Nativa, Sinop, v. 11, n. 1, p. 90-95, 2023.

Pesquisas Agrárias e Ambientais

DOI: https://doi.org/10.31413/nativa.v11i1.13592

ISSN: 2318-7670

Hygienic-sanitary quality of lettuce (

Lactuca sativa

) and arugula (

Eruca

sativa

) produced in an organic farm system in Cuiabá, MT, Brazil

Elisana Cecilia Nunes BUENO1, Andréia Jesuíno QUADROS2, Adelino da CUNHA NETO1,2 ,

Maxsueli Aparecida Moura MACHADO2, Vinicius da Silva CASTRO3,

Eduardo Eustáquio de Souza FIGUEIREDO1,2,3*

1Faculty of Nutrition, Federal University of Mato Grosso, Cuiabá, MT, Brazil.

2Postgraduate Program in Nutrition, Food and Metabolism, Federal University of Mato Grosso, Cuiabá, MT, Brazil.

3Postgraduate Animal Science Program, Federal University of Mato Grosso, MT, Brazil.

*E-mail: eduardofigueiredo@hotmail.com

Submitted on 03/25/2022; Accepted on 02/03/2023; Published on 03/30/2023

ABSTRACT: Demand for organic food has increased as a result of awareness of the health risks posed by the

presence of chemical residues. In this context, this study aimed to verify the safety of lettuce (Lactuca sativa) and

arugula (Eruca sativa) produced organically in the metropolitan region of Cuiabá, MT, Brazil, and identify the

main microbiological contamination sources of this production system. Fifty-five samples, 10 lettuces and 10

arugula, were collected in a farm and supermarket, in addition to five samples of each agricultural adjuvant used

in the production system (irrigation water, vegetable and animal fertilizers). No Salmonella spp. was detected,

although thermotolerant coliforms above the maximum acceptable limit established by the Commission on

Microbiological Specifications for Foods (ICMSF) were observed in 90% (9/10) and 50% (5/10) of the farm

arugula and lettuce samples, 20% (2/10) and 10% (1/10) of the supermarket arugula and lettuce samples, 60%

of animal and vegetable fertilizers (6/10) and 40% (2/5) of irrigation water samples. Over half of the vegetable

samples analyzed herein were, thus, unfit for consumption, indicating the relatively high influence of system

inputs on the hygienic-sanitary quality of the arugula and lettuce produced in the investigated organic farm.

Keywords: fertilization; organic farming; sanitary quality; contamination.

Qualidade higiênico-sanitária de alface (

Lactuca sativa

) e rúcula (

Eruca sativa

)

produzidas em sistema de produção orgânica em Cuiabá, MT, Brasil

RESUMO: A procura por alimentos orgânicos tem aumentado devido a conscientização sobre os riscos à

saúde decorrentes da presença de resíduos químicos. Nesse contexto, este estudo teve como objetivo verificar

a segurança de alface (Lactuca sativa) e rúcula (Eruca sativa) produzidas organicamente na região metropolitana

de Cuiabá, MT, Brasil, e identificar as principais fontes de contaminação microbiológica desse sistema de

produção. Cinquenta e cinco amostras, sendo 10 de alfaces e 10 de rúculas foram coletadas em uma fazenda e

supermercado, além de quinze amostras de adjuvantes agrícola utilizados no sistema de produção. Nenhuma

Salmonella spp. foi detectada, embora coliformes termotolerantes acima do limite máximo aceitável estabelecido

pela Comissão de Especificações Microbiológicas para Alimentos (ICMSF) tenham sido observados em 90%

(9/10) e 50% (5/10) das amostras de rúcula e alface da fazenda, 20 % (2/10) e 10% (1/10) das amostras de

rúcula e alface de supermercado, 60% de fertilizantes animais e vegetais (6/10) e 40% (2/5) de amostras de

água de irrigação. Mais da metade das amostras de hortaliças aqui analisadas estavam, portanto, impróprias para

consumo, indicando a influência relativamente alta dos insumos do sistema na qualidade higiênico-sanitária da

rúcula e alface produzidas na fazenda orgânica investigada.

Palavras-chave: fertilização; agricultura orgânica; qualidade sanitária; contaminação.

1. INTRODUCTION

Consumers are becoming increasingly attentive to the

vegetable cultivation origin and socio-environmental aspects

instead of only availability, appearance, and economic value

(ECHER et al., 2016). An 18.5% increase in the demand for

organic products, considered significantly healthier, was

noted, for example, in Brazil in 2017 (BRASIL, 2017). In the

same year, the Brazilian vegetable market generated US$

5,084.05 million. Lettuce is the most important vegetable in

Brazil (ECHER et al., 2016), and the last agricultural census

carried out by the Brazilian Institute of Geography and

Statistics (Instituto Brasileiro de Geografia e Estatística - IBGE)

indicated a total of 108,382 t year-1 of lettuce produced in the

country, with 7,062 t year-1 produced in the Midwest region

and 2,114 t year-1 in the state of Mato Grosso alone (BRASIL

2017; IBGE, 2017).

Leafy vegetables can be produced by both conventional

and organic production systems, with the latter employing no

phytosanitary products for pest and disease control.

However, the concept of organic products is very complex,

covering management, ecology and social aspects involved in

product marketing (RODRIGUES et al., 2009; BRASIL,

2017).

Several factors can contribute to the origin of pathogens

in fresh vegetables, such as fertilizers from plant compost and

animal, which waste are commonly used in organic

Bueno et al.

Nativa, Sinop, v. 11, n. 1, p. 90-95, 2023.

production systems, and may contribute to the presence of

intestinal parasites (helminths and protozoa), viruses and

bacteria, which may, in turn, contaminate foodstuffs and lead

to foodborne illnesses in consumers (BARKER-REID et al.,

2009; JOHANNESSEN et al., 2004). Other factors include

the use of animal or human manure, the presence of insects,

soil dust contaminated with animals and human feces

(BARKER-REID et al., 2009; POMA et al., 2016), rain,

irrigation and post-harvest washing water, ice, equipment

and, finally, handler hygiene during the harvesting,

processing and transportation steps (JOHANNESSEN et al.,

2002; JUNG et al., 2014).

A total of 83 foodborne disease outbreaks associated to

fresh products have been reported in the United States of

America from 2000 to 2017, ten triggered by the Shiga-toxin

producing Escherichia coli (STEC) serotype and tree by the

Enteritidis, Newport and Paratyphi B serotypes Salmonella,

both microorganisms found in contaminated lettuce

(CARSTENS et al., 2019). Foodborne outbreaks triggered by

the presence of these microorganisms in leafy vegetables

have also been reported from 1973 to 2016 (HERMAN et

al., 2015; WADAMORI et al., 2017; JOHNSON, 2019;

TURNER et al., 2019). Studies evaluating data associated to

foodborne outbreaks from 2000 to 2018 in Brazil report the

presence of both Salmonella spp. coliforms and E. coli in fruits

and vegetables (ELIAS et al., 2018; FINGER et al., 2019).

These microorganisms can cause conditions ranging from

enteritis to systemic diseases, mainly affecting low-income

populations in developing countries and resulting in public

health and economy impacts (BENNETT et al., 2018).

Monitoring the hygienic conditions of vegetable production

is, thus, recommended, which can be carried out indirectly by

microbiological evaluations (BERGER et al., 2010).

Contamination in organic production systems can occur

due to the use of contaminated irrigation water and fertilizers,

as well as in the harvest, transport, and handling stages and

during marketing. Previous microbiological studies have, in

fact, indicated the presence of E. coli in Brazil even in organic

vegetables (MAFFEI et al., 2013), Norway (LONCAREVIC

et al., 2005), and Zambia (NGUZ et al., 2005). In this context,

this study aimed to verify the microbial safety of organic

lettuce (Lactuca sativa) and arugula (Eruca sativa) produced in

Cuiabá, in the state of Mato Grosso, Brazil, by assessing the

main microbiological contamination sources in organic

production systems.

2. MATERIAL AND METHODS

2.1. Sample collection

Samplings were performed in an organic leafy vegetable

farm that produces lettuce, arugula, chives, parsley, cilantro,

and vegetables such as carrots, cherry tomatoes, beets and

broccoli, located in the rural area of the city of Cuiaba,

approximately 12 km from the capital. The farm is certified

for organic production by an accredited Brazilian National

Institute of Metrology, Quality and Technology (Instituto

Nacional de Metrologia, Qualidade e Tecnologia - INMETRO)

company. A total of 10 lettuces and 10 arugulas packaged for

sale directly on the farm, as well as 10 samples of each

vegetable sold in supermarkets and five samples of irrigation

water, vegetable fertilizer and animal fertilizer (chicken waste)

each were obtained, totaling fifty-five samples. The samples

were packed in first-use plastic bags, placed on ice in an

isothermal box and transported to the Laboratory of

Molecular Microbiology of Food (LabMMA) belonging to

the Faculty of Nutrition at the Federal University of Mato

Grosso (UFMT).

2.2. Microbiological analyses

Microbiological analyses were performed according to

American Public Health Association (APHA), these

methodologies were applied for total and thermotolerant

coliform determinations (SILVA et al., 2017). The

International Organization for Standardization (ISO) 6579

methodology was applied for Salmonella spp. determinations

(ISO, 2002). For coliforms, the same amount was diluted in

225 mL of 0.1% peptone saline solution followed by

subsequent dilutions up to 10-3. Total (35 °C) and

thermotolerant (45 °C) coliforms were determined by the

multiple tube method, through the determination of the most

probable number (MPN g– 1). Briefly, 1 mL aliquot dilutions

were inoculated in a series of three tubes containing 9 mL of

Lauryl Sulfate Tryptose (LST) broth (Himedia®, Mumbai,

India) and incubated at 35 ± 1 °C for 24 - 48 hours. Samples

displaying turbidity and gas formation were considered

positive (Silva, Junqueira, Silveira, Taniwaki, & Gomes, 2017)

and subsequently inoculated in Brilliant Green Bile (VB)

broth (Himedia®, Mumbai, India) and incubated at 35 ± 1

°C for 24 - 48 h, and inoculated in Escherichia coli broth (EC)

at 44.5 ± 0.5 °C for 24 - 48 h.

Concerning Salmonella sp., 25 g of each sample were

inoculated in 225 mL of 1% Buffered Peptone Water

(Oxoid®, Basingstoke, United Kingdom), incubated at 35 ±

1 °C for 24 h. Subsequently, 1 mL and 0.1 mL aliquots were

mixed with Tetrathionate and Rappaport-Vassiliadis broths

(Oxoid®, Basingstoke, United Kingdom), and incubated at

35 ± 1 °C and 42 °C for 24 h respectively. Aliquots were then

plated in (BGA) Brilliant Green Agar (Himedia®, Mumbai,

India) and (XLD) Xylose Lysine Deoxycholate (Himedia®,

Mumbai, India) Agar and incubated at 35 ± 1 °C for 24 h.

Typical translucent colonies with a red halo in BGA and a

black center in XLD agar were subjected to biochemical tests

(TSI-Triple Sugar Iron Agar, LIA-Lysine Iron Agar and Urea

Agar [Christensen] - Himedia®, Mumbai, India) for the

presumptive confirmation of Salmonella spp. (ISO, 2002).

Regarding reference standards, 1 Log MPN/100 mL was

set as the maximum acceptable limit for thermotolerant

coliforms in irrigation water, 2.30 Log MPN g-1 for the

evaluated fresh leafy vegetables, and 2 Log MPN g-1 for

fertilizer samples. The absence of Salmonella spp. is indicative

of satisfactory quality according to the International

Commission for Microbiological Specifications for Food

(ICMSF, 2015).

3. RESULTS

No Salmonella spp. was detected in any of the 55

vegetable, water or fertilizer samples obtained from the

organic leafy vegetable production farm located in the

metropolitan region of Cuiabá, MT, Brazil (Tables 1 and 2).

Acceptable coliform counts were detected in the lettuce,

arugula and irrigation water samples (ICMSF, 2015). These

counts were the highest in 90% of the arugula farm samples,

followed by 50% of the lettuce farm samples (Table 1), in

contrast with 10% and 20% supermarket lettuce and arugula

samples (Table 1) and 40% irrigation water samples obtained

on days 1 and 3. On the other hand, 60% of the organic

fertilizers exhibited thermotolerant coliforms above the

maximum recommended limit established by the ICMSF

(2015) (Table 2).

Hygienic-sanitary quality of lettuce (Lactuca sativa) and arugula (Eruca sativa) produced in an organic …

Nativa, Sinop, v. 11, n. 1, p. 90-95, 2023.

Table 1. Total coliforms (35 °C), thermotolerant coliforms (45 °C) and Salmonella spp. in arugula (Eruca sativa) and lettuce (Lactuca sativa)

samples produced in an organic system in the metropolitan region of Cuiabá, Mato Grosso, Brazil, obtained directly from the vegetable

farm and from supermarkets.

Tabela 1. Coliformes totais (35 °C), coliformes termotolerantes (45 °C) e Salmonella spp. em amostras de rúcula (Eruca sativa) e alface (Lactuca

sativa) produzidas em sistema orgânico na região metropolitana de Cuiabá, Mato Grosso, Brasil, obtidas diretamente da horta e de

supermercados.

Harvest

days Samples

Farm samples

Supermarket

samples

Coliforms (Log

MPN g

-1

)

Salmonella

spp.

in 25 g-1

Coliforms (Log

MPN g

-1

)

Salmonella

spp.

in 25 g-1

35 °C

45 °C

35 °C

45 °C

Lettuce 1

≥3.04

Absent

1.60

Absent

Lettuce 2

≥3.04

Absent

0.093

Absent

Arugula 1

≥3.04

Absent

2.30

0.22

Absent

Arugula 2

≥3.04

Absent

1.90

0.091

Absent

Lettuce 1

≥3.04

2.04

Absent

3.00

Absent

Lettuce 2

≥3.04

Absent

2.70

0.40

Absent

Arugula 1

2.04

≥3.04

Absent

≥3.04

Absent

Arugula 2

≥3.04

Absent

≥3.04

0.48

Absent

Lettuce 1

≥3.04

2.04

Absent

2.30

1.60

Absent

Lettuce 2

≥3.04

Absent

0.51

0.032

Absent

Arugula 1

≥3.04

Absent

0.51

0.09

Absent

Arugula 2

≥3.04

2.32

Absent

2.20

0.51

Absent

Lettuce 1

2.04

2.32

Absent

2.70

0.66

Absent

Lettuce 2

2.04

2.17

Absent

2.20

Absent

Arugula 1

2.04

≥3.04

Absent

≥3.04

0.091

Absent

Arugula 2

≥3.04

Absent

≥3.04

Absent

Lettuce 1

2.66

<0.3

Absent

2.10

0.32

Absent

Lettuce 2

≥3.04

2.17

Absent

≥3.04

3.00

Absent

Arugula 1

≥3.04

Absent

≥3.04

2.30

Absent

Arugula

2.04

2.17

Absent

≥3.04

0.51

Absent

MPN = Most Probable Number. NMP = Número Mais Provável.

Table 2. Total coliforms (35 °C), thermotolerant coliforms (45 °C) and detection of Salmonella spp. in vegetable and animal origin (chicken

waste) fertilizers employed in an organic vegetable farm in the metropolitan region of Cuiabá, Mato Grosso, Brazil.

Tabela 2. Coliformes totais (35 °C), coliformes termotolerantes (45 °C) e detecção de Salmonella spp. em fertilizantes de origem vegetal e

animal (resíduos de frango) empregados em horta orgânica na região metropolitana de Cuiabá, Mato Grosso, Brasil.

Fertilizer products / Days

Coliforms Log

MPN g

-1

Salmonella

spp. in 25 g

-1

35 °C

45 °C

Vegetable fertilizer (Day 1)

≥3.04

2.04

Absent

Animal fertilizer (Day 1)

≥3.04

2.04

Absent

Vegetable fertilizer (Day 2)

≥3.04

Absent

Animal fertilizer (Day 2)

≥3.04

2.17

Absent

Vegetable fertilizer (Day 3)

≥3.04

2.17

Absent

Animal fertilizer (Day 3)

≥3.04

1.63

Absent

Vegetable fertilizer (Day 4)

2.04

1.87

Absent

Animal fertilizer (Day 4)

≥3.04

2.66

Absent

Vegetable fertilizer (Day 5)

2.04

1.17

Absent

Animal

fertilizer (Day 5)

2.66

1.44

Absent

MPN = Most Probable Number. NMP = Número Mais Provável.

4. DISCUSSION

Organic vegetable production systems fertilized with

improperly composted animal manure can transmit E. coli, a

thermotolerant coliform, to the soil and to leafy vegetables

(LUNA-GUEVARA et al., 2019). In the present study, 60%

of the samples were positive for thermotolerant coliforms.

This corroborates other studies performed in Brazil, for

example, in one study, 40% of control lettuce samples and

20% of lettuce samples fertilized with chicken and bovine

manure animals tested positive for thermotolerant coliforms

(ABREU et al., 2010). In another assessment, Arbos et al.

(2010) reported 20% (1/5) of contaminated organic lettuce

in the city of Curitiba, in the state of Paraná, while Niguma

et al. (2017) reported 12.5% (5/40) of organic samples

positive for thermotolerant coliforms in the city of Londrina,

also in the state of Paraná. This group of coliforms was also

reported in 19.3% (12/62) of lettuce samples and 35.7%

(5/14) of arugula samples produced in the region of

Campinas, in the state of São Paulo, in conventional farms

(SIMÕES et al., 2001), as well as in 32.5% of lettuce and

coriander samples produced in conventional farms marketed

in Santo Antônio de Jesus, in the state of Bahia (SILVA et al.,

2016). Thus, it is clear that contaminated fertilizers can

contribute to fecal vegetable contamination, confirmed by

our findings and in accordance with previous studies.

Furthermore, irrigation water may have also influenced

arugula and lettuce sample contamination from days 1 and 3

(Table 1), while the applied vegetable fertilizer significantly

Bueno et al.

Nativa, Sinop, v. 11, n. 1, p. 90-95, 2023.

affected a higher number of samples, i.e., two arugula

samples from days 1, 2 and 3 and two lettuce samples from

day 1 and one from days 2 to 3 the most noteworthy (Table

1). Animal fertilizer, however, contributed to the

contamination of the two arugula samples collected on days

1, 2 and 4, and two lettuces samples obtained on day 1 and

one sample obtained on days 2 and 4 (Table 1). Both

fertilizers contained thermotolerant coliform contamination

on days 2 and 4 (Tables 1 and 2). These data refer to the

samples collected on the farm. However, the limited data

reported herein does not allow for a conclusive relationship

between positive thermotolerant coliform vegetable samples

and fertilizer and irrigation water contamination, in contrast

to that reported by Loncarevic et al. (2005) in Norway.

However, the number of contaminated irrigation water

samples was lower than that reported by Abreu et al. (2010),

of 100%, perhaps due to the low presence of humans and

domestic animals near the irrigation water collection point,

similarly to that reported by Araújo et al. (2015) for irrigation

water collection points in a stream denominated Córrego Sujo,

in the state of Rio de Janeiro, Brazil. The inadequate

management of manure employed as fertilizer can also

influence thermotolerant coliform soil and water

contamination, subsequently affecting vegetable production

(CADONA et al., 2016).

Thermotolerant coliform counts in the investigated water

samples were mostly below the maximum acceptable limits,

while most fertilizer samples (animal and vegetable)

presented counts above the maximum established limits

(ICMSF, 2015). Thus, good agricultural practices in the

handling and use of water and fertilizer inputs seem to not

have been followed on the investigated property, as following

the Good Agricultural Practices (GAP) program results in

low or absent counts of this group of organisms (NIGUMA

et al., 2017). At the assessed property, vegetables are

harvested and sold directly to the final consumer. Thus, if

good practices are not applied in the local vegetable

production chain, comprising production, harvest, hygiene,

and distribution steps, the produced vegetables may

represent consumer health risks (SOTO et al., 2018).

Low thermotolerant coliform counts were observed in

the supermarket lettuce and arugula samples (Table 1), lower

than those detected in the previous farm planting, harvesting,

and distribution stages. Leafy vegetable storage and transport

under well-controlled temperature conditions (4 °C) may

control total and thermotolerant coliform counts (ALLEN et

al., 2013; FAOUR-KLINGBEIL et al., 2016), which may

account for this finding. Furthermore, the arugula

supermarket samples contained roots, although no visible

dirt was verified, demonstrating thorough cleaning of this

product.

Organic product production has increased in recent years,

alongside challenges associated to better production and

good quality (BRASIL, 2017). This can be achieved by

controlling factors that can contribute to pathogen

transmission to fresh vegetables, such as the presence of

insects, environmental soil and water quality, and, finally,

adequate equipment and product handling and marketing

(JOHANNESSEN et al., 2002; JOHANNESSEN et al.,

2004; BARKER-REID et al., 2009; JUNG et al., 2014;

POMA et al., 2016).

5. CONCLUSIONS

The microbiological quality of organic lettuce and arugula

marketed in the metropolitan region of Cuiabá, Brazil, is not

entirely satisfactory, as high thermotolerant coliform counts

were detected. Therefore, it seems that good practices for the

production of agricultural products are not being followed,

and vegetable contamination by potential pathogens may

consequently represent a risk to consumer health, even

though Salmonella spp. was absent from all samples, including

animal fertilizer products.

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Author Contributions:

E.C.N.B – conceptualization, methodology, research and data

collection, writing (original draft); A.J.Q - conceptualization,

methodology, investigation and data collection, writing (original

draft); A.C.N - methodology, research supervision, writing

(proofreading and editing); V.S.C - methodology, statistical

treatment, writing (critical review of the work), translation; E.E.S.F

– conceptualization, acquisition of funding, coordination, research

planning, writing (critical review of the work).

Institutional Review Board Statement:

Not applicable.

Informed Consent Statement:

Not applicable.

Data Availability Statement:

The research data will be made available via e-mail to the

corresponding author or responsible for the research project.

Conflicts of Interest:

We inform that there was no scientific, economic, social (among

others) conflict of interest during the development of the research

and preparation of the article.