A comparison of clinical characteristics and outcome in pyogenic liver abscess patients with and without diabetes mellitus: A case-control study

Haitao Sun; Yuxian Yang; Eric A Klomparens; Dong Zhao

doi:10.4103/ed.ed_6_19

ORIGINAL ARTICLE

Year : 2019 | Volume : 4 | Issue : 1 | Page : 23-27

A comparison of clinical characteristics and outcome in pyogenic liver abscess patients with and without diabetes mellitus: A case-control study

Haitao Sun¹, Yuxian Yang², Eric A Klomparens³, Dong Zhao²
¹ Department of General Surgery, Luhe Hospital, Capital Medical University, Beijing, China
² Department of Endocrinology, Luhe Hospital, Capital Medical University, Beijing, China
³ Department of Neurological Surgery, Wayne State University School of Medicine, Detroit, MI, USA

Date of Submission	22-Jan-2019
Date of Acceptance	05-Mar-2019
Date of Web Publication	9-Apr-2019

Correspondence Address:
Dr. Dong Zhao
Department of Endocrinology, Beijing Luhe Hospital, Capital Medical University, No. 82 Xinhua South Road, Tongzhou District, Beijing 101149
China

Source of Support: None, Conflict of Interest: None

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DOI: 10.4103/ed.ed_6_19

Abstract

Background: Pyogenic liver abscess (PLA) is a relatively rare and potentially life-threatening disease. The incidence of PLA has been increasing steadily over the past few decades. PLA is relatively common in patients with diabetes mellitus (DM). Although multiple studies have explored the relationship between PLA and DM, it remains controversial, and the evidence comes primarily from case reports. Because of this, more studies are necessary to compare the characteristics of PLA patients with and without DM to explore the relationship between PLA and DM.
Materials and Methods: A total of 115 PLA patients admitted in Beijing Luhe Hospital from December 2012 to August 2017 were divided into two groups based on the presence of DM (the DM group and the non-DM group) for the comparison of clinical characteristics and outcomes of patients. Chi-square, Fisher's exact, and t-tests were used to analyze the differences between the two groups.
Results: Of 115 patients included, 50.4% of patients had DM. The DM group had a lower prevalence of abdominal pain (28% vs. 51%, P = 0.011) and pain to palpation (48% vs. 67%, P = 0.046). Moreover, the DM group had a higher prevalence of misdiagnosis (45% vs. 16%, P = 0.001) and poor outcomes (9% vs. 0%, P = 0.03).
Conclusions: We found that patients with DM may have less typical symptoms of PLA than those without DM, which may explain the higher prevalence of misdiagnosis of PLA in patients with DM. Moreover, patients with DM have worse outcomes than those without DM.

Keywords: Characteristic, diabetes mellitus, pyogenic liver abscess

How to cite this article:
Sun H, Yang Y, Klomparens EA, Zhao D. A comparison of clinical characteristics and outcome in pyogenic liver abscess patients with and without diabetes mellitus: A case-control study. Environ Dis 2019;4:23-7

How to cite this URL:
Sun H, Yang Y, Klomparens EA, Zhao D. A comparison of clinical characteristics and outcome in pyogenic liver abscess patients with and without diabetes mellitus: A case-control study. Environ Dis [serial online] 2019 [cited 2023 May 28];4:23-7. Available from: http://www.environmentmed.org/text.asp?2019/4/1/23/255738

Introduction

Pyogenic liver abscess (PLA) is a relatively rare and potentially life-threatening disease. Studies have shown that the incidence of PLA has been increasing steadily over the past few decades.^[1],[2],[3] Due to various risk factors such as the use of upper gastrointestinal endoscopy,^[4],[5] chronic kidney disease,^[6] and pneumonia,^[7] PLA has become common in China.^[8] Although the mortality has decreased slightly due to surgical intervention, appropriate antibiotics combined with percutaneous drainage of the liver abscess, PLA is still a disease with high mortality.^[9],[10]

It is reported that diabetes mellitus (DM) is a risk factor for various diseases, such as cardiovascular diseases, cancers, and infectious diseases.^{[11],[12],[13],[14],[15],[16]} Patients with DM usually have abnormalities in both cell-mediated and humoral immune responses, leading to increased susceptibility to various infectious diseases.^[17] Because of this, PLA is more common in DM patients. It has been shown that, in Taiwan, 48.3% of patients with PLA also have DM.^[18] One study in China has reported that the prevalence of DM in PLA patients is 44.3%.^[19] It is reported that patients with DM have a 3.6-fold increased risk of experiencing PLA.^[20]

Multiple studies have explored the relationship between PLA and DM. Several epidemiological studies have suggested that DM is an important risk factor for PLA and may contribute to worse outcomes.^[20],[21] However, other studies have suggested that DM does not increase the fatality rate of PLA.^[18],[19] Few studies focus specifically on the relationship between PLA and DM in Chinese patients, nor on a comparison of the clinical characteristics of PLA in patients with and without DM. In addition, the evidence for the relationship between PLA and DM primarily comes from case reports,^{[22],[23],[24],[25],[26],[27],[28],[29]} and the relationship between PLA and DM remains controversial. Therefore, we conducted a retrospective case–control study in Beijing Luhe Hospital to compare the clinical characteristics of PLA patients with and without DM and explore the relationship between PLA and DM, hoping to provide evidence for clinical practice.

Materials and Methods

Study population

We included all patients who were hospitalized between December 2012 and August 2017 at Beijing Luhe Hospital (The Affiliated Hospital of Capital Medical University) with a diagnosis of PLA at discharge. The study was approved by the Ethics Committee of Beijing Luhe Hospital. Informed consent was obtained from each person who participated in this study.

Patients were diagnosed with PLA by meeting the following criteria: ultrasonography (US) and computerized tomography (CT) results consistent with PLA, in addition to one of the following: (i) associated clinical symptoms: fever, right upper abdominal pain, etc.; (ii) characteristic laboratory results, such as leukocytosis and abnormal liver function; (iii) a positive blood or pus culture of pathogen; (iv) resolution of the lesions after antibiotic therapy in cases lacking evidence from cultures. We excluded the following patients: (i) those who were discharged from the hospital against medical advice, (ii) those who had primary liver cancer or a metastatic liver tumor, (iii) those who had an extrahepatic abdominal abscess without coexisting PLA, and (iv) those who had severe abdominal trauma, including hepatic or splenic rupture. Finally, after the screening, a total of 115 patients were included in this study. These patients were divided into two groups based on the presence or absence of DM, namely, the DM group and the non-DM group. DM was defined according to the following criteria from 1997: a history of DM or the typical symptoms of DM; random blood glucose concentration >200 mg/dL; fasting plasma glucose >126 mg/dL; or 2-h plasma glucose >200 mg/dL during an oral glucose tolerance test.^[30]

Data collection

We collected the data by browsing the medical records of each patient. Clinical information such as gender, age, clinical manifestation, treatment strategy, and outcome were collected. Major laboratory and pathology test results, including those regarding liver function, renal function, plasma glucose, and pathogen identification from blood or pus, were collected as much detail as possible. Characteristics of PLA evidenced by US or CT were recorded for all patients, including abscess position, size, quantity, and the presence or absence of gas formation. Poor outcome was defined as persistence of fever, abdominal pain, and abscess lesions at discharge, or death during hospitalization. Misdiagnosis was defined as when the diagnosis upon admission was different from the final diagnosis of PLA. When the primary diagnosis was different from the discharge diagnosis, we defined this as a “misdiagnosis” of PLA.

Statistical analysis

All statistical analysis was performed using SPSS statistical software (version 20.0). Descriptive data are presented as mean with standard deviation for continuous data and as percentages for categorical data. The Chi-squared test and Fisher's exact test were applied to evaluate the differences in categorical variables. Student's t-test was used to evaluate the differences in continuous variables.

Results

General characteristics of subjects

Altogether, a total of 123 patients with PLA received treatment at the hospital during the study period, but eight patients who did not fit the inclusion criteria were excluded from the study: three patients had metastatic or primary tumors, two patients had other severe infections, one patient who had splenic rupture, one patient left the hospital against medical advice, and one patient had leukemia. Of the included 115 patients with PLA, 58 (50.4%) patients had DM. There was no statistically significant difference in the male-to-female ratio between the DM and non-DM groups (1.42 vs. 1.60, P = 0.761). The mean age in the DM and non-DM groups was not significantly different, either (56.4 ± 12.3 vs. 56.6 ± 16.7, P = 0.962) [Table 1].

Table 1: Characteristics and clinical findings of pyogenic liver abscess patients with and without diabetes mellitus

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Clinical symptoms and signs

In this study, between the DM and non-DM groups, there were no obvious differences in the percentage of patients with fever (90% vs. 86%, P = 0.545) or chills (66% vs. 56%, P = 0.303). However, the DM group had a lower prevalence of abdominal pain (28% vs. 51%, P = 0.011) and pain to palpation (48% vs. 67%, P = 0.046) than the non-DM group [Table 1]. In addition, the DM group was more prone to have metastatic lesions (60% vs. 41%, P = 0.161), but this difference was not statistically significant [Table 1]. Moreover, our study found that the most common location of the metastatic lesion in the DM group was the lung (26%), while a lesion in the gallbladder (11%) was more common in the non-DM group (data not shown).

Laboratory, imaging, and microbiological findings

The DM group had significantly more patients with elevated fasting blood glucose levels than the non-DM group (>6.7 mmol/L) (84% vs. 33%, P < 0.001), which can be explained by the inherent characteristics of DM. Compared with the non-DM group, more patients in the DM group had low platelet levels (≤100 × 10⁹/L) (23% vs. 9%, P = 0.040). Moreover, patients in the DM group had elevated plasma triglyceride (TG) levels than the non-DM group (>1.7 mmol/L) (37% vs. 11%, P = 0.002). There was no significant difference in white blood cell count, neutrophil count, hemoglobin, alanine aminotransferase, aspartate aminotransferase, creatinine, blood urea nitrogen, total bilirubin, direct bilirubin, total cholesterol, or lactate dehydrogenase between the two groups [Table 2]. Regarding imaging findings, no significant differences were found in abscess position, size, quantity, or the presence of gas formation between the two groups [Table 3]. Only a portion of the patients in this study underwent blood culture (40%) or pus culture (32%) (data not shown). The pathogen results were various and included Klebsiella pneumoniae, Escherichia ^{More Details} coli, Mycoplasma pneumoniae, Staphylococcus, viridans streptococci, Acinetobacter baumannii, and various fungi. K. pneumoniae was the most common pathogen.

Table 2: Laboratory findings of pyogenic liver abscess patients with and without diabetes mellitus

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Table 3: Imaging findings and microorganism of pyogenic liver abscess patients with and without diabetes mellitus

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Diagnosis, therapy, and outcome

After comparing the primary diagnosis of each patient at the time of admission and the discharge diagnosis, we found that many patients were not diagnosed with PLA initially (35/115, 30%). A large proportion of patients were misdiagnosed with having other diseases, including acute appendicitis, acute cholecystitis, cholelithiasis, acute intestinal obstruction, pancreatitis, gastroenteritis, primary liver cancer, and peptic ulcer. Notably, patients in the DM group had a higher prevalence of misdiagnosis of PLA than patients in the non-DM group (45% vs. 16%, P = 0.001) [Table 1]. As for the therapy, combination of antibiotics and catheterization was the most common treatment strategy in both groups. No patients underwent surgical drainage in this study. In addition, the DM group and the non-DM group had similar hospital stay (15.2 vs. 13.9 days, P = 0.415). A higher proportion of patients in the DM group had a poor outcome than the non-DM group (5/58 vs. 0/57, P = 0.03). All patients with PLA in the non-DM group recovered, whereas five patients in the DM group had a poor outcome, including four patients whose condition deteriorated and one mortality.

Discussion

Previous studies have indicated that DM is a potential risk factor for PLA and is associated with a worse outcome.^[20],[21] In this study, the DM group did have a higher prevalence of a poor outcome. This result is similar to that seen in another case–control study,^[20] which found that patients with DM had a 3.6-fold increased risk of experiencing PLA than patients without DM and had a higher risk of mortality when they acquired PLA. However, other studies have reported that DM does not increase the fatality rate of PLA.^[18],[19] Therefore, the association between PLA and DM remains controversial.

In general, fever, chills, and abdominal pain were the most common symptoms in this study, which is similar to previous studies.^{[18],[20],[31]} However, the prevalence of abdominal pain and pain to palpation in the DM group was much lower than in the non-DM group, which has not been reported previously.^[18],[19] Reduced pain symptoms in patients with DM may occur because chronic hyperglycemia can damage sensory nerves.^[32],[33] Reduced symptomatology in DM patients may explain why the DM group had a much higher prevalence of misdiagnosis than the non-DM group. About 30% of all PLA patients were not diagnosed with PLA initially and were instead misdiagnosed as having other diseases. Many factors may contribute to this high rate of misdiagnosis, such as insufficient awareness of this disease, and a lack of specific clinical symptoms and laboratory findings.

The study also showed that more patients in the DM group developed metastatic lesions, although this difference did not reach statistical significance. In addition, the most common location of metastatic lesions in the DM group was the lung (26%) as compared to the gallbladder (11%) in the non-DM group. This result differs from a previous study in Taiwan which found that the most common metastatic infection focus was the urinary tract in patients with DM, and in the form of a lung empyema in patients without DM.^[18] In addition, the current study found no difference in age between the two groups, which contradicts the results of previous studies which have suggested that PLA patients with DM are generally older than those without DM.^[18],[19] This may be partly explained by the younger onset of DM in recent decades and the relatively poorer glycemic control seen in younger patients.

For the laboratory findings, the DM group had higher blood glucose and TG concentrations than the non-DM group, which is likely due to the nature of DM. In addition, the DM group had a higher prevalence of insufficient platelet count (≤100 × 10⁹/L) (23% vs. 9%, P = 0.04), consistent with a similar study in Taiwan.^[18] The mechanism mediating this difference in platelet count between the two groups remains unclear; autoimmune responses may be involved. Regarding imaging findings, the quantity of abscesses in each patient was not significantly different between the two groups. This is consistent with the results of a study published in 2010.^[18] However, Tian et al. reported that patients with DM are more prone to developing multiple abscesses,^[19] which differs from the results published in Lancet in 1966 which suggested a possible relationship between DM and solitary PLA.^[22] The inconsistency in this result may be explained partly by ethnic differences between studies and a large amount of time separating the studies. Moreover, previous studies have suggested that DM patients have a higher prevalence of having a gas-forming PLA.^[18],[19] However, no statistical differences existed in the prevalence of gas formation of PLA between the two groups in the current study. The location and size of the abscess were not significantly different between the two groups either, which is consistent with a study done in Taiwan in 2010.^[18] In general, we found that most abscesses were located in the right lobe of the liver, possibly because of its larger size and the distribution of the hepatic vessels.

There were some limitations in this study. The sample size used in this study was relatively small, which may have disallowed us from finding some significant differences. Second, patients were recruited only from Beijing Luhe Hospital in Tongzhou District, which limits the generalizability of the results. Third, only hospitalized patients were included in the study. Outpatients were not considered in this study because they lack detailed medical records and have less thorough laboratory data available to analyze. A larger sample and multi-center studies are still needed to fully elucidate the relationship between PLA and DM.

Conclusions

There are differences in clinical characteristics of PLA between patients with and without DM. The DM group had a lower prevalence of abdominal pain and pain to palpation. The DM group also had a higher prevalence of misdiagnosis. DM, as a risk factor, may also affect the outcome and fatality rate of PLA patients. This may have important implications for the clinical practice in PLA patients in future.

Acknowledgment

We are grateful for the support of the medical record department for the total list of PLA patients in recent years.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

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