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Elsevier - PMC COVID-19 Collection logoLink to Elsevier - PMC COVID-19 Collection
. 2020 Jun 12;14(4):375–379. doi: 10.1016/j.orcp.2020.06.001

Obesity is the comorbidity more strongly associated for Covid-19 in Mexico. A case-control study

Eduardo Hernández-Garduño 1,
PMCID: PMC7290168  PMID: 32536475

Abstract

Some comorbidities are associated with severe coronavirus disease (Covid-19) but it is unclear whether some increase susceptibility to Covid-19. In this case-control Mexican study we found that obesity represents the strongest predictor for Covid-19 followed by diabetes and hypertension in both sexes and chronic renal failure in females only. Active smoking was associated with decreased odds of Covid-19. These findings indicate that these comorbidities are not only associated with severity of disease but also predispose for getting Covid-19. Future research is needed to establish the mechanisms involved in each comorbidity and the apparent “protective” effect of cigarette smoking.

Keywords: COVID-19, SARS-CoV-2, Obesity, Risk factor, Comorbidities, Pandemic

Introduction

Early reports have identified obesity among other comorbidities such as diabetes, hypertension, coronary artery disease, and heart failure, as risk factors associated with severe outcomes in hospitalized patients with Covid-19 [[1], [2], [3], [4]]. However, only one cross sectional study so far has determined risk factors for Covid-19 in the general population and found obesity and chronic kidney disease (CKD) to be predictors with no statistically significant association for other chronic conditions [5]. This study included patients with two or more comorbidities which may have underestimated the strength of association between obesity and CKD with Covid-19 because the correlation of comorbidities, for example diabetes with obesity, or with hypertension, and the assumption of little or no multicollinearity in the multivariable logistic regression analysis would not be met which may explain why other chronic conditions were not associated with Covid-19 in that study. In this study we determined comorbidities associated with increased risk for Covid-19 in a population based-study of Mexicans reporting one comorbidity as of May 15, 2020. The present study updates a previous study (Unpublished results as of May 7, 2020) with a bigger sample size of patients.

Methods

This study used the publicly available Covid-19 data base of the Mexican Ministry of Health through the “Dirección General de Epidemiología” website [6] from which information was obtained of all patients assessed for Covid-19 as of May 15, of 2020. Variables in the data base include non-nominal ID (randomly assigned), age, gender, current smoker, history of contact with Covid-19, type of patient: ambulatory vs hospitalized and whether or not the patient was hospitalized in the intensive care unit (ICU) or had been intubated (tracheal intubation for mechanical ventilation). Information also included answers “yes, no, unknown” or no answer when questioned about the presence/absence of the following conditions and comorbidities: pregnancy in women, diabetes, hypertension, cardiovascular disease, chronic obstructive pulmonary disease (COPD), asthma, obesity, chronic renal failure (CRF) and immunosuppression conditions without specification of each. The presence of pneumonia was also recorded but was considered part of the clinical picture of Covid-19 rather than comorbidity. Only patients who answered “yes or no” to all the above questions were included in the analysis. Patients who did not respond or with missing information were excluded. Some patients presented with multiple comorbidities that may be correlated, for example diabetes and obesity, and the assumption of little or no multicollinearity of logistic regression analysis would not be met. To separate the effect of two or more comorbidities and determine the independent effect of each on Covid-19, the analysis was limited to patients reporting only one comorbidity. Laboratory test results of Covid-19 PCR test were reported as “positive for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)”, “negative for SARS-CoV-2” or “pending result”. Cases were defined as those with a positive test regardless of symptoms according to World Health Organization case definition [7]. Controls were those with negative test.

In univariable analysis, proportions for categorical variables were compared using the χ2 test. Median age of both groups was compared with the Mann–Whitney U test. To determine comorbidities associated with Covid-19, odds ratios (OR) and 95% confidence intervals were estimated using multivariable logistic regression with the backward elimination procedure. Indicator variables for each comorbidity were included in the model with absence of each as the reference group. Statistical analyses were performed using SAS (Statistical Analysis System, Cary, NC, USA) version 9.4 software.

Results

A total 32,583 patients (12,304 cases and 20,279 controls) were identified with one comorbidity.

Cases were older than controls, median age in years (interquartile range) of 48 (38–59) vs 42 (32–54) respectively, and more likely to be: males (58.7 vs 47% females) and hospitalized (45 vs 23% ambulatory) or to have had pneumonia (34.3 vs 15.2%) diabetes (21.1 vs 13.3%), hypertension (23.5 vs 21.3%), obesity (38.4 vs 32.4%) admitted to the ICU (10.4 vs 8.2%) intubated (10.5 vs 6.5%) respectively. Cases were also more likely to have died (12.2 vs 2.7%) respectively. Univariable analysis showed controls more likely to have had a history of: contact with Covid-19, current smoking, cardiovascular, COPD, asthma or immunosuppressed conditions, all p-values<0.0001, Table 1 . After controlling by variables associated with Covid-19 in univariate analysis, the following comorbidities remained statistically significant in the multivariable analysis by sex: obesity (females-aOR = 5.55, males-aOR = 4.72), diabetes (females-aOR = 3.91, males-aOR = 3.50), hypertension (females-aOR = 3.25, males-aOR = 2.70) and chronic renal failure (females-aOR = 2.25). Active smoking was associated with decreased odds of Covid-19 (females-aOR = 0.49, males-aOR = 0.64) as was the group of immunosuppressed conditions in males (aOR = 0.50), Table 2, Table 3 .

Table 1.

Characteristics of cases and controls of the whole sample as of May 15, 2020. Univariate and multivariate logistic regression analyses for increasing risk of Covid-19.

Cases SARS-CoV-2 positive
Controls SARS-CoV-2 Negative
Total
uOR (95% CI)a pb aOR (95% CI)c p
n = 12,304 % n = 20,279 % n = 32,583 %
Males 7221 58.7 9510 46.9 16,731 51.3 1.6 (1.5–1.7) <.0001 1.48 (1.31–1.68) <.0001
Females 5083 41.3 10,769 53.1 15,852 48.7



Median age (IQR) in years, range 48 (38–59), 0–113 42 (32–54), 0–102 45 (34–56), 0–113 <.0001



Age group (years)
0–29 1092 8.9 3885 19.2 4977 15.3 1 1
30–52 6492 52.8 10,894 53.7 17,386 53.4 1.25 (1.22–1.27) <.0001 2.49 (1.97–3.15) <.0001
53 + 4720 38.4 5500 27.1 10,220 31.4 1.45 (1.42–1.48) <.0001 2.59 (2.04–3.28) <.0001



Hospitalized 5539 45.0 4636 22.9 10,175 31.2 2.76 (2.63–2.9) <.0001 1.48 (1.31–1.68) <.0001
Outpatient 6765 55.0 15,643 77.1 22,408 68.8 1 1



Contact with COVID-19
Yes 3141 43.3 6491 49.3 9632 47.2 0.79 (0.74–0.83) <.0001 1.29 (1.11–1.5) 0.0008
No 4109 56.7 6666 50.7 10,775 52.8 1 1



Smoking history
Yes 1191 9.7 2399 11.8 3590 11.0 0.8 (0.74–0.86) <.0001 0.63 (0.51–0.77) <.0001
No 11,083 90.3 17,861 88.2 28,944 89.0 1 1



Pneumonia 4219 34.3 3090 15.2 7309 22.4 2.9 (2.8–3.1) <.0001 1.46 (1.27–1.67) <.0001
No-pneumonia 8084 65.7 17,187 84.8 25,271 77.6 1 1



Obesity 4717 38.4 6560 32.4 11,277 34.7 1.31 (1.25–1.37) <.0001 6.92 (5.54–8.65) <.0001
Non-obesity 7552 61.6 13,706 67.6 21,258 65.3 1 1



Diabetes 2596 21.1 2701 13.3 5297 16.3 1.74 (1.64–1.85) <.0001 5.02 (4.02–6.25) <.0001
No-diabetes 9680 78.9 17,549 86.7 27,229 83.7 1 1



Hypertension 2887 23.5 4306 21.3 7193 22.1 1.14 (1.08–1.2) <.0001 3.99 (3.17–5.01) <.0001
No-hypertension 9389 76.5 15,953 78.7 25,342 77.9 1 1



Cardiovascular disease 212 1.7 583 2.9 795 2.4 0.59 (0.51–0.7) <.0001 1.8 (1.21–2.69) 0.0039
No-cardiovascular diseas 12,061 98.3 19,672 97.1 31,733 97.6 1 1



COPD 194 1.6 491 2.4 685 2.1 0.65 (0.55–0.76) <.0001 NS
No-COPD 12,081 98.4 19,767 97.6 31,848 97.9 1



Asthma 623 5.1 2439 12.0 3062 9.4 0.39 (0.36–0.43) <.0001 1.73 (1.2–2.49) 0.0036
Non-asthma 11,647 94.9 17,823 88.0 29,470 90.6 1 1



Immunosuppression 213 1.7 777 3.8 990 3.0 0.44 (0.38–0.52) <.0001 NS
Non-inmmunesuppression 12,057 98.3 19,471 96.2 31,528 97.0 1



Chronic renal failure 167 1.4 309 1.5 476 1.5 0.89 (0.74–1.08) 0.23 2.66 (1.73–4.11) <.0001
No-chronic renal failure 12,103 98.6 19,954 98.5 32,057 98.5 1 1



Pregnant 63 1.2 174 1.6 237 1.5 0.76 (0.57–1.02) 0.07 NI
No-pregnant 5005 98.8 10,567 98.4 15,572 98.5 1



Tracheally intubated 580 10.5 301 6.5 881 8.7 1.68 (1.46–1.95) <.0001 NS
Non-intubated 4956 89.5 4327 93.5 9283 91.3 1



In ICU 575 10.4 381 8.2 956 9.4 1.29 (1.13–1.48) 0.0002 NS
Non-ICU 4960 89.6 4247 91.8 9207 90.6 1



Death 1502 12.2 544 2.7 2046 6.3 5.0 (4.56–5.58) <.0001 2.52 (2.12–3) <.0001
Alive 10,802 87.8 19,735 97.3 30,537 93.7 1 1

SARS-CoV-2: Severe acute respiratory syndrome coronavirus 2; IQR: interquartile range; COPD: chronic obstructive pulmonary disease; ICU: intensive care unit; NS: not selected by the backward elimination procedure in the multivariable logistic regression analysis with a significance level set at 0.2; NI: not included in the multivariate analysis; Covid-19: coronavirus disease.

a

Unadjusted odds ratio and 95% confidence interval.

b

Differences between cases and controls. Totals may not add up due to missing data.

c

Adjusted odds ratio and 95% confidence interval.

Table 2.

Characteristics of females as of May 15, 2020. Univariate and multivariate logistic regression analyses for increasing risk of Covid-19.

Cases SARS-CoV-2 positive
Controls SARS-CoV-2 Negative
Total
uOR (95% CI)a pb aOR (95% CI)c p
n = 5083 % n = 10,769 % n = 15,852 %
Median age (IQR) in years, range 48 (37–58), 0–113 42 (32–52), 0–102 44 (34–54), 0–113 <.0001



Age group (years)
0-29 519 10.2 2077 19.3 2596 16.4 1 1
30-52 2720 53.5 6008 55.8 8728 55.1 1.16 (1.13–1.19) <.0001 2.05 (1.46–2.89) <.0001
53 + 1844 36.3 2684 24.9 4528 28.6 1.34 (1.30–1.39) <.0001 2.55 (1.80–3.58) <.0001
Hospitalized 1883 37.0 2050 19.0 3933 24.8 2.50 (2.32–2.69) <.0001 NS
Outpatient 3200 63.0 8719 81.0 11,919 75.2 1



Contact with COVID-19
Yes 1465 49.4 3483 50.2 4948 50.0 0.96 (0.88–1.05) 0.45 1.42 (1.13–1.8) 0.0025
No 1500 50.6 3452 49.8 4952 50.0 1 1



Smoking history
Yes 289 5.7 891 8.3 1180 7.5 0.68 (0.58–0.76) <.0001 0.49 (0.31–0.78) <.0023
No 4788 94.3 9868 91.7 14,656 92.5 1 1



Pneumonia 1414 27.8 1292 12.0 2706 17.1 2.82 (2.59–3.07) <.0001 1.56 (1.25–1.93) <.0001
No-pneumonia 3668 72.2 9476 88.0 13,144 82.9 1 1



Obesity 1967 38.8 3582 33.3 5549 35.0 1.26 (1.18–1.36) <.0001 5.55 (4.09–7.51) <.0001
Non-obesity 3107 61.2 7181 66.7 10,288 65.0 1 1



Diabetes 914 18.0 1309 12.2 2223 14.0 1.58 (1.44–1.73) <.0001 3.91 (2.98–5.29) <.0001
No-diabetes 4161 82.0 9446 87.8 13,607 86.0 1 1



Hypertension 1158 22.8 2099 19.5 3257 20.6 1.21 (1.12–1.32) <.0001 3.25 (3.36–4.48) <.0001
No-hypertension 3920 77.2 8660 80.5 12,580 79.4 1 1



Cardiovascular disease 78 1.5 280 2.6 358 2.3 0.58 (0.45–0.75) <.0001 NS
No-cardiovascular diseas 4999 98.5 10,476 97.4 15,475 97.7 1



COPD 68 1.3 222 2.1 290 1.8 0.64 (0.49–0.84) 0.0015 NS
No-COPD 5009 98.7 10,536 97.9 15,545 98.2 1



Asthma 350 6.9 1488 13.8 1838 11.6 0.46 (0.40–0.52) <.0001 NS
Non-asthma 4725 93.1 9276 86.2 14,001 88.4 1



Immunosuppression 95 1.9 402 3.7 497 3.1 0.49 (0.39–0.61) <.0001 NS
Non-inmmunesuppression 4977 98.1 10,353 96.3 15,330 96.9 1



Chronic renal failure 64 1.3 136 1.3 200 1.3 0.99 (0.74–1.34) 0.99 2.25 (1.69–3.01) 0.0011
No-chronic renal failure 5010 98.7 10,626 98.7 15,636 98.7 1 1



Pregnant 63 1.2 174 1.6 237 1.5 0.76 (0.57–1.02) 0.07 -NS
No-pregnant 5005 98.8 10,567 98.4 15,572 98.5 1



Tracheally intubated 151 8.0 133 6.5 284 7.2 1.25 (0.98–1.59) 0.06 NS
Non-intubated 1731 92.0 1912 93.5 3643 92.8 1



In ICU 176 9.4 155 7.6 331 8.4 1.25 (1.0–1.57) 0.04 NS
Non-ICU 1705 90.6 1890 92.4 3595 91.6 1



Death 424 8.3 220 2.0 644 4.1 4.3 (3.69–5.15) <.0001 2.25 (1.69–3.01) <.0001
Alive 4659 91.7 10,549 98.0 15,208 95.9 1 1

SARS-CoV-2: Severe acute respiratory syndrome coronavirus 2; IQR: interquartile range; COPD: chronic obstructive pulmonary disease; ICU: intensive care unit; NS: not selected by the backward elimination procedure in the multivariable logistic regression analysis with a significance level set at 0.2; NI: not included in the multivariate analysis; Covid-19:coronavirus disease.

a

Unadjusted odds ratio and 95% confidence interval.

b

Differences between cases and controls. Totals may not add up due to missing data.

c

Adjusted odds ratio and 95% confidence interval.

Table 3.

Characteristics of males as of May 15, 2020. Univariate and multivariate logistic regression analyses for increasing risk of Covid-19.

Cases SARS-CoV-2 positive
Controls SARS-CoV-2 Negative
Total
uOR (95% CI)a pb aOR (95% CI) c p
n = 7221 % n = 9510 % n = 16,731 %
Median age (IQR) in years, range 49 (39–59), 0–103 43 (32–55), 0–99 46 (34–57), 0–103 <.0001



Age group (years)
0-29 573 7.9 1808 19.0 2381 14.2 1 1
30-52 3772 52.2 4886 51.4 8658 51.7 1.34 (1.30–1.38) <.0001 2.87 (2.07–3.98) <.0001
53 + 2876 39.8 2816 29.6 5692 34.0 1.53 (1.48–1.58) <.0001 2.59 (1.87–3.60) <.0001



hospitalized 3656 50.6 2586 27.2 6242 37.3 2.74 (2.57–2.92) <.0001 NS
outpatient 3565 49.4 6924 72.8 10,489 62.7 1



Contact with COVID-19
Yes 1676 39.1 3008 48.3 4684 44.6 0.68 (0.63–0.74) <.0001 1.21 (1.00–1.47) 0.0466
No 2609 60.9 3214 51.7 5823 55.4 1 1



Smoking history
Yes 902 12.5 1508 15.9 2410 14.4 0.75 (0.69–0.83) <.0001 0.64 (0.51–0.81) 0.0002
No 6295 87.5 7993 84.1 14,288 85.6 1 1



Pneumonia 2805 38.8 1798 18.9 4603 27.5 2.72 (2.54-2.92) <.0001 1.37 (1.15–1.64) 0.0004
no-pneumonia 4416 61.2 7711 81.1 12,127 72.5 1 1



Obesity 2750 38.2 2978 31.3 5728 34.3 1.35 (1.27–1.44) <.0001 4.72 (3.69–6.04) <.0001
non-obesity 4445 61.8 6525 68.7 10,970 65.7 1 1



Diabetes 1682 23.4 1392 14.7 3074 18.4 1.77 (1.64–1.91) <.0001 3.50 (2.74–4.46) <.0001
no-diabetes 5519 76.6 8103 85.3 13,622 81.6 1 1



Hypertension 1729 24.0 2207 23.2 3936 23.6 1.04 (0.97–1.12) 0.23 2.70 (2.09–3.48) <.0001
no-hypertension 5469 76.0 7293 76.8 12,762 76.4 1 1



Cardiovascular disease 134 1.9 303 3.2 437 2.6 0.57 (0.46–0.70) <.0001 NS
no-cardiovascular diseas 7062 98.1 9196 96.8 16,258 97.4 1



COPD 126 1.8 269 2.8 395 2.4 0.61 (0.49–0.75) <.0001 NS
no-COPD 7072 98.2 9231 97.2 16,303 97.6 1



Asthma 273 3.8 951 10.0 1224 7.3 0.35 (0.30–0.40) <.0001 NS
non-asthma 6922 96.2 8547 90.0 15,469 92.7 1



Immunosuppression 118 1.6 375 4.0 493 3.0 0.40 (0.32–0.49) <.0001 0.50 (0.31-0.82) 0.0065
non-inmmunesuppression 7080 98.4 9118 96.0 16,198 97.0 1



Chronic renal failure 103 1.4 173 1.8 276 1.7 0.78 (0.61–1.0) 0.0506 NS
no-chronic renal failure 7093 98.6 9328 98.2 16,421 98.3 1



tracheally intubated 429 11.7 168 6.5 597 9.6 1.91 (1.58–2.30) <.0001 NS
non-intubated 3225 88.3 2415 93.5 5640 90.4 1



in ICU 399 10.9 226 8.7 625 10.0 1.28 (1.07–1.52) 0.0049 NS
non-ICU 3255 89.1 2357 91.3 5612 90.0 1



death 1078 14.9 324 3.4 1402 8.4 4.97 (4.37–5.65) <.0001 2.68 (2.15–3.34) <.0001
alive 6143 85.1 9186 96.6 15,329 91.6 1 1

SARS-CoV-2: Severe acute respiratory syndrome coronavirus 2; IQR: interquartile range; COPD: chronic obstructive pulmonary disease; ICU: intensive care unit; NS: not selected by the backward elimination procedure in the multivariable logistic regression analysis with a significance level set at 0.2; NI: not included in the multivariate analysis; Covid-19:coronavirus disease.

a

Unadjusted odds ratio and 95% confidence interval.

b

Differences between cases and controls. Totals may not add up due to missing data.

c

Adjusted odds ratio and 95% confidence interval.

Discussion

The findings of this update and the previous analysis of data of May 7, 2020 (Unpublished results) indicate that obesity is the strongest predictor for Covid-19 among Mexicans followed by diabetes and hypertension. CRF was a risk factor in females only. This risk increase for Covid-19 is alarming. The higher odds ratios in females than males suggest that females with obesity, diabetes and hypertension are more susceptible for Covid-19.

These findings indicate that common comorbidities associated with severe Covid-19 outcomes also predispose this disease. Among the potential mechanisms for the association include the higher susceptibility of the obese to respiratory viral infections including influenza A [8] and increased duration of virus shedding [9] which may also be the case for SARS-CoV-2. Obesity is a state of low grade chronic inflammation that can contribute to the onset of dyslipidemia, insulin resistance and diabetes and can modify innate and adaptive immune responses, resulting in a less responsive immune system to vaccinations, antivirals and antimicrobial drugs and more vulnerable to infections [10]. Further research is needed to confirm whether obesity represents the strongest predictor for getting Covid-19 in other populations and settings.

Potential implicated mechanisms on the association between diabetes and Covid-19 include chronic inflammation, increased coagulation activity, immune response impairment, and potential direct pancreatic damage by SARS-CoV-2 [11]. Diabetics are particularly more susceptible to bacterial, mycotic, parasitic and viral infections [12].

SARS-CoV-2 binds to angiotensin converting enzyme (ACE) 2 in the lung to enter cells [13,14], this cell surface diminution of ACE2 may contribute to widespread inflammation observed with Covid-19. Angiotensin-converting enzyme inhibitors are recommended treatments for cardiovascular diseases, hypertension and chronic kidney disease and have been postulated to impact SARS-CoV-2 host-cell interactions [15]. Unfortunately information regarding patients undergoing treatment for these conditions is unavailable in the data base and needs to be explored to establish whether medication types predispose Covid-19 in Mexican patients with these comorbidities and determine the potential mechanisms involved. The increased risk of Covid-19 among females with CRF also warrants further investigation as does the mechanisms involved.

Asthma was associated with Covid-19 but only in the analysis of the whole sample. The lack of association in either sex may be related with the relative small sample size. The relationship between asthma and respiratory virus infection has been recognized [16] but is not well understood. A larger sample size would yield more data as to the population of asthmatics and the mechanism of Covid-19 susceptibility.

The decreased odds of Covid-19 among immunosuppressed males may be influenced by relatively small sample size and needs confirmation in future studies as well as identifying the specific immunosuppression illnesses associated with Covid-19.

The lower smoking prevalence in patients with Covid-19 compared with controls found in this study is consistent with preliminary estimates showing the same trend [17]. Active smoking remained statistically significant in the multivariable analysis which is consistent with recent findings [5]. Nicotine has been proposed as a therapeutic option for Covid-19 [18]. Further research is needed to confirm the “protective” effect of active smoking on Covid-19.

Pregnancy was not associated with Covid-19 in the multivariate analysis restricted to women, Table 2.

This study has some limitations namely that patients presenting symptoms of Covid-19 would be more investigated for comorbidities and/or tested representing selection bias affecting the estimates. Unfortunately, body mass index (BMI), symptoms, laboratory results and treatment of comorbidities was not available in the data base. Future studies including this information will more accurately determine the association of comorbidities with Covid-19.

This study is one of the first Mexican studies on Covid-19 indicating that obesity is the comorbidity more strongly associated with Covid-19. In 2016 the prevalence of overweight and obesity combined was 72.5% in Mexican adults aged 20 years or older [19] and was declared public health emergency by the government of Mexico. Diabetes, hypertension and CRF were also risk factors of disease.

This work compares a previous analysis of the database extracted may 7, 2020 (Unpublished results) and the results of both analyses are similar. Both indicate that comorbidities frequently found in patients with severe Covid-19 are also risk factors for the disease. Future studies will determine the potential mechanisms behind the association between these predisposing comorbidities with Covid-19.

Patients with comorbidities found to be associated with this disease should take extreme preventive measures and physicians should be aware of such associations when assessing patients with Covid-19 symptoms and take appropriate precautions.

Funding

None.

Ethics statement

Ethics approval was not required as the study was based on de-identified routine daily data publicly available.

Conflict of interest

The author has no conflicts of interest relevant to this article.

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