Abstract
Purpose
Nosocomial infection is a major threat to the health care system and patient welfare. After the pandemic, new protocols were established in hospitals and communities to protect against the transmission of COVID-19, which may have changed the incidence of nosocomial transmission. This study was conducted to compare the incidence of nosocomial infection before and after the COVID-19 pandemic.
Methods
This was a retrospective cohort study performed on trauma patients who were admitted, from May 22, 2018 to November 22, 2021, to the largest level-1 trauma center in Shiraz, Iran (Shahid Rajaei Trauma Hospital). All the trauma patients over 15 years old admitted during the study time were included in this study. Individuals who were declared dead upon arrival were excluded. Patients were evaluated in 2 periods: before the pandemic (May 22, 2018 – February 19, 2020) and after the pandemic (February 19, 2020 – November 22, 2021). Patients were assessed based on demographic information (age, gender, length of hospital stay, and patient outcome), the occurrence of hospital infection, and the type of infection. The analysis was done using SPSS version 25.
Results
Overall, 60,561 patients were admitted, with a mean age of 40 years. Nosocomial infection was diagnosed in 4.00% (n = 2423) of all admitted patients. The incidence rate of post-COVID-19 hospital-acquired infections decreased by 16.28% (p < 0.001) when compared to before the pandemic; in contrast, surgical site infection (p < 0.001) and urinary tract infection (p = 0.043) were responsible for this change, while hospital-acquired pneumonia (p = 0.568) and bloodstream infection (p = 0.156) were not significantly different. Overall mortality was 1.79%, while 28.52% of all patients with nosocomial infections died. During the pandemic, there was a 25.78% increase (p < 0.001) in the overall incidence rate of mortality, which was also observed among patients with nosocomial infections (17.84%).
Conclusion
The incidence of nosocomial infection has decreased during the pandemic, possibly due to the use of more personal protective equipment and modified protocols after the outbreak. This also explains the difference in the change in incidence rates of nosocomial infection subtypes.
Keywords: Injuries, COVID-19, Cross infection, Incidence
Introduction
Hospital-acquired infections occur in patients under medical care at least 48 h after hospitalization.1 Hospital-acquired pneumonia (HAP), central line-associated bloodstream infection (BSI), surgical site infection (SSI), catheter-associated urinary tract infection (UTI), and ventilator-associated pneumonia (VAP) are different types of these infections.1,2 Increased length of hospital stay, morbidity, microbial resistance, death rate, and economic burden are only small portions of the damage they caused.1,3,4
A considerable number of patients suffer from nosocomial infections.5 A study (2011) reported the incidence of hospital-acquired infections to be 3.5% – 12% and 5.7% – 19.1% in high-income and middle- to low-income countries, respectively.6 In 2017, these rates were 7% and 10%.3 This number can rise to 42.8% in intensive care unit (ICU).1 Hospital-acquired infections are transmitted either in endogenous or exogenous ways. The exogenous contamination is mainly associated with microorganisms from the environment or other people (other patients, health care workers, etc.).1,7 Many factors can affect the contraction of nosocomial infection, such as age, comorbidities, immunosuppressive treatments, and invasive procedures. However, health care workers are responsible for about 15% of nosocomial infections in hospitalized patients.3,7 Guidelines emphasize frequent handwashing and aseptic techniques to prevent the transmission of infectious agents between patients and healthcare providers.8
The occurrence of the COVID-19 pandemic challenged the medical system with a shortage of staff and resources, and the need for extra measures to prevent the transmission of the disease; precautions at the beginning of the outbreak included contact, droplet, and aerial transmission.9,10 Since the beginning of the epidemic, visiting hours have been canceled, and in the rare cases, where it was possible to visit patients only when a complete set of personal protection equipped. The Center for Disease Control and Prevention and World Health Organization provided dynamic guidelines on preventive protocols.11, 12, 13 There were also guidelines suggesting that elective surgical intervention should be delayed14, and as a result, the epidemiology of nosocomial infections changed9. This article looked at how the types and rates of nosocomial infections in a trauma center in the south of Iran changed over time.
Methods
Study design
This was a retrospective cohort study performed on trauma patients admitted from May 22, 2018 to November 22, 2021 in the largest level-1 trauma center in (Shahid Rajaei Trauma Hospital) in Shiraz, Iran. The first case of COVID-19 was detected in Iran on February 19, 2020 in Qom15, and to compare the incidence of nosocomial infection, patients were evaluated in 2 time periods (each 21 months) before the pandemic (May 22, 2018 to February 19, 2020) and after the pandemic (February 19, 2020 to November 22, 2021). Our study included all patients over the age of 15 years who were admitted to the hospital during the specified time period. Individuals who were declared dead upon arrival were excluded from our study.
Data collection
Demographic data, including age, gender, length of hospital stay, and patient outcome, were collected from the hospital information system. The criteria for diagnosing nosocomial infections (central line-associated BSI16, catheter-associated UTIs17, SSI18, and VAP19) are based on the definitions of the hospital infection care system of the Center for Disease Control and Prevention. A patient with suspected hospital infection symptoms or his radiological images revealed infection is reported to the hospital's infection control supervisor or infectious disease specialist. The patient will be examined by the doctor and infection control officer. If necessary, a sample from the area suspected of hospital infection will be sent to the hospital laboratory. A file is created for an infectious patient that records the patient's name, date of sample collection, culture date, number of cultures, type of infection, location of culture, date of receiving the answer, and the diagnosis. The information related to nosocomial infection used in this study was collected using the mentioned files.
Statistical analysis
Mean and frequency methods were used to determine quantitative and qualitative information. The Chi-square test was used to compare ratios, and the t-test was used to compare means. In all cases, a p value less than 0.05 was considered significant. The analysis was done using SPSS version 25.
Results
As shown in Table 1, 60,561 patients were admitted to Shahid Rajaei Trauma Hospital, with a mean age of 40 years (SD = 19) and a male to female ratio of 2.46. Nosocomial infection was diagnosed in 4.00% (2423) of all admitted patients. The most nosocomial infections (n = 1611) were caused by HAP, followed by SSI (n = 810). During the pandemic, the length of hospital stay decreased for all patients (p < 0.001); however, for patients with nosocomial infections, admission time did not change (p = 0.330). Overall mortality was 1.79%, while 28.52% of all patients with nosocomial infections died.
Table 1.
Characteristics of all the studied patients.
| Variables | Before pandemic (n = 31,383) | After pandemic (n = 29,178) | Total (n = 60,561) | p value |
|---|---|---|---|---|
| Gender, n | < 0.001 | |||
| Male | 21,330 | 21,728 | 43,058 | |
| Female | 10,053 | 7450 | 17,503 | |
| Age (year), mean (SD) | 40.7 (19.2) | 39.6 (18.8) | 40.1 (19.02) | < 0.001 |
| LOS (day), mean (SD) | 4.8 (13.8) | 4.3 (7.3) | 4.6 (11.2) | < 0.001 |
| Nosocomial infections, n (%) | 1361 (4.34) | 1062 (3.64) | 2423 (4.00) | < 0.001 |
| Pneumonia | 592 (1.89) | 569 (1.95) | 1161 (1.92) | 0.568 |
| SSI | 509 (1.62) | 301 (1.03) | 810 (1.34) | < 0.001 |
| BSI | 131 (0.42) | 101 (0.35) | 232 (0.38) | 0.156 |
| UTI | 129 (0.41) | 91 (0.31) | 220 (0.36) | 0.043 |
| Outcome | < 0.001 | |||
| Alive | 30,883 (98.41) | 28,593 (98.00) | 59,476 (98.21) | |
| Deceased | 500 (1.59) | 585 (2.00) | 1085 (1.79) |
SD: standard deviation; LOS: length of hospital stay; SSI: surgical site infection; BSI: bloodstream infection; UTI: urinary tract infection.
Our comparison of patients hospitalized before and after the COVID-19 pandemic revealed that those hospitalized after the pandemic began had a 16.28% lower risk of acquiring nosocomial infections (p < 0.001). While SSI (p < 0.001) and UTI (p = 0.043) were responsible for this change, HAP (p = 0.568) and BSI (p = 0.156) were not significantly different. In Fig. 1, Fig. 2, Fig. 3, Fig. 4, the most common pathogen causing infections in each of these 4 groups are demonstrated. Hospitalized patients during the pandemic had a significantly higher risk of mortality (25.78%) compared to those hospitalized before the pandemic (p < 0.001), which was also observed among patients with nosocomial infections (17.84%) (p = 0.011) (Table 2).
Fig. 1.
Pathogens causing hospital-acquired pneumonia.
Fig. 2.
Pathogens causing surgical site infection. SSI: surgical site infection.
Fig. 3.
Pathogens causing bloodstream infection. BSI: bloodstream infection.
Fig. 4.
Pathogens causing urinary tract infection. UTI: urinary tract infection.
Table 2.
Characteristics of patients with nosocomial infection.
| Variables | Before pandemic (n = 1361) | After pandemic (n = 1062) | Total population (n = 2423) | p value |
|---|---|---|---|---|
| Gender, n (%) | 0.645 | |||
| Male | 1078 (79.21) | 833 (78.44) | 1911 (78.86) | |
| Female | 283 (20.79) | 229 (21.56) | 512 (21.13) | |
| Age (year), mean (SD) | 45.7 (21.9) | 45.7 (21.2) | 45.7 (21.6) | 0.999 |
| ICU ward incidence, n (%) | 1024 (75.24) | 911 (85.78) | 1935 (79.86) | < 0.001 |
| LOS (day), mean (SD) | 32.5 (22.7) | 31.6 (20.4) | 32.1 (21.7) | 0.330 |
| Outcome, n (%) | 0.011 | |||
| Alive | 1001 (73.55) | 731 (68.83) | 1732 (71.48) | |
| Dead | 360 (26.45) | 331 (31.17) | 691 (28.52) |
SD: standard deviation; ICU: intensive care unit; LOS: length of hosptial stay.
When patients were classified according to the type of nosocomial infection, the male-to-female ratio was almost similar in all groups (4:1), except in patients with UTIs (1.4:1). Also, the highest average age was related to the UTI group (55 years). As shown in Table 1, patients hospitalized during the pandemic were younger (p < 0.001), but the mean age did not differ in any category of nosocomial infections.
Nosocomial infection incidence among patients who were admitted to the ICU increased significantly during the pandemic in the HAP (p = 0.005), SSI (p = 0.045), and UTI (p < 0.001) groups. About 93.61% of patients who developed HAP or BSI were hospitalized in the ICU; this percentage was the lowest among patients with SSI (58.51%). In contrast to other nosocomial infections that showed no significant change, SSI mortality increased significantly during the pandemic (p = 0.055). The highest mortality rate was observed in patients with BSI (37.06%) and HAP (35.65%), and the lowest mortality rate was observed in patients with SSI (16.66%).
Discussion
This study showed that patients who hospitalized after the COVID-19 pandemic began had a 16.28% lower risk of acquiring nosocomial infections compared to hospitalize patients before the pandemic. SSI and UTI rates significantly decreased after the outbreak, while HAP and BSI rates did not change dramatically. Although the length of stay decreased for all patients during the pandemic, the admission time for nosocomial infections did not change. The incidence of nosocomial infection increased after the onset of the COVID-19 pandemic in the ICU. The overall mortality rate was 1.79%, while 28.52% of all patients with nosocomial infections died. During the pandemic, patients with nosocomial infections had a significantly higher risk of mortality (17.84%) compared to those before the pandemic.
Our results demonstrated that the nosocomial incidence rate after the pandemic compared to before it was 0.84. A study in China reported the same results and a decrease in fatal cases of hospital-acquired infection.20 In 2018, the incidence of nosocomial infection in Iran was 4.5%21; after the COVID-19 outbreak in 2019, this number declined9. Standard handwashing, more protective equipment and health care staff per patient during the pandemic, following infection control protocols, and educating personnel on this matter can be reasons for this decrease.20,22
Our study showed the risk of mortality was significantly higher (25.78%) for patients who were hospitalized during the pandemic as compared to those who were hospitalized before it. This trend was also observed among patients who acquired nosocomial infections during the pandemic (17.8%). The patients with BSI and HAP had the highest mortality rates, whereas those with SSI had the lowest rates. This could be due to the novelty of the virus and the lack of knowledge about effective measures against it at the beginning of the pandemic. Even after enough information was gained on the virus, the shortage of resources and staff during the peaks could have affected the adherence to protective protocols and resulted in more transmission of the COVID-19 from other patients, thus increasing the mortality rate.23,24 Also, trauma hospital policies after the start of the epidemic were geared towards the earlier discharge of patients who suffered from less severe injuries. Therefore, patients who stayed longer in the hospital and were more susceptible to nosocomial infection had more severe injuries and, as a result, were more likely to die.
The present study showed a significant decrease in the SSI incidence rate after the pandemic. Other studies report the same finding.9,25 SSI is the second most frequent nosocomial infection, and the leading microorganism causing, it is Staphylococcus aureus.26 However, the most frequently isolated microorganism from our patients was Coagulase-negative staphylococcus. About 2% – 5% of patients who undergo surgery will develop SSI. Still, this number can rise to 20%, depending on the procedure and the setting.26,27 In developing countries, the incidence rate of SSI is higher due to a lack of resources and infection control surveillance.28 Therefore, the more strict protocols during the pandemic can be the reason for the reduction in SSI numbers.25 In addition, during the COVID-19 outbreak, many elective surgeries were canceled, and the overall number of surgeries declined.14 This can be another explanation for the SSI decline after COVID-19.
According to our findings, the incidence of UTI decreased significantly following the emergence of COVID-19. This is in line with results from another study in Iran9, while a Chinese study reports no change in the UTI incidence in their center20. The most frequently isolated pathogens from our patients were Escherichia coli and Klebsiella. Applying infection control protocols and hand hygiene, which were emphasized during the pandemic, has proved effective in reducing UTI.29
BSI is associated with a high mortality rate, especially in ICU, due to multidrug-resistant microorganisms.30,31 A study in the United Kingdom reported a significant decrease in Enterobacterales bacteraemias and a considerable increase in Coagulase-negative staphylococcu-related BSI during a COVID-19 peak in the United Kingdom. Their explanation was that the staff was unfamiliar with performing procedures in uncomfortable personal protective equipment and, therefore, performed more failed or unsterile venipuncture.32 Another reason can be the increased request for blood cultures during the outbreak due to the febrile nature of the disease.33 In contrast, the BSI incidence rate did not appear to change after or before the COVID-19, and the most common microorganism causing BSI in our patients was Coagulase negative staphylococcus. Implementing and maintaining a catheter care practice reduces BSI incidence.34 Strict adherence to these protocols before the pandemic may explain our center's stable and low incidence of BSI.
HAP comprised the most considerable portion of our nosocomial infections in this study. The incidence of nosocomial pneumonia did not have a statistically significant change after COVID-19 compared to before it. However, Su et al.20 reported a significant decrease in hospital-acquired respiratory infections, particularly infections caused by Acinetobacter and fungi, in a center in China. In this study, the nosocomial infection rate in the ICU ward decreased in number but increased in proportion during the pandemic. Most of our nosocomial pneumonia patients were admitted to the ICU, and the most frequently isolated pathogens from our pneumonia patients were Acinetobacter and Klebsiella. Su et al.20 reported a decrease in nosocomial infection incidence in every ward except for the ICU after the COVID-19 incidence.
The incidence of nosocomial infections in ICU is higher than in other wards despite fewer patients. The longer length of stays of patients in these wards can cause this rise.35,36 On the other hand, nosocomial infections significantly increase the length of hospital stays and mortality, creating a vicious cycle. The ICU length of stay and mortality rate for patients with nosocomial infection is 14.4 days and 25.14%, respectively, compared to 5.4 days and 10.57% in ICU patients without them.37 Mechanical ventilation duration can affect patients negatively regarding nosocomial infections and survival.36 VAP can occur in 9% – 27% of mechanically ventilated patients38, and 86% of all nosocomial pneumonias are related to mechanical ventilation.39 Effective infection control strategies, medical team training, appropriate use of personal protective equipment, appropriate handwashing, noninvasive mechanical ventilation when possible, suctioning the secretions, oral hygiene, and adherence to ventilator-related protocols can reduce VAP incidence.9,40
Our study population includes patients admitted to a trauma referral center in surgical wards and ICUs. We collected data from 21 months before the COVID-19 pandemic until 21 months after its incidence. A total of 60,561 patients were evaluated, and 2423 patients entered the study. The size of this study's population and the almost 4-year data collection period strengthen the results' reliability. Still, this study also has limitations. Post-pandemic mortality rates have increased, and we theorize that this is due to an increased percentage of critically ill patients. Still, we do not have data on their injury severity, such as injury severity score or trauma and injury severity score, to support our theory. Also, the impact of COVID-19 infection on nosocomial infections could not be assessed in our study due to the lack of data on polymerase chain reaction test results. Unfortunately, we did not have access to patients' length of ICU stay, which could help us better analyze our data.
The incidence of nosocomial infection has decreased during the pandemic, possibly due to the use of more personal protective equipment and modified protocols (earlier discharge of stable trauma patients and restricted visiting hours) after the outbreak. This can also be the result of changes in the behavior of individuals in society (more hand washing and increased use of hand sanitizers and masks). Although the pandemic appears to be almost under control, continued use of these protocols after they have been adapted for the post-pandemic era can help reduce the burden on the health system and the economy by reducing the incidence of nosocomial infections.
Funding
This study was funded by the Vice-chancellor for Research and Technology of Shiraz University of Medical Sciences (contract number 22269).
Ethical statement
Ethical approval was obtained from the Institutional Review Board and Research Ethics Committee of Shiraz University of Medical Sciences (Ethical number: IR. SUMS.REC.1400.166).
Declaration of competing interest
The authors declare that they have no competing interests.
Author contributions
Mahnaz Yadollahi: Conceptualization, methodology, resources, writing - review & editing.
Mahsa Ahadi: Methodology, writing - original draft, writing - review & editing.
Amir Hossein Shams: Methodology, formal analysis, resources, writing - original draft, writing - review & editing.
Footnotes
Peer review under responsibility of Chinese Medical Association.
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