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Salmonella infection is a major public health concern worldwide, has contributed to an increased economic burden on the health systems. Non-typhoidal Salmonella (NTS) is a common cause of bacterial enteritis in humans, causing 93.8 million cases of gastroenteritis globally each year, with 155,000 deaths. Guangzhou city is situated in the south of China and has a sub-tropical climate, the heat and heavy rainfall helps the spread of NTS. However, no information of NTS infection is available in humans in Conghua District, the largest administrative district of Guangzhou. To understand the prevalence, serotype distribution, risk factors and drug resistance of NTS infection in humans in the survey area, an epidemiological investigation was conducted in hospitalized patients in Conghua District in Guangzhou, China. A total of 255 fecal specimens were collected from hospitalized patients (one each), with a questionnaire for each participant, and NTS infection was identified by culture, as well as serotypes confirmed by slide agglutination tests. An average prevalence of 20.39% (52/255) was observed and three serogroups were identified—serogroup B (n = 46), serogroup C1 (n = 4) and serogroup D1 (n = 2). Among them, Salmonella Typhimurium (n = 39) was the most common serotype. Children aged <3 years were observed to have a statistically higher prevalence of NTS infection than adults (25.15% versus 4.65%, P = 0.006); children with artificial feeding had a statistically higher prevalence than those with breastfeeding (30.77% versus 8.33%, P = 0.044). Antimicrobial resistance testing revealed that the majority of strains were resistant to ampicillin (92.16%), as well as 47.06% of all strains were multi-drug resistant. Therefore, it is necessary to continuous monitoring and rational use of antibiotics, which will be helpful to reduce the prevalence of resistant strains. These data will aid in making efficient control strategies to intervene with and prevent occurrence of salmonellosis.
沙门氏菌感染是世界范围内的主要公共卫生问题，导致卫生系统的经济负担增加。非伤寒沙门氏菌 （NTS） 是人类细菌性肠炎的常见原因，全球每年导致 9380 万例胃肠炎病例，其中 155,000 人死亡。广州市位于中国南部，属亚热带气候，高温和强降雨有助于 NTS 的传播。然而，在广州市最大的行政区从化区，没有关于人类感染NTS的信息。为了解调查地区人类 NTS 感染的患病率、血清型分布、危险因素和耐药性，对中国广州从化区住院患者进行了流行病学调查。共从住院患者 （每人 1 份） 中收集了 255 份粪便标本，并为每位参与者提供了一份问卷，并通过培养鉴定了 NTS 感染，并通过玻片凝集试验确认了血清型。观察到平均患病率为 20.39% （52/255），并确定了三个血清型 — 血清型 B （n = 46）、血清型 C1 （n = 4） 和血清型 D1 （n = 2）。其中，鼠伤寒沙门氏菌 （n = 39） 是最常见的血清型。观察到 <3 岁儿童的 NTS 感染患病率高于成人 （25.15% 对 4.65%，P = 0.006）;人工喂养儿童的患病率高于母乳喂养儿童 （30.77% vs 8.33%，P = 0.044）。抗菌素耐药性检测显示，大多数菌株对氨苄西林耐药 （92.16%），47.06% 的菌株对氨苄青霉素耐药。 因此，有必要持续监测和合理使用抗生素，这将有助于降低耐药菌株的流行。这些数据将有助于制定有效的控制策略来干预和预防沙门氏菌病的发生。

Introduction 介绍

Salmonella infection is a major public health concern worldwide, in both industrialized and developing countries, has contributed to an increased economic burden on the health systems. Non-typhoidal Salmonella (NTS) is a common cause of bacterial enteritis in humans, causing 93.8 million cases of gastroenteritis globally each year, with 155,000 deaths (Ngogo et al., 2020).
沙门氏菌感染是世界范围内的主要公共卫生问题，无论是在工业化国家还是发展中国家，都导致卫生系统的经济负担增加。非伤寒沙门氏菌 （NTS） 是人类细菌性肠炎的常见原因，全球每年导致 9380 万例胃肠炎病例，其中 155,000 人死亡（Ngogo 等 人，2020 年）。

NTS causes a disease characterized mainly by gastroenteritis, a localized infection of the terminal ileum and colon characterized by diarrhea, vomiting and abdominal cramps (Lokken et al., 2016). However, clinical signs and symptoms are variable depending on the health status of infected hosts, and the genetic background and infective doses of this pathogen (Blaser and Newman, 1982; Hu et al., 2021). Usually, asymptomatic infection, diarrhea and other common symptoms of gastroenteritis occurs in immunocompetent or healthy individuals while bacteremia or focal infections at systemic sites may occur in immunodeficient or immuno-compromised individuals, such as infants, the elderly, individuals undergoing cancer chemotherapy and those with underlying diseases (Lokken et al., 2016).
NTS 导致一种主要以胃肠炎为特征的疾病，这是一种以腹泻、呕吐和腹部绞痛为特征的末端回肠和结肠的局部感染（Lokken 等 人，2016 年）。然而，临床体征和症状是可变的，具体取决于受感染宿主的健康状况，以及这种病原体的遗传背景和感染剂量（Blaser 和 Newman，1982 年;胡 et al.， 2021）。通常，无症状感染、腹泻和其他胃肠炎的常见症状发生在免疫功能正常或健康的个体中，而全身部位的菌血症或局灶性感染可能发生在免疫缺陷或免疫功能低下的个体中，例如婴儿、老年人、接受癌症化疗的个体和患有潜在疾病的人（Lokken 等 人，2016 年）。

According to the White–Kauffmann–Le Minor scheme, Salmonella composed of over 2600 serotypes, where most (approximately 1600 serotypes) of the them belong to the subspecies enterica (Elnekave et al., 2020). Though many serotypes (more than 200) have been identified as capable agents of producing pathology in humans, Salmonella Enteritidis (S. Enteritidis) and Salmonella Typhimurium (S. Typhimurium) are the two most common serotypes causing human salmonellosis (Xue et al., 2021; Xu et al., 2021).
根据 White-Kauffmann-Le Minor 方案，沙门氏菌由 2600 多种血清型组成，其中大多数（约 1600 种血清型）属于肠道亚种（Elnekave等 人，2020 年）。尽管许多血清型（超过 200 种）已被确定为能够在人类中产生病理学的病原体，但肠炎沙门氏菌 （S. Enteritidis） 和鼠伤寒沙门氏菌 （S. Typhimurium） 是导致人类沙门氏菌病的两种最常见血清型（Xue et al.， 2021;Xu et al.， 2021）。

Salmonella has been found in a variety of hosts, including human and animals (such as reptiles, rodents, birds and amphibian). Therefore, infection can be acquired through close-contact with humans or animals infected with Salmonella. (Haeusler and Curtis, 2013). However, most human infections of Salmonella are considered to result from ingesting contaminated food or water. Salmonella is one of the major cause of foodborne illness worldwide, accounts for 80.3 million foodborne cases per year (Mukherjee et al., 2019). Live poultry, eggs, meat or meat products, and dairy products are recognized as one of the major sources of human salmonellosis (Wu et al., 2015). In fact, the risk of Salmonella infection is related to a variety of factors, such as different lifestyle, dietary habits and environmental condition. For people living in low-income countries, poor hygiene and lack of access to safe water and food are major cause of high infection rate of Salmonella (Galgallo et al., 2018); for people living in developed countries, the consumption of contaminated fresh fruits and vegetables, and meat are the main reason (Carstens et al., 2019).
沙门氏菌存在于多种宿主中，包括人类和动物（如爬行动物、啮齿动物、鸟类和两栖动物）。因此，可以通过密切接触感染沙门氏菌的人或动物而获得感染。（Haeusler 和 Curtis，2013 年）。然而，大多数人类感染沙门氏菌被认为是由摄入受污染的食物或水引起的。沙门氏菌是全球食源性疾病的主要原因之一，每年占 8030 万例食源性病例（Mukherjee 等 人，2019 年）。活禽、蛋类、肉类或肉制品以及乳制品被认为是人类沙门氏菌病的主要来源之一（Wu 等 人，2015 年）。事实上，沙门氏菌感染的风险与多种因素有关，例如不同的生活方式、饮食习惯和环境条件。对于生活在低收入国家的人们来说，卫生条件差和无法获得安全的水和食物是沙门氏菌感染率高的主要原因（Galgallo 等 人，2018 年）;对于生活在发达国家的人们来说，食用受污染的新鲜水果和蔬菜以及肉类是主要原因（Carstens 等 人，2019 年）。

Currently, worldwide surveillance data has demonstrated a noticeable increase in antibiotic resistance among NTS (Haeusler and Curtis, 2013). Occurrence of antibiotic-resistant NTS are hampering the use of conventional antibiotics, and associated with an increased risk of treatment failure (Su et al., 2004). Meanwhile, the spread of these resistant strains to other parts of the world could pose a major public health challenge, causing significant morbidity and even mortality. Therefore, it is necessary to understand the situation of Salmonella infection and drug-resistance in different areas, it will be helpful to guide the clinical rational use of drugs and curb the development of antibiotic resistance.
目前，全球监测数据表明 NTS 的抗生素耐药性显着增加（Haeusler 和 Curtis，2013 年）。抗生素耐药性 NTS 的发生阻碍了传统抗生素的使用，并且与治疗失败的风险增加有关（Su 等 人，2004 年）。同时，这些耐药菌株传播到世界其他地区可能构成重大公共卫生挑战，导致严重的发病率甚至死亡率。因此，有必要了解不同地区的沙门氏菌感染和耐药情况，将有助于指导临床合理使用药物，遏制抗生素耐药性的发展。

In China, since the first report of salmonellosis caused by Salmonella in humans in Hong Kong in 1977, this pathogen has been attracting increased attention (Chau and Huang, 1977). Guangzhou city is situated in the south of China and has a sub-tropical climate, the heat and heavy rainfall helps the spread of NTS (Guentchev et al., 2016; Milazzo et al., 2016; Kraay et al., 2020). Some studies have reported occurrence of NTS in Guangzhou. However, no reports about prevalence, serotype distribution and antibiotic susceptibility of NTS infection in humans in Conghua District, the largest administrative district of Guangzhou. Conghua District is a region whose economy is relatively backward, agriculture and tourism are important to its economy. According to the clinical results in recent years, it was shown that the prevalence peak of NTS infection occurred in summer or autumn in this area. Thus, a cross-sectional epidemiological survey of NTS was carried out to understand the status of NTS infection, distribution of various NTS serotypes and drug susceptibility in hospitalized patients in Conghua District by culture, serological experiments and antimicrobial susceptibility testing. Meanwhile, possible risk factors for NTS infection were assessed in the investigated areas. The finding from the present study may assist in setting appropriate measures for the prevention and control of salmonellosis, and to provide reference basis for clinical rational drug use.
在中国，自 1977 年香港首次报告沙门氏菌在人类中引起沙门氏菌病以来，这种病原体一直受到越来越多的关注（Chau 和 Huang，1977 年）。广州市位于中国南部，属亚热带气候，高温和强降雨有助于 NTS 的传播（Guentchev 等 人，2016 年;Milazzo et al.， 2016;Kraay et al.， 2020）。一些研究报道了广州市 NTS 的发生率。然而，在广州市最大的行政区从化区，没有关于人类 NTS 感染的患病率、血清型分布和抗生素敏感性的报道。从化区是一个经济相对落后的地区，农业和旅游业对其经济很重要。根据近年来的临床结果，NTS 感染的流行高峰出现在该地区的夏季或秋季。因此，开展了 NTS 横断面流行病学调查，通过培养、血清学实验和药敏试验等方式了解从化区住院患者的 NTS 感染状况、各种 NTS 血清型的分布和药物敏感性。同时，在调查区域评估了 NTS 感染的可能危险因素。本研究结果可能有助于制定适当的防控沙门氏菌病措施，并为临床合理用药提供参考依据。

Materials and Methods 材料和方法

Ethics Statement 道德声明

The present study was reviewed and approved by the Ethics Committee of the Fifth Affiliated Hospital of Southern Medical University. All study participants were informed about the study objectives and the procedures involved in study participation at enrollment. Prior to collection of fecal specimens, signed informed consents was obtained from each adult individual. Additionally, for minors under 18 years of age, a written consent form was signed by the parent or legal guardian.
本研究由南方医科大学第五附属医院伦理委员会审查批准。所有研究参与者在入组时都被告知研究目标和参与研究所涉及的程序。在收集粪便标本之前，从每个成年人那里获得了签署的知情同意书。此外，对于 18 岁以下的未成年人，父母或法定监护人应签署书面同意书。

Study Area 研究区域

Guangzhou is the capital city of Guangdong Province in the southern part of China with 11 regions (aka Districts), and has a population of over 18 million. Guangzhou has a subtropical marine monsoon climate. The annual average temperature is 21.5°C–22.2°C, with the lowest (averaging 9°C–16°C) in January and the highest (averaging 28.7°C) in July. The annual rainfall averages nearly 1800 millimeters. Our study was carried out in Conghua District (population over 0.71 million), which is located on the north-east of Guangzhou, with a total area of 1974.5 square kilometers, as the largest administrative district of Guangzhou (geographical coordinates: 23.22° N–23.56° N latitude, 113.17° E–114.04° E longitude).
广州是中国南部广东省的省会城市，拥有 11 个地区（又名区），人口超过 1800 万。广州属亚热带海洋性季风气候。年平均气温为 21.5°C-22.2°C，1 月最低（平均 9°C-16°C），7 月最高（平均 28.7°C）。年平均降