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. 2024 Mar 2;8(2):rkae027. doi: 10.1093/rap/rkae027

Characteristics of long COVID in patients with autoimmune rheumatic diseases: a systematic review and meta-analysis

Der-Yuan Chen 1,2,3, Po-I Huang 4, Kuo-Tung Tang 5,6,7,✉
PMCID: PMC10980592  PMID: 38560644

Abstract

Objectives

Numerous cases of long coronavirus disease (long COVID) have been reported in patients with autoimmune rheumatic diseases (ARDs). Despite the reviews on clinical manifestations of long COVID in the general population, systematic reviews on ARD patients are scarce. Herein, we conducted a systematic review and meta-analysis on the prevalence and characteristics of long COVID in ARD patients.

Methods

We searched the literature in PubMed and Embase as of 27 December 2022. Cohort, cross-sectional and case–control studies relevant to long COVID in ARD patients were collected. Stratification based on the severity of COVID infection and subtypes of rheumatic diseases [systemic autoimmune rheumatic disease (SARD) vs non-autoimmune rheumatic disease (NARD)] was also undertaken. A random-effects model was used in the meta-analysis.

Results

A total of 15 relevant studies were identified from the literature. The prevalence of long COVID was 56% (95% CI 34, 76) in 2995 patients. Hospitalized COVID patients had a higher proportion of long COVID than non-hospitalized patients. The prevalence of long COVID was similar between SARD and NARD patients. In terms of symptoms, fatigue, arthralgia and pain were commonly reported in long COVID patients with ARDs.

Conclusion

The characteristics of long COVID in ARD patients are generally similar to those in the general population despite a higher prevalence and a higher proportion of arthralgia and pain.

Keywords: fibromyalgia, long COVID, rheumatic disease, systemic autoimmune rheumatic disease

Key messages.

  • Studies on clinical manifestations of long COVID in rheumatic patients are relatively few.

  • Long COVID is more prevalent and associated with more arthralgia and pain in rheumatic patients.

  • Vaccination and timely treatment for COVID in rheumatic patients may prevent long COVID.

Introduction

The coronavirus disease 2019 (COVID-19) pandemic has been a great challenge worldwide over the last 3 years. Its clinical manifestations involve multiple organs and include fever, cough, shortness of breath, sore throat, myalgia, arthralgia, headache, rhinorrhoea, nausea, vomiting, diarrhoea and olfactory and gustatory dysfunctions [1, 2]. Despite the heterogeneity of symptoms between individuals and disease severity assessment across studies [3, 4], most patients were asymptomatic or presented with only mild symptoms. Some patients suffered from severe symptoms, with even life-threatening complications. Notably, a small proportion of COVID-19 patients developed persistent residual symptoms months after recovery from infections of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Such a phenomenon is known as either long COVID, post-COVID syndrome or post–acute COVID-19 sequelae [5]. A number of studies have shown that long COVID is prevalent in COVID-19 patients [6]. The persistent symptoms are variable and they involve organs such as the heart, brain, spleen, liver, gastrointestinal tract, kidney, pancreas and lung [7]. Currently, no definition of long COVID exists with consensus, mainly due to the heterogeneity of its symptoms [8]. Nevertheless, both the persistent and the new-onset symptoms after acute SARS-CoV-2 infection are included. The time points at which symptoms are assessed after the COVID-19 infection vary; e.g. for the Centers for Disease Control and Prevention (CDC), the time is at least 4 weeks later; for the World Health Organization (WHO) and National Institute for Health and Care Excellence (NICE), it is at least 12 weeks later [8].

The pathogenesis of long COVID remains unclear. The role of the immune system has been implicated [5]. Recently, the results of large cohort studies reported a higher risk of developing systemic autoimmune rheumatic disease (SARD) in COVID-19 patients, which suggested a persistent immune dysregulation long after resolution of COVID-19 infection [9, 10]. Both the disease severity and prognosis after SARS-CoV-2 infection are worse in SARD patients [11]. However, relevant studies regarding long COVID in these patients are scarce. Furthermore, clinical features of long COVID syndrome may be modified by the use of corticosteroids and immunosuppressants in patients with autoimmune rheumatic diseases (ARDs). In this systematic review, we aimed to summarize the characteristics of long COVID in ARD patients.

Materials and methods

Literature search

We focused on studies investigating long COVID syndrome in ARD patients. We searched both the Embase and MEDLINE databases and reviewed literature through 27 December 2022, irrespective of the language of publication. The search strategy is illustrated in Supplementary Table S1, available at Rheumatology Advances in Practice online, combining two sets of terms: one set involved a variety of ARDs and the other involved long COVID. A total of 15 studies were identified (Fig. 1) [12–26]. This systematic review was registered in PROSPERO (CRD42023451768).

Figure 1.

Figure 1.

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The algorithm of the literature search

Selection of studies

All three authors (K.T.T., P.I.H. and D.Y.C.) independently assessed the titles and abstracts identified. The relevant full-text articles were then retrieved. Two authors (K.T.T. and P.I.H.) independently evaluated the full-text articles for eligibility, i.e. articles on long COVID in ARD patients. We included observational studies such as case–control, cross-sectional and cohort studies. Conference abstracts were also included, but preprints, case reports and case series were excluded. Controversy, if present, was resolved through group discussion.

Data extraction

Information regarding the prevalence in ARD patients was retrieved and recorded in a standardized Excel file (Microsoft, Redmond, WA, USA). The outcome measures included the prevalence of long COVID and its symptoms. The risk factors for long COVID development were also documented and represented as odds ratios (ORs).

Risk of bias

Risk of bias was evaluated based on the Risk of Bias in Non-Randomised Studies of Interventions (ROBINS-I) [27, 28]. This tool incorporates seven major domains, including confounding, selection of participants, classification of intervention, deviation from interventions, missing outcome data, measurement of outcomes and selection of the reported result. The overall risk of bias was rated as 0, no information; 1, low risk; 2, moderate risk; 3, serious risk; and 4, critical risk. Two authors (P.I.H. and K.T.T.) independently assessed these risks of bias. Any disagreement, if present, was resolved through group discussion.

Data synthesis and statistical analyses

We summarized the prevalence of long COVID in all ARD patients. Stratification was made based on the severity of COVID-19 infection and subtypes of rheumatic diseases [SARD vs non-autoimmune rheumatic disease (NARD)]. A random-effects model was used in the meta-analysis based on the procedure of DerSimonian and Laird [29]. Heterogeneity was quantified using τ2, χ2 and I2 as measured in the Mantel–Haenszel model. Funnel plots, as well as Begg’s and Egger’s tests, were used to evaluate the publication bias if more than two studies were included in the meta-analyses. All statistical analyses were performed using Stata version 14.0 (StataCorp, College Station, TX, USA).

Results

Study characteristics

Characteristics of the enrolled studies are shown in Supplementary Table S2, available at Rheumatology Advances in Practice online. Most study participants were adult female Caucasians in Western countries. The mean/median age of study participants ranged from 47 to 71 years. Most studies involved SARD patients. The most common SARD was RA and the most common NARD was FM. Most of the studies surveyed long COVID symptoms based on clinical evaluation, with these persistent symptoms lasting for a minimum of 28 days after COVID-19 infection.

Prevalence of long COVID in ARD patients

As illustrated in Fig. 2, the prevalence of long COVID in SARS-CoV-2-infected ARD patients was 56% (95% CI 34, 76). Its prevalence appeared higher in hospitalized COVID-19 patients when compared with non-hospitalized patients [69% (95% CI 61, 77) vs 41% (95% CI 33, 49)] (Fig. 3). There was no difference in the prevalence rates of long COVID between SARD and NARD patients [62% (95% CI 55, 69] vs 67% (95% CI 48, 83)].

Figure 2.

Figure 2.

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The prevalence of long COVID in patients with rheumatic diseases. The black squares represent the effect estimates of the individual studies and the diamonds represent the summary effect estimates

Figure 3.

Figure 3.

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The prevalence of long COVID in rheumatic patients after stratification by hospitalization status and disease subtypes. The black squares represent the effect estimates of the individual studies and the diamonds represent the summary effect estimates

Symptoms of long COVID in ARD patients

As shown in Fig. 4, fatigue was reported as the most common symptom and its prevalence was 33% (95% CI 14, 54). Arthralgia and pain were the second and third most common symptoms. The prevalence of arthralgia was 31% (95% CI 5, 66) and the prevalence of pain was 25% (95% CI 21, 29). Respiratory distress was also common and its prevalence was 21% (95% CI 9, 38). One, two or three long COVID symptoms were found in 20–89%, 35–61% and 39–76%, respectively, in ARD patients with long COVID [14, 15, 19, 22, 23, 26]. In SARD patients in the Danish national health registry hospitalized due to COVID-19 infection, Nogard et al. reported higher risks for later hospitalization due to respiratory diseases [adjusted hazard ratio (HR) 1.20 (95% CI 1.02, 1.58)] and infections [adjusted HR 1.55 (95% CI 1.26, 1.92)] [24]. In rheumatic patients with long COVID, Barbhaiya et al. [13] observed worse anxiety and depression based on the Patient-Reported Outcomes Measurement Information System (PROMIS) when compared with patients without long COVID. Cox et al. [17] conducted a survey using the 36-item Short-Form in COVID-19-infected rheumatic patients and found that mental components, but not physical components, were worse in those patients who developed long COVID vs those who did not.

Figure 4.

Figure 4.

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The prevalence of long COVID symptoms in patients with rheumatic diseases. The black squares represent the summary effect estimates.

Potential risk factors for long COVID in ARD patients

As shown in Table 1, the severity of COVID-19 infection (hospitalization, pneumonia, symptoms severity, length of hospitalization/intensive care unit stay) was associated with the development of long COVID in ARD patients. Notably, hospitalization due to COVID-19 was associated with long COVID development, with an OR of 3.54–8.29 [15, 21]. Gomez et al. [19] previously reported a higher risk for long COVID in non-Caucasians. In terms of disease activity, Gomez et al. [19] reported no difference in the proportion of low disease activity/remission between those patients who developed and those who did not develop long COVID. Aronova et al. [12] also observed no difference in disease activity of RA between those patients who developed and those who did not develop long COVID. In terms of the prescribed medications, the use of hydroxychloroquine during COVID-19 infection was positively associated with the development of long COVID [OR 2.52 (95% CI 1.00, 6.47)]. Prior use of systemic corticosteroids and cyclophosphamide was similarly associated with long COVID [OR 4.95 (95% CI 1.65, 14.82) and 11.35 (95% CI 1.56, 112.97), respectively].

Table 1.

Risk factors for long COVID in rheumatic patients

Study Risk factors
Barbhaiya et al. [13] Comorbidities [OR 3.17 (95% CI 1.89, 5.32)], smoking [OR 2.21 (95% CI 1.19, 4.09)], corticosteroids use [OR 4.95 (95% CI 1.65, 14.82)] and COVID-19 symptoms
Batıbay et al. [14] Non-smoking [OR 7.70 (95% CI 1.67, 35.43)]
Brito-Zerón et al. [15] Elevated CRP [OR 8.60 (95% CI 1.33, 104.44)], hydroxychloroquine use [OR 2.52 (95% CI 1.00, 6.47)] and hospital admission [OR 4.96 (95% CI 1.91, 13.87)]
Gomez et al. [19] Non-Caucasian [OR 1.44 (95% CI 1.07, 1.95)], years of education [OR 1.05 (95% CI 1.00, 1.09)], cyclophosphamide [OR 11.35 (95% CI 1.56, 112.97)], symptoms of COVID-19 [OR 13.26 (95% CI 2.75, 242.08)], severe COVID-19 disease [OR 2.46 (95% CI 1.68, 3.57)] and intensive care unit hospitalization days [OR 1.09 (95% CI 1.05, 1.14)]
Husni et al. [20] Better pre-COVID patient-reported outcomes
De Iorio et al. [21] Hospitalization for COVID-19 [OR 3.54 (95% CI 1.27, 9.87)] and initial COVID-19 symptom count [OR 1.38 (95% CI 1.17, 1.63)]
Leon et al. [22] Female sex [OR 3.53 (95% CI 1.24, 10.08)], age >60 years (OR 0.09–0.11), comorbidities [OR 1.90 (95% CI 1.09, 3.31)], lymphopenia [OR 3.17 (95% CI 1.07, 9.40)] and pneumonia [OR 10.1 (95% CI 1.50, 66.01)]
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Long COVID in FM patients

Büyükşireci et al. [16] compared 77 FM patients recovering from COVID-19 infection, irrespective of the presence of long COVID, and 57 FM patients who did not contract COVID-19. They found that COVID-19-infected FM patients had similar disease severity, but had higher HADS anxiety scores and widespread pain index when compared with patients who did not contract COVID-19. Rivera et al. [21] compared 78 FM patients and 56 SARD patients after COVID-19 infection and found that FM patients reported more long COVID symptoms and worse patient global assessment compared with SARD patients.

Risk of bias

As shown in Supplementary Fig. S1, available at Rheumatology Advances in Practice online, 5 (33%) of the 15 studies were recognized as having a serious risk of bias.

Publication bias

We demonstrated the existence of potential publication bias with regards to the prevalence of long COVID and its symptoms in rheumatic patients except for anosmia (Supplementary Figs S2 and S3, available at Rheumatology Advances in Practice online).

Discussion

In this systematic review and meta-analysis, we found a higher prevalence of long COVID in ARD patients when compared with the general population. In addition, the proportion of arthralgia and pain appeared higher in ARD patients with long COVID. The prevalence of long COVID was similar between SARD and NARD patients. Disease severity of acute COVID-19 infection was associated with an increased risk for long COVID in ARD patients. Despite the limited number of studies, the use of medications might affect such risk in these patients.

Several factors have been implicated in the generation of long COVID, including viral persistence, tissue damage, metabolic change, autonomic dysfunction and psychosocial burden [30–33]. SARS-CoV-2 infection could promote the production of a myriad of cytokines and chemokines, the so-called cytokine storm, which likely leads to autoimmune and rheumatic manifestations [34]. The immune system is probably involved in the pathogenesis of long COVID. Previous reports of long COVID patients showed elevated levels of type I and type III IFNs, TNF-α, G-CSF, IL-17A, IL-6, IL-1β and IL-13, whereas IFN-γ-induced protein 10 (IP-10) levels decreased, when compared with levels in the acute phase of COVID-19 infection [35, 36]. Long COVID patients also had activated innate immune cells such as myeloid cells, Th9, CD4+ effector memory T cells, CD8+ effector T cells and naïve B cells [35, 36]. Furthermore, persistently elevated levels of anti-SARS-CoV-2 IgG antibodies were noted in these patients [35]. Interestingly, a murine experiment showed neuroinflammation after SARS-CoV-2 infection and, in particular, CCL11 persistently impaired neurogenesis and glial activity [5]. Consistent with this, circulating levels of CCL11 are elevated in long COVID patients with cognitive symptoms.

Owing to global efforts, the occurrence of devastating complications of acute COVID-19 infection, such as sepsis, respiratory failure and even death, have decreased. However, long-term sequelae of COVID-19 infection emerged [8]. Long COVID comprises >100 symptoms and significantly impairs patients’ quality of life. It is the next conundrum we need to face in the post-pandemic era. SARD patients have a more severe disease course and higher mortality during acute COVID infection when compared with the general population. Moreover, the use of Janus kinase inhibitors and rituximab was associated with severe COVID-19 in patients with RA [37]. We hypothesized that ARD patients are predisposed to long COVID due to pre-existing immune dysregulation and therefore show more severe symptoms with acute COVID-19 infections. A prior meta-analysis estimated the prevalence of long COVID in the general population at 43% (95% CI 0.39, 0.46) [38]. We noted a higher prevalence of long COVID among ARD patients despite heterogeneity across studies. On the other hand, Fernández de las Peñas et al. [18] conducted a multicentre study in Spain based on telephone interviews of 1969 participants. They found that pre-existing rheumatic diseases are not independently associated with the development of long COVID [OR 1.46 (95% CI 0.89, 2.40)]. In addition, SARD patients, who had an inherently exaggerated immune response, are not more likely to develop long COVID than NARD patients. More cohort studies are needed to clarify this issue.

In terms of symptoms of long COVID, fatigue was most commonly found. This is consistent with results in the general population [38]. In the study of Brito-Zerón et al. [15], >90% of SARD patients with long COVID have fatigue. Pain-related symptoms were the second most common symptom in ARD patients with long COVID, which was different from that in the general population (memory problems) [38]. This is probably due to the inherent pain susceptibility in ARD patients [39].

We found that the prevalence of long COVID in ARD patients with hospitalization due to COVID-19 was higher than that in patients without hospitalization. This finding is consistent with that in the general population [38]. COVID-19 severity, as measured by different parameters, is also a potential risk factor based on studies of ARD patients. It is therefore possible to alleviate the severity of acute COVID-19 infection to reduce the occurrence of long COVID. The prevalence of long COVID was slightly higher in Asian countries than in Europe and the USA [38]. Interestingly, non-Caucasian ethnicity was associated with a higher risk for long COVID [OR 1.44 (95% CI 1.07, 1.95)] in ARD patients, as reported by Gomez et al. [19]. In terms of medications, the limited data suggest a potential influence of hydroxychloroquine, corticosteroids and cyclophosphamide on the risk for long COVID in ARD patients. Such associations may be confounded and further studies of larger cohorts are needed.

FM patients had a similar symptom profile with long COVID [40]. In addition, viral illness has been reported to cause FM syndromes [41]. Two studies investigated long COVID in FM patients. Rivera et al. [25] found a trend of a higher percentage of long COVID in FM patients when compared with SARD patients (80% vs 66%; P = 0.081). As expected, FM patients reported more long COVID symptoms than SARD patients, likely related to the similarity of symptoms between FM and long COVID. However, they did not find an increased severity of FM, as measured by the Polysymptomatic Distress Scale, after COVID-19 infection, although a previous report showed increased FM severity during acute COVID infection [42]. Büyükşireci et al. [16] found no difference in disease severity, except for anxiety, between FM patients with and without prior COVID-19 infection. These findings do not corroborate the thesis that FM and long COVID share similar pathogenic mechanisms.

Currently there is no effective treatment for long COVID. The National Institutes of Health recently launched trials on the Researching COVID to Enhance Recovery initiative. Across the USA, trial interventions included a longer dosing of antiviral agents (nirmatrelvir and ritonavir), cognitive training and transcranial direct current stimulation. Results of these trials will likely shed light on the treatment options for long COVID. In terms of preventive measures, vaccination and antiviral agents have been shown to be associated with a lower risk for development of long COVID in cohort studies, although little is known on ARD patients [43, 44].

Our review has some limitations. First, the baseline demographics of study populations, their comorbidities, variants of the SARS-CoV-2 virus [45] and outcome definitions varied considerably across studies. Such heterogeneity in the study population makes interpretation of the results difficult. For instance, the I2 statistic was 98.9% in terms of the meta-analysis of the prevalence of long COVID-19 in ARD patients. Second, underrepresentation of other ethnic groups such as Asians, and age groups such as adolescents and children, is obviously a knowledge gap that requires more data. Lastly, the relatively few studies with a small sample size and significant risk of bias suggested an urgent need to conduct more research to elucidate the question in ARD patients, who are potentially susceptible to the development of long COVID. We performed analyses after excluding studies with a serious risk of bias. The results changed slightly and the prevalence of long COVID was even higher [65% (95% CI 48, 81)] in ARD patients (Supplementary Fig. S4, available at Rheumatology Advances in Practice online). The most common symptom was arthralgia [with a prevalence of 41% (95% CI 10, 77)] rather than fatigue [with a prevalence of 39% (95% CI 21, 57)] in these patients. Notwithstanding these limitations, our review provides an overview of long COVID in ARD patients.

Conclusions

Characteristics of long COVID in ARD patients are basically similar to those in the general population despite a higher prevalence and more of them suffering from arthralgia and pain. In ARD patients, severe COVID-19 infection is a potential risk factor for long COVID. Vaccination and timely treatment for COVID-19 in ARD patients could probably reduce the incidence of long COVID and should be recommended by rheumatologists.

Supplementary Material

rkae027_Supplementary_Data
rkae027_supplementary_data.docx (613.3KB, docx)

Contributor Information

Der-Yuan Chen, Rheumatology and Immunology Center, China Medical University Hospital, Taichung, Taiwan; College of Medicine, China Medical University, Taichung, Taiwan; College of Medicine, National Chung Hsing University, Taichung, Taiwan.

Po-I Huang, Department of Internal Medicine, Taichung Veterans General Hospital, Taichung, Taiwan.

Kuo-Tung Tang, Division of Allergy, Immunology, and Rheumatology, Taichung Veterans General Hospital, Taichung, Taiwan; Faculty of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan; Ph.D. Program in Translational Medicine and Rong Hsing Research Center for Translational Medicine, National Chung Hsing University, Taichung, Taiwan.

Supplementary material

Supplementary material is available at Rheumatology Advances in Practice online.

Data availability

The data underlying this article will be shared upon reasonable request to the corresponding author.

Authors’ contributions

Concept and design: K.T.T. and D.Y.C. Acquisition, analysis, or interpretation of data: K.T.T. and P.I.H. Drafting of the manuscript: K.T.T. and P.I.H. Review of the manuscript: D.Y.C. Statistical analysis: K.T.T. Supervision: K.T.T. and D.Y.C.

Funding

This work was supported by Taichung Veterans General Hospital (TCVGH-1123801C), Taichung, Taiwan, Republic of China.

Disclosure statement: The authors have declared no conflicts of interest.

References

  • 1. Gandhi RT, Lynch JB, Del Rio C.. Mild or moderate covid-19. N Engl J Med 2020;383:1757–66. [DOI] [PubMed] [Google Scholar]
  • 2. Guan WJ, Ni ZY, Hu Y. et al. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med 2020;382:1708–20. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3. Guerin PJ, McLean ARD, Rashan S. et al. Definitions matter: heterogeneity of COVID-19 disease severity criteria and incomplete reporting compromise meta-analysis. PLOS Glob Public Health 2022;2:e0000561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4. Rodebaugh TL, Frumkin MR, Reiersen AM. et al. Acute symptoms of mild to moderate COVID-19 are highly heterogeneous across individuals and over time. Open Forum Infect Dis 2021;8:ofab090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5. Su Y, Yuan D, Chen DG. et al. Multiple early factors anticipate post-acute COVID-19 sequelae. Cell 2022;185:881–95 e20. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6. Borchers A, Pieler T.. Programming pluripotent precursor cells derived from Xenopus embryos to generate specific tissues and organs. Genes (Basel) 2010;1:413–26. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7. Crook H, Raza S, Nowell J, Young M, Edison P.. Long covid—mechanisms, risk factors, and management. BMJ 2021;374:n1648. [DOI] [PubMed] [Google Scholar]
  • 8. Scharf RE, Anaya JM.. Post-COVID syndrome in adults—an overview. Viruses 2023;15:15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9. Chang R, Yen-Ting Chen T, Wang SI. et al. Risk of autoimmune diseases in patients with COVID-19: a retrospective cohort study. EClinicalMedicine 2023;56:101783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10. Tesch F, Ehm F, Vivirito A. et al. Incident autoimmune diseases in association with SARS-CoV-2 infection: a matched cohort study. Clin Rheumatol 2023;42:2919–20. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11. Tang KT, Hsu BC, Chen DY.. Immunogenicity, effectiveness, and safety of COVID-19 vaccines in rheumatic patients: an updated systematic review and meta-analysis. Biomedicines 2022;10:10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12. Aronova E, Gridneva G, Belov B.. Characteristics of post-COVID syndrome in patients with rheumatoid arthritis. Ann Rheum Dis 2022;81:1669–70.35985811 [Google Scholar]
  • 13. Barbhaiya M, Jannat-Khah D, Levine J.. Risk factors for “long haul” COVID-19 in rheumatology outpatients in New York City. Arthritis Rheumatol 2021;73(Suppl 9):abstract 0095. [Google Scholar]
  • 14. Batıbay S, Kocak UR, Gunendi Z, Gogus F.. The prevalence and clinical spectrum of post-Covid syndrome in patients with rheumatic diseases: a single-center experience. Reumatismo 2022;74:1481. [DOI] [PubMed] [Google Scholar]
  • 15. Brito-Zerón P, Acar-Denizli N, Romao VC. et al. Post-COVID-19 syndrome in patients with primary Sjogren’s syndrome after acute SARS-CoV-2 infection. Clin Exp Rheumatol 2021;39(Suppl 133):57–65. [DOI] [PubMed] [Google Scholar]
  • 16. Büyükşireci DE, Türk AÇ, Erden E, Erden E.. Evaluation of pain, disease activity, anxiety, depression, and neuropathic pain levels after COVID-19 infection in fibromyalgia patients. Ir J Med Sci 2023;192:1387–93. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17. Cox N, Raizada SR, Barkham N, Bateman J.. Long COVID is associated with poor mental health in patients with rheumatic disease: results from a 14-month longitudinal study. Rheumatology (Oxford) 2022;61(Suppl 1):keac133.074. [Google Scholar]
  • 18. Fernández-de-Las-Peñas C, Martín-Guerrero JD, Navarro-Pardo E. et al. The presence of rheumatological conditions is not a risk factor of long-term post-COVID symptoms after SARS-CoV-2 infection: a multicenter study. Clin Rheumatol 2022;41:585–6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19. Gomez CAG, Cosatti M, Coello VVC. et al. Prevalence of long COVID in rheumatic disease patients: analysis of SAR COVID registry. Ann Rheum Dis 2022;81:1668–9. [Google Scholar]
  • 20. Husni ECC, Lapin B, Kirchner E, Calabrese L.. Impact of COVID-19 infection on patient-reported outcomes in rheumatic disease patients: a cross sectional study. Arthritis Rheumatol 2021;73(Suppl 9):abstract 1537. [Google Scholar]
  • 21. Di Iorio M, Cook CE, Vanni KMM. et al. DMARD disruption, rheumatic disease flare, and prolonged COVID-19 symptom duration after acute COVID-19 among patients with rheumatic disease: a prospective study. Semin Arthritis Rheum 2022;55:152025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22. Leon L, Perez-Sancristobal I, Madrid A. et al. Persistent post-discharge symptoms after COVID-19 in rheumatic and musculoskeletal diseases. Rheumatol Adv Pract 2022;6:rkac008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23. Mukhamadieva V, Lapshina S, Shamsutdinova N. et al. Clinical characteristics of patients with spondyloarthritis with COVID-19 in anamnesis in the Republic of Tatarstan. Ann Rheum Dis 2022;81:1553. [Google Scholar]
  • 24. Norgard BM, Zegers FD, Nielsen J, Kjeldsen J.. Post COVID-19 hospitalizations in patients with chronic inflammatory diseases—a nationwide cohort study. J Autoimmun 2021;125:102739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25. Rivera J, Rodriguez T, Pallares M. et al. Prevalence of post-COVID-19 in patients with fibromyalgia: a comparative study with other inflammatory and autoimmune rheumatic diseases. BMC Musculoskelet Disord 2022;23:471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26. Shamsutdinova N, Lapshina S, Mukhamadieva V. et al. Clinical characteristics of patients with rheumatoid arthritis who underwent COVID-19 in the Republic of Tatarstan. Ann Rheum Dis 2022;81:1695.35973806 [Google Scholar]
  • 27. Sterne JA, Hernan MA, Reeves BC. et al. ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions. BMJ 2016;355:i4919. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28. Schunemann HJ, Cuello C, Akl EA. et al. GRADE guidelines: 18. How ROBINS-I and other tools to assess risk of bias in nonrandomized studies should be used to rate the certainty of a body of evidence. J Clin Epidemiol 2019;111:105–14. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29. DerSimonian R, Laird N.. Meta-analysis in clinical trials. Control Clin Trials 1986;7:177–88. [DOI] [PubMed] [Google Scholar]
  • 30. Delorme C, Paccoud O, Kas A. et al. COVID-19-related encephalopathy: a case series with brain FDG-positron-emission tomography/computed tomography findings. Eur J Neurol 2020;27:2651–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31. Al-Hakeim HK, Al-Rubaye HT, Al-Hadrawi DS, Almulla AF, Maes M.. Long-COVID post-viral chronic fatigue and affective symptoms are associated with oxidative damage, lowered antioxidant defenses and inflammation: a proof of concept and mechanism study. Mol Psychiatry 2023;28:564–78. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32. Dani M, Dirksen A, Taraborrelli P. et al. Autonomic dysfunction in ‘long COVID’: rationale, physiology and management strategies. Clin Med (Lond) 2021;21:e63–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33. Passavanti M, Argentieri A, Barbieri DM. et al. The psychological impact of COVID-19 and restrictive measures in the world. J Affect Disord 2021;283:36–51. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34. Tang KT, Hsu BC, Chen DY.. Autoimmune and rheumatic manifestations associated with COVID-19 in adults: an updated systematic review. Front Immunol 2021;12:645013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35. Acosta-Ampudia Y, Monsalve DM, Rojas M. et al. Persistent autoimmune activation and proinflammatory state in post-coronavirus disease 2019 syndrome. J Infect Dis 2022;225:2155–62. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36. Phetsouphanh C, Darley DR, Wilson DB. et al. Immunological dysfunction persists for 8 months following initial mild-to-moderate SARS-CoV-2 infection. Nat Immunol 2022;23:210–6. [DOI] [PubMed] [Google Scholar]
  • 37. Sparks JA, Wallace ZS, Seet AM. et al. Associations of baseline use of biologic or targeted synthetic DMARDs with COVID-19 severity in rheumatoid arthritis: results from the COVID-19 Global Rheumatology Alliance physician registry. Ann Rheum Dis 2021;80:1137–46. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38. Chen C, Haupert SR, Zimmermann L. et al. Global prevalence of post-coronavirus disease 2019 (COVID-19) condition or long COVID: a meta-analysis and systematic review. J Infect Dis 2022;226:1593–607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39. Phillips K, Clauw DJ.. Central pain mechanisms in the rheumatic diseases: future directions. Arthritis Rheum 2013;65:291–302. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40. Clauw DJ, Calabrese L.. Rheumatology and long COVID: lessons from the study of fibromyalgia. Ann Rheum Dis 2023;83:136–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41. Tang KT, Lin CC, Chen YH. et al. Direct-acting antiviral drugs reduce fibromyalgia symptoms in patients with chronic hepatitis C. J Clin Med 2022;11:5327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42. Salaffi F, Giorgi V, Sirotti S. et al. The effect of novel coronavirus disease-2019 (COVID-19) on fibromyalgia syndrome. Clin Exp Rheumatol 2021;39(Suppl 130):72–7. [DOI] [PubMed] [Google Scholar]
  • 43. Brannock MD, Chew RF, Preiss AJ. et al. Long COVID risk and pre-COVID vaccination in an EHR-based cohort study from the RECOVER program. Nat Commun 2023;14:2914. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44. Xie Y, Choi T, Al-Aly Z.. Association of treatment with nirmatrelvir and the risk of post-COVID-19 condition. JAMA Intern Med 2023;183:554–64. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45. Antonelli M, Pujol JC, Spector TD, Ourselin S, Steves CJ.. Risk of long COVID associated with delta versus omicron variants of SARS-CoV-2. Lancet 2022;399:2263–4. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

rkae027_Supplementary_Data
rkae027_supplementary_data.docx (613.3KB, docx)

Data Availability Statement

The data underlying this article will be shared upon reasonable request to the corresponding author.

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