
==== Front
Investig Clin Urol
Investig Clin Urol
ICU
Investigative and Clinical Urology
2466-0493
2466-054X
The Korean Urological Association

39249921
10.4111/icu.20240152
Original Article
Infection/Inflammation
Occurrence of liver abscess in patients with acute prostatitis
https://orcid.org/0000-0003-0650-7569
Choi Jeonghyouk
https://orcid.org/0000-0001-7369-9252
Lee Dong-Gi
Department of Urology, Kyung Hee University College of Medicine, Seoul, Korea.
Corresponding Author: Dong-Gi Lee. Department of Urology, Kyung Hee University Hospital at Gangdong, Kyung Hee University College of Medicine, 892 Dongnam-ro, Gangdong-gu, Seoul 05278, Korea. TEL: +82-2-440-7735, FAX: +82-2-440-7744, drpedurology@gmail.com
9 2024
21 8 2024
65 5 480486
08 5 2024
12 6 2024
15 7 2024
© The Korean Urological Association
2024
The Korean Urological Association
https://creativecommons.org/licenses/by-nc/4.0/ 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 non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Purpose

Liver abscesses concomitant with acute prostatitis are rare and potentially fatal. We analyzed the occurrence of this condition and clinical characteristics of the affected patients.

Materials and Methods

The medical records of 474 patients diagnosed with acute prostatitis between June 2006 and July 2022 were retrospectively reviewed. Patients in whom pathogens were not detected in serum or urine cultures were excluded. A total of 271 patients were included in the analysis. Patient characteristics and laboratory test results were compared between patients with acute prostatitis with and without liver abscesses.

Results

Fifteen patients (5.5%) were identified with simultaneous liver abscesses and acute prostatitis. The liver abscess group was younger than the non-liver abscess group in terms of mean age. In the univariate analysis, a high proportion of patients had diabetes mellitus, whereas a low proportion had hypertension. None of the underlying diseases, including benign prostatic hyperplasia, malignancy, or alcoholism, demonstrated a significant association with liver abscess in multivariate analysis; however, an association was observed in liver function test results. All patients with liver abscesses tested positive for Klebsiella pneumoniae.

Conclusions

When K. pneumoniae is identified in patients with acute prostatitis and abnormal liver function tests, considering the possibility of metastatic infection in other organs, including the liver, and performing an active evaluation is essential.

Graphical Abstract

Klebsiella pneumoniae
Liver abscess
Prostatitis
==== Body
pmcINTRODUCTION

Acute prostatitis (AP) is characterized by lower urinary tract symptoms such as dysuria, urinary frequency, and tenesmus, as well as systemic manifestations including fever and chills. Although AP accounts for only 5% of all prostatitis cases [1], if not properly treated, the disease can worsen significantly or become chronic. Diabetes mellitus (DM), liver cirrhosis, immune suppression, unprotected sexual intercourse, and phimosis are known risk factors for acute bacterial prostatitis [2]. Urinary interventions, such as transrectal prostate biopsy and indwelling urethral catheters, can also cause AP [123]. This disease can be easily diagnosed clinically or through urine culture and is usually treated with antibiotics for 2–4 weeks [4]. Escherichia coli is the primary causative organism of AP (50%–80%), followed by Enterobacteriaceae including Klebsiella and Proteus [56]. Among these, Klebsiella pneumoniae (KP) is the second most common pathogen causing prostate abscesses in South Korea [78].

Liver abscesses are generally caused by bacteria and are associated with various types of liver cancer. The annual incidence rate in the United States is 2.9–3.59/100,000 person-years; however, in Taiwan, the incidence is significantly higher at 17.59/100,000 person-years [910]. Invasive liver abscess syndrome is defined as the development of extrahepatic metastatic infection at distant sites in the presence of a liver abscess [1112]. Metastatic infections manifest as endophthalmitis, meningitis, lung abscess, otitis media, and prostate infection [13]. The incidence of liver abscess syndrome is high in East Asian countries, such as Taiwan and South Korea, and is known to be mainly caused by KP [14] unlike in Western countries, where E. coli is the main pathogen. Caution is required for this disease owing to its high morbidity and mortality [15].

Liver abscesses are uncommon in patients with AP, making differentiation challenging owing to similar systemic symptoms, such as fever and myalgia. As liver abscesses require proper drainage, early detection and collaboration with experts are important. Research on the epidemiology and characteristics of these patients is limited because of their rarity.

Therefore, we conducted this study to identify the clinical characteristics that may accompany liver abscesses in patients with AP and to analyze the characteristic differences in bacterial species.

MATERIALS AND METHODS

This retrospective observational study was approved by the Institutional Review Board of Kyung Hee University Hospital at Gangdong (approval number: 2024-03-037). The written informed consent was waived due to the study’s retrospective design. We retrospectively analyzed 474 patients diagnosed with AP at our institution between June 2006 and July 2022. No patient was diagnosed with prostate cancer, and AP was identified based on clinical features and abnormalities in serum or urine laboratory results demonstrating infection and prostate-specific antigen (PSA) elevation. Blood and urine cultures were performed to determine the presence of pathogenic bacteria and drug resistance. Cases in which AP was present or the infection was attributed to other diseases were excluded. Patients in whom the bacterial organism was not identified by culture were also excluded because of the need to confirm the association between AP and liver abscesses based on the pathogen from urine and abscess cultures.

A liver abscess was diagnosed on abdominal computed tomography (Fig. 1). Patients with AP were divided into two groups: those with and without liver abscesses. Demographic characteristics, medical histories, and laboratory data of the patients in each group were retrieved. These included age, presence of underlying diseases (DM, hypertension [HTN], benign prostatic hyperplasia [BPH], malignancy, HIV, alcohol history), positive urine or blood culture, antibiotic susceptibility, extended-spectrum beta-lactamase (ESBL), and serum laboratory tests (PSA, glycated hemoglobin [HbA1c]).

Data were analyzed using IBM SPSS version 18.0 (IBM Corp.). Continuous variables were compared using an independent sample t-test, whereas non-continuous variables were compared using Pearson’s chi-square and Fisher’s exact tests. Statistical significance was set at p<0.05.

RESULTS

A total of 271 patients were enrolled in this study. Of these, only 15 patients (5.5%) had liver abscesses concomitant with AP. The clinical characteristics of patients with AP classified by liver abscess are shown in Table 1. The mean ages in the groups with and without liver abscesses were 62.7±10.4 years and 71.5±13.9 years, respectively (p=0.016) on univariate analysis (Table 2). Regarding underlying diseases, patients with DM accounted for a large proportion (nine patients, 60.0%) of the liver abscess group, but only 28.9% of the non-liver abscess group (74 patients; p=0.012). Moreover, the liver abscess group had a lower proportion of patients with HTN (two patients, 13.3%; p=0.016). Patients in both groups had similar percentages of BPH (60.0% vs. 69.5%). Malignancy and a history of alcoholism were not significantly associated with liver abscesses. KP was identified in all patients in the liver abscess group, whereas only 18 patients (7.0%) in the non-liver abscess group showed the presence of KP. ESBL-producing pathogens were not identified in the culture results of the liver abscess group but were identified in 41 patients (16.0%) in the non-liver abscess group (p=0.024). No significant association was observed between PSA (p=0.648) and HbA1c (p=0.055) levels in the initial serum laboratory results.

Compared to the non-liver abscess group, the platelet count and albumin levels were lower in the liver abscess group, but aspartate transaminase, alanine transaminase, and alkaline phosphatase levels were higher. However, gamma-glutamyl transpeptidase and bilirubin levels were not significantly different between the two groups in univariate analysis. Unlike in DM, HbA1c levels were not significantly different between the two groups.

Among the 33 patients for whom KP was cultured, 15 patients (45.5%) had liver abscesses. In the liver abscess group, HbA1c levels were significantly higher, while all other parameters demonstrated no significant relationship in the univariate analysis (Table 3). In the liver abscess group, cultured KP pathogens were ESBL-negative and resistant to ampicillin. In contrast, the KP in the non-liver abscess group was resistant to various antibiotics. Among patients with AP and KP infections, those with elevated HbA1c levels tended to have concomitant liver abscesses.

DISCUSSION

AP is an acute inflammation of the prostate primarily caused by an ascending infection through the urethra. Intrinsic patient factors such as BPH and urethral stricture can also increase the likelihood of developing AP [16]. The incidence is highest in individuals aged 20–40 years and those over 70 years old [17]. About 25% of men are diagnosed with AP at least once in their lifetime, but only 10% are confirmed to have bacterial infections [5]. Elevated PSA levels accompanied by infection are considered definitive evidence. About 70% of patients demonstrated elevated PSA levels, which were 21.36±24.99 ng/mL in the previous study [18]. After treating the infection, monitoring the normalization of PSA levels is important to differentiate it from prostate cancer.

The mortality rate for liver abscesses was high in the past, but advances in treatment techniques, such as percutaneous drainage, have reduced it to approximately 11%–31% [19]. Liver abscesses can be confirmed through liver function abnormalities and imaging tests. In this study, only KP was identified in the urine or blood of patients with both liver abscesses and AP. Lee et al. [6] reported that in a multicenter retrospective cohort study of prostatitis and prostatic abscesses in 142 patients, E. coli accounted for the largest proportion of prostate infections (65.0%), with KP being the second most important causative agent (11.7%). In addition, 50% of the patients with prostate infections and abscesses in organs other than the prostate had liver abscesses, and KP was identified in two-thirds of these cases. They exhibited sensitivity to cefoxitin, cefotaxime, and ciprofloxacin, which is consistent with the culture results in our cases [6].

Several previous studies have investigated the association between KP and prostate cancer. Case reports have been published on KP-induced emphysematous prostatitis or prostatic abscess, which is a potentially fatal form of prostate infection [202122]. Kuo et al. [20] reported the case of a 60-year-old man with emphysematous prostatitis caused by KP. In their review, Gram-negative pathogens were identified in 10 of 17 prostatic abscess cases, including KP. They also explained that two etiologic patterns of bacteria exist in prostate abscesses: the first pattern is of gram-negative bacteria, which are presumed to ascend through the lower urinary tract, and the second pattern is of gram-positive bacteria that are transferred to the prostate from another abscess source [20]. In this study, only gram-negative bacteria were identified in patients with prostatitis accompanied by liver abscess. This suggests the presence of the pathogen in the genitourinary tract; hence, the liver abscess may have resulted from secondary hematogenous spread after AP.

Lin et al. [23] reported a significant association between the occurrence of KP liver abscesses and history of ampicillin use within the last 30 days, and identified a dose—response relationship in this context. Animal experiments demonstrated that ampicillin administration to KP-infected animals was ineffective against pathogens, destroyed the normal barrier formed by intestinal microorganisms, and facilitated pathogen colonization. The authors speculated that this might be attributed to the abuse of antibiotics in modern medicine and agriculture [23]. In our study, KP resistance to ampicillin, regardless of liver abscess, was observed in all patients, which is presumed to be related to the results of the aforementioned study.

Kim et al. [24] reported a higher incidence of prostatic abscesses caused by KP in East Asian countries such as Korea and Taiwan than in other regions. The incidence of liver abscesses caused by KP is increasing in the same region, and 28% of patients experience complications due to hematogenous spread [24]. The complications included endophthalmitis, pneumonia, brain, renal, prostate, and psoas abscesses. This pattern is referred to as invasive liver abscess syndrome, and is caused by KP. Capsular polysaccharide K antigen plays an important role in the metastasis of invasive liver abscesses. Among them, the K1 serotype demonstrated a higher resistance to phagocytosis by KP than the other strains. In addition, the K1 serotype is the dominant form of KP-induced liver abscesses in Taiwan and Korea, whereas this particular strain is rare in the West [131422]. DM is the most widely known risk factor for metastatic infections due to liver abscesses. Inadequate blood glucose control has been reported to reduce the phagocytosis of the K1 serotype KP. In addition to DM, immunocompromised conditions, such as alcoholism or malignancy, significantly impact the pathogenesis [121314].

In this study, the occurrence of liver abscesses was significantly associated with DM in the AP group. The incidence of infections is high in patients with DM. This is supported by the finding that patients with high HbA1c levels have a higher prevalence of liver abscesses than those with KP infections. In addition, the incidence of liver abscesses in our study was high in younger patients and in those without HTN. Younger patients may be more likely to overlook early prostatic infection symptoms, which could lead to a higher risk of liver abscess. Additionally, they may have fewer underlying conditions such as HTN.

The limitations of this study include the small number of patients with concurrent liver abscesses and AP at a single institution. Patients with liver abscesses admitted to the gastroenterology department were not included in the study because prostatitis may not have been routinely investigated. A small sample size leads to lower reliability of the analysis results and challenges in generalizing the findings. The number of ‘AP with liver abscess (LA)’ (15), the events of interest, was also small. In the univariate analysis, there were 13 variables with p-values <0.2, which is the standard for inclusion in multivariate analysis. Events per variable (EPV) is an important indicator for evaluating the reliability of a model, and securing a sufficient EPV is important for increasing the model’s prediction performance. The recommended minimum EPV is 10; therefore, in this study, 15/13<10 increased the risk of overfitting [25]. Accordingly, multivariate analysis could not be performed because of the small sample size of patients with AP with LA. In future studies, it would be better to obtain more valid conclusions through a large-scale data analysis using multicenter studies or health insurance data.

Virulence factors should be identified through genetic analysis of KP liver abscess pathogens. In patients with KP, the presence of the K1 serotype, a known viral factor, should be assessed to determine its association with invasive liver abscess syndrome.

CONCLUSIONS

Although prostate infection with liver abscess accounts for only 5% of all cases, it should be noted that it can be a metastatic form of liver abscess if KP is identified in the bacterial culture. Identifying infectious lesions that may exist in the liver and other organs through imaging workups such as computed tomography is essential, particularly in younger patients with elevated liver function tests or KP culture. If invasive liver abscess syndrome is suspected, prevention of exacerbation of the condition by administering appropriate antibiotics along with strict blood sugar control, draining the abscess, and establishing a rapid treatment plan is crucial.

Fig. 1 Axial plane of abdominal computed tomography of the liver abscess. Computed tomography (CT) revealed prostatitis and liver abscesses. (A) The black arrow indicates a liver abscess with multiple localized hypoattenuating lesions. (B) The black arrow indicates the prostate in the case of prostatitis, displaying a diffusely enlarged, edematous gland and a heterogeneous peripheral zone. (C) The white arrow displays a prostatic abscess with well-defined and homogeneous low attenuation.

Table 1 Clinical features of patients with ABP

	Entire ABP (n=271)	
Age (y)	71 (20–103)	
Liver abscess	15 (5.5)	
Underlying disease		
	DM	83 (30.6)	
	HTN	118 (43.5)	
	BPH	187 (69.0)	
Medical history		
	Malignancy	31 (11.4)	
	Alcoholism	15 (5.5)	
Culture			
	Escherichia coli	136 (50.2)	
	Enterococcus spp.	37 (13.7)	
	Klebsiella pneumoniae	33 (12.2)	
	Staphylococcus spp.	14 (5.2)	
	Pseudomonas spp.	10 (3.7)	
	Acinetobacter spp.	9 (3.3)	
	Enterobacter aerogenes	6 (2.2)	
	Citrobacter koseri	5 (1.8)	
	Proteus mirabilis	5 (1.8)	
	Candida	5 (1.8)	
	Corynebacterium spp.	3 (1.1)	
	Streptococcus agalactiae	3 (1.1)	
	Klebsiella oxytoca	3 (1.1)	
	Aerococcus urinae	1 (0.4)	
	Serratia marcescens	1 (0.4)	
	ESBL positive	41 (15.1)	
Initial laboratory data		
	PSA (ng/mL)	17.7 (0.6–450.9)	
	HbA1c (%)	6.3 (4.8–12.3)	
	Platelet count (×103/µL)	194k (36k–543k)	
	Albumin (g/dL)	4.0 (2.0–5.2)	
	AST (U/L)	24 (11–209)	
	ALT (U/L)	19 (5–161)	
	ALP (U/L)	103 (33–1,434)	
	GGT (U/L)	33 (10–770)	
	Total bilirubin (mg/dL)	0.9 (0.2–19)	
	Direct bilirubin (mg/dL)	0.3 (0.1–2.6)	
Values are presented as median (range) or number (%).

ABP, acute bacterial prostatitis; DM, diabetes mellitus; HTN, hypertension; BPH, benign prostatic hyperplasia; ESBL, extended-spectrum beta-lactamase; PSA, prostate-specific antigen; HbA1c, glycated hemoglobin; AST, aspartate transaminase; ALT, alanine transaminase; ALP, alkaline phosphatase; GGT, gamma-glutamyl transpeptidase.

Table 2 Univariate analysis for the comparison of characteristics of patients with AP according to the presence of liver abscesses

	AP with liver abscess (n=15)	AP without liver abscess (n=256)	p-value	
Age (y)	62.7±10.4	71.5±13.9	0.016*	
Underlying disease				
	DM	9 (60.0)	74 (28.9)	0.012a*	
	HTN	2 (13.3)	116 (45.3)	0.016b*	
	BPH	9 (60.0)	178 (69.5)	0.410a	
Medical history				
	Malignancy	1 (6.7)	30 (11.7)	>0.999a	
	Alcoholism	5 (33.3)	10 (3.9)	0.656b	
Culture				
	Klebsiella pneumoniae	15 (100.0)	18 (7.0)	<0.001a*	
	ESBL	0 (0.0)	41 (16.0)	0.024b*	
Initial laboratory data				
	PSA (ng/mL)	8.0±8.3	35.1±39.1	0.648	
	HbA1c (%)	7.3±1.6	6.6±1.2	0.055	
	Platelet count (×103/µL)	150k±76.1k	191k±89.6k	0.034*	
	Albumin (g/dL)	3.0±0.3	3.9±0.5	0.001*	
	AST (U/L)	72.7±5.8	36.4±45.4	0.001*	
	ALT (U/L)	85.0±58.2	23.2±24.5	0.002*	
	ALP (U/L)	551±298	116±92.6	0.008*	
	GGT (U/L)	194±65.5	61.3±105	0.086	
	Total bilirubin (mg/dL)	1.0±65.5	13.9±44.4	0.684	
	Direct bilirubin (mg/dL)	0.5±0.2	0.3±0.2	0.055	
Values are presented as mean±standard deviation or number (%).

AP, acute prostatitis; DM, diabetes mellitus; HTN, hypertension; BPH, benign prostatic hyperplasia; ESBL, extended-spectrum beta-lactamase; PSA, prostate-specific antigen; HbA1c, glycated hemoglobin; AST, aspartate transaminase; ALT, alanine transaminase; ALP, alkaline phosphatase; GGT, gamma-glutamyl transpeptidase.

a:Pearson’s chi-squared test.

b:Fisher’s exact test.

*p<0.05.

Table 3 Comparative characteristics of Klebsiella pneumoniae carriers according to the existence of liver abscesses

	Liver abscess with K. pneumoniae (n=15)	Non-liver abscess with K. pneumoniae (n=18)	p-value	
Age (y)	62.7±10.4	69.9±16.8	0.159	
Underlying disease				
	DM	9 (60.0)	6 (33.3)	0.170a	
	HTN	2 (13.3)	6 (33.3)	0.242b	
	BPH	9 (60.0)	13 (72.2)	0.712a	
Medical history				
	Malignancy	1 (6.7)	1 (5.6)	0.894a	
	Alcoholism	5 (33.3)	1 (5.6)	0.338b	
Resistance of pathogen				
	Ampicillin	15 (100.0)	18 (100.0)		
	Amikacin	0 (0.0)	2 (11.1)	0.489b	
	Amoxicillin/clavulanate	0 (0.0)	4 (22.2)	0.108b	
	Cefazolin	0 (0.0)	5 (27.8)	0.049b*	
	Cefepime	0 (0.0)	3 (16.7)	0.233b	
	Cefotaxime	0 (0.0)	3 (16.7)	0.233b	
	Ciprofloxacin	0 (0.0)	4 (22.2)	0.108b	
	Gentamicin	0 (0.0)	2 (11.1)	0.489b	
	Piperacillin/tazobactam	0 (0.0)	3 (16.7)	0.233b	
	Trimethoprim/sulfamethoxazole	0 (0.0)	3 (16.7)	0.233b	
	ESBL	0 (0.0)	3 (16.7)	0.233b	
Initial laboratory data				
	PSA (ng/mL)	24.8±24.3	31.7±36.0	0.538	
	HbA1c (%)	8.5±2.6	6.3±0.9	0.024*	
	Platelet count (×103/µL)	162k±99.9k	195k±93.1k	0.344	
Values are presented as mean±standard deviation or number (%).

DM, diabetes mellitus; HTN, hypertension; BPH, benign prostatic hyperplasia; ESBL, extended-spectrum beta-lactamase; PSA, prostate-specific antigen; HbA1c, glycated hemoglobin.

a:Pearson’s chi-squared test.

b:Fisher’s exact test.

*p<0.05.

CONFLICTS OF INTEREST: The authors have nothing to disclose.

FUNDING: None.

AUTHORS’ CONTRIBUTIONS: Research conception and design: Dong-Gi Lee.

Data acquisition: Jeonghyouk Choi.

Statistical analysis: Jeonghyouk Choi.

Data analysis and interpretation: Jeonghyouk Choi.

Drafting of the manuscript: Jeonghyouk Choi.

Critical revision of the manuscript: Dong-Gi Lee.

Administrative, technical, or material support: Dong-Gi Lee.

Supervision: Dong-Gi Lee.

Approval of the final manuscript: Dong-Gi Lee.
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