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Anexos / Arquivos

The burden of disease attributable to Covid-19 in Maranhão

RC: 148899
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DOI: 10.32749/



PINTO, João Amadeu Lima [1], NUNES, Sheila Elke Araújo [2], BELFORT, Márcia Guelma Santos [3], PEREIRA, Keise Adrielle Santos [4]

PINTO, João Amadeu Lima. et al. The burden of disease attributable to Covid-19 in Maranhão. Revista Científica Multidisciplinar Núcleo do Conhecimento. Year 08, Issue 06, Volume 03, pp. 17-34. June 2023. ISSN: 2448-0959, Access link:, DOI: 10.32749/


The objective of this study was to estimate the burden of morbidity and mortality of Covid-19 in Maranhão over a 24-month period, between the years 2020 and 2022. For this purpose, the data used were obtained from the bulletins of the State Department of Health of Maranhão, the IBGE portal, and the 2019 Global Burden of Disease Study. Using this information (confirmed cases and deaths, life expectancy, and disability weights), the average fatality rate and DALYs for the period were estimated. In the calculation of YLLs, two age distributions were used: 10-year age groups and individual ages. An average fatality rate of 2.58% (3.51% for men and 1.86% for women) and a mortality rate of 0.15% (151.73 deaths per 100,000 inhabitants) were observed. According to IBGE, life expectancy in Maranhão in 2021 was 68 years for men and 76 for women. Based on this, an estimate of 95,206 YLLs and 938.377539 YLDs was obtained, totaling 96,144.377 DALYs for the period or 1,344 DALYs per 100,000 inhabitants. Thus, it can be concluded that these results place Covid-19 at a very high level of morbidity and mortality, surpassing the DALYs recorded for all lower respiratory diseases in Maranhão in 2018 and 2019. These values make studies on the burden of Covid-19 in the region important efforts in understanding the damage caused by this disease.

Keywords: Pandemic, Disease burden, Sars-Cov-2.


The SARS-CoV-2 virus has caused significant loss of life and human health globally since the beginning of 2020, resulting from the ongoing pandemic, named Covid-19. Following its first notification on December 31, 2019, this disease quickly spread worldwide and was declared a pandemic on March 11, 2020, leading to the death of approximately 7.727 million individuals by April 1, 2023, as projected at the beginning of the same year (WHO, 2020; IHME, 2023). Brazil, having reported its first case on February 26, 2020, soon became a major global hotspot for Covid-19, with 363,211 confirmed cases and 22,666 deaths by May 25, 2020 (3 SIMÕES and SILVA et al., 2020).

Maranhão had its first confirmed case on March 20 and the first death by March 29 of the same month. During the first wave of infections (first half of 2020), the state reached 1,396 cases by April 20 and exceeded 30,000 by the end of May, according to data from the State Department of Health of Maranhão (4 SES-MA, 2020). By March 16, 2022, already in the observed third wave of infections, Maranhão had accumulated 420,183 confirmed cases and 10,854 deaths (SES-MA, 2020).

In this context, it is useful to apply a disease burden study to Covid-19. Such studies are systematic efforts to quantify the comparative magnitude of health loss due to diseases, injuries, and risk factors by age, sex, and geography at a specific moment. The units used to measure human health are Years of Life Lost (YLL), Years Lived with Disability (YLD), and Disability-Adjusted Life Years (DALY), the sum of the two previous factors (CAMPOS et al., 2020).

In general, for an appropriate response to epidemiological emergencies, it is necessary to know the costs of the disease to human health, as well as the burden of such disease on healthcare systems and their clinical protocols. Such measures can assist in the management of medical resources, such as preventive materials, beds, and medicines. Furthermore, for Covid-19, the scientific literature emphasizes the importance of diagnosing and treating the disease as well as preventive measures and post-discharge patient surveillance to prevent lasting sequelae. In summary, these efforts contribute to maximizing the number of total recoveries, as well as organizing health actions in the face of similar diseases in the future.

In addition to the diagnostic costs, in the recent past and currently, Covid-19 has been consuming various human and financial resources, making it particularly useful to identify its debilitating potential, an ongoing process. In this context, the aim here is to estimate the burden of Covid-19 for the state of Maranhão, gather epidemiological and demographic information about the disease, and conduct a comparative analysis of the burden of this infection on public health compared to other diseases.



Records of Covid-19 cases between 16/02/2020 and 16/03/2022 were included, including the number of confirmed cases, deaths due to Covid-19, and their age group. The literature search involved general terms: life expectancy in Maranhão, population of Maranhão, convalescence period of Covid-19, infection weights, and Covid-19-related sequelae. Information regarding the progression of the disease in Maranhão was extracted from the available epidemiological bulletins of the State Department of Health of Maranhão (SES-MA). Life expectancies for men and women in the Maranhão population were obtained from IBGE.

The values of the weights for the disease and its sequelae were derived from the 2019 Global Burden of Disease study (GBD 2019), whose weight spreadsheet is available on the Global Health Data Exchange (GHDx) portal of IHME. The variables of interest were input into the calculation model to estimate years of life lost due to mortality and morbidity. In total, the disease prevalence, Years of Life Lost (YLL), and Years Lived with Disability (YLD) were estimated. The sum of these last two values allowed the estimation of Disability-Adjusted Life Years (DALY).


Careful monitoring of Covid-19-related deaths yielded specific values for the number of deaths at each identified age. This monitoring allows for the verification of deaths by specific ages for both men and women. Thus, the calculation of YLLs in this study could account for individual years of life, using the formula below, where “Equação 1 ” it represents the number of deaths for each death at a specific age (“i”) in the analyzed gender (“g”) (for both men and women), “LE” indicates life expectancy for each analyzed gender, and “I” indicates the age in question, measured in years).

Equação 2The presented expression is based on an adaptation of the age group formula used by two authors, Vieira et al., (2021) and Mitra et al., (2020). Both in studies of measurement and analysis, respectively, of YLLs in the context of Covid-19, both following the methodological contributions recommended by WHO. The measurement of YLLs in this study was based on the methodology used for GBD 2010 onwards, thus it does not involve the use of age weights or time discounting.

Life expectancy values were, for practical purposes, approximated to the nearest whole numbers in both calculations.


For the calculation of YLDs, a numerical estimate of the severity of Covid-19 and its short- and long-term symptoms (based on incidence) was necessary. This estimate involves applying disability weights (ranging from 0 to 1), where “0” indicates perfect health and “1” indicates death. In essence, the inclusion of weights involves fractionalization of the years lost to account for the loss of quality of life during the specific period. Therefore, the formula for calculating this value is as follows:

Equação 3

In the formula above, used under different terms by Rommel et al. (2021), the years lost due to disability (YLD) result from a summation of the products obtained by directly multiplying the incident cases  Equação 4  by the average duration of symptoms in years (“D”) and the disability weight for the condition Equação 5regarding the average duration of the symptomatic phase of the disease for each type of manifestation, an average of 14 days was used for mild and moderate cases, 21 days for severe cases, and 32 days for critical cases, with a frequency of 42%, 25%, 27%, 5%, and 1% for asymptomatic, mild, moderate, severe, and critical cases, respectively. These values were extracted from the Covid-19 burden study conducted by Rommel et al. (2021) in Germany, based on data extracted from 1.7 million cases detected throughout 2020. Additionally, the duration values were reinforced based on Ferreira et al. (2022), which determined an average of 15.9 days (or approximately 2 weeks) for the total duration of symptoms in most home cases, as well as the recommendation of a 14-day isolation period issued by the WHO, since the symptomatology of Covid-19 presents a high variability in duration (13 GRENDENE et al., 2021).

As for the long-term effects of Covid-19, a disability weight of 0.006 was determined for cases of post-acute sequelae. This value corresponds to the weight assigned to mild infections, as the symptoms observed in long Covid-19 are similar in terms of severity (MORENO-PÉREZ et al., 2021). The average duration of the post-acute syndrome varies widely, with several studies reporting between 3 to 24 weeks after the acute phase, with an incidence between 4.7% to 80% (CABRERA MARTIMBIANCO et al., 2021). In our study, an average duration of 12 weeks was assumed, with a frequency of 50% of affected cases, values that approximate those used by Petersen et al. (2021) and Moreno-Pérez (2021) in Denmark and Spain, respectively. A more accurate determination of the nature of the post-acute phase should be an immediate objective of future studies analyzing the clinical and symptomatic characteristics of Covid-19.


This research, involving consultation of publicly available secondary databases where identification of any subjects is not possible, is exempt from submission to the Research Ethics Committee.


According to the epidemiological bulletin of March 16, 2022, from the State Department of Health of Maranhão, there were 420,183 confirmed cases of Covid-19 in the state since the beginning of the count (03/16/2020). During this same period, 10,854 deaths due to the disease were recorded in a territory with 7,153,262 inhabitants (IBGE, 2021). Furthermore, an average fatality rate of 2.58% (3.52% for men and 1.86% for women) and an average mortality rate of 0.152% (151.73 deaths per 100,000 inhabitants) were recorded in the same interval.

The calculation of YLLs resulted in a total of 95,206 years of life lost for all age groups considered, summing the totals for men and women (with an average of 1,236.441 per specific year) (Table 1 and Graph 1).

Table 1 – YLLs by specific age in men and women in Maranhão between 3/2020 and 3/2022

Ages Male Deaths Female Deaths Male YLLs Female YLLs Total YLLs
      >1 11 8 748 608 1356
1 4 6 268 450 718
2 1 1 66 74 140
3 1 2 65 146 211
4 0 2 0 144 144
5 1 0 63 0 63
6 3 0 186 0 186
7 0 1 0 69 69
8 2 0 120 0 120
9 0 1 0 67 67
10 1 0 58 0 58
11 1 0 57 0 57
12 1 1 56 64 120
13 3 1 165 63 228
14 2 0 108 0 108
15 4 3 212 183 395
16 1 2 52 120 172
17 3 2 153 118 271
18 3 0 150 0 150
19 6 5 294 285 579
20 1 7 48 392 440
21 10 5 470 275 745
22 7 3 322 162 484
23 9 3 405 159 564
24 6 6 264 312 576
25 7 4 301 204 505
26 11 9 462 450 912
27 16 8 656 392 1048
28 11 7 440 336 776
29 12 14 468 658 1126
30 15 12 570 552 1122
31 17 12 629 540 1169
32 27 10 972 440 1412
33 27 12 945 516 1461
34 29 18 986 756 1742
35 33 18 1089 738 1827
36 45 24 1440 960 2400
37 37 24 1147 936 2083
38 53 21 1590 798 2388
39 52 27 1508 999 2507
40 53 39 1484 1404 2888
41 53 25 1431 875 2306
42 47 29 1222 986 2208
43 49 21 1225 693 1918
44 58 33 1392 1056 2448
45 48 24 1104 744 1848
46 49 42 1078 1260 2338
47 46 34 966 986 1952
48 66 31 1320 868 2188
49 75 45 1425 1215 2640
50 70 49 1260 1274 2534
51 81 37 1377 925 2302
52 74 55 1184 1320 2504
53 81 51 1215 1173 2388
54 84 59 1176 1298 2474
55 88 55 1144 1155 2299
56 96 62 1152 1240 2392
57 102 73 1122 1387 2509
58 102 75 1020 1350 2370
59 128 64 1152 1088 2240
60 122 72 976 1152 2128
61 107 86 749 1290 2039
62 124 94 744 1316 2060
63 143 88 715 1144 1859
64 125 98 500 1176 1676
65 151 98 453 1078 1531
66 150 108 300 1080 1380
67 150 116 150 1044 1194
68 156 113 0 904 904
69 177 123 0 861 861
70 174 107 0 642 642
71 161 118 0 590 590
72 164 100 0 400 400
73 194 118 0 354 354
74 148 104 0 208 208
75 159 135 0 135 135
76 118 119 0 0 0

Source: Authors, 2023.

Graph 1 – Comparison of YLLs by specific age and by gender, due to Covid-19 in the State of Maranhão, from 2020 to 2022

Comparativo dos YLLs por idade específica e por sexo, em decorrência da Covid-19 no Estado do Maranhão, no período de 2020 a 2022
Source: Authors, 2023.

Table 2 shows the preliminary values used and the total amount of Years Lived with Disability – YLDs.

Table 2 – YLDs Estimate due to Covid-19 in Maranhão from 2020 to 2022

Severity Frequency Weight Duration (in years) YLDs
Asymptomatic 42% 0.000 0.03833 0,00
Mild 25% 0.006 0.03833 24,158421
Moderate 27% 0.051 0.03833 221,77431
Severe 5% 0.133 0.05749 160,639532
Critical 1% 0.655 0.08761 241,120124
Post-Acute Syndrome (Long Covid) 50% 0.006 0.23061 290,695205
Total 100% ** ** 938,377539

Source: Authors, 2023.

In Maranhão during the study period, the number of YLLs was 95,206, YLDs were 938.377, and DALYs* were 96,144.377 (The value of Disability-Adjusted Life Years – DALYs, is equivalent to the simple arithmetic sum of YLLs and YLDs).


This study aimed to provide an initial estimate of the disease burden of Covid-19 in Maranhão for a broad period of 2 years. To do so, epidemiological and demographic data from the state were aggregated, a comparison was made between the morbidity and mortality of Covid-19 and other diseases, and the current state of research on the global burden of diseases at the national level was assessed.

The average YLLs per 10-year age group was 11,900.75 (with 1,236.44 being the average for each individual year). Additionally, the average years lost for each of the 6,130 deaths considered was 15,531.1. This result is similar to the average of 16 years obtained by Pifaré I Arolas et al. (2021) in a compilation of 81 studies seeking a universal sum of YLLs due to Covid-19 in 2020 and is significantly higher than the 9.6 YLLs per death obtained by Rommel et al. (2021).

The age group with the highest YLLs was 50 to 59 years, with 24,230 YLLs in the period (sum of individual years), followed by the age groups 40 to 49 years (22,801 YLLs), 60 to 69 years (18,477 YLLs), and 30 to 39 years (15,118 YLLs). These results partially reflect international estimates that classify the 50 to 70 age group as the largest contributors to the total YLLs, accounting for approximately 44.85% of representation (PIFARÉ I AROLAS et al., 2021). The age strata with the lowest number of YLLs were 10 to 19 (1,596 YLLs), 0 to 9 years (3,074 YLLs), and 20 to 29 years (6,003 YLLs).

The age group with the lowest number of years of life lost per confirmed case was 10 to 19 years (also with the lowest number of deaths), with 0.0506 YLLs per case, while the ages with the highest number were between 60 and 69 years, with 0.5820 YLLs per case.

In the calculation of individual years, it was observed that the specific age most affected was 42 years, with 2,888 YLLs added per 92 registered deaths. It is suggested that such variations in years may be related to the conjunction of random events of contagion in populations of certain ages and the balance between their vulnerability to severe clinical manifestations of Covid-19 and the high number of years of life remaining in the face of average life expectancy. Studies that have explored Covid-19 burden elements by individual years have not been located at this time, so comparisons at this level cannot be made.

Regarding mortality by gender, a total of 46,569 YLLs were observed in men and 48,637 YLLs in women. However, the average years lost per specific age were 674.913 and 631.649 in men and women, respectively. These two comparisons express the higher number of YLLs in women due to their higher life expectancy and the higher average of YLLs in men due to their greater vulnerability to the lethal manifestations of the disease, producing higher lethality.

The population of Maranhão is estimated at 7.15 million in 2021 (IBGE), which yields an average of 0.01331 YLLs per person (or 4.86 days lost), or 1,331 YLLs for every 100,000 inhabitants of the state. This value is considerably below that of other socioeconomically similar regions, such as the 1,998 YLLs per 100,000 inhabitants in Malaysia, according to another study covering 2 years of the pandemic (TAN et al., 2022). It also falls below the DALYs measured in severely affected regions at the beginning of the pandemic and with a high proportion of elderly people in the population, such as Italy, which obtained an average of 2010 DALYs per 100,000 inhabitants (NURCHIS et al., 2020).

Regarding the averages of DALYs, 0.01344 per person (4.91 days lost) or 13.44 DALYs for every 100,000 inhabitants were obtained. As for the YLDs, the values were 0.0001311 per person (1.14 hours lost) or 13.11 YLDs for every 100,000 inhabitants. The total YLDs obtained constitute 0.0976% of the total DALYs

(99.9024% YLLs), and 69% (647.69238 YLDs) are represented by the acute phase of Covid-19, within which critical manifestations of the disease were the largest contributors, with 241.1201 YLDs, followed by moderate (221.7743 YLDs) and severe (160.6395 YLDs) phases, respectively. The largest individual contributor to the disability component was the post-acute phase, with 290.695205 YLDs in the period (cases that exceeded the end date were considered, provided they originated within the period of interest).

Similar proportions between YLLs and YLDs in this context are seen in various studies, such as Tan et al. (2022), with 99.5% YLLs, and Jo et al. (2020), with 98.2%, respectively. It is worth mentioning that, with the differences in lethality by age group, such proportions vary according to age, as evidenced by Jo et al. (2020) in a study in South Korea at the beginning of the pandemic, in which a variation of 1.8% was observed between YLLs and YLDs between ages 0 and 30 years, and those ages above 80 years (high regional life expectancy).


For a better understanding of the burden of this disease on public health, the final result was compared to the DALYs per 100,000 inhabitants related to the seven major general causes of morbidity and mortality in Maranhão in 2018 and 2019 (according to GBD 2019 data). These causes were: Ischemic heart diseases, type 2 diabetes mellitus, physical violence by firearms, lower respiratory infections, complications from premature birth, neonatal encephalopathies due to trauma or asphyxia, lower back pain, and anxiety disorders (IHME, 2019).

Figure 6 – DALYs resulting from the major aggregated causes of morbidity and mortality in Maranhão between 2018 and 2019, and Covid-19 from 3/2020 to 3/2022

DALYs resultantes das maiores causas agregadas de morbimortalidade no Maranhão entre 2018 e 2019, e a Covid-19 no período de 32020 a 32022
Source: Author’s elaboration.

It is possible to observe that Covid-19, from March 2020 to March 2022, ranks ninth among the major causes of morbidity and mortality in the state (ICD-10 elements) for the years 2018 and 2019. It is also noted that Covid-19 accounted for 67.07% of the total DALYs per population share compared to the aggregate of lower respiratory infections from the two years preceding the pandemic.

Furthermore, Covid-19 as a communicable disease (lower respiratory tract) surpassed all seven communicable diseases with the highest morbidity and mortality in Maranhão in 2018 and 2019 in terms of DALYs per 100,000 inhabitants. These are, by etiology: Pneumococcus, Influenza, Respiratory Syncytial Virus, Shigella, Rotavirus, Entamoeba, and Norovirus. These data also stem from GBD Compare for 2018 and 2019 (IHME, 2019).

Figure 7 – Comparison between the morbidity and mortality of the most influential communicable diseases in Maranhão between 2018 and 2019, and Covid-19 (by etiological agent), from 3/2020 to 3/2022

Comparativo entre a morbimortalidade das mais influentes doenças comunicáveis no Maranhão entre 2018 e 2019, e da Covid-19 (por agente etiológico), entre 32020 e 32022
Source: Author’s elaboration.

It is observed that Covid-19 obtained 8.44% more DALYs per 100,000 inhabitants than pneumococcal diseases (etiologic agent Streptococcus pneumoniae or Pneumococcus) and 345.25% more DALYs per 100,000 inhabitants than influenza infections (etiologic agent Influenza viruses). Thus, the Sars-Cov-2 virus and its various variants of concern stand out for their high capacity to inflict damage on public health. It is worth noting that during the course of the Covid-19 pandemic, infection mitigation strategies such as hygiene and social distancing led to a global reduction in the transmissibility of various communicable diseases, which may result in a more pronounced discrepancy in morbidity and mortality between the years 2020 and 2022 (KITANO, 2021).


Currently, there are few studies measuring the burden of Covid-19 on the general population over long periods of time. Studies in the Brazilian context mostly pertain to the early stages of the pandemic, such as Silva et al. (2021), used as methodological reference for this work, which observed 498.1 DALYs (216.02 DALYs per 100,000 inhabitants) among nursing professionals in Brazil from March 20 to May 5, 2020. Other national studies on this topic are primarily literature reviews and discussion articles, like Campos et al. (2020), which proposes the use of Covid-19 disease burden studies to aid health actions during the pandemic.

No disease burden studies of Covid-19 in Maranhão were found. The available publications focus on epidemiological characterization in the state or municipalities, such as Dos Santos Almeida et al. (2020), which identified a rapid increase in confirmed cases between March and April 2020. Therefore, this work is the first study on the disease burden of Covid-19 to be conducted in Maranhão and the region, and is among the first at the national level.

The perspective of studying Covid-19 and its sequelae as a risk factor for future diseases, as well as the psychological burden during the pandemic, is difficult to ascertain at this time. This perspective can be observed in certain national studies such as Ferreira da Mata et al. (2021) and Pereira et al. (2021), in literature reviews that highlighted significant impacts of the pandemic on the mental health of young individuals and healthcare professionals, respectively.

The scarcity of Covid-19 disease burden studies (especially in Brazil) posed certain challenges in conducting this project. Notably, the weights used here for calculating YLDs are based on methodological foundations from the last decade and the body of research on this topic since the beginning of the pandemic. Therefore, several assumptions about the behavior of the disease on a large scale had to be made, such as the use of disability weights related to lower respiratory diseases from the latest editions of the GBD for a disease that, in many cases, has a systemic reach. These uncertainties are shared with all available literature at the moment, making the determination of the exact nature of Covid-19 and the magnitude of its long-term sequelae a topic of fundamental importance for future studies in the field.


The observed data attest, in fine detail, to the extremely high clinical significance of Covid-19 for public health in Maranhão during the analyzed period, being the second major general cause of morbidity and mortality, and the most influential communicable disease in the state within the 2020s. Inside and outside the context of the Covid-19 pandemic that shook the world in recent years, the impact of this disease will have long-term repercussions, as its wide range of direct and indirect sequelae will continue to affect the public to some extent, even after the control of the disease and its variants, necessitating proper healthcare preparedness.

It is hoped that this work contributes to the expansion of the available knowledge base regarding the impact of Covid-19 and the behavior of the Sars-Cov-2 virus on a large scale in the state of Maranhão and similar regions. Information useful in the design of future disease burden studies, as well as other epidemiological monitoring actions involving the history of the disease in the North and Northeast regions of Brazil during the early 2020s, was consolidated here.


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[1] Bachelor of Biological Sciences (UEMASUL). ORCID: 0000-0002-5524-4892. Currículo Lattes:

[2] Advisor. ORCID: 0000-0002-2309-7314.

[3] Co-advisor. ORCID: 0000-0003-3131-2237.

[4] Co-advisor. ORCID: 0000-0002-1209-250X.

Submitted: May 16, 2023.

Approved: May 17, 2023.

5/5 - (10 votes)
João Amadeu Lima Pinto

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