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Assessment of mold and yeast in some bakery products of Lahore, Pakistan

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Article  in  Microscopy Research and Technique · November 2018

DOI: 10.1002/jemt.23103

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DOI: 10.1002/jemt.23103

RESEARCH ARTICLE

Assessment of mold and yeast in some bakery products of

Lahore, Pakistan based on LM and SEM
Iqra Saeed1 | Shabnum Shaheen1 | Khadim Hussain2 | Muhammad Asaf Khan2 |
Mehwish Jaffer1 | Tariq Mahmood3 | Sana Khalid1 | Samina Sarwar1 | Arifa Tahir1 |
Farah Khan1

1
Department of Plant Sciences, Lahore College
for Women University, Lahore, Pakistan
2
Department of Bioinformatics &
Biotechnology, Government College
University, Faisalabad, Pakistan
3
Department of Pharmacy, University of
Central Punjab, Lahore, Pakistan
Correspondence
Department of Plant Sciences, Lahore College
for Women University
Lahore, Pakistan.
Email: shabnum_shaheen78@hotmail.com
Abstract
The present investigation was designed to throw light on the microbial status of bakery products
available in bakeries and supermarkets of Lahore. Different bakery samples such as biscuits, pizza,
patties were collected from different localities such as Anar Kali, Chauburji, Faisal Town, Iqbal Town,
Model Town, Muslim Town were investigated for mold and yeast using serial dilution technique inoc-
ulated over malt extract agar and potato dextrose agar under sterilized conditions. Isolated fungi
were namely Alternaria alternata, Aspergillus niger, Aspergillus flavus, Aspergillus fumigatus, Aspergillus
terreus, Curvularia americana, Fusarium solani, Penicillium digitatum, Saccharomyces cerevisiae, and Geo-
trichum candidum. Results depicted maximum fungal viable count in biscuits, collected from Model
Town while minimum count was in the samples of Chauburji. In the case of pizza, the maximum fun-
gal viable count was found in the sample of Muslim Town. In the case of patties, the maximum fungal
viable count was found in the sample of Muslim Town while minimum count was found in the sam-
ple of Iqbal Town. Prevalence of microorganisms may be due to the use of contaminated raw mate-
rial, use of polluted waters, human handling, and the use of contaminated containers. Contaminated
food intake can lead to measurable signs of liver injury, inflammation, etc. Preventive measures like
washing and drying of hands before preparing food, cleaning of food preparation areas, and the use
of clean equipment can avoid microbes which cause hazards to human health.

Research Highlights
Bakery products of Lahore, Pakistan is investigated for the first time on the basis of light
microscopy (LM) and scanning electron microscopy (SEM) and found very significant to check
the quality of bakery products or not.

KEYWORDS

contamination, microbial examination, mycotoxins, serial dilution, spoilage

1 | I N T RO D UC T I O N
Bakery products (breads, rolls, cookies, pies, pastries, muffins, etc.) are
important staple food in most countries and cultures (Guynot, Marin,
Sanchis, & Ramos, 2003). The consumption of these products is increas-
ing day by day. These products are usually prepared from flour or meal
derived from some form of grains and cooked by dry heat process espe-
cially in some kind of oven. People are affectionate toward these prod-
ucts because of taste, easy to cook, high nutritional value, cheap, and
easy to digest (Pinho & Furlong, 2000). Baked items such as bread and
pastries have a shelf life in the range of 2–5 days, whereas other items
such as biscuits and some type of cakes have a shelf life of several
months when correctly packed. Today, bakery products make a major
component of our daily diet. Several studies in both developed and
developing countries showed that bakery products provide a significant
portion of energy intake (Agte, Tarwadi, Mengale, Hinge, & Chiplonkar,
2002; Bartrina, Rodrigo, Majem, & Rubio, 2004; Vanelli et al., 2005).
Dietary fibers are the functional ingredients used by the food industry
(Chau & Huang, 2003). Dietary fibers include a mixture of plant carbohy-
drate polymers, both oligosaccharides and polysaccharides. Intake of
dietary fiber reduces risk of heart disease, diabetes, obesity, and some
forms of cancer (Mann & Cummings, 2009). It is investigated that bakery

Microsc Res Tech. 2018;1–7. wileyonlinelibrary.com/journal/jemt © 2018 Wiley Periodicals, Inc. 1

2 SAEED ET AL.

Food spoilage is a metabolic process that causes foods to be unde-

FIGURE 1 a: Fungal growth in petri plate, b: Different fungal colonies,
c: Isolation of mold from samples, d: Isolation of yeast from different
samples [Color figure can be viewed at wileyonlinelibrary.com]
products contain high level of refined sugar, white flour, and trans fat,
polyunsaturated fat, carbohydrates with traces of vitamins, proteins, and
minerals (Achterberg, McDonnell, & Bagby, 1994; FAO, 2009).
sirable or unacceptable for human consumption due to changes in sen-
sory characteristics (Doyle, 2007; Edward, 2007; Montville & Matthews,
2008; Smith, Daifas, El-Khoury, Koukoutsis, & El-Khoury, 2004). Micro-
organisms play key role in manufacturing of baked products and also in
the flavoring of the baked products, but microbes also play major role in
the spoilage of the baked products due to inadequate preparatory steps
(cooling, slicing, and transport) (Ponte, 1987). Mold and yeast growth
limits the shelf life of bakery product. It was mainly observed that there
is the production of mycotoxins on the bakery products that may
become the cause of acidification. Mycotoxins are secondary metabo-
lites and toxic to human and animals (Oranusi, Braide, & Oguoma, 2013).
Microbial spoilage is a problem because it can induce nutritional losses,
off-flavors, and potentially allergenic spores. Unwanted fungal growth
can cause food borne diseases which have serious health hazards. Con-
tamination of products by yeasts normally results from unclean utensils
and equipment. The yeast contamination can be maintained by good
manufacturing practices for bakeries. The contamination of bakery prod-
ucts by yeast may be controlled by using aseptic techniques. Mold spoil-
age is a serious problem for bakeries because it limits the shelf life of
bakery products which ultimately leads to economic losses. Consump-
tion of fast food in the world has been associated with obesity leading
to many diseases (Canadian Institute for Health Information, 2007).
Use of bakery products is increasing day by day but sometimes
these products contain high level of contaminants which cause human
illness diseases. So, it is very necessary to caution people about the

FIGURE 2 a: LM of Aspergillis niger, b: LM of Mold, c: Fungal spores, d: Fungal filament, e: Conidial distribution of Aspergillus sp, f: Conidial
dispersal, g: LM of conidiophore, h: LM of mold isolated from bakery items, i: clear LM view of Fungus, j: Microscopic and stained view of Mold
isolation from bakery item [Color figure can be viewed at wileyonlinelibrary.com]
SAEED ET AL.
FIGURE 3 a: SEM of Aspergillus niger, b: Conidiophore under SEM, c:
Conidia under scanning electron microscopy, d: Reproductive Hyphae,
e: mold under SEM, g: Chain of conidia, h: Mold specimens, i: pectoral
view of SEM, j: hyphal view of fungus
level of contamination in bakery products. Literature is deficient of
information about the level of microbial contamination of bakery
products. Hence, there is a need to explore fungal contaminants that
may spoil the bakery products, so that precautionary measures can be
taken that may ultimately lower the value of contaminants. The pre-
sent study aimed at investigation of bakery items with reference to its
safe consumption by human-being, isolation, and identification of
fungi related to spoilage of bakery products in Lahore.
2 | MATERIAL AND METHODS
2.1 | Sample collection
Various samples of bakery products such as (i) biscuits composed of
wheat flour, sugar, cocoa powder, maize starch, egg and milk, (ii) pizza
FIGURE 4 Comparison of yeast value in total yeast count in biscuits
of different localities of Lahore [Color figure can be viewed at
wileyonlinelibrary.com]
3
FIGURE 5 Comparison of different percentage fungal isolates in
patties of different localities of Lahore [Color figure can be viewed at
wileyonlinelibrary.com]
FIGURE 6 Comparison of different percentage fungal isolates in
pizza of different localities of Lahore [Color figure can be viewed at
wileyonlinelibrary.com]
containing yeast, flour, chicken, cheese, and crushed vegetables,
(iii) patties composed of flour, wheat, chicken, yeast, mayonnaise, and
crushed vegetable were collected from different localities of the Lahore.
The visited localities were Anar Kali, Chuburji, Faisal Town, Iqbal Town,
Model Town, and Muslim town. These samples were collected in sterile
plastic bags immediately after purchase. The respective samples were
taken to the laboratory and analyzed within 2 hr after collection.
2.2 | Sterilization
Sterilizer was first cleaned with cotton soaked in 95% ethanol to
ensure microbe-free sterilizing environment. Petri plates and pipette
were washed with distilled water and dried. Petri plates were then
placed in oven (Memmert oven) at 180 C for 2 hr.
2.3 | Media preparation
For the growth of mold and yeast, potato dextrose agar and malt
extract agar media were prepared by following methodology by with
slight modifications.
Potato dextrose agar was prepared by weighing 4 g of potato
dextrose agar and poured it in to a beaker. About 100 ml of water
was added and heated for 2–3 min. Continuous stirring was provided
to the solution during heating to make homogenous mixture. Malt
extract agar was prepared by dissolving 2 g of malt extract and 2 g of
agar in distilled water to make the volume up to 100 ml. The solution
was mixed and gently heated till boiling. After preparation of satu-
rated solutions, 10 ml of the solution was poured in three test tubes.
4 SAEED ET AL.

The test tubes were then covered tightly with cotton plugs. This 2.7 | Percentage contribution of each species
medium was then autoclaved at about 15 lbs and 121 C for 15 min.
To find out percentage contribution following formula was used:
After autoclave, media from test tubes were poured into freshly steril-
ized Petri plates and set to cool. Totalno:of CFU of an individual species
%contribution = × 100
total number of CFU

2.4 | Serial dilution • CFU: colony forming unit

The serial dilution technique was employed according to the work by

Aneja (2003) and Jay, (2005) with slight modifications. For the obser- 3 | RESULTS AND DISCUSSION
vation of mold and yeast, 1 ml of bakery product was transferred to
100 ml of sterilized distilled water. It gave dilution of 1:10. Briefly, 3.1 | Microorganisms isolated from bakery samples
1 ml of suspension from 1:10 was transferred to second test tube
In the present study, distribution and incidence of food pathogens in
which gave 1:100 dilutions. Similarly 1:1,000, 1:10,000, and
bakery products from different localities of Lahore were identified.
1:100,000 dilutions were made. Dilutions were transferred to the
The result revealed that a total of ten species were isolated. Out of
sterilized Petri plates containing media. Then these Petri plates were
which eight species of mold and two species of yeasts were identified
incubated at 30  2 C for 3–7 days for microscopic and macroscopic
that were mentioned in Table 1.
identification.

3.2 | Total viable count of mold and yeast in biscuits

2.5 | Mold and yeast count
After incubation plates, numbers of Petri plates were counted and
multiplied by dilution factor to find out the number of spores per gram
of a sample.
No:of spores=g = No:of colonies × Dilution factor:
 
Dilution factor = Reciprocal of dilution e:g:,10 − 5 = 105 :
2.6 | Identification
Fungi were identified on the basis of morphological and cultural char-
acteristics such as color of the colony, surface, appearance according
to the methods described in “Fungi and Food Spoilage” (Pitt & Hock-
ing, 2009).
In the case of biscuits, maximum fungal count was found in samples of
Chauburji (10.56 cfu/ml) and minimum count in Iqbal Town (6 × 103
to 8 × 10–3 cfu/ml). Maximum yeast count was found in Muslim Town
(3.48 cfu/ml), minimum count was in Model Town (3.00 cfu/mL).
High mold count may be due to high sugar contents because they
tend to support the growth of the mold better than other microbes,
but some other yeast can also attack on the products. These results
were in agreement with the previous studies as poor handling and
storage condition can be a cause of contamination (Odumeru et al.,
1997; Pelczar, Chane, & Kreig, 2006; Woodward, 1996). Several fac-
tors cause food contamination such as hands, wiping cloths, and uten-
sils (chopping boards and knives) because even a minor interaction
with food can transfer microorganisms. Meng and Doyle (1998) also
reported that mode of handling, time of storage, and conditions of

TABLE 1 Species of mold and yeast in bakery products from different localities of Lahore

Biscuits Patties Pizza

Locality Mold Yeast Mold Yeast Mold Yeast
Anar Kali A. niger, F. solani, A. terreus, A. niger, F. solani, A. niger, A. terreus, S. cerevisiae,
A. flavus, C. americana A. terreus, A. flavus C. americana, F. solani, G. candidum
P. digitatum
Chuburji A. Niger, A. alternata, S. cerevisiae, A. niger, A. fumigatus, S. cerevisiae, A. niger, A. alternata, S. cerevisiae,
P. digitatum G. candidum A. alternata, G. candidum P. digitatum G. candidum
P. digitatum
Faisal Town A. niger, A. terreus, A. niger, A. fumigatus, G. candidum A. niger, A. fumigatus, S. cerevisiae,
A. alternata, F. solani A. alternata, A. alternate, G. candidum
C. americana P. digitatum
Iqbal Town A. niger, A. fumigatus, S. cerevisiae A. fumigatus, S. cerevisiae, A. fumigatus, F. solani S. cerevisiae
A. alternata, F. solani A. terreus
Model Town A. niger, A. terreus, A. flavus, S. cerevisiae, A. niger, A. flavus, S cerevisiae, A. terreus, A. flavus, S. cerevisiae,
A. fumigatus, A. alternata, G. candidum A. alternata, G. candidum P. digitatum G. candidum
P. digitatum P. digitatum
Muslim Town A. niger, F. solani A. terreus, S. cerevisiae, A. niger, A. terreus, S. cerevisiae, A. niger, A. terreus, S. cerevisiae,
A. flavus, A. alternata, G. candidum A. flavus, G. candidum A. flavus, A. alternata G. candidum
A. alternata

1: A. niger = Aspergillus niger; 2: A. flavus = Aspergillus flavus; 3: A. terreus = Aspergillus terreus; 4: A. fumigatus = Aspergillus fumigatus;
5: A. alternata = Alterneria alternate; 6: C. americana = Curvularia americana; 7: F. solani = Fusarium solani; 8: P. digitatum = Penicillium digitatum;
9: G. candidum = Geotrichum candidum; 10: S. cerevisiae = Saccharomyces cerevisiae.
SAEED ET AL. 5

TABLE 2 Cultural, morphological, and microscopic features of identified species

Shape and
Size diameter of Conidial head shape
Species name (mm) Colony shape and color vesicle and size Seriation Conidiophore
Aspergillus niger 45–55 Black densely packed Sub-globose Globose 4–6 μm Biserate Brownish, long
conidia 37–52 μm conidiophore
with smooth surface
Aspergillus terreus 45–55 Brown Sub-globose Columnar 3–5 μm Biserate Colorless, short, smooth
26–43 μm conidiophore
Aspergillus flavus 50–55 Light green mycelia Radiate Columnar 3.5–5 μm Uniseriate Colorless relatively
with white 18–36 μm OR Biserate short rough
boundaries conidiophore
Aspergillus fumigatus 24–40 Bluish green with rough Spathulate to Short columnar 2–3 μm Uniserate Smooth wall, long, erect
texture Clavate
19–31 μm
Alternaria alternata 20–32 Black with entire Ellipsoid Obclavate 8–12 μm, Biserate 3–5 transverse,
margins 20–35 μm 1 longitudinal, solitary
or in small fascicles
Curvularia americana 18–37 Black to green Clavate Columnar 3.8–6.3 μm Biserate Solitary or groups, rarely
11–20 μm branched, straight or
curved
Fusarium solani 53–59 Wooly white Pyriform Globose 2.5–3.5 μm Biserate Short monophialides
17–40 μm
Penicillium digitatum 45–50 Dark green with Radiate Radiate 4.0–4.5 μm Uniserate Branched conidium
Velvety touch 19–35 μm
Saccharomyces cerevisiae 45–55 Creamy white Ellipsoid Globose 4.8–12.5 μm Uniserate
25–30
Geotrichum candidum Creamy white Sub-globose 2.4–2.5 μm
6–12 μm

storage could be a source of contamination. Aspergillus niger was com-
mon in all biscuits samples, showing that it can grow on all the food
samples. Change in nutrient composition, moisture, and pH do not
affect its growth. Study by Rompré, Servais, Baudart, de-Roubin, and
Laurent (2002) also demonstrated that A. niger mostly occur in water,
soil, and fecal matter because water, soil, and vegetation are their nat-
ural habitat.
3.3 | Total viable count of mold and yeast in patties
Maximum mold count in patties sample was found in Muslim Town
(5.78 cfu/ml) and minimum count was in Faisal Town (3.30 cfu/ml).
Higher yeast count was in Iqbal Town (5.30 cfu/ml) and lower count
was in Model Town (3.30 cfu/ml). Contamination level in patties
sample might be due to unhygienic condition under which patties
were manufactured in bakery. So, microbes were continuously added
from air and utensils. In patties sample, patties in which main ingredi-
ent is vegetable is highly lauded with microorganisms. Total mold
count is 10 × 103 and 3 × 103 for Yeast. This agrees to the previous
report by Uzeh, Alade, and Bankole (2009), they also isolated Mucor
sp., Aspergillus fumigatus, and A. niger from salad consisting of fresh
vegetables. Micro biota of patties reflects the quality of vegetables
and chicken, the unsanitary conditions of the equipment used to
manufacture the patties. Microbial contamination in patties sample
which have chicken and vegetable is highly contaminated. In such
kind of samples entry of microbes is due to raw meat and poor sani-
tary conditions. This agrees with the report by Kayaardi, Kayacier,
and Gok (2006). As they reported, several factors causing microbio-
logical contamination in bakery products are quality of uncooked
meat and other ingredients, conditions of utensils, improper cooking,
and sanitary practices.
3.4 | Total viable count of mold and yeast in pizza
In the case of pizza sample, maximum mold count was in Muslim town
(5.78 cfu/ml) and minimum count was in Model Town (2.48 cfu/ml).
Maximum yeast count was in Muslim town (5.30 cfu/ml) and mini-
mum count was in model Town (2.48 cfu/ml). Contamination in pizza
may be due to pizza bread. Water is the important factor encouraging
the microbiological contamination in bakery products. High moisture
level promotes the growth of yeasts and molds in bakery products
(Frazier & Westhoff, 2000; Jay et al., 2005). As ingredients of pizza
are chicken, vegetable, and cheese, microorganisms found in the sam-
ple were usually common as in previous studies. Yeast isolates usually
present on the surface of vegetables cause contamination in products.
Vegetables have high water content that may encourage spoilage if
not preserved well. The isolation of A. niger from vegetables is further
confirmed by studies by Efiuvwevwere (2000) and Chuku, Ogbonna,
Onuegbu, and Adeleke (2008). Onyia et al. (2005) also separated
A. niger from rotten tomato. Our findings substantiate the findings by
Woodward (1996). Vegetables and meats were mainly contaminated
with pathogens and this may be due to unsterilized method of han-
dling, the long-term storage period, and poor conditions of storage.
Due to the presence of several nutrients in food, growth of microbes
increased (ICMSF, 1996; Makukutu & Guthrie, 1986; Odumeru et al.,
1997; Pelczar et al., 2006; Smith & Fratamico, 1995). The presence of
yeast and mold indicates after baking contamination. Usually fungal
spores are killed by baking process and spoilage is caused by post
6 SAEED ET AL.

backing. High level of contaminated air with spores of fungus in bak-

log 10 cfu/g
eries often attributed to the high level of contaminated products.

Yeast

5.30
3.60
4.85
5.30
3.00
5.30
4 | CO NCLUSIO N

Muslim Town

log 10 cfu/g
The present study mentioned the presence of yeast and mold in the

Mold

3.78
3.85
4.70
5.78
3.78
5.78
studied samples of District Lahore, Pakistan. So care should be taken
log 10 cfu/g by the manufacturing industries to avoid the contamination in the
bakery products as it can be hazardous for the people health. The
sterilized and health safety methods should be used during processing
Yeast

3.00

3.60
2.48
3.00
4.00
of the goods.
–
Model Town

log 10 cfu/g

ACKNOWLEDGMENT
Mold

The authors acknowledge the Department of Botany Government

3.78
3.95
3.30
3.30
3.60
4.00

College of Science Wahdat Road, for providing Laboratory facilities

for the analysis of mold and yeast.
log 10 cfu/g
Yeast

3.48
3.48
4.30
3.00

5.30

C ON FL I CT OF I N TE RE ST
–
Iqbal Town

The authors declare that there are no conflicts of interest regarding

10 cfu/g

the publication of this paper. It is confirmed that Department of Bot-

Mold

5.30
3.00

3.60
4.48
log

any, Lahore College for Women University, Lahore and Government

–

College of Science Wahdat Road in Lahore did not provide any fund-
log 10 cfu/g

ing and did not lead to any conflicts of interest regarding the publica-
tion of this paper.
Yeast

3.00
3.30

5.00
–
–

ORCID
log 10 cfu/g
Faisal Town

Shabnum Shaheen https://orcid.org/0000-0002-9178-6963

Mold

3.78
3.90
3.60
3.00
3.30
5.00

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How to cite this article: Saeed I, Shaheen S, Hussain K, et al.
Assessment of mold and yeast in some bakery products of
Lahore, Pakistan based on LM and SEM. Microsc Res Tech.
2018;1–7. https://doi.org/10.1002/jemt.23103