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Severe acute respiratory syndrome coronavirus 2 antibody prevalence in adult patients with short bowel syndrome—A German multicenter cross‐sectional study

Abstract Background Not all patients suffer from a severe course of severe acute respiratory syndrome coronavirus 2 (SARS‐CoV‐2) infection, demanding a definition of groups at risk. Short bowel syndrome (SBS) has been assumed to be a risk factor, because of the complexity of disease, the need for interdisciplinary care, and frequent contact with caretakers. We aimed to establish data on the course of infection and prevalence of SARS‐CoV‐2 seropositivity in SBS patients in Germany. Methods From January 2021 until January 2022 a total of 119 patients from three different tertiary care centers with SBS were included. All patients received an antibody test against the nucleocapsid (N) antigen and were asked to fill out a questionnaire, which included frequency of contact with medical personnel, risk behavior and worries. Results Sixty‐seven percent of SBS patients received parenteral nutrition with a median of 6 days per week. The seroprevalence of SARS‐CoV‐2 antibodies was 7.6% (n = 9). Seven patients with positive antibodies had coronavirus disease 2019 (COVID‐19) with a mild course. None of the patients were hospitalized or needed further treatment. There was no difference in willingness to take risks in SARS‐CoV‐2 antibody–positive and –negative patients (P = 0.61). Patients were predominantly worried about the economy (61%) and transmitting COVID‐19 (52%), less frequent (26%) about receiving insufficient medical treatment. Conclusion These are the first clinical results concerning SARS‐CoV‐2 seropositivity and COVID‐19 disease in patients with SBS. The seropositivity is comparable to national data, which we attribute to increased risk awareness and avoidance. Further studies are warranted to investigate effects of COVID‐19 infection in SBS patients.


CLINICAL RELEVANCY STATEMENT
Patients with short bowel syndrome (SBS) are proposed to be a group at high-risk for a severe course of coronavirus disease 2019.
This multicenter cross-sectional study analyzes the prevalence of antibodies against the nucleocapsid antigen in patients with SBS, their risk behavior and frequency of contact with medical personnel. The overall severe acute respiratory syndrome coronavirus 2 seropositivity in SBS patient was comparable to national data, possibly attributed to increased risk awareness and avoidance. infection, symptomatic or asymptomatic, causes a rapid antibody response. 3 Measurement of the nucleocapsid (N) antigen against SARS-CoV-2 is therefore an adequate tool to quantify the spread of the virus in a population. 4 Of particular clinical relevance are seroprevalence studies concerning patient groups at risk, which tend to have more severe cases of COVID-19, potentially requiring intensive care or even dying from COVID-19. Patient groups at higher risk of a severe course of COVID-19 are people of older age, people living in long-term care facilities, and people with underlying health conditions such as diabetes, chronic kidney disease, or a chronic respiratory disease.
Several national and international guidelines 5,6 have highlighted the need for prioritization of vaccination in these subgroups as well as allocation of medical care. Although these risk groups have been adequately researched thus far, 7 data on orphan diseases such as short bowel syndrome (SBS) and SARS-CoV-2 seroprevalence are lacking.
SBS is a result of surgical reduction of the small intestine and consequently of the absorptive surface area. The majority of SBS patients require long-term parenteral nutrition if oral autonomy cannot be achieved. 8 Complications of parenteral nutrition include catheter-associated bloodstream infections, thrombosis, and intestinal failure-associated liver disease. 9 Furthermore, individual parenteral nutrition is vital to adequately manage nutrition and metabolic needs of the patients. Patients with SBS require interdisciplinary care and therefore frequent contact with caretakers, even in times of contact restrictions to prevent the spread of COVID-19.
The combination of malnourishment in some cases, frequent caretaker contact and SBS as a disturbance of the immune system itself result in patients with SBS being categorized as high-risk patients regarding COVID-19, although reliable data are missing. 10,11 Therefore, we aimed to establish data on prevalence of seropositivity for SARS-CoV-2 antibodies in a subgroup of SBS patients in Germany and assess data on their clinical course of COVID-19. Additionally, we tried to identify risk factors as well as protective factors in SBS patients with a previous case of COVID-19.

Study design
Patients with SBS managed at three tertiary care centers across

Statistical analysis
Statistical analysis was performed with R version 4.

Patient population
Over the 13-month study period, 119 patients from three different German tertiary care centers were included in the study. More patients were female (67%). Median patient age was 60 years (IQR, 25.5 years), and the median patient BMI, 20.99 kg/m 2 (IQR, 5.15 kg/ m 2 ). Most common etiology for SBS was ischemia (20%) followed by ileus and surgical complications (Table 1). A third of patients (36%) had a stoma, and 67% of patients required parenteral nutrition with 6 days (IQR, 7 days) per week on average.
Sixty-six percent of patients were retired or disabled, and of those who worked, 32% performed exclusive home office at study time. Only few patients had respiratory symptoms such as a cough or running nose at time of presentation or within the last 6 months prior to the routine visit at the SBS center.

Risk behavior and patient worries
There was no significant difference in willingness-as assessed by the standardized questionnaire-to take risks in patients that were SARS-CoV-2 antibody-positive and those that were not (4.5 [IQR,  Study). 16,17 All the infections in our SBS cohort had mild clinical courses, with two patients having no symptoms at all. This would be unexpected in a group of high-risk patients. There has been discussion about an improvement of micronutrient supplementation, that is, with zinc, selenium, and vitamin D to reduce low-grade inflammation and therefore raising antiviral resistance against COVID-19. [18][19][20] Although highly speculative, it is possible, that adequate parenteral nutrition with a heightened awareness for micronutrition contributed to milder courses of COVID-19 in our study population.
Worrying was a relevant topic for patients with SBS.
With high and very high subjective worry concerning the economy, COVID-19 transmission, and receiving insufficient medical treatment. Especially reassuring patients that they will get adequate treatment can be difficult due to changing contact restrictions and, in some cases, delayed outpatient appointments.
Financial aspects played a further role for our SBS patients. With many patients in early retirement and currently rising costs of living in many major German cities. These aspects were, however, not associated with seropositivity for SARS-CoV-2.
Seroprevalence studies vary greatly depending on study region, study population and study time point. 14,21 Our study duration of one year saw the appearance of two new SARS-CoV-2 variants, namely Delta and Omicron, both with their individual infection peaks. 22 Furthermore, severity of disease varied greatly with the emergence of the omicron variant.
The relatively small sample size of nine infected patients and their mild course of disease might therefore not adequately represent the severity of disease. Additionally cross-sectional data on vaccination, at a time of new implementation, may not adequately reflect the status quo. Nevertheless, we managed to achieve a formidable sample size despite SBS being an orphan disease and propose at least some transferability of our study data.