Scientific Achievements in the Study of the Occurrence and Antimicrobial Susceptibility Profile of Major Foodborne Pathogenic Bacteria in Foods and Food Processing Environments in Romania: Review of the Last Decade

Table 1

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
Salmonella spp.
1.	Raw pork (33/146, 22.6)	S. Typhimurium (9), S. Rissen (8), S. Infantis (6), S. Bredeney (2), S. Derby (2), S. Brandenburg (1), S. Enteritidis (1), S. Gloucester (1), S. Goldcoast (1), S. Kottbus (1), S. Ruzizi (1)	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., [4]
	Raw chicken (12/132, 9.1)	S. Infantis (12)
	Eggshell (3/48, 6.3)	S. Enteritidis (2), S. Infantis (1)
	Sausage (3/37, 8.1)	S. Typhimurium (2), S. Derby (1)
2.	Absorbent food pads from packages with raw chicken meat (1/24, 4.2)	S. Infantis	N. A.		Gaspar et al., [12]
3.	Bovine, sheep carcasses (2/2499, 0.1)	S. Manchester	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., [6]
	Chicken carcasses (34/1888, 1.8)	S. Saintpaul (9), S. Enteritidis (4), S. Typhimurium (4), S. Bredeney (3), S. Colorado (2), S. Derby (2), S. Agona (1), S. Blockley (1), S. Concord (1), S. Hadar (1), S. Heidelberg (1), S. Infantis (1), S. Norwich (1), S. Reading (1), S. Rissen (1), S. Tennesse (1)
	Raw pork (51/6442, 0.8)	S. Saintpaul (15), S. Bredeney (12), S. Enteritidis (6), S. Concord (5), S. Rissen (4), S. Derby (3), S. Hadar (3), S. Typhimurium (2), S. Choleraesuis (1)
	Mechanically processed poultry meat (16/833, 1.9)	S. Saintpaul (4), S. Agona (3), S. Bredeney (3), S. Enteritidis (3), S. Concord (1), S. Heidelberg (1), S. Newport (1)
	Mechanically processed red meat (37/12797, 0.3)	S. Saintpaul (13), S. Agona (7), S. Typhimurium (9), S. Bredeney (2), S. Concord (2), S. Enteritidis (2), S. Hadar (1), S. Newport (1)
	RTE meat products (4/3172, 0.1)	S. Hadar (2), S. Parkroyal (2)
4.	Illegally sold RTE food in Romanian markets (0/200)	—	—	—	Ciolacu et al., [10]
5.	Pasteurized melange (0/20)	—	—	—	Nistor et al., [11]
6.	Raw chicken (7/N.A.)	S. Infantis	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., [9]
	Raw pork (2/N.A.)	S. Infantis, S. Derby
7.	Chicken carcasses (37/289, 12.8)	S. infantis (18), S. Bredeney (7), S. Virchow (6), S. Djugu (4), S. Grampian (4), S. Brandenburg (1), S. Derby (1), S. Ruzizi (1)	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., [3]
	Raw retail chicken (5/28, 17.9)
8.	Chicken carcasses (5/144, 3.5)	S. Enteritidis (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., [5]
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., [7]
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., [8]
	Sausage (1/N.A.)	S. Arizonae
11.	Raw pork (48/208, 23.1)	S. Infantis (73), S. Typhimurium (19), S. Derby (15), S. Colindale (14), S. Rissen (6), S. Ruzizi (5), S. Virkow (5), S. Brandenburg (4), S. Bredeney (4), S. Calabar (1), S. Enteritidis (1), S. Muenchen (1), S. Kortrijk (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., [2]; Barbour et al., [25]
	Raw chicken (101/442, 22.9)
Listeria monocytogenes
12.	Domestic refrigerators (2/15, 13.3)	N. A.	N. A.	—	Dumitrașcu et al., [13]
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., [17]
	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., [6]
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]; Genetic lineage II–1/2a[ST20] (5), 1/2a[ST155] (4), 1/2a[ST8] (2), 1/2a[ST121] (2), 1/2C[ST9]	N. A.	N. A.	Ciolacu et al., 2016; Ciolacu et al., [10]
16.	Nonfood contact surfaces (16/81, 19.8); Food contact surfaces (28/85, 32.9); Raw materials (9/20, 45); RTE meat products (8/40, 20)	42 selected strains: 1/2a[3a] (35), 1/2c [3c] (7)	N. A.	N. A.	Bolocan et al., [14]
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., [5]
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 [16]
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., [15]
E. coli
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., [12]
21.	Raw meat (1/501, 0.2),	Biotype I (126)	N. A.	N. A.	Zaulet et al., [6]
	Ground meat (125/10548, 1.2)
22.	Illegally sold RTE foods in Romanian markets (0/200)	O157:H7 (0)	—	—	Ciolacu et al., [22]
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 [5]
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., [19]
Staphylococcus aureus/spp.
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., [12]
26.	Raw and ground meat (0/212)	N. A.	N. A.	N. A.	Zaulet et al., [6]
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)	S. aureus (16)—t449 (4), t304 (3), t1606 (2), t524 (2), t011, t091, t3625, t803, unknown (1)	N. A.	N. A.	Ciolacu et al., [22]
		S. aureus—MSSA/MRSA (9), MRSA (5), MSSA (1)
28.	Black-market sold food (16/200, 8)	S. aureus—MSSA (31), MRSA—t398 (1)	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., [21]
29.	Milk (2/2, 100)	S. aureus—t902 (2)	N. A.	N. A.	Coldea et al., [23]
Campylobacter spp.
30.	Raw chicken (10/34, 29.4)	C. coli (7), C. jejuni (3)	CIP (80), NAL (80), TET (40), ERY (10), STR (10)	GEN	Tîrziu et al., [4]
31.	Illegally sold RTE foods in Romanian markets (0/200)	—	—	—	Ciolacu et al., [22]
32.	Chicken carcasses (22/144, 15.3)	C. jejuni (22)	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., [5]
Yersinia spp.
33.	Chicken carcasses (0/144)	—	—	—	Dan et al., [5]

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 S. aureus; MSSA: methicillin-sensitive S. aureus; MUP: mupirocin; MXF: moxifloxacin; NAL: nalidixic acid; NEO: neomycin; NIT: nitrofurantoin; NOR: norfloxacin; OFL: ofloxacin; OXA: oxacillin; PEN: penicillin; PIP: piperacillin; QUI: quinolones; RIF: rifampicin; SAM: ampicillin-sulbactam; SFN: sulfonamides; SMX: sulfamethoxazole; SP: spectinomycin; STR: streptomycin; TBZ: tazobactam; TET: tetracycline; TGC: tigecycline; TIC: ticarcillin; TMP: trimethoprim; TOB: tobramicin; TPL: teicoplanin; VAN: vancomycin; N.A. : not available data.