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Original articles
Оригинальные статьи
Russian Journal of Infection and Immunity = Infektsiya i immunitet Инфекция и иммунитет
2022, vol. 12, no. 6, pp. 1081-1090 2022, Т. 12, № 6, с. 1081-1090
SEROGROUPS AND ANTIMICROBIAL SUSCEPTIBILITY OF SALMONELLA ISOLATED FROM PEOPLE AND FOOD ITEMS IN SOUTHERN PROVINCES OF VIETNAM
S.A. Egorova1, Q.N. Truong2, L.A. Kaftyreva13, E.A. Kozhukhova4, M.A. Makarova13, Q.H. Cuong2, H.N. Vu2, T.D. Huong2, T.Q.T. Lan5, K.V. Tram6, T.N. Long6, T.N.N. Diep6, L.K.B. Tu6, L.K.N. Thu6
1 St. Petersburg Pasteur Institute, St. Petersburg, Russian Federation
2 Pasteur Institute in Ho Chi Minh City, Vietnam
3 I.I. Mechnikov North-Western State Medical University, St. Petersburg, Russian Federation 4Pavlov First Saint Petersburg State Medical University, St. Petersburg, Russian Federation
5 University of Agriculture and Forestry (Nong Lam University), Ho Chi Minh, Vietnam 6Department of Animal Husbandry and Veterinary Medicine, Ho Chi Minh City, Vietnam
Abstract. This article presents current relevant data on the serogroups and antimicrobial susceptibility of Salmonella strains isolated in the southern provinces of the Socialist Republic of Vietnam. There were examined 189 Salmonella strains isolated from: human feces in acute diarrhea (86 strains); and pork samples (103 strains). Serological O-group identification was performed by slide agglutination with O- and H-antisera and multiplex PCR to detect H phase-1 and phase-2. Antimicrobial susceptibility testing was performed by using the disk-diffusion method according to the EUCAST (version 2019) recommendations. Strains isolated from humans predominantly belonged to O4 group (69.8%). The percentage of other serogroups varied from 1.2% (rare group O16) to 11.6% (O9). About a half of strains (44.7%) isolated from pork samples turned out to belong to the О3,10 serogroup (vs 7.0% of strains from humans). Serogroups О7,
04 and О8 were less frequent (22.3%, 14.6% and 13.6%, respectively). Single strains belonged to serogroups О9, О13, and О18. Regardless of the isolation source, about 80% of Salmonella strains were resistant to antibiotics from different antimicrobial groups (besides carbapenems): 67.0% were resistant to tetracycline; about half were resistant to pefloxa-cin, ampicillin and chloramphenicol (54.0%, 47.1%, 46.6%); and up to 40% were resistant to trimethoprim/sulfameth-oxazole and nalidixic acid. The proportion of strains resistant to ceftriaxone and gentamycin was markedly higher in those of human vs pork origin: 12.8% vs 1.0% and 30.2 vs 1.9%, respectively. Moreover, 62.8% and 43.7% strains of human and pork origin, respectively, showed multidrug resistance (to 3 and more antimicrobial groups). In addition, simultaneous resistance to 6 antimicrobial groups was detected much more frequently in Salmonella strains isolated from humans vs pork samples (15.1% vs 1.0%, respectively). Multidrug resistance (MDR) was observed in strains of different serovars, predominantly S. Typhimurium (36.4%). The predominant MDR (30.3%) phenotype (AMP, TE, QN, C, SXT) was revealed in serovars of S. Typhimurium, S. Bredeney, S. Corvallis, S. Give, S. London, S. Rissen, and S. Meleagridis. Thus, Salmonella strains isolated in the southern Vietnamese provinces featured resistance to fluoro-
Адрес для переписки:
Егорова Светлана Александровна
197101, Россия, Санкт-Петербург, ул. Мира, 14,
ФБУН НИИ эпидемиологии и микробиологии имени Пастера.
Тел.: 8 (812) 232-48-83 (служебн.).
E-mail: [email protected]
Для цитирования:
Егорова С.А., Чуонг К.Н., Кафтырева Л.А., Кожухова Е.А., Макарова М.А., Куонг К.Х., Ву Х.Н., Хуонг Т.З., Лан Т.К.Ч., Чам К.В., Лонг Т.Н., Диеп Т.Н.Н., Ту Л.К.Б., Тху Л.К.Н. Серологическая структура и чувствительность к антибиотикам штаммов Salmonella, выделенных от людей и из пищевых продуктов в южных провинциях Вьетнама // Инфекция и иммунитет. 2022. Т. 12, № 6. C. 1081-1090. doi: 10.15789/2220-7619-SPA-1954
© Egorova S.A. et al., 2022
Contacts:
Svetlana A. Egorova
197101, Russian Federation, St. Petersburg, Mira str., 14, St. Petersburg Pasteur Institute. Phone: +7 (812) 232-48-83 (office). E-mail: [email protected]
Citation:
Egorova S.A., Truong Q.N., Kaftyreva L.A., Kozhukhova E.A., Makarova M.A., Cuong Q.H., Vu H.N., Huong T.D., Lan T.Q.T., Tram K.V., Long T.N., Diep T.N.N., Tu L.K.B., Thu L.K.N. Serogroups and antimicrobial susceptibility of Salmonella isolated from people and food items in southern provinces of Vietnam // Russian Journal of Infection and Immunity = Infektsiya i immunitet, 2022, vol. 12, no. 6, pp. 1081-1090. doi: 10.15789/2220-7619-SPA-1954
DOI: http://dx.doi.org/10.15789/2220-7619-SPA-1954
quinolones and cephalosporins. Taking into account simultaneous loss of susceptibility to "old" antimicrobials (am-picillin, chloramphenicol, trimethoprim/sulfamethoxazole), it crucially restricts the list of effective medicines to treat complicated salmonellosis cases.
Key words: Salmonella, antimicrobial resistance, multidrug resistance, serovar.
СЕРОЛОГИЧЕСКАЯ СТРУКТУРА И ЧУВСТВИТЕЛЬНОСТЬ К АНТИБИОТИКАМ ШТАММОВ SALMONELLA, ВЫДЕЛЕННЫХ ОТ ЛЮДЕЙ И ИЗ ПИЩЕВЫХ ПРОДУКТОВ В ЮЖНЫХ ПРОВИНЦИЯХ ВЬЕТНАМА
Егорова С.А.1, Чуонг К.Н.2, Кафтырева Л.А.13, Кожухова Е.А.4, Макарова М.А.13, Куонг К.Х.2, Ву Х.Н.2, Хуонг Т.З.2, Лан T.К.Ч.5, Чам К.В.6, Лонг Т.Н.6, Диеп Т.Н.Н.6, Ту Л.К.Б.6, Тху Л.К.Н.6
1ФБУН НИИ эпидемиологии и микробиологии имени Пастера, Санкт-Петербург, Россия 2Институт Пастера в г. Хо Ши Мин, г. Хо Ши Мин, Социалистическая Республика Вьетнам
3 ФГБОУВО Северо-Западный государственный медицинский университет им И.И. Мечникова, Санкт-Петербург, Россия
4 ФГБОУ ВО Первый Санкт-Петербургский государственный медицинский университет им. акад. И.П. Павлова, Санкт-Петербург, Россия
5Университет сельского и лесного хозяйства, г. Хо Ши Мин, Социалистическая Республика Вьетнам 6 Департамент животноводства и ветеринарии г. Хо Ши Мин, Социалистическая Республика Вьетнам
Резюме. В статье представлены современные данные о серогрупповой структуре и чувствительности к антибиотикам штаммов Salmonella, выделенных в южных провинциях Социалистической Республики Вьетнам. Всего исследовано 189 штаммов из коллекции Института Пастера в г. Хошимин: выделенных от людей — 86 и из свинины — 103 штамма. Штаммы идентифицировали до серовара с использованием реакции агглютинации на стекле с O- и H-сыворотками и мультиплексных ПЦР для выявления Н 1 и 2 фазы. Чувствительность к антибиотикам определяли диско-диффузионным методом согласно рекомендациям EUCAST (2019 г.). Штаммы, выделенные от людей, преимущественно принадлежали серогруппе O4 (69,8%), доля штаммов других серогрупп колебалась от 1,2% (редкая группа О16) до 11,6% (O9). Около половины штаммов (44,7%), выделенных из свинины, относились к серогруппе 03,10 (от людей — только 7,0% штаммов); штаммы серогрупп О7, 04 и 08 выделяли значительно реже (22,3%, 14,6% и 13,6%); к группам 09, 013 и 018 принадлежали единичные штаммы. Вне зависимости от источника выделения около 80,0% штаммов Salmonella были устойчивы к антибиотикам различных групп (исключая карбапенемы): 70,0% — к тетрациклинам, около половины (54,0%, 47,1% и 46,6%) — к пефлоксацину, аминопенициллинам и хлорамфениколу, почти 40% — к триметоприм/ сульфаметоксазолу и налидиксовой кислоте. Доля устойчивых к цефтриаксону и гентамицину была значительно выше у штаммов, выделенных от людей, чем из свинины: 12,8% и 1,0%, 30,2% и 1,9% соответственно. Множественной резистентностью (к 3 и более группам антибиотиков) обладали 62,8% штаммов, выделенных от людей и 43,7% — из свинины. Следует отметить, что резистентность к 6 группам антибиотиков чаще выявляли у штаммов, выделенных от людей, чем из свинины (15,1% и 1,0% соответственно). Множественную резистентность отмечали у штаммов различных сероваров, но преимущественно у S. Typhimurium (36,4%). Наиболее часто встречали фенотип множественной устойчивости AMP, TE, QN, C, SXT (30,3%), выявленный у штаммов сероваров S. Typhimurium, S. Bredeney, S. Corvallis, S. Give, S. London, S. Rissen, S. Meleagridis. Таким образом, у штаммов Salmonella, выделенных в южных провинциях Вьетнама, выявлена устойчивость к современным препаратам выбора (фторхинолонам и цефалоспоринам), что, наряду с потерей чувствительности к «традиционным» антибиотикам (ампициллин, хлорамфеникол, триметоприм/ сульфаметоксазол), существенно сокращает арсенал антимикробных (этиотропных) препаратов, потенциально эффективных для терапии осложненных форм сальмонеллеза.
Ключевые слова: Salmonella, устойчивость к антибиотикам, множественная резистентность, серовар.
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 sero-groups 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 fluoroqui-nolones, extended spectrum cephalosporins, or tri-
methoprim/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 cip-rofloxacin (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 P-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 B, with S. Paratyphi B included [23]. This study's objective was to characterize the sero-group 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 diskdiffusion method with Mueller-Hinton agar and antibiotic disks (Oxoid). The tested antimicrobials belonged to different antibiotic classes: P-lactams (ampicillin, ceftazidime, ceftriaxone, meropenem); quinolones (nalidixic acid, pefloxacin); tetracy-cline; 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/
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
O-group Serovar Number of strains isolated from
human pork Total
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.
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): 04 (B) - 75 strains (39.7%); 03,10 (E) -52 strains (27.5%); 07 (Q) - 30 (15.9%); 08 (C2) -16 (8.5%); 09 (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.
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 03,10 (versus 7.0% in strains from humans). Serogroups 07, 04, and 08 were less frequent (22.3%, 14.6% and 13.6%, respectively). Single strains from pork belonged to serogroups
09, 013, and 018. 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).
Up to 70.0% of strains were resistant to tetracycline. About half of strains were resistant to pefloxa-cin, 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 amoxi-cillin/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
Salmonella from human (n = 86)
Salmonella from pork (n = 103)
□ 04
■ 03,10
□ 07 0 08 HI 09
■ 016
□ 013
Fcl 018
09
013 018
,„„, 1,0% 1,9% 04 1.9* —— 14,6%
Figure. Serogroup pattern of Salmonella spp. isolated from humans and pork in southern provinces of Vietnam
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.
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).
In general, MDR was detected in 52.4% (n = 99) of Salmonella belonging to different serovars, but se-rovar 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 se-rovars 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 03,10, 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% ofbeef samples; up to 70.0% ofpork; 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.
Table 3. MDR phenotypes of Salmonella isolated from different sources in southern provinces of Vietnam
Resistance phenotypes (antibiotic groupsi) 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 0:3,10 group 0:8 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 0:7 S. Stanley 4 group 0:3,10 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 0:3,10 3
AMP, C3-4, QN, C 1 group 0:3,10 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 0:3,10 S. Heidelberg S. Rissen S. Stanley S. Typhimurium 22 group 0:7 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 0:7 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 0:9 S. Typhimurium 0 - 3
TOTAL MDR strains 54 45 - 99
Note. MDR — multidrug resistant. 1 Antibiotic groups: AMP — amlnopenlcllllns (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.
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 fluoroqui-nolones (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
References
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The appearance of Salmonella producing extended spectrum в-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 03,10.
The resistance to fluoroquinolones and cepha-losporins observed, simultaneous with the loss of Salmonella susceptibility to "old" antimicrobials (ampicillin, chloramphenicol, trimethoprim/sul-famethoxazole), 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.
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Авторы:
Егорова С.А., д.м.н., старший научный сотрудник лаборатории кишечных инфекций ФБУН НИИ эпидемиологии и микробиологии имени Пастера, Санкт-Петербург, Россия; Чуонг К.Н., исследователь лаборатории кишечных инфекций отдела микробиологии и иммунологии Института Пастера в г. Хо Ши Мин, г. Хо Ши Мин, Социалистическая Республика Вьетнам;
Кафтырева Л.А., д.м.н., профессор, зав. лабораторией кишечных инфекций ФБУН НИИ эпидемиологии и микробиологии имени Пастера, Санкт-Петербург, Россия; Кожухова Е.А., к.м.н., старший научный сотрудник лаборатории хронических вирусных инфекций НИЦ при кафедре инфекционных болезней и эпидемиологии Первого Санкт-Петербургского государственного медицинского университета им. И.П. Павлова, Санкт-Петербург, Россия;
Макарова М.А., д.м.н., старший научный сотрудник лаборатории кишечных инфекций ФБУН НИИ эпидемиологии и микробиологии имени Пастера, Санкт-Петербург, Россия; доцент кафедры медицинской микробиологии ФГБОУ ВО Северо-Западный государственный медицинский университет им И.И. Мечникова, Санкт-Петербург, Россия; Куонг К.Х., к.м.н., зам. директора Института Пастера в г. Хо Ши Мин, г. Хо Ши Мин, Социалистическая Республика Вьетнам; Ву Х.Н., зав. лабораторией кишечных инфекций отдела микробиологии и иммунологии Института Пастера в г. Хо Ши Мин, г. Хо Ши Мин, Социалистическая Республика Вьетнам; Хуонг Т.З., исследователь лаборатории кишечных инфекций отдела микробиологии и иммунологии Института Пастера в г. Хо Ши Мин, г. Хо Ши Мин, Социалистическая Республика Вьетнам;
Лан Т.К.Ч., зав. отделом ветеринарных наук факультета животноводства и ветеринарии Университета сельского и лесного хозяйства, г. Хо Ши Мин, Социалистическая Республика Вьетнам;
Чам К.В., зав. лабораторией здоровья животных и терапевтическим отделом Департамента животноводства и ветеринарии, г. Хо Ши Мин, Социалистическая Республика Вьетнам;
Лонг Т.Н., сотрудник Департамента животноводства и ветеринарии, г. Хо Ши Мин, Социалистическая Республика Вьетнам;
Диеп Т.Н.Н., сотрудник Департамента животноводства и ветеринарии, г. Хо Ши Мин, Социалистическая Республика Вьетнам;
Ту Л.К.Б., сотрудник лаборатории здоровья животных и терапевтического отдела Департамента животноводства и ветеринарии, г. Хо Ши Мин, Социалистическая Республика Вьетнам;
Тху Л.К.Н., сотрудник лаборатории здоровья животных и терапевтического отдела Департамента животноводства и ветеринарии, г. Хо Ши Мин, Социалистическая Республика Вьетнам
Поступила в редакцию 25.05.2022 Принята к печати 23.08.2022
Authors:
Egorova S.A., PhD, MD (Medicine), Senior Researcher, Laboratory of Enteric Infections, St. Petersburg Pasteur Institute, St. Petersburg, Russian Federation; Truong Q.N., MSc (Biotechnology), Researcher, Laboratory of Enteric Infections, Department of Microbiology and Immunology, Pasteur Institute in Ho Chi Minh City, Ho Chi Minh, Vietnam; Kaftyreva L.A., PhD, MD (Medicine), Professor, Head of the Laboratory of Enteric Infections, St. Petersburg Pasteur Institute, St. Petersburg, Russian Federation;
Kozhukhova E.A., PhD (Medicine), Senior Researcher, Chronic Viral I nfection Laboratory of the Research Center (Branch of the Infectious Diseases and Epidemiology Department), Pavlov First St. Petersburg State Medical University, St. Petersburg, Russian Federation;
Makarova M.A., PhD, MD (Medicine), Senior Researcher, Laboratory of Enteric Infections, St. Petersburg Pasteur Institute, St. Petersburg, Russian Federation; Associate Professor, Department of Medical Microbiology, I.I. Mechnikov North-Western State Medical University, St. Petersburg, Russian Federation; Cuong Q.H., PhD (Medicine), Deputy Director, Pasteur Institute in Ho Chi Minh City, Ho Chi Minh, Vietnam;
Vu H.N., MSc (Biology), Head of the Laboratory of Enteric Infections,
Department of Microbiology and Immunology, Pasteur Institute in Ho
Chi Minh City, Ho Chi Minh, Vietnam;
Huong T.D., BSc (Biotechnology), Researcher, Laboratory
of Enteric Infections, Department of Microbiology and Immunology,
Pasteur Institute in Ho Chi Minh City, Ho Chi Minh, Vietnam;
Lan T.Q.T., PhD, MSc, D.V.M., Head and Lecturer, Department
of Veterinary Biosciences, University of Agriculture and Forestry
(Nong Lam University), Ho Chi Minh, Vietnam;
Tram K.V., MSc, Dr (Medicine), Head of the Laboratory of Animal
Health and Treatment Division, Department of Animal Husbandry
and Veterinary Medicine, Ho Chi Minh City, Vietnam;
Long T.N., MSc (Biotechnology), Member of Stuff, Department
of Animal Husbandry and Veterinary Medicine of Ho Chi Minh City,
Ho Chi Minh City, Vietnam;
Diep T.N.N., MSc, Dr (Veterinarian), Member of Stuff, Department of Animal Husbandry and Veterinary Medicine of Ho Chi Minh City, Ho Chi Minh City, Vietnam;
Tu L.K.B., Dr (Veterinarian), Member of Stuff, Animal Health Laboratory and Treatment Division, Department of Animal Husbandry and Veterinary Medicine of Ho Chi Minh City, Ho Chi Minh City, Vietnam;
Thu L.K.N., Dr (Veterinarian), Member of Stuff, Animal Health Laboratory and Treatment Division, Department of Animal Husbandry and Veterinary Medicine of Ho Chi Minh City, Ho Chi Minh City, Vietnam.
Received 25.05.2022 Accepted 23.08.2022
