Серологическая структура и чувствительность к антибиотикам штаммов Salmonella, выделенных от людей и из пищевых продуктов в южных провинциях Вьетнама

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Introduction

According to WHO data, from 1 to 1.7 billion cases of acute diarrhea are registered annually. Thus, they are the leading infectious illness, followed only by acute respiratory infection. Globally, acute diarrhea accounts for more than 500 000 deaths in children, occupying second place in mortality in those younger than 5 years old (https://www.who.int/news-room/fact-sheets/detail/diarrhoeal-disease). In Russia as well as in European countries, the causative agents in up to 70% of acute diarrheal cases (especially food-borne outbreaks) are Rotavirus and Norwalk viruses. The most widespread bacterial agents of acute diarrhea cases are Salmonella and Campylobacter [8, 12]. Salmonellosis is known to have different clinical patterns, predominantly resulting from digestive tract effects, with potential to spread beyond it with development of toxic and dehydration syndromes of various severity. Salmonella has potential to cause food-born infection with small and large outbreaks [12].

In Vietnam, the prevalence of acute diarrhea in infants is 271 per 1000 children. In more than 70% of cases, there were detected such viruses as Rotavirus (50.0% of samples) and Norwalk (24.0%). Among bacterial agents, Campylobacter (20.0%), Salmonella (18.0%), and Shigella (16.0%) were found [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 Russia, where serovar S. Enteritidis accounts for more than 80.0% of cases and has dominated for many years, in Vietnam the serogroup spectrum of Salmonella isolated both from humans and food is more diverse. For example, an examination of adult hospitalized cases in 2008–2013 revealed S. Enteritidis and S. Typhimurium in 48.0% and 26.0% of cases, respectively [20]. Salmonella isolated from healthy food workers in different years belonged to different serogroups and serovars. For example, Salmonella isolates in 2011 were as follows: 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 (except S. Enteritidis) (12.5%); and serogroups A and E (10.0%). In 2013, strains from serogroups B, E, and C dominated (55.6%, 22.2% and 16.7%, respectively) [23].

In Vietnam, there have been many examinations of samples taken from food-producing animals, poultry, prawns, fish, and food items as potential sources and vehicles of Salmonella transmission to humans. High levels of contamination with Salmonella (belonging to 28–53 serogroups) have been described [16, 17, 19, 22, 25, 26, 27].

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 shrimp farm in the Mekong delta covering three Vietnamese provinces [19]. Some studies (2004–2016 in provinces of Southern Vietnam) 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 and healthy pigs (61.5% and 8.8%, respectively). In Dong Thap, the percentage of Salmonella contaminated samples was 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 (e.g., fever longer than 48 hours); age less than 6 months or more than 50 years; with immune deficiency; or with severe concurrent diseases. Empiric therapy suggests prescribing fluoroquinolones, extended spectrum cephalosporins, or trimethoprim/sulfamethoxazole [1, 6, 10, 21]. However, Salmonella isolated from humans, animals, and food items is displaying increasing antimicrobial resistance in many countries [13]. In Russia, the percentage of such Salmonella strains (isolated from humans, animals, and food items) is up to 50–70.0% [2, 3, 4, 5, 7].

Most Salmonella strains (about 60.0%) examined by different researchers in 2004–2017 in Vietnam were resistant to such antibiotics as: ampicillin (more than 40.0% of strains); tetracycline (more than 50.0%); trimethoprim/sulfamethoxazole (up to 60.0%); chloramphenicol (up to 50.0%); and ciprofloxacin (more than 30.0% of strains) [16, 17, 18, 19, 22, 23, 25, 26, 27, 28]. According to different research data, from 17 to 52.2% of strains had multidrug resistance (MDR). S. Kentucky ST198 was considered the most frequent MDR serovar, with high levels of resistance to β-lactams and quinolones.

Notably, there was one strain (from pork) exhibiting colistin resistance. It is the first colistin-resistant Salmonella found in meat in Vietnam [18, 28]. Some data indicate that the percentage of Salmonella strains producing ESBL (TEM and CTX genetic families) is equal to 5.3%. Strains predominantly belonged to serogroup В, with S. Рaratyphi B included [23]. This study’s objective was to characterize the serogroup structure and to evaluate antimicrobial susceptibility of Salmonella isolated from humans and food samples in South Vietnam.

Materials and methods

The study was performed within a framework of scientific cooperation between the St. Petersburg Pasteur Institute and the Pasteur Institute in Ho Chi Minh City. The samples studied were 189 Salmonella strains isolated in South Vietnam: 86 strains from feces of humans with acute diarrhea; and 103 from pork samples.

Salmonella serological identification to O-group was first determined by slide agglutination with O-group antisera (St. Petersburg Scientific Research Institute of Vaccine and Serum, Russia). Phase-1 and phase-2 were then detected by multiplex PCR [11, 14], with subsequent confirmation by slide agglutination with phase-1 and phase-2 antisera.

Antimicrobial susceptibility testing was done according EUCAST recommendations (version 2019, https://www.eucast.org/ast_of_bacteria) by the disk-diffusion method with Mueller–Hinton agar and antibiotic disks (Oxoid). The tested antimicrobials belonged to different antibiotic classes: β-lactams (ampicillin, ceftazidime, ceftriaxone, meropenem); quinolones (nalidixic acid, pefloxacin); tetracycline; phenicols (chloramphenicol); trimethoprim/sulfamethoxazole; polymyxins (colistin); and aminoglycosides (gentamycin, amikacin). 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”, the following breakpoints (zone of inhibition) were used: pefloxacin < 24 mm; and nalidixic acid < 16 mm.

Results

Salmonella strains belonged to several O-groups (Table 1): 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%). Some differences in serogroup spectrum were revealed in strains isolated from humans versus those from pork items as presented in Fig.

 

Table 1. Salmonella serovars isolated from humans and pork in southern provinces of Vietnam (number of strains, proportion, 95% confidence 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

Note. *Differences are statistically significant.

 

Figure. Serogroup pattern of Salmonella spp. isolated from humans and pork in southern provinces of Vietnam

 

Strains isolated from humans predominantly belonged to group O4 (69.8%). The percentages of other serogroups varied from 1.2% (rare groups) to 11.6% (O9). About half of strains isolated from pork (44.7%) belonged to serogroup О3,10 (versus 7.0% in strains from humans). Serogroups О7, О4, and О8 were less frequent (22.3%, 14.6% and 13.6%, respectively). Single strains from pork belonged to serogroups О9, О13, and О18. It is 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 humans (69.7% and 11.6%, respectively).

The studied Salmonella strains were resistant (about 80%) to antibiotics from different antimicrobial groups. More than half of strains (52.4%) had MDR to 3 or more antimicrobial groups (Table 2). For the majority of antimicrobials tested, there was no significant difference in the proportion of resistant strains (resistant/overall) in terms of sample source (humans, pork).

 

Table 2. Antimicrobial susceptibility and resistance of Salmonella spp. isolated from different sources in southern provinces of Vietnam

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 or 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
– ceftazidime	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/sulfamethoxazole	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

Note. *MDR — multidrug resistant; **differences are statistically significant.

 

Up to 70.0% of strains were resistant to tetracycline. About half of strains were resistant to pefloxacin, ampicillin, and chloramphenicol. About 40% were resistant to trimethoprim/sulfamethoxazole and nalidixic acid. However, it’s worth mentioning that in pork strains none featured resistance to amoxicillin/clavulanic acid, ceftazidime and amikacin. The proportion of strains resistant to ceftriaxone and gentamycin, in those from humans versus those from pork, were significantly different: 12.8% vs 1.0%; and 30.2 vs 1.9%, respectively (Table 2). Noteworthy is the fact that 16.4% of Salmonella strains were resistant to pefloxacin, but susceptible to nalidixic acid. This indicates transferable resistance mechanisms to fluoroquinolones. All tested Salmonella strains were susceptible to carbapenems.

Multidrug resistant Salmonella strains were identified in samples both from humans and pork (62.8% and 43.7%, respectively) (Table 3). However, simultaneous resistance to 6 antimicrobials was detected much more frequently in Salmonella strains isolated from humans than in those isolated from pork (15.1% vs 1.0%, respectively).

 

Table 3. MDR phenotypes of Salmonella isolated from different sources in southern provinces of Vietnam

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	group 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	group O:9	6
Resistant to 4 groups	13		17		30
TE, QN, C, SXT	4	S. Newport S. Saintpaul S. Stanley S. Typhimurium	6	group O:4 group 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

Note. MDR — multidrug resistant. 1 Antibiotic groups: AMP — aminopenicillins (ampicillin); C3–4 — cephalosporins of 3–4 generations (ceftriaxone, ceftazidime); CARB — carbapenems (meropenem); QN — quinolones (nalidixic acid, pefloxacin); AMG — aminoglycosides (gentamycin, amikacin); TE — tetracyclines (tetracycline); C — phenicols (chloramphenicol); SXT — trimethoprim/sulfamethoxazole.

 

In general, MDR was detected in 52.4% (n = 99) of Salmonella belonging to different serovars, but serovar S. Typhimurium represented the biggest proportion of MDR strains (36.4%, n = 36). The predominant MDR phenotype (AMP, TE, QN, C, SXT) was detected in 30.3% of MDR strains belonging to serovars S. Typhimurium, S. Bredeney, S. Corvallis, S. Give, S. London, S. Rissen, and S. Meleagridis. Most of these strains were isolated from pork samples.

Discussion

Our research results suggest that in southern provinces of Vietnam, Salmonella strains isolated from people predominantly belonged to serogroup O4 (about 70.0%). The proportion of strains belonging to other serogroups (13–15 serovars) was much lower, varying from 1.2% to 11.6%. The spectrum of Salmonella strains isolated in Vietnam differs significantly from that in Russia, where more than 70.0% of strains isolated from humans belong to serogroup O9 (S. Enteritidis) [8]. The difference likely results from the Vietnamese tradition of consuming sea food, which is frequently contaminated by Salmonella strains of a 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 serogroup О3,10, whereas 35 Salmonella serovars were isolated in total.

Our data are consistent with results of other studies. Analysis of raw meat samples, taken in markets and supermarkets in different cities and provinces of Vietnam, revealed a high level of Salmonella contamination: 58.3% of beef samples; up to 70.0% of pork; up to 65.0% of chicken meat; up to 50.0% of cultured shrimp; and 37.0% of cultured fish. The serovar spectrum varied from 14 to 53: S. Weltevreden, S. Rissen, S. Anatum, S. London, S. Derby, S. Infantis, S. Typhimurium, S. Reading, S. Agona, S. Dabou, S. Albany, S. Emek, and S. Corvallis [22, 26].

The difference in serogroup spectrum of strains isolated in Vietnam from human and pork samples can likely also be explained by gastronomic (food cooking) traditions in Vietnamese society where seafood, poultry meat, and eggs are considered the main factor in transmission of Salmonella to humans.

Our research results suggest that more than 70.0% of Salmonella strains (isolated both from human and pork samples in Vietnam) were resistant to antimicrobials. Moreover, every second strain carried an MDR phenotype. The research revealed quite a high percentage of strains resistant to tetracycline (67.2%), fluoroquinolones (54.0%), ampicillin (47.1%), trimethoprim/sulfamethoxazole (42.3%), and chloramphenicol (46.6%). Strains resistant to 3rd/4th generation cephalosporins were seen (6.4%). Our results don’t contradict earlier published research carried out in Vietnam [16, 17, 18, 19, 22, 23, 25, 26, 27, 28]. Similar research carried out in Russia has suggested that: more than 60% of local Salmonella strains are resistant to quinolones; not more than 10.0% are resistant to “old” antimicrobials (tetracycline, chloramphenicol, ampicillin); and less than 2.0% are resistant to 3rd/4th generation cephalosporins. The percentage of MDR strains was much lower (about 15.0%) versus that in Vietnamese strains [4].

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

The appearance of Salmonella producing extended spectrum β-lactamase (ESBL) makes the empiric usage of extended spectrum cephalosporins (ESC) restricted for salmonellosis treatment. In conformity with published data in Russia, 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. They belonged to S. Typhimurium (group O4), with some strains of group О3,10.

The resistance to fluoroquinolones and cephalosporins observed, simultaneous with the loss of Salmonella susceptibility to “old” antimicrobials (ampicillin, chloramphenicol, trimethoprim/sulfamethoxazole), crucially restrict the list of medicines potent to treat complicated salmonellosis. Antimicrobial usage in raising of farm livestock may account for the appearance of resistant Salmonella strains and their spread to humans. As such, resistance restriction requires prevention of resistance formation in strains circulating in farm livestock.

Об авторах

Светлана Александровна Егорова

ФБУН НИИ эпидемиологии и микробиологии имени Пастера

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

д.м.н., старший научный сотрудник лаборатории кишечных инфекций

Россия, 197101, Санкт-Петербург, ул.Мира, 14

К. Н. Чуонг

Институт Пастера

Email: truongou@gmail.com

исследователь лаборатории кишечных инфекций отдела микробиологии и иммунологии

Вьетнам, Хо Ши Мин

Лидия Алексеевна Кафтырева

ФБУН НИИ эпидемиологии и микробиологии имени Пастера; ФГБОУ ВО Северо-Западный государственный медицинский университет им И.И. Мечникова

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

д.м.н., профессор, зав. лабораторией кишечных инфекций

 

Россия, 197101, Санкт-Петербург, улица Мира, 14; Санкт-Петербург

Елена Алексеевна Кожухова

ФГБОУ ВО Первый Санкт-Петербургский государственный медицинский университет им. акад. И.П. Павлова

Email: elko35@gmail.com

к.м.н., старший научный сотрудник лаборатории хронических вирусных инфекций НИЦ при кафедре инфекционных болезней и эпидемиологии

Россия, 197101, Санкт-Петербург, ул. Мира, 14

Мария Александровна Макарова

ФБУН НИИ эпидемиологии и микробиологии имени Пастера; ФГБОУ ВО Северо-Западный государственный медицинский университет им И.И. Мечникова

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

д.м.н., старший научный сотрудник лаборатории кишечных инфекций; доцент кафедры медицинской микробиологии 

Россия, 197101, Санкт-Петербург, ул. Мира, 14; Санкт-Петербург

К. Х. Куонг

Институт Пастера

Email: cuonghqpasteur@gmail.com

к.м.н., зам. директора Института Пастера в г. Хо Ши Мин

Вьетнам, Хо Ши Мин

Х. Н. Ву

Институт Пастера

Email: vhoangvu@yahoo.com

зав. лабораторией кишечных инфекций отдела микробиологии и иммунологии

Вьетнам, Хо Ши Мин

Т. З. Хуонг

Институт Пастера

Email: dangthuyhuong0489@gmail.com

исследователь лаборатории кишечных инфекций отдела микробиологии и иммунологии

Вьетнам, Хо Ши Мин

T. К.Ч. Лан

Университет сельского и лесного хозяйства

Email: Thlan.tranthiquynh@hcmuaf.edu.vn

зав. отделом ветеринарных наук факультета животноводства и ветеринарии

Вьетнам, Хо Ши Ми

К. В. Чам

Департамент животноводства и ветеринарии

Email: vktram@chicuccntyhcm.gov.vn

зав. лабораторией здоровья животных и терапевтическим отделом

Вьетнам, Хо Ши Мин

Т. Н. Лонг

Департамент животноводства и ветеринарии

Email: ntlong@chicuccntyhcm.gov.vn

сотрудник Департамента животноводства и ветеринарии

Вьетнам, Хо Ши Мин

Т. Н.Н. Диеп

Департамент животноводства и ветеринарии

Email: ntndiep@chicuccntyhcm.gov.vn

сотрудник Департамента животноводства и ветеринарии

Вьетнам, Хо Ши Мин

Л. К.Б. Ту

Департамент животноводства и ветеринарии

Email: khatu09021990@gmail.com

сотрудник лаборатории здоровья животных и терапевтического отдела Департамента животноводства и ветеринарии

Вьетнам, Хо Ши Мин

Л. К.Н. Тху

Департамент животноводства и ветеринарии

Автор, ответственный за переписку.
Email: nlkthu@chicuccntyhcm.gov.vn

сотрудник лаборатории здоровья животных и терапевтического отдела

Вьетнам, Хо Ши Мин

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