A Systematic Review on Drug Resistant Urinary Tract Infection Among Pregnant Women in Developing Countries in Africa and Asia; 2005–2016

Figures & data

Table 1 Characteristics of Eligible Studies and Distribution of Uropathogens Causing Urinary Tract Infection in Pregnant Women Reviewed from Africa and Asia from 2005 to 2016

First Author	Country	Pub. Year	Setting	Sample Size	UTI Overall Prev. N (%)	Uropathogens Causing Urinary Tract Infection N (%)
						E. coli	Klebsiella species	S. aureus	CN. Staphylococci	P. mirabilis	Enterococcus	P. aeruginosa	Enterobacter	Non-hemolytic streptococci	Citrobacter
Derese^Citation15	Ethiopia	2016	Hospital	180	26 (14.4)	9 (34.6)	3 (11.5)	2 (7.7)	5 (19.2)	2 (7.7)	-	-	-	-	2 (7.7)
Jenifer^Citation36	Sri Lanka	2012	Hospital	250	9 (3.6)	6 (66.6)	-	2 (22.2)	1 (11.1)	-	-	-	-	-	-
Labi^Citation39	Ghana	2015	Hospital	274	15 (5.5)	2 (13.3)	-	-	2 (13.3)	3 (20)	4 (26.7)	-	1 (6.7)	2 (13.3)	1 (6.7)
Sibi^Citation19	India	2014	Hospital	395	180 (46.6)	79 (43.9)	59 (32.7)	7 (2.2)	10 (5.5)	9 (5)	12 (6.7)	4 (1.7)	-	-	-
Thapa^Citation21	Nepal	2015	Hospital	300	92 (30.5)	48 (52)	16 (17.3)	7 (7.3)	1 (1.3)	15 (16)	-	1 (0.7)	4 (4)	-	1(1.3)
Vaijanathrao^Citation3	India	2015	Hospital	2445	491 (20.1)	233 (47.5)	89 (18.1)	34 (6.9)	31 (6.3)	7 (1.4)	53 (10.8)	23 (4.7)	21 (4.3)	-	-
Oli^Citation22	Nigeria	2010	Hospital	357	65 (18.21)	21 (25.6)	11 (13.4)	17 (20.73)	13 (15.8)	3 (3.66)	-	-	-	-	-
Alemu^Citation14	Ethiopia	2012	Hospital	385	40 (10.4)	19 (47.5)	4 (10)	4 (10)	9 (22.5)	2 (5)	-	4 (10)	2 (5)	-	-
Turpin^Citation25	Ghana	2007	Hospital	220	16 (7.3)	6 (37.5)	2 (12.5)	5 (31.2)	1 (6.25)	-	2 (12.5)	-	-	-	-
Moghadas ^Citation26	Iran	2009	HC	297	10 (3.3)	7 (70)	2 (20)	-	-	-	-	-	1 (10)	-	-
Hamdan^Citation27	Sudan	2011	Hospital	235	33 (14)	14 (42.4)	3 (9)	13 (39.3)	-	-	-	1 (3)	-	2 (6)	-
Mokube^Citation28	Cameroon	2013	HC, Hospital & clinics	102	24 (23.5)	9 (37.5)	8 (33.3)	-	-	-	-	3 (12.5)	4 (16.6)	-	–
Al-Haddad^Citation29	Yemen	2005	Hospital	137	41 (30)	17 (41.5)	4 (9.8)	8 (19.5)	-	5 (12.2)	-	-	-	2 (4.9)	-
Lewis^Citation30	S. Africa	2013	Hospital	425	203 (47.8)	160 (79.6)	5 (2.5)	-	5 (2.5)	10 (5)	3 (1.5)	-	-	7 (3.5)	1 (0.5)
Andabati^Citation31	Uganda	2010	Hospital	218	29 (13.1)	15 (51.2)	5 (18)	2 (6.2)	6 (20.2)	-	1 (0.8)	2 (6)	-	-	-
Sharifa^Citation32	Saudi Arabia	2010	Hospital & clinics	9698	166 (1.7)	88 (53)	1 (0.6)	8 (4.8)	-	1 (0.6)	-	-	-	18 (10.8)	-
Okon^Citation23	Nigeria	2012	Hospital	200	118 (59)	23 (19.5)	47 (39.8)	27 (22.9)	-	11 (9.3)	-	10 (8.5)	-	-	-
Sabrina^Citation33	Tanzania	2010	Hospital	200	42 (21)	14 (33.3)	9 (21.4)	6 (14.3)	7 (16.7)	3 (7.1)	3 (7.1)	-	-	-	-
Demlie^Citation17	Ethiopia	2012	Hospital	367	35 (9.5)	16 (45.7)	-	4 (11.4)	6 (17.1)	-	-	-	-	-	-
Ullah^Citation35	Bangladesh	2007	Hospital	1800	430 (23.8)	320 (74.4)	18 (4.2)	84 (19.5)	-	8 (1.8)	-	-	-	-	-
Manjula^Citation20	India	2013	Hospital & clinics	417	206 (49.4)	117 (56.8)	41 (19.9)	-	-	12 (5.8)	2 (0.9)	13 (6.3)	8 (3.8)	10 (4.8)	3 (1.4)
Haider^Citation37	Pakistan	2010	Hospital	232	10 (4.3)	7 (70)	-	3 (30)	-	-	-	-	-	-	-
Enayat ^Citation38	Iran	2008	Clinics	1505	134 (8.9)	79 (58.9)	-	18 (13.4)	22 (16.4)	-	-	-	-	-	-
Thairu^Citation24	Nigeria	2013	Hospital	180	78 (43.3)	18 (23.1)	9 (11.5)	8 (10.2)	12 (15.4)	8 (10.2)	5 (6.4)	4 (5.1)	9 (11.5)	5 (6.4)	-
Masinde^Citation34	Tanzania	2009	Hospital	247	36 (14.5)	16 (44.4)	2 (5.5)	-	-	-	-	4 (11.1)	3 (8.3)	-	-
Kabew^Citation40	Ethiopia	2013	Hospital	3182	742 (23.3)	361 (48.6)	136 (18.3)	25 (3.4)	49 (6.6)	9 (1.2)	41 (5.5)	27 (3.6)	29 (3.9)	4 (0.5)	27 (3.6)
Total				24,248	3271 (13.5)	1804 (55.2)	479 (14.6)	284 (8.3)	180 (5.3)	108 (3.2)	126 (3.7)	96 (2.8)	92 (2.8)	57 (1.5)	34 (1)

Notes: Study targets of all reviewed studies were pregnant women. Sample source for all studies were urine of pregnant women. Percentage is calculated from the sample size of individual studies. While the percentage in the total raw is calculated from the total sample size.

Abbreviations: E. coli, Escherichia coli; S. aureus, Staphylococcus aureus; CN. Staphylococci, Coagulase negative Staphylococci; P. mirabilis, Proteus mirabilis; P. aeruginosa, Pseudomonas aeruginosa; HC, health center; UTI, urinary tract infection; Pub. year, publication year; Prev, prevalence.

Figure 1 Frequency of uropathogenic bacteria among pregnant women in developing countries in Africa and Asia from 2005 to 2016.

Table 2 Review on Antimicrobial Resistance Patterns of Uropathogens Causing UTI Among Pregnant Women in Developing Countries Conducted in Asia from 2005 to 2016

Author	Uropathogens	Resistance Patterns, N (%)
		AMP	CIP	NA	SXT	GM	NOR	F	AMO	CRO
Sibi^Citation19	E.coli	N/D	18 (22.8)	41 (51.9)	13 (16.5)	69 (87.4)	34 (43.1)	N/D	75 (94.9)	32 (40.5)
	S. aureus	N/D	3 (48)	2 (25)	2 (25)	3 (50)	5 (75)	N/D	3 (50)	7 (100)
	CN Staphylococci	N/D	4 (40)	2 (20)	1 (10)	5 (50)	6 (60)	N/D	3 (30)	4 (40)
	Klebsiellaspp.	N/D	24 (35.5)	9 (33)	17 (25)	29 (42)	16 (57)	N/D	47 (68)	40 (58)
	P. aeruginosa	N/D	0 (0)	1 (33.3)	0(0)	1 (33.4)	1 (33.3)	N/D	2 (50)	1 (33.3)
	P. mirabilis	N/D	1 (10.1)	0 (0)	3 (33.3)	6 (66.7)	3 (33.3)	N/D	2 (22.8)	1 (12)
	Enterococcus	N/D	4 (33.3)	0 (0)	2 (16.7)	8 (66.7)	3 (25)	N/D	3 (25)	5 (42)
Thapa^Citation21	E. coli	44 (56.4)	32 (41)	N/D	32 (41)	6 (7.7)	46 (58.9)	8 (10.3)	N/D	N/D
	Klebsiellaspp.	20 (76.4)	10 (38.5)	N/D	10 (38.5)	3 (11.5)	2 (7.69)	7 (26.9)	N/D	N/D
	P. aeruginosa	0 (0)	0 (0)	N/D	1 (100)	0 (0)	1 (100)	0 (0)	N/D	N/D
	P. mirabilis	13 (54.2)	7 (29.2)	N/D	12 (50)	3 (12.5)	1 (4.2)	4 (16.7)	N/D	N/D
	Enterococcus	4 (66.7)	3 (50)	N/D	4 (66.7)	0 (0)	3 (50)	0 (0)	N/D	N/D
	Citrobacter	1 (50)	1 (50)	N/D	2 (100)	0 (0)	1 (50)	1 (50)	N/D	N/D
Ullah^Citation35	E. coli	N/D	8 (2.5)	186 (58.1)	222 (69.4)	N/D	N/D	160 (50)	170 (53)	N/D
	CN Staphylococci	N/D	6 (7.1)	40 (47.6)	58 (66.7)	N/D	N/D	36 (42.4)	34 (40.5)	N/D
	Klebsiellaspp.	N/D	0 (0)	6 (33.3)	16 (88.9)	N/D	N/D	4 (22.2)	10 (55.6)	N/D
	P. mirabilis	N/D	0 (0)	2 (25)	6 (75)	N/D	N/D	2 (25)	4 (50)	N/D
Enayat^Citation38	E. coli	77 (97.5)	10 (92.7)	64 (81.1)	59 (74.7)	75 (94.9)	21 (26.6)	56 (70.9)	N/D	N/D
	S. aureus	12 (66.7)	12 (66.7)	N/D	14 (77.7)	N/D	3 (16.6)	10 (55.5)	N/D	N/D
	CN Staphylococci	14 (63.6)	8 (38.4)	2 (27.3)	18 (81.8)	N/D	12 (54.6)	12 (54.6)	N/D	N/D
	Klebsiellaspp.	2 (40)	1 (20)	4 (80)	4 (80)	2 (40)	N/D	N/D	N/D	N/D
	Enterobacter	6 (60)	2 (20)	1 (10)	3 (30)	3 (30)	6 (60)	4 (40)	N/D	N/D

Notes: Resistance patterns for each studies were calculated as a percentage of individual bacterial isolates. All studies use Clinical and Laboratory Standards Institute (CLSI) guideline to depict the resistance patterns of each bacterial isolate.

Abbreviations: N/D, resistance pattern not determined; AMP, ampicillin; CIP, ciprofloxacin; NA, nalidixic acid; SXT, trimethoprim-sulfamethoxazole; GM, gentamicin; NOR, norfloxacin; F, nitrofurantoin; AMO, amoxicillin; CRO, ceftriaxone.

Table 3 Review on Antimicrobial Resistance Patterns of Uropathogens Causing UTI Among Pregnant Women in Developing Countries Conducted in Africa from 2005 to 2016

Author	Uropathogens	Resistance Patterns, N (%)
		AMP	CIP	NA	SXT	GM	NOR	F	AMO	CRO
Derese^Citation15	E. coli	7 (77.7)	1 (11.1)	4 (44.5)	1 (11.1)	0 (0)	N/D	4 (44.4)	7 (77.7)	0 (0)
	S. aureus	2 (100)	1 (50)	N/D	1 (50)	0 (0)	N/D	1 (50)	1 (50)	1 (50)
	Klebsiellaspp.	3 (100)	1 (33.3)	1 (33.5)	2 (66.7)	1 (33.3)	N/D	3 (100)	3 (100)	0 (0)
	P. aeruginosa	4 (100)	1 (25)	3 (75)	4 (100)	2 (50)	N/D	3 (75)	2 (50)	1 (25)
	P. mirabilis	2 (100)	0 (0)	1 (50)	1 (50)	0 (0)	N/D	1 (50)	2 (100)	0 (0)
	Citrobacter	1 (100)	0 (0)	1 (100)	0 (0)	0 (0)	N/D	0 (0)	0 (0)	0 (0)
	CN staphylococci	4 (80)	2 (40)	N/D	4 (80)	0 (0)	N/D	1 (20)	4 (80)	1 (20)
Labi^Citation39	E. coli	2 (100)	N/D	2 (100)	2 (100)	2 (100)	N/D	0 (0)	N/D	N/D
	CN Staphylococcus	2 (100)	N/D	1 (50)	2 (100)	2 (100)	N/D	0 (0)	N/D	N/D
	P. mirabilis	3 (100)	N/D	3 (100)	3 (100)	2 (66.6)	N/D	0 (0)	N/D	N/D
	Enterococcus	4 (100)	N/D	3 (75)	4 (100)	4 (100)	N/D	0 (0)	N/D	N/D
Oli^Citation22	E. coli	16 (76.2)	N/D	16 (76.7)	12 (57.2)	7 (33.3)	N/D	10 (47.6)	11 (52.4)	3 (14.3)
	S. aureus	15 (88.3)	N/D	14 (82.4)	12 (70.6)	10 (58.8)	N/D	14 (82.4)	11 (64.7)	6 (35.3)
	CN. staphylococcus	8 (61.5)	N/D	9 (69.3)	10 (76.9)	3 (23.1)	N/D	9 (69.3)	6 (46.2)	0 (0)
	Klebsiella spp.	9 (81.8)	N/D	6 (54.5)	7 (63.6)	5 (45.5)	N/D	8 (72.3)	7 (63.7)	2 (17.3)
	P. mirabilis	2 (76.7)	N/D	1 (33.3)	2 (76.7)	1 (33.3)	N/D	1 (33.3)	1 (33.3)	0 (0)
Thairu^Citation24	E.coli	11 (60)	N/D	N/D	9 (52.5)	6 (31.2)	N/D	4 (20)	1 (8)	1 (5)
	S. aureus	0(0)	N/D	N/D	5 (59)	4 (44)	N/D	3 (41.5)	0 (0)	1 (3.2)
	CN. staphylococcus	1 (4)	N/D	N/D	8 (67)	7 (60)	N/D	7 (55)	0 (0)	4 (34)
	Klebsiellaspp.	5 (55)	N/D	N/D	2 (22)	4 (49.2)	N/D	0 (0)	1 (10)	3 (33.2)
	P. aeruginosa	2 (56)	N/D	N/D	4(100)	3 (87.3)	N/D	3 (68)	1 (33.4)	3 (79.5)
	P. mirabilis	4 (50)	N/D	N/D	7 (90)	4 (53.7)	N/D	4 (53.5)	1 (13.6)	5 (55.4)
	Streptococcus	4 (81.5)	N/D	N/D	5 (89.2)	3 (67.4)	N/D	3 (53.1)	0 (0)	2 (39.4)
	Enterococcus	1 (22)	N/D	N/D	3 (68)	2 (45)	N/D	2 (42.7)	0 (0)	1 (12)
	Enterobacter	6 (70)	N/D	N/D	4 (41.3)	1 (2.4)	N/D	5 (50)	2 (20)	6 (70)

Notes: Resistance patterns for each study were calculated as a percentage of individual bacterial isolates. All studies use Clinical and Laboratory Standards Institute (CLSI) guideline to depict the resistance patterns of each bacterial isolate.

Abbreviations: N/D, resistance pattern not determined; AMP, ampicillin; CIP, ciprofloxacin; NA, nalidixic acid; SXT, trimethoprim-sulfamethoxazole; GM, gentamicin; NOR, norfloxacin; F, nitrofurantoin; AMO, amoxicillin; CRO, ceftriaxone.

Table 4 Risk Factors Associated with UTI Among Pregnant Women Reviewed from Asia and Africa from 2005 to 2016

First Author	Continent	Significantly Associated with Bacteriuria	Not Significantly Associated with Bacteriuria
Derese^Citation15	Africa	Past history of UTI, family monthly income ≤500 birr and 501–1000 birr, age groups of 25–34 years, and educational level	History of catheter, History of antibiotics, Parity, gestational age
Jenifer^Citation36	Asia	–	Gestational diabetes, past UTI, multiparity, advanced maternal age, lower education level, advanced gestational age and lower socioeconomic status.
Labi^Citation39	Africa	Being frequently sexually active during pregnancy	Educational status, parity, gestational age, marital status and the number of fetuses carried, sexual frequency
Sibi^Citation19	Asia	Age group between 25–34 years, High sexual activities, recent use of diaphragm with spermicide	Gestational age of pregnancy
Thapa^Citation21	Asia	Parity, education status, occupation of pregnant women, times of bathing, history of UTI	Age group, pregnancy Trimester, Smoking habit
Vaijanathrao^Citation3	Asia	–	Gestational diabetic mellitus, Gestational age
Oli^Citation22	Africa	Educational level,	Gestational age
Alemu^Citation14	Africa	History of catheterization and previous history of UTI	Maternal age, address, parity, gravidity, trimester, occupation, marital status, education
Turpin^Citation25	Africa	Gestational age	Parity
Hamdan^Citation27	Africa	–	Age, gestational age, parity, and history of UTI
Mokube^Citation28	Africa	–	Gravidity, parity
Andabati^Citation31	Africa	–	Education level, Marital status, Smoking, Alcohol, Gravidity, Antibiotic (oral/injectable) used in the previous two weeks, gestational age
Sharifa^Citation32	Asia	Age, gravidity	History of previous abortions
Okon^Citation23	Africa	Tertiary education, third trimester, multi-gravidity, multiparity	-
Manjula^Citation20	Asia	Gestational age, parity, age group	-
Haider^Citation37	Asia	Illiteracy (Educational status), history of sexual activity, low socioeconomic (monthly income < Rs. 10,000/month) group, past history of UTI and multiparity	Age group, haemoglobin level
Enayat^Citation38	Asia	Hemoglobin level	Age, gravidity, Parity,
Thairu^Citation24	Africa	Age group, fever, previous symptoms of UTI, gestational age,	Gravidity
Masinde^Citation34	Africa	Low socioeconomic status	Maternal age, parity, gestational age, occupation, marital status, educational level

Figure 2 A diagrammatic illustration elucidating the possible risk factors of acquiring UTI and mechanism of bacterial drug resistance among pregnant women.

Table 5 Pooled Range and Mean of Antimicrobial Resistance Patterns of Uropathogenic Bacteria Causing Urinary Tract Infection in Pregnant Women Reviewed from Africa and Asia from 2005 to 2016

Uropathogens	Resistance Patterns, N (%)
	AMP		CIP		NA		SXT		GM		NOR		F		AMO		CRO
	PR	PM	PR	PM	PR	PM	PR	PM	PR	PM	PR	PM	PR	PM	PR	PM	PR	PM
E. coli	56.4–100	77.9	11.1–92.7	34.0	44.5–100	68.7	11.1–100	52.8	0–94.9	50.6	19.2–58.9	36.9	0–70.9	34.7	8–94.9	57.2	0–40.5	14.9
No. of studies	6		5		6		8		7		4		7		5		4
S. aureus	0–100	63.7	48–66.7	54.9			25–77.7	51.3			16.6–75	45.8
No. of studies	4		3				2				2
CN staphylococci	4–100	61.8	7.1–40	31.4	20–69.3	42.8	10–100	68.9	0–100	46.6	54.6–60	57.3	0–69.3	40.2	0–80	39.3	0–40	23.5
No. of studies	5		4		5		7		5		2		6		5		4
Klebsiella spp.	40–100	70.6	0–38.5	25.5	33–80	46.8	22–88.9	54.9	11.5–49.2	36.9	7.69–57	32.3	0–100	44.3	10–100	59.5	0–58	27.1
No. of studies	5		5		5		7		6		2		5		5		4
P. aeruginosa	0–100	52	0–25	8.3	33.3–75	54.2	0–100	75	0–87.3	42.6	33.3–100	66.6	0–75	47.6	33.4–50	44.5	25–79.5	45.9
No. of studies	3		3		2		4		4		2		3		3		3
P. mirabilis	50–100	76.2	0–29.2	9.8	0–100	41.6	33.3–100	67.8	0–66.7	38.8	4.2–33.3	18.7	0–53.5	29.7	13.6–100	43.9	0–55.4	16.8
No. of studies	5		4		5		7		6		2		6		5		4
Enterococcus	22–100	62.9	33.3–50	41.6	0–75	37.5	16.7–100	62.8	0–100	52.9	25–50	37.5	0–42.7	14.2	0–25	12.5	12–42	27
No. of studies	3		2		2		4		4		2		3		2		2
Citrobacter	50–100	75	0–50	25			0–100	50					0–50	25
No. of studies	2		2				2						2
Enterobacter	60–70	65					30–41.3	35.6	2.4–30	16.2			40–50	45
No. of studies	2						2		2				2

Abbreviations: AMP, ampicillin; CIP, ciprofloxacin; NA, nalidixic acid; SXT, trimethoprim-sulfamethoxazole; GM, gentamicin; NOR, norfloxacin; F, nitrofurantoin; AMO, amoxicillin; CRO, ceftriaxone; PR, pooled range; PM, pooled mean.

Figure 3 Pooled mean antimicrobial resistance patterns of uropathogenic bacteria among pregnant women in developing countries in Africa and Asia from 2005 to 2016.

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