A review on Sero diversity and antimicrobial resistance patterns of Shigella species in Africa, Asia and South America, 2001-2014.

BACKGROUND: Shigella, gram negative bacterium, is responsible for Shigellosis/bacillary dysentery. It is a global concern although it predominates in developing countries. These are Shigella dysenteriae, Shigella flexneri, Shigella boydii and Shigella sonnei. Drug resistance by Shigella species is another headache of the world. Therefore; this study aimed to review distribution of Shigella Serogroups and their antimicrobial patterns carried out in Africa, Asia and South America.
METHODS: A literature search was performed to identify published studies between January 2001 and December 2014. Published studies were identified using an initial search of the MEDLINE/Index Medicus Database, PubMed, Project Management Consultant, Google Scholar, Science Direct, BioMed Central and Index Copernicus.
RESULTS: Shigella flexneri was isolated predominately from seven studies in four African countries and eight studies in five Asian countries. The countries in which eligible studies carried out were Ethiopia, Kenya, Eritrea and Ghana in Africa and Pakistan, Iran, China, Nepal and India in Asia. S. sonnei was isolated predominately from one study in Africa, four in Asia and two South America. The countries in which eligible studies carried out were Ethiopia from Africa, Thailand, Vietnam and Iran from Asia and Chile and Trinidad from South America. S. dysentery was also reported majorly from one eligible study in Egypt and one in Nepal. S. boydii did not score highest prevalence in any one of the eligible studies. Three studies from Africa, five from Asia and one from South America were reviewed for antimicrobial resistance patterns of Shigella Serogroups. In all the regions, Ampicillin developed highly resistance to almost all the Serogroups of Shigella whereas all the strains were sensitive to Ciprofloxacin.
CONCLUSION: The incidence of Shigella Serogroups in the selected three regions is different. The domination of S. flexneri is observed in Africa and Asia although S. sonnei in South America is dominant. Shigella Serogroups are becoming resistance to the commonly prescribed antimicrobial drugs in developing countries.

Background

Shigella, a group of Gram-negative, non-spore forming and rod shaped bacterium, is the causative agent of shigellosis (or bacillary dysentery). Shigella Serogroups are considered to be highly infectious due to their low infectious dose (10–100 organisms) [1]. Shigella is primarily transmitted through the fecal-oral route; therefore, it is still a main global public health threat, particularly in developing countries due to poor sanitation conditions [2].

Shigella bacteria are serologically grouped into four species named as Shigella dysenteriae, Shigella flexneri, Shigella boydii and Shigella sonnei. However Serogroups of Shigella bacteria have similar property of pathogenesis and epidemiologically they have peculiar characteristics. S. flexneri found predominantly in developing world, while S. sonnei is the most common species found in the industrialized countries [3]. The severity of Serogroups of Shigella is different one from the other that S. sonnei and S. flexneri cause mild infection whereas S. boydii and S. dysenteriae cause severe and most serious infection respectively [2]. The infection caused by S. sonnei and S. boydii lasts with short duration and mostly found in industrialized countries. The distribution of Shigella sonnei in the United States of America is 74–79 % [4] and 61 % in Europe [5].

The emerging of multi drug resistance is becoming a serious problem in the treatment of shigellosis. An increment of multidrug resistance to shigellosis is equivalent to a widespread uncontrolled use of antibiotics in developing countries. This emergency of drug resistance calls for the rational use of effective drugs and underscores the need for alternative drugs to treat infections caused by resistant strains [6].

Shigella is more associated with low socio economic status and poor sanitation of under developed countries [2]. Researches were done by different researchers concerning the Serogroups and antimicrobial susceptibility patterns of Shigella in Africa, Asia and South America as a result this study aimed in reviewing the distribution of Serogroups of Shigella and the resistance patterns of antimicrobial drugs which were conducted in the developing countries in the past 14 years.

Methods

Search strategy and selection criteria

A literature search was performed to identify published studies between January 2001 and December 2014. Published studies were identified using an initial search of the MEDLINE/Index Medicus Database, PubMed, PMC, Google Scholar, Science Direct, BioMed Central and Index Copernicus.

The study initially screened all unique publications for eligibility based on the relevancy of the title and then screened the full manuscripts for inclusion and exclusion criteria. The following Keywords were used to search all the published papers from the above engines. These were Prevalence, isolation, Sero diversity, occurrence, epidemiology, Magnitude, burden, estimation, distribution, diversity and antimicrobial resistance patterns of Shigella. Studies conducted before 2001 and researches which concerned only prevalence and antimicrobial susceptibility patterns of Shigella were excluded.

Data extraction

The first author, country, year of publication, setting, sample size, children and all age, sample source, prevalence and distribution of Serogroups of Shigella were extracted from the eligible studies. Ampicillin, Tetracycline, Chloramphenicol, Ciprofloxacin, Cotrimoxazole, Nalidixic acid and Gentamicin resistance patterns of the four Sero groups of Shigella were extracted from the eligible studies.

Studies were included in the review if they fulfill the following criteria:

Isolation and identifying of Shigella from stool samples should be based on standard bacteriological methods and Shigella Serogroups were detected serologically using slide agglutination and antimicrobial resistance patterns of Shigella Serogroups should be based on Clinical Standards Laboratory Institute guidelines using disc diffusion methods.

Full text articles studied in Africa, Asia, and South America and published in English everywhere in the globe were included.

Results

Majority of the reviewed articles were Hospital based studies. About 40 % of the study participants were children under 15 years old. Stool samples were the source of specimens in all the eligible studies. A total of 69,849 stool specimens’ data were collected. Eighteen (72 %) of the eligible studies were published before 2010 and the rest seven were published from 2010 to 2014 (Table 1).

Table 1

Characteristics of appropriate studies and distribution of Serogroups of Shigella reviewed from Africa, Asia and South America from 2001 to 2014

First author	Country	Pub. year	Setting	Age group	Sample sources	Sample size	Shig. Pos. (N)	Shigella Serogroups Pos. N (%)
								A	B	C	D
Mache [8]	Ethiopia	2001	Hosp & HC	Children	Stool	384	77	23 (29.9)	31 (40.3)	15 (19.5)	8 (10.4)
Brooks [9]	Kenya	2003	Laboratory	All ages	Stool	2374	198	80 (40.4)	97 (49)	13 (6.6)	8 (4)
Abu-Elyazeed [10]	Egypt	2004	Surveillance	Children	Stool	696	131	74 (56.5)	30 (22.9)	26 (19.8)	1 (0.8)
Chompook [18]	Thailand	2005	Population	All ages	Stool	6536	146	–	24 (16.4)	–	122 (83.6)
Wang [19]	China	2005	Community	All ages	Stool	10,105	331	–	306 (93)	–	25 (7)
Bhattacharya [20]	Nepal	2005	Hospital	All ages	Stool	1396	53	39 (73.6)	12 (22.6)	2 (3.8)	–
Fulla [21]	Chile	2005	HC	Children	Stool	4080	178	–	77 (43.3)	–	101 (56.7)
Mashouf [22]	Iran	2006	Hospital	Children	Stool	1686	166	56 (33.7)	67 (40.3)	25 (15)	18 (11)
Wilson [23]	Nepal	2006	Hospital	All ages	Stool	770	83	12 (14.5)	56 (67.5)	5 (6.0)	10 (12)
Nguyen [24]	Vietnam	2006	Hospital	All ages	Stool	587	28	–	7 (25)	1 (3.6)	20 (71.4)
Naik [11]	Eritrea	2006	CHL	Children	Stool	2420	84	28 (33.3)	54 (64.3)	–	2 (2.4)
Ghaemi [25]	Iran	2007	Hospital	Children	Stool	634	56	10 (18)	12(22)	3 (5)	31 (55)
Opintan and Newman [12]	Ghana	2007	Hospital	All ages	Stool	594	24	4 (16.7)	17 (70.8)	2 (8.3)	1 (4.2)
Jafari [26]	Iran	2008	Hospital	Children	Stool	1120	157	13 (8)	48 (31)	8 (5)	88 (56)
Orrett [30]	Trinidad	2008	Hospital	All ages	Stool	5187	392	7 (1.8)	75 (19.1)	16 (4.1)	294 (75)
Tiruneh [6]	Ethiopia	2009	Hospital	All ages	Stool	1200	90	9 (10)	65 (72.2)	8 (8.9)	8 (8.9)
Sherchand [15]	Nepal	2009	Hospital	Children	Stool	440	21	14 (66.7)	2 (9.5)	5 (23.8)	–
Zafar [16]	Pakistan	2009	Community	All ages	Stool	8155	394	37 (9)	242 (62)	43 (11)	72 (18)
Pourakbari [17]	Iran	2010	Community	All ages	Stool	15,255	682	34 (5)	327 (48)	14 (2)	307(45)
Xia [27]	China	2011	Hospital	All ages	Stool	3531	467	–	354 (76)	–	113(24)
Nunes [31]	Brazil	2012	Hospital	children	Stool	250	26	–	21 (80.8)	–	5 (19.2)
Khan [28]	Nepal	2013	Hospital	All ages	Stool	507	69	19 (27)	29 (42)	15 (22)	6 (9)
Mengstu [13]	Ethiopia	2014	HC	All ages	Stool	382	17	3 (17.6)	5 (29.4)	3(16.7)	6(35.3)
Mulatu [14]	Ethiopia	2014	Hospital	Children	Stool	158	11	–	11 (100)	–	–
Kumar [29]	India	2014	Hospital	All ages	Stool	1402	146	3 (2.1)	98 (67.1)	8 (5.4)	37 (25.3)
Total						69,849	4027 (5.8)	463 (11.5)	2067 (51.3)	212 (5.3)	1249 (33.2)

A = Shigella dysentery, B = Shigella flexneri, C = Shigella boydii, D = Shigella sonnei

HC health centre, PHL public health laboratories, CHL central health laboratories, Pub publication, Pos positive

Shigella flexneri was isolated predominately from Ethiopia [7, 8, 14], Kenya [9, 13], Eritrea [11], Ghana [12], Pakistan [16], Iran [17, 22], China [19, 27], Nepal [23, 28], India [29] and Brazil [31] (Table 1). S. sonnei was also isolated predominately from Ethiopia [13], Thailand [18], Vietnam [24] and Iran [25, 26], Chile [21] and Trinidad [30]. S. dysentery was also reported majorly from Egypt [10] and Nepal [15]. S. boydii did not score highest prevalence in any one of the eligible studies (Table 1).

Shigella sonnei was not isolated from studies conducted in Ethiopia [14] and Nepal [20]. S. dysentery was not isolated from the studies conducted in Ethiopia [14], Thailand [18], China [19, 27], Chile [21], Brazil [31], and Vietnam [24]. S. boydii was not also isolated from the studies conducted in Ethiopia [14], Eritrea [11], Thailand [18], China [19, 27], Chile [21] and Brazil [31] (Table 1).

Nine studies were eligible for antimicrobial susceptibility testing [AST] of Shigella Serogroups. Those are three from Africa, five from Asia and one from South America. In all the regions, Ampicillin developed highly resistance to almost all the Serogroups of Shigella whereas all the strains were sensitive to Ciprofloxacin. Hundred percent of isolates revealed by Orrette in South America were resistance for Ampicillin but 100 % sensitive to Tetracycline, Chloramphenicol, Ciprofloxacin and Cotrimoxazole (Table 2). In most of the studies observed in Africa (Table 3) and Asia (Table 4), Serogroups of Shigella were developed resistance to Tetracycline, Chloramphencol and Cotrimoxazole.

Table 2

Review on antimicrobial resistance patterns of Serogroups of Shigella conducted in South America

Author	Serogroup	Resistance patterns, N (%)
		AMP	T	C	CIP	NA	SXT	GM
Orrett [30]	S. dysentery	7 (100)	0 (0.0)	0 (0.0)	0 (0.0)	–	0 (0.0)	0 (0.0)
	S. flexneri	36 (46)	9 (12)	0 (0.0)	0 (0.0)	–	16 (21)	0 (0.0)
	S. boydii	10 (63)	6 (38)	3 (3.9)	0 (0.0)	–	3 (19)	0 (0.0)
	S. sonnei	27 (9)	106 (36)	4 (1.4)	2 (0.7)	–	97 (33)	4 (1.4)

Table 3

Review on antimicrobial resistance patterns of Serogroups of Shigella conducted in Africa

Authors	Serogroups	Resistance patterns, N(%)
		AMP	T	C	CIP	NA	SXT	GM
Mache [8]	S. dysentery	17 (73.9)	15 (64.2)	12 (52.2)	–	11 (8.7)	9 (39.1)	0 (0.0)
	S. flexneri	22 (71)	20 (64.5)	13 (41.9)	–	3 (9.7)	9 (29)	1 (3.2)
	S. boydii	10 (66.7)	8 (53.3)	4 (25)	–	0 (0.0)	5 (33.3)	0 (0.0)
	S. sonnei	5 (62.5)	6 (75)	2 (25)	–	0 (0.0)	2 (25)	0 (0.0)
Tiruneh [6]	S. dysentery	8 (89)	7 (77.8)	1 (11)	0 (0.0)	0 (0.0)	7 (77.8)	1 (11)
	S. flexneri	54 (83)	62 (95.4)	45 (69)	2 (31)	0 (0.0)	59 (90.8)	7 (10.8)
	S. boydii	4 (50)	7 (87.5)	2 (25)	0 (0.0)	0 (0.0)	4 (50)	2 (25)
	S. sonnei	3 (37.5)	8 (100)	2 (25)	0 (0.0)	0 (0.0)	6 (75)	1 (12.5)
Naik [11]	S. dysentery	19 (95)	–	18 (90)	0 (0.0)	–	0 (0.0)	–
	S. flexneri	42 (78)	–	34 (67)	0 (0.0)	–	3 (6)	–

Table 4

Review on antimicrobial resistance patterns of Serogroups of Shigella conducted in Asia

Author	Serogroups	Resistance patterns, N (%)
		AMP	T	C	CIP	NA	SXT	GM
Wang [19]	S. flexneri	292 (95.4)	–	–	18 (5.9)	305 (99.7)	206 (67.3)	7 (2.3)
	S. sonnei	2 (8)	–	–	0 (0.0)	24 (96)	24 (96)	0 (0.0)
Bhattacharya [20]	S. dysentery	32 (82.1)	–	–	13 (33.3)	33 (84.6)	35 (89.5)	–
	S. flexneri	12 (100)	–	–	2 (16.7)	4 (33.3)	11 (91.7)	–
	S. boydii	2 (100)	–	–	1 (50)	0 (0.0)	1 (50)	–
Mashouf [22]	S. dysentery	54 (96.4)	50 (89.2)	52 (92.8)	3 (3.5)	48 (85.7)	52 (92.8)	–
	S. flexneri	63 (94)	61 (91.1)	61 (91.1)	0 (0.0)	3 (44.7)	59 (88.1)	–
	S. boydii	17 (68)	13 (52)	21 (84)	0 (0.0)	0 (0.0)	15 (60)	–
	S. sonnei	15 (83.3)	15 (83.3)	17 (94.4)	0 (0.0)	7 (38.8)	14 (77.7)	–
Wilson [23]	S. dysentery	6 (75)	7 (87.5)	5 (62.5)	1 (12.5)	5 (62.5)	51 (100)	6 (75)
	S. flexneri	33 (64.7)	49 (96)	23 (45.1)	1 (2)	16 (31.4)	8 (100)	34 (66.7)
Jafari [26]	S. dysentery	3 (37.5)	8 (100)	0 (0.0)	0 (0.0)	0 (0.0)	7 (87.5)	0 (0.0)
	S. flexneri	23 (47.9)	46 (95.8)	23 (47.9)	0 (0.0)	0 (0.0)	42 (87.5)	2 (4)
	S. boydii	5 (38.4)	11 (84.6)	1 (7.6)	0 (0.0)	2 (15.4)	10 (76.9)	0 (0.0)

Discussion

This review addressed the status of the distribution of the Serogroups of Shigella and antimicrobial resistance patterns conducted in 25 eligible studies reviewed from Africa, Asia and South America.

Shigella flexneri was revealed 100 % from all the eligible studies reviewed in eight African, fourteen Asian and three South American countries. S. dysentery was reviewed from 87, 72 and 33 % of the eight African, fourteen Asian and three South American countries respectively. S. boydii was reviewed from 75, 79 and 33 % of the studies carried out in eight Africa, fourteen Asia and three South America respectively. S. sonnei was also reviewed in 87, 86 and 100 % of the studies conducted in eight Africa, fourteen Asia and three South American countries respectively (Table 1).

Of the total 69,849 stool sample data collected from the 25 eligible studies published from 2001 to 2014, 4027 Shigella bacteria were isolated which is 5.8 %. Above 50 % of the proportion of Shigella Serogroups was covered by S. flexneri which was followed by S. sonnei (33 %). S. boydii was contributed five percent of the four Serogroups of Shigella (Table 1).

The pooled mean resistance of S. dysentriae to Ampicillin, Tetracycline, Cotrimoxazole, Chloramphenicol, Nalidix acid, Gentamicin and Ciprofloxacin were 72.1, 69.4, 60, 44, 40, 17 and 7 % respectively. The pooled mean resistance of S. flexneri to Tetracycline, Ampicillin, Nalidix acid, Cotrimoxazole, Chloramphenicol, Gentamicin and Ciprofloxacin were 75.8, 75.6, 74.5, 72.7, 51.7, 14.5 and 7 % respectively. The pooled mean resistance of S. boydii to Ampicillin, Tetracycline, Cotrimoxazole, Chloramphenicol, Ciprofloxacin, Gentamicin and Nalidix acid were 64, 63, 48, 29, 10, 6 and 3 % respectively. The pooled mean resistance of S. sonnei to Tetracycline, Cotrimoxazole, Nalidix acid, Ampicillin, Chloramphenicol, Gentamicin and Ciprofloxacin were 79, 71, 54, 47, 35, 16 and 0 % respectively (Table 5).

Table 5

Pooled range and mean of antimicrobial resistance patterns of Shigella Serogroups

Serogroups of Shigella	Resistance (%)
	AMP		T		C		CIP		NA		SXT		GM
	PR	PM	PR	PM	PR	PM	PR	PM	PR	PM	PR	PM	PR	PM
S. dysentery	37.5−100	72.1	0−100	69.4	0−92.8	44.1	0−33.3	7	0−85.7	40.3	0−100	60.8	0−75	17.2
No. of studies	8		6		7		7		6		8		5
S. flexneri	46−100	75.6	12−95.8	75.8	0−91.1	51.7	0−31	7	0−99.7	74.1	6−100	72.7	0−66.7	14.5
No. of studies	9		6		7		8		7		9		6
S. boydii	38.4−100	64.4	38−87.5	63.1	3.9−84	29.1	0−50	10	0−15.4	3.1	19−76.9	48.2	0−25	6.3
No. of studies	6		5		5		5		5		6		4
S. sonnei	8−83.3	46.9	36−100	79.4	1.4−94.4	35.4	0−0.7	0.12	0−96	54.8	25−100	71.9	0−12.5	16.6
No. of studies	7		6		6		6		6		6		6

AMP Ampicillin, T Tetracycline, C Chloramphenicol, CIP Ciprofloxacin, NA Nalidixic acid, SXT sulphamethoxazole trimethoprim/Cotrimoxazole, GM gentamicin, PR pooled range, PM pooled mean, No Number

Above 50 % of all Serogroups of Shigella developed resistance to Ampicillin, Tetracycline, Cotrimoxazole and Chloramphenicol which are the commonly prescribed antimicrobial drugs.

Conclusions

The incidence of Shigella Serogroups in the selected three regions is different. The domination of S. flexneri is observed in Africa and Asia although S. sonnei, the most dominant in South America, is predominately isolated in one study in Ethiopia. This may give clue to the scientific world about the migration and movement of strains from one region to the other region. Shigella Serogroups are becoming resistance to the commonly prescribed antimicrobial drugs in developing countries.