Prevalence of Clostridium perfringens and Detection of Its Toxins in Meat Products in Selected Areas of West Kazakhstan
by
, , ,
Arman Issimov
1,*,
Torebek Baibatyrov
2,
Aigul Tayeva
3,
Shynar Kenenbay
3,
Sholpan Abzhanova
4,
Gulnara Shambulova
3,
Gaukhar Kuzembayeva
3,
Madina Kozhakhiyeva
3,
Inna Brel-Kisseleva
5
,
Olga Safronova
6,
Lyailya Bauzhanova
7,
Gulzhan Yeszhanova
8,
Kainar Bukarbayev
4,
Alma Katasheva
4 and
Francisco A. Uzal
9 1
Sydney School of Veterinary Science, Faculty of Science, University of Sydney, Sydney 2006, Australia
2
Department of Food Technology, Zhangir Khan West Kazakhstan Agrarian—Technical University, Oral 09000, Kazakhstan
3
Department of Food Technology, Almaty Technological University, Almaty 050000, Kazakhstan
4
Department of Food Biotechnology, Almaty Technological University, Almaty 050000, Kazakhstan
5
Department of Livestock Production Technologies, A. Baitursynov Kostanay Regional University, Kostanay 110000, Kazakhstan
6
Laboratory of Agrochemical Analyzes, Zarechnoye Agricultural Experimental Station LLP, Kostanay 110000, Kazakhstan
7
Department of Zootechnology and Genetics, Toraighyrov University, Pavlodar 140000, Kazakhstan
8
Department of Veterinary Medicine, Saken Seifullin Kazakh Agrotechnical University, Nur-Sultan 010000, Kazakhstan
9
California Animal Health and Food Safety Laboratory System, San Bernardino Branch, University of California, Davis, CA 92408, USA
*
Author to whom correspondence should be addressed.
Agriculture 2022, 12(9), 1357; https://doi.org/10.3390/agriculture12091357
Submission received: 18 July 2022
/
Revised: 26 August 2022
/
Accepted: 29 August 2022
/
Published: 1 September 2022
(This article belongs to the Section Agricultural Product Quality and Safety)
Abstract
:Objectives. The current study aimed to investigate the prevalence of Clostridium perfringens in meat products at meat fairs in four cities of West Kazakhstan from April to October 2021. Methods. In total, 240 samples were collected and subsequently examined for the presence of Clostridium perfringens and its associated toxins using a standard culture method and multiplex PCR assay. Results. In the 240 samples, 67 (30%) tested positive for Clostridium perfringens. All isolates were classified as biotype A with the ability to produce α toxin. The prevalence of Clostridium perfringens was found in almost all types of meat products tested. Beef samples 20/40 (50%) were found the most contaminated with a pathogen, followed by minced lamb 16/40 (40%), ground beef 11/40 (27.5%), lamb 9/40 (22.5%), beef intestines 7/40 (17.5%) and lamb intestines 4/40 (10%). Conclusions. The outcomes of our study demonstrated the high contamination rate of Clostridium perfringens in local meat products. This study is also the first survey on Clostridium perfringens prevalence in meats in Kazakhstan. The findings in this report will enhance knowledge of epidemiology and help develop coordinated actions to prevent and control possible food poisoning outbreaks.
1. Introduction
Clostridium perfringens, a spore-forming anaerobic Gram-positive bacterium, is a foodborne pathogen that induces food poisoning and enteric infections in humans and animals [1,2]. Previously, Clostridium perfringens was classified into five toxic strains (A-E) based on the synthesis of four significant toxins; alpha (α), beta (β), epsilon (ε), iota (ι) [3,4]. In 2018, two more biotypes were identified. They were subsequently introduced as a type F which produces α-toxin and enterotoxin (CPE), and type G, which produces α-toxin and necrotic enteritis toxin (NetB) [5].
Clostridium perfringens-associated food poisoning cases are reported in developed countries, while they are rarely investigated in developing countries [6]. In humans, Clostridium perfringens biotypes can be found in the gastrointestinal tract and genital organs and, under certain circumstances, may serve as a causative agent of food poisoning, gas gangrene, and multiple organ failure [1,7,8,9].
According to the Center for Disease Control and Prevention, Clostridium perfringens has become the second most prevalent pathogen associated with foodborne disease in the USA, causing 1 million cases every year [10]. In Kazakhstan, food poisoning caused by foodborne pathogens, including Clostridium perfringens, is poorly reported; however, detection of Clostridium perfringens type A and its associated α toxin in Kazakh honey samples has been published recently [11]. It is suggested that food poisoning develops mostly following consumption of meat products contaminated with Clostridium perfringens at a level of 106 CFU/g [12].
Beef and lamb meat products are a major source of dietary protein among the Kazakhstani population. To the best of our knowledge, there were no studies conducted to determine the prevalence of Clostridium perfringens in meat products in street markets of West Kazakhstan. Additionally, the biotypes of Clostridium perfringens and the presence of a specific cpe gene in the isolates were analyzed.
2. Materials and Methods
2.1. Study Area and Sample Collection
The research was carried out in the West Kazakhstan region (51°55′–43°54′ N, 45°73′–61°82′ E) between April and October 2021. According to the national census, the oblast has a population of approximately 2.5 million in an area of 736,129 km2. The region consists of four major oblasts and one administrative center. Three provinces (Atyrau, Aktobe, Aksay) and an administrative center (Oral) were selected for sample collection. These areas were selected as they are the main meat-producing regions in West Kazakhstan.
Overall, samples of 240 beef and lamb products (beef and lamb intestines, ground beef, minced lamb) were taken from fair markets in the area studied. Ten samples of each meat type were collected from each region. The temperature of samples taken varied between 13 and 19 °C. All samples collected were stored at 4 °C in a 50-mL sterile plastic tube and immediately transported to the laboratory. Microbiological and PCR examination of samples were run within 6 h following delivery.
2.2. Microbiological Examination
Examination of the samples for the presence of Clostridium perfringens was conducted according to the international protocol based on ISO 7937 (ISO, 2004) [13] guidelines. In brief, each specimen (25 g) was transferred into a sterile blender jar containing 225 mL peptone dilution fluid (1:10 dilution) and subsequently homogenized for 1 min at 1500× g. Next, tenfold serial dilutions from 10−1 to 10−6 were made using the 1:10 dilution mentioned above. Then, 0.1 mL of each dilution was introduced into the center of solidified TSC agar supplemented with egg yolk emulsion (Neogen Perfringens Agar Base, Thermo Fisher Scientific, Billerica, MA, USA). To establish anaerobic settings, plates were then overlaid with 10 mL of TSC agar without egg yolk emulsion and allowed to incubate at 37 °C for 24 h.
Identification of presumptive Clostridium perfringens colonies was based on their characteristic morphology. Accordingly, plates containing 20–200 black colonies were considered positive after incubation in an egg yolk medium with an opaque white zone surrounding the colony due to lecithinase activity. Black colonies were counted, and a calculation of Clostridium cells per gram of specimen was made using the Quebec colony counter (Reichert, Darkfield Quebec, Thermo Fisher Scientific, Billerica, MA, USA). The experiment was run in triplicate, and plates were sent for genomic confirmation.
2.3. DNA Manipulation and PCR Amplification
For DNA extraction, a Bacterial Genomic Miniprep Kit (Sigma-Aldrich Inc, Rockville, MD, USA) was used according to the manufacturer’s instructions.
Following Clostridium perfringens reference strains were utilized as a positive controls of toxin typing: C. perfringens type A, National Collection of Type Culture (NCTC) 528 (cpa); type C, NCTC 3180 (cpb), NCTC 4989 (cpb, cpb2); type D, NCTC 8346 (etx) and type E, NCTC 8084 (iap, cpe). For toxin genotyping of isolates, multiplex PCR (mPCR) was performed according to the protocol described by Baums et al. [14] with modification [15]. This technique allows the detection of cpa, cpb, cpb2, cpe, etx, and iap genes of Clostridium perfringens biotypes in a single reaction. The conditions for DNA amplification in a Thermal Cycler (Eppendorf Mastercycler) were as follows: 95 °C for 2 min 30 s, 95 °C for 1 min, 55 °C for 1 min, 72 °C for 1 min 20 s (35 cycles), and 72 °C for 2 min. The mPCR products obtained were administered in 1% agarose gel electrophoresis in the presence of Ethidium bromide, and the results were visualized using Bio-Imaging Systems (MiniBIS Pro, Jerusalem, Israel).
3. Results
Detection of Clostridium perfringens
The identification of Clostridium perfringens in samples of beef and lamb products taken from meat fairs is demonstrated in Table 1. Out of 240 samples examined, 67 (28%) tested positive for the presence of Clostridium perfringens strains. All strains isolated belonged to the Clostridium perfringens biotype A with the ability to produce the α gene. Clostridium perfringens isolates were found in almost every meat type sampled. Moreover, the meat fairs of each province were contaminated with this pathogen. The highest prevalence of Clostridium perfringens isolates was found at the meat fair of the Oral administrative unit accounting for 25/40 positive samples, followed by Atyrau 16/40, Aksay 12/40, and Aktobe 7/40 districts (Table 2). The anaerobic count of Clostridium perfringens ranged from 1.5 × 102 to 6 × 104 per gram. The highest bacterial load was observed in minced lamb, whereas the lowest was observed in the beef intestine (Table 3).
4. Discussion
Clostridium perfringens is a ubiquitous anaerobic spore-forming bacteria that cause various diseases in humans and animals. It ranks as the most important foodborne pathogen causing food poisoning worldwide [10,16]. In the current study, about 30% of meat fair products tested were positive for the presence of Clostridium perfringens, similar to those reported by Miwa et al. [17] and Wen and McClane [18].
In developed countries, foodborne illnesses caused by Clostridium perfringens biotype-F (CPE-producing strain) are responsible for human food poisoning. Moreover, Clostridium perfringens foodborne outbreaks among children have been reported in Northern Greece [19].
In Kazakhstan, the presence of Clostridium perfringens in raw meat products has never been reported. However, our study demonstrated a high prevalence of Clostridium perfringens biotype-A in meat fairs in the most populous cities in West Kazakhstan. Smallholder farmers from remote rural areas are the main participants at meat fairs. Meat fairs are usually organized in the open air during the spring and autumn months. Personal communications revealed that individual farmers travel a long distance (about 500 km) before attending meat fairs. Moreover, meat products, in most cases, are transported without proper packaging and without a refrigeration system. It should be taken into account that slaughtering is often performed on the farm site in the evening before the meat fair. Carcasses and meat cuts are kept at the slaughtering site overnight and are transported to the fair at dawn. Furthermore, the circumstances are aggravated because meat counters in fairs are not equipped with refrigerators. Accordingly, farmers are forced to store their products under unfavorable conditions for an additional 5 h, from 7.00 a.m. to 12.00 p.m. On the fair site, meat cuts remain on meat counters unwrapped or uncovered, and meat delicacy (intestines, beef tongue) are left in the plastic cabinet at the ambient temperature for several hours, which increases the temperature of the meat. These factors have a positive effect on Clostridium perfringens proliferation. It is reported that vegetative cells of this foodborne pathogen are capable of fast and dynamic growth at 20 °C to 53 °C, whereas spores can survive up to 95 °C for 1 h [20,21]. Additionally, the violation of hygienic practices during slaughtering, processing, and handling can affect bacterial loads [22].
Previous studies indicated that meat and meat products are common sources of Clostridium perfringens infection [23,24]. Although the heterogeneous nature of Clostridium perfringens possesses high diversity of biotypes (A, B, C, D, E, F, and G) and could be explained by their recombination, in-vivo and in-vitro horizontal gene transfer, and evolutionary dynamism [5,25] our study demonstrated low heterogeneity of the isolates tested, belonging to biotype A only.
In the Oral district, the prevalence of Clostridium perfringens biotype A carrying the characteristic cpa gene was higher than in other districts investigated. Among meat types tested, Clostridium perfringens biotype A prevailed in samples taken from beef and minced lamb. No food-poisoning-associated biotype F isolates were found; additionally, the presence of cpb, cpb2, etx, iap, and cpe genes was negative in all isolates tested.
Our results agree with Cooper et al. [26] and [27,28] where the prevalence rate of Type A among Clostridium perfringens strains isolated from meat products varied 86–100%. In addition, Smedley et al. [29] reported that less than 5% of all Clostridium perfringens strains are capable of producing enterotoxin. In humans, gastroenteritis associated with CP infection is usually produced by enterotoxigenic type F strains of this microorganism. Since no type F strains were found in our study, but other types of CP were found in many meat samples, this suggests that the samples analyzed were not involved in human disease. Our results suggest, however, poor hygiene and food management. Based on this, Clostridium perfringens biotype A is not supposed to pose a big risk for enteric disease (encodes only alpha-toxin).
However, the presence of Clostridium perfringens in these popularly-consumed meat products illustrates their potential to serve as an etiologic agent of gas gangrene and sepsis in humans. Therefore it is suggested that Kazakhstani sanitary authorities should take strict control measures on the microbiological quality of meat products being sold in fairs.
Author Contributions
A.I.: Supervision, conceptualization, methodology, writing— original draft. T.B.: Data analysis, validation. A.T., S.K., S.A., G.S., G.K., M.K.: Funding acquisition, validation, resources, conceptualization, methodology, investigation. I.B.-K., O.S.: Software, formal analysis. L.B., G.Y., K.B., A.K.: Resources, conceptualization, methodology, funding acquisition, data curation, formal analysis, validation, investigation. F.A.U.: Investigation, writing—review and editing. All authors have read and agreed to the published version of the manuscript.
Funding
This research received no external funding.
Institutional Review Board Statement
Not applicable.
Informed Consent Statement
Not applicable.
Data Availability Statement
Not applicable.
Conflicts of Interest
The authors declare no conflict of interest.
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Table 1.
Detection of Clostridium perfringens isolates and associated genes in examined meat products (n = 240) from meat fairs (n = 4) in four areas in west Kazakhstan.
Table 1.
Detection of Clostridium perfringens isolates and associated genes in examined meat products (n = 240) from meat fairs (n = 4) in four areas in west Kazakhstan.
| Sample | Number of Samples Tested | Number of Samples Tested Positive/% | C. perfringens Toxin Type | Toxin Gene | |||||
|---|---|---|---|---|---|---|---|---|---|
| cpa | cpb | cpb2 | etx | iap | cpe | ||||
| Beef | 40 | 20/50 | A | 20 | - | - | - | - | - |
| Lamb | 40 | 9/22.5 | A | 9 | - | - | - | - | - |
| Beef intestines | 40 | 7/17.5 | A | 7 | - | - | - | - | - |
| Lamb intestines | 40 | 4/10 | A | 4 | - | - | - | - | - |
| Ground beef | 40 | 11/27.5 | A | 11 | - | - | - | - | - |
| Minced lamb | 40 | 16/40 | A | 16 | - | - | - | - | - |
| Total | 240 | 67/27.9 | - | 67 | - | - | - | - | - |
Table 2.
Prevalence of C. perfringens isolates in meat samples (n = 240) taken from meat fairs (n = 4) in West Kazakhstan.
Table 2.
Prevalence of C. perfringens isolates in meat samples (n = 240) taken from meat fairs (n = 4) in West Kazakhstan.
| Districts | Number of Clostridium perfringens Isolates (Meat Type) | Total in Districts (%) |
|---|---|---|
| Atyrau | 6 (beef), 1 (beef intestines), 2 (lamb intestines), 4 (ground beef), 3 (minced lamb) | 16 (40%) |
| Aktobe | 4 (beef), 1 (lamb), 2 (ground beef), 1 (minced lamb) | 7 (17.5%) |
| Aksay | 2 (beef), 2 (lamb), 3 (beef intestines), 2 (lamb intestines), 2 (ground beef), 1 (minced lamb) | 12 (30%) |
| Oral (administrative centre) | 8 (beef), 5 (lamb), 4 (beef intestines), 3 (ground beef), 5 (minced lamb) | 25 (62.5%) |
Table 3.
The total number of vegetative Clostridium perfringens cells in meat products (n = 240) collected from meat fairs (n = 4) in West Kazakhstan.
Table 3.
The total number of vegetative Clostridium perfringens cells in meat products (n = 240) collected from meat fairs (n = 4) in West Kazakhstan.
| Sample | Clostridium perfringens CFU/g, Mean |
|---|---|
| Beef | 2 × 104 |
| Lamb | 4 × 102 |
| Beef intestines | 2 × 102 |
| Lamb intestines | 4.2 × 103 |
| Ground beef | 3 × 103 |
| Minced lamb | 6 × 104 |
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Issimov, A.; Baibatyrov, T.; Tayeva, A.; Kenenbay, S.; Abzhanova, S.; Shambulova, G.; Kuzembayeva, G.; Kozhakhiyeva, M.; Brel-Kisseleva, I.; Safronova, O.; et al. Prevalence of Clostridium perfringens and Detection of Its Toxins in Meat Products in Selected Areas of West Kazakhstan. Agriculture 2022, 12, 1357. https://doi.org/10.3390/agriculture12091357
AMA Style
Issimov A, Baibatyrov T, Tayeva A, Kenenbay S, Abzhanova S, Shambulova G, Kuzembayeva G, Kozhakhiyeva M, Brel-Kisseleva I, Safronova O, et al. Prevalence of Clostridium perfringens and Detection of Its Toxins in Meat Products in Selected Areas of West Kazakhstan. Agriculture. 2022; 12(9):1357. https://doi.org/10.3390/agriculture12091357
Chicago/Turabian StyleIssimov, Arman, Torebek Baibatyrov, Aigul Tayeva, Shynar Kenenbay, Sholpan Abzhanova, Gulnara Shambulova, Gaukhar Kuzembayeva, Madina Kozhakhiyeva, Inna Brel-Kisseleva, Olga Safronova, and et al. 2022. "Prevalence of Clostridium perfringens and Detection of Its Toxins in Meat Products in Selected Areas of West Kazakhstan" Agriculture 12, no. 9: 1357. https://doi.org/10.3390/agriculture12091357
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