High Prevalence of Multi-Drug Resistance and Extended-Spectrum Beta-Lactamase-Producing Enterobacteriaceae Among Hospitalized Patients Presumptive for Bacterial Infection at Debre Berhan Comprehensive Specialized Hospital, Ethiopia

Figures & data

Table 1 Sociodemographic Characteristics of Study Participants at Debre Berhan Comprehensive Specialized Hospital from January to May 2021

Sociodemographic Characteristics	Categories	n (%)
Sex	Male	154(40.1)
	Female	230(59.9)
Age	0–15	149(38.8)
	16–25	62(16.1)
	26–40	96(25)
	41–60	64(16.7)
	>60	13(3.4)
Place of residence	Rural	240(62.5)
	Urban	144(37.5)
Adult marital status	Married	170(75.5)
	Single	22(9.6)
	Divorced	30(13.5)
	Widowed	3(1.3)
Educational status	Illiterate	17(4.4)
	Read and write	79(20.6)
	Primary	158(41.1)
	Secondary	22(5.7)
	Diploma and above	28(7.3)
	Not applicable	80(20.8)
Adult occupational status	Governmental employed	13(5.7)
	Merchant	23(10.4)
	Housewife	56(24.7)
	Daily labour	13(5.7)
	Farmer	105(46.6)
	Other	15(6.8)
Average family income	<1000ETB	276(71.9)
	1000–2000ETB	80(20.8)
	>2000ETB	28(7.3)
Hand washing habit before meal	Yes	321(83.6)
	No	63(16.4)
Habit of eating uncooked vegetable	Yes	38(9.9)
	No	346(90.1)
Habit of eat uncooked animal product	Yes	21(5.5)
	No	363(94.5)

Note: Not applicable for educational status indicates: under age.

Abbreviation: ETB, Ethiopian birr.

Table 2 Clinical Profile of the Study Participants at Debre Berhan Comprehensive Specialized Hospital from January to May 2021

Variables	Categories	n (%)
History of antibiotic use for last 3 months	Yes	106(27.6)
	No	278(72.4)
Discontinuing of antibiotics	Yes	3(0.8)
	No	103(26.8)
History of hospitalization in the last three months	Yes	76(19.8)
	No	308(80.2)
Previous history of ICU stays	Yes	1(0.3)
	No	383(99.7)
History of invasive procedure	Yes	21(5.5)
	No	363(94.5)
Types of invasive procedure	Catherization	11(2.9)
	Surgery	8(2.1)
	Other	2(0.5)
Admission ward	Neonatal ICU	68(17.7)
	Paediatric	80(20.8)
	Medical	91(23.7)
	Surgery	53(13.8)
	Adult ICU	24(6.3)
	Gynaecology and obstetrics	57(14.8)
	Ophthalmology	11(2.9)
Duration in the ward in days	3–7	357(93.0)
	8–15	27(7.0)
Chronic underlying disease	Yes	42(10.9)
	No	342(89.1)
Types of chronic disease	Diabetes mellitus	18(4.7)
	HIV	14(3.6)
	Hypertension	4(1.0)
	Other	6(1.5)
Previous history of UTI	Yes	10(2.6)
	No	374(97.4)
Number of patients per room	2–4	165(43.0)
	5–8	219(57.0)
Number of beds per room	2–4	79(20.6)
	2–8	305(79.4)

Abbreviation: ICU, intensive care unit.

Table 3 ESBL-PE Isolates Against Clinical Specimen Types at Debre Berhan Comprehensive Specialized Hospital from January to May 2021

Isolates	Clinical Sample	ESBL Production (n=164)		Total n (%)
		Positive n (%)	Negative n (%)
E. coli	Blood	14(8.5)	3(1.8)	17(10.4)
	Urine	22(13.4)	9(5.5)	31(18.9)
	Wound	9(5.5)	5(3.0)	14 (8.5)
	Sputum	–	2(1.2)	2(1.2)
	Stool	5(3.0)	5(3.0)	10(6.1)
	Total	50(30.4)	24(14.6)	74(45.1)
K. pneumoniae	Blood	8(4.9)	5(3.0)	13(7.9)
	Stool	2(1.2)	1(0.6)	3(1.8)
	Urine	10(6.1)	13(7.9)	23(14.0)
	Wound	4(2.4)	4(2.4)	8(4.9)
	Total	24(14.6)	23(14.0)	47(28.7)
K. oxytoca	Blood	2(1.2)	2(1.2)	4(2.4)
	Stool	3(1.8)	–	3(1.8)
	Total	5(3.0)	2(1.2)	7(4.3)
C. divresus	Wound	1(0.6)	–	1(0.6)
	Stool	1(0.6)	–	1(0.6)
	Blood	5(3.0)	1(0.6)	6(3.7)
	Urine	–	2(1.2)	2(1.2)
	Total	7(4.3)	3(1.8)	11(6.7)
E. aerogenes	Wound	1(0.6)	–	1(0.6)
	Urine	1(0.6)	2(1.2)	3(1.8)
	Stool	1(0.6)	2(1.2)	3(1.8)
	Total	3(1.8)	4(2.4)	7(4.3)
M. morganii	Urine	–	1(0.6)	1(0.6)
	Stool	1(0.6)	–	1(0.6)
	Total	1(0.6)	1(0.6)	2(1.2)
K. ozaenae	Blood	3(1.8)	–	3(1.8)
	Urine	1(0.6)	–	1(0.6)
	Total	4(2.4)	–	4(2.4)
P. stuartii	Urine	3(1.8)	–	3(1.8)
	Blood	1(0.6)	–	1(0.6)
	Stool	–	1(0.6)	1(0.6)
	Total	4(2.4)	1(0.6)	4(2.4)
E. cloacae	Urine	3(1.8)	1(0.6)	4(2.4)
	Stool	1(0.6)	1(0.6)	2(1.2)
	Total	4(2.4)	2(1.2)	6(3.7)
Citrobacter spp	Wound	1(0.6)	–	1(0.6)
	Total	1(0.6)	–	1(0.6)
C. freundii	Stool	1(0.6)	–	1(0.6)
	Total	1(0.6)	–	1(0.6)
Total		104(63.4)	60(36.6)	164(100)

Table 4 Antimicrobial Resistance Pattern of Enterobacteriaceae Isolates at Debre Berhan Comprehensive Specialized Hospital from January to May 2021

Isolates	AST	Antibacterial Agents Level n (%) (n = 164)
		AMP	FOX	GEN	CIP	STX	AMC	MER	IMP	CTX	CAZ	CRO	TET	FEP	C
E. coli (74)	S	–	46(62.1)	42(56.8	7(9.5)	16(21.6)	20(27.0)	56(75.7)	60(81.1)	12(16.2)	12(16.2)	15(20.3)	–	14(29.7)	42(56.8)
	I	–	–	5(6.7)	25(33.7		7(9.5)	2(2.7)	–	–	–	3(4.1)	–	–	1(1.4)
	R	74(100)	28(38.0)	27(36.5)	42(56.8)	58(85.4)	47(63.5)	16(21.6	14(18.9)	62(83.2)	62(83.8)	56(75.7)	74(100)	52(70.3)	31(41.8)
K. pneumoniae (47)	S	–	20(42.6)	26(55.3	2(4.3)	8(17.0)	8(17.00)	31(66.0)	37(78.7)	10(21.3)	10(21.3)	14(29.8)	3(6.4)	14(29.8)	22(46.8)
	I	–		2(4.3)	15(31.9)		3(6.40)	1(2.1)	–	–	2(4.3)	1(2.1)	–	–	–
	R	47(100	27(57.4)	19(40.4)	30(63.8)	39(83.0)	36(76.6)	15(31.9)	10(21.3)	37(78.7)	37(78.7)	32(68.1)	44(93.6)	33(70.2)	25(53.2)
K. oxytoca (7)	S	–	1(14.2)	1(14.3)	–	1(14.3)	–	3(42.90	4(57.1)	–	–	1(14.3)	–	–	2(28.6)
	I	–	–	–	1(14.3)		–	–	–	–	–	–	–	–	–
	R	7(100)	6(85.8)	6(85.7)	6(85.7)	6(85.7)	7(100)	4(57.1)	3(42.9)	7(100)	7(100)	6(86.7)	7(100)	7(100)	5(71.4)
Citrobacter spp (1)	S	–	1(100)	–			–	1(100)	1(100)	–	–		–	–	–
	I	–		–	–		–		–	–	–	–	–	–	–
	R	1(100)	–	1(100)	1(1000	1(100)	1(100)		–	1(00)	1(100)	1(100)	1(100)	1(100)	1(100)
E. aerogens (7)	S	–	5(71.4)	4(57.1)	1(14.3)	29(28.6)	4(57.1)	6985.7)	7(100)	2(28.6)	4(57.1)	4(57.1)	–	4(57.1)	4(57.1)
	I	–	–	–	5(71.4)		1(14.3)	–	–	2(28.6)	–	–	–	–	–
	R	7(100)	2(28.6)	3(42.9)	1(14.3)	5(71.4)	2(28.6)	1(14.3)	–	3(42.8)	3(42.9)	4(42.9	7(100)	4(42.9)	3(42.9)
P. stuartii (5)	S	–	1(20.0)	2(40.0)	1(20.0)		–	1(20.0)	1(20.0)	1(20.0)	–	1(20.0)	–	–	1(14.3)
	I	–		–	–		–	–	–	–	–	–	–	–	–
	R	5(100)	4(80.0)	3(60.0)	4(80.0)	5(100)	5(100)	4(80.0)	4(80.0)	4(80.0)	5(100)	4(80.0)	5(100)	5(100)	4(80.0)
M. morganii (2)	S	–	–	1(50.0)	–			2(100)	2(100)	1(100)	1(50.0)	–	–	–	1(50.0)
	I	–		(50.0)	950.0)			–		–	–	–	–	–	–
	R	2(100)	2(100)	–	1(50.0)	2(100)	2(100)			1(50.0)	1(50.0)	2(100)	2(100)	2(100)	1(50.0)
E. cloacae (6)	S	–	3(50.0)	1(16.7)	–	1(16.7)	2(33.3)	5(83.3)	1(16.7)	1(16.7)	1(16.7)	2(33.3)	–	1(16.7)	2(33.3)
	I	–		2(33.3)	2(33.3)		–	1(16.7)	–	–	–	–	–	–	–
	R	6(100)	3(50.0)	3(50.0)	4(66.7)	5(83.3)	4(66.7)	–	5(83.3)	5(83.7)	5(83.3)	4(66.7)	6(100)	5(83.3)	4(66.7)
C. diverus (10)	S	–	3(30.0)	4(40.0)	2(20.0)	3(30.0)	1(10.0)	7(70.0)	6(60.0)	3(30.0)	1(10.0)	3(30.0)	–	1(10.0)	5(50.0)
	I	–	–	–	1(10.0)		–		–	–	–	–	–	–	–
	R	10(100)	7(70.0)	6(60.0)	7(70.0)	7(70.0	9(90.0)	3(30.00	4(40.00	7(70.0)	9(90.0)	7(70.0)	10(100)	9(90.0)	5(50.0)
C. freundii (1)	S	–	1(100)	1(100)	–		–	1(100)	1(100)	–	–	–	–	–	1(50.0)
	I	–	–	–	–		–	–	–	–	–	–	–	–	–
	R	1(100)	–	–	1(100)	1(100)	1(100)	–	–	1(100)	1(100)	1(100	1(100)	1(100)	1(50.0)
K. ozaenae (4)	S	–	3(75.0)	1(25.0)	–	1(25.0)	1(25.0)	3(75.0)	3(75.0)	1(25.0)	–	–	–	–	2(50.0)
	I	–	–	–	–	–		–	–	–	–	–	–	–	–
	R	4(100)	1(25.0	3(75.0)	4(100)	3(75.)	3(75.0)	1(25.0	1(25.0	4(75.0)	4(100)	4(100)	4(100)	4(100)	2(50.0)
Total (164)	S	–	85(51.8)	84(51.2)	17(10.4)	34(20.7)	127(77.4)	116(70.7)	38(23.2)	33(2.1)	30(18.3)	42(25.6)	4(2.4)	43(26.2)	81(49.4)
	I	–	–	9(5.5)	47(28.8)	–	3(1.8)	4(2.4)	3(4.4))	5(3.0)	2(1.2)	4(2.4)	–	–	1(0.6)
	R	164(100)	79(48.2)	71(43.3	100(61.0)	130(85)	34(20.7)	44(26.8)	115(70.7)	126(76.8)	132(80.5)	118(72.0)	160(97.6)	121(73.8)	82(50.0)

Abbreviations: AMP, ampicillin; FOX, cefoxitin; GM, gentamycin; CIP, ciprofloxacin; COT, cotrimoxazole; IMP, imipenem; MER, meropenem; AMC, amoxicillin–clavulanic acid; CTX, cefotaxime; CAZ, ceftazidime; CRO, ceftriaxone; TE, tetracycline; FEP, cefepime; C, chloramphenicol; S, susceptible; R, resistance; I, intermediate.

Table 5 Multi-Drug Resistance Patterns of Enterobacteriaceae Isolates at Debre Berhan Comprehensive Specialized Hospital from January to May 2021

Level of Antibiotic Resistance n (%)
Isolates (Number)	R0	R1	R2	R3	R4	R5	R6	≥R7	Total MDR R≥3
E. coli (n = 74)	0(0.0)	1(1.4)	5(6.8)	2(2.7)	2(2.7)	7(9.1)	5(6.8)	52(70.3)	68(91.9)
K. pneumoniae (n = 47)	0(0.0)	0(0.0)	1(2.1)	4(8.5)	4(8.5)	2(4.3)	2(4.3)	34(72.3)	46(97.9)
E. cloacae (n = 7)	0(0.0)	0(0.0)	0(0.0)	1(14.3)	1(14.3)	0(0.0)	0(0.0)	4(57.1)	6(85.7)
E. aerogens (n = 7)	0(0.0)	0(0.0)	2(33.3)	1(16.7)	1(16.7)	0(0.0)	0(0.0)	3(42.3)	5(71.4)
K. oxytoca (n = 7)	0(0.0)	0(0.0)	0(0.0)	0(0.0)	1(14.3)	0(0.0)	0(0.0)	6(85.7)	7(100)
M. morganii (n = 2)	0(0.0)	0(0.0)	1(50.0)	0(0.0)	0(0.0)	0(0.0)	0(0.0)	1(50.0)	1(50.0)
C. diverus (n = 10)	0(0.0)	1(10.0)	1(10.0)	1(10.0)	0(0.0)	0(0.0)	1(10.0)	6(60.0)	8(80.0)
C. freundii (n = 1)	0(0.0)	0(0.0)	0(0.0)	0(0.0)	0(0.0)	0(0.0)	0(0.0)	1(100)	1(100)
P. stuartii (n = 5)	0(0.0)	1(20.0)	0(0.0)	0(0.0)	0(0.0)	0(0.0)	0(0.0)	4(80.0)	4(80.0)
Citrobacter spp (n = 1)	0(0.0	0(0.0)	0(0.0)	0(0.0)	0(0.0)	0(0.0)	0(0.0)	1(100)	1(100)
K. ozaenae (n = 4)	0(0.0	0(0.0)	0(0.0)	0(0.0)	0(0.0)	0(0.0)	0(0.0)	4(100)	4(100)
Total (n = 164)	0(0.0)	2(1.2)	9(5.5)	9(5.5)	9(5.5)	9(5.5)	8(4.9)	116(70.1)	151(92.1)

Abbreviations: R0, resistance to no antibiotics; R1-7, resistance to 1, 2, 3, 4, 5, 6, and 7 antibiotics; ≥R3, resistance to 3 or more antibiotics from different classes (resistant to one or more antibiotics in three or more classes).

Figure 1 Distribution of ESBL-PE at Debre Berhan Comprehensive Specialized Hospital from January to May 2021.

Figure 2 Antibiotics susceptibility pattern of ESBL positive and ESBL negative to different classes of antibiotics at Debre Berhan Comprehensive Hospital from January to May 2021.

Abbreviations IMP, imipenem; MER, meropenem; AMC, amoxicillin–clavulanic acid; CTX, cefotaxime; CAZ, ceftazidime; CRO, ceftriaxone; TET, tetracycline; FEP, cefepime; C, chloramphenicol.

Table 6 Distribution of ESBL-PE and MDR Isolates at Debre Berhan Comprehensive Specialised Hospital from January to May 2021

Isolates	ESBL n (%)		MDR n (%)
	Positive	Negative
E. coli (n= 74)	50(73.5)	18(26.5)	68(91.9)
K. pneumoniae (n = 47)	24(52.2)	22(47.2)	46(97.9)
E. cloacae (n = 7)	4(66.6)	2(33.3)	6(85.7)
E. aerogens (n = 7)	3(60.0)	2(40.0)	5(71.4)
K. oxytoca (n = 7)	5(71.4)	2(28.6)	7(100)
M. morganii (n = 2)	1(100)	0(0.0)	1(50.0)
C. diverus (n = 10)	7(87.5)	1(12.5)	8(80.0)
C. freundii (n = 1)	1(100)	0(0.0)	1(100)
P. stuartii (n = 5)	4(100)	0(0.0)	4(80.0)
Citrobacter spp (n = 1)	1(100)	0(0.0)	1(100)
K.ozaenae (n = 4)	4(100)	0(0.0)	4(100)
Total (n = 164)	104(68.9)	47(31.1)	151(92.1)

Table 7 Associated Risk Factors for ESBL-PE Infection Using Bivariate and Multivariate Analysis at Debre Berhan Comprehensive Specialized Hospital from January to May 2021

Variables	Categories	ESBL Production		COR (95% CI)	P-value	AOR (95% CI)	P-value
		Positive n (%)	Negative n (%)
Hand washing habit before the meal	Yes	92(56.1)	43(26.2)	Ref
	No	12(7.3)	17(10.4)	3(13–6.9	0.00	2.5(0.5–11)	0.23
Habit of eating uncooked vegetable	Yes	28(17.1)	5(3.0)	4(1.5–11.2)	0.07	2.2(0.5–8.7)	0.26
	No	76(46.3)	55(33.5)	Ref
History of antibiotic use for the last three months	Yes	54(32.9)	15(9.1)	3.2(1.6–6.5)	0.0	6.3(1.8–21.6)	0.001**
	No	50(30.5)	45(27.4)	Ref
History of hospital stays	Yes	62(37.8)	6(3.7)	13(5.2–34)	0.00	1.9(1.4–6.9)	0.001**
	No	42(25.6)	54(32.9)	Ref
Admission ward	Medical	26(15.9)	12(7.3)	0.7(0.2)	0.51	1.9(0.3–9.7)	0.40
	Surgical	18(11.0)	6(3.7)	0.9(0.3–3.5)	0.94	0.3(0.0–2.3)	0.28
	Paediatric	30(18.3)	15(9.1)	0.6(0.2–1.9)	0.41	1.3(0.3–5.7)	0.70
	NICU	10(6.1)	17(10.4)	0.2(0.1–0.6)	0.06	0.1(0.0–0.7)	0.02**
	Adult ICU	1(0.6)	4(2.4)	0.1(0.0–0.8)	0.04	0.4(0.0–5.4)	0.49
	G/obs	19(11.5)	6(3.7)	Ref
Chronic diseases	Yes	21(12.8)	3(1.8)	4(1.1–14.0)	0.03	4.9(1.1–22.9)	0.04**
	No	83(50.6)	57(34.8)	Ref

Note: **(P<0.05).

Abbreviations: COR, crude odds ratio; AOR, adjusted odds ratio; CI, confidence interval; Ref, Reference; NICU, neonatal intensive care unit; ICU, intensive care unit; G/obs, gynecology and obstetrics.