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Revista mexicana de ciencias agrícolas

versão impressa ISSN 2007-0934

Rev. Mex. Cienc. Agríc vol.14 no.1 Texcoco Jan./Fev. 2023  Epub 19-Jun-2023

https://doi.org/10.29312/remexca.v14i1.2966 

Essays

Epidemiological behavior of Salmonella sp. in plant-based foods by intercontinental region

María Teresa Berrocal Martínez1 

Daniel Ruiz-Juárez2  § 

Mónica Gutiérrez-Rojas2 

Javier Olivares-Orozco2 

1Maestría en Ciencias Agropecuarias-Universidad Autónoma Metropolitana-Unidad Xochimilco. Calzada del Hueso 1100, Coyoacán, Ciudad de México, México. CP. 04960. (amyet96@hotmail.com).

2Departamento de Producción Agrícola y Animal-Universidad Autónoma Metropolitana-Unidad Xochimilco. Calzada del Hueso 1100, Coyoacán, Ciudad de México, México. CP. 04960. Tel. 55 44626217. (olivares@correo.xoc.uam.mx; mgutierrez@correo.xoc.uam.mx).

Abstract

The epidemiological behavior and specific serotypes of Salmonella sp. in plant-based foods are represented by state, country, and intercontinental region. Histograms show incidences of outbreaks in the population of Africa, Europe and North America, spatial distribution of serotypes and the cumulative relative frequency curve. The foodborne diseases were due to Salmonella Infantis, S. Derby, S. Enteritidis, S. 1,4,[5],12:i:-, S. Agona, S. Panama, S. Typhi, S. Braenderup, S. Typhimurium, S. Newport, S. Saintpaul, S. Poona, S. Abony, S. Urbana, S. Adelaide and S. Uganda. On the African continent, the epidemiological behavior of S. enterica showed significant statistical differences (p≤ 0.0001), with cumulative prevalence for North Africa (49.9%), East Africa (12%), South Africa (3%), and West and Central Africa (13%), in contrast to the incidence observed for non-typhoid S. In Europe, the epidemiological behavior of Salmonella sp. by year of study showed statistically significant differences (p≤ 0.0001) in the observed incidence among 28 countries, also, the Fi of outbreaks of Salmonella sp. was higher in the last year. Between the United States and Mexican states, significant differences (p≤ 0.0001) were also observed in the incidence of the number of epidemiological outbreaks by year. However, as of 2019, a decrease in the epidemiological curve was observed. Among the regions of Africa, Europe and North America, the epidemiological behavior of Salmonella sp. presented incidences of 4.08, 30.82 and 65.1% respectively, due to the consumption of contaminated plant-based foods.

Keywords: cross-contamination; enterobacteria; foodborne disease; risk analysis

Resumen

Se representa el comportamiento epidemiológico y los serotipos específicos de Salmonella sp., en alimentos de origen vegetal por estado, país y región intercontinental. Los histogramas muestran incidencias de brotes en la población de África, Europa y América del Norte, distribución espacial de los serotipos y la curva de frecuencia relativa acumulada. Las enfermedades transmitidas por alimentos se debieron a Salmonella Infantis, S. Derby, S. Enteritidis, S. 1,4,[5],12:i:-, S. Agona, S. Panama, S. Typhi, S. Braenderup, S. Typhimurium, S. Newport, S. Saintpaul, S. Poona, S. Abony, S. Urbana, S. Adelaide y S. Uganda. En el continente africano, el comportamiento epidemiológico de S. enterica mostró diferencias estadísticas significativas (p≤ 0.0001), con prevalencia acumulada para África del Norte (49.9%), África Oriental (12%), Sudáfrica (3%) y África Occidental y Central (13%), en contraste con la incidencia observada para S. no tifoidea. En Europa, el comportamiento epidemiológico de Salmonella sp., por año de estudio mostró diferencias estadísticamente significativas (p≤ 0.0001) en la incidencia observada entre 28 países, así como la Fi de brotes de Salmonella sp., fue mayor en el último año. Entre las entidades federativas de EE. UU y México, también se observaron diferencias significativas (p≤ 0.0001) en la incidencia del número de brotes epidemiológicos por año. Sin embargo, a partir de 2019 se observó disminución en la curva epidemiológica. Entre las regiones de África, Europa y América del Norte, el comportamiento epidemiológico de Salmonella sp. presentó incidencias de 4.08, 30.82 y 65.1% respectivamente, debido al consumo de alimentos contaminados de origen vegetal.

Palabras clave: análisis del riesgo; contaminación cruzada; enfermedades transmitidas por los alimentos; enterobacterias

Contamination of plant foods of agricultural origin

In 2014, the World Health Organization (WHO) defined foodborne diseases (FBDs) as a major public health problem in the world and the main index of mortality in infants under five years of age (1.5 million per year) in developing countries. Epidemiological outbreaks caused by FBDs in humans can be due to consumption of plant-based foods, contaminated with pathogenic bacteria transmitted during primary production, until the harvest of food (Hernández et al., 2011), due to incorrect use of water for irrigation, cross-contamination during harvest practices, vegetable washing process after harvest and food handling in packaging, transport and shelf life (ICMSF, 2005; Jung et al., 2014).

Also, due to the interaction of pathogenic microorganisms of the families Enterobacteriaceae and Vibrionaceae, Gram-negative bacteria, Staphylococcus sp., Gram-positive bacteria (Soto et al., 2016). The main genera and species are Vibrio sp., Campylobacter sp., Yersinia enterocolitica, Shigella flexneri, Listeria monocytogenes, Escherichia coli and Salmonella sp., the latter is the main precursor of FBDs in animals and humans (50%) (OMS, 2005; Betancor et al., 2006; Barreto et al., 2016; Andrews et al., 2021), which presents epidemiological impact in the world due to the effects on public health (Alam, 2014; Anderson et al., 2016; Soodb et al., 2018).

Epidemiological behavior and spatial distribution of Salmonella sp. by region

In 2021, the US. Food & Drug Administration (FDA) recognizes that gastroenteritis and typhoid fever have an epidemiological effect of global distribution and are periodically expressed in developed and developing countries (Andrews et al., 2021). Annually there are 153 million epidemiological outbreaks caused by Salmonella, 91.28% is transmitted by food and 8.72% due to an unknown cause. Fifty-seven thousand cases end in deaths from non-typhoid Salmonella (NTS) (Majowicz et al., 2010; Healy and Bruce, 2018). The severity caused by Salmonella sp., with respect to human infections, varies depending on the serotype involved which affects children under five years of age, the elderly (Nair et al., 2015) and immunosuppressed patients (Majowicz et al., 2010).

Distribution of Salmonella sp. in the African continent

In Africa, Salmonella sp. affects the public health of inhabitants by region (Majowicz et al., 2010; Reddy et al., 2010). From 1984 to 2006, human epidemiological outbreaks caused by Salmonella species were monitored among the five regions of the continent (Table 1). The epidemiological behavior of S. enterica in the regions of the continent showed significant statistical differences (p≤ 0.0001) in the cumulative prevalence in North Africa (49.9%), East Africa (12%), South Africa (3%) and West and Central Africa (13%) (Reddy et al., 2010).

The increase in outbreaks of S. enterica contamination among regions of the continent may be due to population growth, who demands food products without safety and hygiene measures, availability of drinking water, application of good agricultural practices to produce safe foods and viability of international trade to offer healthy foods (Mtove et al., 2010; FAO, 2017). In Algeria, Egypt, Jordan, Lebanon, Libya, Morocco, Iraq, Pakistan, Palestine, Saudi Arabia, Sudan, Tunisia, Oman, Palestine and the United Arab Emirates, percentages of S. Enteritidis (29.8%), S. Typhimurium (23.6%), S. Kentucky (20.3%) and other salmonella (26.3%) were detected (Al-Rifai et al., 2019). The incidence of Salmonella sp. was due to the percentage in salads and sandwiches (25%), fresh fruits and vegetables (5.8%), meat products, dairy, egg and seafood (69.2%) (Al-Rifai et al., 2019).

Table 1 Incidence of Salmonella sp. due to consumption of contaminated plant-based foods in the African continent from 1984 to 2006. 

Region Serotype No. of cases Infected population Incidence (%)
North Africa S. enterica 10 230 5 105 49.9 ±0.75 a
East Africa 21 317 2 558 12 ±0.55 c
South Africa 23 893 717 3 ±0.25 d
West and Central Africa 5 887 765 13 ±0.8 b
North Africa S. no typhoid 10 230 5 125 50.1 ±0.15 c
East Africa 21 317 18 759 88 ±0.5 b
South Africa 23 893 23 176 97 ±0.5 a
West and Central Africa 5 887 5 122 87 ±0.5 b

Levels not connected by the same letter are significantly different. Data extracted and analyzed from Reddy et al. (2010).

Status of Salmonella sp. in Europe

In 2017, the European Food Safety Authority (EFSA) and the European Centre for Disease Prevention and Control (ECDC) reported cases of Salmonella sp. infection, in 28 countries from 2012 to 2016 (94 278, 87 753, 92 012, 94 597 and 94 530, respectively) (Table 2) (EFSA and ECDC, 2017). By year, the incidence on the epidemiological behavior of Salmonella sp. among the countries of the continent showed significant statistical differences (p≤ 0.0001).

Table 2 Epidemiological behavior of Salmonella sp. due to consumption of contaminated plant-based foods among regions of the European continent. 

Country Year/Incidence (%)
2012 2013 2014 2015 2016
Austria 1.88 ±0.01 m 1.6 ±0.1 m 1.8 ±0.1 k 1.63 ±0.01 l 1.5 ±0.1 h
Belgium 3.29 ±0.01 j 2.88 ±0.01 k 2.93 ±0.01 i 3.35 ±0.01 i 2.97 ±0.01 g
Bulgaria 0.89 ±0.01 o 0.87 ±0.01 q 0.79 ±0.01 p 1.14 ±0.01 n 0.76 ±0.01 ij
Croatia 0 ±0 w 0 ±0 w 1.62 ±0.01 m 1.68 ±0.01 kl 1.31 ±0.01 hi
Cyprus 0.1 ±0.01 v 0.09 ±0.01 vw 0.1 ±0.01 t 0.07 ±0.01 t 0.08 ±0.01 k
Czech Republic 10.67 ±0.01 b 11.16 ±0.01b 14.41 ±0.01 b 13.12 ±0.01 b 12.28 ±0.01 b
Denmark 1.28 ±0.01 n 1.3 ±0.1 o 1.22 ±0.01 n 0.98 ±0.01 o 1.14 ±0.01 hi
Estonia 0.26 ±0.01 t 0.21 ±0.01 t 0.1 ±0.01 t 0.12 ±0.01 t 0.37 ±0 jk
Finland 2.34 ±0.01 l 2.26 ±0.01 l 1.76 ±0.01 kl 1.74 ±0.01 k 1.6 ±0.1 h
France 9.23 ±0.01 d 10.17 ±0.01 c 9.65 ±0.01 c 10.89 ±0.01 c 9.39 ±0.01 d
Germany 21.74 ±0.01 a 21.31 ±0.01 a 17.39 ±0.01 a 14.45 ±0.01 a 13.6 ±0.1 a
Greece 0.43 ±0.01 r 0.47 ±0.01 r 0.38 ±0.01 r 0.49 ±0.01 p 0.78 ±0.01 ij
Hungary 5.79 ±0.01 f 5.64 ±0.01 g 5.7 ±0.1 f 5.17 ±0.01 g 5 ±0.1 e
Ireland 0.33 ±0.01 s 0.37 ±0.01 s 0.28 ±0.01 r 0.29 ±0.01 s 0.32 ±0.01 jk
Italy 5.12 ±0.01 g 5.75 ±0.01 f 4.85 ±0.01 g 4.04 ±0.01 h 4.37 ±0.01 f
Latvia 0.58 ±0.01 q 0.44 ±0.01 rs 0.3 ±0.1 r 0.4 ±0.1 qr 0.48 ±0.01 jk
Lithuania 1.87 ±0.01 m 1.37 ±0.01 o 1.24 ±0.01 n 1.14 ±0.01 n 1.14 ±0.01 hi
Luxembourg 0.14 ±0.01 uv 0.14 ±0.01 tuv 0.12 ±0.01 t 0.11 ±0.01 t 0.11 ±0.01 k
Malta 0.09 ±0.01 v 0.1 ±0.01 v 0.14 ±0.01 st 0.13 ±0.01 t 0.17 ±0.01 jk
Holland 2.33 ±0.01 l 1.12 ±0.01 p 1.05 ±0.01 o 1.03 ±0.01 u 1.22 ±0.01 hi
Poland 8.44 ±0.01 e 8.34 ±0.01 e 8.74 ±0.01 d 8.72 ±0.01 f 10.28 ±0.01 c
Portugal 0.2 ±0.01 tu 0.19 ±0.01 tu 0.27 ±0.01 rs 0.34 ±0.01 rs 0.4 ±0.1 jk
Romania 0.74 ±0.01 p 1.48 ±0.01 n 1.64 ±0.01 lm 1.41 ±0.01 m 1.56 ±0.01 h
Slovakia 4.91 ±0.01 h 4.34 ±0.01 i 4.43 ±0.01 h 5.12 ±0.01 g 5.61 ±0.01 e
Slovenia 0.42 ±0.01 r 0.36 ±0.01 s 0.65 ±0.01 q 0.42 ±0.01 q 0.33 ±0.01 jk
Spain 4.48 ±0.01 i 5.17 ±0.01 h 7.21 ±0.01 e 9.53 ±0.01 e 10.39 ±0.01 c
Sweden 3.1 ±0.1 k 3.24 ±0.01 j 2.4 ±0.1 j 2.44 ±0.01 j 2.38 ±0.01 g
United Kingdom 9.35 ±0.01 c 9.65 ±0.01 d 8.8 ±0.1 d 10.03 ±0.01 d 10.47 ±0.01 c

Levels not connected by the same letter are significantly different. Data extracted and analyzed from EFSA-ECDC (EFSA and ECDC, 2017).

Figure 1 shows the epidemiological behavior of Salmonella sp. in a histogram with incidence of outbreaks in the population of 28 countries in Europe from 2012 to 2016. The cumulative relative frequency (Fi) curve is presented, which was obtained based on the following formula:

Fi=Nin

Where: Fi= cumulative relative frequency; Ni= cumulative absolute frequency; and n= absolute frequency. The arithmetic mean was calculated with the average number of epidemiological outbreaks obtained from data extracted and analyzed from EFSA-ECDC (2017).

Figure 1 Histogram of incidence of Salmonella sp. in 28 countries in Europe due to consumption of contaminated plant-based foods. Data extracted and analyzed from EFSA-ECDC (2017). 

The histogram showed that the Fi of outbreaks of Salmonella sp. was higher in the last year. In the same period, the epidemiological behavior of Salmonella sp. present in fresh fruits and vegetables was 28 512, 10 684, 10 652, 7 370 and 8 013 cases respectively, with serotypes S. Enteritidis, S. Typhimurium monophasic, S. Typhimurium, S. Infantis and S. Derby (EFSA and ECDC, 2016; EFSA and ECDC, 2017).

Situation of Salmonella sp. in North America

The US. Centers for Disease Control and Prevention (CDC) reported 1.35 million Salmonella sp. infections per year in humans due to consuming contaminated foods, of the total cases 420 end in death (CDC, 2021). From 2010 to April 2021, the epidemiological behavior of salmonellosis in the population of the United States of America (USA), 3 246 reported cases due to the consumption of fresh plant-based foods contaminated with Salmonella sp. were studied. By year, the epidemiological behavior of Salmonella sp. serotypes among the states showed significant statistical differences (p≤ 0.0001) in incidence (Table 3).

Table 3 Incidence and spatial distribution of Salmonella serotypes due to consumption of contaminated plant-based foods by US. state from 2010 to April 2021. 

Year State Food Serotype Incidence (%)
2010 CA y NV Mamey pulp S. Typhi 0.28 ±0.01 o
IL, MO, IN, PA, WI, MA, NY, TN, VA, CT, AR, CA, CO, DC, GA, HI, IA, KY, LA, MD, NE, NV, NJ, NC, OR, SC y SD Alfalfa sprouts S. 1,4, [5], 12 i: 4.31 ±0.01 d
2011 NY Turkish pine nuts S. Enteritidis 1.32 ±0.01 l
TX, IL, NY, CA, GA, WA, AZ, MN, MO, NM, NE, VA, WI, LA, PA, AR, CO, IN, KY, MA, NV, NJ, OH, OK, y TN Papaya S. Agona 3.27 ±0.01 g
OR, WA, CA, AZ, CO, MD, MT, NV, UT y PA Melon S. Panama 0.62 ±0.01 n
2012 WA, HI, NY, TX, IL, DE, ID, ME, MI, MT, NE, NJ, OR y WI Daniela mango S. Braenderup 3.91 ±0.01 e
KY, IL, IN, AL, MO, GA, IA, WI, MI, TN, MS, AR, OH, NC, SC, MN, NJ, PA, TX, FL, MD, MT, OK y VA. Melon S. Typhimurium y S. Newport 8.04 ±0.01 c
2013 CA, AZ, MN, TX, IL, NC, VA, OH, CO, ID, NM, SD, WI, OR, LA, MD, MA y NV Cucumbers S. Saintpaul 2.59 ±0.01 i
2014 MA, NY, PA, CT, RI, MD, NH, ME, OH, VT, MT y VA Soybean sprouts S. Enteritidis 3.54 ±0.01 f
2015 Without registration Cucumbers S. Poona 27.94 ±0.01 b
2016 CO, KS, NE, WY, MN, MO, NY, OR y TX Alfalfa sprouts S. Abony 1.11 ±0.01 m
2017 NJ, NY y PA Maradol papaya S. Urbana 0.22 ±0.01 p
2018 MI, IN, MO, IL, OH, AR, FL, KY y TN Melon S. Adelaide 2.37 ±0.01 k
2019 NY, NJ, CT, MA, PA, FL, DE, RI y TX Papaya S. Uganda 2.5 ±0.01 j
2020 WA, CA, UT, OR, MT, IL, MI, ID, AZ, CO, IA, WY, PA, AK, SD, MN, NY, NV, GA, MO, OH, WI, NJ, NE, VA, ND, FL, MD, TN, ME, NC, MS, IN, HI, KS, KY, NM, RI, WV, AL, AR, CT, DE, MA, TX, NH, OK y SC Onion S. Newport 34.72 ±0.01 a
MN, MI, NY, IA, NJ, WI, PA, VA, MO, CA, CT, IL, KS, KY, MD, OH y VT Peaches S. Enteritidis 3.11 ±0.01 h
2021 FL, CA y TN Plant-based products S. Duisburg 0.15 ±0.01 q

AL= Alabama; AK= Alaska; AZ= Arizona; AR= Arkansas; CA= California; NC= North Carolina; SC= South Carolina; CO= Colorado; CT= Connecticut; ND= North Dakota; SD= South Dakota; DE= Delaware; DC= District of Columbia; FL= Florida; GA= Georgia; HI= Hawaii; ID= Idaho; IL= Illinois; IN= Indiana; IA= Iowa; KS= Kansas; KY= Kentucky; LA= Louisiana; ME= Maine; MD= Maryland; MA= Massachusetts; MI= Michigan; MN= Minnesota; MS= Mississippi; MO= Missouri; MT= Montana; NE= Nebraska; NV= Nevada; NH= New Hampshire; NJ= New Jersey; NY= New York; NM= New Mexico; OH= Ohio; OK= Oklahoma; OR= Oregon; PA= Pennsylvania; RI= Rhode Island; TN= Tennessee; TX= Texas; UT= Utah; VT= Vermont; VA= Virginia; WV= West Virginia; WA= Washington; WI= Wisconsin; WY= Wyoming. Levels not connected by the same letter are significantly different. Data extracted and analyzed from CDC and FDA (2010; 2011a; 2011b; 2011c; 2011d; 2012a; 2012b; 2013; 2014; 2015; 2016; 2017; 2018; 2019; 2020a; 2020b; 2021).

Figure 2 shows the epidemiological behavior of Salmonella sp. in a histogram with the incidence of serotypes and the Fi curve present in the USA from 2010 to April 2021. In this country, the epidemiological impact of Salmonella sp. that occurs throughout history is due to the diversity of serotypes, in addition to the expression and typing of virulence genes by serotype. In 2015 and 2020, the highest peak of epidemiological outbreaks due to Salmonella sp. was observed, it was also observed that, due to health management measures, the disease was flattened and controlled. However, in recent years the incidence and the Fi curve may be indicators of the epidemiological behavior of Salmonella serotypes, which interact with the population due to the consumption of contaminated foods.

Figure 2 Histogram of Incidence of Salmonella sp. serotypes in the United States of North America due to consumption of contaminated plant-based foods. Data extracted and analyzed from CDC and FDA (2010-2021). 

Epidemiological behavior of Salmonella sp. in Mexico

The National Epidemiological Surveillance System of the General Directorate of Epidemiology (SINAVE-DGE), for their acronyms in Spanish of the Secretariat of Health of Mexico, from 2010 to April 202, reported 975 321 infections by Salmonella sp. in humans for consuming contaminated plant-based foods (SINAVE-DGE-SSM, 2021a and 2021b). Table 4 shows by state the epidemiological behavior of Salmonella sp. present in plant-based foods. By year, the incidence of epidemiological behavior of Salmonella sp. showed significant statistical differences (p≤ 0.0001) between states.

Table 4 Epidemiological behavior of Salmonella sp. due to consumption of contaminated plant-based foods by state in Mexico from 2010 to April 2021. 

State Year/incidence (%)
2010 2011 2012 2013 2014 2015 2016 2017 2018 2019 2020 2021
Aguascalientes 2.35 ±0.01n 2.19 ±0.01k 2.25 ±0.01j 2.11 ±0.01m 0.93 ±0.01r 1.48 ±0.01q 1.88 ±0.01m 1.25 ±0.01o 0.62 ±0.01r 0.7 ±0.01q 0.44 ±0.01t 0.48 ±0.01s
Baja California 1.68 ±0.01p 1.49 ±0.01n 1.52 ±0.01o 1.47 ±0.01q 2.06 ±0.01l 2.66 ±0.01j 2.26 ±0.01k 1.36 ±0.01n 1.24 ±0.01n 0.84 ±0.01p 0.8 ±0.01q 0.33 ±0.01t
Baja California Sur 0.35 ±0.01z 0.29 ±0.01w 0.25 ±0.01x 0.27 ±0.01x 0.18 ±0.01y 0.21 ±0.01y 0.23 ±0.01z 0.24 ±0.01w 0.21 ±0.01w 0.16 ±0.01v 0.16 ±0.01yz 0.25 ±0.01u
Campeche 1.28 ±0.01r 1.25 ±0.01q 1.11 ±0.01p 1.65 ±0.01o 1.38 ±0.01o 1.8 ±0.01n 1.55 ±0.01q 0.71 ±0.01r 0.42 ±0.01t 0.09 ±0.01wx 0.15 ±0.01z 0.23 ±0.01u
Coahuila 9.22 ±0.01d 7.74 ±0.01d 8.43 ±0.01d 8.57 ±0.01d 7.86 ±0.01d 4.12 ±0.01f 1.67 ±0.01p 6.14 ±0.01e 2.34 ±0.01i 3.35 ±0.01g 2.2 ±0.01k 1.68 ±0.01k
Colima 0.26 ±0.01 ∞ 0.12 ±0.01x 0.11 ±0.01y 0.13 ±0.01z 0.19 ±0.01y 0.22 ±0.01y 0.18 ±0.01 ∞ 0.16 ±0.01x 0.19 ±0.01w 0.11 ±0.01w 0.2 ±0.01x 0.33 ±0.01t
Chiapas 18.16 ±0.01a 20.35 ±0.01a 21.21 ±0.01a 23.06 ±0.01a 28.55 ±0.01a 26.17 ±0.01a 27.03 ±0.01a 24.31 ±0.01a 25.73 ±0.01a 25.54 ±0.01a 29.99 ±0.01a 32.07 ±0.01a
Chihuahua 5.1 ±0.01e 4.74 ±0.01e 4.17 ±0.01e 4.44 ±0.01e 2.66 ±0.01j 3.27 ±0.01g 3.55 ±0.01f 4.04 ±0.01f 4.18 ±0.01e 4.2 ±0.01f 2.98 ±0.01h 3.11 ±0.01f
Mexico City 0.91 ±0.01v 1.43 ±0.01o 0.64 ±0.01t 0.91 ±0.01s 0.55 ±0.01w 0.55 ±0.01u 0.62 ±0.01w 0.44 ±0.01u 0.98 ±0.01p 1 ±0.01o 0.71 ±0.01r 0.85 ±0.01p
Durango 0.02 ±0.01 δ 0.03 ±0.01y 0.03 ±0.01z 0.04 ±0.01 ∞ 0.12 ±0.01z 0.01 ±0.01z 0.04 ±0.01 β 0.02 ±0.01y 0.03 ±0.01x 0.01 ±0.01y 0.03 ±0.01 ∞ 0.05 ±0.01w
Guanajuato 0.51 ±0.01y 0.53 ±0.01v 0.53 ±0.01u 0.87 ±0.01t 0.66 ±0.01u 0.56 ±0.01u 1.09 ±0.01r 1.15 ±0.01p 0.95 ±0.01p 1.35 ±0.01n 1.25 ±0.01p 1.32 ±0.01n
Guerrero 3.47 ±0.01i 3.04 ±0.01i 3.49 ±0.01h 3.73 ±0.01g 0.87 ±0.01s 1.64 ±0.01p 2.2 ±0.01l 1.8 ±0.01m 1.81 ±0.01l 1.76 ±0.01m 1.96 ±0.01m 1.55 ±0.01m
Hidalgo 0.11 ±0.01 β 0.14 ±0.01x 0.11 ±0.01y 0.23 ±0.01y 0.3 ±0.01x 0.26 ±0.01x 0.27 ±0.01y 0.26 ±0.01vw 0.32 ±0.01u 0.34 ±0.01t| 0.19 ±0.01xy 0.23 ±0.01u
Jalisco 4.51 ±0.01f 4.42 ±0.01f 3.76 ±0.01g 3.47 ±0.01h 1.88 ±0.01n 3.1 ±0.01h 3.04 ±0.01g 2.98 ±0.01i 2.37 ±0.01i 2.17 ±0.01k 3.28 ±0.01g 2.82 ±0.01g
State of México 2.75 ±0.01l 2.41 ±0.01j 2.09 ±0.01k 1.94 ±0.01n 2.49 ±0.01k 2.53 ±0.01k 2.29 ±0.01k 1.89 ±0.01l 1.91 ±0.01k 2.25 ±0.01j 2.37 ±0.01i 2.02 ±0.01i
Michoacán 2.55 ±0.01m 2.18 ±0.01k 1.94 ±0.01l 1.55 ±0.01p 1.96 ±0.01m 2.27 ±0.01m 2.61 ±0.01j 2.18 ±0.01j 2.36 ±0.01i 2.47 ±0.01i 2.26 ±0.01j 1.86 ±0.01j
Morelos 0.51 ±0.01y 0.75 ±0.01t 0.46 ±0.01v 0.33 ±0.01w 0.63 ±0.01uv 0.49 ±0.01v 0.28 ±0.01y 0.24 ±0.01w 0.25 ±0.01v 0.21 ±0.01u 0.19 ±0.01xy 0.01 ±0.01x
Nayarit 1.06 ±0.01u 1.04 ±0.01r 1.71 ±0.01m 2.35 ±0.01l 4.35 ±0.01f 4.7 ±0.01e 2.94 ±0.01h 2.02 ±0.01k 3.3 ±0.01f 5.01 ±0.01e 5.02 ±0.01e 2.55 ±0.01h
Nuevo León 1.1 ±0.01t 1.3 ±0.01p 1.13 ±0.01p 0.65 ±0.01v 1.05 ±0.01q 0.4 ±0.01w 0.61 ±0.01w 0.5 ±0.01t 0.49 ±0.01s 0.42 ±0.01s 0.29 ±0.01w 0.16 ±0.01v
Oaxaca 2 ±0.01o 1.99 ±0.01l 2.06 ±0.01k 2.08 ±0.01m 1.99 ±0.01m 1.71 ±0.01o 1.78 ±0.01o 1.35 ±0.01n 2.06 ±0.01j 2.14 ±0.01k 2.04 ±0.01l 1.63 ±0.01l
Puebla 4.43 ±0.01h 4.39 ±0.01f 4.05 ±0.01f 4.24 ±0.01f 6.57 ±0.01e 7.29 ±0.01d 6.55 ±0.01d 6.27 ±0.01d 6.17 ±0.01d 5.46 ±0.01d 5.45 ±0.01d 5.78 ±0.01d
Querétaro 0.68 ±0.01x 0.66 ±0.01u 0.42 ±0.01w 0.24 ±0.01xy 0.12 ±0.01z 0.29 ±0.01x 0.4 ±0.01x 0.28 ±0.01v 0.19 ±0.01w 0.06 ±0.01x 0.03 ±0.01 ∞ 0.03 ±0.01wx
Quintana Roo 3.16 ±0.01j 3.46 ±0.01h 3.43 ±0.01i 2.9 ±0.01j 2.86 ±0.01i 2.44 ±0.01l 2.94 ±0.01h 3.61 ±0.01g 3.14 ±0.01g 1.97 ±0.01l 1.52 ±0.01o 1.86 ±0.01j
San Luis Potosí 0.69 ±0.01x 0.83 ±0.01s 0.71 ±0.01s 0.88 ±0.01st 1.11 ±0.01p 1.29 ±0.01r 0.86 ±0.01t 1.15 ±0.01p 1.34 ±0.01m 1.02 ±0.01o 0.69 ±0.01r 0.46 ±0.01s
Sinaloa 4.47 ±0.01g 4.25 ±0.01g 4.04 ±0.01f 2.61 ±0.01k 3.71 ±0.01g 2.94 ±0.01i 2.78 ±0.01i 3.38 ±0.01h 2.95 ±0.01h 2.98 ±0.01h 4.07 ±0.01f 4.4 ±0.01e
Sonora 1.19 ±0.01s 1.25 ±0.01q 1.06 ±0.01q 0.62 ±0.01v 0.76 ±0.01t 0.97 ±0.01s 1 ±0.01s 0.81 ±0.01q 0.65 ±0.01r 0.36 ±0.01t 0.37 ±0.01v 0.65 ±0.01q
Tabasco 9.8 ±0.01c 10.88 ±0.01c 10.21 ±0.01c 11.34 ±0.01b 8.6 ±0.01c 10.17 ±0.01c 10.53 ±0.01c 9.64 ±0.01c 9.89 ±0.01c 9 ±0.01c 7.22 ±0.01c 6.85 ±0.01c
Tamaulipas 2.86 ±0.01k 3.04 ±0.01i 3.74 ±0.01g 3.11 ±0.01i 3.55 ±0.01h 2.94 ±0.01i 3.99 ±0.01e 3.58 ±0.01g 3.14 ±0.01g 2 ±0.01l 1.63 ±0.01n 1.85 ±0.01j
Tlaxcala 0.77 ±0.01w 0.68 ±0.01u 0.84 ±0.01r 0.79 ±0.01u 0.62 ±0.01v 0.79 ±0.01t 0.71 ±0.01u 0.65 ±0.01s 0.82 ±0.01q 0.62 ±0.01r 0.4 ±0.01uv 0.55 ±0.01r
Veracruz 12.01 ±0.01b 11.03 ±0.01b 12.35 ±0.01b 10.24 ±0.01c 9.8 ±0.01b 10.73 ±0.01b 11.62 ±0.01b 15.07 ±0.01b 17.55 ±0.01b 20.34 ±0.01b 21.04 ±0.01b 22.73 ±0.01b
Yucatán 0.5 ±0.01y 0.5 ±0.01v 0.56 ±0.01u 1.06 ±0.01r 0.52 ±0.01w 0.56 ±0.01u 0.67 ±0.01v 1.23 ±0.01o 1.24 ±0.01n 1.35 ±0.01n 0.43 ±0.01tu 0.3 ±0.01t
Zacatecas 1.54 ±0.01q 1.61 ±0.01m 1.61 ±0.01n 2.09 ±0.01m 1.14 ±0.01p 1.46 ±0.01q 1.82 ±0.01n 1.26 ±0.01o 1.14 ±0.01o 0.71 ±0.01q 0.59 ±0.01s 1.03 ±0.01o

Levels not connected by the same letter are significantly different. Data extracted and analyzed from SINAVE-DGE-SSM (2021a and 2021b).

Figure 3 shows the epidemiological behavior of Salmonella sp. in a histogram with incidence of salmonellosis and the Fi curve present in Mexico from 2010 to 2021. In the histogram, the Fi of Salmonella sp. outbreaks declined 43.75% in 2020 with respect to 2019. The epidemiological behavior in the first four-month period of 2021, the percentage of cases presented a trend of 13.24% in contrast to 2019, Chiapas, Veracruz, Tabasco, Durango, Puebla and Coahuila were the states with the highest incidence.

Figure 3 Histogram of Incidence of Salmonella sp. in Mexico due to consumption of contaminated plant-based foods. Data extracted and analyzed from SINAVE-DGE-SSM (2021a and 2021b). 

The epidemiological behavior of Salmonella sp. among regions of Africa, Europe and North America presented incidences of 4.08, 30.82 and 65.1%, respectively. Figure 4 shows the histogram of salmonellosis incidence in the population by region, due to the consumption of contaminated plant-based foods, plus the Fi curve (Reddy et al., 2010; CDC-FDA, 2011c; EFSA-ECDC, 2017; SINAVE-DGE-SSM, 2021a and 2021b).

Figure 4 Histogram of Incidence of Salmonella spp. among the population of the regions of Africa, Europe and North America, due to consumption of contaminated plant-based foods. Data extracted and analyzed from Reddy et al. (2010), CDC-FDA (2011c), EFSA-ECDC (2017), SINAVE-DGE-SSM (2021a and 2021b). 

Conclusions

The epidemiological behavior of Salmonella enterica in plant-based foods showed the highest prevalence (49.9%) in the North African region. On the European continent, the epidemiological status of Salmonella sp. increased in 2015. In 2021, the states of the United States and Mexico showed a radical decrease in the epidemiological curve. Among the regions of Africa, Europe and North America, the epidemiological behavior of Salmonella sp. in plant-based foods presented incidences of 4.08, 30.82 and 65.1% respectively, due to the consumption of contaminated plant-based foods.

Acknowledgements

To the National Council of Science and Technology (CONACYT), for its acronym in Spanish for the granting of a national scholarship.

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Received: January 01, 2023; Accepted: January 27, 2023

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