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Abstract
Objectives Mississippi (MS) is one of the southern states with high rates of foodborne infections. The objectives of this paper are to determine the extent of Salmonella and Escherichia coli infections in MS, and determine the Salmonella infections correlation with socioeconomic status using geographical information system (GIS) and neural network models.
Methods In this study, the relevant updated data of foodborne illness for southern states, from 2002 to 2011, were collected and used in the GIS and neural networks models. Data were collected from the Centers for Disease Control and Prevention (CDC), MS state Department of Health and the other states department of health. The correlation between low socioeconomic status and Salmonella infections were determined using models created by several software packages, including SAS, ArcGIS @RISK and NeuroShell.
Results Results of this study showed a significant increase in Salmonella outbreaks in MS during the study period, with highest rates in 2011 (47.84±24.41 cases/100 000; p<0.001). MS had the highest rates of Salmonella outbreaks compared with other states (36±6.29 cases/100 000; p<0.001). Regional and district variations in the rates were also observed. GIS maps of Salmonella outbreaks in MS in 2010 and 2011 showed the districts with higher rates of Salmonella. Regression analysis and neural network models showed a moderate correlation between cases of Salmonella infections and low socioeconomic factors. Poverty was shown to have a negative correlation with Salmonella outbreaks (R2=0.152, p<0.05).
Conclusions Geographic location besides socioeconomic status may contribute to the high rates of Salmonella outbreaks in MS. Understanding the geographical and economic relationship with infectious diseases will help to determine effective methods to reduce outbreaks within low socioeconomic status communities.
- EPIDEMIOLOGY
- Salmonella, E. coli, Mississippi, GIS, Neural network
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Strengths and limitations of this study
Socioeconomic and demographic indicators may be used to predict which individuals and communities are at an increased risk of acquiring foodborne infections.
Neural network and geographical information system modelling were shown in this study to be useful tools to predict the correlation of Salmonella outbreaks with socioeconomic factors.
The southern parts of the USA, including Mississippi, are more vulnerable to increase outbreaks of foodborne illnesses due to low socioeconomic status, climatic changes and agricultural practices.
Research is critically needed in disadvantaged states and areas with low socioeconomic status such as Mississippi.
The study is limited by the availability of data and the accurate reporting. In addition, data were collected from several sources which may increase the uncertainty of the resulting models.
Methodologies used in this paper may need further validation.
Introduction
Foodborne diseases are a major public health concern. Studies had estimated that each year in the USA alone, 31 pathogens cause 37.2 million illnesses; of these, 9.4 million were foodborne.1 The prevalence of Escherichia coli O157:H7 infection has grown since its first description and, despite the best control measures, E. coli O157:H7 remains a serious health concern.2–4 E. coli O157:H7 is responsible for an estimated 73 480 cases of illness, 2168 hospitalisations, and 61 deaths annually in the USA.3 The majority of such E. coli O157:H7 outbreaks in the USA are associated with foodborne transmission. Whereas there were approximately 93.8 million human cases of gastroenteritis and 155 000 deaths due to Salmonella infection around the world each year.5 In the USA alone, Salmonella causes an estimated 1.4 million human cases, 15 000 hospitalisations and more than 400 deaths annually.6 Salmonella rates varied considerably by geographic region. This heterogeneity is likely in part due to differences in reporting. Differences in salmonellosis case rates between geographically and socioeconomically similar US states have been documented, with rates differing by as much as 200% between neighbouring states.5
The southern parts of the USA are more vulnerable to increase outbreaks of foodborne illnesses due to socioeconomic status, climatic changes and agricultural practices. Our previous studies examined the effects of climatic changes on Salmonella infections in the southern states, and results showed a significant effect of increased temperature on the rate of outbreaks.7
The Mississippi State Department of Health (MSDH) indicated that the most common foodborne illnesses in Mississippi (MS) are salmonellosis, campylobacteriosis and shigellosis. It is not uncommon for the 82 counties of MS to report 200 cases of Salmonella a month. In 2011, the MSDH reported a total of 1440 cases of salmonellosis, 239 cases of shigellosis, 71 cases of campylobacteriosis and 15 cases of E. coli O157:H7/HUS. In 2009, a consumer report investigation revealed that 67% broiler chicken had tested positive for Salmonella and Campylobacter.
Limited studies had examined foodborne illnesses in the state of MS. It is critical to determine the extent of these illnesses in the state and their correlation with socioeconomic status.
MS is one of the leading agriculture states with low socioeconomic status (LSES) and high rates of obesity and associated health disparities. A comprehensive food safety study will delineate the true nature of foodborne illnesses in MS.
The objectives of this paper are to determine the extent of Salmonella and E. coli infections in MS and compare it with other southern states and with two reference states in the northern USA, and to determine the infections’ correlation with socioeconomic status using several modelling approaches including geographical information system (GIS) and neural network (NN).
GIS mapping
A GIS integrates hardware, software and data for capturing, managing, analysing and displaying all forms of geographically referenced information. GIS may be applied to number of disciplines. GIS has been used to visualise, quantify and analyse geographic components of health research. Studies have ranged from analysis of geographic variation in the use of surgical procedures8 and examination of the relationships between ethnicity, low birth weight and area socioeconomic status,9 to assessing the relation between the respiratory health status and exposure to heavy traffic pollution,10 ,11 and tracing the movement of AIDS epidemic.12 These studies demonstrate the wide range of uses for GIS.
NN models (using NeuroShell)
Artificial NNs (ANNs) are mathematical constructs that use previously solved examples to build a system of neurons to make a new decision, classify and forecast. ANN models have been applied in diagnosing myocardial infarction, pulmonary emboli and gastrointestinal (GI) haemorrhage and conditions; in addition to mortality prediction from cardiovascular risk factors.13 An ANN modelling technique is based on the observed behaviours of biological neurons, used to mimic the performance of the human system.14 NeuroShell2 is a program that mimics the human brain’s ability to classify patterns or to make predictions or decisions based on past experience. The human brain relies on neural stimuli while the NN uses data sets. It enables the building of sophisticated custom problem-solving applications without programming. These weighted inputs are simply summed inside the neuron, which pass through a suitable threshold (activation). Similarly, the activated outputs from previous layers transfer to the output layer, passing through another activation, produce an output to simulate a desired output (target) at the end. By a learning algorithm, the neural net achieves learning by modifying weights proportional to the difference between the target and the gained output.13
Methods
Data collection
Data of laboratory-confirmed E. coli and Salmonella cases were collected, from 2002 to 2012, for the selected states including MS, Alabama (AL), Tennessee (TN), Louisiana (LA), Montana (MT) and Michigan (MI). Southern states including AL, TN and LA were selected as neighbouring states to MS, while MT and MI were selected as a reference states in the northern USA based on their geographical and climatic conditions. E. coli and Salmonella cases were defined by Centers for Disease Control and Prevention (CDC) as ‘confirmed’ with the isolation of bacteria from a clinical specimen.
MS E. coli and Salmonella monthly outbreak cases were grouped by year and districts. Data sources for this study include the CDC and the States Department of Health Epidemiology Departments.15–18 Data were adjusted to 100 000 of population.19
In addition to Salmonella infections, data for MS, socioeconomic factors for MS counties, categorised by public health districts, for the year 2010–2011, were retrieved from the MSDH County Health Ranking Mississippi Data.20 The selected factors include poverty, uninsured, unemployment and primary care providers’ rates,
Data analysis
Data were analysed using SAS V.9.4, ArcGIS V.10, @Risk and NeuroShell2 software packages (Palisade Corporation. @Risk 4.0: a new standard in risk analysis. Ithaca, New York, USA: Palisade Corporation, 2011. http://www.palisade.com/risk; SAS Institute Inc. SAS user's guide: statistics Version 9.4 ed. Cary, North Carolina, USA: SAS Institute Inc, 2014; Ward Systems Group. 1993 NeuroShell 2 user's manual. Frederick, Maryland, USA: Ward Systems Group Inc, 1993; ESRI 2011. ArcGIS Desktop: Release 10. Redlands, California, USA: Environmental Systems Research Institute). E. coli and Salmonella rates were analysed using analysis of variance (ANOVA). ANOVA (PROC GLM, SAS V.9.4) was carried out to determine the level of significance between the selected variables: years, month, districts and states, which were used as classification variables, while E. coli and Salmonella outbreaks’ rates were used as response variables. TUKEY all pair wise test was followed for further classification.
Regression analysis
Multiple regression analysis was carried out (PROC REG, SAS V.9.4), to test the relationship between Salmonella rates and socioeconomic factors: including poverty, uninsured, unemployment and primary care providers’ rates. Socioeconomic factors were used as classification variables and Salmonella infection rate as a response variable.
GIS mapping
A GIS integrates hardware, software and data for capturing, managing, analysing and displaying all forms of geographically referenced information.
Study area for GIS map
Located in the southern USA, MS (32.9906° N, 89.5261° W) is bordered by TN on the north, Gulf of Mexico on the south, AL on the east, and Arkansas and LA on the west. It covers a total area of 47 689 square miles. GIS allows for the integration and analysis of geographic data, such as coordinates and area perimeters, and tabular data (ie, attributes of geographic data points). Data are imported into mapping software in layers, where each layer represents a different visual component of the map. Shape files are layers which provide visual output of coordinates and area perimeters on the map.
MS counties data were pooled and grouped by public health districts. Background map was obtained from ESRI ArcGIS (ESRI 2011. ArcGIS Desktop: Release 10. Redlands, California, USA: Environmental Systems Research Institute) online resources. Maps’ layers for Salmonella, unemployment and primary care providers’ rates were created for the years 2010 and 2011, to visually analyse areas with higher disease rates and socioeconomic status.
NN model
NN models for MS were developed using @RISK (Palisade Corporation. @Risk 4.0: a new standard in risk analysis. Ithaca, New York, USA: Palisade Corporation, 2011. http://www.palisade.com/risk) and NeuroShell2 (Ward Systems Group. 1993 NeuroShell 2 user's manual. Frederick, Maryland, USA: Ward Systems Group Inc, 1993) software packages. The network is exposed to the problem being predicted or classified, and NeuroShell2 will be able to ‘learn’ patterns from training data and be able to make its own classifications, predictions or decisions when presented with new unseen data.
MS districts’ Salmonella outbreaks and socioeconomic data were used for NN models. Mean and SD were calculated for each variable, including Salmonella, poverty, uninsured, and unemployment and primary care providers’ rates. Those means and SD were subsequently used to generate data with 500 iterations using @RISK in Risk Normal distribution. The simulated data were then used as training examples for the NN models, while the original data were used for testing with NeuroShell2 software. Advanced NNs were selected and the simulated data files were imported. The network was built by defining poverty, uninsured, unemployment and primary care providers’ rates were used as input variables while Salmonella outbreaks as output. A General Regression Neural Network (GRNN) model was selected from the software design architecture. This model was trained with the simulated data. The test file containing the original data was imported to the system and applied to previously saved trained NN models. Results were exported to Excel where graphs were created to show the association between actual data and the predicted model.
Results
Results of this study showed highest rates of Salmonella outbreaks in MS compared with other states (36±6.29 cases/100 000; p<0.001), while the lowest rate was found in MI (9.10±0.65 cases/100 000). No significant change in Salmonella rates was observed during the past 10 years in the selected states; however, the highest states’ average of Salmonella were in 2011 (22.05±14.37; p>0.05). Results also showed no significant change in E. coli outbreaks from 2002 to 2011 (p>0.05). The highest rates of E. coli outbreaks were found in MT (3.41±0.67 cases/100 000; p<0.001), while the lowest rates were in LA (0.30±0.16 cases/100 000; figure 1).
Salmonella and Escherichia coli rates in Mississippi (MS), Alabama (AL), Tennessee (TN), Louisiana (LA), Montana (MT) and Michigan (MI). The highest rates of Salmonella were found in MS, while highest rates of E. coli were found in MT from 2002 to 2011.
In addition, results showed a significant increase in Salmonella outbreaks in MS with highest rates in 2011 (47.84±24.41 cases/100 000; p<0.001), and the lowest in 2006 (26.69±10.67 cases/100 000). However, no significant change in E. coli rates was observed over time (p>0.05). The highest outbreaks of E. coli were observed in 2010 (2.40±4.06 cases/100 000; figure 2).
Total number of Salmonella and Escherichia coli cases in Mississippi 2002–2011. Highest rates of Salmonella were observed during 2011. Highest rates of E. coli were observed in 2010.
ANOVA showed a significant variation within the different districts of MS. Highest rates of Salmonella outbreaks were found in the northeast district of MS with an average of 47.76±21.59 cases/100 000 (p<0.001), and the lowest rates were found in the Delta area (17.39±4.93 cases/100 000).
E. coli rates were shown in this study to be higher in the Tombigbee region of the state (1.02±1.58 cases/100 000), and the lowest in the Northwest region of state (0.32±0.35). However, E. coli rates were not significantly different between the districts (p>0.05).
Regression analysis between poverty, unemployment, uninsured and primary care providers rates showed a moderate correlation with Salmonella outbreaks (R2=0.34). A negative correlation was observed between Salmonella and poverty rate (R2=0.152). Areas with high poverty rates were shown to have low rates of Salmonella outbreaks. However, a positive correlation was shown between increased Salmonella rates and per cent of unemployed, uninsured and primary care providers’ rates.
GIS maps of Salmonella outbreaks in MS in 2010 and 2011 created by ArcGIS showed higher rates of Salmonella outbreaks in the northeast and Tombigbee regions. To determine the relationship between Salmonella outbreaks and the socioeconomic factors, GIS maps showed highest rates of unemployment in the northeast, northwest, Tombigbee and Delta, for both years. An average of 42% increase in unemployment rate was observed in these regions in 2011.
Primary care provider rate was shown to be the lowest in the northwest and east-central regions of MS. An average of 17% decrease in primary care provider rates was observed in these regions. On the other hand, highest rate of primary care providers were found in in west-central and southeast regions of the state, with 2% increase from 2010 to 2011 (figure 3).
GIS maps of Salmonella outbreak, unemployment rate and PCP in MS districts 2010–2011. Substantial regional differences in the incidence of Salmonella infections were found. Higher rates of Salmonella outbreaks were found in the northeast and Tombigbee regions. The northern region of the state including northeast, northwest, Tombigbee and Delta district had the highest rates of unemployment. Primary care provider rate was shown to be the lowest in the northwest and east-central regions. The highest rates of primary care providers were found in west-central and southeast regions. GIS, geographical information system; MS, Mississippi; PCP, primary care providers rate.
NN model for salmonella and socioeconomic status (including poverty, unemployment, uninsured, unemployment and primary care provider rates including poverty, unemployment, uninsured, unemployment and primary care provider rates) showed a moderate correlation (R2=0.41) between the actual and predicted network (results are shown in table 1 and figure 4).
Results of neural network model
General Regression Neural Network model for Salmonella outbreaks and socioeconomic factors. The network was built by defining poverty, uninsured, unemployment and primary care providers’ rates were used as input variables while Salmonella outbreaks as output. The blue line represents the actual Salmonella cases in the nine districts of Mississippi (MS). The orange line represented the Salmonella cases predicted by the network, while the grey line represents the difference between the models.
Discussion
Results of this study showed highest rates of Salmonella outbreaks in MS when compared with other selected states, including AL, TN, LA, MT and MI. The average Salmonella outbreaks in MS (36 cases/100 000) were more than twice than the average US Salmonella outbreaks (16.42 cases/100 000).21 A significant variation was observed in this study between the neighbouring southern states and with northern states. Rates were higher in the southern states compared with northern states, with MS having the highest rates of Salmonella.
Substantial regional differences in the incidence of Salmonella infections have been reported previously.22 The study reported particularly large relative increases in incidence occurred at sites in the southern USA, and a northeastern state had the highest mean annual incidence in FoodNet.
On the other hand, MS had low rates of E. coli outbreaks during the study period. An average of 0.38 cases/100 000 were observed, which was lower than the US average of 1.12 cases/100 000.21 A geographical variation was also observed for E. coli rates with MT having the highest rates. Cattle and fresh produce are the major source of E. coli outbreaks.
In MS, 1440 cases of salmonellosis were reported to MSDH in 2011. This marked a continued increase in the rate and number of reported cases in MS, since 2009. The CDC reported that for every case of Salmonella and E. coli reported, there are 29 and 26 cases that are not diagnosed or reported, respectively.21
Targeted studies of regional factors, such as egg or chicken suppliers, state egg quality assurance programmes, and consumer and food handler educational initiatives, might help clarify reasons for the regional incidence variability.22
A significant variation was observed in Salmonella and E. coli outbreaks among the MS districts. GIS mapping, regression analysis and NN models were used to determine the relationships of outbreaks with socioeconomic factors. GIS allows for the integration and analysis of geographic data, such as coordinates and area perimeters, and tabular data (ie, attributes of geographic data points).
The northern region of the state including northeast, northwest, Tombigbee and Delta district had the highest rates of unemployment as well. An average of 42% increase in unemployment rate was observed in the region in 2011. Primary care provider rate was shown to be the lowest in the northwest and east-central regions of MS. An average of 17% decrease in primary care provider rates was observed in these regions. On the other hand, highest rates of primary care providers were found in west-central and southeast regions of the state, with 2% increase from 2010 to 2011.
Socioeconomic and demographic indicators can be used to predict which individuals and communities are at an increased risk of acquiring infections. Generally, LSES is an important predictor of several poor health outcomes including chronic diseases, mental illnesses and mortality, which is the case in MS as shown in this study.
In this study, regression analysis results showed a positive correlation between low socioeconomic factors and increased rates of Salmonella infections, with the exception of poverty rates, which were negatively correlated with Salmonella outbreaks. Poverty and the availability of physician care showed the highest correlation with Salmonella outbreaks.
Under-reporting is an important issue in disease surveillance systems, especially for enteric infections. Generally only those patients with severe symptoms go to see the doctor and are notified to health authorities. As of 2011, more than 22.6% of MS populations are living under poverty line. According to the United States Department of Agriculture (USDA) Economic Research Service, the average percapita income for MS residents in 2011 was $32 000, although rural percapita income lagged at $29 550. Moreover, there are 96 hospitals in MS, 163 rural health clinics and 21 federally qualified health centres that provide services at 170 sites in the state. An average of 19.0% of MS residents lack health insurance.19 ,20
A geographical variation of poverty rates was also observed in different districts of the state. In the Delta region of MS, for example, the poverty rate was 44.2%. The lowest Salmonella rates were observed in this region as well. With high rates of poverty, many individuals cannot afford to seek medical care, which may result in under-reporting of the disease.
Studies suggested that high socioeconomic status (HSES) groups may be over-represented in incidence statistics. It is possible that since LSES groups tend not to have health insurance or financial means to seek medical care in the event of illness, the ratio of HSES to LSES cases may be skewed in the opposite direction. Access to healthcare may be an important influence on rates of reported bacterial infection. In an economy without universal healthcare coverage, propensity to seek care for GI infection has been associated with having health insurance.1 ,23 However, the new Affordable Care Act (ACA) is expected to expand insurance coverage for millions of people in the USA. As a result, rates of reported cases of diseases and infections are expected to increase. In future projects, we will try to understand the impact of ACA on diseases reporting, especially among minority and LSES groups.
In MS, the west-central region of the state showed higher rates of Salmonella infections and lower poverty rates (36%), when compared with the Delta region. However, more medical facilities are available in west-central region, resulting in higher identification and reporting of diseases. In addition, in 2011, 20% of the populations in west-central region are college graduate, with 10% unemployment rate, while only 14% of populations at the Delta region are college graduate and 13% are unemployed.
A study had identified lower rates of shigellosis and salmonellosis in communities with high rates of unemployment. The authors speculate that the reduction in access to healthcare due to lack of employment may lead to underdetection of disease in unemployed individuals.24
Other studies had similarly utilised GIS to examine the relationships between area-based socioeconomic measures and incidence of salmonellosis.23 ,25 Their results showed higher incidences of salmonellosis in the groups with high education compared with the less educated groups. They suggested that education may play a significant role in health-seeking behaviour and the predisposition for Salmonella infections at the population level.25
NN modelling was shown in this study to be a useful tool to predict the correlation of Salmonella outbreaks with socioeconomic factors. A moderate correlation between actual and network-predicted output was observed of 41% which is shown to be an acceptable level considering the biological system.
ANNs are non-linear mapping structures based on the function of the human brain. They have been shown to be universal and highly flexible function approximates for any data. ANNs were developed initially to model biological functions.13 ,14 ,26 ,27 NN molding has been used previously for prediction of T-cell epitopes,28 prediction of cancer using gene expression profiling,29 temperature prediction,30 diabetes prediction,14 poultry growth modelling,31 egg price forecasting,32 in addition to predicting the relation between obesity and high blood pressure.27
Our results are different from reported individual-level epidemiological studies that have found a higher level of foodborne infections among low-education and low-income groups.
In the USA, MS ranked 50th among all the states for healthcare, according to the Commonwealth Fund, a non-profit foundation working to advance performance of the healthcare system. For the past 3 years, more than 30% of MS residents, and 22.8% of the state’s children, have been classified as obese. On top of obesity, MS had the highest rates in the nation for high blood pressure, diabetes and adult inactivity.27
Social and economic conditions underpin poverty and can directly and indirectly affect health status and health outcomes. Major epidemics emerge and chronic conditions cluster and persist wherever poverty is widespread.33
Conclusion
Human foodborne illnesses are significant public health concerns. In the current study, foodborne illnesses in southern USA with particular emphasis to MS were examined. This study showed a significant correlation between socioeconomic status and the increased rates of Salmonella especially in MS which had higher rates than other neighbouring states and some of the northern states. A significant increase in Salmonella outbreaks for the past 3 years in MS were observed, with no change in E. coli outbreaks. A correlation between increase in outbreaks of Salmonella and the LSES was also observed. NN models were shown to be a useful tool to model and predict outbreaks. The model was created using four input variables and one output. NN models accounting for non-linearity predicted better association than regression models. GIS mapping was also shown to be a very useful instrument to map and visualise the areas and districts of highest Salmonella outbreaks in addition to socioeconomic status. Our results showed that Northeast and Tombigbee regions of MS had the highest rates of Salmonella outbreaks. The northern region also had the highest rate of unemployment, and primary care provider rate was shown to be the lowest in the northwest and east-central.
Understanding the geographical and economic relation with infectious diseases will help to determine effective methods to reduce outbreaks within these communities.
References
Footnotes
Contributors LA and HAA designed the paper, wrote and reviewed the manuscript. LA collected and analysed the data.
Funding The project described was supported by grant number G12RR013459 from the National Center of Research Resources, G12MD007581 from NIH/NIHMHD and PGA-P210944 from the US Department of State.
Competing interests None declared.
Provenance and peer review Not commissioned; externally peer reviewed.
Data sharing statement No additional data are available.