Clostridioides difficile in COVID-19 Patients, Detroit, Michigan, USA, March–April 2020

We describe 9 patients at a medical center in Detroit, Michigan, USA, with severe acute respiratory syndrome coronavirus 2 and Clostridioides difficile. Both infections can manifest as digestive symptoms and merit screening when assessing patients with diarrhea during the coronavirus disease pandemic. These co-infections also highlight the continued importance of antimicrobial stewardship.

Detroit Medical Center (Detroit, Michigan, USA). We screened patients by using TheraDoc software (https://www.theradoc.com) during March 11-April 22, 2020. We abstracted data regarding baseline demographics, medical history, symptoms, laboratory values, microbiologic findings, concomitant antibiotic use, and treatment for CDI. We obtained institutional review board approval for this study.
We identified 9 cases of co-infection with SARS-CoV-2 and C. difficile. This cohort mainly included elderly patients who were predominantly female (Table). The rate of CDI at the center was 3.32/10,000 patientdays during January-February 2020 and increased to 3.6/10,000 patient-days during March-April 2020.
We noted prior CDI in 3 patients; these infections occurred 1-4 months before admission. All patients were confirmed to be positive for C. difficile by PCR and showed symptoms of diarrhea in addition to other characteristic signs and symptoms, such as abdominal pain, nausea, and vomiting. Two patients had diarrhea and were found to be positive for C. difficile at admission, whereas the remaining 7 had onset of diarrhea only after COVID-19 diagnosis; median duration from CDI diagnosis to COVID-19 diagnosis in these 7 patients was 6 days. This group of patients  were severely ill, having high ATLAS scores (https:// www.mdcalc.com/atlas-score-clostridium-difficileinfection) and multiple underlying conditions; hypertension (n = 8) and diabetes (n = 5) were the most frequent of these conditions. Three patients received antibiotics in the month before admission; 8 received antibiotics at admission. One patient was initiated on antibiotics on day 15; this patient was also receiving antibiotics the month before admission. The most commonly administered antibiotics were cefepime (n = 5), ceftriaxone (n = 3), meropenem (n = 2), and azithromycin (n = 2). Specific CDI therapies were oral vancomycin (n = 6); vancomycin and intravenous metronidazole (n = 1); no treatment (n = 1); and a combination of oral vancomycin, intravenous metronidazole, rectal vancomycin, fidaxomicin, and fecal microbiota transplantation (n = 1). One patient who did not receive antibiotics was considered to be colonized with C. difficile. Four (44.4%) patients died during hospital admission, 1 (11.1%) was discharged to hospice, 1 (11.1%) is still hospitalized, and 3 (33.3%) were discharged to a longterm care facility.
CDI is a challenging disease, with a recurrence rate of 15%-20% and a mortality rate of 5% (8). When CDI is present as a co-infection with COVID-19, CDI therapy can be difficult to monitor if diarrhea persists because of COVID-19.
These cases highlight the importance of judicious use of antibiotics for potential secondary bacterial infection in patients with COVID-19. Antibiotics are known to have unintended consequences, such as C. difficile infection. All 9 patients received antibiotics; the median duration of antibiotic use before PCRpositive CDI was 5 days. All patients in our cohort were elderly, an age group at higher risk for complications from overuse of antibiotics, such as adverse events, antibiotic resistance, and concomitant infections like CDI (9). Secondary infections on top of CDI can increase the risk for death in patients with severe COVID-19; in this cohort, 4 patients died and 1 was discharged to hospice. To prevent CDI co-infections during the COVID-19 pandemic, integrated use of antimicrobial stewardship is needed to monitor appropriate antibiotic use.
Symptoms of CDI can complicate diagnosis of COVID-19 because both conditions can have similar manifestations; in a study of 206 COVID-19 patients, 19.4% had diarrhea as the first symptom onset (10). Of the 2 patients who had CDI diagnosed at admission, 1 patient solely had gastrointestinal symptoms, which possibly led to delayed diagnosis of COVID-19. Both COVID-19 and CDI should be considered when evaluating patients with diarrhea during the COV-ID-19 pandemic. Distinguishing between actual CDI versus colonization also is vital; 1 patient in our cohort was colonized. A limitation of this study is the small number of cases. However, in the face of the COVID-19 pandemic and the extensive use of antibiotics, clinicians should remain aware of possible CDI and SARS-CoV-2 co-infection. G.T. is a consultant to Melinta, Crestone, Ferring, AirMmax, and Shionogi. Other authors in the manuscript have no relevant conflict of interest or financial disclosure. No funding was needed for this manuscript.

About the Author
Dr. Sandhu is an infectious diseases-epidemiology fellow at Detroit Medical Center, Wayne State University School of Medicine. Her current research interest is in multidrugresistant hospital-acquired infections. I n late 2019, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) emerged in China (1), spreading primarily through droplets and contact with respiratory secretions or fecal materials (2,3). It has been shown that SARS-CoV-2 remains viable on plastic and stainless steel for 72 hours (4), and SARS-CoV on wood for 60 hours (5). Chopsticks have been essential eating utensils for >3 millennia, particularly in Asia, and are made mainly of wood and plastic; metal chopsticks are found in some countries, such as South Korea. Personal chopsticks are often used to pick food from communal dishes. We investigated whether chopsticks could be a potential vehicle of transmission for SARS-CoV-2.
We recruited 5 consecutive patients admitted for isolation and care at our hospital: 1 patient who was asymptomatic, 2 whose symptoms had subsided, 1 with moderate coronavirus disease (COVID-19) caused by SARS-CoV-2 infection, and 1 with severe COVID-19. Before mealtimes, each patient was given a pair of wooden chopsticks packed in a sealed plastic bag. These chopsticks are widely available in Hong Kong, including in canteens of public hospitals. They are made of plain wood, not bamboo, and not painted with color or lacquer. After mealtimes, we collected the used chopsticks. We dipped the tips of the chopsticks in 1 mL of phosphate-buffered normal saline and shook them for 30 sec to release saliva and oral fluid. We detected SARS-CoV-2 RNA by quantitative reverse transcription PCR (6). We collected serial sputum samples and nasopharyngeal and throat swabs to document respiratory shedding and for comparison of viral RNA concentrations among specimen types. The Joint Chinese University of Hong Kong-New Territories East Cluster Research Ethics Committee approved this study.
Patient A, 47-year-old woman, was a close contact of a confirmed case-patient. Her diagnosis was based on a surveillance throat sample collected during quarantine. She was admitted to the hospital for isolation and appeared asymptomatic throughout her stay. A pair of chopsticks collected 2 days after admission (12 days after her last exposure) was positive for SARS-CoV-2 RNA (Figure). Two respiratory samples collected after admission were also positive. High-resolution computed tomography (HRCT) of her lungs revealed small consolidations and groundglass opacities in both lower lobes, left upper lobe, and right middle lobe. Patient B, a 22-year-old woman, had a runny nose, headache, and fever develop on the day she returned from Europe. Her symptoms subsided after admission. Two chopsticks collected 1-2 days after symptoms had subsided were positive for SARS-CoV-2 RNA (Figure). Viral RNA was detected from respiratory specimens until 8 days after symptoms had subsided. HRCT revealed small patchy groundglass opacity in the anterior segment of the left upper lobe of the lungs.
Patient C, a 67-year-old man with hypertension and minor coronary artery disease, had fever, cough with whitish sputum, and loose bowel movements develop 2 days after returning from Europe. Chopsticks collected 5 and 7 days after illness onset were positive for SARS-CoV-2 RNA (Figure). All respiratory 2274 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 26, No. 9, September 2020

RESEARCH LETTERS
We detected severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) RNA on disposable wooden chopsticks used by 5 consecutive asymptomatic and postsymptomatic patients admitted for isolation and care at our hospital. Although we did not assess virus viability, our findings may suggest potential for transmission through shared eating utensils.