https://doi.org/10.52973/rcfcv-e34301
Received: 08/08/2023 Accepted: 25/10/2023 Published: 02/01/2024
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Revista Científica, FCV-LUZ / Vol. XXXIV, rcfcv-e34301
ABSTRACT
The main goal of this article was to conduct a meta–analysis, to
estimate the hygienic quality of the raw milk intended for human
consumption and subsequently relative risk factors that may impact
milk quality in Algeria. Weighted random–effects meta–analysis
models were employed to analyze the data in this study. A total of
4,685 sampling results from 61 included studies, investigating the
bacterial quality of raw milk across 35/48 Provinces in Algeria, from
2009 to 2022. In this meta–analysis, the average level of contamination
by Total Aerobic Mesophilic Bacteria (TAMB) was 5.84 log
10
CFU·mL
-1
.
95% CI [5.55–6.13]. The P–value was 0.001. The I
2
test indicates the
presence of substantial statistical heterogeneity across studies;
(I
2
=86.26%, P<0,001). No signicant publication bias was observed
using the funnel plots and Egger’s test (P=0.885). In this article TAMB
values did not differ signicantly among species (P>0.05).The average
contamination level TAMB was lower in milk samples collected from
individual milking and farm tank milk (4.57 log
10
CFU·mL
-1
and 5.89 log
10
CFU·mL
-1
), compared to those recorded in milk samples collected from
the collector, dairy, and sales (6.59 log
10
CFU·mL
-1
, 6.60 log
10
CFU·mL
-1
,
and 6.74 log
10
CFU·mL
-1
, respectively). The contamination level of milk
by TAMB was higher during summer and spring (6.80 log
10
CFU·mL
-1
and 6.70 log
10
CFU·mL
-1
), compared to winter and autumn (4.27 log
10
CFU·mL
-1
and 5.64 log
10
CFU·mL
-1
).
Key words: Cow’s milk; camel’s milk; goat’s milk; sheep’s milk; total
aerobic bacteria
RESUMEN
El objetivo principal de este artículo fue llevar a cabo un meta–análisis
para estimar la calidad higiénica de la leche cruda destinada al consumo
humano y posteriormente identicar los factores de riesgos relativos
que pueden afectar la calidad de la leche en Argelia. Se utilizaron
modelos de metaanálisis de efectos aleatorios ponderados para
analizar los datos en este estudio. Se obtuvieron un total de 4.685
resultados del muestreo de 61 estudios incluidos, que investigaron la
calidad bacteriana de la leche cruda en 35/48 provincias de Argelia,
desde 2009 hasta 2022. En este metaanálisis, el nivel promedio de
contaminación por Bacterias Mesólas Aerobias Totales (TAMB) fue
de 5,84 log
10
UFC·mL
-1
, IC del 95 % [5,55–6,13]. El valor de P fue 0,001.
La prueba I
2
indica la presencia de una heterogeneidad estadística
sustancial entre los estudios (I
2
=86,26 %, P<0,001). No se observó
sesgo signicativo de publicación utilizando los grácos de embudo y
la prueba de Egger (P=0,885). En este artículo, los valores de TAMB no
diferían signicativamente entre especies (P>0,05). El nivel promedio de
contaminación (TAMB) fue más bajo en las muestras de leche recogidas
de ordeño individual y de tanques de granja (4,57 log
10
UFC·mL
-1
y
5,89 log
10
UFC·mL
-1
, respectivamente), en comparación con aquellos
registrados en muestras de leche recogidas de recolectores, lecherías
y ventas (6,59 log10 UFC·mL
-1
, 6,60 log
10
UFC·mL
-1
y 6,74 log
10
UFC·mL
-1
,
respectivamente). El nivel de TAMB fue más alto durante el verano y la
primavera (6,80 log
10
UFC·mL
-1
y 6,70 log
10
UFC·mL
-1
), en comparación
con el invierno y el otoño (4,27 log
10
UFC·mL
-1
y 5,64 log
10
UFC·mL
-1
).
Palabras clave: Leche de vaca; leche de camello; leche de cabra;
leche de oveja; bacterias aeróbicas totales
The Hygienic Quality of Raw milk intended for Human consumption in
Algeria: Meta–analysis
La calidad higiénica de la leche cruda destinada al consumo humano en Argelia: Metaanálisis
Nadjah Guergueb
1,2
*
1
University of Batna 1, Department of Veterinary Medicine. Batna, Algeria.
2
University of Biskra, Department of Agricultural Sciences. Biskra, Algeria.
*Corresponding author: g.nadjah@yahoo.fr
FIGURE 1. Annual milk production from dierent lactating mammals intended
for human consumption in Algeria (1961–2021). Source FAOSTAT (Mar 30,2023)
Meta-analysis of the microbiological quality of raw milk / Guergueb ________________________________________________________________
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INTRODUCTION
Milk has played a major contribution to the human diet in many
different Countries across the World since the dawn of time [1].
Nutritional richness is unquestionable; it is a good source of high
biological value proteins in addition to important vitamins and
essential minerals [2]. Cow’s milk is a rich and cheap source of protein
and calcium, and a valuable food for bone health [3]. Globally, 16.9%
of milk consumed by humans comes from species other than bovine
(Bos taurus) [4]. There has been an increased interest in Caprine
(Capra hircus) milk and goat milk products Worldwide because of their
high nutritional content and health benets. Goat milk has various
effects on human health considering the total solid, fat, protein,
lactose, mineral, and vitamin contents [5]. The benecial role of
Ovine (Ovis aries) milk results from its fatty acid, immunoglobulin and
non–immune protein contents [6]. Consumption of sheep milk may
positively inuence the structural integrity of bone, which may result
in an enhancement of bone health [7]. The unique physicochemical
and biochemical properties of sheep milk also include prebiotics and
probiotics which make it perfect functional food for human health
promotion and disease risk reduction [6]. Camel (Camelus bactrianus)
milk showed more nutritional and medicinal properties than other
ruminant milks [8], camel milk has anti–microbial and antioxidant
properties, camel milk may be a good add–on against breast cancer,
liver cancer, human colorectal cancer and hepatitis to relieve the
oxidative stress [9].
Composition, nutritional value, and other intrinsic factors, make
milk and many milk products attractive for the growth of a variety of
microorganisms under suitable conditions [10]. The consumption of
raw milk poses a risk to public health due to potential contamination
with human pathogenic microorganisms [11]. Moreover bacterial
contaminants can cause spoilage of milk and its secondary products
[12]. After milking, contaminating microorganisms from equipments
and utensils, from environment and even from the employees
responsible for obtaining and handling milk, are the most important
sources of contamination [13].
With an average consumption of 130 L of milk per person per year,
Algeria is the largest consumer of milk in the Maghreb Region [14].
Local milk production estimated at 2.5 billion L was provided largely
(nearly 80%) by cattle [15], the rest is represented by sheep, goat,
however camel milk production is very marginal (FIG. 1) [16]. Over the
past decades, several studies have been published on the hygienic
quality of milk produced in Algeria, but the results are highly divergent
and have been obtained under highly variable conditions.
The objective pursued in this article, therefore, to perform a
synthesis of these data through a meta–analysis. And subsequently to
estimate the relative risk factors that can affect milk quality in Algeria.
Meta–analysis can be a valuable tool for summarizing research
ndings across studies. It permits reviewers to describe the results
of each study on a common effect size metric, combine information
from many studies in an optimal fashion, and understand the degree to
which the ndings from different studies agree with one another [17].
MATERIALS AND METHODS
To conduct this meta–analysis, the guidelines provided by PRISMA
were adhered (Preferred Reporting Items for Systematic Reviews
and Meta–analyses).
Data collection
The aim of this systematic literature review was to conduct a meta–
analysis, to investigate the potential risk factors that may inuence
milk quality in Algeria.
It was conducted a search for studies published in specific
repositories and indexed sources (Google Scholar, Pubmed, Science
Direct), as well as both undergraduate and graduate degree works in
Algerian University repositories. The search query employed in two
languages French and English, was as follows: “Milk and cattle, goat,
sheep, camel and hygiene, TAMB (Total Aerobic Mesophilic Bacteria)
and Quality and Algeria”. A thorough and comprehensive search across
all available data bases was performed.
Multiple criteria were employed to determine the inclusion of eligible
studies: it was included studies that allowed for the detection of TAMB
in raw milk, focusing on its hygienic characteristics collected from
different stage of production (Farm, Dairy, Sale), and during different
seasons (Spring, Summer, Autumn, Winter). The search executed on
09/12/2022 with the nal update performed on 28/02/2023, yielded
332 studies. Duplicate entries were subsequently removed, and an
initial screening was conducted based on a preliminary review of
the study titles. Pasteurized milk, Powder milk, Cheese, Yogurt and
Whey studies were excluded from consideration. Following this initial
screening, a total of 96 studies were selected for further analysis. A
second screening was conducted to identify 61 eligible articles that
were ultimately included in the meta–analysis. Publications that lacked
clarity in their methodology or results; those without any statistical
or quantitative contributions and those with incomplete data were
excluded from consideration.
A owchart was created to summarize the step–by–step process
of study selection in the meta–analysis. This owchart provides a
visual representation of how studies were identied, screened, and
included or excluded at each stage of the selection process (FIG. 2).
FIGURE 2. Flow chart summarizing the process of study selection
FIGURE 3. Map of locations of studies included in the meta–analysis. Algerian
map was downloaded from Vemaps.com
FIGURE 4. Funnel plot for the Total Aerobic Mesophilic Bacteria (TAMB) level
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Statistical analysis
Meta–analysis can be a valuable tool for summarizing research
ndings across studies [17]. Outcomes from a meta–analysis may
include a more precise estimate of the risk factor, or other outcomes,
than any individual study contributing to the pooled analysis [18].
Weighted random–effects meta–analysis models were employed
to analyze the data in this study. The results of meta–analyses are
often presented in a forest plot. Heterogeneity of results among
trials is quantied using the inconsistency index I
2
.Funnel plots and
the Egger’s test were used to assess publication bias. The statistical
signicance level was set at P<0.05, R (version 3.5.1) software was
used for all analyses.
RESULTS AND DISCUSSION
Milk has a composition that creates favorable conditions for the
growth of various microorganisms. However, this can pose a risk
to public health. Additionally, bacterial contaminants can lead to
spoilage of milk and its derived products.
This meta–analysis was conducted to examine milk quality produced
from different geographical areas in Algeria, intended for human
consumption. Milk contamination level was determined by the TAMB
method at 30°C, for each sample of milk. Meta–analysis is a statistical
method to combine results of different studies, especially those with
small sample size or with conicting results [19].
The mesophilic microorganism is ones of the more general and
extensively microbiological indicators of food quality, indicating the
adequacy of temperature and sanitation control during processing,
transport, and storage, and revealing sources of contamination during
manufacture [20]. The total aerobic count is the most common method
for evaluation of bacterial quality of raw milk. This count estimates
the total number of bacteria present in raw milk at the time of pickup.
It provides an overall measure of hygienic quality of milk [21]. The
legal total bacterial counts limit in farm raw milk is set at 100,000
cells·mL
-1
., across the Europe and the Americas [12]. Local limits on
TAMB in raw milk for human consumption range from less than or equal
to 3.10
5
CFU·mL
-1
to less than or equal to 3.10
6
CFU·mL
-1
[22]. When
total bacterial counts in grade A unpasteurized milk is less than the
regulatory limit of 100,000 CFU·mL
-1
, it is assumed that all pathogenic
and most nonpathogenic bacteria are destroyed by pasteurization [23].
Study identication
It was collected a total of 4,685 sampling results from 61 studies
investigating the bacterial quality (TAMB) of raw milk across 35/48
Provinces in Algeria from 2009 to 2022 (FIG. 3).
Publication bias
No signicant publication bias was observed using the funnel plots
for asymmetry (FIG.4) and Egger’s test (P= 0.885).
FIGURE 5. Forest plot of the overall studies
FIGURE 6. Forest plot of the bacterial load of the Camel’s raw milk
FIGURE 7. Forest plot of the bacterial load of the Dairy’s milk
Meta-analysis of the microbiological quality of raw milk / Guergueb ________________________________________________________________
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Assessment of heterogeneity
The I
2
test indicates the presence of substantial statistical
heterogeneity across studies; (I
2
= 86.26 %, degrees of freedom [d.f.]
= 102, P< 0.001). The conduct of a meta–analysis is therefore justied.
Thus, in an effort to reduce this heterogeneity, it was performed
subgroup analyses to explore factors that may explain the heterogeneity.
Overall results of the studies
In this meta–analysis, the average level of contamination by TAMB was
5.84 log
10
CFU·mL
-1
. 95% CI [5.55–6.13]. The P–value was 0.001 for a total
of 4,685 samples from 61 included studies are presented in [24, 25, 26,
27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46,
47, 48, 49, 50, 51, 52, 53, 54, 55, 56, 57, 58, 59, 60, 61, 62, 63, 64, 65, 66,
67, 68, 69, 70, 71, 72, 73, 74, 75, 76, 77, 78, 79, 80, 81, 82, 83, 84] (FIG. 5).
The summarized results of the meta–analysis about the level of
contamination by TAMB found in included studies, are presented in
tabular form (TABLEI), concerning different species (Cow, Camel,
Goat, Sheep), stage of production (Farm, Collector, Dairy unit, Local
market), seasons (Winter, Spring, Summer, Autumn). It also displays
the number of studies analyzed, the total number of samples, and
the heterogeneity (I
2
). Moreover, four forest plots are provided as
examples (FIGS.5, 6, 7 and 8).
TABLE I
Summarized results of the meta–analysis
Variable Level
Number of Observations
/ Sample
I
2
(%)
TAMB
(log
10
CFU·mL
-1
)
IC 95%
P–value
Species
Cow’s milk 71/4223 72.79 6.05 5.78–6.32
0.620
Camel’ milk 12/166 80.47 4.91 3.88–5.93
Goat’s milk 17/135 72.56 5.82 4.67–6.93
Sheep’s milk 3/161 60.85 5.60 4.09–7.09
Production
step
Individual 26/415 65.62 4.57 3.99–5.14
0.001
Farm (tank) 46/2931 69.36 5.89 5.52–6.26
Collector 3/155 45.09 6.59 6.21–6.95
Dairy Unit 13/512 38.93 6.60 6.02–7.13
Local Market 33/555 70.48 6.74 6.16–7.32
Season
Winter 4/105 28.14 4.27 2.99–5.58
0.045
Spring 12/333 29.86 6.70 6.04–7.36
Summer 3/201 0.01 6.80 6.59–7.01
Autumn 4/47 0.01 5.64 4.32–6.95
Source: Research data
FIGURE 8. Forest plot of the contamination level in raw milk by Total aerobic
mesophilic bacteria (TAMB) during spring
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The hygienic quality of milk according to the species
Studies focusing on sheep showed low heterogeneity (I
2
= 60.85%),
whereas studies on Camel, Cow, and Goat exhibited higher heterogeneity
(I
2
= 80.47, 72.79 and 72.56%, respectively). The average contamination
level measured by TAMB was lower (4.91 log
10
CFU·mL
-1
) in camel milk
(FIG. 6), compared to the average microbial contamination level in
sheep, goat, and bovine milk (5.60 log
10
CFU·mL
-1
, 5.82 log
10
CFU·mL
-1
,
6.05 log
10
CFU·mL
-1
, respectively).
In this article, TAMB values did not differ signicantly (P–value>0.05)
among species. Similar results were conducted by Verraes et al.,
[11], who conclude that there is no signicant difference in the total
plate count results of raw milk from goats, sheep and cows. It should
be noted that these frequencies can be explained by the season in
which the samples were taken, the size of the farm, the density of
the animal population, regional differences in the keeping and taking
care of animals [11].
Total bacteria count in raw milk at different stages in the dairy chain
Heterogeneity was very high in studies addressing the hygienic
quality of milk samples collected at the Local Market level (I
2
= 70.84%),
whereas studies focusing on milk samples from other production
stages (Dairy Unit, Collector, Individual Milking, Farm’s milk from
tank) showed lower heterogeneity rates (I
2
= 38.93, 45.09, 65.62
and 69.36% respectively). The TAMB was lower (4.57 log
10
CFU·mL
-1
and 5.89 log
10
CFU·mL
-1
) in milk samples collected from individual
milking and farm tank milk (FIG. 7), compared to those recorded in
milk samples collected from the collector, dairy, and sales (6.59 log
10
CFU·mL
-1
, 6.74 log
10
CFU·mL
-1
, and 6.75 log
10
CFU·mL
-1
, respectively).
Raw milk quality at farm level is an important component inuencing
the performance of the whole dairy chain [85]. It was concluded
that milk from the cow is of good hygienic quality, but milk is often
contaminated after milking, and the hygienic quality is very low when
it reaches the consumers [86]. The deterioration in milk hygiene
quality between cow and farm tank level was probably due to
contaminated milking vessels and tank milk containers [86]. Improper
and inadequate cleaning and sanitizing of milking equipment (e.g.,
milking machine, bulk tank) is probably the most signicant source
of environmental contamination of milk. In addition, equipment of
poor sanitary design, or that has not been maintained, contribute to
microbial contamination of the milk.
Other factors related to refrigerated storage (storage temperature,
and storage time) are important to minimizing their growth [10].
The high total bacteria count in milk from milk collection center
suggests proliferation or recontamination of milk by bacteria during
transportation [87]. The hygienic quality of the milk, shown as total
bacteria count, became so much worse during storage already at the
farm and continued to decrease a further along the dairy chain [86].
Bacterial quality of milk according to the season
Heterogeneity was absent in studies focusing on milk samples
collected during Summer, and Autumn. Studies involving milk samples
collected during Spring and Winter showed higher heterogeneity (I
2
= 29.86%, I
2
= 28.14). The contamination level of milk by TAMB was
higher during Spring (FIG. 8) and Summer (6.70 log
10
CFU·mL
-1
and
6.80 log
10
CFU·mL
-1
, respectively), compared to Winter and Autumn
(4.27 log
10
CFU·mL
-1
and 5.64 log
10
CFU·mL
-1
).
The season also plays a signicant role; uctuations in temperature
can exert signicant inuence on bacterial counts in raw milk. TAMB
values were signicantly affected by sampling month. Seasonal
variation of TBC, with high values during Summer and Spring, and
lower values during Winter, is consistent with previous studies.
Similar results were reported by Zucali et al. [85] in a study in dairy
farms situated in the North of Italy (Lombardy), who observed strong
seasonal variations in total aerobic counts, with higher total aerobic
counts in the Summer. Season affects total aerobic count with a
positive trend during Summer and an opposite one in Winter, as
shown by Elmoslemany et al. [21] in a study on dairy herds of Prince
Edward Island, who concluded that higher milk bacterial counts during
Summer and Spring, may be related to warmer ambient temperature,
allowing bacteria to grow faster.
Good hygiene practices during milking and subsequent handling
of milk are essential to reduce the risk of contamination on the farm
and in the milk processing plant [88]. Two alternative approaches
are observed Worldwide to ensure the sanitary safety of milk: in
the United States of America, emphasis is placed on control and
sterilization, while in Europe; the focus is on quality and safety
management throughout the supply chain. The latter approach seems
more appropriate for Southern Countries where state control systems
are weak and the risks of contamination are numerous [4].
CONCLUSIONS
In conclusion, the meta–analysis conducted in this study sheds light
on the bacterial quality of raw milk intended for human consumption
in Algeria. The ndings reveal an average contamination level of total
aerobic bacteria (TAMB) at 5.84 log
10
CFU·mL
-1
, with a statistically
signicant presence of heterogeneity among the included studies.
Despite this variation, no signicant publication bias was observed.
The analysis also underscores the impact of different factors on milk
quality. The source of milk collection exhibited noteworthy differences,
with lower TAMB levels observed in samples collected from individual
milking and farm tanks compared to those obtained from collectors,
dairies, and sales. Additionally, seasonal variations played a role, as
higher contamination levels were recorded during the summer and
spring months compared to the winter and autumn seasons.
It is noteworthy that TAMB values did not show significant
variations among different species, highlighting the importance
of monitoring and improving overall hygiene practices throughout
Meta-analysis of the microbiological quality of raw milk / Guergueb ________________________________________________________________
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the milk production process. These results emphasize the need
for consistent efforts to enhance the hygienic quality of raw milk in
Algeria and suggest potential areas for targeted interventions, such
as during specic seasons and stages of milk collection.
As future research progresses, these insights can contribute to
the development of effective strategies to ensure the safety and
quality of raw milk for human consumption. It is evident that ongoing
monitoring, research, and collaboration among stakeholders are crucial
to maintaining and improving the bacterial quality of raw milk, thereby
safeguarding public health and promoting the well–being of consumers.
Conicts of interest
The authors declare no conict of interest.
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