Is COVID-19 Still a Threat? An Expert Opinion Review on the Continued Healthcare Burden in Immunocompromised Individuals.

Key Summary Points

Introduction

The emergence of coronavirus disease (COVID-19), caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), has unquestionably left a profound mark on global health and well-being. As of June 2024, more than 700 million cases of SARS-CoV-2 infections have been confirmed worldwide, with a staggering death toll that exceeds 7 million lives lost [ 1 ]. The rapid development of COVID-19 vaccines achieved just months after the pandemic’s onset has been a pivotal factor in controlling the spread of this disease. On May 5, 2023, the World Health Organization (WHO) announced that COVID-19 is no longer classified as a public health emergency, raising the possibility of it becoming endemic in the near future [ 2 ]. Recent data indicate that approximately two-thirds of the world’s population, including 89% of healthcare workers and 82% of adults > 60 years, have received at least two doses of a COVID-19 vaccine, which is a testament to the remarkable progress made in vaccination programs globally [ 2 – 4 ]. Despite the success of vaccination programs, the risk of SARS-CoV-2 infection and severe outcomes remain ongoing challenges, particularly for individuals with immunocompromising conditions—a population in which immunization considered sufficient may not confer adequate benefit [ 5 , 6 ].

Individuals with immunocompromising conditions constitute a heterogenous group who are at high risk of morbidity and mortality due to underlying diseases or ongoing immunosuppressive therapies [ 5 ]. In the United States (US) and United Kingdom (UK), this vulnerable group makes up 2–4% of the total population [ 7 – 9 ]. This prevalence may vary depending on the definition of the underlying immunocompromising population and the assessment of who remains at risk of severe COVID-19 despite vaccination. These individuals often have an inadequate immune response after being vaccinated [ 10 – 12 ], necessitating vaccine booster doses for additional protection [ 10 , 13 ]. Furthermore, these individuals are at a higher risk of experiencing breakthrough SARS-CoV-2 infections, with some studies reporting that > 40% of such cases occur in this population [ 14 – 17 ]. Their immunocompromising condition increases the likelihood of developing severe, potentially life-threatening diseases, and they are particularly susceptible to persistent SARS-CoV-2 infections [ 18 ]. Moreover, individuals who contract COVID-19 have a greater likelihood of developing immunocompromising conditions, such as autoimmune diseases [ 19 ]. Recovery from prior infection can improve prognosis but reinfection can still be challenging for these individuals [ 20 ]. The putative seasonality of SARS-CoV-2 infection poses a challenge in determining the optimal timing and implementation of preventive measures [ 21 ]. Moreover, certain options for preventing and treating COVID-19 in these individuals are limited, especially with the continued emergence of new variants [ 22 ].

Preventing severe infections in immunocompromised individuals involves employing strategies such as vaccination, prophylactic medication, use of face masks, and rigorous hygiene practices [ 23 ]. While vaccination is the primary approach, it may not always provide sufficient protection. The recent US Food and Drug Administration authorization for emergency use of pemivibart for pre-exposure prophylaxis in immunocompromised individuals underscores the urgent need to safeguard this population [ 24 ]. Consequently, many individuals with immunocompromising conditions feel compelled to choose physical and social isolation, which may have a detrimental impact on their mental health, health-related quality of life (HRQoL), and employment prospects. Additionally, those who experience breakthrough SARS-CoV-2 infections have limited treatment options, many of which may not be suitable for those with a compromised immune system [ 25 ].

While the prognosis for individuals with different immunocompromising conditions may vary, symptoms in those with SARS-CoV-2 infection, both from underlying disease and multiple SARS-CoV-2 variants, can have a profound impact. In addition to acute symptoms, post-viral syndromes, such as long COVID or post-acute sequelae of COVID-19, have become prevalent [ 26 , 27 ]. Individuals with weakened immune systems face elevated risks of breakthrough and severe COVID-19 compared with the general population, rendering them more vulnerable to long COVID. Those with immunocompromising conditions who experience long COVID may suffer from severe physical and mental health consequences [ 26 ].

Individuals with immunocompromising conditions are at a particularly higher risk of hospitalization and death from COVID-19 compared with the general population. The management of COVID-19 in these individuals is associated with prolonged stays in hospital and intensive care units (ICUs), imposing substantial financial burden on healthcare systems and families [ 28 – 31 ]. Recent studies conducted in the US reported that hospitalizations for COVID-19 amounted to more than US$1 billion; individuals with immunocompromising conditions accounted for $310 million of these costs [ 8 , 32 ].

The implementation of preventive measures, including social distancing, quarantining, and school and business closures, was intended to protect clinically vulnerable individuals such as those with immunocompromising conditions [ 29 – 31 , 33 ]. To protect these high-risk individuals from potential exposure, numerous facilities pivoted to telemedicine or virtual consultations in lieu of in-person appointments. Nonetheless, these measures inadvertently resulted in setbacks to receiving timely medical care and caused disruption in healthcare access for this vulnerable group [ 34 – 36 ]. For example, a reduction in onsite clinic visits and phlebotomy services led to individuals with critical conditions [such as advanced chronic kidney disease (CKD)] missing regular review appointments, thereby preventing timely preparation for dialysis, with the postponement of vascular access creation meaning dialysis was commenced via a central venous catheter, which poses heightened risk of infection. Additionally, lengthy delays while on a transplant waiting list could extend the dialysis period and lead to unfavorable medical outcomes [ 37 ].

Apart from the delays caused by preventive measures, prolonged SARS-CoV-2 replication in this susceptible population may further contribute to treatment modifications/delays, ultimately worsening individuals’ prognoses [ 38 , 39 ]. In one study, individuals with malignant brain tumor and SARS-CoV-2 infection were found to have 2.2 times greater odds of mortality than those without COVID-19, presenting a unique clinical dilemma where withholding chemotherapy and steroid treatment may be considered to avoid exacerbating the SARS-CoV-2 infection and immunosuppression [ 40 ].

Given the diverse symptoms and indirect effects of COVID-19, the economic and humanistic burden of the disease in this high-risk group warrants a thorough assessment, to understand the value of treatments, vaccination, and preventive measures. This expert review aims to evaluate the recent evidence on healthcare resource utilization (HCRU), including hospitalization, ICU admission, and mechanical ventilation (MV) use and costs associated with COVID-19, along with the ongoing impact of the disease on mental health and HRQoL in this immunocompromised population. By doing so, this expert opinion review aims to illuminate the ongoing burden of COVID-19 in individuals with immunocompromising conditions as well as during any potential future infectious disease outbreaks.

Methods

We conducted a combination of systematic literature and scoping reviews using the MEDLINE, Embase, PsycInfo, and EconLit databases. The search was limited to human studies published between January 2020 and November 2023. To capture relevant studies, a combination of free-text search terms and controlled vocabulary terms for the diseases was utilized (Supplemental Tables 1–4). All records in English, including original articles and abstracts, were retrieved and evaluated for eligibility; all duplicates were eliminated. In total, three literature searches were performed to maintain currency, and 8529 peer-reviewed publications were screened. Of these, 848 were considered via full-text evaluation, resulting in 283 publications prioritized for this review (Supplemental Fig. 1). Selected articles herein were mutually agreed by authors. In addition, this expert opinion review has been informed by the insights of experts in a variety of medical fields (nephrology, transplantation, oncology, genomics, virology, infectiology, immunology, and epidemiology) who also serve as authors of this manuscript. This article is based on previously conducted studies and does not contain any new studies with human participants or animals performed by any of the authors.

Overview

The impact of the COVID-19 pandemic on individuals varies widely, with greater consequences reported for individuals with immunocompromising conditions (Table 1 ) [ 28 ]. This expert opinion review highlights the current findings of studies assessing the economic and humanistic burden of COVID-19 in individuals with immunocompromising conditions. Most studies identified were carried out in the pre-Omicron era, with only a few conducted since Omicron dominated. The variant type was assumed, where necessary, based on the study enrollment date (Tables 2 , 3 , 4 , 5 ).

Individuals with immunocompromising conditions have a compromised immune system because of underlying diseases and treatments, which makes them more susceptible to prolonged SARS-CoV-2 infection and COVID-19-related mortality than the general population [ 9 , 28 , 41 , 42 ].

Impact on Healthcare Resources

Healthcare Resource Utilization (HCRU)

Based on the medical literature evidence reviewed herein, COVID-19-related HCRU was higher in individuals with immunocompromising conditions compared with the general population or those with immunocompromising conditions without COVID-19, with most requiring hospitalization, ICU, and ventilatory support (Table 2 ). Among these individuals, HCRU typically was highest for individuals with cancers and solid organ transplants [ 6 , 43 – 57 ]. Individuals with cancer generally experienced higher HCRU compared to respective control populations [ 47 , 58 ]. HCRU was the highest for individuals with hematologic cancer compared with those with other cancer types [ 6 , 43 – 50 ].

For individuals receiving solid organ transplantation, COVID-19-related HCRU was high compared with non-transplant recipients and transplant recipients without COVID-19 [ 59 , 60 ]. The highest HCRU was reported among kidney transplant recipients [ 51 , 53 , 54 , 56 , 61 – 68 ]. Based on several comparative studies, HCRU in individuals with CKD was also higher compared with the general population in both the pre-Omicron and Omicron eras [ 6 , 69 – 72 ].

Individuals living with human immunodeficiency virus (HIV) and COVID-19 also required higher HCRU compared with immunocompetent populations [ 73 , 74 ]. HCRU in individuals receiving active immunosuppressive treatments (high-dose corticosteroids, alkylating agents, antimetabolites, transplant-related immunosuppressive drugs, cancer chemotherapeutic agents classified as severely immunosuppressive, or tumor necrosis factor inhibitors) was lower compared with other populations with immunocompromising conditions described here; however, this varied across studies [ 28 , 73 , 75 ]. Additionally, studies conducted in the Omicron era showed that populations with immunocompromising conditions were also particularly vulnerable to higher HCRU compared with those without, despite vaccination status [ 9 , 69 , 76 – 78 ].

Hospitalization Risk and Rates

In the pre-Omicron era, COVID-19-related hospitalization rates were generally higher in individuals with hematologic cancers than solid tumors (18–84% vs. < 1–65%; Table 2 ) [ 6 , 43 , 44 , 46 – 50 ]. In a Brazilian study, the mean length of stay (LOS) was significantly greater in individuals with cancer and COVID-19 than among the general population with COVID-19 (13.1 days vs. 11.5 days, respectively; p < 0.001) [ 58 ]. Median LOS for individuals with cancer and COVID-19 in the UK was ~ 6 days [ 79 ]. In addition, solid organ transplant recipients with COVID-19 tend to require more hospital-related resource use compared with non-transplant recipients and transplant recipients without COVID-19 [ 44 , 59 , 60 ]. Hospitalization rates ranged from < 1 to 87% (Table 2 ) [ 44 , 51 – 57 , 59 – 61 ]; median LOS in the hospital ranged from 5 to 33 days [ 17 , 57 , 59 , 80 ].

The overall COVID-19-related hospitalization rate was also high in individuals with primary immunodeficiency disorder infected with SARS-COV-2, ranging from 6% in children with inborn errors of immunity and SARS-CoV-2 infection, to 66% in those with Good’s syndrome and SARS-CoV-2 infection [ 81 ]. In SARS-COV-2 infected individuals with HIV, the frequency of hospitalization varied, with rates ranging from 16 to 42% [ 82 , 83 ].

Rates of COVID-19-related hospitalizations were slightly lower than the pre-Omicron era, but continued to remain high in individuals with cancer as the Omicron variant began to emerge (Table 2 ) [ 84 – 86 ]. Hospital-related resource use was lower in patients with COVID-19 on receipt of chimeric antigen receptor T-cell therapy or hematopoietic stem cell transplant (HSCT) (4.3%) during this period compared with those in the pre-Omicron era (40.4%) [ 87 ]. A study was conducted in Italy to examine the impact of COVID-19 vaccination (≥ 1 dose) on hospitalization in individuals with cancer. While COVID-19 vaccination led to a reduction in hospitalization frequency in most patients with cancer (3–26% vs. 8–47%) compared with their non-vaccinated counterparts, it was less efficient in mitigating hospitalization risk among patients with hematologic cancer, such as leukemia [ 88 ].

In another study, individuals with peritoneal dialysis who were diagnosed with COVID-19 between August 2021 and July 2022 had a hospitalization rate of 62%; almost two thirds of those hospitalized required oxygen or other invasive respiratory support [ 89 ]. In an Italian study, COVID-19 hospitalization among patients with kidney transplant was 27% higher prior to vaccination, but lower among individuals with three doses of a COVID-19 vaccine (8%) [ 67 ]. In separate studies conducted in Scotland, COVID-19 hospitalization rates among patients receiving dialysis or with kidney transplant who received two doses of a COVID-19 vaccine were 31%, and 22% among those who received three doses [ 90 , 91 ]. In general, individuals with immunocompromising conditions and COVID-19 continued to face a greater likelihood of hospitalization than those without such conditions (Table 2 ) [ 28 , 64 ]. This trend persisted in the context of Omicron variants, as indicated by several studies [ 9 , 75 , 76 ], one of which found that clinically extremely vulnerable (CEV) individuals had a much higher incidence of cumulative breakthrough hospitalization, indicating a risk ratio of 14.2 (95% confidence interval [CI]: 10.2–19.7) and 15.8 (95% CI: 13.2–19.0) compared with matched non-CEV individuals for two- and three-dose recipients, respectively [ 76 ].

In the Omicron era, rates of COVID-19-related hospitalization remained high in individuals with immunocompromising conditions, despite vaccination (Table 2 ) [ 9 , 68 , 75 – 78 , 92 – 96 ]. In individuals with hematologic cancers, rates of COVID-19-related hospitalizations ranged from 10 to 30% (Table 2 ) [ 78 , 92 ]. One study reported a 74% hospitalization rate among HSCT recipients [ 69 ]. COVID-19-related hospitalization rates among patients with solid organ transplant varied across studies, but were marginally lower during the Omicron era than those observed in the pre-Omicron era (Table 2 ); this has been attributed to increased vaccination coverage [ 65 , 67 , 68 , 93 , 94 , 97 – 99 ]. A study in Thailand demonstrated that patients with kidney transplant with COVID-19 who had received a vaccine booster dose (third dose) had lower hospitalization rates (12%) compared with those receiving one (81%) or two (48%) doses [ 68 ]. Additionally, a Chinese study conducted during the Omicron era reported that the COVID-19-related hospitalization rate for patients with liver transplant who received two vaccine doses was 11% [ 94 ]. Nevertheless, rates have been found to vary regionally, as, in a single center retrospective US study of patients with solid organ transplant, a hospitalization rate of 32% was observed during the Omicron era [ 93 ]. Finally, another study conducted in Chile reported a 14% rate of hospitalization for COVID-19 in patients with end-stage renal disease (ESRD) [ 100 ]. Although the HCRU in individuals receiving active immunosuppressive treatments was lower than that in those with other immunocompromising conditions described here, several comparative studies found that, overall, the risk of COVID-19-related hospitalization was higher in those receiving immunosuppressive treatment compared to those who were not [ 28 , 73 , 75 ].

Very limited data exist on the burden of COVID-19 in individuals with other immunocompromising conditions including primary immunodeficiency disorder, HIV, and ESRD during this time. One study found that those with primary immunodeficiency disorder were at a high risk for COVID-19-related hospitalization [adjusted incidence rate ratio (aiRR): 9.7; 95% CI: 6.3–14.9] and hospitalization risk was low in individuals with ESRD (aiRR: 3.7; 95% CI: 3.39–4.13) and HIV (aiRR: 2.6; 95% CI: 1.20–5.43) [ 9 ]. A study conducted in Canada, comparing risk of hospitalization for COVID-19 in individuals with/without HIV during the pre-Omicron and Omicron era, showed that those with HIV had approximately twice the risk than HIV-negative individuals during both the pre-Omicron and Omicron periods, with relative risk more pronounced in unvaccinated individuals [ 95 ].

ICU Admissions

Among individuals with COVID-19, those who had cancer and recent treatment had a higher risk of ICU admission [odds ratio (OR): 1.7 vs. 1.0] than those without cancer (reference group) [ 101 ]. ICU admissions were higher among individuals with hematologic cancers versus the general population (Table 2 ) [ 6 , 47 ]. Two studies reported ICU admissions, which ranged from 10% in children and young adults with COVID-19 to 23% in a cohort of individuals with COVID-19 who had undergone allogeneic or autologous hematopoietic cell transplantation [ 102 , 103 ]. Another study reported that a higher percentage of patients with cancer and COVID-19 were admitted to the ICU than those with cancer and no COVID-19; here, ICU LOS was noted to be similar among patients with cancer and COVID-19 (10.9 days) and those patients with cancer without COVID-19 (11.1 days) [ 58 ].

ICU admission rates due to COVID-19 in solid organ transplant recipients also varied between studies (Table 2 ) [ 51 – 53 , 55 , 56 , 59 – 61 ]. Overall, these rates were higher in transplant recipients than in the general population and significantly higher in transplant recipients hospitalized for COVID-19 than those without COVID-19 [ 6 , 59 , 60 ]. ICU admissions were also higher in vaccinated versus unvaccinated individuals with solid organ transplant (23% vs. 14%) [ 55 ].

One retrospective study reported an ICU admission rate of 19% for individuals with inborn errors of immunity and SARS-CoV-2 infection [ 104 ]; ICU admission rates were high in those with CKD (13–48%) and HIV (5–81%) [ 56 , 70 , 83 , 105 ]. Another study assessed the rate of ICU admission in individuals with COVID-19 who tested HIV positive and negative, and found that there was no significant difference ( p = 0.273) in duration between the two groups (11.1 vs 9.7, respectively) [ 106 ].

Overall, ICU admission rates remained consistently high in individuals with cancer (4–45%) and solid organ transplant (1–74%) during the pre-Omicron era and the emergence of Omicron (Table 2 ) [ 28 , 45 , 63 , 64 , 66 , 85 , 86 , 98 , 107 – 110 ]. Despite the Omicron variant being less virulent, solid organ transplant recipients continued to experience elevated ICU admissions [ 93 , 96 ]. One study found that the rate of ICU admission in individuals who were HIV positive in Brazil in 2021 (39%) was comparable to that in 2020 (44%), with no significant difference. This could be because of low immunization rates in Brazil due to the unavailability of vaccines in the first half of 2021 [ 111 ]. A study conducted in South Korea focusing on individuals with ESRD indicated that ~ 6% of these patients required ICU admission, even after vaccination [ 112 ]. In the Omicron era, there were minimal reported cases of ICU utilization among individuals with immunocompromising conditions.

MV Use

MV rates were higher in individuals with hematologic cancer (11–22%) compared to those with solid cancer (5–7%) in the pre-Omicron era (Table 2 ) [ 43 , 46 , 50 , 101 ]. Solid organ transplant recipients with COVID-19 had higher rates of MV versus those without transplant and versus transplant recipients without COVID-19 [ 59 , 60 ]. In two studies of individuals with primary immunodeficiency disorder and COVID-19, rates of MV ranged from 13 to 21% [ 81 , 104 ]. Incidence of MV use was ~ 7% in individuals receiving active immunosuppressive treatments [ 113 ].

MV use decreased substantially in patients with cancer (3–4%) during the emergence of the Omicron era compared to the pre-Omicron period (5–22%), likely attributable to vaccination (Table 2 ) [ 28 , 43 , 45 , 46 , 50 , 87 , 101 , 108 ]. According to a study conducted in South Korea, only 2% of individuals with ESRD who received the third vaccine dose required MV [ 112 ]. Conversely, MV use was high (4–48%) in solid organ transplant recipients during this period [ 63 , 64 , 107 , 114 ]. One study noted a similar usage of MV among Brazilian HIV-positive individuals in 2021 (34%) compared with those in 2020 (36%), attributed to low immunization rates in the country given the unavailability of vaccines in early 2021 [ 111 ]. Limited data are available on MV use in patients with immunocompromising conditions during the Omicron-dominant phase. A US retrospective study reported that 5% of solid organ transplant recipients who were hospitalized for COVID-19 required MV [ 93 ]. Two studies indicated that solid organ transplant recipients who had received two or three doses of the COVID-19 vaccine had a lower MV requirement compared with those who were unvaccinated or received one dose of COVID-19 vaccine [ 68 , 96 ]. A retrospective study conducted in Israel found that a fourth COVID-19 vaccine dose significantly protected immunocompromised elderly individuals from MV or death (OR: 0.51; 95% CI: 0.3–0.87) compared with those receiving three doses [ 77 ].

Overall Considerations on Healthcare Resource Impact

The data presented above underscore that through the evolution of COVID-19, immunocompromised individuals have remained at high risk compared with non-immunocompromised individuals and the overall general population. Prior to the availability of vaccines, as well as pre-Omicron, outcomes from a hospitalization, ICU admission, and MV perspective were heightened in those who were immunocompromised.

In the pre-Omicron era, a US retrospective cohort study of over 220,000 patients with confirmed or suspected COVID-19 found that immunosuppressed patients had a 36% greater risk of invasive MV compared with those who were not immunosuppressed (9% vs. 6%, unadjusted HR: 1.3) [ 113 ]. This was further substantiated by another large US cohort study of over 500,000 patients diagnosed with COVID-19, where individuals with cancer and recent (≤ 3 months) treatment (e.g., chemotherapy ± immunotherapy) had a 19% and 69% higher overall risk of hospitalization and ICU stay, respectively, compared with those without cancer—interestingly, those with cancer but no recent treatment had similar outcomes to those without cancer [ 101 ].

As immunization efforts began to reshape the pandemic, the burden remained among high-risk and immunocompromised individuals, even those who were vaccinated. A large UK cohort study, covering 15.5 million fully vaccinated individuals, found that despite vaccination, high-risk populations had substantially higher incidence rates of COVID-19-related hospitalization and ICU admissions compared with the general population (4.77 and 0.33 per 1000 person-years, respectively) [ 5 ]. Comparator populations of note included immunocompromised individuals (16.45 and 1.88, respectively) and those with hematological malignancies (24.35 and 2.79, respectively). Another prospective cohort study found that adults with COVID-19 (> 80% of whom were vaccinated) were 19% more likely to be admitted to the ICU and 21% more likely to receive MV than those considered immunocompetent [ 27 ].

As the COVID-19 pandemic progressed and opportunity for additional vaccination was available, outcomes continued to remain high risk among the immunocompromised. A Canadian population-based study of over 300,000 individuals noted hospitalization risk ratios ranging from 2.8 to 15.8 among individuals with varying levels of immune dysfunction (72% of whom were vaccinated with three doses) compared with those not immunocompromised (56% vaccinated with three doses) [ 18 ]. In a UK prospective cohort study of 13.8 million individuals who completed a primary vaccine schedule and a booster dose, those receiving immunosuppressants remained at risk of severe COVID-19 outcomes despite the booster dose (adjusted relative risk: 5.8) compared with no immunosuppressants, emphasizing the importance of prioritizing specific populations for additional means to prevent COVID-19 [ 75 ].

Economic Impact

Limited data exist on the economic impact of COVID-19 in immunocompromised individuals (Table 3 ). One study compared hospitalization costs in COVID-19-affected individuals with and without autoimmune disease in the US. Costs were significantly higher in those with versus those without autoimmune disease {$2635/day vs. $2607/day [2020 United States dollars (USD)]; p < 0.038}. Mean ICU admission costs for individuals with autoimmune disease were US$3940/day [ 115 ]. Another study in England evaluated HCRU cost in immunocompromised and immunocompetent patients with COVID-19. The median healthcare cost per hospitalization was £8727 [2020/2021 British pound sterling (GBP)] in both immunocompromised and immunocompetent patients; median critical care costs were higher among immunocompetent (£17,439) than immunocompromised patients (£14,551). Mean critical care costs requiring MV use were also similar (immunocompromised: £39,029; immunocompetent: £40,148) [ 116 ]. In a separate US study, hospitalizations ( n = 14,516) for COVID-19 among patients with immunocompromising conditions amounted to nearly US$1 billion, with overall hospitalization costs ranging from $30,671 (2021 USD) for patients with hematologic malignancies and solid tumors to $102,224 (2021 USD) for those with ESRD [ 8 ]. An updated analysis of this study revealed that between January and December 2022, hospitalizations associated with first COVID-19 diagnosis exceeded US$1 billion, with individuals with immunocompromising conditions contributing to US$310 million of these costs [ 32 ].

The societal impact of COVID-19 in individuals with immunocompromising conditions has also been evaluated, although the data are very limited. One study reported indirect costs for individuals with HIV in Vietnam during the pandemic. Of the 1243 individuals with HIV or on antiretroviral therapy, 14% lost their jobs and 20% reported a reduction in household income due to the pandemic [ 117 ].

Impact on Mental Health

Several studies have examined the impact of COVID-19 on mental health in individuals with solid tumors and hematologic malignancies during the pre-Omicron period (Table 4 ) [ 118 – 127 ]. In these studies, the impact of COVID-19 on mental health was assessed using a variety of patient-reported outcome (PRO) instruments.

Elevated levels of anxiety, depression, and distress were seen in individuals with cancer during the pre-Omicron period [ 118 , 119 , 127 ]. A cross-sectional study, investigating the mental health of individuals with advanced solid tumors during and after lockdown using the Brief Symptom Inventory instrument, observed that over one-third presented with clinically significant anxiety (36%) and depression (35%) [ 119 ]. However, another similar study, using the Hospital Anxiety and Depression Scale (HADS), found that depression, but not anxiety, was significantly reduced after lockdown [ 120 ]. A cross-sectional survey reported significantly worsened mental health in adolescents and young adults with cancer during the pandemic versus pre-pandemic times [ 122 ]. According to another study, the primary factor contributing to insomnia in these patients with cancer was found to be distress during the pandemic [ 126 ]. Additionally, a separate study revealed that approximately half of young adults with cancer experienced loneliness during this time [ 121 ]. Low to moderate levels of post-traumatic stress disorder (PTSD) were also experienced by most individuals with cancer during the pandemic [ 123 , 125 ]. Another cross-sectional survey evaluating mental health in individuals with cancer (95.5% vaccinated) revealed a mean score of 13.5 using the Fear of COVID-19 scale, suggesting relatively low concern about COVID-19, which was attributed to a positive attitude toward vaccination [ 124 ].

Several studies have reported mental health outcomes in solid organ transplant recipients receiving immunosuppressive therapy (Table 4 ). One study found that action competence (ability to plan and execute) was significantly worse in those with organ transplantation during the pandemic versus pre-pandemic, and versus the general population [ 128 ]. One study reported more pronounced risk-avoidance behavior and a higher perception of loneliness in solid organ transplant recipients compared with non-transplant individuals [ 129 ]. In general, most showed a good level of resilience [ 130 ].

Depression and anxiety scores in HSCT recipients, measured using HADS during the pandemic, were below the cut-offs for clinical symptoms, and were comparable to pre-pandemic levels [ 131 ]; additionally, PTSD, measured during the pandemic using the PTSD Checklist-Civilian Version, was similar to pre-pandemic levels. However, another study did report moderate depression and anxiety or stress in those with HSCT during the pandemic [ 132 ].

In individuals with HIV, studies reported a negative impact of COVID-19 on mental health, including distress, anxiety, and depression during the pandemic [ 117 , 133 ]. The mental health of individuals with CKD and those receiving dialysis worsened during the pandemic compared to pre-pandemic. These individuals with CKD experienced moderate to severe anxiety, mild insomnia/poor sleep, and abnormal depression [ 134 – 136 ]. Additional studies found that individuals using corticosteroids or immunosuppressive medications had moderate levels of stress, anxiety, and depression [ 137 – 139 ].

Research on the mental health status in individuals with immunocompromising conditions from the late pre-Omicron era to the present period has been very limited (Table 4 ). Amidst the emergence of the Omicron variant, as many as 40% of individuals with cancer reported heightened distress, even though most were fully vaccinated; younger age, feeling isolated, and more negative attitude toward staying at home were linked with COVID-19-related distress [ 140 ]. A study conducted among a German rehabilitation-stay population that received high-dose chemotherapy with HSCT reported lower anxiety symptoms during the pandemic versus pre-pandemic [ 141 ]. Additionally, it was found that resilience, measured using the Brief Resilient Coping Scale questionnaire, was enhanced by spirituality in Spanish patients with cancer during the pandemic [ 142 ]. Similarly, a separate study in Iran involving individuals with cancer undergoing chemotherapy revealed a positive association between spiritual well-being and resilience, as well as a negative correlation between spiritual well-being and anxiety related to COVID-19, indicating that spiritual well-being might have boosted individuals’ resilience against illness in the pandemic, while alleviating COVID-19-related anxiety [ 143 ].

Impact on HRQoL

HRQoL of individuals with hematologic malignancies and solid tumors has been assessed in multiple studies that used a range of PRO measures pre-Omicron (Table 5 ) [ 120 , 144 – 148 ].

Individuals with pancreatic cancer who contracted COVID-19 had a lower HRQoL [measured using the European Organisation for Research and Treatment of Cancer-Quality of Life Questionnaire-C30 (EORTC-QLQ-C30)] during versus pre-pandemic [ 145 ]. While in lockdown, individuals with gynecologic cancer exhibited lower HRQoL [12-item Short-Form Survey (SF-12) mental health scores] compared with after lockdown [ 120 ]; those with solid tumors and/or hematologic cancer had significantly higher scores on the mental component of the SF-12 HRQoL questionnaire, but significantly reduced scores on the physical component of SF-12 than the general population [ 149 ]. Another study, conducted in Denmark, found no significant difference in the EORTC-QLQ-C30 HRQoL scores between the pandemic and pre-pandemic periods among individuals with solid tumors ( N = 4571) [ 147 ]. This could be attributed to patients feeling secure as the entire Danish population was adhering to social-distancing measures and precautions were being implemented to reduce in-person hospital attendance.

In solid organ transplant recipients receiving immunotherapy, HRQoL worsened during the COVID-19 pandemic, or was lower compared to general control populations; physical and/or mental health were also worse in these individuals compared with pre-pandemic levels (Table 5 ) [ 130 , 150 – 152 ]. A prospective cohort study involving kidney transplant recipients showed a significant difference ( p = 0.04) in HRQoL before (EuroQol 5-dimensions score: 99.5 ± 0.75) versus after COVID-19 (95.6 ± 3.25); pain and anxiety/depression were the components that contributed most significantly to the total score differences regardless of COVID-19 severity [ 153 ]. A cross-sectional survey comparing HRQoL in patients with transplants with an age-matched UK population revealed that the health status of transplant recipients [health status index score: 0.75 (0.73–0.77)] was significantly poorer than the general population [Health Survey England score: 0.82 (0.81–0.83)] [ 130 ]. HRQoL and fatigue scores in those with HSCT during the pandemic were similar to pre-pandemic levels [ 131 ]. However, another study reported a general health score of 59.64 ± 20.04 in these individuals during the pandemic [ 132 ].

In individuals with HIV, HRQoL during the pandemic was worse compared with the pre-pandemic levels [ 154 ]. A cross-sectional study assessing sleep patterns in immunocompromised individuals (due to rheumatic disease, liver, kidney, and gastrointestinal conditions) during lockdown in Brazil found that they had poorer sleep quality, which was associated with increased screen time and intrafamilial violence compared to a control population [ 155 ].

Very few studies have explored the impact of COVID-19 on HRQoL in individuals with CKD (Table 5 ). HRQoL worsened during the pandemic in these individuals and in those receiving dialysis [ 135 ]. In a study conducted in the Netherlands, HRQoL measured using SF-12 in individuals undergoing dialysis showed that the physical component score significantly improved during the pandemic compared to pre-pandemic ( p = 0.02), while the mental component score remained unchanged [ 156 ].

Avoidance and Preventive Behavior

At the start of the pandemic, unprecedented interventions, “preventive behaviors,” and “isolation” were designed to protect individuals with immunocompromising conditions from COVID-19 [ 29 – 31 , 33 ]. Following these recommended behaviors led to poorer physical and mental health in the general population and in many high-risk individuals, because of limited access to healthcare or treatment delays (such as delays in surgery or radiotherapy, cancellation of doctor appointments or pharmacy visits) [ 34 , 157 , 158 ]. One study examined coping strategies used during preventive behaviors by lung, heart, liver, and kidney transplant recipients in the UK, and found that most showed good levels of resilience and acceptable HRQoL in general, although health status was lower than that in the pre-pandemic transplant cohort [ 130 ]. Compared to the general population, poorer self-perception of health status/utility was observed in these solid organ transplant recipients practicing avoidance and preventive behavior [ 130 ]. Moreover, a study conducted in Canada among people with HIV reported frequent adoption of preventive behaviors during the pandemic, while those with a prior history of COVID-19 before enrollment in the study were also more inclined to self-quarantine following potential exposure, even if asymptomatic (65% vs. 23%; p < 0.001; Chi-square test) [ 159 ]. Recent studies have shown detrimental effects of these practices on HRQoL, with increased feelings of isolation and feeling “left behind” as the general population returned to pre-pandemic living [ 160 , 161 ]. Even after the official declaration from WHO that COVID-19 is no longer classified a public health emergency, additional studies assessing HRQoL in this population remain important and will continue to emerge.

Conclusions

Studies showed that, overall, individuals with immunocompromising conditions had higher resource use compared to those without COVID-19 or the general population. Rates of hospitalization, ICU admission, and MV use were high in these individuals during the pre-Omicron era, and remained high during Omicron, despite vaccination. While HCRU decreased during Omicron compared to pre-Omicron, it remained elevated in this group compared to the general population, despite ongoing vaccination efforts. Based on the medical literature reviewed here, individuals with immunocompromising conditions, particularly those with cancers and solid organ transplants, exhibited the highest HCRU compared to other individuals with immunocompromising conditions described in this paper. Very few studies reported costs associated with COVID-19. Data on humanistic burden varied across studies and populations in the pre-Omicron era; only a limited number explored mental health status and HRQoL in the Omicron era. Overall, the mental health of individuals with different immunocompromising conditions worsened during the pandemic. Increased rates of depression, distress, or anxiety were seen in individuals with immunocompromising conditions during the pandemic versus pre-pandemic. HRQoL was also worse in individuals with different immunocompromising conditions who had COVID-19 compared to those without COVID-19 or the general population. Additionally, in studies comparing HRQoL during the pandemic versus pre-pandemic, HRQoL worsened in individuals with hematologic cancer, solid organ transplant, and those receiving active immunosuppressive treatments. Data on preventive behaviors, health state utilities (health status), and caregiver burden in this population were underreported in published literature. Although data on vaccination status were limited in the pre-Omicron period, it is well known that individuals with immunocompromising conditions have suboptimal responses to the COVID-19 vaccination, and thus are at increased risk of breakthrough infections and severe outcomes compared to the general population [ 162 ]. Overall, COVID-19 has, and likely continues to increase HCRU and costs, impairs mental health, and reduces HRQoL in individuals with different immunocompromising conditions compared to the general population. As such, the medical community continues to face challenges posed by COVID-19, especially in these individuals with immunocompromising conditions. Despite progress through vaccination, less potent variants, and ongoing adherence to preventive measures, mitigating the adverse effects of the SARS-CoV-2 virus remains a complex task. There remains a need to explore alternative strategies to prevent infection, limit its spread, and address the detrimental outcomes associated with this persistent health threat.

Suggestions for Future Research

Several studies have investigated HCRU in individuals with immunocompromising conditions over a longer term (follow-up of ≥ 4 weeks) but none aimed to identify the impact of long COVID-19 in this population [ 43 , 163 , 164 ]. Hence, robust studies are needed to evaluate its impact in different high-risk populations and settings. Most HCRU data reported here were ancillary endpoints within larger clinical studies, whereas hospitalizations, ICU admissions, and requirement for MV use were endpoints for clinical effectiveness. Numerous studies included in this review were conducted at single centers and had small sample sizes. Hence, real-world studies with large sample sizes that include a range of immunocompromising conditions and focus on HCRU and economic impact are needed. Overall, the quality of data varied, with studies differing in design and sample size, necessitating careful consideration of their relative impact. Considering the ongoing impact of COVID-19 on individuals with immunocompromising conditions, it is crucial to investigate the current mental health status and HRQoL in this patient population. Given that most of the studies described here are illustrative of the COVID-19 burden during the pre-Omicron era (Alpha and Delta variant period) and the start of the Omicron era, assessing the ongoing burden in vaccinated individuals with immunocompromising conditions who are still at risk is essential. Additionally, it is important to identify high-risk subgroups among immunocompromised individuals. Understanding the factors that make them more susceptible to severe infection will help implement targeted prevention and interventions. Novel strategies to optimize management and prevention of infection in these individuals should also be explored.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 394 KB)

Acknowledgments

Medical Writing, Editorial, and Other Assistance

This study was funded by AstraZeneca. Medical writing support, which was in accordance with Good Publication Practice (GPP3) guidelines, was provided by Noopur Mandrekar, PhD, of Parexel and was funded by AstraZeneca.

Authorship

All authors met the International Committee of Medical Journal Editors (ICMJE) criteria for authorship for this article, take responsibility for the integrity of the work as a whole, and have given their approval for this version to be published.

Author Contributions

Conceptualization: all authors; Data curation: Christoph D Spinner, Samira Bell, Hermann Einsele, Cécile Tremblay, Michel Goldman, Zain Chagla, Axel Finckh, Christopher J Edwards, Igor Aurer, Odile Launay, Carolina Casañas i Comabella, Samantha James, Sabada Dube, Katarzyna Borkowska, Fungwe Jah, Walid Kandeil, Cécile Artaud, Jacques-Eric Gottenberg, Loreto Gesualdo, Dominique Bertrand, Sofie Arnetorp, Gkikas Magiorkinis; Formal analysis: Carolina Casañas i Comabella, Samantha James, Katarzyna Borkowska, Sofie Arnetorp; Funding acquisition: none; Investigation: none; Methodology: Carolina Casañas i Comabella, Samantha James, Katarzyna Borkowska, Renata T C Yokota, Sofie Arnetorp; Project administration: Carolina Casañas i Comabella, Samantha James, Sabada Dube, Katarzyna Borkowska, Fungwe Jah, Renata T C Yokota, Sofie Arnetorp; Resources: Sofie Arnetorp; Software: none; Supervision: Sofie Arnetorp; Validation: Carolina Casañas i Comabella, Samantha James, Katarzyna Borkowska; Visualization: Christoph D Spinner, Michel Goldman, Zain Chagla, Axel Finckh, Igor Aurer, Dominique Bertrand, Gkikas Magiorkinis; Writing – review & editing: all authors.

Funding

Open Access funding enabled and organized by Projekt DEAL. This manuscript and the journal’s rapid service and open access fees were funded by AstraZeneca.

Data Availability

Data sharing is not applicable to this review as no datasets were generated or analyzed during the current study.

Declarations

Conflict of Interest

Axel Finckh received consulting fees from AbbVie, AstraZeneca, Bristol Myers Squibb, Eli Lilly, MSD and Pfizer, payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from AbbVie, Bristol Myers Squibb, Eli Lilly, MSD and Pfizer, and grants or contracts from Bristol Myers Squibb, Eli Lilly, Galapagos and Pfizer. Cécile Tremblay received consulting fees from AbbVie, AstraZeneca, Gilead, GlaxoSmithKline, Medicago, Merck, Moderna, Novovax, and VIIV, payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from AstraZeneca, Gilead, GlaxoSmithKline, Merck, Moderna, Pfizer, and Sanofi, participation on a data safety monitoring board or advisory board for DalCor Pharmaceuticals, hespiridin, and Takeda Pharmaceuticals, and received grants or contracts from CIHR, Réseau FRQS SIDAMI, Gilead, Merck, and National Institutes of Health. Christoph D Spinner received grants, personal fees from AbbVie, AstraZeneca, BioNtech, Eli Lilly, GlaxoSmithKline, Formycon, Molecular partners, MSD, Pfizer, Roche, Shionogi, SOBI (during the conduct of the study) and Synairgen, personal fees and non-financial support from B. Braun Melsungen, grants, personal fees and non-financial support from Gilead Sciences, grants and personal fees from Janssen-Cilag, MSD, and ViiV Healthcare, outside the submitted work, other from Apeiron and Eli Lilly, and grants from Cepheid. Hermann Einsele has nothing to disclose. Christopher J Edwards received consulting fees from AbbVie, AstraZeneca, Gilead, GlaxoSmithKline, Eli Lilly, and AbbVie, payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from AbbVie, Bristol Myers Squibb, Eli Lilly, Galapagos, Gilead, GlaxoSmithKline, Pfizer, Roche, and Sandoz, received support for attending meetings and/or travel from Eli Lilly and is a Chair of EULAR Education Committee. Dominique Bertrand has nothing to disclose. Gkikas Magiorkinis received payment or honoraria from Gilead Sciences and Roche; support for attending meetings and/or travel from AstraZeneca, and participation on a data safety monitoring board or advisory board from AstraZeneca and GlaxoSmithKline. Igor Aurer received consulting fees, payment or honoraria, support for attending meetings/travel fees and participation on a data safety monitoring board or advisory board for AstraZeneca and Roche, chairman of KroHem—Croatian Cooperative Group for Hematologic Diseases, and board member of Croatian Society for Hematology. Jacques-Eric Gottenberg received consulting fees from AbbVie and AstraZeneca, and received grants or contracts from AbbVie, Eli Lilly, and Pfizer. Loreto Gesualdo received consulting fees from AstraZeneca, Baxter, Chinook, Estor, GlaxoSmithKline, Medtronic, Mundipharma, Novartis, Pharmadoc, Roche, Sandoz, Sanofi, and Travere, payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from Astellas, AstraZeneca, Estor, Fresenius, Novartis, Travere, and Werfen, received support for attending meetings and/or travel from Takeda Pharmaceuticals, participation on a data safety monitoring board or advisory board for AstraZeneca, Baxter, Chinook, Estor, GlaxoSmithKline, Medtronic, Mundipharma, Novartis, Pharmadoc, Roche, Sandoz, Sanofi, and Travere, and grants or contracts from Abionyx and Sanofi. Michel Goldman received consulting fees from AstraZeneca for Revive Committee, and leadership or fiduciary role in other board, society, committee or advocacy group, paid or unpaid from ABOLERIS company, Davos Alzheimer Collaboration, SANTERO company and Tuberculosis Vaccine Initiative. Odile Launay received consulting fees from AstraZeneca, GlaxoSmithKline, Moderna, MSD, Sanofi, and Sequirus, payment or honoraria for educational events from AstraZeneca, GlaxoSmithKline, and Sanofi, participation on a data safety monitoring board or advisory board for Sanofi, and received contracts from AstraZeneca to perform clinical trials. Samira Bell received consulting fees from AstraZeneca and GlaxoSmithKline, participation on a data safety monitoring board or advisory board for AstraZeneca, and received all support for the present manuscript from AstraZeneca. Zain Chagla received payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from AstraZeneca, Gilead, GlaxoSmithKline, Merck, Moderna, Pfizer, and Roche, and grants or contracts from Gilead, Merck, Pfizer, and Roche for research support. Carolina Casañas i Comabella, Samantha James, and Katarzyna Borkowska are employees of Evidera. Evidera received funding from AstraZeneca to conduct literature review supporting the manuscript content. Cécile Artaud, Fungwe Jah, Sabada Dube, and Sofie Arnetorp are employees of AstraZeneca and hold or may hold stock. Renata T C Yokota received consulting fees from AstraZeneca. Walid Kandeil was an employee of AstraZeneca at time of study, and holds or may hold stock.

Ethical Approval

This article is based on previously conducted studies and does not contain any new studies with human participants or animals performed by any of the authors.

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Associated Data

Supplementary Materials

Supplementary file1 (PDF 394 KB)

Data Availability Statement

Data sharing is not applicable to this review as no datasets were generated or analyzed during the current study.