing and editing of the review. This manu- script did not utilize any grants, and it has not been presented in abstract form. This clinical review has not been published, it is not under consideration for publication elsewhere, its publication is approved by all authors and tacitly or explicitly by the responsible authorities where the work was carried out, and that, if accepted, it will not be published elsewhere in the same form, in English or in any other language, includ- ing electronically without the written consent of the copyright-holder.

This review does not reflect the views or opinions of the U.S. govern- ment, Department of Defense, U.S. Army, U.S. Air Force, or SAUSHEC EM Residency Program.

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