Available via license: CC BY 4.0
Content may be subject to copyright.
http://www.visaemdebate.incqs.ocruz.br/ Vigil. sanit. debate 2017;5(2):127-140 | 127
REVISÃO
https://doi.org/10.22239/2317-269x.00779
Microbiological safety aspects of mangoes (Mangifera
indica) and papayas (Carica papaya): a mini-review
Aspectos de segurança microbiológica de manga (Mangifera indica)
e papaya (Carica papaya): mini revisão
Ana Lúcia PenteadoI,*
Empresa Brasileira de Pesquisa
Agropecuária (Embrapa),
Jaguariúna, SP, Brasil
*E-mail: analucia.penteado@embrapa.br
Recebido: 20 maio 2016
Aceito: 24 mar 2017
ABSTRACT
This review describes several aspects related to microbiological safety in mangoes and
papayas, such as incidence, outbreaks, internalisation and growth/survival of bacterial
pathogens. Mangoes and papayas are often served sliced in food establishments in fresh
pieces at salad bars, deli counters and as pulp juice. In general, these products do not
undergo any process to eliminate pathogenic microorganisms before consumption, and
a long shelf life could theoretically provide time for these microorganisms to multiply
without aecting the organoleptic qualities of the fruit, thereby increasing the risks
of food-borne illness. The data presented in this review show that low temperatures
can impede microbial growth, but not completely inhibit such growth in mangoes and
papayas. Highest growth rates were observed in the range between 22 and 37oC. In the
last 20 years, several outbreaks of salmonellosis caused by these fruits or by food made
with these fruits have been reported. The control of the temperature in the fruit washing
water is important to prevent the internalisation of Salmonella spp. The implementation
of strategies such as Good Agricultural Practices, Good Manufacturing Practices and
Hazard Analysis Critical is important, as these methods can eliminate or signicantly
reduce microbial contamination.
KEYWORDS: Mango; Papaya; Safety; Pathogens; bacterium
RESUMO
Esta revisão descreve diversos aspectos relacionados à segurança microbiológica em manga
e mamão papaya como; incidência, surtos, internalização e crescimento/sobrevivência
de patógenos bacterianos nestas frutas. Mangas e papayas são frequentemente servidas
fatiadas em estabelecimentos alimentícios como pedaços frescos, em misturas para
saladas, expostas em balcões e como polpas de frutas. No geral, estes produtos não
passam por qualquer processo para eliminar microrganismos patogênicos antes do seu
consumo e uma vida longa de prateleira poderia teoricamente fornecer tempo para que
estes microrganismos se multipliquem sem afetar as qualidades organolépticas destas
frutas e assim aumentar o risco de doenças de origem alimentar. Os dados apresentados
nesta revisão mostram que baixas temperaturas podem diminuir o crescimento de
microrganismos mas não inibi-los em mangas e papayas. Os melhores crescimentos foram
observados na faixa de 22–37oC. Nos últimos 20 anos diversos surtos de salmonelose nestas
frutas ou produtos feitos com as mesmas foram relatados. O controle da temperatura da
água de lavagem de frutas é importante para prevenir a internalização de Salmonella spp.
A implementação de estratégias como Boas Práticas Agrícolas, Boas Práticas de Produção
e Análise Crítica de Pontos de Controle são importantes já que podem eliminar ou reduzir
signicantemente a contaminação microbiana.
PALAVRAS- CHAVE: Manga; Papaya; Segurança; Patógenos; bactérias
http://www.visaemdebate.incqs.ocruz.br/ Vigil. sanit. debate 2017;5(2):127-140 | 128
Penteado AL. Microbiological safety aspects of mango and papaya
INTRODUCTION
The consumption of fresh produce, an important source of nutri-
ents, vitamins and bre for humans, is steadily increasing world-
wide. The World Health Organisation (WHO) and the Food and
Agricultural Organisation (FAO) recommend a minimum of 400 g
of fruit and vegetables per day for the prevention of chronic
diseases, such as heart disease, cancer, diabetes and obesity,
and for the prevention and alleviation of several micronutrient
deciencies, especially in less developed countries1,2.
From 1980 to 2004, global fruit and vegetable production
increased. This resulted in higher food industry prots and
export rates, but also in more frequent disease outbreaks and
spoilage problems2,3,4.
Mango (Mangifera indica Linn) and papaya (Carica papaya) are
tropical fruits of great economic importance and some of the
most commonly eaten fruits in tropical countries around the
world5. According to the FAO in 2013, India leads the world
production of papaya with 5,544,000,00 tonnes, followed by
Brazil (1,582,638,000 tonnes), Nigeria (773,000,000 tonnes) and
Mexico (764,514,000 tonnes). India also has the highest mango
production (18,002,000,000 tonnes), followed by Indonesia
(2,058,607,000 tonnes), Mexico (1,901,871,000 tonnes), Pakistan
(1,658,562,000 tonnes) and Brazil (1,163,000,000 tonnes)6,7.
At all stages of production, harvesting and processing, fruits
and vegetables can become contaminated with microorganisms
capable of causing human diseases8.
Fresh produce, such as fruit and salad, is often consumed raw
without undergoing processing, such as cooking, to inactivate
harmful microorganisms. In addition, further cutting, slicing or
peeling causes tissue damage, which releases nutrients and facil-
itates microbial growth, putting consumers at risk of infection
by contaminating organisms9,10. Mangoes and papayas are often
served sliced in food establishments at salad bars and deli count-
ers and as raw pulp juice. Preventing fruit and vegetable con-
tamination with pathogenic microorganisms is complex because
pathogens are normally present in the soil and may therefore be
present on the surfaces of fruits and vegetables at harvesting8.
Strategies for limiting microbiological contamination of frits
according to Kokkinakis and Fragkiadakis11, Strawn et al.12, and
Estrada-Acosta et al.13, implementation of good agricultural
practices (GAPs) and good manufacturing practices (GMPs)
enhances the safety of fresh produce and its value throughout
the food chain. This also facilitates the implementation of Haz-
ard Analysis Critical Control Points (HACCP), which have been
developed to identify specic risks related to food processing
and as risk control measures. Generally, HACCP programs are a
proactive way to limit food safety risks.
On an international level, GAPs and GMPs are described in the
Codex Alimentarius Commission’s code of hygienic practice for
fresh fruits and vegetables14. This code helps to control microbial,
chemical and physical hazards associated with all stages of fruit
and vegetable production (i.e. environmental hygiene, agricul-
tural input requirements, water for primary production, manure,
biosolids and other natural fertilisers, soil, indoor facilities associ-
ated with growing and harvesting, personnel health, hygiene and
sanitary facilities, equipment associated with growing and har-
vesting, handling, storage and transport, cleaning, maintenance
and sanitation of premises and harvesting equipment).
Meanwhile, the HACCP is a tool to assess hazards and estab-
lish control systems that focus on prevention rather than rely
mainly on end-product testing; it consists of seven principles as
described by the Codex Alimentarius15.
To minimise the risk associated with microbial hazards of fruits,
producers and processors have access to several detailed codes,
guidelines and regulations, such as “The guide to minimise
the microbial food safety hazards for fresh fruits and vegeta-
bles, Guidance for industry (FDA)16” “Microbiological hazards in
fresh fruits and vegetables (FAO/WHO)17”; “Microbiological Risk
Assessment (Codex)18 and Microbial Risk Assessment Guideline
(FSIS/USDA)19”.
Intervention methods to extend shelf-life and enhance safety
the best method to eliminate pathogens from produce is to
prevent contamination in the rst place. However, this is not
always possible, and the need to wash and sanitise many types
of produce remains of paramount importance to prevent disease
outbreaks20 and increase shelf life. As a result, dierent treat-
ment methods can be applied to fresh produce, such as chemi-
cal, physical, controlled atmosphere storage and modied atmo-
sphere packaging.
Chemical methods
Calcium-based solutions. Calcium treatments have been used to
extend the shelf life of fruits and vegetables. Calcium helps to
maintain the vegetable cell wall integrity by interacting with
pectin to form calcium pectate21. One of the most used com-
pounds is calcium lactate, which has antibacterial properties
due to its ability to uncouple microbial transport processes 22.
Chlorine (hypochlorite) chemicals are often used to sanitise
produce and surfaces in produce processing facilities as well as
to reduce microbial populations in water used for cleaning and
packaging operations. However, there are safety concerns about
the production of chlorinated organic compounds and their
impacts on human and environmental safety. Liquid chlorine and
hypochlorites are generally used in the 50 to 200 ppm concentra-
tion range, with a contact time of 1 to 2 min to sanitise produce
surfaces and processing equipment20.
Chlorine dioxide is a strong oxidising agent and a safe bactericide;
it generates only a small amount of trihalomethans (THMs) as a
byproduct23. The Food and Drug Administration24 has allowed the
http://www.visaemdebate.incqs.ocruz.br/ Vigil. sanit. debate 2017;5(2):127-140 | 129
Penteado AL. Microbiological safety aspects of mango and papaya
use of aqueous chlorine dioxide in washing fruits and vegetables.
A maximum of 3 ppm is allowed for contact with whole produce 20.
Electrolyzed water. There are two types of electrolysed water
with sanitising properties: acidic electrolysed water, or elec-
trolysed oxidising water (AEW), and neutral electrolysed water
(NEW). These solutions are conventionally generated by electrol-
ysis of aqueous sodium chloride, and an electrolysed acidic solu-
tion (AEW) or an electrolysed basic solution (NEW) is produced
at the anode and cathode, respectively22. Recently, the use of
electrolysed water as a sanitising agent for fresh produce has
received considerable attention in microbial load reduction25.
Hydrogen peroxide is a colourless gas at room temperature. Because
of its high oxidation potential, it has high bacteriostatic and bacte-
ricidal properties and has gained interest as a potential disinfectant
in the fresh produce industry because of its strong oxidising power.
It does not react with the organic compounds present in perishables
to produce carcinogenic compounds and breaks down into water
and oxygen. It has gained the status of Generally Regarded as Safe
(GRAS) in 1986 for some of the food commodities25.
Ozone is ecient in reducing pathogens on fresh produce because
of its strong oxidising capacity. However, using ozone as a disinfec-
tant has disadvantages, including its instability and reactivity with
organic materials. Thus, the eective elimination of microorgan-
isms may require high concentrations, which may, in turn, cause
sensory defects in fresh produce2. The eectiveness of ozone
treatment on microbial loads depends on several factors, such as
product type, target microorganism, initial microbial load level,
physiological state of the bacterial cells and zone physical state,
which may explain the diversity of published results26.
Quaternary ammonium compounds, commonly called “QAC”, are
cationic surfactants that are able to penetrate food contact sur-
faces more readily than other sanitisers22. The mode of action
of these compounds against bacterial cells involves a general
perturbation of lipid bilayer membranes27. Although they are not
approved for direct food contact, QAC may only partly be use-
ful when applied to whole produce, since the product must be
peeled prior to consumption20.
Organic acids (e.g. lactic, citric, acetic or tartaric acid).
The antimicrobial action of organic acids is due to a pH reduction
of the environment, disruption of membrane transport and/or
permeability, anion accumulation or reduction in internal cel-
lular pH20. Organic acids have a potential to reduce microbial
populations on fresh vegetables27.
Physical methods
Irradiation
Gamma-ray, X-ray and electron beams are called ionizing radia-
tions, because they are capable of producing ions, electronically
charged atoms or molecules. They have the same mechanisms in
terms of their eects on foods and microrganisms22. Irradiation is
an alternative treatment which is eective in decreasing micro-
bial counts on ready-to-eat vegetables28.
Steam jet-injection
Application of heat treatment is the most used method for sta-
bilising foods not involving any chemicals, based on its capac-
ity to destroy microorganisms and inactivate enzymes. How-
ever, heat can impair many organoleptic properties of foods
and reduce the contents or bioavailability of some nutrients29.
Short-time steam processing can be used as an alternative to
chlorine in sanitising fresh–cut lettuce; such treatment can sig-
nicantly reduce antioxidant levels, especially ascorbic acid
concentration, and, to a lower extend, carotenoid levels30.
From a safety point of view, steam treatment can keep the
mesophilic load as low as chlorine treatment30.
Temperature
Control of temperature is a key point in microbial growth con-
trol. Either refrigerating or heating can be applied to control or
reduce microbial load, respectively. Furthermore, the air tem-
perature can also be reduced to delay microbial proliferation.
However, this method should be used as complementary tech-
nique as, on its own, it is not eective enough to ensure prod-
uct safety31. The hygiene and temperature of water used during
the handling of produce are of primary importance. Immersion
of warm whole or fresh-cut produce in cool process solutions
may induce inltration of the solution (including contaminating
microorganisms) into the product through openings in the peel,
such as stem-end vascular tissue, lenticels, stomata, puncture
wounds or other physical disruptions20.
Ultrasound is a nonthermal technology using sonic waves and
requires the presence of a liquid medium for power transmis-
sion32,22. The inactivation of microorganisms through ultrasound is a
complex process, and a number of factors inuence its eciency32.
Ultraviolet light is one alternative to decrease pathogenic bac-
terial levels on fresh produce; the maximum eect of the use
of ultraviolet C (UV-C) light is obtained at a wavelength at
254 nm33,34. A dose in the range from 0.5 to 20 Jm-2 leads to lethal-
ity by directly altering microbial DNA through dimer formation,
thereby eliminating the risk of microbially induced disease33. Most
commonly, UV-C is applied to fresh fruits and vegetables, since it
acts directly or indirectly as an antimicrobial agent22.
Cold Atmospheric Plasma (CAP) is an emerging antimicrobial
technology for decontaminating infected surfaces. The treat-
ment uses non-thermal ionised gases (cold gas plasmas)22 that
are produced by the excitation of gas with electrical discharges
at room temperature and atmospheric pressure35. This treatment
shows signicant potential for sanitation of fresh produce2.
Modied atmosphere packaging (MAP) involves the modication
of the internal atmosphere composition of a package by reducing
the amount of oxygen (O2) and replacing it by carbon dioxide (CO2)
and/or nitrogen (N2)22. The MAP can be achieved passively (the pack-
age is sealed under normal air conditions) or actively (the package
is ushed with a gas mixture before being closed)21. In combination
with low temperatures, MAP could be used as a mild preservation
technique to enhance the safety of minimally processed products36.
http://www.visaemdebate.incqs.ocruz.br/ Vigil. sanit. debate 2017;5(2):127-140 | 130
Penteado AL. Microbiological safety aspects of mango and papaya
Active packaging has been dened as a packaging system actively
changing the condition of the package to improve food safety,
extend shelf life, enhance sensory properties and maintain the qual-
ity of the products37. There are dierent concepts of active food
packaging, including oxygen scavengers, carbon dioxide absorbers
and emitters, moisture absorbers, ethylene scavengers, ultravio-
let (UV) barriers and other mechanisms delivering antioxidant,
avouring or antimicrobial activity38,39. Substances responsible for
the active function can be obtained in a separate container, for
instance in a small paper sachet, or be directly incorporated in the
packaging material39. The substances that can be added are diverse
ranging from organic acids, enzymes, bacteriocins, fungicides, nat-
ural extracts and ions to ethanol39,40. Currently, active packaging
with ethylene scavengers, moisture and liquid absorbers as well as
with antimicrobial eects is used in commercial fruit distribution41.
There are dierent technologies to reduce/eliminate the micro-
organisms present in fresh-cut fruits and vegetables. However,
none of these sanitising methods can control all the parameters
that maintain the quality and shelf-life of MPFVs. Therefore, the
use of combined methods is crucial22.
In this review, the main focus was on the incidence, outbreaks,
growth/survival and internalisation of bacterial pathogens in
mangoes and papayas.
METHOD
Search strategy
The search for data on the incidence, outbreaks, growth/survival
and internalisation of bacterial pathogens in mangoes and papa-
yas was conducted from 1986 to 2016. Electronic searches were
conducted using the following scientic bases: Web of Science,
PubMed, Science Direct, Scopus and data from the “Centers for
Disease Control-CDC-USA”. The keywords used were incidence,
isolation, prevalence, detection, growth, behaviour, survival,
fruits, papayas, mangoes, internalisation, fruits, microbiologi-
cal, quality, safety, outbreak.
RESULTS
Incidence
From farm to table, there are multiple opportunities for fresh
produce to become contaminated by Salmonella, Escherichia coli
O157:H7, Campylobacter jejuni, Vibrio cholerae, parasites and
viruses that may contaminate raw manure or unpotable water as
well as animals or potentially tainted surfaces, including human
hands. In addition, pathogens such as Listeria monocytogenes,
Bacillus cereus and Clostridium botulinum are naturally present
in the soil42 and may also be a problem.
An important consideration when addressing safety issues is the
incidence of pathogens and outbreaks associated with particular
food products9.The following studies show the incidence of bac-
terial pathogens in mangoes and papayas.
One hundred and fty samples of fresh fruits and vegetables, col-
lected over a period of 12 months from various localities in Karachi,
Pakistan, were screened for Listeria monocytogenes. Two out of
thirty samples of papaya were positive for this pathogen43.
The microbiological quality of street-sold fruits in San José, Costa
Rica, was analysed over a two-year period from March 1990 to
March 1993. Researchers evaluated the presence of Salmonella
spp., Shigella spp., Escherichia coli and faecal coliforms in sev-
eral foods. The results showed that E. coli was present in more
than 10% of the mango and papaya samples, while Salmonella
spp. and Shigella spp. could not be isolated from these fruits44.
Thirty samples of ripe papaya (Carica papaya) slices were col-
lected in Calcutta, India, from itinerant roadside vendors over a
three-month period. Salmonella and Vibrio cholerae results were
positive in one sample each, and low levels of coagulase-positive
Staphylococcus aureus were detected in 17% of the samples45.
Bordini et al.46 analysed 100 mango samples produced in the
Northeastern region of Brazil from September 2001 to May 2002
and marketed in the state of São Paulo. The authors did not
observe the presence of Salmonella in any of the 33 samples of
mangoes destined for export. However, Salmonella was detected
in 2 out of 67 samples destined for the internal market.
The prevalence and quantity of Salmonella spp., Salmonella
Typhi and Salmonella Typhimurium were identied in sliced fruits
from hawker stalls and hypermarkets in Kuala Lumpur, Malaysia.
Salmonella spp. and Salmonella Typhi were found, respectively,
in six and three out of twenty samples of papaya and in two and
one out of twenty samples of mango from hawker stalls47.
A total of 125 samples of fresh produce were collected from
major supermarkets and local markets across Singapore and
characterised with respect to microbiological quality. Salmonella
and E. coli O 157:H7 were absent in only ten mango samples48.
Outbreaks
Foodborne illness is a major public health concern worldwide
in terms of the number of persons aected and the entailed
economic costs2. According to the WHO49 , in the year 2010,
31 foodborne global hazards caused 600 million foodborne ill-
nesses and 420,000 deaths worldwide. Foodborne diarrhoeal dis-
ease agents caused 230,000 deaths, particularly non-typhoidal
Salmonella enterica.
In the USA, in 2013, the Centers for Disease Control and Preven-
tion (CDC) reported 818 foodborne disease outbreaks, resulting
in 13,360 illnesses, 1,062 hospitalisations, 16 deaths and 14 food
recalls (CDC, 2013)50. In the developing world,2epidemiological
data on foodborne diseases remain scarce. Even the most visible
foodborne outbreaks often go unrecognised, uninvestigated or
unreported and may only be visible if connected to major public
health or economic impacts49.
According to the Brazilian Ministry of Health51, from 2007 to
2016, 6.848 outbreaks were related to the consumption of
http://www.visaemdebate.incqs.ocruz.br/ Vigil. sanit. debate 2017;5(2):127-140 | 131
Penteado AL. Microbiological safety aspects of mango and papaya
contaminated food, with 121.283 illnesses, 17.517 hospital-
isations and 111 deaths. Fruits and food were responsible for
0.6% of the outbreaks, while the number of non-identied foods
related to the total of the outbreaks is still as high as 66.9%.
The following reported outbreaks are related to the consump-
tion of mango and papaya contaminated by bacteria. A large
outbreak of food poisoning occurred in September 1996 and
involved at least 116 workers at a shipyard in Jurong, Singapore.
Four samples of cut watermelon, pineapple, papaya and honey-
dew melon were tested positive for Salmonella weltevreden52.
In 1998, an outbreak caused by S. Oranienburg, with nine cases
and three hospitalisations, occurred in a private home in Wash-
ington state and was associated with the consumption of fresh
imported mangoes purchased from a particular grocery chain53.
In December 1999, the rst reported outbreak of salmonello-
sis with mangoes in the United States occurred. Seventy-eight
patients from 13 states were infected with Salmonella Newport.
Fifteen patients were hospitalised and two died. The mangoes
had been imported from a single farm in Brazil54. Another out-
break in 2001 of S. enterica, associated with the consumption
of imported mangoes from Peru, occurred in the United States.
The serotype was Saintpaul; 26 cases were reported55. In 2003,
an outbreak due to the consumption of mangoes contaminated
with S. saintpaul in a restaurant/delicatessen occurred in Cal-
ifornia, US, with 17 cases56. During the period from October
2006 to January 2007, an outbreak with 26 cases of Salmonella
Litcheld infection occurred in Australia. This was the rst Aus-
tralian Salmonella outbreak associated with the consumption of
papaya57. A total of 106 individuals were infected with Salmo-
nella Agona in 25 states in the US from January 1 to August 25,
2011; no deaths were reported. This outbreak was related to
eating fresh, whole imported papayas from Mexico58.
During August 2012, a multistate outbreak of Salmonella
Braenderup in the USA occurred due to the consumption of
imported mangoes from Mexico. A total of 127 persons were
infected; 33 were hospitalised, but no deaths were reported.
From July to August 2012, a similar strain of S. braederup caused
21 illnesses in Canada; the infection was linked to mangoes
from Mexico59. In 2013, a multistate (4) outbreak occurred in
the USA due to the consumption of papaya contaminated with S.
Thomson, resulting in 13 cases, 6 hospitalisations and 1 death60.
In 2014, two outbreaks due to the consumption of mango con-
taminated with Salmonella were reported in the USA, one mul-
tistate and the other in the state of Connecticut, each with four
illnesses and one hospitalisation61.
All cited outbreaks were caused by Salmonella spp. Other patho-
gens, such as L. monocytogenes, are not suciently established
as relevant fruit juice-borne pathogens in the scientic litera-
ture, as compared to Salmonella and E. coli O157:H7. However,
this pathogen is of concern in fresh fruits and fruit juices, due
to its ability to survive under a variety of adverse conditions.
The reason why there are no reports of listerioses linked to the
consumption of fruit or fresh juices, in contrast to the variety of
outbreaks related to other enteropathogens, is unclear3.
Internalisation
Physical barriers, such as skin or rind, do not necessarily pre-
vent the contamination of produce, because cutting and slicing
eliminate this protection and microbes can invade the internal
tissue. In addition, bacterial microorganisms from contaminated
washing water can enter fruits and vegetables under certain
conditions45,62. Mangoes and papayas are tree fruits with simi-
lar processing procedures on the farm57. For example, at least
three salmonellosis outbreaks may have been caused by the
same mechanism through the immersion of warm papaya/mango
in cooler water, resulting in a pressure dierence between the
produce core and the surrounding water, which allowed Salmo-
nella present in the water to enter the fruit, generally through
the area around the stem54,55,57.
Growth/survival
The survival and/or growth of pathogens on fresh produce is
inuenced by the organism, produce item and environmental
conditions in the eld and thereafter, including storage condi-
tions. In general, pathogens will survive, but not grow on the
uninjured outer surface of fresh fruits or vegetables, partly due
to the protective character of the plant´s natural barriers (for
example, cell walls and wax layers). In some cases, pathogen
levels will decline on the outer surface9. One exception is the
study conducted by Bordini et al.46, which reported that the
number of Salmonella present on mango rind surfaces depended
on the storage temperature; at 22oC, an increase up to 2.30 logs
was observed, while at 8oC, no signicant variation occurred.
Microorganisms can grow and survive on mangoes and papayas,
as shown in the following studies. The ability of ve strains
of enteropathogenic bacteria (Shigella sonnei, S. exneri,
S. dysenteriae, Salmonella derby and S. typhi) to survive and
grow on sliced jicama, papaya and watermelon was investigated.
Small increases in the numbers of Shigella species occurred on
inoculated papaya after storage for only 2 h at 25–27oC, and
an increase of about 1.4 in 6 hours at room temperature was
observed for S. typhi inoculated on this fruit. Both microorgan-
isms could grow on papaya stored at temperatures of 22–27oC63.
Castillo and Escartin64 studied the survival of Campylobacter jejuni
on sliced watermelon and papaya. The populations on papaya
cubes inoculated with this microorganism survived for at least 6 h.
The percentage of survivors at 6 hours of storage ranged from 7.7
to 9.4. Decreases in count were substantial at 2 h of storage.
Yegeremu et al.65 studied the fate of Salmonella species and
E. coli in fresh-prepared orange, avocado, papaya and pineapple
juices. They observed that S. typhimurium and S. choleraesuis
could proliferate in papaya juice when stored at ambient tem-
peratures. Salmonella typhimurium reached counts as high as
109 CFU/mL in 24 h, steadily increasing until 48 h. Salmonella
choleraesuis reached its maximum count (108 CFU/ml) at 24 h,
with a slight decrease thereafter. Counts of both Salmonella spe-
cies increased by one log unit in 24 h at 4oC, but did not exceed
105 CFU/ml throughout the storage time.
http://www.visaemdebate.incqs.ocruz.br/ Vigil. sanit. debate 2017;5(2):127-140 | 132
Penteado AL. Microbiological safety aspects of mango and papaya
Penteado and Leitão66,67 investigated the growth of L. monocyto-
genes and S. enteritidis in papaya pulp. For L. monocytogenes,
maximum populations of about 5, 4 and 7 log units were reached
at temperatures of 10, 20 and 30oC, respectively, at the end
of the incubation periods. Generation times (g) of 15.05, 6.42
and 1.16 were obtained and decreased as the temperatures
increased. The same authors observed maximum populations of
108 CFU/g for 24- and 48-hr incubation periods and generation
times of 16.61, 1.74, and 0.66 hrs at incubation temperatures of
10, 20 and 30oC, respectively.
Mutaku et al.68 evaluated the growth potential of E. coli O 157:H7
in fresh juices of papaya, pineapple and avocado. In papaya juice,
counts of the test strains increased at varying rates at both stor-
age temperatures, ambient (20–25oC) and refrigeration (4oC).
Bordini et al.46 studied Salmonella enterica behaviour in man-
goes stored at temperatures of 8 and 22oC for 24 and 144 h and
observed that mean population numbers increased in the rind,
stem, middle and blossom end of the fruits at 22oC, over a period
of 24 h, with values of 0.53, 1.16, 1.47 and 1.36 logs, respec-
tively. With an incubation period of 144 h, the values were 1.84,
1.74, 2.30 and 2.30, respectively. At an incubation temperature
of 8oC, the increase in the number of bacteria was smaller: 0.59
log in the stem end, 0.82 log in the middle side and 0.80 log
in the blossom end after 24 h of incubation and 0.21, 0.22 and
0.47 log, respectively, after 144 h. At the rind surface, there was
a decrease in the number of bacteria: 0.41 log MPN/g after 144 h.
Strawn and Danyluk69 reported growth of Salmonella on cut man-
goes stored at 23 ± 2oC and survival at 4 ± 2oC, regardless of initial
inoculum concentrations. Population level was a factor at 12 ± 2oC,
with Salmonella growth only at the high (5 log CFU/g) and medium
(3 log CFU/g) inoculum levels. Escherichia coli O157:H7 grew rap-
idly on fresh-cut papayas at 23 ± 2oC and 12 ± 2oC and survived
throughout the shelf life of cut, refrigerated papayas. Similarly,
Salmonella grew rapidly on fresh-cut papayas at 23 ± 2oC and 12 ±
2oC and survived throughout the shelf life of refrigerated fresh-cut
papayas (4 ± 2oC). Inoculum levels had no eect on Salmonella
behaviour in cut papaya. Both microorganisms can survive on fro-
zen cut mangoes and papayas for at least 180 days.
Barbosa et al.70 inoculated mango slices with S. aureus and
L. monocytogenes (107 CFU/g), and the viable cell numbers
exhibited a reduction of only one log unit after six days of stor-
age for S. aureus, while being constant at 107 CFU/g for L. mono-
cytogenes over the same period.
Penteado et al.71 studied the growth of S. enteritidis and L. mono-
cytogenes in mangoes pulp at dierent temperatures and incuba-
tion times. At 25°C, the authors observed an increase of about 4.8
cycles log-1 after 48 h of incubation and a maximum population of
7.6 log units for S. enteritidis, while L. monocytogenes exhibited
an increase of about 6 cycles log-1, with a maximum population
of 8.6 log for the same temperature and period of incubation.
At 10oC, no growth could be observed for S. enteritidis. For L.
monocytogenes, an increase of about 4 cycles log-1 was observed,
with a maximum population of 7 log units after 200 h. At 4oC, both
bacterial populations survived for eight days. At -20oC, S. enterit-
idis was able to survive for ve months, while L. monocytogenes
could still be recovered after eight months.
Ma et al.72 studied the behaviour of Salmonella spp. on fresh-cut
tropical fruits, such as dragon fruit, banana, starfruit, mango,
pineapple, guava and wax apple, at 28 and 4oC at four inoculum
levels: 0.1, 1.0, 2.0 and 3.0 log CFU/g. The population of Salmo-
nella in mango remained equal to the initial inoculum level after
six days of storage at 4oC for all fruits tested. At 28 ± 2oC/two
days, there were increases of 0.11, 0.51 and 0.56 for inoculation
levels of 0.1, 2.0 and 3.0, respectively, and a decrease of -0.39
for the inoculation level of 1.0 log CFU/g.
Table 1 shows the important factors to consider when conducting
a bacterial growth study in fresh mango and papaya, including
inoculation, storage conditions, incubation temperature and
time, type of microorganism and pH. Along with storage tem-
perature, pH is cited as the principal determinant of bacterial
growth on fresh fruits. Many acidic fruits do not support the
growth of human pathogens and even inactivate them73,74.
The chemical and biochemical composition of mango varies with
cultivation, variety and stage of maturity. The major constitu-
ents of the pulp are water, carbohydrates, organic acids, fats,
minerals, pigments, tannins, vitamins and avour compounds76,77.
Fruits can be divided in two groups: those with pH ≤ 4 (high-acid
fruits), where the growth of microbial pathogens is unlikely to
occur, and those with a pH above 4 (low-acid fruits), where
microbial growth is more likely (e.g. mango and papaya)8. Vari-
ation in pH exists among varieties, growing conditions and pro-
cessing methods77, as in the case of the Dashehari mango cultivar.
During ripening, the pH rose from 3.0 to 5.278, demonstrating the
importance of determining pH when conducting a growth study.
Papaya has low acidity when compared to other tropical fruits,
which is a nutritional advantage, as it allows its consumption
by people sensitive to fruit acids; however, this low acidity is
a problem faced by processors, because high pH values favour
enzymatic activity and microbial growth79.
As shown in Table 2, variation in pH occurs in both fruits,
depending on the variables mentioned, which is of paramount
importance when conducting studies related to the behaviour of
microorganisms in this food.
DISCUSSION
Mangoes and papayas are good substrates for pathogen growth
and survival when stored in a variety of temperatures. Consider-
ing they are frequently manipulated, sliced and served in restau-
rants, hotels and at home (alone, mixed with other foods and as
pulp juice) and remain exposed for hours on restaurant tables,
normally at room temperature, these fruits could be considered
as potential vehicles for foodborne diseases.
Possible microbiological contamination could be reduced if man-
goes and papayas were cooked before consumption. This process is
http://www.visaemdebate.incqs.ocruz.br/ Vigil. sanit. debate 2017;5(2):127-140 | 133
Penteado AL. Microbiological safety aspects of mango and papaya
Table 1. Growth and survival of pathogenic bacteria on mango and papaya.
Pathogen Fruit type pHo-pHf Method of
inoculation Storage conditions Temp.
(oC)
Initial
counts
Incub.
Time
Final
counts Unit Comments Reference
Salmonella Typhi Papaya cubes 5.69
Spot inoculation, cells
suspended in saline
solution, 1 drop
12 cm2 cubes, inoculated
stored in covered glass
trays
25–27 2.9 6 h 4.3 CFU/cube nd 63
Shigella (three
species) Papaya cubes 5.69
Spot inoculation, cells
suspended in saline
solution, 1 drop
12 cm2 cubes,
inoculated, stored in
covered glass trays
25–27 1.9–2.2 6 h 3.8–4.4 CFU/cube
S. sonnei
63S. exneri
S. dysenteriae
Campylobacter jejuni Papaya cubes 5.6–5.0
Spot inoculation cells
suspended in saline
solution, 0.02 ml
inoculated per cube
24 cm2 cubes. Stored in
sterile stainless-steel
trays with cover
25–29 2.8 6 h 1.7 CFU/cube Serotype Penner 50 64
Salmonella
typhimurium Papaya juice 5.7–4.69
Inoculated with
overnight broth
culture
Inside screw cap bottles
4
3.99
24 h 5.2
CFU/mL
100 ml water/400
ml papaya.
Steamed before
inoculation100oC/10
min/ papaya fresh
ripened
65
48 h 4.43
37
24 h 9.15
48 h 9.23
Salmonella
choleraesuis Papaya juice 5.7–4.69
Inoculated with
overnight broth
culture
Inside screw cap bottles
4
3.52
24 h 4.45
CFU/mL
100 ml water/400
ml papaya.
Steamed before
inoculation100oC/10
min/ papaya fresh
ripened
65
48 h 4.08
37
24 h 8.66
48h 8.18
E. coli (25922) Papaya juice 5.7–4.69
Inoculated with
overnight broth
culture
Inside screw cap bottles
4 3.52 24 h 4.45
CFU/mL
100 ml water/400
ml papaya.
Steamed before
inoculation100oC/10
min/ papaya fresh
ripened
65
48 h 4.08
37 2.70
24 h 9.36
48 h 9.40
E. coli (9637) Papaya juice 5.7–4.69
Inoculated with
overnight broth
culture
Inside screw cap bottles
4
2.78
24 h 2.54
CFU/mL
100 ml water/400
ml papaya.
Steamed before
inoculation100oC/10
min/ papaya fresh
ripened
65
48 h 2.53
37
24 h 9.1
48 h 9.4
Salmonella
Enteritidis Papaya pulp 4.87
Bacterial suspension
diluted in 0.1%
peptone water
50 g pulp, inoculated
and stored in Erlenmeyer
asks
10 2.58 168 h 4.46
CFU/g
Pulps pasteurised
(80oC/1 min) before
inoculation tests
6620 2.42 48 h 8.68
30 2.54 24 h 8.81
Listeria
monocytogenes Papaya pulp 4.87
Bacterial suspension
diluted in 0.1%
peptone water
50g pulp, inoculated and
stored in Erlenmeyer
asks
10 2.45 168 h 4.84
CFU/g
Pulps pasteurised
(80oC/1min) before
inoculation tests
6720 2.59 48 h 4.43
30 2.61 24 h 7.36
E. coli O 157:H7 Papaya fresh
juice 5.17
Bacterial suspension
at TSB + 0.6% yeast
extract
250 ml juice inoculated
and stored in screw-
capped bottles
25 ~3.3 96 9 CFU/ml
Four strains of E. coli
O 157:H7
68
pH 4.5 after 120 hr/
juices steamed at
100oC/10min. before
inoculation
Continue
http://www.visaemdebate.incqs.ocruz.br/ Vigil. sanit. debate 2017;5(2):127-140 | 134
Penteado AL. Microbiological safety aspects of mango and papaya
Continuation
Salmonella enterica Mangoes 4.49 Immersion in water
with the inoculum Inside sterile plastic bags
8
24
2.5 S1
CFU/g
*MPN/g
Dierent portions of
the mango (Stem-S,
Middle-M, Blossom-B
and Rind-R)
46
1.58 M2
1.91 S1 1.3 B3
0.76 M21.29* R4
0.5 B3
1.7 R4*
144
2.29 S1
0.98 M2
0.97 B3
0.7* R4
22
24
3.07
2.23
1.91 S 1.86
0.76 M 2.23
0.5 B
1.7 R*
144
3.65
3.06
2.8
3.5*
Salmonella Mangoes
slices nd
Inoculation by
drops on the fruit
surface of bacterial
suspension diluted
in 0.1% peptone
water
Samples inoculated
and placed into sterile
stomacher bags
12 4.5 24 hr 5.9
CFU/g
Cocktail of S.
serovars. S. Michigan,
S. Montevideo, S.
Munchen, S. Newport,
S. Saintpaul Mangoes
cv Tommy Atkins
(ripe)
69
28 d 0.6
23 2.9
24 h 6.0
7 d 2.4
E. coli O157:H7
Mangoes
slices nd
Drops inoculation on
the fruit surface of
bacterial suspension
diluted in 0.1%
peptone water
Samples inoculated
and placed into sterile
stomacher bags
12 4.6 24 hr 4.5
CFU/g
Cocktail of four
strains Mangoes cv
Tommy Atkins (ripe)
69
28 d 1.5
23 2.9 24 h 4.7
7 d 4.0
Papayas cubes nd
Drop inoculation on
the fruit surface of
bacterial suspension
diluted in 0.1%
peptone water
Samples inoculated
and placed into sterile
stomacher bags
12 3.9 24 h 5.0
CFU/g
Cocktail of four
strains Papayas cv
Red Lady (ripe)
69
28 d 4.3
23 2.6 24 h 6.0
7 d 6.3
Salmonella Papayas cubes nd
Drop inoculation on
the fruit surface of
bacterial suspension
diluted in 0.1%
peptone water
Samples inoculated
and placed into sterile
stomacher bags
12 4.1 24 h 5.2
CFU/g
Cocktail of S
serovars. S. Michigan,
S.Montevideo, S.
Munchen, S. Newport,
S. Saintpaul Papayas
cv Red Lady (ripe)
69
28 d 3.5
23 2.6
24 h 6.2
7 d 6.6
S. aureus
Mangoes cv
Tommy Atkins
slices
4.30-4.0
Immersion of slices
in 0.1% peptone
with cell suspension
Packed in polystyrene
trays covered with PVC
lm
5 7.0 12 d 5.0 CFU/g Mangoes at mature-
green stage 70
L. monocytogene
Mangoes cv
Tommy Atkins
slices
4.30-4.29
Immersion of slices
in 0.1% peptone
with cell suspension
Packed in polystyrene
trays covered with PVC
lm
5 7.0 12 d 6.0 CFU/g Mangoes at mature-
green stage 70
Continue
http://www.visaemdebate.incqs.ocruz.br/ Vigil. sanit. debate 2017;5(2):127-140 | 135
Penteado AL. Microbiological safety aspects of mango and papaya
Salmonella
Enteritidis Mango pulp 5.16
Bacterial suspension
diluted in 0.1%
peptone water
50 g pulp, inoculated
and stored in Erlenmeyer
asks
25 2.8 24 h 4.94 CFU/g
Pulps pasteurised
(80oC/1min) before
inoculation tests
71
48 h 7.6
Listeria
monocytogenes
Mango pulp 5.16
Bacterial suspension
diluted in 0.1%
peptone water
50 g pulp, inoculated
and stored in Erlenmeyer
asks
25 2.79 24 6.14 CFU/g
Pulps pasteurised
(80oC/1min) before
inoculation tests
71
48 h 8.6
Mango slices 4.19
Bacterial suspension
diluted in 0.1%
peptone water
10g, inoculated, packed
in polystyrene trays
covered with PVC lm
5 2.3 1 d ~4.0
CFU/g Cocktail of six strains 7513 2.3 6 d 7.7
25 2.3 4 d 6.8
Papaya slices 5.99
Bacterial suspension
diluted in 0.1%
peptone water
10g, inoculated, packed
in polystyrene trays
covered with PVC lm
5 2.2 5 d ~4.0
CFU/g Cocktail of six strains 7513 2.2 6 d 4.2
25 2.2 4 d 7.6
S. aureus
Mango slices 4.19
Bacterial suspension
diluted in 0.1%
peptone water
10g, inoculated, packed
in polystyrene trays
covered with PVC lm
5 3.5 1 d ~3.5
CFU/g Cocktail of four
strains 7513 3.5 6 d 5.4
25 3.5 4 d 8.1
Papaya slices 5.99
Bacterial suspension
diluted in 0.1%
peptone water
10g, inoculated, packed
in polystyrene trays
covered with PVC lm
5 2.5 6 d 4.4
CFU/g Cocktail of four
strains 7513 2.5 6 d 5.3
25 2.5 4 d 6.1
Salmonella Mango (cv
Palmer) nd
Spot inoculated
with 1 cell
suspension
Fruit cubes packaged in
sterilised bags 28
0.1
2 d
0.21
CFU/g
Cocktail 3 serotypes
(S. Newport,
S. Saintpaul S.
rnteritdis)
72
1.0 0.61
2.0 2.51
3.0 3.56
S1 = Stem end; M2 = Middle; B3 =Blossom end; R4 = Rind
Continuation
usually eective in the elimination of any potentially pathogenic
organisms, rendering these fruits safe to be consumed. However,
mangoes and papayas are commonly eaten in a raw state, and the
possible presence of pathogens on their surface or inside the fruits
can be problematic during the manipulation process or even in the
case of internalisation, which would allow the growth/survival of
foodborne pathogens in these foods and pose a problem for the
consumers. Pathogen internalisation into those fruits is a process
that should be controlled with attention to the quality and tem-
perature of the water applied in washing these fruits.
The rst step to prevent contamination is to respect the preven-
tive measures included in the GAPs, GMPs and HACCP.
Studies have shown that the application of preventive measures,
such as washing hands, good personal hygiene, appropriate use of
sanitary facilities, treated manure (fertilisers), quality of the irri-
gation water, avoiding ooding events, cleaning and sanitising of
equipment, can reduce microbial contamination on fresh produce.
Himathongkham and Riemann86 showed that treatment of
dry chicken manure with ammonia results in a signicant
reduction of Salmonella typhimurium, E. co li O 157:H7 and
Listeria monocytogenes.
In cooling and storage facilities, contamination can be reduced
with the use of ozone; treatment of cold rooms has been reported
to be eective in signicantly reducing Listeria monocytogenes87.
Zhou et al.88 studied the eect of ultrasound in combination with
chlorine on the reduction of Escherichia coli O 157:H7 popula-
tions on lettuce coring knives; the results of these treatments
with redesigned coring knives may provide practical options
for minimising microbial safety hazards of lettuce processed by
core-in-eld operations.
According to Park et al.89, microbial contamination of produce
is inuenced by farm management and environmental factors.
Specically, contamination seems to be strongly inuenced by
the time since last irrigation, worker personal hygiene and eld
use prior to planting.
Rodrigues et al.90 mentioned that preventive measures on lettuce
farms, such as microbial quality and method of composting manure
as well the source and quality of irrigation waters and washing
waters, are of utmost importance in accordance with the obtained
microbiological results. The authors also demonstrated that the
fertiliser control program and the water used for irrigation and
washing were important factors to be controlled in the production
chain of organic lettuce in order to ensure food safety and a high
hygiene status. With regards to irrigation and rinsing water, the
results showed the importance of using water from safe sources.
Monagham and Hutchison91 showed that the numbers of generic
Escherichia coli isolated from workers’ hands declined with
increasing thoroughness of hand-washing treatments. As reported
by Park et al.89, contamination with generic E. coli was signi-
cantly reduced with an irrigation lapse time of > ve days as well
as by several factors related to eld workers, including the use
http://www.visaemdebate.incqs.ocruz.br/ Vigil. sanit. debate 2017;5(2):127-140 | 136
Penteado AL. Microbiological safety aspects of mango and papaya
of portable toilets, training to use portable toilets and the use of
hand-washing stations.
Increased microbial load and pathogen prevalence in lettuce
production was revealed for high temperature, ooding of let-
tuce elds, application of contaminated organic fertiliser, irriga-
tion with water of inferior quality and large distances between
the eld and toilets, showing the importance of controlling the
composting process of organic manure and the quality of the irri-
gation water, to improve and/or maintain the safety of lettuce
during primary production92.
As stated by Bracket93, it should be remembered that a systems
approach in maintaining sanitation and quality should be taken.
All steps, from production through consumption, will aect the
microora. Applying proper sanitary procedures and insisting on
utmost hygiene are indispensable. However, employing a good
Table 2. pH values of mangoes and papayas.
Fruit pH Comments References
Mangoes var. Tommy Atkins 4.49 Central portion of the mango 46
Mango pulp (variety Palmer) 5.16 Ripe 66
Manga “Ubá” 3.90–4.29 - 80
Manga cv. Haden 4.28 Pulp 81
Mangoes cv “Tommy Atkins” 4.30 Mature-green stage 38
Mangoes cv Golden 5.39–6.14 Pulp, homogenised in distilled water, dierent maturity stages 82
Mango cv. Haden 2.4–4.5 Mix of pulps of the same maturity stage; pH increase with maturity 44
Mangoes 3.9–4.6 - 83
Papaya cv. “Maradol” red 5.5 Partially ripe 84
Papaya (Carica papaya) 6.4–6.8 Ripe 15
Ripe papaya 5.69 Surface pH 32
Papaya pulp 4.87 Ripe 35
Papaya Formosa cv. Tainung 01 5.06–5.10 Stage 4 (51–75% yellow colour)/fruit juice 47
4.1 75% ripe/fruit 85
Papaya 5.17 Fresh/juice 37
5.2–5.7 - 83
HACCP program is also necessary to assure safety, as the use
of HACCP helps to minimise the potential hazards that may be
associated with fresh-cut produce processing93,94.
The application of HACCP to control enteric pathogens in pro-
cessed crops was reviewed by Leifter et al.95. As mentioned
by Hurst96, HACCP is the most comprehensive, science-based
program for reducing pathogen contamination in fruit and veg-
etable products.
CONCLUSION
Therefore, the implementation of strategies such as Good Agri-
cultural Practices, Good Manufacturing Practices and Hazard
Analysis Critical can eliminate or signicantly reduce microbial
contamination on fresh mangoes and papayas.
1. Food and Agricultural Organization of the United Nations –
FAO. FAO statistical yearbook 2013: world food and agricul-
ture. Rome: FAO; 2013.
2. Olaimat AN, Holley RA. Factors inuencing the micro-
bial safety of fresh produce: a review. Food Microbiol
2012;32(1):1-19. https://doi.org/10.1016/j.fm.2012.04.016
3. Tribst AAL, Sant’Ana AS, Massaguer PR. Review: microbiolo-
gical quality and safety of fruit juices: past, presente and
future perspectives. Crit Rev Microbiol. 2009;35(4):310-39.
https://doi.org/10.3109/10408410903241428
4. Brazilian Fruit Yearbook 2015. Santa Cruz do Sul: Gazeta
Santa Cruz; 2015[cited 2016 Feb 02]. Avalaible from:
http://www.grupogaz.com.br/tratadas/eo_edicao/4/2015/
03/20150301_106c8c2f1/ip/#4
5. Tharanathan RN, Yashoda HM, Prabha TN. Mango
(Mangifera indica L.), “The king of fruits”: an
overview. Food Rev Int. 2006;22(2):95-123.
https://doi.org/10.1080/87559120600574493
6. Oliveira JG, Vitória AP. Papaya: nutritional and pharmacolo-
gical characterization, and quality loss due to physiological
disorders: an overview. Food Res Int. 2011;44(5):1306-13.
https://doi.org/10.1016/j.foodres.2010.12.035
7. Food and Agriculture Organization of the Uni-
ted Nations – FAO. Faostat. Rome: FAO;
2013[cited 2016 Feb 02]. Available from: http://faostat3.
fao.org/download/Q/QC/E
8. Beuchat LR. Surface decontamination of fruits and vegeta-
bles eaten raw: a review. Rome: World Health Organization;
1998[cited 2016 Feb 02]. Available from: http://apps.who.int/
iris/bitstream/10665/64435/1/WHO_FSF_FOS_98.2.pdf
9. Harris LJ, Farber JN, Beuchat LR, Parish ME,
Suslow TV, Garret EH et al. Outbreaks associated
with fresh produce: incidence, growth, and survi-
val of pathogens in fresh and fresh-cut produce.
Compr Rev Food Sci Food Saf. 2003;2(s1):78-141.
https://doi.org/10.1111/j.1541-4337.2003.tb00031.x
REFERENCES
http://www.visaemdebate.incqs.ocruz.br/ Vigil. sanit. debate 2017;5(2):127-140 | 137
Penteado AL. Microbiological safety aspects of mango and papaya
10. Berger CN, Sodha SV, Shaw RK, Grin PM,
Pink D, Hand P et al. Fresh fruit and vegetables
as vehicles for the transmission of human patho-
gens. Environ Microbiol. 2010;12(9):2385-97.
https://doi.org/10.1111/j.1462-2920.2010.02297.x
11. Kokkinakis E, Fragkiadakis GA. HACCP eect on
microbiological quality of minimally processed
vegetables: a survey in six mass catering establish-
ments. Int J Food Sci Technol. 2007;42(1):18-23.
https://doi.org/10.1111/j.1365-2621.2006.01179.x
12. Strawn LK, Schneider KR, Danyluk MD. Microbial safety of
tropical fruits. Crit Rev Food Sci Nutr. 2011;51(2):132-45.
https://doi.org/10.1080/10408390903502864
13. Estrada-Acosta M, Jiménez M, Chaidez C,
León-Félix J, Castro-Del Campo N. Irrigation water
quality and the benets of implementing good agricultu-
ral practices during tomato (Lycopersicum esculentum)
production. Environ Monit Assess. 2014;186(7):4323-30.
https://doi.org/10.1007/s10661-014-3701-1
14. Codex Alimentarius. International Food Standards.
CAC/RCP 53-2003. Code of hygienic practice for fresh fruits
and vegetables. Rome: FAO; 2003.
15. Codex Alimentarius. International Food Standards.CAC/RCP
1-1969. Hazard analysis and critical control point (HACCP)
system and guideline for its application. Rome: FAO; 2003.
16. U.S. Department of Health and Human Services. Food
and Drug Administration. Center for Food Safety and
Applied Nutrition. Guidance for industry: guide to mini-
mise the microbial food safety hazards for fresh fruits and
vegetables. Washington, DC: Center for Food Safety and
Applied Nutrition; 1998 [cited 2017 Feb 6]. Available from:
http://wcmorris.com/gap/les/prodguid.pdf
17. World Health Organization. Food and Agriculture Organization
of the United Nations. Microbiological hazards in fresh fruits
and vegetables: meeting report. Geneva: World Health Orga-
nization; 2008[cited 2017 Feb 6]. (Microbial risk assessment
series. Pre-publication version). Available from: http://www.
who.int/foodsafety/publications/micro/MRA_FruitVeges.pdf
18. Codex Alimentarius. International Food Standards. CAC/GL
30-1999. Principles and guidelines for the conduct of microbiolo-
gical risk assessment. Amendments 2012, 2014. Rome: FAO; 2014.
19. U.S. Department of Agriculture/Food Safety and Inspection
Service –FSIS/USDA Microbial risk assessment guideline:
pathogenic microorganisms with focus on food and water.
Washington, DC: U.S. Department of Agriculture; 2012
[cited 2017 Feb 6]. EPA publication, EPA/100/J12/001. Avai-
lable from: https://www.fsis.usda.gov/wps/wcm/connect/
d79eaa29-c53a-451e-ba1c-36a76a6c6434/Microbial_Risk_
Assessment_Guideline_2012-001.pdf?MOD=AJPERES
20. Parish ME, Beuchat LR, Suslow TV, Harris LJ,
Garret EH, Farber JN et al. Methods to reduce/eli-
minate pathogens from fresh and fresh-cut produce.
Compr Rev Food Sci Food Saf. 2003;2(s1):161-73.
https://doi.org/10.1111/j.1541-4337.2003.tb00033.x
21. Rico D, Martín-Diana AB, Barat JM, Barry-Ryan C. Extending
and measuring the quality of fresh-cut fruit and vegetables:
a review. Trends Food Sci Techol. 2007;18(7):373-86.
https://doi.org/10.1016/j.tifs.2007.03.011
22. Ramos B, Miller FA, Brandão TRS, Teixeira P, Silva CLM. Fresh
fruits and vegetables: an overview on applied methodologies to
improve its quality and safety. Innov Food Sci Emerg Technol.
2013;20:1-15. https://doi.org/10.1016/j.ifset.2013.07.002
23. Chung CC, Huang TC, Yu CH, Shen FY, Chen HH. Bactericidal
eects of fresh-cut vegetables and fruits after subsequent
washing with chlorine dioxide. In Proceedings of Interna-
tional Conference on Food Engineering and Biotechnology,
ICFEB 2011; 2011 May 2011; Bangkok, Thailand. Hong Kong:
CBEES; 2011. p. 107-12.
24. U.S. Government Publishing Oce. Eletronic code of fede-
ral regulations. Title 21: food and drugs. Part 173: Secon-
dary direct food additives permitted in food for human
consumption. Subpart D: specic usage additives. Chlorine
dioxide. Washington, DC: U.S. Government Publishing
Oce; 2016[cited 2017 Fev 6]. Available from: http://
www.ecfr.gov/cgi-bin/retrieveECFR?gp=1&SID=d4e1a22de-
727a4afaf0d5fb2b27a7d5d&ty=HTML&h=L&mc=true&r=SEC-
TION&n=se21.3.173_1300
25. Joshi K, Mahendran R, Alagusundaram K, Norton T, Tiwari BK.
Novel disinfectants for fresh produce. Trends Food Sci Technol.
2013;34(1):54-61. https://doi.org/10.1016/j.tifs.2013.08.008
26. Miller FA, Silva CLM, Brandão TRS. A Review on ozone-based
treatments for fruit and vegetables preservation. Food Eng Rev.
2013;5(2):77-106. https://doi.org/10.1007/s12393-013-9064-5
27. Velázquez LdC, Barbini NB, Escudero ME, Estrada CL,
Guzmán AMS. Evaluation of chlorine, benzalkonium
chloride and lactic acid as saniters for reducing Esche-
richia coli O157:H7 and Yersinia enterocolitica on
fresh vegetables. Food Control. 2009;20(3);262-8.
https://doi.org/10.1016/j.foodcont.2008.05.012
28. Prakash A, Inthajak P, Huibregtse H, Caporaso F, Foley DM.
Eects of Low-dose gamma irradiation and conven-
tional treatments on shelf life and quality characte-
ristics of diced celery. J Food Sci. 2000;65(6):1070-5.
https://doi.org/10.1111/j.1365-2621.2000.tb09420.x
29. Rico D, Martín-Diana AB, Barry-Ryan C, Frias JM,
Henehan GTM, Barat JM. Optimisation of steamer
jet-injection to extend the shelife of fresh cut let-
tuce. Postharvest Biol Technol. 2008;48(3):431-42.
https://doi.org/10.1016/j.postharvbio.2007.09.013
30. Martín-Diana AB, Rico D, Barry-Ryan C, Frías JM,
Henehan GTM, Barat JM. Ecacy of steamer jet-in-
jection as alternative to chlorine in fresh-cut let-
tuce. Postharvest Biol Technol. 2007;45(1):97-107.
https://doi.org/10.1016/j.postharvbio.2007.01.013
31. Meireles A, Giaouris E, Simões M. Alternative
disinfection methods to chlorine for use in the
fresh-cut industry. Food Res Int. 2016;82:71-85.
https://doi.org/10.1016/j.foodres.2016.01.021
32. Otto C, Zahn S, Rost F, Zahn P, Jaros D,
Rohm H. Physical methods for cleaning and disinfec-
tion of surfaces. Food Eng Rev. 2011;3(3-4):171-88.
https://doi.org/10.1007/s12393-011-9038-4
http://www.visaemdebate.incqs.ocruz.br/ Vigil. sanit. debate 2017;5(2):127-140 | 138
Penteado AL. Microbiological safety aspects of mango and papaya
33. Bintsis T, Litopoulou-Tzanetaki E, Robinson RK. Exis-
ting and potential applications of ultraviolet light in
the food industry: a critical review. J Sci Food Agric.
2000;80(6):637-45. https://doi.org/10.1002/(SICI)-
1097-0010(20000501)80:6<637::AID-JSFA603>3.0.CO;2-1
34. Lim W, Harrison A. Eectiveness of UV light as a means
to reduce Salmonella contamination on tomatoes and
food contact surfaces. Food Control. 2016;66:166-73.
https://doi.org/10.1016/j.foodcont.2016.01.043
35. Fernández A, Thompson A. The inactivation of
Salmonella by cold atmospheric plasma tre-
atment. Food Res Int. 2012;45(2):678-84.
https://doi.org/10.1016/j.foodres.2011.04.009
36. Oliveira M, Abadias M, Usall J, Torres R, Teixidó N,
Viñas I. Application of modied atmosphere packaging
as a safety approach to fresh-cut furits and vegetables:
a review. Trends Food Sci Techol. 2015;46(1):13-26.
https://doi.org/10.1016/j.tifs.2015.07.017
37. Bodbodak S, Raee Z. Recent trends in active packaging in
fruits and vegetables. In: Bodbodak S, Raee Z, organizers.
Eco-friendly technology for postharvest produce quality:
recent trends in active packaging in fruits and vegetables.
India: Academic Press; 2016., Chapter 3, Recent trends
in active packaging in fruits and vegetables; p. 77-125.
p. 77 -125, 2016.
38. Otoni CG, Espitia PJP, Avena-Bustillos RJ,
McHugh TH. Review trends in antimicrobial
food packaging systems: emitting sachets and
absorbent pads. Food Res Int. 2016;83:60-73.
https://doi.org/10.1016/j.foodres.2016.02.018
39. Restuccia D, Spizzirri UG, Parisi OI, Cirillo G, Curcio M,
Iemma F et al. New EU regulation aspects and global
market of active and intelligent packaging for food
industry applications. Food Control. 2010;21(11):1425-35.
https://doi.org/10.1016/j.foodcont.2010.04.028
40. Soares NF, Silva CAS, Santiago-Silva P, Espitia PJP,
Gonçalves MPJC, Lopez MJG et al. Active and intelligent
packaging for milk and milk products. In: Coimbra JSR,
Teixeira JA, editors. Engineering aspects of milk and dairy
products. Boca Raton: CRC Press; 2009. p. 175-99.
41. Sarantópoulos C, Cofcewiz LS. Embalagens ativas para produtos
perecíveis. Bol Tecnol Desenvolv Embalagens. 2016;28(3):1-12.
42. Beuchat LR, Ryu JH. Produce handling and proces-
sing practices. Emerg Infect Dis. 1997;3(4):459-65.
https://doi.org/10.3201/eid0304.970407
43. Vahidy R, Jahan F, Nasim R. Isolation of Listeria monocytogenes
from fresh fruits and vegetables. HortScience. 1992;27(6):628.
44. Monge R, Arias ML, Antillón F, Utzinger D. [Microbiological
quality of street sold fruits in San José, Costa Rica]. Arch
Latinoam Nutr. 1995;45(2):117-21. Spanish.
45. Mukhopadhyay R, Mitra A, Roy R, Guha AK. An evaluation of stre-
et-vended sliced papaya (Carica papaya) for bacteria and indica-
tor micro-organisms of public health signicance. Food Microbiol.
2002;19(6):663-7. https://doi.org/10.1006/fmic.2002.0511
46. Bordini MEB, Ristori CA, Jakabi M, Gelli DS. Incidence,
internalization and behavior of Salmonella in mangoes,
var. Tommy Atkins. Food Control. 2007;18(8):1002-7.
https://doi.org/10.1016/j.foodcont.2006.06.003
47. Pui CF, Wong CW, Chai LC, Nillian E, Ghazali FM,
Cheah YK et al. Simultaneous detection of Salmonella spp.,
Salmonella Typhi and Salmonella Typhimurium in sliced
fruits using multiplex PCR. Food Control. 2011;22(2) 337-42.
https://doi.org/10.1016/j.foodcont.2010.05.021
48. Seow J, Agoston R, Phua L, Yuk HG. Microbiolo-
gical quality of fresh vegetables and fruits sold
in Singapore. Food Control. 2012;25(1):39-44.
https://doi.org/10.1016/j.foodcont.2011.10.017
49. World Health Organization – WHO. WHO estimates of the
global burden of foodborne diseases: foodborne disease
burden epidemiology reference group 2007-2015. Geneva:
World Health Organization; 2015.
50. Centers for Disease Control and Prevention – CDC. Sur-
veillance for foodborne disease outbreaks United States,
2013: annual report. Atlanta: US Department of Health and
Human Services; 2015.
51. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde.
Departamento de Vigilância das Doenças Transmissíveis. Sur-
tos de doenças transmitidas por alimentos no Brasil. Brasília,
DF: Ministério da Saúde; 2016[cited 2017 Feb 6]. Available
from: http://portalsaude.saude.gov.br/images/pdf/2016/
dezembro/09/Apresentacao-Surtos-DTA-2016.pdf
52. Ooi PL, Goh KT, Neo KS, Ngan CCL. A shipyard outbreak of
salmonellosis traced to contaminated fruits and vegetables.
Ann Acad Med Singapore. 1997;26(5):539-43.
53. Salmonella Oranineburg, Ontario.Canada Comm Dis Report.
1998;24-22: 177.
54. Sivapalasingam S, Barrett E, Kimura A, Van Duyne S,
De Witt W, Ying M. A multistate outbreak of Salmonella ente-
rica serotype Newport infection linked to mango consump-
tion: impact of water-dip disinfection technology. Clin Infect
Dis. 2003;37(12):1585-90. https://doi.org/10.1086/379710
55. Beatty ME, LaPorte TN, Phan Q, Van Duyne SV, Braden C.
A multistate outbreak of Salmonella enterica serotype
Saintpaul infections linked to mango consumption: a
recurrent theme. Clin Infect Dis. 2004;38(9):1337-8.
https://doi.org/10.1086/383156
56. Center for Disease Control and Prevention – CDC. 2003
Summary statistics: the total number of foodborne disease
outbreaks by etiology. Atlanta: Center for Disease Control and
Prevention; 2013[cited 2016 Feb 02]. Available from: http://
www.cdc.gov/outbreaknet/pdf/surveillance/2003_linelist.pdf
57. Gibbs R, Pingault N, Mazzucchelli T, O’Reilly L, MacKenzie B,
Green J et al. An outbreak of Salmonella enterica serotype
Litcheld infection in Australia linked to consumption of
contaminated papaya. J Food Prot. 2009;72(5):1094-8.
https://doi.org/10.4315/0362-028X-72.5.1094
58. Center for Disease Control and Prevention – CDC. Multistate
outbreak of human Salmonella agona infections linked to
whole, fresh imported papayas (nal update). Atlanta:
Center for Disease Control and Prevention; 2011[cited
2016 Feb 02]. Available from: http://www.cdc.gov/salmo-
nella/2011/papayas-8-29-2011.html
http://www.visaemdebate.incqs.ocruz.br/ Vigil. sanit. debate 2017;5(2):127-140 | 139
Penteado AL. Microbiological safety aspects of mango and papaya
59. Center for Disease Control and Prevention – CDC. Multistate
outbreak of Salmonella Braenderup infections associated
with mangoes (nal update). Atlanta: Center for Disease
Control and Prevention; 2012[cited 2016 Feb 02]. Avaliable
from: http://www.cdc.gov/salmonella/braenderup-08-12
60. Center for Disease Control and Prevention – CDC. Sur-
veillance for foodborne disease outbreaks United States,
2013: annual report. Atlanta: Center for Disease Control
and Prevention; 2013[cited 2016 Feb 02]. Availlable from
http://www.cdc.gov/foodsafety/pdfs/foodborne-disease-
-outbreaks-annual-report-2013-508c.pdf
61. Center for Disease Control and Prevention – CDC. Foodborne
outbreak online database (food tool). Atlanta: Centers for
Disease Control and Prevention; 2016[cited 2016 Feb 24].
Availlable from: http://wwwn.cdc.gov/foodborneoutbreaks
62. Sivapalasingam S, Friedman CR, Cohen L,
Tauxe RV. Fresh produce: a growing cause of outbre-
aks of foodborne illness in the United States, 1973
through 1997. J Food Prot. 2004;67(10):2342-53.
https://doi.org/10.4315/0362-028X-67.10.2342
63. Escartin EF, Ayala AC, Lozano JS. Survival
and growth of Salmonella and Shigella on sli-
ced fresh fruit. J Food Prot. 1989;52(7):471-2.
https://doi.org/10.4315/0362-028X-52.7.471
64. Castillo A, Escartin EF. Survival of Campylobacter jejuni on
sliced watermelon and papaya. J Food Prot. 1994;57(2):166-8.
https://doi.org/10.4315/0362-028X-57.2.166
65. Yigeremu B, Bogale M, Ashena M. Fate of Salmonella species
and E. coli in fresh-prepared orange, avocado, papaya and
pine apple juices. Ethiop. J. Health Sci. 2001;11(2):89-95.
66. Penteado AL, Leitão MFF. Growth of Salmonella Enteritidis
in melon, watermelon and papaya pulp stored at diferent
times and temperatures. Food Control. 2004;15(5):369-73.
https://doi.org/10.1016/S0956-7135(03)00099-9
67. Penteado AL, Leitão MFF. Growth of Listeria mono-
cytogenes in melon, watermelon and papaya
pulps. Int J Food Microbiol. 2004;92(1):89-94.
https://doi.org/10.1016/j.ijfoodmicro.2003.08.020
68. Mutaku I, Erku W, Ashena M. Growth and survival of Esche-
richia coli O 157:H7 in fresh tropical fruit juices at ambient
and cold temperatures. Int J Food Sci Nutr. 2005;56(2):133-9.
https://doi.org/10.1080/09637480500082439
69. Strawn LK, Danyluk MD. Fate of Escherichia coli O 157:H7
and Salmonella spp. on fresh and frozen cut mangoes
and papayas. Int J Food Microbiol. 2010;138(1-2):78-84.
https://doi.org/10.1016/j.ijfoodmicro.2009.12.002
70. Barbosa AAT, Araújo HGS, Matos PN, Carnelossi MAG,
Castro AA. Eects of nisin-incorporated lms on the
microbiological and physicochemical quality of minimally
processed mangoes. Int J Food Microbiol. 2013;164:135-40.
https://doi.org/10.1016/j.ijfoodmicro.2013.04.004
71. Penteado AL, Castro MFPM, Rezende ACB. Salmonella
enterica serovar Enteritidis and Listeria monocytogenes
in mango (Mangifera indica L.) pulp: growth, survival and
cross-contamination. J Sci Food Agriv. 2014;94(13):2746-51.
https://doi.org/10.1002/jsfa.6619
72. Ma C, Li J, Zhang Q. Behavior of Salmonella spp. on
fresh-cut tropical fruits. Food Microbiol. 2016;54:133-41.
https://doi.org/10.1016/j.fm.2015.10.006
73. De Roever C. Microbiological safety evaluations and recom-
mendations on fresh produce. Food Control. 1998;9(6):321-47.
https://doi.org/10.1016/S0956-7135(98)00022-X
74. Bassett J, McClure P. A risk assessment approach for
fresh fruits. J Appl Microbiol. 2008;104(4):925-43.
https://doi.org/10.1111/j.1365-2672.2007.03697.x
75. Feng K, Hu W, Jiang A, Xu Y, Sarengaowa, Li X,
Bai X. Growth potential of Listeria monocytoge-
nes and Staphylococcus aures on fresh-cut tro-
pical fruits. J Food Sci. 2015;80(11):M2548-54.
https://doi.org/10.1111/1750-3841.13089
76. Cardello HMAB, Cardello L. Teor de vitamina C, atividade
de ascorbato oxidase e perl sensorial de manga (Mangi-
fera indica L.) var. Haden, durante o amadurecimento.
Ciênc Tecnol Aliment. 1998;18(2):211-7.
77. Food Safety & Health. pH values of common foods and
ingredients. [place unknown: publisher unknown].
2016[cited 2016 Feb 02]. Available from: http://foodsafety.
wisc.edu/business_food/les/approximate_ph.pdf
78. Tandon DK, Kalra, SK. Pectin changes during the development
of mango fruit cv Dashehari. J Hortic Sci. 1984;59(2):283-6.
https://doi.org/10.1080/00221589.1984.11515198
79. Lima LM, Morais PLD, Medeiros EV, Mendonça V,
Xavier IF, Leite GA. [Postharvest quality of ‘Tainung 01’
papaya formosa traded in dierent types of establish-
ments]. Rev Bras Frutic. 2009;31(3):902-6. Portuguese.
https://doi.org/10.1590/S0100-29452009000300038
80. Benevides SD, Ramos AM, Stringheta PC, Castro VC.
[Quality of the fruits and pulp of Ubá mango]. Ciênc
Tecnol Aliment. 2008;28(3):571-8. Portuguese.
https://doi.org/10.1590/S0101-20612008000300011
81. Branco IG, Gasparetto CA. Response surface metho-
dology applied to the study of temperature eect
on the rheological behavior of ternaries mixtu-
res with mango pulp and orange and carrot jui-
ces. Ciênc Tecnol Aliment. 2003;23 suppl:166-71.
https://doi.org/10.1590/S0101-20612003000400031
82. Correa SF, Souza MS, Pereira T, Alves GVL, Oliveira JG,
Silva MG, Vargas H. Determination of thermal diusi-
vity in papaya pulp as a function of maturation stage.
Rev Bras Frutic Jaboticabal. 2008;30(3):611-5.
https://doi.org/10.1590/S0100-29452008000300008
83. pH values of food products. Food Eng. 1962;98-99.
84. Raybaudi-Massilia R, Calderón-Gabaldón MI,
Mosqueda-Melgar J, Tapia MS. Inactivation of Salmonella
enterica ser: poona and Listeria monocytogenes on fresh-
-cut “Maradol” red papaya (Carica papaya L) treated with
UV-C light and malic acid. J Verbr Lebensm. 2013;8(1):37-
44. https://doi.org/10.1007/s00003-013-0808-1
85. Souza BS, Durigan JF, Donadon JR, Teixeira GHA. [Preserva-
tion of fresh cut ‘Formosa’ papaya stored under refrigera-
tion]. Rev Bras Frut Jaboticabal. 2005;27(2):272-6. Portu-
guese. https://doi.org/10.1590/S0100-29452005000200021
http://www.visaemdebate.incqs.ocruz.br/ Vigil. sanit. debate 2017;5(2):127-140 | 140
Penteado AL. Microbiological safety aspects of mango and papaya
86. Himathongkham S, Riemann H. Destruction of Salmo-
nella typhimurium, Escherichia coli O157:H7 and Listeria
monocytogenes in chicken manure by drying and/or gassing
with ammonia. FEMS Microbiol Lett. 1999;171(2):179-82.
https://doi.org/10.1111/j.1574-6968.1999.tb13430.x
87. Suslow TV. Ozone applications for postharvest disinfec-
tion of edible horticultural crops. Oakland: University
of California; 2004[cited 2017 Feb 6]. Available from:
http://anrcatalog.ucanr.edu/pdf/8133.pdf
88. Zhou B, Luo Y, Millner P, Feng H. Sanitation and design
of lettuce coring knives for minimizing Escherichia coli
O157:H7 contamination. J Food Prot. 2012;75(3):563-6.
https://doi.org/10.4315/0362-028X.JFP-11-218
89. Park S, Navratil S, Gregory A, Bauer A, Srinath I,
Jun M et al. Generic Escherichia coli contamina-
tion of spinach at the preharvest stage: eects
of farm management and environmental fac-
tors. Appl Environ Microbiol. 2013;79(14):4347-58.
https://doi.org/10.1128/AEM.00474-13
90. Rodrigues RQ, Loiko MR, Paula CMD, Hessel CT,
Jacxsens L, Uyttendaele M et al. Microbiological con-
tamination linked to implementation of good agricul-
tural practices in the production of organic lettuce
in Southern Brazil. Food Control. 2014;42:152-64.
https://doi.org/10.1016/j.foodcont.2014.01.043
91. Monaghan JM, Hutchison ML. Ineective hand washing
and the contamination of carrots after using a eld
latrine. Lett Appl Microbiol. 2016;62(4):299-303.
https://doi.org/10.1111/lam.12549
92. Ceuppens S, Hessel CT, Rodrigues RQ, Bartz S,
Tondo EC, Uyttendaele M. Microbiological qua-
lity and safety assessment of lettuce production
in Brazil. Int J Food Microbiol. 2014;181:67-76.
https://doi.org/10.1016/j.ijfoodmicro.2014.04.025
93. Brackett RE. Shelf stability and safety of fresh
produce as inuenced by sanitation and disin-
fection. J Food Prot. 1992;55(10):808-14.
https://doi.org/10.4315/0362-028X-55.10.808
94. Gil MI, Selma MV. Overview of hazards in fresh-cut produce
production: Control and Management of food safety hazards. In:
James J, editor. Microbial hazard identication in fresh fruit and
vegetables. New York: John Wiley & Sons; 2006. p. 156-219.
95. Leifert C, Ball K, Volakakis N, Cooper JM. Control of
enteric pathogens in ready-to-eat vegetable crops in
organic and ‘low input’ production systems: a HACCP-based
approach. J Appl Microbiol. 2008;105(4):931-50.
https://doi.org/10.1111/j.1365-2672.2008.03794.x
96. Hurst WC. Microbiology of fruits and vegetables.
In: Sapers GM, Gorny JR, Yousef AE. HACCP: a process con-
trol approach for fruit and vegetables safety. Boca Raton:
CRC Taylor & Francis; 2006. p. 339-64.
Esta publicação está sob a licença Creative Commons Atribuição 3.0 não Adaptada.
Para ver uma cópia desta licença, visite http://creativecommons.org/licenses/by/3.0/deed.pt_BR.
Conict of Interest
Authors have no potential conict of interest to declare, related to this study’s political or nancial peers and institutions.
