Is COVID-19 a Disease of Poverty: The Relationship Between Food Insecurity and the Likelihood of Hospitalization in Patients with COVID-19

Background: The World Health Organization (WHO) has declared the Corona pandemic as a public health emergency. This pandemic affects the main pillars of food security. This study aimed to investigate the relationship between food insecurity and the probability of hospitalization and the length of the recovery period after getting COVID-19. Methods: This cross-sectional study was performed through the census on COVID-19 patients diagnosed in Fasa, Iran. Informed consent, demographic, and food security questionnaire were completed over the phone. Then, all patients were followed up until recovery. Data were analyzed using SPSS26 and Chi-square test, t-test, and logistic regression (P> 0.05). Results: In this study, 219 COVID-19 patients [100 (54.7%) male and 119 female (54.3%)] with a mean age of 40.05±15.54 years old were examined. Possibility of hospitalization and the length of the recovery period of more than one month was signicantly longer in the food insecure group (P = 0.001) and (P = 0.76), respectively, but the mean length of hospital stay in the two groups was not signicantly different (P = 0.76). After adjusting for all confounding variables, people with food insecurity were 3.9 times more likely to be hospitalized than those with food security. Conclusions: We observed that food-insecure people were signicantly more likely to be hospitalized than the secure group.

especially in food-insecure groups, are crucial to recognizing appropriate intervention strategies and healthcare plans [7]. In addition, with a clear understanding of the relationship between food insecurity and hospitalization, it may be possible to predict the number of people to be hospitalized. This matter may ensure the health system sustainability throughout the duration of the coronavirus pandemic.
The COVID-19 pandemic, like other pandemics, can cause signi cant changes around the world that affect all countries, cities, and villages, it may ultimately lead to changes in lifestyle and food choices and affect food security and access to food for different groups in society [8]. Among these, families with children under 6, female-headed households, adults living alone, people with disabilities, and low-income families are most affected by food insecurity during COVID-19 and also experience food insecurity more than others [9].
Food insecurity can be de ned as " uncertain or limited availability of adequate and healthy food or uncertain or limited ability to acquire acceptable foods in socially acceptable ways" [10].  pandemic affects the four main pillars of food security (availability, access, utilization, stability) [11]. In other words, this pandemic directly and severely affects food access, food availability or distribution, and this shifts consumer demand towards cheaper and less nutritious foods, as a result, it endangers food stability and utilization [11].
Apart from the categories mentioned above, issues such as the quality of the diet, the stability of access to food sources over time and the distance to the source of the food production are also important factors in food security, and the recent pandemic has a potential impact on all of these cases [12]. Besides, this pandemic has pushed up food prices and is expected to increase food prices in most countries as this trend continues [13]. Therefore, in such circumstances, global food insecurity as an important issue should be paid as much attention as possible [14].
Food and Agriculture Organization of the United Nations (FAO) in 2017 published a report which indicates Asian countries are confronted with the highest rate of food insecurity, after African countries [15].In this regard, other studies stated that the range of food insecurity in each family is so varied and this matter could be changed from anxiety of food availability to severe starvation especially in children with no access to food [10]. It noteworthy mentioning, income is a vital issue in obtaining food security, and if a family spends more than 75 percent of their income spend on purchase food, they categorize as the highest level of food insecurity family [16]. It seems that the current pandemic worse this situation, especially in Asian and African countries.
Undoubtedly, having a clear understanding of whether in the arisen crisis, food insecurity can lead to hospitalization or not and whether the speed of recovery from the disease in people with food security will increase or not can help control the recent pandemic as much as possible. Furthermore, knowing the level of household food security and its short-term or long-term impact on the coronavirus pandemic may be a way to reduce the burden of disease and improve food security in the community through government assistance to vulnerable households. Therefore, due to the limited studies in this eld, we decided to conduct the present study to correlate the relationship between food security and the possibility of hospitalization and the length of the recovery period after getting COVID-19 disease through telephone interviews in the city of Fasa, Iran.

Methods:
The present cross-sectional study examined the relationship between food insecurity and the duration of hospitalization and the duration of full recovery after getting the COVID-19 disease in patients covered by Fasa University of Medical Sciences who have been de nitively diagnosed as positive in 2020. In the present study, all those who were de nitively infected with COVID-19 based on diagnostic tests in the city of Fasa up to date 24 May 2020 participated in the study. Considering the fact that all subjects with COVID-19 could be followed (230 subjects), all patients were examined by census.
In the present study, due to the de nitive diagnosis of COVID-19 in participants and to comply with health principles, all interviews were conducted by telephone. First, after explaining the purpose of the project, the informed consent form was read through the telephone interview method for the study population, and if they wished to participate in the study, the phone number and address of the project manager were provided to the subject so that he could easily contact the project manager if he had any questions. It should be noted that people who were unable to respond due to old age, illiteracy, or acute illness, their information completed through one of their rst-degree relatives who lived with the sick ones or had accurate information about their life situation.
After receiving the informed consent form, rst, the demographic questionnaire and then the food security questionnaire were asked from the patient by a trained person in a special order. The demographic questionnaire included factors such as age, sex, place of residence, level of education, height, and weight. After completing the questionnaire through the self-declaration of the interviewee, body mass index (BMI) was obtained by dividing weight (Kg) by height squared (m 2 ). In this study, food insecurity was assessed by 18-item the United States Department of Agriculture (USDA) Questionnaire, which has already been validated in Iran [17]. Also, in the present study, all patients were followed up after the rst contact to determine the duration of hospitalization and the duration of complete recovery (after the negative diagnostic tests). It should be noted that information such as symptoms was extracted from patients' medical records.
Inclusion criteria include: people over 18 years old, all people with COVID-19 disease referred to one of the centers or hospitals under the auspices of Fasa University of Medical Sciences with a de nite positive test result, and exclusion criteria include: unwillingness to participate in the study, excessive disability to respond, mental illness psychosis, multiple sclerosis, and diseases leading to lack of recall (such as Alzheimer's) and unclear recovery status at the end of the study, were considered.
It is noteworthy mentioning that the study protocol was following the Declaration of Helsinki guidelines and was approved by the Institutional Review Board (IRB) of Fasa University of Medical Sciences (Code: IR.FUMS.REC.1399.067).
Measuring food security status Food security status was assessed using the USDA 18-item Household Food Security Questionnaire as a valid questionnaire for epidemiological studies. It should be noted that in this study, the validated Persian version of this questionnaire was used [17].
The USDA Household Food Security Status 18-item questionnaire, based on the method of Gary Bickel et al. [18], is based on the answers "often correct", "sometimes correct", "almost every month", "some Months" and "Yes" are given a positive score (1 point) and the answers "Not correct", "Does not know or refuse", "Only 1 or 2 months", and "No" are given a zero score. Based on the number of positive answers obtained from the questionnaire, individuals are divided into 4 groups: food secure (score of the questionnaire between 0 to 2), food-insecure without hunger (score 3 to 7), food insecure with moderate hunger (score 8 to 12) And food insecurity with severe hunger (scores 13 to 18); In the present study, for better comparison, individuals were divided into two groups: food secure and food insecure (food insecure without hunger, moderate hunger, and severe hunger) and were analyzed.

Statistical Analysis:
Findings were displayed as mean and standard deviation. Qualitative variables were compared between the two groups with and without food security using the Chi-square test. Quantitative variables were compared between the two groups using an independent t-test. Multivariate logistic regression was used to eliminate the effect of confounding variables. In this model, inpatient variables were entered as response variables, and disease-related variables along with contextual variables, and food security variables were entered as independent variables. Signi cance and odds ratios (OR) were reported from this model along with 95% con dence interval. All calculations were performed in SPSS software version 26. A probability value of less than 0.05 was considered signi cant.

Results:
In this study, 230 patients with COVID19 were studied, 4 patients were reluctant to cooperate, 5 were under 18 years old, and 2 died before the end of the study, so the data of 219 patients with COVID19 were examined. Of these, 100 (54.7%) were male and 119 (54.3%) were female with a mean age of 40.05 -15.54 years and a mean BMI of 24.91. 4.52. Among these people, 64 (29.2%) lived alone, 123 (56.2%) were without any xed income, 70 (32.0%) had less than a diploma and 35 (16%) were smokers. Details of the general characteristics of these people are listed in Table 1. The ndings of this study showed that the average score of food security in the study population was 0.85±2.59, thus 22 people (10%) of the population had food insecurity while the rest of the population enjoyed food security. Table 1 also shows the factors affecting food security. Food insecurity in people without income and with variable income (P = 0.04), low literacy (P <0.001), rural (P = 0.02), with poor economic status (P <0.001) and smokers (P = 0.03) were more than other people. The mean age in the food insecurity group was higher than the others (P = 0.03) but the mean body mass index in the two groups was not signi cantly different (P = 0.29).
Fever was the most common symptom among patients (111 patients (50.7%). On the other hand, eye redness (19 patients (8.7%) had the lowest frequency among these symptoms. More details are given in Table 2. Among people with COVID19 disease who faced food insecurity 12 (54.5%), and in the group with food security 42 (21.3%) were hospitalized, which is a statistically signi cant difference (P = 0.001), but the mean length of hospital stay in the two groups was not signi cantly different (P = 0.76). Besides, the duration of recovery between the two groups with and without food insecurity showed a signi cant difference (P = 0.01) and in food-insecure people the recovery time was signi cantly longer than one month. However, the mean length of recovery did not differ between the two groups (P = 37/0) ( Table 3). In addition to Table 4, this relationship is also shown in Figure 1. This gure shows that the risk of hospitalization and recovery time of more than 30 days in food insecure people is signi cantly higher than the food secure group. Table 4 shows that the rate of hospitalization of food insecure people with COVID19 is 4.42 (95% CI: 10.95 -1.79) is higher than patients with food security. The confounding effects of the underlying variables were removed, it was found that the above relationship still exists. Discussion: The present study showed that food-insecure people with COVID-19 had a longer recovery time. Also, our ndings showed that food insecurity signi cantly increases the likelihood of hospitalization, and after adjusting for all confounding variables, people with food insecurity are 3.9 times more likely to be hospitalized than those in the food secure group. The present study is one of the few studies to examine food security in patients with COVID-19. Other studies have addressed food security in the general population.
In the present study, food-insecure individuals were signi cantly more likely to be hospitalized than the food secure group, and this nding remained signi cant after adjusting for variables. Other studies show that people in food-insecure households (especially children) are signi cantly more likely to be hospitalized for infectious diseases [19]. Besides, studies cite reasons such as poor diet quality, medication non-adherence or not having enough money to buy medication, lack of control over some chronic diseases such as diabetes, as factors for more possibility to be hospitalized in food-insecure people [20]. Food choices based on the level of food security can make a signi cant contribution to the prevention or progression of respiratory diseases. Research shows that the quality of food intake in patients with malnutrition or food insecurity is reduced due to the greater tendency of these people to consume western diets to supply their calories [21]. In the western diet, a large portion of foods are related to sugar, re ned grains, and saturated fats, and on the other hand, this group consumes a small amount of ber and unsaturated oils, which are very good for health [21]. Therefore, it can be said that this issue may be one of the reasons for the hospitalization of more people with food insecurity than the food secure group in the present study.
Our ndings show that lack of food security signi cantly increases the recovery time after getting COVID-19. In fact, food insecurity is associated with poor diet quality on the one hand [21] and on the other hand, people with food insecurity are more likely to develop chronic diseases such as diabetes [17] and obesity [22]. These factors may be one of the reasons why food-insecure adults recover longer than food-secure ones. Also, food-insecure people may avoid medication because they do not have enough money for food [23], which itself in the COVID-19 pandemic may worsen or prolong the symptoms of the disease.
Changes in the level and extent of food insecurity during the COVID-19 pandemic can have a signi cant impact on the consequences of this pandemic so that increasing levels of food insecurity are associated with mortality, morbidity, and disease burden in many non-communicable diseases [24] and lack of food security can exacerbate and prolong the effects of COVID-19 [9]. In addition, the total amount of energy received can be directly related to the duration of recovery, so that the WHO considers the amount of energy consumed between 2500 to 3400 kcal per person per day as a measure of healthy living [25] but it seems that most people with food insecurity receive far fewer calories.
According to our ndings, food insecurity was associated with low income or poor economic status, illiteracy, and rural living. Food insecurity and low incomes make people more vulnerable to coronavirus.
Because on the one hand, these people cannot buy all the food they need in one place and this causes more travel and on the other hand, these people are more exposed to severe hunger crises because they do not have enough nancial resources to buy su cient food [26]. Also, in Iran, people with lower incomes usually live in rural areas.
The COVID-19 pandemic has limited all stages of the food supply chain, including processing, production, procurement, and distribution [13]. In addition, in the recent pandemic, business closures, social distancing policies, fear of shopping, and fear of going out to shop because of the risk of exposure to the virus have led to increased food insecurity [9,27]. Besides, food availability, which is one of the categories of food security, is disrupted due to the loss of all or part of the income and the fear of depletion of food stocks [28]. It is very clear that food insecurity and changes in eating habits and behaviors in the short-term can have a signi cant impact on the health of society, especially children [27,28]. The COVID-19 pandemic complicated the strategies used by low-income families further to combat food insecurity, and in some cases, families were unable to maintain their food security [27]. The negative impact may last for years, especially in food insecure and low-income households [9]. Studies in other countries have shown that the COVID-19 pandemic reduced working hours and income in many households. For example, 43% of American households reported losing their jobs or their salaries due to the pandemic. This percentage was even higher than 50% in lower-income households [29]. Moreover, this seems to be even worse in countries that had a higher percentage of food insecurity before the COVID-19 outbreak [9].
Research has shown that income plays an important role in food choices, so that in middle-and low-income countries, poor people spend more than a quarter of their income on basic foods such as wheat, rice, and corn, while this gure was only 14% in non-poor families [11]. Besides, research shows that poor families spend about 50 percent of their income on non-essential foods such as fruits, vegetables, and animal proteins, and reduction of the revenue causes poor families to even give up consuming these food groups [11]. This reduces the dietary diversity in low-income families, as a result, the intake of micronutrients and antioxidants decreases, and eventually endangers their health status [11,30]. Therefore, choosing cheap foods and having an imbalanced diet in families with food insecurity, considering the fact that these foods are high in fat and sugar, is itself a risk factor in the development of respiratory diseases [31].
Having a balanced diet is an integral part of controlling risk management strategies in pandemics, and the recent pandemic is no exception [18]. One of the most frequent recommendations to prevent COVID-19 disease is the high intakes of fruits and vegetables, because this food group is high in antioxidants, they are very effective in boosting the immune system [32]. In addition, the consumption of animal proteins during the recovery period of the disease is highly recommended, because it promotes faster recovery [32]. It is evident that a decrease in income level makes food insecure people unable to consume fruits, vegetables, and proteins, and their food basket tends to consume cheap, high-calorie foods [33,34]. This has a signi cant effect on lowering the level of the immune system and thus worsening the disease and the duration of it in case of having COVID-19.
There is ample evidence that a balanced diet has a signi cant effect on the immune system and disease susceptibility. Meanwhile, studies have shown that certain nutrients are very effectual on the effective activity of the immune system, this mechanism may be caused by the activation of some cells, changes in the production of signaling molecules, and the effect on gene expression [35]. Therefore, de ciency of some macronutrients such as protein and some micronutrients such as iron, zinc, vitamins A, E, B6, B12, which mainly play an important role in maintaining the function of the immune system, in addition to low energy intake can reduce immune system activity and increases the likelihood of susceptibility to infection [36].
On the other hand, having an unbalanced diet, in the long run, activates the innate immune system and inhibits the adaptive response of the immune system to increased oxidative stress, as a result, it causes a delayed response in the adaptive response of the immune system, which is considered as one of the most important strategies of the immune system against pathogens [21]. Therefore, it is recommended to improve food habits and security by having a balanced diet and avoid western diets it may be one of the most important ways to boost the immune system and control infectious respiratory diseases [37].
Evidence suggests that food insecurity can lead to poor health outcomes by activating in ammatory pathways [38,39]. Food insecurity can independently increase the level of in ammatory factors such as Creactive protein (CRP) [39], IL-6, and tumor necrosis factor (TNF) receptor 1 [38]. On the other hand, food insecurity itself is considered a powerful stress factor, as studies show, stress also causes an increase in in ammatory factors in the individual [40]. An increase in these factors may lead to an increase in the level of in ammation in the body, resulting in a late recovery of food insecure people with COVID-19 [9].
The present study had some limitations. First, due to the nature of the study (cross-sectional), the causeand-effect relationship cannot be extracted. Second, in the present study, factors related to mental states such as stress and anxiety were not examined, which is suggested that since food insecurity plays an important role in people's mental health, these factors be examined in future studies. Third, in this study, the interview was conducted by telephone, which in this type of interview, there was a possibility of reporting an error. Fourth, food insecurity was assessed using the USDA retrospective questionnaire, since this questionnaire examines the level of food security in the past year, there is a possibility of non-recall error.
One of the strengths of the present study is that according to the research, this study is one of the rst studies to investigate the relationship between food security with the probability of hospitalization and the length of the recovery period in patients with COVID-19. Also, the use of an 18-item USDA validated questionnaire (not a short-form version) to assess food security adds credibility to our study. The sample size examined in the present study also adds to the strength of the present study because the total sample size was de nitively positive for COVID-19. It is suggested that prospective studies be conducted in the future to better understand the impact of coronavirus pandemic on food security.

Conclusion
The present study observed that food-insecure adults were signi cantly more likely to be hospitalized than the secure group and also the duration of recovery was signi cantly higher in them. Naturally, having information about the level of household food security helps policymakers (governments and global healthrelated organizations) and medical staff (physicians, nurses, and researchers) to cure COVID-19 patients as quickly as possible and reduce the duration of the disease and provide more practical solutions. Furthermore, making sure that food is available and accessible to those who need it ensures that essential nutrients are available to all segments of society to strengthen the immune system, and maybe this is a way to reduce the burden of the disease in society. It is obvious that the current state of long-term or short-term support for food insecure or at-risk individuals by governments and charities are helping a great deal to reduce the likelihood of hospitalization and speed up patient recovery.

Declarations Ethical Approval and Consent to participate
The study protocol was following the Helsinki Declaration and was con rmed by the Ethics Committee of Fasa University of Medical Sciences (Approval Code: IR.FUMS.REC.1399.067). The participants were informed about the research objectives and a consent form through the phone interview was obtained from the subjects before starting the survey.

Consent for publication
Not applicable Availability of supporting data The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request to the corresponding author.

Competing interests
The authors hereby a rm that the manuscript is original, that all statements asserted as facts are based on authors' careful investigation and accuracy, that the manuscript has not been previously published in total or in part and has not been submitted or considered for publication in total or in part elsewhere. Each author acknowledges he/she has participated in the work substantively and is prepared to take public responsibility for the work and authors have no competing interest in the results of the article.

Funding
The study was supported by the Fasa University of Medical Sciences (Grant No.: 99021).