Pathogenic bacteria are recognized as a major cause of foodborne diseases in humans, globally, with negative impact on the economy of each country. The aim of the present review was to obtain a comprehensive understanding about the frequency of isolation, diversity, and antimicrobial susceptibility profile of the six major foodborne pathogenic bacteria in food matrices and food processing environment, in Romania. In this regard, results of relevant epidemiological studies, published during the last decade and retrieved from the Web of Science Core Collection database, were analyzed, with special emphasis on scientific achievements, main knowledge gaps, and future perspectives. The summarized and harmonized results offer useful insight, especially for public health authorities and researchers, having a reference effect in stimulating further opportunities for studies to be carried out to address some of the limitations of the current status.
Bacterial foodborne pathogens are considered the most frequently implicated biological agents in food poisoning syndrome in humans, often called foodborne illness (FBI). FBI is usually characterized by acute health problems, with gastrointestinal (e.g., diarrhea, vomiting, nausea, or abdominal cramps), or neurological (e.g., headaches, paralysis, or paresthesia) manifestations. In “
Currently, due to the existence of several contamination sources with harmful bacteria via the food chain (e.g., animals, soil, water, air, food handlers during production and storage), the obtaining of safe and nutritious food products for the consumer is considered to be a great challenge for the food industry, worldwide. However, adequate cold preservation (e.g., refrigeration or freezing), associated with proper thermal processing of foods can prevent FBI. In case of foodborne diseases, the effectiveness of public health interventions is frequently hampered by the involvement of antibiotic-resistant bacteria. Thus, the continuous monitoring of the antimicrobial resistance phenomenon must be considered a priority for the public health sector [
In each year, the European Food Safety Authority (EFSA), together with the European Center for Disease Prevention and Control (ECDC) and with the contribution of each member state, publishes an open access summarized report about the occurrence of foodborne pathogen bacteria and their antimicrobial resistance profile in the human-animal-food chain [
With these considerations, the present review aimed to obtain an overview of the baseline data on the occurrence of major food-borne pathogenic bacteria (
A search was conducted in the Web of Science Core Collection database, in order to identify papers published in international scientific journals, which have undergone a rigorous peer review process, containing research data generated by Romanian researchers at country-level, between January 1st, 2010 and March 31th, 2020. The search strategy consisted of simultaneous use of three search terms, specifically, the name of one of the targeted foodborne bacteria, including “
At first, the inclusion criteria were based on the individual screening of the title and abstracts in search of resulting publications. Subsequently, if the basic information was deemed appropriate to meet the goal of the study, it was then included in the review and subjected to further, in-depth analysis.
Initial search in the database generated a total of 61 publications. Notwithstanding of that total, only 21 studies contained data that met our inclusion criteria and were subsequently included and processed in this review. The Table
Overview about the occurrence and diversity of major foodborne pathogenic bacteria and their antimicrobial susceptibility profile in foods and food processing environments, in Romania.
No. | Food matrix/environment isolation source (no. positive/examined, %) | Species, serotype (sequence type) (no. of isolates) | Exhibited antimicrobial resistance and susceptibility profile | References | |
---|---|---|---|---|---|
Resistance (%) | Total susceptibility | ||||
1. | Raw pork (33/146, 22.6) | AZM (88.2), TET (54.9), SMX (54.9), CIP (45.1), NAL (43.1), AMP (35.3), CHL (33.3), TGC (25.5), CTX (13.7), CST (13.7), TMP (7.8), GEN (2) | MEM, CAF | Tîrziu et al., [ | |
Raw chicken (12/132, 9.1) | |||||
Eggshell (3/48, 6.3) | |||||
Sausage (3/37, 8.1) | |||||
2. | Absorbent food pads from packages with raw chicken meat (1/24, 4.2) | N. A. | Gaspar et al., [ | ||
3. | Bovine, sheep carcasses (2/2499, 0.1) | FLU (84.7), CSF (78.5), NAL (78.5), NEO (68.2), SP (65.5), TET (63.9), STR (59.7), NOR (34.0), CXM (30.5), NIT (27.8), CIP (25.7), TIC (23.4), EFX (15.3), OFL (15.0), CAF (12.8), SAM (9.1), GEN (6.9) | — | Zaulet et al., [ | |
Chicken carcasses (34/1888, 1.8) | |||||
Raw pork (51/6442, 0.8) | |||||
Mechanically processed poultry meat (16/833, 1.9) | |||||
Mechanically processed red meat (37/12797, 0.3) | |||||
RTE meat products (4/3172, 0.1) | |||||
4. | Illegally sold RTE food in Romanian markets (0/200) | — | — | — | Ciolacu et al., [ |
5. | Pasteurized melange (0/20) | — | — | — | Nistor et al., [ |
6. | Raw chicken (7/N.A.) | LEV (88.9), NAL (88.9), SMX (88.9), TET (77.8), CIP (55.6), NIT (44.4), AMP (33.3), TMP (33.3), CTX (22.2), AMK (11.1), GEN (11.1), PIP (11.1), TOB (11.1), | CAF | Colobatiu et al., [ | |
Raw pork (2/N.A.) | |||||
7. | Chicken carcasses (37/289, 12.8) | TET (66.0), NAL (64.3), SMX (64.3), CIP (61.9), STR (59.5), TMP (33.3), AMP (9.5), CHL (7.1), GEN (2.4) | CAF, CTX, | Tîrziu et al., [ | |
Raw retail chicken (5/28, 17.9) | |||||
8. | Chicken carcasses (5/144, 3.5) | NAL (40), QUI (40), TET (40), CAF (20), CTX (20), GEN (20), SFN (20), SMX (20), SMX/TMP (20), STR (20) | AMP, CHL, CIP, KAN | Dan et al., [ | |
9. | Raw pork (12/47, 25.5), packaged pork products (7/44, 15.9), scald water sludge (1/8, 12.5), detritus from hair removal (6/9, 66.7) | N. A. | TET (61.5), AMP (50), PIP (50), TMP-SMX (34.6), AMC (26.9), NIT (23.1), CFZ (15.4), PIP/TBZ (7.7), CIP (3.8), IMI (3.8), NOR (3.8) | AMK, CAF, CEF, CFX, CTX, GEN | Morar et al., [ |
10. | Raw pork (minced meat) (7/N.A.), | N. A. | AMP (75.0), AMC (62.0), CFZ (62.0), PIP (62.0), TET (50.0), CFX (25), CXM (25.0), CTX (12.0) | AMK, ATM, CAF, CIP, FOS, GEN, IMI, NOR, SMX/TMP | Mateescu et al., [ |
Sausage (1/N.A.) | |||||
11. | Raw pork (48/208, 23.1) | SMX (87.2%), STR (81.2%), TET (80.5%), NAL (65.10%), CIP (42.9%) AMP (20.8%), CHL (16.9%), CAF (11.4%). GEN (0.7%) | CTX | Mihaiu et al., [ | |
Raw chicken (101/442, 22.9) | |||||
12. | Domestic refrigerators (2/15, 13.3) | N. A. | N. A. | — | Dumitrașcu et al., [ |
13. | Food contact surfaces (14/60, 23.3)—conveyor belts (5/15, 33); cutting surfaces (1/5, 20); packing surfaces (1/3, 33.3); personnel (1/7, 14.3), processing (3/11, 27.3) and slaughter (3/12, 25) equipment; storage container (0/7) | N.A. | BPN (100), FA (100), IMI (100), FOS (92.0), OXA (92.0), CLI (88.0), RIF (56.0), SMX/TMP (48.0), TET (44.0), CIP (4.0), | ERY, GEN, LNZ, MXF, TPL, VAN, TGC | Sala et al., [ |
Nonfood contact surfaces (11/37, 29.7)—employee workfow areas (2/8, 25), slaughterhouse drains (5/10, 50), processing plant drains (3/10, 30), cooling chamber walls (1/9, 11.1) | |||||
14. | Different types of meats (7/1841, 0.4)—raw pork (2/292, 0.7), mechanically processed red meat (4/374, 1.1), RTE products (1/1146, 0.1) | N. A. | N. A. | N. A. | Zaulet et al., [ |
15. | Illegally sold RTE foods in Romanian markets (15/200, 7.5)—raw and processed fish (10/61, 16.4), meat and meat products (4/41, 9.8), dairy products (1/73, 1.4) | Genetic lineage I–4b[ST2] | N. A. | N. A. | Ciolacu et al., 2016; Ciolacu et al., [ |
16. | Nonfood contact surfaces (16/81, 19.8) | 42 selected strains: 1/2a[3a] (35), 1/2c [3c] (7) | N. A. | N. A. | Bolocan et al., [ |
17. | Chicken carcasses (19/144, 13.2) | N. A. | TET (31.6), CHL (21.5), QUI (21.1), AMP (10.5), CIP (10.5), NAL (10.5), SFN (5.3), SMX (5.3), SMX/TMP (5.3) | CAF, CTX, GEN, KAN, STR, | Dan et al., [ |
18. | Food products (19/N.A.)—raw minced meat (4), pork (1), beef (1), bacon (2), chicken (2), forcemeat balls (4), sausage (2), shell snails (1), cheese (2) | 1/2a[3a] (12), 1/2b[3b] (2), 1/2c[3c] (2), 4a[4c] (2), 4b[4d, 4e] (1) | N. A. | N. A. | Caplan et al., 2014 [ |
19. | Different food products (25/235, 10.6)—unpasteurized milk (3/22, 13.6), sheep cheese (2/15, 13.3), cream (1/18, 5.6), raw sheep (3/25, 12), raw poultry (1/20, 5), raw pork (2/23, 8.7), raw beef (2/20, 10), snail meat (4/30, 13.3), fresh salad (4/15, 26.7), other foods (0/72) | 1/2c (11), 1/2a (6), 1/2b (3), 4b (2) | N. A. | N. A. | Carp-Cărare et al., [ |
20. | Absorbent food pads from packages with raw chicken meat (8/22, 36.4) | N. A. | CEF (100), FIX (87.5), CIP (75), OFL (75), MEM (12.5) | GEN | Gaspar et al., [ |
21. | Raw meat (1/501, 0.2), | Biotype I (126) | N. A. | N. A. | Zaulet et al., [ |
Ground meat (125/10548, 1.2) | |||||
22. | Illegally sold RTE foods in Romanian markets (0/200) | O157:H7 (0) | — | — | Ciolacu et al., [ |
23. | Chicken carcasses (18/144, 12.5) | N. A. | TET (66.7), QUI (55.5), NAL (44.4), CIP (33.3), AMP (27.7), CHL (22.2), SFN (22.2), SMX (22.2), SMX/TMP (22.2), STR (11.1), GEN (11.1) | CAF, CTX, KAN | Dan et al., 2015 [ |
24. | Raw chicken (51/100, 51) | N. A. | TET (84.3), AMP (73.0), SMX (66.3), SMX/TMP (48.3), NAL (30.3), CIP (16.8), CHL (14.6), STR (9.0), GEN (7.9), CTX (5.6), CAF (3.4) | — | Colobătiu et al., [ |
25. | Absorbent food pads from packages with raw chicken meat (6/15, 40) | Coagulase positive staphylococci (32) | MET (100), CFX (63.3), SMX/TMP (43.3), OXA (10), | — | Gaspar et al., [ |
26. | Raw and ground meat (0/212) | N. A. | N. A. | N. A. | Zaulet et al., [ |
27. | Illegally sold RTE foods in Romanian markets (16/200, 8)—raw and processed fish (5/61, 8), meat and meat products (3/41, 7.3), dairy products (8/72, 11.1), other products (0/16) | N. A. | N. A. | Ciolacu et al., [ | |
28. | Black-market sold food (16/200, 8) | PEN (31.3), TET (12.5), CIP (6.3), AMC (3.1), CFZ (3.1), OXA (3.1) | AMK, CLI, DAP, ERY, FA, FOS, GEN, LEV, LNZ, MUP, RIF, TOB, TPL, VAN | Oniciuc et al., [ | |
29. | Milk (2/2, 100) | N. A. | N. A. | Coldea et al., [ | |
30. | Raw chicken (10/34, 29.4) | CIP (80), NAL (80), TET (40), ERY (10), STR (10) | GEN | Tîrziu et al., [ | |
31. | Illegally sold RTE foods in Romanian markets (0/200) | — | — | — | Ciolacu et al., [ |
32. | Chicken carcasses (22/144, 15.3) | TET (31.8), SFN (13.6), SMX (13.6), SMX/TMP (13.6), CHL (9.1), CIP (9.1), NAL (9.1), QUI (9.1), AMP (4.5), | GEN, CTX, CAF, KAN, STR, | Dan et al., [ | |
33. | Chicken carcasses (0/144) | — | — | Dan et al., [ |
Legend: AMC: amoxicillin-clavulanic acid; AMK: amikacin; AMP: ampicillin; ATM: atromycin; AZM: azithromycin; BPN: benzylpenicillin; CAF: ceftazidime; CEF: cefepime; CFX: cefoxitin; CFZ: cefazolin; CHL: chloramphenicol; CIP: ciprofloxacin; CLI: clindamycin; CSF: colistinsulfate; CST: colistin; CTR: cotrimoxazole; CTX: cefotaxime; CXM: cefuroxime; DAP: daptomycin; EFX: enrofloxacin; ERY: erythromycin; FA: fusidic acid; FIX: cefixime; FLU: flumequine; FOS: fosfomycin; GEN: gentamicin; IMI: imipenem; KAN: kanamycin; LEV: levofloxacin; LNZ: linezolid; MEM: meropenem; MET: methicillin; MRSA: methicillin-resistant
Regarding the investigated food matrices, poultry meat has been reported as being most frequently contaminated with
Among the analyzed categories of nonfood matrices,
Serotyping tools have revealed the occurrence of a total of 35 serotypes. Out of them,
Antimicrobial resistance was recorded for at least one of the 37 antimicrobial agents reported as tested. The exhibited resistance profile of the tested
Over the last decade, in Romania, there was a total of nine studies that published data on the isolation frequency of
Four studies, based on molecular serotyping tools, have provided data on the genetic diversity of a total of 98 L
In the context of the importance of the global fight against antimicrobial resistance, only two studies approaching this problem have been published [
Intestinal and extraintestinal pathogenic variants of
Despite these considerations, a very limited number of studies providing data on the occurrence of
The antimicrobial susceptibility testing profile of a total of 77 chicken meat origin
In Romania, during the last decade, despite the existence of a limited number of studies concerning the occurrence of
The antimicrobial susceptibility profile of the tested
From the species belonging to the
The review data showed the availability of only three studies. These investigations have been focused on
The exhibited multidrug resistance patterns of the isolates highlighted a public health risk, but, at the same time, the total susceptibility against gentamicin, observed in both studies, can constitute an alternative for pathogen control (Table
Human yersiniosis is a foodborne disease, most commonly caused by
As has been highlighted in other review reports achieved in the United States [
Analysis of data obtained from a total of 21 relevant studies showed the common occurrence of the targeted major bacterial pathogens within the food chain, differing broadly in terms of examined matrices and depth of analysis. The resulted overall worrying antimicrobial resistance profile of the tested strains strengthens the urgent need of an integrated surveillance system of the dispersion and transmission of drug-resistant bacteria, within the entire food chain. This action requires an excellent collaboration between the environment, veterinary, and public health sectors, according to the One Health approach.
Although the scientific achievements and progresses are remarkable, it is obvious that the number of published papers is limited, precluding meaningful observations in trends of the pathogen isolation frequency. In addition, the large disparity observed between available investigations, according to the targeted pathogen (e.g.,
The authors declare that there are no conflicts of interest regarding the publication of this paper.
The authors are extremely grateful to PhD Student Tiana SUICI for her indispensable contribution in the English editing of the manuscript. This research paper is supported by the project “Ensuring excellence in the activity of RDI within USAMVBT” code 35PFE, submitted in the competition Program 1-Development of the national system of research-development, Subprogram 1.2-Institutional performance, Institutional development projects-Development projects of excellence in RDI”.