Serological structure and antimicrobial susceptibility of Salmonella isolated from human and food items in Southern provinces of Viet Nam


Cite item

Abstract

The article suggests currently relevant data on the serogroup structure and antibiotic susceptibility of Salmonella strains isolated in the southern provinces of the Socialist Republic of Vietnam. The study included 189 Salmonella strains, isolated from feces of human with acute diarrhea (86 strains) and pork samples (103 strains).   Serological identification to O-group was fulfilled by slide agglutination with O- and H- antisera and multiply PCR to detect H phase-1 and phase-2. Antimicrobial susceptibility testing was made by disk-diffusion method according EUCAST (version 2019). Strains isolated from human predominantly belonged to O4 group (69,8%), percentage of other serogroups fluctuated from  1,2% (rare group O16) to 11,6 % (O9). About a half of strains (44,7%) isolated from pork turned to belong to О3,10 serogroup (versus 7,0 % of strains from human beings). Such serogroups as О7, О4 and О8 happened to be less frequent (22,3%, 14,6% and 13,6%, respectively). The singular strains belonged to serogroups О9, О13 and О18. Whatever the isolation source about 80% Salmonella strains turned to be resistant to antibiotics from different antimicrobial groups (not to carbapenems): 67,0% were resistant to tetracycline, about a half of strains (54,0, 47,1 and 46,6%)  - to pefloxacin, ampicillin and chloramphenicol, up to 40% - to trimetoprime/sulfametoxazole and nalidixic acid.   The proportion of strains resistant to ceftriaxone and gentamycin happened to look obviously bigger in those of human origin versus those of pork origin: 12,8% vs.1,0% and 30,2 vs 1,9%, respectively. More over, 62,8% strains of human origin and 43,7% - from pork demonstrated multidrug resistance (to 3 and more antimicrobial groups). The simultaneous resistance to 6 antimicrobial groups was detected much more frequently in Salmonella strains isolated from human beings than in those isolated from pork samples (15,1% vs. 1,0%, respectively) as well.  Multidrug resistance demonstrated strains of different serovars, predominantly S. Typhimurium (36,4%). Predominant multidrug resistance phenotype AMP, TE, QN, C, SXT (30,3%) was revealed in serovars S. Typhimurium, S. Bredeney, S. Corvallis, S. Give, S. London, S. Rissen, S. Meleagridis. So, Salmonella strains having been isolated in southern provinces of Viet Nam demonstrated the resistance to fluoroquinolones and cephalosporins that given the simultaneous loss of susceptibility to the “old” antimicrobials (ampicillin, chloramphenicol, trimethoprim/ sulfametoxazole) crucially restricts the list of medicines potent to treat complicated salmonellosis cases.

Full Text

Serological structure and antimicrobial susceptibility of Salmonella isolated from human and food items in Southern provinces of Viet Nam

Introduction. According to the WHO data annually up to 1-1,7 billion cases of acute diarrhea are notified as leading infectious diseases following only acute respiratory tract infections. All over the world acute diarrhea accounts for more than 500 thousands deaths in children so far taking the second place in the mortality rate in those younger than 5 years old (https://www.who.int/news-room/fact-sheets/detail/diarrhoeal-disease). In the Russian Federation as well as in European countries the causative agents in up to 70% of acute diarrhea cases (especially food-borne outbreaks) turn to be Rota- and Norwalk viruses. The mostly spread bacterial agents of acute diarrhea cases are Salmonella and Campylobacter [8, 12].    Salmonellosis is known to have different clinical patterns predominantly resulted from digestive tract affecting but potent to spread beyond it with development of toxic and dehydration syndromes of various severity. Salmonella is potent to cause the food-born infection with small and large outbreaks [12]. 

In Viet Nam the incidence of acute diarrhea in infants is 271 per 1000 children. In more than 70% of cases there were detected such viruses as Rota (in 50,0% of samples) and Norwalk (24,0%) whereas among bacterial agents there were found Campylobacter (20,0%), Salmonella (18,0%) and Shigella (16,0%) [9, 15].  In 2009 – 2010 in Ho Chi Minh City non-typhoid Salmonella were detected in 5,4% of acute diarrhea cases in children under 5 years old [24]. Compared to Russian Federation where serovar S. Enteritidis accounts for more than 80,0% of cases and dominates for many years, in Viet Nam the serogroup spectrum of Salmonella isolated both from humans and food is more various. For example, the examination of adult hospitalized cases in 2008-2013 revealed S.Enteritidis and S.Typhimurium in 48,0 and 26,0% respectively [20]. Salmonella having been isolated from food unit healthy staff in different years belonged to different serogroups and serovars. For example, up to 30,0% of Salmonella isolated in 2011 belonged to serogroup E (32,7%), serovar S.Paratyphi B (29,1%) and serogroups C and B (18,2% and 10,9%, respectively). Strains isolated in 2012 belonged to S.Enteritidis (30,0%), serogroup B (17,5%), serogroups C and D (beyond S.Enteritidis) (12,5%), serogroups A and E (10,0%). In 2013 strains of serogroups B, E and C dominated (55,6%, 22,2% and 16,7%, respectively) [23].

 In Viet Nam there were conducted many examinations of samples taken from food producing animals, poultry, prawns, fishes and food items as the potent sources and vehicles (transmitters) of Salmonella to human. The high levels of contamination with Salmonella (belonging to 28 - 53 serogroups) were demonstrated [16, 17, 19, 22, 25, 26, 27].

The examination of pigs and chickens revealed that contaminated samples were found in 50,0% of poultry farms and in 70,0% of pig breeding farms. The isolates belonged to 28 serovars with leading of S.Weltevreden (up to 20,0%), S.Typhimurium (12,0%) and Salmonella 4:12: i:- (11%) [17, 25].  S.Weltevreden was detected in every forth shrimps farms in the Mekong delta covering three Viet Nam provinces [19].  Some studies carried out in 2004 - 2016 in provinces of Southern Viet Nam showed that the prevalence of Salmonella isolated from pigs increased significantly from 5,2% to 64,4% of samples. In Vinh Long, Salmonella was isolated from sick pigs and healthy pigs in 61,5% and 8,8%,  respectively; in Dong Thap, the percentage of Salmonella contaminated samples turned to be 64,7% in chickens and 91,3% in pigs [16, 27].

Antimicrobial therapy is usually prescribed to patients with systemic (invasive) salmonellosis, middle or severe course (fever longer than 48 hours, e.g), age less than 6 months or more than 50 years, immune deficiency or severe concurrent diseases availability. The empiric therapy suggests prescribing fluoroquinolones, extended spectrum cephalosporins, trimethoprim/sulfametoxazole [1, 6, 10, 21]. However, Salmonella  isolated from humans,  animals and food items demonstrate up going  antimicrobial resistance in many countries [13]. In Russian Federation the percentage of such Salmonella strains in those isolated from human beings, animals and food items is up to 50-70,0% [2, 3, 4, 5, 7].

The most Salmonella strains (about 60,0%) examined by different researchers in 2004-2017 in Viet Nam turned to be resistant to such antibiotics as: ampicillin (more than 40,0% of strains), tetracyclin (more than 50,0%), trimethoprim/sulfametoxazole (up to 60,0%), chloramphenicol (up to 50,0%) and ciprofloxacin (more than 30,0% of strains) [16-19, 22, 23, 25-28]. According to different researchers’ data from 17 to 52,2% of strains had multidrug resistance. S.Kentucky ST198 was considered being  the most frequently multidrug-resistant serovar  with high rate of resistance to β-lactams and quinolones.

Noticeably, there was one strain (isolated from pork) exhibiting colistin resistance. It’s the first colistin-resistant Salmonella found in meat in Vietnam [18, 28].

Some data point that the percentage of Salmonella strains producing ESBL (TEM and CTX genetic families) was equal to 5, 3%. Predominantly strains belonged to serogroup В with S. Рaratyphi B included [23].

The study objective was to characterize the serogroup structure and to evaluate antimicrobial susceptibility of Salmonella isolated from human and food samples in South Viet Nam. 

Materials and methods. The study was fulfilled in frame of scientific cooperation between Saint-Petersburg Pasteur Institute and Pasteur Institute in Ho Chi Minh City. The studied  were 189 Salmonella strains, isolated in South Viet Nam:  86 strains - from feces of humans with acute diarrhea and 103 - from pork samples.  

 Salmonella serological identification to O-group was fulfilled firstly by slide agglutination with O-group antisera (produced by Saint-Petersburg Scientific Research Institute of Vaccine and Serum, Russia).  Then phase-1 and phase-2 were detected by multiply PCR [11, 14] with subsequent confirmation by slide agglutination with phase-1 and phase-2 antisera.

 Antimicrobial susceptibility testing was made according EUCAST recommendation (version 2019, https://www.eucast.org/ast_of_bacteria/) by disk-diffusion method with Mueller-Hinton agar and antibiotic disks (Oxoid).

The tested antimicrobials belonged to different antibiotic classes: b-lactames (ampicillin, ceftazidime, ceftriaxone, meropenem), quinolones (nalidixic acid, pefloxacin), tetracycline, phenicols (chloramphenicol), trimethoprim/ sulfametoxazole, polimyxines (colistin) and aminoglycozides (gentamycin, amikacin).

The results were interpreted according EUCAST criteria, version 2019 (https://www.eucast.org/fileadmin/ src/media/PDFs/EUCAST_files/Breakpoint_tables/v_9.0_Breakpoint_Tables.pdf).

For the category “resistant” to fluoroquinolones there were used the following breakpoints:  inhibition zone of pefloxacin < 24 mm, nalidixic acid < 16 mm. 

Results.   Salmonella strains belonged to several O-groups:  О4 (В) – 75 strains (39,7%), О3,10 (E) - 52 strains (27,5%), О7 (С1) – 30 (15,9%), О8 (С2) - 16 (8,5%), О9 (D) – 12 (6,3%) and to rare groups - 4 strains (2,1%) (Table 1, Salmonella serovars isolated from human and pork in Southern provinces of Viet Nam (number of strains, proportion, 95%  confidential interval).

Some differences in serogroup spectrum revealed in strains isolated from human beings versus those from pork items are presented in Picture 1 (Serogroup structure of Salmonella isolated from human and pork in Southern provinces of Viet Nam).

Strains isolated from human beings predominantly belonged to O4 group (69,8 %). Percentage of other serogroup strains fluctuated from  1,2% (rare groups) to 11,6 % (O9). About a half of strains isolated from pork (44,7%) turned to belong to О3,10 serogroup (versus 7,0% in strains from human beings),  such serogroups as О7,  О4 and О8 happened to be present less frequently (22,3%, 14,6% and 13,6%,  respectively). The singular strains from pork belonged to serogroups О9,  О13 and О18. It’s worth mentioning the obvious difference in proportions of serogroup O4 and O9 in strains isolated from pork (14,6% and 1,9%, respectively) versus those from human beings (69,7% and 11,6%, respectively).

The studied Salmonella strains turned to be resistant (about 80%) to antibiotics from different antimicrobial groups and more than a half of strains (52,4%) had multidrug resistance to 3 and more antimicrobial groups (Table 2, Antimicrobial susceptibility and resistance of Salmonella isolated from different sources in Southern provinces of Viet Nam). There was no significant difference in proportion of resistant strains in those of human and pork origin to the majority of tested antimicrobials.

Up to 70,0% of strains were resistant to tetracycline, about a half of strains - to pefloxacin, ampicillin and chloramphenicol, about 40% - to trimetoprime/sulfametoxazole and nalidixic acid. However, it’s worth mentioning that in pork strains no one performed resistance to amoxicillin/clavulanic acid, ceftazidim and amikacin. The proportion of strains resistant to ceftriaxone and gentamycin in those of human origin versus those of pork origin happened to look obviously bigger (12,8% vs.1,0%; 30,2 vs 1,9%, respectively; the differences are statistically significant) (Table 2). Noteworthy is the fact that 16,4% of Salmonella strains were resistant to pefloxacin, but susceptible to nalidixic acid, that indicates transferable resistance mechanisms to fluoroquinolones. All tested Salmonella strains were susceptible to carbapenems.

Multidrug resistant Salmonella strains happened to be revealed in those isolated both from human beings and pork samples (62,8% and 43,7%, respectively) (Table 3, MDR-phenotypes  of Salmonella isolated from different sources in Southern provinces of Viet Nam). However, the simultaneous resistance to 6 antimicrobials was detected much more frequently in Salmonella strains isolated from human beings than in those isolated from pork samples (15,1% vs. 1,0%, respectively).

In general MDR-resistance was detected in 52,4% (n=99) of Salmonella belonging to different serovars, but the serovar S. Typhimurium performed the biggest proportion of MDR-resistant strains  (36,4%, n=36).

The predominant resistance phenotypes were AMP,TE,QN,C,SXT detected in 30,3% of MDR-strains belonging to serovars S. Typhimurium, S. Bredeney, S. Corvallis, S. Give, S. London, S. Rissen, S. Meleagridis. The most of these strains were isolated from pork samples.

Discussion. Our research results suggest that in southern provinces of  Viet Nam Salmonella strains isolated from people predominantly belong to O4 serogroup (about 70,0%).  Proportion of strains belonging to other serogroups (13-15 serovars) turmed to be  much  lower and fluctuated from 1,2 % to 11,6%.

The spectrum of Salmonella strains isolated in Viet Nam differs significantly from that in Russian Federation where more than 70,0% of strains isolated from humans belong to serogroup O9 (S.Enteritidis) [8]. The difference is most probably resulted from Vietnamese tradition to take sea food which is used to being contaminated by Salmonella strains of broad spectrum serovars (such as S. Weltevreden, S. Senftenberg, S. Rissen, S. Lexington, S. Saintpaul, S. Newport, S. Albany, S. Anatum and others). 

About a half of strains isolated from pork belonged to О3,10 serogroup whereas totally there were isolated Salmonella of 35 serovars.

Our data are consistent with results of other studies. So, the examination of raw meat samples taken in markets and supermarkets in different cities and provinces of Viet Nam revealed the high level of contamination with Salmonella: beef - 58,3% of samples, pork – up to 70,0%, chicken meat – up to 65,0%, cultured shrimps – up to 50,0%, cultured fish – 37,0% of samples. The serovar spectrum varied from 14 to 53 ones: S.Weltevreden, S.Rissen, S.Anatum, S.London, S.Derby, S.Infantis,  S.Typhimurium,  S.Reading, S.Agona, S.Dabou, S.Albany, S.Emek, S.Corvallis [22, 26].

The difference in serogroup spectrum of strains isolated in Viet Nam from human and pork samples also probably needs explaning by gastronomic (food cooking) traditions in Vietmamese peple society where sea food, poultry meat and eggs consider being the main factor to transmit Salmonella to human beings.

Our research results suggest that more than 70,0% of Salmonella strains in those isolated both from human and pork samples in Viet Nam turned to be resistant to antimicrobials. Moreover, every second strain performed multidrug resistant phenotype. The research revealed quite high percentage of strains resistant to tetracyclin (67,2%), fluoroquinolones (54,0%), ampicillin (47,1%), trimethoprim/sulfametoxazol (42,3%), chloramphenicol (46,6%), there were found strains resistant to cephalosporins of 3-4 generations (6,4%). Our results don’t fight with those earlier carried out in Viet Nam and published [16-19, 22, 23, 25-28]. The similar research carried out in Russian Federation suggested that more than 60% of local Salmonella strains turned to be resistant to quinolones, not more than 10,0% - to “old” antimicrobials (tetracyclin, chloramphenicol, ampicillin), less than 2,0% - to cephalosporins of 3 - 4 generations. The percentage of multidrug resistant strains happened to be much lower (about 15,0%) versus that in Vietnamese strains [4].

In February 2017 WHO published the list of antibiotic-resistant “priority pathogens” that contains 12 bacteria species as the most threatening to human health [29].  Salmonella resistant to fluoroquinolones (up to recently having been considered as the first line medicines for salmonellosis treatment) now are in highly prioritized group together with such agents as Enterococcus spp., Staphylococcus aureus, Neisseria gonorrhoeae, Helicobacter pylori и Campylobacter spp. In our study the half of isolated Salmonella belonged to this highly prioritized group of resistant bacteria.

The appearance of Salmonella producing extended spectrum ß-lactamase (ESBL) makes the empiric usage of extended spectrum cefalosporins (ESC) restricted for salmonellosis treatment. In conformity with published data in the Russian Federation the percentage of such strains in serovars S. Virchow, S. Enteritidis, S. Typhimurium, S. Newport is 0,2–10,0%, there have been detected ESBL belonging to such genetic groups as СТХ-М and AmpC cephalosporinases [4, 5]. In our study cephalosporin-resistant strains (6,4%) were mainly isolated from humans and belonged to S.Typhimurium (group O4) and some strains of group O3,10.

The resistance to fluoroquinolones and cephalosporins observed simultaneously with the loss of Salmonella susceptibility to the “old” antimicrobials (ampicillin, chloramphenicol, trimethoprim/ sulfametoxazole) crucially restrict the list of medicines potent to treat complicated salmonellosis. The antimicrobial usage when breeding of farm livestock may account for appearance of resistant Salmonella strains and so far, their spread to human beings. So, the resistance restriction requires preventing of resistance forming in strains circulating in farm livestock.

Table 1

Salmonella serovars isolated from human and pork in Southern provinces of Viet Nam (number of strains, proportion, 95% confidential  interval)

O-group

Serovar

Number of strains isolated from

human

pork

Total

4

 

S. Typhimurium

40

5

45

S. Stanley

12

0

12

S. Southampton

2

1

3

S. Saintpaul

2

0

2

S. Remo

1

0

1

S. Heidelberg

1

0

1

S. Derby

0

1

1

S. Vuadens

0

1

1

S. Bredeney

0

3

3

Not identified

2

4

6

Total O4

60

69,8%*

95%CI 58,9-79,2

15

14,6%*

95%CI 8,4-22,9

 

75

39,7%

95%CI 32,7-47,0

3,10

S. Weltevreden

1

1

2

S. Anatum

0

8

8

S. Give

0

13

13

S. Bloomsbury

0

4

4

S. Epicrates

0

1

1

S. Lexington

0

5

5

S. London

0

4

4

S. Meleagridis

0

1

1

Not identified

5

9

14

Total O3,10

6

7,0%*

95%CI 2,6-14,6

46

44,7%*

95%CI 34,9-54,8

52

27,5%

95%CI 21,3-34,5

7

S. Choleraesuis

2

0

2

S. Rissen

1

4

5

S. Larochelle

1

0

1

S. Eingedi

0

1

1

S. Gatow

0

1

1

S. Bonn

0

2

2

S. Afula

0

2

2

S. Lockleaze

0

1

1

S. Djugu

0

3

3

S. Virchow

0

1

1

S. Nola

0

1

1

Not identified

3

7

10

Total O7

7

8,1%

 95%CI 3,3-16,0

23

22,3%

95%CI 14,7-31,6

30

15,8%

95%CI 11,0-21,9

8

S. Newport

1

1

2

S. Corvalis

0

7

7

S. Pakistan

0

1

1

S. Bellevue

0

1

1

Not identified

1

4

5

Total O8

2

 2,3%

95%CI 0,3-8,2

14

13,6%

95%CI 7,6-21,7

16

8,5%

95%CI 4,9-13,4

9

S. Enteritidis

8

0

8

S. Wangata

0

1

1

Not identified

2

1

3

Total O9

10

11,6%

 95%CI 5,7-20,4

2

1,9%

95%CI 0,2-6,8

12

6,4%

95%CI 3,3-10,8

13

S. Myrria

0

1

1

16

S. Hvittingfoss

1

0

1

18

S. Cotia

0

1

1

 

Salmonella II

0

1

1

 

Total other groups

1

1,2%

95%CI 0,03-6,3

3

2,9%

95%CI 0,6-8,3

4

2,1%

95%CI 0,6-5,3

TOTAL

86

103

189

* the differences are statistically significant

Table 2.

Antimicrobial susceptibility and resistance of Salmonella isolated from different sources in Southern provinces of Viet Nam

Resistance phenotype

Isolated from

Total (n=189)

human (n=86)

pork (n=103)

n

%

95% CI

n

%

95% CI

n

%

95% CI

Susceptible

13

15,1

8,3-24,5 

28

27,2

18,9-36,8 

41

21,7

16,0-28,3 

Resistant to 1

 and more antibiotics

73

84,9

75,5-91,7 

75

72,8

63,2-81,1 

148

78,3

71,7-84,0 

Resistant to:

- ampicillin

50

58,1

47,0-68,7 

39

37,9

 28,5-48,0

89

47,1

39,8-54,5 

- amoxicillin/clavulanic acid

2

2,3

0,3-8,2 

0

0,0

0-2,9 

2

1,1

0,1-3,8

- ceftriaxone

11

12,8**

 6,6-21,7

1

1,0**

0,02-5,3 

12

6,4

3,3-10,8 

- ceftazidim

4

4,7

1,3-11,5 

0

0,0

0-2,9 

4

2,1

0,6-5,3 

- pefloxacin

48

55,8

44,7-66,5 

54

52,4

 42,4-62,4

102

54,0

46,6-61,2 

- nalidixic acid

35

40,7

 30,2-51,8

36

35,0

25,8-45,0 

71

37,6

30,6-44,9 

- trimethoprim/

sulfametoxazole

38

44,2

33,5-55,3 

42

40,8

 31,2-50,9

80

42,3

 35,2-49,7

- chloramphenicol

49

57,0

45,9-67,6 

39

37,9

 28,5-48,0

88

46,6

39,3-53,9 

- tetracycline

58

67,4

 56,5-77,2

69

67,0

 57,0-75,9

127

67,2

 60,0-73,8

- gentamycin

26

30,2**

20,8-41,1 

2

1,9**

0,2-6,8 

28

14,8

10,1-20,7 

- amikacin

1

1,2

 0,03-6,3

0

0,0

0-2,9 

1

0,5

0,01-2,9 

Resistant to 3 and more groups (MDR*):

54

62,8

 51,7-73,0

45

43,7

33,9-53,8 

99

52,4

45,0-59,7 

- 3 groups

7

8,1

3,3-16,1

5

4,9

1,6-11,0

12

6,3

3,3-10,8

- 4 groups

13

15,1

8,3-24,5

17

16,5

9,9-25,1

30

15,9

11,0-21,9

- 5 groups

18

20,9

12,9-31,1

22

21,4

13,9-30,5

40

21,2

15,6-27,7

- 6 groups

13

15,1**

8,3-24,5

1

1,0**

0,02-5,3

14

7,4

4,1-12,1

- 7 groups

3

3,5

0,7-9,9

0

0,0

0-2,9

3

1,6

0,3-4,6

           

*MDR – multidrug resistant

** the differences are statistically significant

 

Table 3. 

MDR-phenotypes  of Salmonella isolated from different sources

in Southern provinces of Viet Nam

Resistance phenotypes

 (antibiotic groups1)

Strains isolated from

Total

human

pork

n

serovars

n

serovars

n

Resistant to 3 groups

7

 

5

 

12

TE, QN, SXT

0

-

2

Nhóm O:7

S. Djugu

2

TE, QN, C

1

S. Typhimurium

0

-

1

TE, C, SXT

0

-

1

S. Anatum

1

TE, AMG, QN

1

S. Stanley

0

-

1

AMP, TE, SXT

0

-

1

S. Rissen

1

AMP, TE, QN

5

group O:3,10

group O:8

S. Typhimurium

1

Nhóm O:9

6

Resistant to 4 groups

13

 

17

 

30

TE, QN, C, SXT

4

S. Newport

S. Saintpaul

S. Stanley

S. Typhimurium

6

Nhóm O:4

Nhóm O:7

S. Anatum

10

TE, AMG, QN, C

1

S. Typhimurium

0

-

1

AMP, TE, QN, SXT

0

-

3

group O:4

S. Bonn

3

AMP, TE, QN, C

1

S. Typhimurium

2

S. Derby

S. Gatow

3

AMP, TE, C, SXT

3

group O:7

S. Stanley

4

group O:3,10

S. Eingedi

S. Epicrates

S. Myrria

7

AMP, TE, AMG, C

1

S. Typhimurium

0

-

1

AMP, QN, C, SXT

2

S. Saintpaul

S. Typhimurium

1

group O:3,10

3

AMP, C3-4, QN, C

1

group O:3,10

0

-

1

AMP, AMG, QN, C

0

-

1

S.Typhimurium

1

Resistant to 5 groups

18

 

22

 

40

TE, AMG, QN, C, SXT

2

S. Typhimurium

0

-

2

AMP, TE, QN, C, SXT

8

group O:3,10

S. Heidelberg

S. Rissen

S. Stanley

S. Typhimurium

22

group O:7

S. Bredeney

S. Corvalis

S. Give

S. London

S. Meleagridis

S. Rissen

S. Typhimurium

30

AMP, TE, AMG, QN, C

1

S. Typhimurium

0

-

1

AMP, TE, AMG, C, SXT

2

S. Typhimurium

0

-

2

AMP, C3-4, TE, QN, C

4

S. Choleraesuis

S. Typhimurium

0

-

4

AMP, AMG, QN, C, SXT

1

group O:7

0

-

1

Resistant to 6 groups

13

 

1

 

14

AMP, TE, AMG, QN, C, SXT

12

S. Enteritidis

S. Larochelle

S. Typhimurium

1

S. Give

13

AMP, C3-4, TE, AMG, QN, C

1

S. Typhimurium

0

-

1

Resistant to 7 groups

3

 

0

 

3

AMP,  C3-4,  QN,   TE,   C,  AMG,  SXT

3

group O:9

S. Typhimurium

0

-

3

TOTAL MDR-strains

54

 

45

-

99

MDR- multidrug resistant

Antibiotic groups:

AMP – aminopenicillins (ampicillin) 

C3-4 –  cephalosporins of 3-4 generations (ceftriaxone, ceftazidime)

CARB – carbapenems (meropenem) 

QN – quinolones (nalidixic acid, pefloxacin)

AMG – aminoglycozides (gentamycin, amikacin) 

TE – tetracyclines (tetracycline) 

 

Picture 1.  Serogroup structure of Salmonella isolated from human and pork in Southern provinces of Viet Nam.

C – phenicols (chloramphenicol) 

SXT – trimethoprim/sulfametoxazole 

 

×

About the authors

Svetlana A. Egorova

Saint-Petersburg Pasteur Institute of the Federal Service on Customers’ Rights Protection and Human Well-being Surveillance

Author for correspondence.
Email: egorova72@mail.ru
ORCID iD: 0000-0002-7589-0234
SPIN-code: 4000-4122
Scopus Author ID: 36937138200

PhD (Medicine), Doctor of Science (Medicine), senior researcher of the laboratory of enteric infections

Russian Federation, 14, Mira street, 197101 Saint-Petersburg

Truong Quang Nguyen

Pasteur Institute in Ho Chi Minh City

Email: truongou@gmail.com

MSc (Biotechnology), researcher, Laboratory of enteric infections, Microbiology and Immunology Department

Viet Nam

Lidiia A. Kaftyreva

Saint-Petersburg Pasteur Institute of the Federal Service on Customers’ Rights Protection and Human Well-being Surveillance; State Educational Institution of the Higher Professional Education "North-Western state medical University n.a. I.I. Mechnikov" of the Ministry of health of the Russian Federation

Email: kaflidia@mail.ru
ORCID iD: 0000-0003-0989-1404
SPIN-code: 6721-7873
Scopus Author ID: 6602939287
ResearcherId: K-2708-2014

PhD (Medicine),  Doctor of Science (Medicine),

head of the laboratory; Laboratory of enteric infections of Saint-Petersburg Pasteur Institute; 

professor of the medical microbiology faculty,  "North-Western state medical University n.a. I.I. Mechnikov"

Russian Federation, 14, Mira street, Saint-Petersburg, 197101; 41, Kirochnaya ul., Saint-Petersburg, 191015

Elena A. Kozhukhova

State Educational Institution of the Higher Professional Education “Pavlov University in Saint-Petersburg”

Email: elko35@gmail.com

PhD (Medicine),

senior researcher

Russian Federation, L'va Tolstogo str. 6-8 Saint Petersburg, Russia 197022

Mariia A. Makarova

Saint-Petersburg Pasteur Institute of the Federal Service on Customers’ Rights Protection and Human Well-being Surveillance;
State Educational Institution of the Higher Professional Education "North-Western state medical University n.a. I.I. Mechnikov" of the Ministry of health of the Russian Federation

Email: makmaria@mail.ru
SPIN-code: 7915-1758

PhD (Medicine), Doctor of Science, senior researcher, laboratory of enteric infections, Saint-Petersburg Pasteur Institute;

associate professor of the medical microbiology faculty; State Educational Institution of the Higher Professional Education "North-Western state medical University n.a. I.I. Mechnikov" of the Ministry of health of the Russian Federation

 

 

Russian Federation, Saint-Petersburg, 191015, Kirochnaya ul. 41.

Cuong Quoc Hoang

Pasteur Institute in Ho Chi Minh City

Email: cuonghqpasteur@gmail.com

PhD (Medicine), Deputy Director

Viet Nam

Nguyen Hoang Vu

Pasteur Institute in Ho Chi Minh City

Email: vhoangvu@yahoo.com

MSc (Biology), Head of the Laboratory of enteric infections, Microbiology and Immunology Department

Viet Nam

Huong Thuy Dang

Pasteur Institute in Ho Chi Minh City

Email: dangthuyhuong0489@gmail.com

BSc (Biotechnology), researcher, Laboratory of enteric infections, Microbiology and Immunology Department

Viet Nam

Thi Quynh Lan Tran

University of Agriculture and Forestry (Nong Lam University - Ho Chi Minh city)

Email: Thlan.tranthiquynh@hcmuaf.edu.vn

PhD, MSc, D.V.M, Head and Lecturer of Department of Veterinary Biosciences, Faculty of Animal Science and Veterinary Medicine

Viet Nam

Tram Khac Vo

Department of Animal Husbandry and Veterinary Medicine of Ho Chi Minh City

Email: vktram@chicuccntyhcm.gov.vn

MSc, Dr (Medicine),  Head of the Animal health laboratory and Treatment Division

Viet Nam

Long Thanh Nguyen

Department of Animal Husbandry and Veterinary Medicine of Ho Chi Minh City

Email: ntlong@chicuccntyhcm.gov.vn

MSc (Biotechnology),  Department of Animal Husbandry and Veterinary Medicine of Ho Chi Minh City

Diep Thi Ngoc Nguyen

Department of Animal Husbandry and Veterinary Medicine of Ho Chi Minh City

Email: ntndiep@chicuccntyhcm.gov.vn

MSc, Dr (Veterinarian)

Viet Nam

Tu Le Kha Bui

Department of Animal Husbandry and Veterinary Medicine of Ho Chi Minh City

Email: khatu09021990@gmail.com

Dr (Veterinarian), Animal health laboratory and Treatment Division

Viet Nam

Thu Le Kieu Nguyen

Department of Animal Husbandry and Veterinary Medicine of Ho Chi Minh City

Email: nlkthu@chicuccntyhcm.gov.vn

Dr (Veterinarian),  Animal health laboratory and Treatment Division

Viet Nam

References

  1. Андреева И.В., Стецюк О.У. Отпуск без проблем: современные подходы к профилактике и лечению диареи путешественников // Клиническая микробиология и антимикробная химиотерапия. 2018. Т. 20, № 3. С. 172-180.
  2. Гончар Н.В., Лазарева И.В., Рычкова С.В., Кветная А.С., Альшаник Л.П., Фомичева Ю.В., Ныркова О.И., Кириленко Л.А. Заболеваемость детей сальмонеллезом и уровень резистентности клинических штаммов сальмонелл к антибактериальным препаратам в Санкт-Петербурге // Журнал инфектологии. 2015. Т. 7, № 1. С.80-86.
  3. Евмененкова И.Г., Мурач Л.В. Анализ резистентности штаммов Salmonella spp. к антибиотикам в Смоленском регионе за 2012-2017 гг. // Смоленский Медицинский Альманах. 2018. № 1. С. 93-96.
  4. Егорова С.А., Кафтырева Л.А., Сужаева Л.В., Забровская А.В., Войтенкова Е.В., Матвеева З.Н., Останкова Ю.В., Лихачев И.В., Сатосова Н.В., Кицбабашвили Р.В., Смирнова Е.В., Семченкова Л.И., Быстрая Т.Е., Сокольник С.Е., Уткина Н.П., Сихандо Л.Ю. Устойчивость к антимикробным препаратам и клинически значимые механизмы резистентности штаммов Salmonella, выделенных в 2014-2018 гг. в Санкт-Петербурге, Россия // Клиническая лабораторная диагностика. 2019. Т. 64, № 10. С. 620-626.
  5. Забровская А.В., Егорова С.А., Антипова Н.А., Смирнова Е.В., Семченкова Л.И., Быстрая Т.Е., Сокольник С.Е., Уткина Н.П., Сихандо Л.Ю., Сатосова Н.В. Чувствительность к антибиотикам сальмонелл-доминирующих сероваров, выделенных в Северо-Западном федеральном округе РФ в 2004–2018 гг. из различных источников. Журнал инфектологии. 2022. Т. 14, № 1. С. 131-139.
  6. Козлов С.Н., Козлов Р.С. Современная антимикробная химиотерапия: руководство для врачей. Москва: ООО «Медицинское информационное агентство», 2017, 400 с.
  7. Кузнецова Н.А., Соловьева А.С., Раков А.В. Чувствительность к антибиотикам у штаммов Salmonella Enteritidis, циркулирующих на территории Сибири и Дальнего Востока, по данным многолетнего мониторинга // Здоровье. Медицинская экология. Наука. 2018. Т. 3. С. 50-58.
  8. О состоянии санитарно-эпидемиологического благополучия населения в Российской Федерации в 2020 году: Государственный доклад. М.: Федеральная служба по надзору в сфере защиты прав потребителей и благополучия человека. 2021. 256 с.
  9. Anders K.L., Thompson C.N., Thuy N.T., Nguyet N.M., Tu le T.P., Dung T.T., Phat V.V., Van N.T., Hieu N.T., Tham N.T., Ha P.T., Lien le B., Chau N.V., Baker S., Simmons C.P. The epidemiology and aetiology of diarrhoeal disease in infancy in southern Vietnam: a birth cohort study. Int J Infect Dis., 2015, vol 35, pp. 3-10.
  10. Centers for Disease Control and Prevention. Yellow Book, 2020. Chapter 2. Travelers' Diarrhea.
  11. Echeita M.A., Herrera S., Garaizar J., Usera M.A. Multiplex PCR-based detection and identification of the most common Salmonella second-phase flagellar antigens. Res Microbiol., 2002, vol. 153, no. 2, pp. 107-113.
  12. EFSA and ECDC (European Food Safety Authority and European Centre for Disease Prevention and Control), 2018. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA Journal, 2018, vol. 16, no. 12, e05500, pp. 262.
  13. EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control), 2022. The European Union Summary Report on Antimicrobial Resistance in zoonotic and indicator bacteria from humans, animals and food in 2019–2020. EFSA Journal, 2022, vol. 20, no. 3, e07209, pp 197.
  14. Herrera-León S., McQuiston J.R., Usera M.A., Fields P.I., Garaizar J., Echeita M.A. Multiplex PCR for distinguishing the most common phase-1 flagellar antigens of Salmonella spp. Journal of clinical microbiology, 2004, vol. 42, no. 6, pp. 2581–2586.
  15. Huyen D.T.T., Hong D.T., Trung N.T., Hoa T.T.N., Oanh N.K., Thang H.V., Thao N.T.T., Hung D.M., Iijima M., Fox K., Grabovac V., Heffelfinger J., Batmunkh N., Anh D.D. Epidemiology of acute diarrhea caused by rotavirus in sentinel surveillance sites of Vietnam, 2012-2015. Vaccine, 2018, vol. 36, no. 51, pp. 7894-7900.
  16. An H.T.T., Khai L.T.L. The prevalence and antibiotic resistance of Salmonella spp. isolated from pigs and farm environments in vinh long province. Can Tho University Journal of Science, 2018, vol. 54, Special issue: Agriculture (2018), pp. 26-33.
  17. Lettini A.A., Vo Than T., Marafin E., Longo A., Antonello K., Zavagnin P., Barco L., Mancin M., Cibin V., Morini M., Dang Thi Sao M., Nguyen Thi T., Pham Trung H., Le L., Nguyen Duc T., Ricci A. Distribution
  18. of Salmonella Serovars and Antimicrobial Susceptibility from Poultry and Swine Farms in Central Vietnam. Zoonoses Public Health, 2016, vol. 63, pp.569-576.
  19. Nhung N.T., Van N., Cuong N.V., Duong T., Nha, T.T., Hang T., Nhi N., Kiet B.T., Hien V.B., Ngoc P.T., Campbell J., Thwaites G., Carrique-Mas J. Antimicrobial residues and resistance against critically important antimicrobials in non-typhoidal Salmonella from meat sold at wet markets and supermarkets in Vietnam. International journal of food microbiology, 2018, vol. 266, pp. 301–309.
  20. Noor Uddin G.M., Larsen M.H., Barco L., Minh Phu T., Dalsgaard A. Clonal Occurrence of Salmonella Weltevreden in Cultured Shrimp in the Mekong Delta, Vietnam. PloS one, 2015, vol. 10, no. 7, e0134252.
  21. Phu Huong Lan N., Le Thi Phuong T., Nguyen Huu H., Thuy L., Mather A.E., Park S.E., Marks F., Thwaites G.E., Van Vinh Chau N., Thompson C.N., Baker S. Invasive Non-typhoidal Salmonella Infections in Asia: Clinical Observations, Disease Outcome and Dominant Serovars from an Infectious Disease Hospital in Vietnam. PLoS Negl Trop Dis., 2016, vol. 10. no. 8, e0004857.
  22. Riddle M.S., DuPont H.L., Bradley A., Connor B.A. ACG Clinical Guideline: Diagnosis, Treatment, and Prevention of Acute Diarrheal Infections in Adults. American J Gastroenterology, 2016, vol. 111, no. 5, pp. 602–622.
  23. Ta Y.T., Nguyen T.T., To P.B., Pham da X., Le H.T., Thi G.N., Alali W.Q., Walls I., Doyle M.P. Quantification, serovars, and antibiotic resistance of salmonella isolated from retail raw chicken meat in Vietnam. J Food Prot., 2014, vol. 77, no. 1, pp. 57-66.
  24. Tai DT. Circulation of extended-spectrum β-lactamase producing Salmonella isolated from food handler in Lam Dong provinces. 2nd International Conference on Clinical Microbiology & Microbial Genomics, September 16-17, 2013, Hampton Inn Tropicana, Las Vegas, NV, USA
  25. Thompson C.N., Phan V.T., Le T.P., Pham T.N., Hoang L.P., Ha V., Nguyen V.M., Pham V.M., Nguyen T.V., Cao T.T., Tran T.T., Nguyen T.T., Dao M.T., Campbell J.I., Nguyen T.C., Tang C.T., Ha M.T., Farrar J., Baker S. Epidemiological features and risk factors of Salmonella gastroenteritis in children resident in Ho Chi Minh City, Vietnam. Epidemiol Infect., 2013, vol. 141, no. 8, pp.1604-13.
  26. Trung N.V., Carrique-Mas J.J., Nghia N.H., Tu L.T., Mai H.H., Tuyen H.T., Campbell J., Nhung N.T., Nhung H.N., Minh P.V., Chieu T.T., Hieu T.Q., Mai N.T., Baker S., Wagenaar J.A., Hoa N.T., Schultsz C. Non-Typhoidal Salmonella Colonization in Chickens and Humans in the Mekong Delta of Vietnam. Zoonoses Public Health, 2017, vol. 64, no. 2, pp.94-99.
  27. Thai T.H., Hirai T., Lan N.T., Yamaguchi R. Antibiotic resistance profiles of Salmonella serovars isolated from retail pork and chicken meat in North Vietnam. Int J Food Microbiol., 2012, vol. 156, no. 2, pp. 147-51.
  28. Tu L.T., Hoang N.V., Cuong N.V., Campbell J., Bryant J.E., Hoa N.T., Kiet B.T., Thompson C., Duy D.T., Phat V.V., Hien V.B., Thwaites G., Baker S., Carrique-Mas J.J. High levels of contamination and antimicrobial-resistant non-typhoidal Salmonella serovars on pig and poultry farms in the Mekong Delta of Vietnam. Epidemiology and infection, 2015, vol. 143, no.14,pp. 3074–3086.
  29. Van T.T., Moutafis G., Tran L.T., Coloe P.J. Antibiotic resistance in food-borne bacterial contaminants in Vietnam. Applied and environmental microbiology, 2007, vol. 73, no. 24, pp. 7906–7911.
  30. WHO publishes list of bacteria for which new antibiotics are urgently needed. News Release 27.02.2017

Supplementary files

There are no supplementary files to display.


Copyright (c) Egorova S.A., Nguyen T., Kaftyreva L.A., Kozhukhova E.A., Makarova M.A., Hoang C., Vu N., Dang H., Tran T., Vo T., Nguyen L., Nguyen D., Bui T., Nguyen T.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 64788 от 02.02.2016.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies