Carbapenemase Producing Gram-Negative Bacteria in Tunisia: History of Thirteen Years of Challenge

Figures & data

Table 1 Characteristics of Carbapenemase Producing Gram-Negative Bacteria in Tunisia from 2006 to 2019

Ambler Classes	Carbapenemases	Variants	Concerned Species	Number of Isolates (n)	Sequence Type	Origins	Locations	Isolation Years	Genetic Environment	References
A	KPC	KPC-2	E. coli	1	ST5700	Clinical	National Bone Marrow Transplant Center of Tunisia (Tunis)	2013	Transposon	[^Citation15]
		ND	K. pneumoniae	20	ND	Clinical	Rabta University Hospital of Tunis	2014	ND	[^Citation14]
		KPC-3	E. coli	1	ST167	Seafood (mussels)	Retail market	2015	Tn 4401d Inc FII	[^Citation31]
		ND	ND	–	ND	Wastewater effluents from hospitals	Charles Nicolle Hospital (Tunis) Fattouma Bourguiba Hospital (Monastir) Farhat Hached hospital (Sousse)	2015–2016-2017	ND	[^Citation29]
B	IMP	IMP-1	K. pneumoniae	9	ND	Hospital environment	Kasserine Hospital	2010	ND	[^Citation20]
		IMP-8	K. pneumoniae	6	ND	Polluted-river	Oued Meliane (Rades)	2010	Class1 Integron	[^Citation21]
		IMP-10	K. pneumoniae	8
		IMP-13	K. pneumoniae	2
	VIM	VIM-4	K. pneumoniae	11	ND	Clinical	Habib Bourguiba University Hospital (Sfax)	2005	Plasmid Class1 Integron	[^Citation12]
		VIM-2	P. aeruginosa	30	ND	Clinical	Two hospitals in Sfax	2007	Chromosome	[^Citation53]
			P. aeruginosa	5	ND	Clinical	Sahloul University Hospital (Sousse)	2006–2007	Class 1 Integron Chromosome	[^Citation39]
			P. aeruginosa	35	ND	Clinical	Charles Nicolle Hospital (Tunis)	2002–2003–2004–2005–2006	Class 1 Integron	[^Citation38]
			P. aeruginosa	16	ND	Clinical	Charles Nicolle Hospital (Tunis)	2008	ND	[^Citation54]
			P. aeruginosa	9	ND	8 Clinical +1Hospital environment	Aziza Othmana Hospital (Tunis)	2007–2008	Class 1 Integron	[^Citation55]
			E. coli	4	ND	Hospital environment	Kasserine Hospital	2010	ND	[^Citation20]
		VIM-1	K. pneumoniae H. pylori	3 7	ND	Polluted-river	Oued Meliane (Rades)	2010	ND	[^Citation21]
		ND	K. pneumoniae	20	ND	Clinical	Rabta University Hospital of Tunis	2014	ND	[^Citation14]
B	VIM	ND	K. pneumoniae	5	ND	Clinical	Military Hospital of Tunis	2014–2015–2016	ND	[^Citation56]
		VIM-2	E. cloacae	1	ND	Clinical	Regional Hospital of Djerba	2015–2016	Class1 Integron	[^Citation22]
	NDM	NDM-1	K. pneumoniae	1	ST11	Clinical	Military Hospital of Tunis	2012	Inc N	[^Citation23]
			K. pneumoniae	19	ST147	Clinical	Sahloul University Hospital (Sousse) Tahar Sfar hospital (Mahdia)	2013–2014–2015	Inc FIIk Tn125	[^Citation24]
			A. baumannii	11	ST85	Clinical	Sahloul University Hospital (Sousse)	2013–2014–2015	ΔTn125 Chromosome	[^Citation25]
			K. pneumoniae	1	ST11	Clinical	Sahloul University Hospital (Sousse)	2015	Plasmid	[^Citation57]
			A. baumannii	1	ST85	Clinical	Fattouma Bourguiba Hospital (Monastir)	2013–2014–2015–2016	ΔTn125 Chromosome	[^Citation40]
			K. pneumoniae	30	ST147 ST101	Clinical	Tahar Sfar hospital (Mahdia)	2015–2016	Inc FIIk Tn125	[^Citation43,Citation58]
			K. pneumoniae	7	ND	Fecal and rectal carriage	Charles Nicolle Hospital (Tunis)	2014–2015	ISAba125	[^Citation47,Citation59]
			K. pneumoniae	19	ST147 ST307	Clinical		2010–2011–2012–2013–2014–2015	Inc FIA ISAba125	[^Citation60]
			A. baumannii	2	ST1089	Fecal carriage		2014–2015	ISAba125	[^Citation61]
			K. pneumoniae	13	ND	Clinical	Military Hospital of Tunis	2014–2015–2016	ND	[^Citation56]
			K. pneumoniae	9	ST15 ST147 ST1412	Clinical	Regional Hospital of Djerba	2015–2016	Inc FIIA Inc A/C ISAba125	[^Citation22]
			P. mirabilis	1	ND	Clinical	Charles Nicolle Hospital (Tunis)	–	Plasmids	[^Citation26]
		ND	ND	-	ND	Wastewater effluents from 7 hospitals	Charles Nicolle Hospital (Tunis) Fattouma Bourguiba Hospital (Monastir) Farhat Hached hospital (Sousse) Tahar Sfar Hospital (Mahdia) Hedi Chaker Hospital (Sfax) Regional Hospital (Gafsa) Regional Hospital (Sidi Bouzid)	2015–2016–2017	ND	[^Citation29]
D	OXA-48	OXA-48	K. pneumoniae	21	ND	Clinical	Habib Bourguiba University Hospital (Sfax)	2009–2010	Inc A/C	[^Citation62]
			K. pneumoniae	2	ST101 ST383	Clinical	Private hospital in Tunis Military Hospital of Tunis	2010	Plasmid (60 kb) Tn 1999.1 Tn 1999.2	[^Citation63]
			K. pneumoniae C. freundii	4 1	ND	Clinical	Charles Nicolle Hospital (Tunis)	2010–2011	Inc A/C (54 kb) Chromosome IS1999	[^Citation64]
			P. stuartii	13	ND	Clinical and Environmental	Habib Bourguiba University Hospital (Sfax)	2011	Inc A/C Tn 1999	[^Citation65]
			K. pneumoniae	13	ND	Clinical	Military Hospital of Tunis	2011–2012	Inc A/C Inc R	[^Citation66]
			K. pneumoniae	1	ST11	Clinical	Military Hospital of Tunis	2012	Inc L/M	[^Citation23]
			K. pneumoniae	19	ST11 ST14 ST15 ST101 ST882 ST196 ST1978	Clinical	National Bone Marrow Transplant Center of Tunisia (Tunis)	2011–2012–2013–2014	ND	[^Citation15]
			E. coli	2	ST58 ST227
			K. pneumoniae	4	ST15	Clinical	National Bone Marrow Transplant Center of Tunisia (Tunis)	2011	ND	[^Citation67]
			K. pneumoniae	5	ND	Clinical	National Bone Marrow Transplant Center of Tunisia (Tunis)	2013	ND	[^Citation68]
			K. pneumoniae	1	ST11	Clinical	The Maternity and Neonatology center of Monastir	–	Tn 1999.2	[^Citation42]
			K. pneumoniae	1	ST147	Clinical	Tunisian Hospital	–	Inc L/M Tn 1999.2	[^Citation69]
			K. pneumoniae	3	ST101	Clinical	Avicenne clinic (Tunis)	2014	ND	[^Citation70]
			K. pneumoniae E. cloacae E. aerogenes*	2 1 1	ND	Rectal carriage	Charles Nicolle Hospital (Tunis)	2014	ND	[^Citation59]
			K. pneumoniae	13	ST101 ST147	Fecal carriage	Charles Nicolle Hospital (Tunis)	2014–2015	Tn 1999	[^Citation47]
			K. pneumoniae	3	ST147	Clinical	Charles Nicolle Hospital (Tunis)	2010–2011–2012–2013–2014–2015	Plasmid Tn 1999	[^Citation60]
D	OXA-48	OXA-48	K. pneumoniae	1	ST147	Clinical	Sahloul University Hospital (Sousse)	2014	Inc L Tn 1999.2	[^Citation24]
			K. pneumoniae	5	ST15 ST101	Clinical	Sahloul University Hospital (Sousse)	2012–2013–2014–2015–2016	Plasmid	[^Citation57]
			K. pneumoniae	1	ST101	Clinical	Tahar Sfar hospital (Mahdia)	2012	Inc L/M Tn1999.2	[^Citation71]
			K. pneumoniae	20	ST101 ST147 ST392	Clinical	Tahar Sfar hospital (Mahdia)	2015–2016	Inc L Tn 1999	[^Citation43]
			K. pneumoniae E. coli E. cloacae	79 3 10	ND	Clinical	Military Hospital of Tunis	2014–2015–2016	ND	[^Citation56]
			K. pneumoniae	8	ND	Clinical	Military Hospital of Tunis	2015	ND	[^Citation46]
			K. pneumoniae P. mirabilis	5 1	ST15	Clinical	Regional Hospital of Djerba	2015–2016	NT Plasmid (48,5kb) Tn 1999.2	[^Citation22]
			ND	-	ND	Wastewater effluents from 7 hospitals	Charles Nicolle Hospital (Tunis) Fattouma Bourguiba Hospital (Monastir) Farhat Hached hospital (Sousse) Tahar Sfar Hospital (Mahdia) Hedi Chaker Hospital (Sfax) Regional Hospital (Gafsa) Regional Hospital (Sidi Bouzid)	2015–2016–2017	ND	[^Citation29]
		OXA-204	K. pneumoniae E. coli	1 1	ST101 ST617	Clinical	The Maternity and Neonatology center of Monastir	–	Tn 2016	[^Citation42]
			S. enterica	1	ST198	Clinical	Habib Bourguiba Hospital (Sfax)	2009	Inc A/C	[^Citation72]
			K. pneumoniae	1	ST147	Clinical	Sahloul University Hospital (Sousse)	2013	Plasmid	[^Citation57]
			K. pneumoniae	1	ST147	Clinical	Tahar Sfar hospital (Mahdia)	2013	Inc A/C ISEcp1	[^Citation71]
			K. pneumoniae	4	ST147	Clinical	Tahar Sfar hospital (Mahdia)	2015–2016	Inc A/C Tn 2016	[^Citation43]
D	OXA-48	OXA-204	K. pneumoniae	1	ND	Clinical	Military Hospital of Tunis	2011–2012	IncA/C	[^Citation66]
		OXA-232	K. pneumoniae	3	ST147	Clinical	Military Hospital of Tunis	2015	Plasmid	[^Citation46]
	OXA-23	OXA-23	A. baumannii	13	ND	Clinical	Sahloul University Hospital (Sousse)	2005–2006–2007	ISAba1 Chromosome	[^Citation52]
			A. baumannii	41	ND	Clinical	Charles Nicolle Hospital (Tunis)	2007	ND	[^Citation74]
			A. baumannii	2	ST1	Clinical	Military Hospital of Tunis Mohamed Kassab Orthopedic Institute (Tunis)	2006 2010	ISAba1 Chromosome	[^Citation75]
			A. baumannii	2	ND	Clinical	The Maternity and Neonatology center of Monastir	2011	Plasmid GR6 ISAba1 Chromosome	[^Citation44]
			A. baumannii	2	ST641	Clinical	Sahloul University Hospital (Sousse)	2012	Plasmid Gr6 Tn2008 ISAba1	[^Citation76]
			A. baumannii	235	ST85 (ST1089)	Clinical	Sahloul University Hospital (Sousse)	2013–2014–2015	Plasmid (repAci6-family) Tn2008 ISAba1	[^Citation25]
			A. baumannii	5	ND	Rectal carriage	Charles Nicolle Hospital (Tunis)	2014	ND	[^Citation59]
			A. baumannii	11	ST195	Fecal carriage		2014–2015	ND	[^Citation61]
			A. baumannii	25	ST2 ST1 ST164 ST310 ST570 ST602 ST623 ST636	Clinical	Mohamed Kassab Orthopedic Institute (Tunis)	2013–2014–2015–2016	ND	[^Citation73]
			A. baumannii	83	ND	Clinical	Fattouma Bourguiba Hospital (Monastir)	2013–2014–2015–2016	ISAba1	[^Citation40]
			A. baumannii	3	ND	Clinical	Regional Hospital of Djerba	2015–2016	ISAba1 Chromosome	[^Citation22]
			A. baumannii	2	ST2	Seafood (mussel and Oyster)	Bizerte lagoon	2015–2016	ND	[^Citation32]
D	OXA-51	OXA-51	A. baumannii	19	ND	Clinical	Sahloul University Hospital (Sousse)	2001–2002–2003–2004–2005	Chromosome	[^Citation45]
			A. baumannii	50	ND	Clinical	Charles Nicolle Hospital (Tunis)	2007	Chromosome	[^Citation74]
			A. baumannii	2	ST1	Clinical	Military Hospital of Tunis Mohamed Kassab Orthopedic Institute	2006 2010	Chromosome	[^Citation75]
			A. baumannii	5	ND	Rectal carriage	Charles Nicolle Hospital (Tunis)	2014	ND	[^Citation59]
			A. baumannii	13	ST195	Fecal carriage	Charles Nicolle Hospital (Tunis)	2014–2015	Chromosome	[^Citation61]
			A. baumannii	101	ND	Clinical	Fattouma Bourguiba Hospital (Monastir)	2013–2014–2015–2016	ISAba1 Chromosome	[^Citation40]
			A. baumannii	25	ST2 ST1 ST164 ST310 ST570 ST602 ST623 ST636	Clinical	Mohamed Kassab Orthopedic Institute (Tunis)	2013–2014–2015–2016	Chromosome	[^Citation73]
		OXA-66	A. baumannii	2	ND	Clinical	The Maternity and Neonatology center of Monastir	2011	Chromosome	[^Citation44]
		OXA-82	A. baumannii	2	ST641	Clinical	Sahloul University Hospital (Sousse)	2012	ISAba1 Chromosome	[^Citation76]
		OXA-94	A. baumannii	11	ST85 (ST1089)	Clinical	Sahloul University Hospital (Sousse)	2013–2014–2015	ISAba1 Chromosome	[^Citation25]
	OXA-58	OXA-58	A. baumannii	1	ST1	Clinical	Mohamed Kassab Orthopedic Institute (Tunis)	2013–2014–2015–2016	ND	[^Citation73]
		OXA-97	A. baumannii	19	ND	Clinical	Sahloul University Hospital (Sousse)	2001–2002–2003–2004–2005	Plasmid Chromosome ISAba3	[^Citation45]

Note: *Enterobacter aerogenes has been recently renamed Klebsiella aerogenes.³⁵

Abbreviation: ND, not determined.

Table 2 The Frequencies of Carbapenemases Detected in Each Species in Tunisia from 2006 to 2019

	KPC		VIM		NDM-1		IMP		OXA-48		OXA-23		OXA-51		OXA-58		Total
	n	%	n	%	n	%	n	%	n	%	n	%	n	%	n	%	n	%
A. baumannii	–	–	–	–	14	12.28	–	–	–	–	424	100	230	100	20	100	688	55.62
P. aeruginosa	–	–	95	65.07	–	–	–	–	–	–	–	–	–	–	–	–	95	7.68
K. pneumoniae	20	90.91	39	26.71	99	86.84	25	100	222	86.72	–	–	–	–	–	–	405	32.74
E. coli	2	9.09	4	2.74	–	–	–	–	6	2.34	–	–	–	–	–	–	12	0.97
P. mirabilis	–	–	–	–	1	0.88	–	–	1	0.39	–	–	–	–	–	–	2	0.16
C. freundii	–	–	–	–	–	–	–	–	1	0.39	–	–	–	–	–	–	1	0.08
E. cloacae	–	–	1	0.69	–	–	–	–	11	4.30	–	–	–	–	–	–	12	0.97
E. aerogenes*	–	–	–	–	–	–	–	–	1	0.39	–	–	–	–	–	–	1	0.08
P. stuartii	–	–	–	–	–	–	–	–	13	5.08	–	–	–	–	–	–	13	1.05
S. enterica	–	–	–	–	–	–	–	–	1	0.39	–	–	–	–	–	–	1	0.08
H. pylori	–	–	7	4.79	–	–	–	–	–	–	–	–	–	–	–	–	7	0.57
Total	22	1.78	146	11.80	114	9.22	25	2.02	256	20.69	424	34.28	230	18.59	20	1.62	1237	100

Note: *Enterobacter aerogenes has been recently renamed Klebsiella aerogenes.³⁵

Figure 1 (A) Number of published papers reporting carbapenem-resistant Gram-negative bacteria in Tunisia from 2006 to 2019. (B) Number of published papers per carbapenemase classes in Tunisia from 2006 to 2019.

Figure 2 Regional distribution of carbapenemase producing Gram-negative bacteria in Tunisia from 2006 to 2019.

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