Complications of healthcare-associated infections have been reported in patients with coronavirus disease 2019 (COVID-19). We encountered a case of ventilator-associated pneumonia and lung abscess, complicated with Staphylococcus aureus bacteremia and multiple abscesses, in a patient with COVID-19. Streptococci and anaerobes were cultured from the sputum, which was considered to be the causative organism of the lung abscess. In the management of severe COVID-19, care should be taken to prevent complications of healthcare-associated infections; when secondary respiratory tract infections are suspected, the presence of lung abscess and anaerobic culture should be considered

Fujikura, Hiroyuki

Fukumori, Tatsuya

Furukawa, Ryutaro

Imakita, Natsuko

Kasahara, Kei

Nishihara, Yuji

Nishimura, Tomoko

Okuda, Nao

Sekine, Takahiro

Yamaguchi, Naoki

English

Global Institutional repository of Nara Medical University

(79) A CASE OF CORONA VIRUS DISEASE 2019 COMPLICATED BY VENTILA TOR-ASSOCIATED PNEUMONIA， LUNG ABSCESS， AND STAPHYLOCOCCUS AUREUS BACTEREMIA NAO OKUDA NAOKI YAMAGUCHI， TAKAHIRO SEKINE， YUJI NISHIHARA RYUTARO FURUKAWA HIROYUKI FUJIKURA TATSUYA FUKUMORI， TOMOKO NISHIMURA， N A TSUKO IMAKIT A. and KEI KASAHARA aCenter /0γIn/ectious Dise庇ses0/ Nara Medical ui耳切りsityReceived August 2， 2022 Abstract Complications of healthcare-associated infections have been reported in patients with corona-virus disease 2019 (COVID-19). We encountered a case of ventilator-associated pneumonia and lung abscess， complicated with Staphylococcus aureus bacteremia and multiple abscesses， in a patient with COVID同19.Streptococci and anaerobes were cultured from the sputum， which was considered to be the causative organism of the lung abscess. In the management of severe COVID-19， care should be taken to prevent complications of healthcare-associated infections; when secondary respiratory tract infections are suspected， the presence of lung abscess and an-aerobic culture should be considered. Keywords: COVID-19， lung abscess， Staρhylococcus aureus， healthcare-asociated infection Introduction Coronavirus disease 2019 (COVID-19) isstil prevalent worldwide after first being reported in China in December 2019. Sever色 acuterespiratory syndrome coronavirus 2 (SARS-CoV-2) infects the lower respiratory tract and causes pneumonia. Moreover， various other complications have been reported， such as neurological symptoms1>， thrombosis21， and bacterial infections31• Influenza virus has been reported to facilitate complications of bacterial infections， especialy those caused by Sta.ρhylococcus aureus and Streρtococcus ρneumoniae41• However， the mechanisms of bacte-rial infection remain unclear in COVID-19， and a low frequency of complications with S. aureus infection31 in COVID-19 has been reported. We report a case of ventilator-associated pneumonia and lung abscess caused by oral flora， complicated with S. aureus bacteremia and multiple abscesses in a patient with COVID-19. Case A 52-year-old man with a history of treatment for unstable angina， underlying hypertension， and dyslipidemia had a fever of > 3r C and fatigue. He had no history of smoking. He under-went a SARS-CoV-2 loop-mediated isothermal amplification test， which was positive; thus， he (80) Nao OKUDA et al was diagnosed with COVID-19. The next day. the patient was admitted to the hospital. Chest radiograph revealed no infiltration shadow. Hypoxemia progressed 4 days later. and dexametha sone and favipiravir were initiated. Nine days after symptom onset. hypoxemia exacerbated. and he was transferred to our hospital. Upon arrival at our hospital. he had severe hypoxia with Sp0295% (02 8 L/min) and an infil-trative shadow on the chest radiograph. Blood tests showed elevated levels of white blood c巴ls(WBC) and C-reactive protein (CRP) (Table 1). He was admitted to the intensive care unit (ICU) and immediately intubated. Remdesivir and dexamethasone were administered. Oxygenation Table 1. Laboratory test resllts on admission DaylS on discharge WBC (/μL) 10900 13500 8100 Hgb (g/dL) 13.0 11.1 9.5 PI， (x104/μL) 25.0 2.4 43.6 D-D(μg/mL) 1.6 CRP (mg/dL) 7.27 14.39 1.06 AST (U/L) 46 25 14 ALT (U/L) 53 57 LDH (U/L) 433 261 196 CK (U/L) 41 46 24 BUN (mg/dL) 21 15 Cre (mg/dL) 0.72 0.52 0.58 Na (mEq/L) 135 133 142 K(mEq/L) 4.6 3.6 3.7 Cl (mEq/L) 104 102 103 Amy (U/L) 77 643 16 Fig.lb. Fig.1 Fig.1. Chest compllted tomography (CT) on day 15 (a)， day 16 (b). day 22 (c). and day 115 (d) a: Non-contrast CT showing bilateral infiltrative shadow b: Contrast CT showing a large number of low-density areas in the infiltrating shadows with air bronchogram c: Contrast chest compllted tomography on day 22 Encapsulated f1uid retention on the left side of the aortic arch and pleural effusion in the right pleural cavity. d: Chest computed tomography on day 115 The infiltrative shadows in the bilateral lower lobes improved and low-density areas disappeared A CASE OF CORONAVIRUS DISEASE 2019 COMPLICATED BY VENTILATOR-ASSOCIATED PNEUMONIA， LUNG ABSCESS， AND STAPHYLOCOCCUS AUREUS BACTEREMIA (81) improved， and he was extubated on day 13 of ventilation. The infiltrative shadows seen on the bilaterallower lung fields improved but persisted at th巴timeof transfer to a general ward. On day 15 of hospitalization， amylase levels were elevated (Table 1)， and non-enhanced com-puted tomography (CT) of the abdomen was performed to investigate the cause. Because the pancreatic head was enlarged， the patient was suspected to have pancreatitis， and fasting and infusion therapy were initiated. The lung field on CT showed a bilateral infiltrative shadow (Fig. la). Abdominal contrast-enhanced CT was performed the folowing day to evaluate the severity of pancreatitis. Although the images showed an enlarged pancreatic head， pancreatitis was ruled out. However， on air bronchogram， a large number of low-densitiy areas were observed in the infiltrating shadows that could be considerd multiple abscesses (Fig. lb). Piperacillin-tazobactam was administered (4.5 g every 6 h) after collecting sputum and blood cultures. S. aureus was detected in the blood culture. Streρtococcus dysgalactiae， Prevotela melaninogenica， Prevotela oris， and Fusobacterium nucleatum were isolated from sputum samples colected at the same time. However， S. aureus was detected in the sputum colected the next day. On day 19 of hos-pitalization， he was readmitted to the ICU and reintubated. Blood cultures taken on the third day of treatment were negative. Antimicrobial drugs wer巴 changedto ampicillin-sulbactam (3 g every 6 h) based on S. aureus susceptibilty. During the course of treatment， antimicrobial agents were changed to the folowing due to suspected drug sid巴 effects:cefazolin (2 g， every 8 h) against S. aureus and clindamycin (600 mg， every 8 h) against anaerobic bacteria. On day 23 of hospitalization， there was no worsening of仕lelow-density areas of the lung， but a fluid col-lection adjacent to the aortic arch appeared to be an absces. This was not present in the pre-vious imaging studies (Fig. lc). Right thoracic drainage was performed on day 24. The drained specimen culture was negative. Tracheostomy was performed and mechanical ventilation was weaned of after 22 days. On day 43 of hospitalization， he was transferred to the general ward. Antimicrobial agents were switched to oral form (cefalexin 500 mg thrice a day and clindamycin 300 mg thrice a day) after 7 weeks of intravenous infusion. The patient was discharged on the 78th day of hospitalization. The CT before discharge and the follow-up CT 39days after discharge showed that the abscess adjacent to the aortic arch was gradually shrinking and low-density areas and infiltration in the right lower lobe had disap peared (Fig. ld). Antimicrobial agents were administered for 7 months， and antimicrobial ther apy was terminated after the absence of the low-density areas and abscess were confirmed on imaging. Analysis of the pathogen-related genes of S. aureus showed that the major toxin genes (enterotoxin， TSST-l， and PVL) were not retained. The coagulase gene sequence showed that itwas of type Vb. Multi-locus sequence typing analysis revealed that it was ST188 Discussion We encountered a case of ventilator目associatedpneumonia and lung abscess caused by oral flora， complicated with S. aureus bacteremia and multiple abscesses in a patient with COVID-19. Secondary bacterial pneumonia folowing viral infection is wel known in the case of influerトza5). This is caused by damage to the airway mucosa caused by the influenza virus and usualy develops 4 to 14 days after the improvement of influenza infection. The most common causative (82) Nao OKUDA et al. microorganisms have been S.ρneumoniae and S. aureus. Although no increase in second ary bacterial infections similar to those of influenza cases have b巴enreported for COVID-19. COVID-19 has been associated with a high frequency of healthcare-associated infections such as ventilator-associated pneumonia and intravascular catheter-associated bloodstream infections6.71. In this case of severe COVID-19. ventilator-acquired pneumonia developed and a lung abscess was subsequently confirmed by contrast-enhanced chest CT. The cause of the increase in healthcar巴associatedinfections in COVID-19 has not yet be巴nfully studied. It is believed that in addition to needing intensive medical care in sever巴 cases.health care workers are required to wear personal protective equipment such as gloves and gowns while performing cl巴anand aseptic operations. Furthermore. because of this requirement. it is easy for them to neglect hand disinfection and replacement of personal protective equipment. which is thought to be one of the reasons for horizontal transmission of microorganisms and bacterial contamination of sterile ar eas. The present case was diagnosed as multiple lung abscesses on chest CT on the 27'h day of COVID-19. Although the patient was on ventilator managem巴ntfrom the ninth day to the 20th day of the disease. he was mananged without antimicrobial agents because he originally had ab-normal shadows in the lung fields caused by COVID-19. and a portable chest radiograph did not reveal any new lung lesions. Plain chest CT showed infiltrative shadows with pleural effusion and air bronchograms in both dorsal lower lung fields. and contrast-enhanced CT showed multiple abscesses. Clancy et al. summarized 75 studies including 621 cases with autopsies in COVID-19 and reported that 3.5% had lung abscesses81• Blonz et al. reported in a review of 188 ventilator守associatedpneumonia cases that 1.4% had lung abscesses91. Similarly. Beaucote et al. reported that out of the 57% of ventilator-requiring COVID-19 patients who underwent chest CT. 14% had lung abscesseslOl. It is possible that the actual incidence of lung abscesses may be lower than that estimated because contrast-巴nhancedCT of the chest may be required for its diagnosis. as in this case. COVID-19 may be difficult to evaluate on chest imaging because of the presenc巴 ofabnormal chest shadows due to the primary disease. COVID-19. If a lung abscess is present. the duration of antimicrobial therapy should be extended. and chest imaging should be carefully evaluated. Chest contrast-enhanced CT should be considered to exclude lung abscesses. especially in the case of recurrent or refractory pneumonia Beaucote et al. reported that Pseudomonas aeruginosa. Enterobacteriaceae. and S. au reus were the most common bacteria detected in a study of 17 lung abscesses complicated by COVID-19101. Ippolito et al. conducted a systematic review and meta-analysis of studies on ven-tilator-associated pneumonia among COVID-19 patients and reported that the most common bacteria detected were Enterobacteriaceae and glucose non-fermenting bacteria. In our case. in addition to Str.φtococcus dysgalactiae equisimilis. two species of Prevotella sρρand anaerobic bacteria. such as Fusobacterium nucleatum. were detected It is well known that lung abscesses are caused by commensal bacteria in the oral cavity such as streptococci and anaerobes; anaerobic culture is not performed in some hospital clinical laboratories. and this may have been und巴restimatedin the study of causative microorgan-A CASE OF CORONAVIRUS DISEASE 2019 COMPLICATED BY VENTILATOR-ASSOCIATED PNEUMONIA， LUNG ABSCESS， AND STAPHYLOCOCCUS AUREUS BACTEREMIA (83) isms in pneumonia complicated with COV1D-19. Rattanaburi et a1. r巴portedthat patients with COV1D-19 had a wider variety of oral flora， including Streρtococcus sρecies and Prevotella spe-cies， than patients with influenza infectionll 1t has also been reported that the amount of Prevotela sρρcorrelates with the s巴verityof COV1D-1912l. Based on these findings， itis important to consider the involvement of anaerobic bacteria in addition to Enterobacteriaceae， non-fermenting gram-negative bacteria， and S. au-reus， which are report巴dto .be common in severe COV1D-19 ventilator-associated pneumonia and lung abscess in particular This case was also complicated with S. aureus bacteremia. Although S. aureus was only ini田tialy detected in the blood culture， itwas later detected in the aspirated sputum. 1t is possible that colonization of S. aureus was horizonatlly transmitted during the course of the disease， first causing bacteremia and subsequently invading the respiratory tract to alow detection in the respiratory specimen; however， it is also possible that S. aureus migrated from the blood vessels into the alveolar space in conditions such as septic pulmonary embolism and became one of the microorganisms causing lung abscess. 1tis also possible that S. aureus is a microorgan-ism that causes lung abscesses. 1n this case， lesions that appeared to be abscesses on the chest wall and aortic arch suggested multiple abscesses associated with S. aureus bacteremia. The ST type of S. aureus detected in this case was ST188， which is relatively common in Southeast Asia and does not produce toxins such as TSST-l or PVL， but itis important to note that multi-ple abscess formation is a common characteristic of S. aureus infectionl3l. 1n conclusion， we encountered a case of severe COV1D-19 complicated with a pulmonary abscess caused by oral commensal bacteria， including anaerobic bacteria， after ventilator man-agement that was further complicated with S. aureus bacteremia and multiple abscesses. 1n the management of severe COV1D-19， care should always be taken to prevent complications of healthcare-associated infections; furthermore， when respiratory infections are suspected， the pr巴senceof lung abscesses and bacteremia should be noted Acknowledgements The authors would like to thank J Hisatsune and M. Sugai for their help with the genetic analysis of St~ρhylococcus aureus. Declaration of competing interest None目Ethics statement and informed consent Written consent for case reports isobtained from the patient. References 1) Mao L， Jin H， Wang M， Hu y， Chen S， He Q， Jiang C， Candong H ， Yifan Z ， David W. Xiaoping M， Yanan L， Bo H. : Neurologic manifestations of hospitalized patients with coronavirus disease 2019 in Wuhan. China JAMA Neurol. 77:683・90，2020.2) Helms J.Tacquard C. Severac F. Leonard Lorant I. Ohana lVI. Delabranche X可 MerdjiH， Clere J ehl R， (84) Nao OKUDA et al Schenck M， Gandet FF， Faf Kremer S， Castelain V， Schn巴iderF， Grunebaum L， Angles Cano E， Sattler L， Mertes PM， Meziani F and CR1CS TR1GGERSEP Group. : High risk of thrombosis in patients with severe SARS-CoV-2 infection: a multicenter prospective cohort study. 1ntensive Care Med. 46:1089-98， 2020. 3) Langford BJ， So M， Raybardhan S， Leung V， Westwood D， MacFadden DR. Soucy ]PR. Danemanl N. Bacterial co-infection and secondary infection in patients with COVID-19: a living rapid review and meta analysis. Clin Microbiol 1nfect. 26:1622-1629， 2020. 4) Chertow DS， Memoli M]. : Bacterial coinfection in influenza: a grand rounds review. ]AMA. 309・275-282，2013. 5) Rothberg MB， Haessler SD， Brown RB. : Complications of viral influenza. Am ] Med. 121・258ω264，2008.6) 1ppolito M， Misseri G， Catalisano G， Marino C， Ingoglia G， Alessi M， Consiglio E， C Gregoretti ， Giarratano A， Cortegiani A. : Ventilator-associated pneumonia in patients with COV1D-19・Asystematic r巴Vl巴wand meta analysis. Antibiotics (Basel). 10・545，2021 7) O'Toole RF. : The interface between COVID-19 and bacterial healthcare-associated infections. Clin Microbiol 1nfect. 27:1772-1776， 2021. 8) Clancy C]， Schwartz 1S， Kula B， Nguyen MH. : Bact巴rialsuperinfections among p巴rsonswith coronavirus disease 2019: A comprehensive review of data from postmortem studies. Open Forum 1nfect Dis. 8:ofab065， 2021 9) Blonz G， Kouatchet A， Chudeau N， Pontis E， Lorber J， Lemeur A， Planche L， Lascarrou]B， Colin G Epidemiology and microbiology of ventilator-associated pneumonia in COV1D-19 patients: a multicenter retrospective study in 188 patients in an un-inundated French region. Crit Care. 25・72，2021. 10) Beaucote V， Plantef，色veG， Tirolien ]A， Desaint P， Fraisse M， Contou D. : Lung abscess in critically il coro-navirus disease 2019 patients with ventilator-associated pneumonia: A French monocenter retrospective study. Crit Care Explor. 3・e0482，2021. 11) Rattanaburi S， Sawaswong V， Chitcharoen S， Sivapornnukul P， Nimsamer P， Suntronwong N， Puenpa]， Poovorawan Y， Payungporn S. : Bacterial microbiota in upper respiratoryむactof COVID-19 and influenza patients. Exp Biol Med (Maywood). 247:409-415， 2022 12) Ventero MP， Cuadrat RRC， Vidal 1， Andrade BGN， Molina-Pardines C， Haro-Moreno ]M， Coutinho FH ， Me-rino E， Regitano LCA， Silveira CB， Afli H， Lopez-Perez M， Rodriguez ]C.: Nasopharyngeal microbial com】munities of patients infected with SARS-CoV-2 That Developed COVID-19. Front MicrobioL 12:637430，2021 l3) Dong Q， Liu Y， Li W， Chen M， Li W， Wang X， Fu J， Ye X. : Phenotypic and molecular characteristics of community-associated Staphylococcus aureus infection in neonates. 1nfect Drug Resist. 13:4589-4600， 2020. 

A CASE OF CORONAVIRUS DISEASE 2019 COMPLICATED BY VENTILATORASSOCIATED PNEUMONIA, LUNG ABSCESS, AND STAPHYLOCOCCUS AUREUS BACTEREMIA

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A CASE OF CORONAVIRUS DISEASE 2019 COMPLICATED BY VENTILATORASSOCIATED PNEUMONIA, LUNG ABSCESS, AND STAPHYLOCOCCUS AUREUS BACTEREMIA

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