Microbiological Analyses and Safety Evaluation of Nono: A Fermented Milk Product Consumed in Most Parts of Northern Nigeria
Ogbonna Innocent Okonkwo
Microbiological analyses and safety evaluation of nono was investigated by assaying for the presence of some microorganisms frequently implicated in food safety problems and spoilages including E. coli, S. aureus, Shigella and Salmonella sp. Others included aerobic mesophilic, anaerobic mesophilic, psychrotrophic microorganisms and yeasts and mould counts. E. coli, S. aureus, Shigella, Salmonella, aerobic mesophilic, anaerobic mesophilic, psychrotrophic microorganisms and yeasts and moulds were isolated in varying degrees with a range of 7.89, 6.60, 6.00, 6.50, 8.90, 6.30, 4.30 and 4.30 log10 cfu mL-1, respectively. Overall mean values of these counts were also 2.21, 1.51, 0.30, 1.17, 3.76, 1.76, 0.76 and 1.23 log10 cfu mL-1, respectively. Present Laboratory prepared nono did not contain any of the assayed organisms. There was statistically significant (p<0.05) difference between the means of the microbial groups at 95% confidence interval. Of the market nono samples analyzed, 86 (43%), 56 (28%) and 16 (8%) were positive for E. coli, S. aureus and Shigella sp., respectively. 48 (24%) harboured Salmonella sp. Shigella sp. was not detectable in three areas under study while E. coli approximately had the highest number of occurrence. Nono consumed in the said area has potential health risks to consumers. Proper hygiene in the process-line of nono was recommended.
Received: March 04, 2011;
Accepted: July 16, 2011;
Published: August 02, 2011
Nono (Hausa) is an opaque white to milky coloured liquid food drink got
from fermented raw milk. It is a healthful food whose consumption transverses
the Saharan tribes of West African Sub-region extending to the inhabitants of
the Mediterranean region and also the Middle East. In the Middle East, it is
called dahi or lassi (Nahar et al.,
2007). Nono also called nunu by some tribes in Nigeria contains good quantities
of amino acids, calcium, phosphorous and vitamins A, C, E and the B complex
(Nebedum and Obiakor, 2007).
Predominantly, nono is being prepared and hawked by the nomadic Hausa/Fulani
cattle herdsmen, who control over 80% of Nigerians cattle production.
Consumption of nono was limited to Fulani/Hausa indigenous (Obi
and Ikenebomeh, 2007; Adesokan et al., 2011)
since most non indigenous see their preparation as apparently unhygienic and
since it has poor shelf life (Yahuza, 2001) it is gaining
wider acceptance nowadays.
Raw milk has low keeping quality and at room temperature, spontaneous microbial
spoilage occurs turning the product sour few some days. This is brought about
by the activity of lactic acid bacteria (Wouters et al.,
2002). Depending on its preservation and process-line, microorganisms other
than lactic acid bacteria could be found in the nono. Milks nutritional
composition makes it not only suitable for human nutrition but also ideal for
microbial life. The growth of microorganisms in food could make the food grossly
unwholesome and harmful to consumers. Outbreaks of milk-borne diseases have
occurred despite pasteurisation, as a result of either improper pasteurisation
or product recontamination (Altekruse et al., 1998;
Da Silva et al., 1998; Hartman,
1997; Nebedum and Obiakor, 2007).
It is noticed that raw milk often contains microorganisms which may likely
cause foodborne diseases (Adesiyun et al., 1995;
Headrick et al., 1998; Steele
et al., 1997). Even when the milk is fermented, the fermentation
process with the attendant drop in pH may not rid the product of these organisms
and may be carried to consumers. Salmonellae and other microorganisms
have been known to underscore the importance of milk and milk products as vehicle
for human infections. For these reasons, McEwes et al.
(1988) reasoned that the presence of Salmonellae and other human
pathogens in unpasteurized milk is a public health hazard. Food safety guideline
for food banks recommends that milk and milk products including cream and cream
products, ice cream, frozen desserts, yoghurt and similar foods must be pasteurized,
held and distributed in their original unopened containers.
Different categories of microorganisms including fungi, bacteria, rickettsia and viruses could be found in milk since the udder of the animal could harbour organisms while others come as contaminants due to poor handling. Most handlers or sellers of nono are street peddlers. Often, not all nono sent to the market by peddlers is sold the same day and in most developing countries, such unsold ones have to go back to market with no special attention to preservation or safety. Thus pathogenic organisms that might have gained access into the product have enough time to multiply and/or produce harmful metabolites. The present work was aimed at investigating the microbiological quality and safety of nono consumed in Maiduguri, Nigeria.
MATERIALS AND METHODS
Sample collection: Nono samples were purchased from five different markets namely: Bulunkutu, Gwange, Monday, Bama Road Motor Park and Unimaid Motor Park Markets all within Maiduguri metropolis. Forty samples were randomly purchased from each of the markets. Purchased samples were transported to the University of Maiduguri Microbiology Laboratory in sterile corked plastic tubes packed in iced container. Purchases were done between 9.00 am and 11.00 am each day lasting from September 2009 to February 2010. Our laboratory prepared nono got from fresh cow milk (purchased at Fulani Farm in Maiduguri) was also analysed.
Nono preparation and consumption: It is produced from cow milk collected
in calabash and allowed to ferment naturally for 24h (Eka
and Ohaba, 1977; Olasupo et al., 1996).
Microbiological analyses: Nono samples approximately 40 mL each contained
in pre-autoclaved containers were used for the isolation and enumeration of
the microorganisms. In each isolation protocol, nono sample was shaken and 10
mL of the sample was aseptically introduced into 90 mL of sterile normal saline
solution and homogenized by shaking followed by further decimal dilutions to
up to 10-6 concentrations. A 0.1 mL quantity of appropriately diluted
sample was used to inoculate freshly prepared media and surface-plated. Media
employed for the isolation and enumeration of the organisms included: Baird
Parker Medium (BPM) (Lab M. Ltd, Bury Lancashire BL9 6As, United Kingdom) for
S. aureus; Eosine Methylene Blue Agar (EMBA) (Himedia Laboratories Pot
Ltd, India) for E. coli and Desoxycholate Citrate Agar (DCA) (Park Scientific
Limited, Moultan Park, Northampton) for Salmonella and Shigella
spp. Nutrient Agar (NA) (Biotech Lab. Ipswich, UK) was used for aerobic mesophilic,
anaerobic mesophilic and psychrotrophic microorganisms counts. Yeasts
and mould counts were carried out on a Potato Dextrose Agar (PDA) (Lab M. Ltd,
Bury Lancashire BL9 6As, United Kingdom) plate. Media were sterilized by autoclaving
at 121°C for 15 min except DCA which involved only boiling over gauze. In
all cases of colony counts, the resulting colonies following inoculation and
incubation were counted using digital colony counter (Labtech, New Delhi, India).
Aerobic mesophilic counts (AM): Inoculated NA plates were incubated at 30°C for 48 h.
Anaerobic mesophilic counts (AAM): Inoculated NA plates were incubated
in anaerobic jars (Equtron) containing heated iron nail and candle as recommended
by Cheesbrough (2004) at 30°C for 48 h.
Psychrotrophic microorganisms counts: Inoculated NA plates were incubated at 6.5°C for 24-48 h.
Yeasts and moulds counts: PDA plates containing Chloramphenicol were inoculated as above. Incubation was at 28°C for 5 days. Colonies were thereafter counted.
Isolation and enumeration of E. coli: EMBA plates were inoculated as described previously and incubated at 37°C for 48 h after which typical colonies with greenish metallic sheen were subjected to biochemical tests for E. coli.
Isolation and enumeration of S. aureus: BPM were inoculated as
above and incubated at 37°C for 48 h. Greyish-black or black colonies with
or without a halo were presumptively identified as Staphylococci as recommended
by Macfaddin (1977) and coagulase test was carried out
to further characterize S. aureus.
Isolation and enumeration of Salmonella and Shigella sp:
Isolation and enumeration of Salmonella and Shigella sp. was as
recommended by Macfaddin (1977).
Biochemical identification of the isolates: The biochemical tests for
the identification of the isolates were the citrate utilization, indole, methyl-red,
Voges-proskauer, Triple Sugar Iron (TSI), urease, oxidase, coagulase and catalase
tests. Cowan and Steel (1965) and Cheesbrough
(2004) procedures were used for these biochemical tests.
The sample pH: The pH of various samples was measured using a pH meter (WPA pH Meter, India) after standardization with pH 4, 10 and 7 buffers (BDH England).
Statistical analysis: Data were analyzed by Multiple-sample comparison using STATGRAPHICS Centurion XVI Version 16.1.05 (32-bit). A one-way analysis of variance was performed and when the F-test in the ANOVA was significantly (p≤0.05) different between the means, Multiple range tests were conducted to tell which means were significantly different from others.
||Mean microbial counts (counts were expressed as log10cfu
mL-1) and mean pH of samples of nono from different markets in
|NB: Ec: E. coli, Sa: S. aureus, Sg: Shigella,
Ss: Salmonella counts, Am: Aerobic mesophilic, Aam: Anaerobic mesophilic
counts, Pm: Psychrotrophic microorganism, Ym: Yeast and mould counts. *Indicate
statistically significant difference (p<0.05) between organisms in the
column and other organisms in the same row
||Minimum and maximum values of count of microorganism isolated
from different markets in Maiduguri
|Counts were expressed as log10 cfu mL-1.
Total No. of samples = 40 from each market. NB: Ec: E. coli, Sa:
S. aureus, Sg: Shigella, Ss: Salmonella counts, Am:
Aerobic mesophilic, Aam: Anaerobic mesophilic counts, Pm: Psychrotrophic
microorganism, Ym: Yeast and mould counts
E. coli count (log10 cfu mL-1): The mean
E. coli counts (log10 cfu mL-1) were between 1.37
and 3.29 from the different markets (Table1) with an overall
mean of 2.21 log10 cfu mL-1. The mean E. coli count
of Unimaid was significantly higher (p≤0.05) than Monday, Gwange and Bama
but homogeneous with Bulunkutu market. E. coli count from different markets
ranged from 0.0 to 7.89 log10 cfu mL-1 (Table
S. aureus count (log10 cfu mL-1): The mean S. aureus counts fell between 2.98 and 0.76 with an overall mean of 1.51 log10 cfu mL-1 (Table 1). The mean S. aureus count of Bulunkutu market was significantly higher (p≤0.05) than that got from other markets. The S. aureus count of the samples ranged from 0.0 to 6.60 log10 cfu mL-1(Table 2).
Shigella sp count (log10 cfu mL-1): The mean Shigella count was between 0.0 and 0.92 and had an overall mean of 0.30 log10 cfu mL-1. There was no significant (p≤0.05) difference between the means of Shigella from the markets. The range values of count of Shigella fell between 0.0 and 6.0 and percentage distribution between 0.0 and 12.0. Shigella was not isolated from three markets under study (Table 1-3).
Salmonella count (log10 cfu mL-1): The mean Salmonella count was between 0.43 and 2.37 and the overall mean was 1.17 log10 cfu mL-1(Table 1). Bulunkutu market value was significantly higher (p = 0.05) than that of other markets. The range value of counts of Salmonella was between 0.0 and 6.5 and the distribution and percentage frequency of occurrence between 4.0 and 22.0 (Table 3).
|| Distribution and (%) frequency of occurrence of different
microorganisms isolated from nono samples
|Values in parenthesis are individual market (%) frequency.
In each market, 40 nono samples were analysed (n = 40)
Aerobic mesophilic count (log10 cfu mL-1) (AMC): The mean AMC from the different markets fell between 2.53 and 4.89. The overall mean AMC was 3.76 log10 cfu mL-1 (Table 1). There was no significant difference between the means of AMC (Table 2). The range values of AMC fell between 0.0 and 8.90.
Anaerobic mesophilic counts (log10 cfu mL-1) (AAMC): The mean AAMC was between 0.69 and 4.09 with an overall mean of 1.76 log10 cfu mL-1 (Table 1). There was a significant (p≤0.05) difference between the means obtained from Bulunkutu and other markets analysed. The range values of AAMC were between 0.0-6.30 (Table 1).
Psychrotrophic microbial count (PMC) (log10 cfu mL-1): The mean PMC (log10 cfu mL-1) was between 0.86 and 6.45 from the different markets. The overall market mean for PMC was 0.76 log10 cfu mL-1 (Table 1). There was no significant difference between the means obtained from the markets. The range values of PMC fell between 0.0 and 4.3 (Table 2).
Yeast and mould count (YMC) (log10 cfu mL-1): The mean YMC fell between 0.81 and 1.61. The overall mean YMC was 1.23 log10 cfu mL-1 (Table 1). There was no significant difference between the mean values obtained from the markets. The range values of YMC from the markets were between 0.0 and 5.00 (Table 2).
The sample pH: The pH range of the nono samples from the various markets was between 3.8 and 5.4 (Table 1).
The presence of E. coli (43%), S. aureus (28%), Shigella
(8%) and Salmonella (24%) in nono sold within Maiduguri Metropolis is
quite high to attract public health attention. From the results, E. coli
was the most frequent isolate (Table 1-3).
Results obtained for % E. coli content of the samples fell within the
range of 15-65 which supports that obtained by Soomro et
al. (2002) but lower than not detectable to 20% reported by Ekici
et al. (2004) and 2.5% by Mohamed and El-Zubeir
(2007). The mean E. coli count of log 2.21 cfu mL-1 supports
that obtained by Abdalla and El-Zubeir (2006). While
originally E. coli had been associated with the contamination of milk
and milk products (Kulshrestha, 1990), researches have
linked the presence of E. coli with the presence of other enteric pathogens
(Adesiyun et al., 1995; Norwegian
Food Control Authority, 1994; Smoot and Pierson, 1997;
Van den Berg, 1988).
The mean S. aureus counts (log10 cfu mL-1) of
1.51 contradicts a lower mean of 0.48 obtained by Abdalla
and El-Zubeir (2006) from yoghurt samples and the % distribution in samples
of 28 was lower than 75% obtained by Ekici et al.
(2004) from cow milk and 60% from goat milk Tormo et
al. (2011). The range value of count of S. aureus between 0.0
and 6.60 also contradicts Abdalla and El-Zubeir (2006)
results of 0.00-2.90 log cfu mL-1. Processing operations and fermentation
parameters could have brought about the discrepancy. The presence of S. aureus
in the milk samples corroborates the finding of Tormo et
al. (2011) that Staphylococcus was the dominant bacterial sp.
of milk and inferior health condition of the animal increased the contamination
of milk with Staphylococci. Jablonski and Bohach (1997)
noted that S. aureus could be spread from humans to food by direct contact,
indirectly by skin fragments, or through respiratory tract droplet nuclei. Mastitis
udder also harbours S. aureus (Wellenberg et al.,
2002). Consequently, milk from mastitis cows could be another reservoir
for S. aureus (Gran et al., 2002). The
range of S. aureus in this study exceeded the estimated minimum for the
organism to produce intoxication and also, the pH (3.8-5.4), temperature (30-45°C)
and the holding time conditions agreed with the requirement for S. aureus
to produce sufficient enterotoxin (Rorvik and Granum, 1999).
Shigella sp. was not detectable in three areas under study. This organism
is not an intrinsic flora of the animal; therefore, contamination of the fermented
milk with the organism could have arisen from handling. Twenty-four percent
of the assayed samples showed the presence of Salmonella spp. The mean
Salmonella counts (log cfu mL-1) of 5.9 contradicts 1.12 obtained
by Abdalla and El-Zubeir, (2006) and % distribution
of 24 contrasts not detectable reported by Ekici et al.
(2004) and Mohamed and El-Zubeir, (2007). Salmonella
are pathogens that could originate from the animals themselves. Thus, presence
of Salmonella in fermented milk is not surprising since they could either
be transmitted from the animal before preparation or could have come via cross
contamination. Since, these organisms including E. coli and S. aureus
were not isolated from our laboratory prepared nono, it is possible to get pathogen-free
nono via general hygiene of the process line thereby saving consumers from the
potential health risks.
The aerobic mesophilic count (AM) ranged from not detectable 0 to 8.9 log10
cfu mL-1 and the mean AM counts was 3.76 log10 cfu mL-1
(Table 2). The mean aerobic mesophilic count (log cfu
mL-1) of 3.76 agreed closely with 3.6 average bacterial counts of
Tormo et al. (2011). Aerobic colony count is
useful for indicating the overall microbial quality of food product. It generally
does not relate to food safety hazards but acts as an indicator for food quality
and shelf-life duration (Pianetti et al., 2008).
Except for Bulunkutu, anaerobic organisms were generally very low throughout
the study. The reason for this could be their absence during nono preparation
and distribution. The mean Psychrotrophic microbial counts (log cfu mL-1)
of nono were low throughout the counts with ranges between 0 and 4.3 log10
cfu mL-1. It stands to reason that storage of the product at such
temperature could increase its shelf life.
The mean YMC of 1.23 log10 cfu mL-1 was higher than not
detectable recorded by Ukwuru and Ogbodo (2011) from
fermented tigernut- a milk product but however contradicts higher value of 3.48
reported by Awad et al. (2006) from similar product.
Range yeast and mould count of 0.81-1.61 was partly in support of 1.44-2.06
obtained by Nahar et al. (2007) but lower than
1.83x103-3.7x106 obtained by Savadogo
et al. (2004). The reason for the contradictions could be linked
to the chance fermentation practiced by many local producers as differences
in YMC of the same product from different manufacturers had been documented
(El-Bakri and El-Zubeir, 2009). Yeasts are known to
cause spoilage in products such as yoghurt and sour milk; however they are also
important because they produce desirable favours as in cheese ripening (Fleet,
1990; Rohm et al., 1992; Jakobsen
and Narvhus, 1996). The mean YMC of 1.23 log10 cfu mL-1
(Table 1) was lower than 105-106 cells
g-1 reported to cause pronounced spoilage (Fleet,
The pH range of samples between 3.8 and 5.4 supports that obtained by El-Bakri
and El-Zubeir (2009) but however contradicts 5.51-6.29 reported by Adesokan
et al. (2011) and 5.7 by Obi and Ikenebomeh (2007).
The differences in pH could be as a result of some factors including; length
of fermentation and the starter culture. If the keeping time of nono increases
prior to consumption, the acidity increases and his determines the number and
kind of contaminating organisms.
The significant (p≤0.05) difference between the means of the microbial groups
in this study could be due to lack of standardized method of nono preparation,
or the health status of the milk producing animal or other environmental variables.
The recommendation of the food safety guideline for the pasteurization of food
like milk and distribution in unopened form for food safety could account for
the many microorganisms isolated from the nono. The practice of preparation
and distribution of nono in open calabash contravenes such principles. Proper
hygiene in the process-line of nono is recommended since the markets selected
were the major nono selling points in Maiduguri and since the laboratory prepared
nono had no detectable pathogen.
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