Arthritis Care & Research
Vol. 0, No. 0, Month 2023, pp 1–10
DOI 10.1002/acr.25169
© 2023 American College of Rheumatology.
R E V I EW A R T I C L E
Global Perspective on the Impact of the COVID-19 Pandemic
on Rheumatology and Health Equity
Evelyn Hsieh,1 Dzifa Dey,2 Rebecca Grainger,3 Mengtao Li,4 Pedro M. Machado,5
Manuel F. Ugarte-Gil,6 and Jinoos Yazdany7
Although the public health emergency associated with the COVID-19 pandemic has ended, challenges remain,
especially for individuals with rheumatic diseases. We aimed to assess the historical and ongoing effects of
COVID-19 on individuals with rheumatic diseases and rheumatology practices globally, with specific attention to
vulnerable communities and lessons learned. We reviewed literature from several countries and regions, including
Africa, Australia and New Zealand, China, Europe, Latin America, and the US. In this review, we summarize literature
that not only examines the impact of the pandemic on individuals with rheumatic diseases, but also research that
reports the lasting changes to rheumatology patient care and practice, and health service use. Across countries,
challenges faced by individuals with rheumatic diseases during the pandemic included disruptions in health care and
medication supply shortages. These challenges were associated with worse disease and mental health outcomes in
some studies, particularly among those who had social vulnerabilities defined by socioeconomic, race, or rurality.
Moreover, rheumatology practice was impacted in all regions, with the uptake of telemedicine and changes in health
care utilization. While many regions developed rapid guidelines to disseminate scientific information, misinformation
and disinformation remained widespread. Finally, vaccine uptake among individuals with rheumatic diseases has been
uneven across the world. As the acute phase of the pandemic wanes, ongoing efforts are needed to improve health
care access, stabilize rheumatology drug supplies, improve public health communication, and implement evidence-
based vaccination practices to reduce COVID-19 morbidity and mortality among individuals with rheumatic diseases.
INTRODUCTION Three years into the pandemic, it is important to reflect on the
impact of COVID-19 on both individuals with rheumatic disease
The COVID-19 pandemic created significant challenges for
and on rheumatology practice. In this review, a global team of
individuals with rheumatic diseases, particularly those who were
rheumatologists reviewed the literature on the impacts
members of vulnerable populations. Challenges included maldis-
of COVID-19 in rheumatology in several countries and regions,
tribution of testing and vaccines, unequal access to health care,
including Africa, Australia/New Zealand, China, Europe, Latin
and more severe outcomes of infection, all of which have dispro- America, and the US. Where possible, we focused our literature
portionately affected individuals with low socioeconomic status. review specifically on people from socioeconomic, racial, or ethnic
The pandemic has also exposed disparities in health and health groups with historically fewer resources and access to care,
care that already existed in many countries, highlighting the need indigenous populations, and rural populations. In this review, we
for both local and global responses to address differential summarize literature that not only examines the impact of the pan-
outcomes in populations at higher risk of severe COVID-19. demic on these populations, but also research that reports the
1Evelyn Hsieh, MD, PhD: Yale School of Medicine, New Haven, Connecti- Centre, University College London Hospitals NHS Foundation Trust, North-
cut, and VA Connecticut Healthcare System, West Haven, Connecticut; 2Dzifa wick Park Hospital, and London North West University Healthcare NHS Trust,
Dey, FRCP, FWACP, FGCP, MSc: Korle-bu Teaching Hospital and the University London, UK; 6Manuel F. Ugarte-Gil, MD, MSc: Universidad Científica del Sur
of Ghana Medical School, Accra, Ghana; 3Rebecca Grainger, MBChB (Dstn), and Hospital Nacional Guillermo Almenara Irigoyen - EsSalud, Lima, Perú;
BMedSci (Dstn), FRACP, PhD: University of Otago, Wellington, New Zealand; 7Jinoos Yazdany, MD, MPH: San Francisco General Hospital and University of
4Mengtao Li, MD: Peking Union Medical College Hospital, Chinese Academy California, San Francisco.
of Medical Sciences, Peking Union Medical College, National Clinical Research Author disclosures are available at https://onlinelibrary.wiley.com/doi/
Center for Dermatologic and Immunologic Diseases, Ministry of Science & 10.1002/acr.25169.
Technology, State Key Laboratory of Complex Severe and Rare Diseases, Address correspondence via email to Evelyn Hsieh, MD, PhD, at evelyn.
and Key Laboratory of Rheumatology and Clinical Immunology, Ministry of hsieh@yale.edu, and Jinoos Yazdany, MD, MPH, at jinoos.yazdany@ucsf.edu.
Education, Beijing, China; 5Pedro M. Machado, MD, PhD: University College Submitted for publication May 5, 2023; accepted in revised form May
London, NIHR University College London Hospitals Biomedical Research 30, 2023.
1
2 HSIEH ET AL
lasting changes to rheumatology patient care and practice, and reductions in daily hospital activities, such as infusions and other
on health service use. By providing this synthesis of the literature, outpatient activities; these changes have also corresponded to
we aim to identify lessons learned that the global rheumatology significant negative impacts on mental health being reported by
community can apply to improve care for individuals with rheu- rheumatologists (9,10).
matic diseases. One of the most remarkable efforts to respond to challenges
and uncertainties created by COVID-19 in rheumatology practice
in Africa was the formation of a special task force that aimed to
Africa
develop recommendations for the management of rheumatic dis-
The earlier forecasts of COVID-19 pandemic impact from ease during the pandemic (11). A pan-African survey on experi-
public health experts projected a bleak image for Africa (1). Health ences of rheumatologists provided comprehensive insight into
systems in the continent were described as having varied and less the rheumatology service organization and the extent of service
preparedness compared to other parts of the world, hence the disruption caused by the COVID-19 pandemic (5,12).
region was anticipated to suffer a disproportionate burden of dis- Vaccination has presented another major challenge in Africa.
ease and death. Fortunately, these predictions did not pan out, as There has been a high level of skepticism and hesitancy towards
fewer deaths than expected have been reported on the continent. vaccination (13). These data show a reluctance across the whole
The pandemic nevertheless had dire consequences on the socio- population toward receiving COVID-19 vaccines, though this
economic and political landscape and health systems of improved over time.
Africa (2,3). Some governments in Africa prioritized patients with rheu-
Impact on patients in Africa. The impact of the pandemic on matic diseases for COVID-19 vaccination. In South Africa,
individuals with rheumatic disease has been profound, including patients with comorbidities, including RA, were included in the
disruptions in access to care, shortages of drugs, and a rise in second phase of the national vaccination program (14). In
self-reported mental health issues. Several African studies have Nigeria, individuals with underlying medical conditions, including
sought to quantify some of the associated burden. In a regional rheumatic diseases, were in the priority group for vaccination
study to determine the impact of COVID-19 on individuals with (15). Unlike other parts of the world, not much has been done to
chronic rheumatic diseases, the pandemic negatively impacted look at antibody response in rheumatic patients. In Egypt and
rheumatology visits (82% of cases), availability of hydroxychloro- Morocco, it was found that there was lower antibody responses
quine (HCQ) (47%), and mental health (73%) (4). to the Sinopharm vaccine and Sinovac vaccines among the gen-
The African League of Associations for Rheumatology eral population and health workers (16,17).
reported an acute shortage of HCQ, noted by 7 of 10 rheumatolo- Lessons learned in Africa. In Africa, priorities include patient
gists, and 1 of 5 had to lower the amounts they prescribed to and population education regarding vaccination and mental
patients to make the supply last (5). A retrospective study of health support. The health system could benefit from ongoing
342 South Africans patients receiving care at an academic rheu- medical education for doctors, advocacy for rheumatology,
matology center reported that 80% of patients had interruptions access to drugs (biologic treatments and HCQ), an accessible
in chloroquine access and 69 patients experienced a physician- telemedicine platform, more organized rheumatology units, and
determined disease flare (6). adequate supplies of personal protective equipment (PPE); these
Other data suggest negative impacts on disease control and are among the top-cited unmet needs to deal with rheumatic dis-
quality of life in patients in Africa. A study of patients with rheuma- eases in Africa in the wake of the COVID-19 pandemic.
toid arthritis (RA) from a single center in Benin reported the mean
± SD Disease Activity Score in 28 joints scores increasing from
China
3.4 ± 1.5 pre-pandemic to 4.7 ± 2.04 in May 2020. Quality of life
also decreased, with the physical component summary score As the first country heavily struck by the COVID-19 outbreak,
and mental component summary scores of the Medical Outcome China adopted a series of policies to contain virus spread includ-
Study Short Form 36 measured as a mean ± SD 71.1 ± 20.3 and ing lockdown, a strict zero-COVID policy, mobilization of
67.1 ± 16.02 pre-pandemic compared to 38.1 ± 4.96 and resources, vaccination, and drug development. These policies,
36.8 ± 3.8, respectively (7). Among an Egyptian rheumatic disease which were in place through December 2022, were intended to
group, patients were found to be more vulnerable to mental health spare no efforts to reduce mortality rates and protect vulnerable
disorders and psychological distress, with 49%, 29%, and 1% of populations such as the elderly and patients with chronic dis-
patients having experienced moderate, severe, and extremely eases including rheumatic diseases and were largely successful
severe anxiety, respectively, as a result of COVID-19 (8). from the perspective of mitigating COVID-19–related outcomes.
Impact on health care providers and practice in Africa. The Impact on patients in China. In China, the impact of
pandemic has pushed many rheumatology clinics across Africa COVID-19 on individuals with rheumatic diseases has been
to adopt more virtual consultations (telemedicine), with significant multifaceted, including less access to routine health care,
 21514658, 0, Downloaded from https://acrjournals.onlinelibrary.wiley.com/doi/10.1002/acr.25169 by University of Ghana - Accra, Wiley Online Library on [08/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
GLOBAL IMPACT OF COVID-19 ON RHEUMATOLOGY AND HEALTH EQUITY 3
increased risk of infection and severe disease, and concerns about intensive methods against the spread of infection play an impor-
vaccination. Several studies have evaluated how COVID-19 has tant role in the protection of vulnerable populations who are at
influenced clinical outcomes (e.g., frequency of infections or flares), higher risk of infection and severe outcomes. Second, patients
health-related concerns and behaviors (e.g., vaccination-related with chronic disease may have less access to routine health care
concerns and uptake), and changes in access to care for patients due to restriction of traveling to avoid infection, which may further
with rheumatic diseases since the emergence of the pandemic. result in poor monitoring, delayed adjustment of treatment regi-
For example, a number of retrospective studies in Wuhan—the mens, and excessive risk of flare. Thus, the expansion of telemed-
capital of Hubei province, and the first city in China impacted by icine has been a welcome innovation. Third, better understanding
the COVID-19 pandemic in early 2020—reported outcomes in of the concerns of patients and more individualized education are
patients with rheumatic diseases (18–21). required to improve vaccination rates among these vulnerable
Similar to findings from other regions, patients with rheumatic populations. Proper guidance for patients (31) is not only the duty
diseases in China were found to be more susceptible to COVID- of rheumatologists, but also requires collaborative efforts from
19 infection compared to the general population (21). Rheumatic social media and the government.
diseases were also shown to aggravate the course of infection
(18) and increase the risk of respiratory failure (19). However,
Australia and New Zealand
additional data including data from studies outside of Wuhan
found that with adequate medical intervention in China, COVID- Both Australia and Aotearoa New Zealand adopted “zero-
19 was not necessarily associated with increased likelihood of COVID” suppression/elimination strategies. In March 2020 these
critical outcomes such as intensive care unit occupancy (22), island states, along with most in Oceania, established strict bor-
mechanical ventilation (21), and death (18). Based on these find- der control with quarantine after entry. Both countries had com-
ings, national rheumatology associations in China and Asia Pacific prehensive testing and case isolation systems and implemented
League of Associations for Rheumatology have published recom- social distancing measures with lockdowns when community
mendations to improve the outcomes of COVID-19 in patients transmission occurred. National COVID-19 vaccination programs
with rheumatic diseases (23). began in 2021, obtaining high levels of vaccination by late 2021.
Impact on health care providers and practice in China. The New Zealand avoided widespread community transmission of
COVID-19 pandemic had a substantial impact on the long-term COVID-19 until 2022 and can report the overall best mortality pro-
follow-up of patients with rheumatic disease in China. Early and tection outcomes among countries in the Organization for Eco-
intensive measures were adopted to contain COVID-19 with strict nomic Co-operation and Development (OECD), and performed
mask mandates, social distancing and routine testing require- better compared to the OECD average economically (32).
ments, and swift lockdowns coupled with contact tracing when Australia controlled a significant outbreak in Melbourne in late
cases were identified. While these measures disrupted in-person 2020 that particularly impacted older adults in aged residential
care for many patients with rheumatic disease, they were also care, then continued with a zero-COVID strategy until mid-2021
viewed as an effective means to protect vulnerable populations (33). These approaches have been successful but with some
from COVID-19 (24). In response, the use of telemedicine in rheu- areas for improvement (34).
matology care was rapidly and significantly expanded in Impact on patients in Australia and New Zealand. Given
China (25,26). largely successful early COVID-19 containment strategies, indi-
Despite the availability of vaccines, COVID-19 vaccination viduals with rheumatic disease were able to reduce risk of expo-
rates in Asian countries, including China, remain low (27). Other sure comparatively easily. There were also long periods in 2020
than the messenger RNA and adenovirus vector vaccines used and 2021 when there was no COVID-19 transmission, and in-
in western countries, inactivated COVID-19 vaccines were widely person health services were not disrupted. During periods of
used in China. The efficacy and safety of these vaccines have required physical distancing, most ambulatory rheumatology care
been confirmed (28). Although more research is needed, some was moved to virtual care, often via telephone (35). In Australia,
data suggest that patients may experience disease flare after vac- individuals with rheumatic disease reported high confidence in
cination (28). A nationwide, multicenter survey conducted to accessing health care, with high acceptability for telemedicine-
investigate vaccination-related concerns in Chinese patients with delivered care reported early in the pandemic (36,37). While there
rheumatic diseases found that concerns regarding adverse were short-lived restrictions on HCQ dispensing, supplies were
effects and disease flare were the main factors affecting vaccina- not interrupted. Tocilizumab became unavailable for rheumatic
tion willingness (29). Recommendations have been published in disease indications in both countries, forcing changes to treat-
China to address vaccine hesitancy (30). ment for those relying on this medication. In New Zealand this
Lessons learned in China. There are some key lessons resulted in the first government subsidization of JAK inhibitors in
learned from the management of patients with rheumatic dis- late 2021. Australia implemented rapid changes in funding autho-
eases during the COVID-19 pandemic. First, policies for early rization of advanced therapies to ensure continuity of care.
 21514658, 0, Downloaded from https://acrjournals.onlinelibrary.wiley.com/doi/10.1002/acr.25169 by University of Ghana - Accra, Wiley Online Library on [08/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
4 HSIEH ET AL
Overall, there were some changes and delays to patient care, but Impact on patients in Europe. An online survey of 1,800
most were managed proactively. patients conducted at the start of the pandemic revealed that
While there is not yet published data on COVID-19 outcomes 58% had their rheumatology appointments canceled, and 46%
in individuals with rheumatic disease in Australasia, it seems likely were not given any information about how SARS–CoV-2 infection
that patterns will follow those seen in other high-income countries might affect their rheumatic disease and treatment. In addition,
with high rates of vaccination. Population data shows older indi- 46% of patients were unable to continue exercising regularly,
viduals and some ethnic groups experienced high rates of poor 25% increased smoking, and 18% increased alcohol consump-
outcomes from COVID-19 (38) with Ma
ori and Pacific peoples tion. Based on scores on the Hospital Anxiety and Depression
experiencing higher rates of COVID-19 infections, in part due to Scale, 46% of patients had depression, and 58% were at risk for
inequitable delivery of public health measures, such as contact anxiety. Half of the patients reported poor well-being (45).
tracing (39). Inequalities in COVID-19 mortality rates still exist. The Health
Impact of health care providers and practice in Australia and Foundation, an independent charitable organization in the UK,
New Zealand. There were, however, negative impacts on patient reports mortality rates are 3–4 times higher in the poorest areas.
care delivery at times during the pandemic. Data from 2 retrospec- However, compared to the first year of the pandemic, the overall
tive studies involving medical record review in single centers with number of COVID-19 deaths is now significantly lower. Vaccina-
telephone-based care during the initial lockdowns of 2020 tion programs have played a key role in reducing COVID-19 mor-
reported no decrease in service volumes but lower frequency of tality rates, but for some populations, uptake is still low,
change in rheumatic disease medications (40,41). Diagnosis was particularly for individuals living in poorer areas and those from
more often deferred, and high rates of earlier than expected some minority ethnic groups (46).
follow-up appointments were also noted (10). Impact on health care providers and practice in Europe. A
In 2023, both countries are moving toward managing Europe-wide survey of 1,286 rheumatologists from 35 countries
COVID-19 as an endemic infection. Rheumatology care has revealed that >80% canceled or postponed face-to-face visits
largely returned to pre-pandemic patterns. Australian rheuma- with new patients, and 91% did the same for follow-up visits.
tology practices had been early adopters of telemedicine to Treatment choices were frequently delayed, and >70% of rheu-
meet needs of a geographically dispersed rural population matologists were hesitant to prescribe biological/targeted syn-
and to extend the reach of a limited rheumatology workforce thetic disease-modifying antirheumatic drugs (DMARDs) during
(42). In Queensland, a state 7 times the size of Great Britain, the early stages of the pandemic, primarily due to patient anxiety,
75% of rheumatologists had used telemedicine before the scarcity of screening tools, and decline in the availability of rheu-
pandemic, mostly with a hub model of a health care provider matologic services. This is a missed opportunity for the best
located with the patient (43). During the pandemic, rheumatol- patient care (47). Variations were observed among countries due
ogists had low confidence in telephone-based rheumatology to the impact of the pandemic, response strategies, and telemed-
care delivery and anticipated ongoing barriers to telemedicine icine regulations (48).
adoption including quality of care, efficiency, and reimburse- From the perspective of training, in a survey of 302 rheuma-
ment (43). Some practices have been more successful in tology trainees (30% from Europe, 38% from the US, and 32%
incorporating virtual care into ongoing rheumatology prac- from other countries), a negative impact of the pandemic on learn-
tice (44). ing opportunities during rheumatology training, including outpa-
Lessons learned in Australia and New Zealand. The bold tient clinics (79%), inpatient consultations (59%), didactic
public health approaches of the Australian and New Zealand gov- teaching (55%), procedures (53%), teaching opportunities
ernments have led to lower COVID-19 health burden and main- (52%), and ultrasonography (36%) was reported. Moreover,
tained economic activity. While data on health and other 39% of trainees reported that COVID-19 negatively affected their
outcomes for individuals with rheumatic disease are awaited, we ability to continue their pre-pandemic research (49).
anticipate these to also be favorable. Underpinnings that enabled Additional reports have suggested that COVID-19–related
these outcomes included universal health care access and strong issues, such as prioritization of COVID-19 research, redeploy-
public trust in government processes. ment of research staff, and the requirement for social distancing,
have had a negative impact on the recruitment of participants to
non–COVID-19–related research (50). According to a survey of
Europe
>1,000 individuals with rheumatic diseases, the willingness
The COVID-19 pandemic has transformed rheumatology of patients to participate in research during the pandemic also
health care delivery in Europe. The pandemic is likely to have decreased. Respondents were less likely to participate in obser-
had detrimental effects on patient management and quality of vational or interventional research studies during COVID-19 com-
care, despite the efforts and teamwork displayed by the rheuma- pared to before the pandemic (86% versus 64%, and 61% versus
tology community in its worldwide and integrated response. 44%, respectively) (51).
 21514658, 0, Downloaded from https://acrjournals.onlinelibrary.wiley.com/doi/10.1002/acr.25169 by University of Ghana - Accra, Wiley Online Library on [08/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
GLOBAL IMPACT OF COVID-19 ON RHEUMATOLOGY AND HEALTH EQUITY 5
The management of rheumatic diseases within the context of socioeconomic status, and social support for these groups was
COVID-19 has been addressed by overarching European institu- insufficient (60). Since this population had limited in-person and vir-
tions, such as EULAR. EULAR monitored the published literature tual health care access, their diagnosis was usually delayed, por-
and provided recommendations on the risk and prognosis of tending poorer outcomes (61). Moreover, social media networks
SARS–CoV-2 infection as well as the safety and efficacy of vacci- were not helpful vehicles for educational outreach in these popula-
nation against SARS–CoV-2 in patients with rheumatic dis- tions (62), creating barriers to disseminating COVID-19–related
eases (52–55). information and other information during the pandemic.
Lessons learned in Europe. Repercussions of COVID-19 Furthermore, in the Pan American League of Associations for
were vast and are far from over, and we will need to continue Rheumatology (PANLAR) patient survey study, 23.4% of partici-
addressing its long-term impacts. Omicron has become the most pants reported discontinuing at least 1 antirheumatic drug. The
prominent variant, leading to less severe infections, and resulting main reasons included fear that the medication would increase
in a decrease in COVID-19 public concern. However, the long- the risk of infection, and economic or administrative issues (63).
term sequelae of COVID-19, commonly referred to as Long However, actual adherence levels may have been even lower,
COVID, continue to affect millions of people in Europe and world- since those with less access to health care also had less access
wide (48). It remains unclear whether Long COVID is more fre- to the internet and were less likely to participate in the study. Like-
quent in individuals with rheumatic diseases, and further studies wise, another study of physicians reported a 50% reduction in
are warranted. New questions are now being raised since most patient adherence to medication (64).
individuals with rheumatic diseases have received at least 1 com- It is important to point out that historically in Latin America
plete vaccination cycle and a booster. There appears to be signif- there is a high rate of vaccination, particularly in children; this
icant individual variation in immunogenicity, and it is still unknown was not the case for COVID-19, where a large percentage of
how frequently the general population, let alone those with rheu- patients with autoimmune diseases said they would decline the
matic diseases and those receiving different immunosuppressive vaccine (65). This lack of confidence could be related to the nov-
treatments, will need to be revaccinated (53). Therefore, there is elty of the vaccine, or misinformation in the media and/or from
a need to conduct well-designed longitudinal studies to better political authorities. However, it is important to point out that
understand vaccine immunogenicity and to determine the best despite these misgivings, 70% of the Latin American population
timing and dosing of COVID-19 vaccines in patients with rheu- completed the initial COVID-19 vaccination protocol by May
matic diseases. 2022, compared to 58% worldwide (66). Furthermore, in Latin
America, individuals with autoimmune disease were prioritized,
so they were vaccinated even earlier.
Latin America
Impact on health care providers/practice in Latin America.
Latin America had some of the highest COVID-19 death One of the main changes during the pandemic was the increased
rates in the world, resulting from a combination of factors includ- use of telehealth, to which access was unequal. For example, in
ing political instability, corruption, social unrest, fragile health sys- the PANLAR patient survey, only 32.3% of respondents whose
tems, and inequality of income, health, and education. For medical appointments were canceled had a telehealth consulta-
example, 54% of all work carried out in Latin America is informal; tion. Among these, 49.9% were completed by telephone calls,
such workers have little-to-no access to health care and often and 36.4% by video calls (63). PANLAR physicians reported the
have to work when ill to earn a living. For these individuals, quar- time of face-to-face activity was limited. Telehealth was adopted
antine and social distancing measures were just not possible. by 80.0% of rheumatologists, of whom 50.6% used video calls
Additionally, as the large majority of Latin American countries are and 45.5% used phone calls (64). The scarcity of video
lower-middle income, they are often overlooked in global health calls impacted the ability of providers to make an accurate diag-
efforts targeting low-income countries (56). These disparities dis- nosis and treatment plan. Nevertheless, one study demonstrated
proportionately affect individuals with chronic diseases, including that in some Latin American settings, telehealth was useful for
those with autoimmune diseases who experience barriers within monitoring patients with stable RA (67). These findings suggested
and outside the health care system. a mixed model could be an option for certain patients, in particular
Impact on patients in Latin America. Low socioeconomic sta- those who live in rural areas.
tus (SES) has been associated with poorer outcomes, including Lesson learned in Latin America. Much work is needed to
higher risk of infection, less access to health care, and a higher reduce disparities in Latin America. Outcomes of autoimmune
number of comorbidities (57). In Argentina, Mestizo populations diseases during the pandemic were affected by poverty, health
and individuals cared for in the public health system were more care access, and health literacy; therefore, reducing morbidity
likely to require hospitalization (58). Additionally, small cities lacked from these factors should be the subject of advocacy efforts by
the necessary infrastructure for pandemic management (59). Infor- rheumatologists and other professionals. Collaborative work
mal work is much more common in populations with lower between health care professionals and patients within the region,
 21514658, 0, Downloaded from https://acrjournals.onlinelibrary.wiley.com/doi/10.1002/acr.25169 by University of Ghana - Accra, Wiley Online Library on [08/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
6 HSIEH ET AL
and with other regions, should be strongly encouraged to reduce identifying as Black, Latino, or Asian had more severe COVID-19
these disparities. outcomes than those who were White (75,76).
Impact on providers/practices in the US. Rheumatology care
delivery during the pandemic became significantly more complex
US
in the setting of competing demands (e.g., diversion of resources
Individuals with rheumatic diseases faced numerous chal- to COVID-19 care), social distancing, obstacles to effective risk
lenges during the COVID-19 pandemic in the US, ranging from communication, and challenges of transitioning rapidly and equi-
disruptions in health care and medication access, mental health tably to virtual care. The American College of Rheumatology
impacts, and in some cases, more severe outcomes from infec- (ACR) developed a series of guidance documents to assist rheu-
tion. Furthermore, many rheumatic diseases disproportionately matologists in navigating the pandemic (77). In addition, 3 large
affect individuals with lower SES (e.g., Black, Latino, and Native national studies examined changes in rheumatology practice pat-
American individuals), populations in which striking disparities in terns during the early months of the pandemic (through the Vet-
COVID-19 health outcomes were well documented. erans Administration [VA] [78], the ACR Rheumatology
Impact on patients in the US. Several studies focused on Informatics System for Effectiveness registry [79], and the Ameri-
the concerns of patients regarding COVID-19 itself or the rela- can Arthritis and Rheumatology Associates network [74]).
tionship between COVID-19 and their underlying rheumatic Rheumatologists in the VA reported comfort managing sta-
disease, changes in health-related behaviors during the pan- ble patients using telemedicine, but not new patients or estab-
demic, and access to medications and care, including adjust- lished patients requiring ongoing therapeutic changes. Providers
ment to telemedicine. COVID-19–related concerns tended to also perceived potential increases in health care disparities in Afri-
be higher among patients receiving biologic DMARDs (68) or can American patients, Latino patients, those in low SES groups,
JAK inhibitors (69), and were associated with increased social and those living in rural areas (78). Li et al compared visit counts
distancing behaviors (69). Disruptions in medication use and fromMarch to August 2020 to the same period in 2019 and found
health care visits stemmed from both changes in health-related an 11.5% decrease in visits in states with shelter-in-place orders
behaviors (e.g., taking medications as prescribed, going to compared to 5.3% in states without. The authors also noted a
appointments) and physical barriers to access (e.g., limited significant decrease in the proportion of RA patients with disease
supply of medications such as HCQ, shelter-in-place orders), activity measures documented, which not only impacts patient
and were associated with increased disease activity and care but also physician reimbursement (79). There is little data
flares (70,71). describing the longitudinal impact that this massive uptake in tele-
While discontinuation of medications was initially associated medicine has had on rheumatology practice, patient care-seeking
with concerns regarding vulnerability to COVID-19 or severe out- behaviors, and long-term health outcomes.
comes, these concerns improved over the course of 2020. How- Lessons learned in the US. The literature identified several
ever, a large nation-wide study showed that from December 2020 “lessons learned” for rheumatology patients and practice in the
to May 2021, interruptions in DMARD use increased by 80%, and US. First, early and sustained attention to equity is necessary to
a minority of discontinuations were physician guided (71). Con- protect vulnerable patients during a national health emergency.
currently, patients adapted to telemedicine, but generally pre- Rather than reactive policies around drug shortages or unfolding
ferred in-person initial evaluations (72), and older patients were health disparities, proactive measures to ensure access to health
less enthusiastic about virtual appointments. As vaccines became care, critical medications, and life-saving measures such as PPE
increasingly available in 2021, a desire to return to normal routines and vaccinations would improve outcomes. Misinformation and
promoted uptake; however, this was counterbalanced by fears disinformation presented challenges in the US and often spread
about side effects (including flare of underlying rheumatic disease) to other countries via social media and other online content. Nota-
or distrust of the vaccines (73). bly, misinformation disproportionately impacted vulnerable com-
As early as April 2020, disparities in access and outcomes munities. Efforts to improve health education and public health
between White individuals and patients from racial and ethnic communication are needed.
minority groups, those with lower SES, or those living in rural
areas were becoming alarmingly apparent. Among patients with
Conclusion
rheumatic diseases, these disparities were pervasive across
domains including clinical outcomes, access to care and tele- The COVID-19 pandemic has created significant challenges
medicine, vaccine uptake, and participation in research, in part for individuals with rheumatic diseases, particularly vulnerable
due to structural barriers but also in part fueled by mistrust populations with historically less access to health care resources.
(e.g., misinformation about minorities being targeted as “guinea Disparities in health and health care that already existed were
pigs”) (69,74). For example, 2 studies from the Global Rheumatol- augmented, highlighting the need for both local and global
ogy Alliance registry found that patients with rheumatic disease responses to address differential outcomes in populations at
 21514658, 0, Downloaded from https://acrjournals.onlinelibrary.wiley.com/doi/10.1002/acr.25169 by University of Ghana - Accra, Wiley Online Library on [08/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
GLOBAL IMPACT OF COVID-19 ON RHEUMATOLOGY AND HEALTH EQUITY 7
Table 1. Global lessons learned from the impact of COVID-19 on individuals with rheumatic disease and on rheumatology practices
Setting Major challenges Lessons learned
Individuals with Increased risk of Clear public health messaging about wearing masks, social distancing, maintaining or adjusting
rheumatic disease infection immunosuppressive medications, and vaccination can help protect vulnerable individuals
with rheumatic diseases
Mental health Resources to address social isolation, anxiety, and depression should be put into place as early
concerns as possible
Health equity Improve access to care and target outreach to patients with rheumatic disease from vulnerable
communities regarding vaccination and other preventive strategies
Rheumatology Disruptions in Telemedicine serves as a useful tool to improve access to care globally
practices access to care
Medication supply Collaborative efforts by rheumatologists, government agencies, pharmacies, and insurance
interruptions companies are needed to ensure a stable drug supply for patients with rheumatic diseases
Health Rheumatologists play a crucial role in providing clear and culturally sensitive communication to
communication ensure that patients know how to protect themselves
Rheumatology professional society guidelines can serve as one tool to combat misinformation
during public health emergencies
Coordination of public health messaging to the rheumatic disease community across
organizations is needed to increase the impact of public health messaging
higher risk of severe COVID-19. Patients across all regions faced Rheumatology, Peking Union Medical College Hospital, Beijing, China),
disruptions in rheumatology care, drug shortages, and struggles Alyssa Grimshaw (Cushing/Whitney Medical Library, Yale University,
New Haven, Connecticut), William Odell (Section of Rheumatology,
with social isolation and worsening mental health during peak Allergy and Immunology, Department of Medicine, Yale School of Medi-
pandemic periods. For providers and health systems, telemedi- cine, New Haven, Connecticut), Bright Katso (Rheumatology Unit,
cine capacity and uptake expanded rapidly, and professional Department of Medicine and Therapeutics, Korle-Bu Teaching Hospita,
Accra, Ghana), and Graciela S. Alarcon (Division of Clinical Immunology
societies came together proactively to create guidelines for the and Rheumatology, Department of Medicine, The University of Alabama
management of patients with rheumatic disease during the pan- at Birmingham Heersink School of Medicine, Birmingham, AL; Depart-
demic, and guidelines regarding the efficacy and safety of ment of Medicine, School of Medicine, Universidad Peruana Cayetano
SARS CoV-2 vaccination. Heredia, Lima, Perú). As part of the literature search process, different–
strategies were employed in initial scoping of the literature to identify
Key lessons learned are shown in Table 1, and include: 1) potentially suitable publications for different regions. These approaches
early and authentic attention to disparities in clinical outcomes, included using a large language model (i.e., ChatGPT), using a formal
health services, and research related to COVID-19 is paramount librarian-led search strategy, performing a review of the gray literature,
and citation chaining of relevant articles identified. Large language mod-
to ensure equity, even as the acute phase of the pandemic els were not used for any other activities related to the preparation
wanes; 2) effective health education and public health communi- and/or synthesis of information for this review.
cation play critical roles in promoting health-related behaviors
and are closely linked with public trust (in many settings, both mis-
information and disinformation presented tangible challenges to AUTHOR CONTRIBUTIONS
informed patient decision-making during the pandemic and All authors were involved in drafting the article or revising it critically
for important intellectual content, and all authors approved the final ver-
amplified public mistrust); 3) advocacy, in partnership with profes- sion to be submitted for publication. Drs. Hseih and Yazdany had full
sional societies and community-based organizations, can help access to all of the data in the study and takes responsibility for the integ-
bring about timely and effective policies or regulatory changes to rity of the data and the accuracy of the data analysis.
Study conception and design. Hsieh, Yazdany.
address gaps and inequities in resources (e.g., medication Acquisition of data. Hsieh, Dey, Grainger, Li, Machado, Ugarte-Gil,
access, PPE) and infrastructure (e.g., telemedicine capacity); 4) Yazdany.
well-designed prospective studies are needed to evaluate the Analysis and interpretation of data.Hsieh, Dey, Grainger, Li, Machado,
long-term impact of the pandemic on health outcomes and health Ugarte-Gil, Yazdany.
care delivery for patients with rheumatic diseases—particularly
those who are most vulnerable; and 5) studies are needed to fill REFERENCES
gaps in our understanding of SARS–CoV-2 vaccine immunoge-
1. Mutapi F. How has COVID-19 hit Africa? Here’s what the data
nicity (including ongoing vaccine booster doses) across different tells us. World Economic Forum. 2021. URL: https://www.weforum.
regions and vaccine types, and optimal timing and dosing of org/agenda/2021/10/why-africa-must-gather-its-own-data-to-tackle-
these COVID-19 vaccines in patients with rheumatic diseases. the-pandemic/.
2. Frimpong OB, Bihuzo RM, Commodore R. Wilson Center: Africa Pro-
gram occasional paper. The COVID-19 pandemic in Africa: impact,
ACKNOWLEDGMENTS responses, and lessons from Ghana, the Democratic Republic of the
Congo, and Rwanda. URL: https://www.wilsoncenter.org/publication/
We would like to thank the following individuals for their contribu- covid-19-pandemic-africa-impact-responses-and-lessons-ghana-
tions to the preparation of this manuscript: Shangyi Jin (Department of democratic-republic-congo.
 21514658, 0, Downloaded from https://acrjournals.onlinelibrary.wiley.com/doi/10.1002/acr.25169 by University of Ghana - Accra, Wiley Online Library on [08/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
8 HSIEH ET AL
3. OECD. COVID-19 and Africa: socio-economic implications and policy 22. Zhao Y, Du J, Li Z, et al. It is time to improve the acceptance of
responses. 2020. URL: https://www.oecd.org/coronavirus/policy- COVID-19 vaccines among individuals with chronic diseases: a sys-
responses/covid-19-and-africa-socio-economic-implications-and- tematic review and meta-analysis [review]. J Med Virol 2023;95:
policy-responses-96e1b282/. e28509.
4. Ziadé N, El Kibbi L, Hmamouchi I, et al. Impact of the COVID-19 pan- 23. Tam LS, Tanaka Y, Handa R, et al. Updated APLAR consensus state-
demic on patients with chronic rheumatic diseases: a study in 15 Arab ments on care for patients with rheumatic diseases during the COVID-
countries. Int J Rheum Dis 2020;23:1550–7. 19 pandemic. Int J Rheum Dis 2021;24:733–45.
5. Akintayo RO, Akpabio A, Kalla A, et al. COVID-19 and the practice of 24. Su Z, Cheshmehzangi A, McDonnell D, et al. The advantages of the
rheumatology in Africa: big changes to services from the shockwave zero-COVID-19 strategy [review]. Int J Environ Res Public Health
of a pandemic. Ann Rheum Dis 2021;80:e100. 2022;19:8767.
6. Ntshalintshali SD, Geldenhuys EM, Moosajee F, et al. Access to chlo- 25. Ahmed S, Grainger R, Santosa A, et al. APLAR recommendations on
roquine in patients with rheumatic and musculoskeletal diseases the practice of telemedicine in rheumatology. Int J Rheum Dis 2022;
attending rheumatology outpatient clinics during the COVID-19 pan- 25:247–58.
demic. S Afr Med J 2021;111:720–3. 26. Zhang Y, Wang J, Zhao L, et al. Online management of rheumatoid
7. Zomalheto Z, Assogba C, Dossou-yovo H. Impact of the severe acute arthritis during COVID-19 pandemic. Ann Rheum Dis 2021;80:e4.
respiratory syndrome coronavirus 2 (SARS-CoV2) infection and 27. Zeng H, Liu H, Liu Z, et al. Safety and immunogenicity of inactivated
disease-2019 (COVID-19) on the quality of life of rheumatoid arthritis COVID-19 vaccination in adult rheumatic patients in South China: a
patients in Benin. Egypt Rheumatol 2021;43:23–7. prospective study. Hum Vaccin Immunother 2022;18:2090176.
8. El Khouly RM, Elsabagh HM,Moawad AA, et al. Functional andmental 28. Fan Y, Geng Y, Wang Y, et al. Safety and disease flare of autoimmune
health affection (depression, anxiety, stress) among Egyptian rheu- inflammatory rheumatic diseases: a large real-world survey on inacti-
matic diseases patients during COVID-19 pandemic. Eur Rev Med vated COVID-19 vaccines. Ann Rheum Dis 2022;81:443–5.
Pharmacol Sci 2022;26:4477–85.
29. Yi Z, Yao Z, Xu D, et al. Attitudes toward COVID-19 vaccination: a sur-
9. Ziadé N, Hmamouchi I, El Kibbi L, et al. The impact of COVID-19 pan- vey of Chinese patients with rheumatic diseases. Vaccines (Basel)
demic on rheumatology practice: a cross-sectional multinational 2022;10:1604.
study. Clin Rheumatol 2020;39:3205–13.
30. Shen M, Dong L, Li M, et al. Recommendations on SARS-CoV-2 vac-
10. Akintayo RO, Akpabio AA, Kalla AA, et al. The impact of COVID-19 on cination in adult patients with rheumatic diseases. Rheumatol Immu-
rheumatology practice across Africa. Rheumatology (Oxford) 2021; nol Res 2021;2:213–6.
60:392–8.
31. Chinese Society of Infectious Diseases, Chinese Medical Association,
11. Akintayo RO, Bahiri R, El Miedany Y, et al. African League Against Chinese Society of Rheumatology, et al. Expert recommendation on
Rheumatism (AFLAR) preliminary recommendations on the manage- severe acute respiratory syndrome Coronavirus 2 vaccination in
ment of rheumatic diseases during the COVID-19 pandemic. Clin patients with chronic liver diseases, tuberculosis or rheumatoid dis-
Rheumatol 2021;40:3445–54. eases. Infectious Dis Immunity 2021;1:137–43.
12. Akintayo RO, Kalla A, Adebajo A. COVID-19 and African rheumatol- 32. Wilson N, Grout L, Summers JA, et al. Use of the elimination strategy
ogy: progress in adversity. Lancet Rheumatol 2020;2:e732–4. in response to the COVID-19 pandemic: health and economic
13. Africa Centres for Disease Control and Prevention. COVID 19 vaccine impacts for New Zealand relative to other OECD countries. medRxiv
perceptions: a 15 country study. 2021. URL: https://africacdc.org/ doi: https://doi.org/10.1101/2021.06.25.21259556. 2021. E-pub
download/covid-19-vaccine-perceptions-a-15-country-study/. ahead of print.
14. National Institute for Communicable Diseases. COVID-19 vaccine roll- 33. Stobart A, Duckett S. Australia’s response to COVID-19. Health Econ
out strategy FAQ. 2021. URL: https://www.nicd.ac.za/covid-19- Policy Law 2022;17:95–106.
vaccine-rollout-strategy-faq/. 34. Basseal JM, Bennett CM, Collignon P, et al. Key lessons from the
15. National Primary Health Care Development Agency. Frequently asked COVID-19 public health response in Australia [review]. Lancet Reg
questions. 2022. URL: https://nphcda.gov.ng/general-faqs/. Health West Pac 2023;30:100616.
16. Omran EA, Habashy RE, Ezz Elarab LA, et al. Anti-spike and neutraliz- 35. Cai K, He J, Wong PK, et al. The impact of COVID-19 on rheumatol-
ing antibodies after two doses of COVID-19 Sinopharm/BIBP vac- ogy clinical practice and university teaching in Sydney, Australia. Eur
cine. Vaccines (Basel) 2022;10:1340. J Rheumatol 2020;7 Suppl 2:S91–3.
17. Ben Houmich T, Tali A, Debbagh F, et al. Seroprevalence of SARS- 36. Oh Y, Hennessey A, Young L, et al. Evaluation of patient satisfaction
CoV-2 antibodies in vaccinated healthcare workers in Marrakech for telehealth (telephone and video) in rheumatology outpatients dur-
(Morocco). Int J Immunopathol Pharmacol 2022;36: ing COVID-19 pandemic. Intern Med J 2022;52:559–65.
3946320221133697. 37. Rischin A, Liew D, Black R, et al. Healthcare access and attitudes
18. Qi G, Wang H, Guo Y, et al. Clinical outcomes of COVID-19 patients towards telehealth during the early phase of the COVID-19 pandemic
with rheumatic diseases: a retrospective cohort study and synthesis among an Australian cohort with inflammatory arthritis. Intern Med J
analysis in Wuhan, China. Clin Rheumatol 2022;41:1899–910. 2021;51:788–92.
19. Ye C, Cai S, Shen G, et al. Clinical features of rheumatic patients 38. Jefferies S, French N, Gilkison C, et al. COVID-19 in New Zealand and
infected with COVID-19 in Wuhan, China. Ann Rheum Dis 2020;79: the impact of the national response: a descriptive epidemiological
1007–13. study. Lancet Public Health 2020;5:e612–23.
20. Zhao J, Pang R, Wu J, et al. Clinical characteristics and outcomes of 39. Sonder GJ, Grey C, Anglemyer A, et al. The August 2020 COVID-19
patients with COVID-19 and rheumatic disease in China ‘hot spot’ outbreak in Aotearoa, New Zealand: delayed contact tracing for
versus in US ‘hot spot’: similarities and differences. Ann Rheum Dis Pacific people contributes to widening health disparities. IJID Reg
2021;80:e63. 2023;6:177–83.
21. Zhong J, Shen G, Yang H, et al. COVID-19 in patients with rheumatic 40. Mair J, Woolley M, Grainger R. Abrupt change to telephone follow-up
disease in Hubei province, China: a multicentre retrospective obser- clinics in a regional rheumatology service during COVID-19: analysis
vational study. Lancet Rheumatol 2020;2:e557–64. of treatment decisions. Intern Med J 2021;51:960–4.
 21514658, 0, Downloaded from https://acrjournals.onlinelibrary.wiley.com/doi/10.1002/acr.25169 by University of Ghana - Accra, Wiley Online Library on [08/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
GLOBAL IMPACT OF COVID-19 ON RHEUMATOLOGY AND HEALTH EQUITY 9
41. Zhu W, De Silva T, Eades L, et al. The impact of telerheumatology and 59. Andrus JK, Evans-Gilbert T, Santos JI, et al. Perspectives on battling
COVID-19 on outcomes in a tertiary rheumatology service: a retro- COVID-19 in countries of Latin America and the Caribbean.
spective audit. Rheumatology (Oxford) 2021;60:3478–80. Am J Trop Med Hyg 2020;103:593–6.
42. Roberts LJ, Lamont EG, Lim I, et al. Telerheumatology: an idea whose 60. Busso M, Camacho J, Messina J, et al. Social protection and infor-
time has come. Intern Med J 2012;42:1072–8. mality in Latin America during the COVID-19 pandemic. PLoS One
2021;16:e0259050.
43. Jhaveri D, Emeto TI, Alele FO, et al. Use of telemedicine for rheumatol-
ogy practice in Queensland, Australia: experiences before and during 61. Gamboa-Cardenas RV, Barzola-Cerron S, Toledo-Neira D, et al. Pre-
the COVID-19 pandemic. Intern Med J 2022;52:1685–90. dictors of hospitalization for COVID-19 in patients with autoimmune
rheumatic diseases: results from a community cohort follow-up. Clin
44. Lim I. Private practice and telerheumatology. In: Peoples C, editor. Rheumatol 2021;40:4725–34.
Telerheumatology: origins, current practice, and future directions.
New York (NY): Springer Publishing; 2022. p. 281 9. 62. Quintana R, Fernandez S, Guggia L, et al. Social networks as educa-–
tion strategies for indigenous patients with rheumatoid arthritis during
45. Garrido-Cumbrera M, Marzo-Ortega H, Christen L, et al. Assessment COVID-19 pandemic. Are they useful? Clin Rheumatol 2022;41:
of impact of the COVID-19 pandemic from the perspective of patients 3313–8.
with rheumatic and musculoskeletal diseases in Europe: results from
the REUMAVID study (phase 1). RMD Open 2021;7:e001546. 63. Fernandez-Ávila DG, Barahona-Correa J, Romero-Alvernia D, et al.
Impact of COVID-19 pandemic on patients with rheumatic diseases
46. Finch D, Tinson A. The continuing impact of COVID-19 on health and in Latin America. Rheumatol Int 2022;42:41–9.
inequalities. The Health Foundation. 2022. URL: https://www.health.
org.uk/publications/long-reads/the-continuing-impact-of-covid-19- 64. Fernandez-Ávila DG, Barahona-Correa J, Romero-Alvernia D, et al.
on-health-and-inequalities. Impact of COVID-19 pandemic on rheumatology practice in Latin
America. J Rheumatol 2021;48:1616–22.
47. Dejaco C, Alunno A, Bijlsma JW, et al. Influence of COVID-19 pan-
65. Felten R, Dubois M, Ugarte-Gil MF, et al. Cluster analysis reveals three
demic on decisions for the management of people with inflammatory
main patterns of beliefs and intention with respect to SARS-CoV-2
rheumatic and musculoskeletal diseases: a survey among EULAR
vaccination in patients with autoimmune and inflammatory diseases.
countries. Ann Rheum Dis 2021;80:518–26.
Rheumatology (Oxford) 2021;60:SI68–76.
48. Machado PM, Verschueren P, Grainger R, et al. Impact of COVID-19 66. Mathieu E, Ritchie H, Rodés-Guirao L, et al. Coronavirus pandemic
pandemic on the management of patients with RA: a survey of rheu- (COVID-19). Our World in Data. 2020. URL: https://ourworldindata.
matologists in six European countries. Rheumatol Adv Pract 2022;7: org/coronavirus.
rkac108.
67. Santos-Moreno P, Rodríguez-Vargas GS, Casanova R, et al. Evalua-
49. Young K, Yeoh SA, Putman M, et al. The impact of COVID-19 on tion of a non-face-to-face multidisciplinary health care model in a pop-
rheumatology training-results from the COVID-19 Global Rheumatol- ulation with rheumatoid arthritis vulnerable to COVID-19 in a health
ogy Alliance trainee survey. Rheumatol Adv Pract 2022;6:rkac001. emergency situation. Healthcare (Basel) 2021;9:1744.
50. Mitchell EJ, Ahmed K, Breeman S, et al. It is unprecedented: trial man- 68. George MD, Venkatachalam S, Banerjee S, et al. Concerns, health-
agement during the COVID-19 pandemic and beyond. Trials 2020; care use, and treatment interruptions in patients with common auto-
21:784. immune rheumatic diseases during the COVID-19 pandemic.
51. Mirza M, Siebert S, Pratt A, et al. Impact of the COVID-19 pandemic J Rheumatol 2021;48:603–7.
on recruitment to clinical research studies in rheumatology. Musculo- 69. George MD, Baker JF, Banerjee S, et al. Social distancing, health care
skeletal Care 2022;20:209–13. disruptions, telemedicine use, and treatment interruption during the
52. Bijlsma JW, EULAR COVID-19 Task Force. EULAR 2021 updated COVID-19 pandemic in patients with or without autoimmune rheu-
viewpoints on SARS-CoV-2 vaccination in patients with RMDs: a matic disease. ACR Open Rheumatol 2021;3:381–9.
guidance to answer patients’ questions. Ann Rheum Dis 2022;81: 70. Maldonado D, Tu E, Mahmood SN, et al. Association of medication
786–8. access difficulty and COVID-19-related distress with disease flares in
rheumatology patients during the COVID-19 pandemic. Arthritis Care
53. Kroon FP, Najm A, Alunno A, et al. Risk and prognosis of SARS- Res (Hoboken) 2021;73:1162–70.
CoV-2 infection and vaccination against SARS-CoV-2 in rheumatic
and musculoskeletal diseases: a systematic literature review to inform 71. Dharia T, Venkatachalam S, Baker JF, et al. Medication interruptions
EULAR recommendations. Ann Rheum Dis 2022;81:422–32. and subsequent disease flares during the COVID-19 pandemic: a lon-
gitudinal online study of patients with rheumatic disease. Arthritis Care
54. Landewé RB, Machado PM, Kroon F, et al. EULAR provisional recom- Res (Hoboken) 2022;74:733–40.
mendations for the management of rheumatic and musculoskeletal
diseases in the context of SARS-CoV-2. Ann Rheum Dis 2020;79: 72. Mortezavi M, Lokineni S, Garg M, et al. Rheumatology patient satis-
851 8. faction with telemedicine during the COVID-19 pandemic in the–
United States. J Patient Exp 2021;8:23743735211008825.
55. Landewé RB, Kroon FP, Alunno A, et al. EULAR recommendations for 73. Shaw YP, Hustek S, Nguyen N, et al. Rheumatic disease patient
the management and vaccination of people with rheumatic and mus- decision-making about COVID-19 vaccination: a qualitative analysis.
culoskeletal diseases in the context of SARS-CoV-2: the November BMC Rheumatol 2022;6:76.
2021 update. Ann Rheum Dis 2022;81:1628–39.
74. George MD, Danila MI, Watrous D, et al. Disruptions in rheumatology
56. The Lancet. COVID-19 in Latin America: a humanitarian crisis [edito- care and the rise of telehealth in response to the COVID-19 pandemic
rial]. Lancet 2020;396:1463. in a community practice-based network. Arthritis Care Res (Hoboken)
57. Elera-Fitzcarrald C, Ugarte-Gil MF, Alarcon GS. COVID-19 and its 2021;73:1153–61.
potential effect on patients with rheumatic diseases in Latin America. 75. Gianfrancesco MA, Leykina LA, Izadi Z, et al. Association of race and
J Clin Rheumatol 2020;26:215–7. ethnicity with COVID-19 outcomes in rheumatic disease: data from
58. Isnardi CA, Roberts K, Saurit V, et al. Sociodemographic and clinical the COVID-19 Global Rheumatology Alliance Physician Registry.
factors associated with poor COVID-19 outcomes in patients with Arthritis Rheumatol 2021;73:374–80.
rheumatic diseases: data from the SAR-COVID Registry. Clin Rheu- 76. Ugarte-Gil MF, Alarcon GS, Seet AM, et al. Association between
matol 2023;42:563–78. race/ethnicity and COVID-19 outcomes in systemic lupus
 21514658, 0, Downloaded from https://acrjournals.onlinelibrary.wiley.com/doi/10.1002/acr.25169 by University of Ghana - Accra, Wiley Online Library on [08/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
10 HSIEH ET AL
erythematosus patients from the United States: data from the COVID- 78. Singh JA, Richards JS, Chang E, et al. Management of rheumatic dis-
19 Global Rheumatology Alliance. Arthritis Care Res (Hoboken) 2023; eases during the COVID-19 pandemic: a national Veterans Affairs survey
75:53–60. of rheumatologists. Arthritis Care Res (Hoboken) 2021;73:998–1003.
77. Curtis JR, Johnson SR, Anthony DD, et al. American College of Rheu- 79. Li J, Ringold S, Curtis JR, et al. Effects of the SARS-CoV-2 global
matology Guidance for COVID-19 vaccination in patients with pandemic on U.S. rheumatology outpatient care delivery and use of
rheumatic and musculoskeletal diseases: version 4. Arthritis Rheuma- telemedicine: an analysis of data from the RISE registry. Rheumatol
tol 2022;74:e21–36. Int 2021;41:1755–61.
 21514658, 0, Downloaded from https://acrjournals.onlinelibrary.wiley.com/doi/10.1002/acr.25169 by University of Ghana - Accra, Wiley Online Library on [08/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License