Artigos

INTRODUCTION
The COVID-19 pandemic has triggered several changes in health care service at all levels1. With the fast disease dissemination and consequently increased mortality, health care services needed to be restructured and adjusted worldwide2. Urgency and emergency medical services were prioritized3, and primary and specialized care services had to be restructured hampering patients follow-up. Thus, this scenario led to impaired disease management of patients with non-communicable diseases (NCDs), worsening the clinical status of their pre-existing disease4.
A study conducted in the Americas showed that NCDs prevention and treatment services were impaired because health care professionals were reallocated to aid patients with COVID-195. Patients with diabetes, cardiovascular disease and cancer decreased their health care utilization in Germany during social restriction measures6. In Brazil, a study showed that scheduling appointments, acquiring medications, and accessing scheduled appointments were difficult for people with NCDs7. This population uses health services twice as much compared to people without NCDs7 and they have a 70.0% higher risk of complications due to COVID infection, increasing their vulnerability when chronic conditions are not well controlled and managed8. A study conducted in the Rio Grande do Sul state, southern Brazil, revealed that 43.1% of people with NCDs required medical care, and 28.% reported difficulties in managing their condition during social distancing 9 .
These changes generate negative impacts on the health of people with NCDs since COVID-19 can aggravate COVID-19 their condition increasing the risk of death 10. Furthermore, evidence on health care utilization is important for planning future actions to reduce mortality and disease-related complications. Thus, this study aimed to evaluate health care utilization after COVID-19 in people with non-communicable diseases (NCDs) in individuals from Rio Grande, Rio Grande do Sul, Brazil.

METHODS
Study design
We analyzed the baseline data from the Sulcovid-19 study, a longitudinal study that track health indicators in individuals infected by SARS-CoV-2 in the city of Rio Grande, Rio Grande do Sul, Brazil. Participants were 18 or older, have received a COVID-19 diagnosis through RT-PCR testing between December 2020 and March 2021, experienced symptoms related to COVID-19, and have sought medical care in Rio Grande. The study protocol was approved by the Health Research Ethics Committee (CEPAS) of the Federal University of Rio Grande (FURG) (CAAE: 39081120.0.0000.5324) following the rules and regulatory guidelines for Research involving human beings. The participants had their rights respected, ensuring their willingness, anonymity, and the possibility of withdrawal at any time, as recommended by the Resolution of the National Health Council No. 466, dated December 12th, 2012. Ethical principles were upheld through verbal (during telephone data collection) and consent form signature (during home visits). Both consents were thoroughly explained to the participants, and the verbal consent was approved by the Research Ethics Committee.
Setting
The study was conducted in the city of Rio Grande, Rio Grande do Sul state, Brazil. Rio Grande is located at the southern coast of the state and has a population of approximately 212,881 inhabitants. We contacted the Epidemiological Health Surveillance department of Rio Grande. Subsequently, a list comprising 4,014 individuals who had tested positive for SARS-CoV-2 through RT-PCR, along with their relevant details such as name, address, phone number, and the presence of symptoms was compiled. We excluded individuals who had incomplete data in the epidemiological surveillance patient list, any cognitive impairment, and who were in long-stay institutions or deprived of freedom (prisons), leading to 3,822 individuals being considered eligible for the study. Further details can be found in Flowchart 1.

Participants
Eligible participants were contacted by a telephone call and invited to take part in the study. When telephone calls were not possible or participants were not reached after five attempts, a home visit was made. Individuals who were not located after five contact attempts and two home visits were considered as lost. The interviews were conducted by previously trained interviewers and lasted 15-20 minutes.
The data were collected using the Redcap software. The instrument was designed to be applied both by phone and in-person (using tablets), covering semi-structured questions that were built based on standardized instruments. Questions addressed socioeconomic variables, COVID-19 symptoms during and after the acute infection phase, health care utilization, health conditions, fatigue, physical activity, behavior and food safety, functional capacity, musculoskeletal symptoms, and behavioral characteristics. The instrument was previously tested through a pilot study conducted with individuals meeting the inclusion criteria but who had been infected in a period prior to that specified in the study. Further information regarding the study design and recruitment process can be found elsewhere11.
Variables
We asked participants about a medical diagnosis of the following NCDs: systemic arterial hypertension (SAH), diabetes mellitus (DM), respiratory diseases (ie., asthma/bronchitis/emphysema/chronic obstructive pulmonary diseases) (RD), and heart diseases (HD). The NCDs variable was created considering those participants with at least one of the four self-reported diseases as a dichotomized variable (no/yes).
We asked participants whether they used health care after COVID-19. The following services were listed: urgency and emergency services (e.g., Emergency room, urgent care unit), Basic health unit, general practitioner, Emergency room (in portuguese “Pronto socorro”), Emergency care unit (in portuguese “Unidade de pronto atendimento”), Private emergency care unit (in portuguese “Unidade de pronto atendimento particular”), Medical specialists (i.e., Pulmonologist, cardiologist, psychiatrist, neurologist), Specialized services (e.g., Neurologist, pulmonologist, cardiologist, psychiatrist, psychologist, physical therapist, speech therapist), Pulmonologist, Neurologist, Cardiologist, Psychiatrist, Physical therapist, Psychologist, and Speech therapist. All questions related to health care utilization were dichotomized (yes/no).
The following covariates were used to adjust for possible confounding: sex (male/female), age (19-29/ 30-39/ 40-49/ 50-59/ 60 or more), ethnicity (White; yellow/black; brown; indigenous), educational level (Elementary school/ High school/College education), marital status (Married; living with partner/ Single; separated; widowed) and economic class (A/ B; C; D/E)12.
Statistical methods
Descriptive data is presented as proportions (%) with their corresponding 95% confidence intervals (95%CI).We used Poisson regression to evaluate the relationship between health care utilization after COVID-19 and NCDs. Adjusted analyzes were performed using Poisson regression with robust adjustment of variance. Furthermore, the Poisson model estimates measures of prevalence ratio (PR) with 95%CI. All associations with 95%CI with no overlap between categories were considered statistically significant. Data were analyzed using the statistical package Stata 16.1.
RESULTS
A total of 3,822 participants with a positive COVID-19 test were eligible for the study and after losses and refusals 2,919 were interviewed (76.4%). Participant’s characteristics are displayed in Table 1. Briefly, most of the participants aged 18-59 (83.3%), were female (58.6%), white (77.9%), lived with a partner (60.6%), had high school education (42.2%), and were from economic class C (54.8%). NCDs diagnosis was reported by 41.5%, being 25.3% SAH, 10.1% DM, 9.0% HD, and 16.8% RD.
Table 2 shows the prevalence of health care utilization according to independent variables. Private emergency care units showed the highest prevalence regardless of disease. When analyzed by disease, the highest prevalence observed was for private emergency care units for HD (53.5%; 95%CI 35.1-70.7), and the lowest prevalence for speech therapist for SAH (0.3; 95%CI 0.07-1.1), and DM (0.3; 95%CI 0.05-2.4). Health care utilization among individuals with NCDs was higher in all services when compared to those without NCDs. These differences ranged from 2 to 50%, as observed in the use of private emergency for HD.
The crude analysis between healthcare services and NCDs can be found in Supplementary Material 1. Table 3 shows the adjusted analyzes between these variables. Overall, the high prevalence of health care utilization among participants with NCDs was up to four times when compared to participants without NCDs. Specifically, participants with NCDs had a 1.67 (95%CI 1.33; 2.11) times higher prevalence urgent and emergency services utilization, compared to individuals without NCDs. When analyzed by specific NCDs, only HD was associated with emergency room and emergency care unit use (PR 2.14, 95%CI 1.30; 3.54; PR1.70, 95%CI 1.31;2.20, respectively). The high prevalence basic health unit utilization was increased in those participants with at least one NCD (PR 1.29, 95%CI 1.13; 1.46), as well as in those with SAH (PR 1.24, 95%CI 1.07; 1.43), DM (PR 1.23, 95%CI 1.02; 1.47) and HD (PR1.27, 95%CI 1.10; 1.47). The higher utilization of medical specialists and specialized services draws attention, which can be up to 3 times higher among individuals with NCDs. Among specialists, an increased use of specialized services (i.e., cardiologist) is highlighted among individuals with at least one NCD (PR 3.77, 95%CI 2.97; 4.80), SAH (PR 3.47, 95%CI 2.97; 4.31), and DM (PR 3.87; 95%CI 3.11; 4.81).


DISCUSSION
We revealed a high prevalence of health care utilization after COVID-19 by people with NCDs, regardless of disease. Urgency and emergency services were highly used by participants with SAH and HD. When analyzing all NCDs, basic health units were used 30% more, except for RD. An increased use was observed for medical specialists and specialized services, with emphasis for cardiologist.
Urgency and emergency services utilization was 70% higher among participants with NCDs infected with COVID-19. Because of the COVID-19 pandemic healthcare services were reorganized and directed all their efforts to care infected patients5,13. NCDs are a risk factor for COVID-19 severity14, and the course of infection can aggravate pre-existing conditions13. Monitoring NCDs in primary care might have been impaired due to the increased demand and focus directed to COVID patients15. Consequently, the increased utilization of urgency and emergency services for these patients can be explained by the lack of follow-up and further complications related to NCDs16. Only HD was associated with emergency rooms utilization , which is one of the main risk factors for increasing COVID-19 severity17. In addition, COVID-19 has serious implications for the cardiac system which can aggravate pre-existing conditions18 requiring the use of urgency and emergency services.
In Brazil, basic health units are linked to the Unified Health System (known as SUS, for its initials in Portuguese), and offer health care free of charge to the entire population. More than 70% of the Brazilian population depends exclusively on SUS. NCDs patients are one of the priority care lines of this service, being monitored by the basic health units and ensuring a qualified, integral, and longitudinal care19. Considering the characteristics of this health care service, an increased utilization was expected. Regardless of COVID-19, a national survey conducted during the pandemic reported a health care utilization prevalence of 24% among people with NCDs20. This is similar to the prevalence found before the pandemic (25.6%) when compared to those without NCDs7.
The high prevalence of specialized health care utilization was threefold in participants with NCDs when compared to their peers without chronic conditions. People with NCDs are regularly using the healthcare system to manage their diseases, having regular GP appointments or assessing prescribed medication21. However, people with NCDs have a high prevalence of ICU admission and endotracheal intubation, which might exacerbate the disease scenario changing treatment strategies in the long-term, since the inflammatory response of COVID-19 has the potential to provoke an atypical immune system response, consequently affecting several body systems22. Also, in Brazil there is a delay in appointments for specialized services (e.g., cardiologist) in the public health system, and in some cases people choose to pay for these services out of pocket23. Most of our sample is highly educated and at least from the middle class, which might increase their access to specialized services, as well as their NCDs management.
Historically access to specialized care in SUS presents hardships related to the insufficient number of medical doctors and vacancies for appointments, high dependence on the private sector, and budget difficulties leading to fragmentation, disorganization, and discontinuity of services, and especially a repressed demand for specialized services24. The greater difficulty in using health services and consequently the increase in the problem can be explained by the extinction of government health policies such as the Family Health Support Center (NASF), policies to promote higher education in regions of greater social vulnerability, the return to the poverty line and the increased demand for services due to the sequelae of COVID or even the lack of continuity of care in periods of isolation, in addition to the political context experienced in Brazil in recent years19,25.
Translated with DeepL.com (free version)Our results must be interpreted taking into account their limitations and strengths. Firstly, as interviews were conducted after COVID-19 without a specific time frame, memory bias cannot be discarded. Secondly, we only interviewed symptomatic subjects tested with RT PCR. Thus, precluding an evaluation of health care utilization in asymptomatic patients or those diagnosed through serological tests. Thirdly, our study was conducted with data from COVID-19 survivors, and survival bias might be a concern. Finally, as this is a cross-sectional study, caution is needed regard to recall bias, and it is important to note that the data belong to a local population and, therefore, cannot be extrapolated to other regions or cities. However, our study shows unprecedented data regarding health care utilization in patients with NCDs and COVID-19 in southern Brazil with a non-hospital representative sample.
CONCLUSION
Our results showed an association between people with NCDs and increased health care utilization after COVID-19, regardless of their specific disease. Also, one should note that both primary and secondary health care utilization showed higher prevalence among this population. Whilst there was a concern of a healthcare collapse during COVID-19 outbreak in a short- and mid-term, the increased in health care utilization in the long-term for people who had COVID-19, and specifically people with NCDs should be a concern for policy makers and stakeholders.

Finally, this study provides relevant information about the health care service burden for people with NCDs who have contracted SARS-CoV-2. People with NCDs tend to access health care services more frequently compared to healthy individuals, and the infection can intensify this demand. Future studies should focus on the long-term health care service burden, as well as strategies to alleviate the system through new treatments and disease management approaches.

ACKNOWLEDGMENT
The study was carried out with financial support from FAPERGS (Fundação de Amparo á Pesquisa do Rio Grande do Sul, Brazil) Grant No. 21/2551-0000107-0 SUS Research Program: shared health management (PPSUS).

REFERENCES
1. Chang AY, Cullen MR, Harrington RA, Barry M. The impact of novel coronavirus COVID?19 on noncommunicable disease patients and health systems: a review. J Intern Med 2021;289(4):450–62.
2. Shin JH, Takada D, Morishita T, et al. Economic impact of the first wave of the COVID-19 pandemic on acute care hospitals in Japan. PLoS One [Internet] 2020;15(12 December):1–11. Available from: http://dx.doi.org/10.1371/journal.pone.0244852
3. dos Santos RC, Carvalho TA, Souza Neto IF, et al. Urgency and emergency in times of COVID-19 – an integrative literature review. Res Soc Dev 2021;10(3):e9110313027.
4. Barone MTU, Harnik SB, de Luca PV, et al. The impact of COVID-19 on people with diabetes in Brazil. Diabetes Res Clin Pract [Internet] 2020;166:108304. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0168822720305568
5. Organización Panamericana de Salud - Organización Mundial de Salud. Rapid Assessment Report on Noncommunicable Disease Service Delivery during the COVID-19 Pandemic in the Americas. Ops 2020;8.
6. Scheidt-Nave C, Barnes B, Beyer A-K, et al. Care for the chronically ill in Germany - The challenges during the COVID-19 pandemic. J Heal Monit 2021;5(Suppl 10):2–27.
7. Malta DC, Bernal RTI, Lima MG, et al. Noncommunicable diseases and the use of health services: analysis of the National Health Survey in Brazil. Rev Saude Publica 2017;51(suppl 1).
8. BRASIL. Ministry of Health. Public Health Emergency Operations Center. COE COVID-19 Bulletin n. 13 [Internet]. 2020;Available from: https://portalarquivos.saude.gov.br/images/pdf/2020/ April/21/BE13---Boletim-do-COE.pdf
9. Leite JS, Feter N, Caputo EL, Doring IR, Reichet FF, Silva MC, Rombaldi AJ. Managing noncommunicable diseases during the COVID-19 pandemic in Brazil: findings from the PAMPA cohort. Ciência & Saúde Coletiva [online]. v. 26, n. 3 [Accessed 18 December 2023] , pp. 987-1000. Available from: .

10. Kluge HHP, Wickramasinghe K, Rippin HL, et al. Prevention and control of non-communicable diseases in the COVID-19 response. Lancet 2020;395(10238):1678–80.
11. Saes MO, Rocha JQS, Rutz AAM; Silva CN; Camilo LS, Oliveira BC, Ritta MC; Goncalves CS; Vieira YP, Duro SMS. Aspectos metodológicos e resultados da linha de base do monitoramento da saúde de adultos e idosos após infecção pela Covid- 19 (SulCovid-19). Revista Contexto e Saúde, 2023.
12. ABEP. Associação Brasileira de Empresas de Pesquisa. 2021;Available from: www.abep.org
13. Medina MG, Giovanella L, Bousquat A, Mendonça MHM de, Aquino R. Primary health care in times of COVID-19: what to do? Cad Saude Publica [Internet] 2020;36(8). Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0102-311X2020000800502&tlng=pt
14. Yang J, Zheng Y, Gou X, et al. Prevalence of comorbidities and its effects in patients infected with SARS-CoV-2: a systematic review and meta-analysis. Int J Infect Dis [Internet] 2020;94(March):91–5. Available from: https://linkinghub.elsevier.com/retrieve/pii/S1201971220301363
15. Gummidi B, John O, Jha V. Continuum of care for non-communicable diseases during COVID-19 pandemic in rural India: A mixed methods study. J Fam Med Prim Care 2020;9(12):6012.
16. Poveda-Moral S, Bosch-Alcaraz A, Falcó-Pegueroles A. Advance decision planning as a preventive strategy for ethical conflicts in urgencies and emergencies during and after COVID-19. Rev Bioética y Derecho 2020;(50):189–203.
17. Ganatra S, Hammond SP, Nohria A. The Novel Coronavirus Disease (COVID-19) Threat for Patients With Cardiovascular Disease and Cancer. JACC CardioOncology [Internet] 2020;2(2):350–5. Available from: https://doi.org/10.1016/j.jaccao.2020.03.001
18. Liu F, Liu F, Wang L. COVID-19 and cardiovascular diseases. J Mol Cell Biol [Internet] 2021;13(3):161–7. Available from: https://academic.oup.com/jmcb/article/13/3/161/5998653
19. Castro MC, Massuda A, Almeida G, et al. Brazil’s unified health system: the first 30 years and prospects for the future. Lancet [Internet] 2019;394(10195):345–56. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0140673619312437
20. Malta DC, Gomes CS, da Silva AG, et al. Use of health services and adherence to social distancing by adults with noncommunicable diseases during the COVID-19 pandemic, Brazil, 2020. Cienc e Saude Coletiva 2021;26(7):2833–42.
21. Hernandez-Romieu AC, Leung S, Mbanya A, et al. Health Care Utilization and Clinical Characteristics of Nonhospitalized Adults in an Integrated Health Care System 28–180 Days After COVID-19 Diagnosis — Georgia, May 2020–March 2021. MMWR Morb Mortal Wkly Rep [Internet] 2021;70(17):644–50. Available from: http://www.cdc.gov/mmwr/volumes/70/wr/mm7017e3.htm?s_cid=mm7017e3_w
22. Fernández-de-las-Peñas C, Palacios-Ceña D, Gómez-Mayordomo V, et al. Prevalence of post-COVID-19 symptoms in hospitalized and non-hospitalized COVID-19 survivors: A systematic review and meta-analysis. Eur J Intern Med [Internet] 2021;92:55–70. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0953620521002089
23. Paim J, Travassos C, Almeida C, Bahia L, Macinko J. The Brazilian health system: history, advances, and challenges. Lancet [Internet] 2011;377(9779):1778–97. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0140673611600548
24. Silva CR, Carvalho BG, Cordoni Júnior L, Nunes E de FP de A. Difficulty of access to medium-complexity services in small-sized municipalities: a case study. Cien Saude Colet [Internet] 2017;22(4):1109–20. Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1413-81232017002401109&lng=pt&tlng=pt
25. Massuda A. Changes in the financing of Primary Health Care in the Brazilian Health System: progress or regression? Cien Saude Colet [Internet] 2020;25(4):1181–8. Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1413-81232020000401181&tlng=pt