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Salud Pública de México

versión impresa ISSN 0036-3634

Salud pública Méx vol.63 no.3 Cuernavaca may./jul. 2021  Epub 20-Feb-2023

https://doi.org/10.21149/11817 

Artículos originales

On the increasing incidence of SARSCoV-2 in older adolescents and younger adults during the epidemic in Mexico

Sobre la incidencia creciente de SARS-CoV-2 en adolescentes mayores y adultos jóvenes durante la epidemia en México

Dalia Stern, PhD(1) 

Martin Lajous, ScD(2  3) 

Blanca De la Rosa, MPH(4) 

Edward Goldstein, PhD(5) 

(1) Cátedra Conacyt, Centro de Investigación en Salud Poblacional, Instituto Nacional de Salud Pública. Cuernavaca, Morelos, Mexico.

(2) Centro de Investigación en Salud Poblacional, Instituto Nacional de Salud Pública. Cuernavaca, Morelos, Mexico.

(3) Department of Global Health and Population, Harvard T.H. Chan School of Public Health. Boston, United States.

(4) Dirección General de Epidemiología, Dirección de Información Epidemiológica, Secretaría de Salud. Mexico City, Mexico.

(5) Center for Communicable Disease Dynamics, Department of Epidemiology, Harvard T.H. Chan School of Public Health. Boston, United States


Abstract

Objective:

To estimate temporary changes in the incidence of SARS-CoV-2-confirmed hospitalizations (by date of symptom onset) by age group during and after the national lockdown.

Materials and methods:

For each age group g, we computed the proportion E(g) of individuals in that age group among all cases aged 10-59y during the early lockdown period (April 20-May 3, 2020), and the corresponding proportion L(g) during the late lockdown (May 18-31, 2020) and post-lockdown (June 15-28, 2020) periods and computed the prevalence ratio: PR(g)=L(g)/E(g).

Results:

For the late lockdown and post-lockdown periods, the highest PR values were found in age groups 15-19y (late: PR=1.69, 95%CI 1.05,2.72; post-lockdown: PR=2.05, 1.30,3.24) and 20-24y (late: PR=1.43, 1.10,1.86; post-lockdown: PR=1.49, 1.15,1.93). These estimates were higher in individuals 15-24y compared to those ≥30y.

Conclusions:

Adolescents and younger adults had an increased relative incidence of SARS-CoV-2 during late lockdown and post-lockdown periods. The role of these age groups should be considered when implementing future pandemic response efforts.

Keywords: SARS-CoV-2; Mexico; age distribution; incidence; mitigation; lockdown

Resumen

Objetivo:

Estimar los cambios temporales en la incidencia de hospitalizaciones confirmadas por SARS-CoV-2 (por fecha de inicio de los síntomas) por grupo de edad durante y después del cierre nacional.

Material y métodos:

Para cada grupo de edad g, calculamos la proporción E(g) de individuos en ese grupo de edad entre todos los casos de 10 a 59 años durante el periodo de cierre temprano (del 20 de abril al 3 de mayo de 2020) y la proporción correspondiente L(g) durante los periodos de cierre tardío (18-31 de mayo de 2020) y posterior al cierre (15-28 de junio de 2020), y se calculó la razón de prevalencia: RP(g)=L(g)/E(g).

Resultados:

Para los periodos de cierre tardío y posterior al cierre, los valores de RP más altos se dieron en los grupos de edad de 15 a 19 años (tardío: RP=1.69, IC95% 1.05,2.72; después del cierre: RP=2.05, 1.30,3.24) y 20-24 años (tardío: RP=1.43, 1.10,1.86; después del cierre: RP=1.49, 1.15,1.93). Estas estimaciones fueron más altas en personas de 15 a 24 años en comparación con las de ≥ 30 años

Conclusiones:

Los adolescentes y los adultos jóvenes tuvieron una mayor incidencia relativa de SARS-CoV-2 durante los periodos de cierre tardío y posteriores al cierre. El papel de estos grupos de edad en la transmisión de la enfermedad debe tenerse en cuenta al implementar futuros esfuerzos de respuesta a una pandemia.

Palabras clave: SARS-CoV-2; México; distribución por edad; incidencia; mitigación; confinamiento

Introduction

The SARS-CoV-2 epidemic in Mexico is growing, with 1 070 487 cases and 103 597 deaths registered by November 25th, 2020.1 In Mexico, on March 23rd (and until May 30th) a call for a nationwide lockdown was made.2,3 On June 1st, Mexico implemented postlockdown mitigation strategies that, depending on community transmission and hospital capacity, eased some of the initial restrictions.4 In order to understand the transmission of SARS-CoV-2 under different mitigation strategies, it is important to study the role that different age groups have played on propagating the spread of the virus. Variations in transmission of SARS-CoV-2 by age may take place during the course of an epidemic due to changing mixing patterns,5 with subsequent implications for epidemic control.

Evidence has accumulated that susceptibility to SARS-CoV-2 infection increases with age.6,7 Yet, this does not suggest that the oldest groups in a population necessarily play the leading role in the spread of SARS-CoV-2 in the community. Actually, several serological studies suggest that adolescents and younger adults often experience the highest cumulative rates of infection.8,9,10,11,12,13,14,15 In England, the highest rates of SARS-CoV-2 infection during the fall of 2020 occurred in individuals aged 13-17y and 18-24y (figure 8 in reference 16).16 Under the physical distancing measures implemented in Mexico, mixing patterns among individuals of different age groups may be quite different from the regular mixing patterns.5,6 Also, similarly to other low- and middle-income countries, a sizeable proportion of Mexico’s population consists of relatively young informal workers who live from day to day, for whom shelter-in-place policies may represent a significant economic burden. The role that older adolescents, younger adults and other age groups play in propagating the SARS-CoV-2 epidemic in Mexico is unknown. In order to address this issue, we estimated temporary changes in SARS-CoV-2 incidence by age group during and after the national lockdown period. We applied the methodology developed previously17,18,19 to assess the temporal changes in the incidence of different age groups of individuals between the ages of 10 to 59 years during the epidemic in Mexico.

Materials and methods

Data sources

Information on daily hospitalized Covid-19 cases by age group was obtained from the General Directorate of Epidemiology (Dirección General de Epidemiología) of the National Epidemiological Surveillance System (Sisver, by its acronym in spanish) in Mexico. We retrieved data on reported hospitalized cases of PCR-confirmed SARS-CoV-2 infection, along with available information on the date of symptom onset (September 28, 2020). We excluded healthcare workers because of the significant non-community transmission in that population group. We also excluded cases from private hospitals because it is unclear how cases were ascertained and whether case-ascertainment has changed over time. Finally, we excluded non-hospitalized cases because testing for non-severe Covid-19 may have changed over time for different age groups, while the criteria for testing of cases requiring hospitalization for SARS-CoV-2 infection have been consistent over time.

Relative change in SARS-CoV-2 infection by age-group

We included laboratory confirmed hospitalizations in ten 5-year age groups: 10-14 years through 55-59 years. Older adults were not included because of potential temporal changes in ascertainment, as well as presence of some hospitalizations stemming from infections that do not reflect community transmission (e.g., infections in long-term care facilities, with rates of infection in those facilities being quite higher than in the corresponding age groups in the community). We also excluded children under 10 years for two reasons: first, ascertainment of infection in those age groups might have changed with time as more severe episodes in younger children appeared as the epidemic progressed; second, there is evidence of lower susceptibility to infection in children aged under 10 years compared to adults and older adolescents,20 so these children are unlikely to play a significant role in the progression of the epidemic.

We selected three periods: April 20-May 3 (early lockdown period; we selected this date because earlier numbers of cases in certain age groups were limited and may have rendered our estimates unstable), 18-31 May (late lockdown period, the end of the national lockdown) and 15-25 June (post-lockdown period, starting two weeks after the national lockdown, in order to detect changes in symptom onset).

We applied a previously described procedure17,18,19 for estimating the age-specific proportion ratios for late lockdown (May 18-31, 2020) and post-lockdown (June 15-28, 2020) periods, relative to the early lockdown (April 20-May 3, 2020), as follows: let E(g) be the number of hospitalization with confirmed SARS-CoV-2 infection in age group g and h E(h) the total number of cases in age groups h=1 (10-14 years) to h=10 (55-59 years) during early lockdown, and L(g) and hL(h) be the corresponding numbers during late lockdown (and post-lockdown). The proportion ratio (PR) statistic in age group g for the late vs. early lockdown comparison is:

PR(g)=Lg(hL(h)/Eg(hE(h) (1)

That is, the ratio between the proportion of cases in age group g among all cases in the late lockdown period and the proportion of cases in age group g in the early lockdown. The logarithm ln(PR(g)) of the PR(g) is approximately normally distributed21 with the standard error:

SE=lL(g)+lE(g)-lhLh-lhEh (2)

We repeated these calculations after substituting the cases in the late lockdown with the cases in the post-lockdown period.

In order to examine whether the PR in certain age groups is significantly higher than in others, we consider the corresponding pairwise odds ratios (ORs). For each pair of age groups g1 and g2, the proportion ratios PR(g1) and PR(g2) are compared using the odds ratio (OR):

ORg1,g2=PR(g1)PR(g1) (3)

It follows from equation 1 that OR(g1,g2) equals:

OR=L(g1)E(g1)/L(g2)E(g2) (4)

Which is the OR for a hospitalized case of confirmed SARS-CoV-2 infection occurring in age group g1 vs. g2 for the early lockdown period and the late lockdown period. We repeated these calculations for the comparison of early lockdown to post-lockdown. Estimates for pairwise OR were made using Fisher’s exact test.

Results

Table I shows the number of hospitalizations for confirmed SARS-CoV-2 infection in the different age groups (10-14 through 55-59 years) during the early lockdown (April 20-May 3, 2020), the late lockdown (May 18-31, 2020) and the post-lockdown (June 15-28, 2020) periods, as well as the corresponding estimates of the PR statistic (equations 1,2).

Table I: Number of hospitalizations for confirmed SARS-CoV-2 infection by age groups (10-14 through 55-59 years) and by time period, and estimates of the prevalence ratio (PR) statistic (n=23 013). Mexico, 2020 

Age Group, y

Early lockdown period

Late lockdown period

Post-lockdown period

Prevalence Ratio

PR (95%CI)

April 20-26

April 27 - May 3

May 18-24

May 25-31

June 15-21

June 22-28

Late vs. early lockdown period

Post-lockdown vs. early lockdown period

10-14

9

7

13

16

28

21

1.13 (0.62-2.09)

1.66 (0.94-2.91)

15-19

11

12

35

27

45

42

1.69 (1.05-2.72)

2.05 (1.30-3.24)

20-24

34

44

87

91

115

100

1.43 (1.10-1.86)

1.49 (1.15-1.93)

25-29

103

108

195

179

216

199

1.11 (0.94-1.31)

1.07 (0.91-1.25)

30-34

164

186

288

276

347

355

1.01 (0.89-1.15)

1.09 (0.96-1.23)

35-39

251

239

385

430

461

454

1.04 (0.94- 1.16)

1.01 (0.91-1.12)

40-44

330

385

559

555

620

587

0.98 (0.89-1.06)

0.91 (0.84-1.00)

45-49

465

547

741

747

869

878

0.92 (0.86-0.99)

0.93 (0.87-1.00)

50-54

555

581

865

902

1 030

957

0.97 (0.91-1.04)

0.95 (0.89-1.01)

55-59

544

603

915

968

1 114

1 123

1.03 (0.96-1.10)

1.06 (0.99-1.12)

Total

2 466

2 712

4 083

4 191

4 845

4 716

For the late lockdown vs. the early lockdown period, the highest PR (95%CI) estimates correspond to individuals aged 15-19 years (PR=1.69 [1.05,2.72]) and 20-24 years (PR=1.43[1.10,1.86]) (table I). The PR estimates in individuals aged over 30 years were significantly lower compared to individuals aged 15-24 years. Table II gives the estimates of ORs for different pairs of age groups (10-14y through 55-59y) for hospitalized cases of confirmed SARS-CoV-2 infection occurring during the period May 18-31 vs. April 20-May 3 (equation 3, 4). Our results suggest that, for individuals aged 15-24y, the corresponding OR relative to any age group over 30y is above 1 (table II).

Table II: Odds ratios for different pairs of age groups for a hospitalized case of confirmed SARS-CoV-2 infection occurring between the late lockdown (May 18-31) vs. the early lockdown period (April 20-May 3). Mexico, 2020 

15-19

20-24

25-29

30-34

35-39

40-44

45-49

50-54

55-59

10-14

0.67

(0.29-1.58)

0.79

(0.39-1.66)

1.02

(0.52-2.06)

1.12

(0.58-2.25)

1.09

(0.57-2.17)

1.16

(0.61-2.31)

1.23

(0.64-2.44)

1.17

(0.61-2.31)

1.10

(0.58-2.19)

15-19

1.18

(0.67-2.15)

1.52

(0.90-2.65)

1.67

(1.00-2.88)

1.62

(0.97-2.78)

1.73

(1.05-2.95)

1.83

(1.11-3.12)

1.73

(1.05-2.95)

1.64

(1.00-2.79)

20-24

1.29

(0.93-1.79)

1.42

(1.04-1.93)

1.37

(1.02-1.86)

1.46

(1.10-1.97)

1.55

(1.17-2.08)

1.47

(1.11-1.96)

1.39

(1.05-1.86)

25-29

1.10

(0.88-1.37)

1.07

(0.87-1.31)

1.14

(0.93-1.39)

1.21

(1.00-1.46)

1.14

(0.94-1.38)

1.08

(0.89-1.30)

30-34

0.97

(0.81-1.16)

1.03

(0.88-1.22)

1.10

(0.94-1.28)

1.04

(0.89-1.21)

0.98

(0.84-1.14)

35-39

1.07

(0.92-1.24)

1.13

(0.98-1.30)

1.07

(0.93-1.23)

1.01

(0.88-1.16)

40-44

1.06

(0.93-1.20)

1.00

(0.89-1.13)

0.95

(0.84-1.07)

45-49

0.95

(0.85-1.06)

0.90

(0.80-1.00)

50-54

0.95

(0.85-1.05)

Odds ratios (ORs) for different pairs of age groups (10-14y through 55-59y) for hospitalized cases of confirmed SARS-CoV-2 infection in Mexico occurring during the May 18-31 period vs. April 20-May 3 (equation 4).

For the post-lockdown vs. the early lockdown period, the highest PR estimates (95%CI) corresponded to individuals aged 15-19 years (PR=2.05[1.30,3.24]) and 20-24 years (PR=1.49 [1.15,1.93]) (table I). The PR estimates for individuals aged over 30 years were significantly lower than those for individuals aged 15-24 years. Table III shows the estimates of ORs during the post-lockdown period of June 15-28 vs. the lockdown period April 20-May 3. The corresponding OR for individuals aged 15-24y relative to any age group over 30y is significantly above 1 for the post-lockdown period compared to the early lockdown period. This suggests a relative increase in the incidence of SARS-CoV-2 infection in individuals aged 15-24y, compared to those aged 30-59y for the post-lockdown period relative to the early lockdown period.

Table III: Odds ratios for different pairs of age groups for hospitalized cases of confirmed SARS-CoV-2 infection occurring between the post-lockdown (June 15-18) vs. the early lockdown period (April 20-May 3). Mexico, 2020 

15-19

20-24

25-29

30-34

35-39

40-44

45-49

50-54

55-59

10-14

0.81

(0.37-1.80)

1.11

(0.58-2.19)

1.56

(0.85-3.00)

1.53

(0.84-2.92)

1.64

(0.91-3.12)

1.81

(1.00-3.44)

1.77

(0.99-3.36)

1.75

(0.97-3.31)

1.57

(0.87-2.97)

15-19

1.37

(0.79-2.44)

1.92

(1.16-3.28)

1.89

(1.16-3.18)

2.03

(1.25-3.40)

2.24

(1.39-3.75)

2.19

(1.36-3.66)

2.16

(1.34-3.61)

1.94

(1.21-3.24)

20-24

1.40

(1.02-1.93)

1.37

(1.02-1.86)

1.48

(1.11-1.98)

1.63

(1.23-2.18)

1.60

(1.21-2.12)

1.58

(1.20-2.09)

1.41

(1.07-1.87)

25-29

0.98

(0.79-1.22)

1.05

(0.86-1.29)

1.17

(0.96-1.42)

1.14

(0.94-1.37)

1.12

(0.93-1.35)

1.01

(0.84-1.21)

30-34

1.07

(0.90-1.28)

1.19

(1.01-1.40)

1.16

(1.00-1.35)

1.15

(0.99-1.33)

1.03

(0.89-1.19)

35-39

1.11

(0.96-1.28)

1.08

(0.94-1.24)

1.07

(0.93-1.22)

0.96

(0.84-1.09)

40-44

0.98

(0.87-1.11)

0.97

(0.86-1.09)

0.87

(0.77-0.97)

45-49

0.99

(0.89-1.10)

0.89

(0.80-0.98)

50-54

0.90

(0.81-0.99)

Odds ratios (ORs) for different pairs of age groups (10-14y through 55-59y) for hospitalized cases of confirmed SARS-CoV-2 infection in Mexico occurring during the period of June 15-28 vs. April 20-May 3 (equation 4).

Discussion

We applied the previously developed methodology17,18,19 to study changes in the relative incidence of SARSCoV-2 infections in different age groups during national lockdown and post-lockdown in Mexico. Compared with early lockdown, the greatest relative increase in the incidence of infection belongs to persons aged 15-24 years in both the late lockdown and post-lockdown periods. We note that, in England, the highest rates of SARS-CoV-2 infection during the Fall of 2020 are found among individuals aged 18-24y and 13-17y (figure 8 in reference 16),16 consistently with our findings about the epidemiological importance of older adolescents and younger adults during the epidemic.

We hypothesize that there are two potential explanations for the increase in the incidence of SARS-CoV-2 infection in older adolescents and younger adults in Mexico: 1) the need for young informal workers to return to work due to increasing economic burden of physical distancing measures and 2) fatigue from adhering to the physical distancing measures, resulting in less and less adherence. Other explanations, such as changing social responsibilities and increased use of public transportation may also apply, and further work is required to understand those issues in order to better inform future mitigation efforts. A serological evaluation that may confirm our observations is underway.

Our results are consistent with observations carried out in Germany, where, with the same methodology, a higher relative incidence of infection was found in older adolescents and younger adults following the introduction of physical distancing measures.17

In Spain, applying the same methodology that was used in source,17 individuals aged 40-64 years were observed to have a higher relative incidence of infection during the initial lockdown period, when non-essential work was allowed, than in the pre-lockdown period. However, during the later strengthened lockdown, older adolescents and younger adults had an increased relative incidence of SARS-CoV-2 infection.22 Our results, together with these observations, highlight the fact that control measures during a pandemic have differential effectiveness in different age groups.

Our study is not without limitations. However, our study is not without limitations. Our findings may be affected by age-differential changes in case ascertainment, over time, or across regions. However, we restricted the analysis to hospitalized cases, rather than including all confirmed Covid-19 cases in the community, because changes in healthcare seeking behavior (e.g., for ambulatory visits) and changes in testing in the outpatient setting may affect the relation between the incidence of SARS-CoV-2 infection and the rates of detected Covid-19 cases. However, such temporary changes are less likely to occur in hospitalized cases, as uniform guidelines for testing hospitalized cases are applied in Mexico and there is a low likelihood of mild cases resulting in hospitalization during certain time periods. Second, the perception of the potential severity of the disease may have changed over time, and clinicians, even with an existing case definition, may have preferentially tested certain age groups. We explored whether testing for hospitalized patients in all age groups had changed over time and found no evidence for this (figure 1). Third, we used the date of symptom onset to temporally classify cases from an administrative database. Thus, the possibility of error in registration is present; however, this error is probably random and unlikely to affect results. Alternatively, there might be differences across age groups in their recall of the date of onset, yet this seems unlikely. Fourth, it is important to notice that the database from the Ministry of Health is not updated over time. In other words, we do not know whether a case that was originally registered as an ambulatory case was later hospitalized.

Figure 1 Trends in the distribution of SARS-CoV-2 tests (RT-PCR) by age group among hospitalized individuals. Mexico, 2020 

In conclusion, our paper provides evidence for an increased relative incidence of SARS-CoV-2 infection among individuals aged 15-24 years when the lockdown interventions were lifted. Our results suggest that the age structure was an important factor in the effect of lockdown interventions. Multigenerational

household arrangements are common in Mexico. Therefore, efforts aimed at spreading risk awareness in adolescents and young adults and limiting social interactions for members of certain age groups in certain venues may be considered to stem the increase of Covid-19 incidence among the community in Mexico.

Acknowledgements

We thank Rodrigo Huerta for helping with the preliminary data analysis. We also thank Tonatiuh Barrientos and Hector Lamadrid, of Instituto Nacional de Salud Pública, and Ruy-López Ridaura, of the Mexican Ministry of Health, who provided feedback on the results. We also want to thank all the epidemiologists and personnel who compiled and managed the surveillance dataset. Without their work, this manuscript would have not been possible.

Funding

This work was funded by Award Number U54GM088558 from the National Institute of General Medical Sciences (EG)

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Received: July 06, 2020; Accepted: December 11, 2020; Published: May 03, 2021

Corresponding author: Martin Lajous. 7ª Cerrada de Fray Pedro de Gante 50, col. Sección XVI Tlalpan. 14080 Ciudad de México, México. email: mlajous@insp.mx

Declaration of conflict of interests. The authors declare that they have no conflict of interests.

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