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Rossi, F.; Santonicola, S.; Amadoro, C.; Marino, L.; Colavita, G. Bacterial Opportunistic Infections via the Dietary Route. Encyclopedia. Available online: https://encyclopedia.pub/entry/53616 (accessed on 25 June 2024).
Rossi F, Santonicola S, Amadoro C, Marino L, Colavita G. Bacterial Opportunistic Infections via the Dietary Route. Encyclopedia. Available at: https://encyclopedia.pub/entry/53616. Accessed June 25, 2024.
Rossi, Franca, Serena Santonicola, Carmela Amadoro, Lucio Marino, Giampaolo Colavita. "Bacterial Opportunistic Infections via the Dietary Route" Encyclopedia, https://encyclopedia.pub/entry/53616 (accessed June 25, 2024).
Rossi, F., Santonicola, S., Amadoro, C., Marino, L., & Colavita, G. (2024, January 09). Bacterial Opportunistic Infections via the Dietary Route. In Encyclopedia. https://encyclopedia.pub/entry/53616
Rossi, Franca, et al. "Bacterial Opportunistic Infections via the Dietary Route." Encyclopedia. Web. 09 January, 2024.
Bacterial Opportunistic Infections via the Dietary Route
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Different bacterial groups present in food or drinking water, other than the major pathogens which are objects of specific surveillance and control measures according to food legislation norms, may behave as opportunistic pathogens in people with underlying conditions or predisposing factors. These belong to bacterial genera or species that cause mild or no illness in immunocompetent persons but can cause life-threatening infections in vulnerable subjects. As an example, lactobacilli, which are essential for food fermentation and probiotics with in vivo proven beneficial effects, were the cause of bacteremia, endocarditis, and other localized infections most often in immunocompromised, diabetic persons, or patients with a history of predisposing events such as medical interventions, diseases, or oral infections and dental procedures. The bacterial groups involved in opportunistic infections, the illnesses caused and sources of infection are described below.

dietary route bacteria opportunistic pathogens recent infection records risk factors

1. Aeromonas spp.

The genus Aeromonas comprises Gram-negative gas-producing bacilli belonging to the class Gammaproteobacteria, classified in 36 species. Among these, Aeromonas hydrophila, A. caviae, A. dhakensis, A. veronii, A. salmonicida, and A. sobria are known to cause human infections mainly in the form of mild gastroenteritis [1][2]. These bacteria can be isolated from fresh water and sea water, soil, fish, meat, and other foods. The major virulence factors of Aeromonas spp. are hemolysins, enterotoxins, invasins, aerolysin, adhesins, proteases, phospholipase, and lipase [1].
A. sobria may act as an opportunistic pathogen and cause bacteremia, intestinal, and extraintestinal infections predominantly in patients with chronic hepatic disease, gastroenteritis, malignancy, and an immunocompromised status. Gastroenteritis is the most common infection caused by Aeromonas spp., but peritonitis is not uncommon, especially in patients with cirrhosis [1].
A. sobria caused peritonitis in a 37-year-old man affected by renal failure and under peritoneal dialysis (PD). He was admitted to the hospital with a fever, vomiting, abdominal pain, diarrhea, and cloudy dialysate several hours after eating stinky tofu. Stinky tofu, a kind of traditional Chinese food, is usually considered unhygienic for the particular production process in which the tofu is placed in water for a long time to increase the unique smell. Therefore, it was speculated that the stinky tofu was the source of infection in this case. Bacterial translocation through the intestinal barrier plays an important role in the pathogenesis of PD-related peritonitis. Amikacin and levofloxacin treatment allowed for the patient to recover [1].
A. hydrophila causes acute gastroenteritis or diarrhea most often through the ingestion of infected fish and seafood with an incubation period of less than 24 h. A case of gastroenteritis complication involved a 74-year-old woman admitted to the hospital with worsening epigastric pain, vomiting, and diarrhea that started 3 days previously after eating raw ayu fish. Her husband also had eaten the fish and was affected by mild diarrhea. The woman, who did not present underlying conditions and was not a smoker or alcohol consumer, presented mild renal failure and sepsis. Abdominal computed tomography (CT) revealed branched portal vein gas in the right hepatic lobes and a thickened gastric wall and intestinal edema. A submucosal tumor-like elevation in the posterior wall of the gastric corpus, which contained an ulcer at the center of the lesion, was revealed through digestive endoscopy. A. hydrophila was isolated from the stool and identified using microbial identification techniques so the diagnosis was of phlegmonous gastritis caused by A. hydrophila with a hepatic venous pressure gradient (HPVG) and without necrosis of the intestinal tract. After treatment with levofloxacin, then switched to cefmetazole, the symptoms gradually improved. In this case, the predisposing factor for the A. hydrophila infection presentation was most probably the presence of an ulcer lesion in the stomach that favored the invasion of the gastric wall and phlegmon formation [3].

2. Acinetobacter spp.

The genus Acinetobacter currently comprises approx. 80 species of strictly aerobic Gram-negative coccobacilli [4]. A. baumannii is the species most often involved in infections, but also cases attributed to A. calcoaceticus, A. lwoffii, A. haemolyticus, A. johnsonii, A. junii, A. nosocomialis, A. pittii, A. bereziniae, A. serfertii, A. schindleri, and A. ursingii were described. The community-acquired infections reported for A. baumannii include respiratory infections in children, immunocompromised individuals, and patients with risk factors such as alcoholism, smoking, and diabetes mellitus as underlying conditions [5].
The presence of this genus, mainly represented by the species A. baumannii, A. calcoaceticus, and A. lowfii, in milk, even pasteurized, dairy products, bacon, eggs, chicken, fish, fresh meat, fresh fruits, and produce is well established based on reports from different countries [4][6][7]. In the latter food category, these bacteria may persist after mild disinfection with vinegar or hypochlorite [7]. Moreover, A. lwoffii and A. johnsonii can survive in a wide range of temperatures, low pH values, and are resistant to disinfectants, irradiation, and desiccation [6].
However, the relevance of A. baumannii as an opportunistic pathogen is mainly attributable to nosocomial infections that can be transmitted from one patient to another as a consequence of environmental contamination transferred to medical devices, such as tubes and catheters, as observed in COVID-19 patients [5][8].
A. baumannii carbapenem resistant variants (CRAB) emerge in contexts with a high antibiotic pressure and an underregulated usage of antibiotics [9], which represent the most relevant concern posed by this bacterial species. This is among the six “ESKAPE” pathogens (Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter species), whose multi-drug resistance and ability to escape antimicrobial treatments make them responsible for the majority of nosocomial infections with a high mortality rate [10]. However, in clinical settings, the origin of the bacterium has remained unknown in many cases [5].
Hospital-acquired Acinetobacter infections may occur in patients with malignancies, patients in intensive care units (ICU) and burn units, and patients who have undergone major surgical procedures, are neutropenic, or have underlying chronic diseases such as diabetes mellitus and chronic pulmonary diseases [11]. These infections include bacteremia, meningitis, pneumonia, and other infections such as central nervous system infections after neurosurgery. Colistin sulfate, a derivative of polymyxin E, is the last resort drug for treating CRAB infections [12]. The viable but not culturable (VBNC) state was proposed as a persistence mechanism allowing A. baumannii for coping with environmental stresses [13].
An outbreak of A. baumannii infections that occurred through ingestion was reported in mechanically ventilated patients in an emergency ICU who received oral care after drinking water from contaminated taps [14].
Recent reports on the direct involvement of the dietary route in the transmission of Acinetobacter spp. are lacking and one retrieved report was published in 2009 [6]. The case regarded the gastrointestinal symptoms and bacteremia caused by A. lwoffii in a previously healthy 64-year-old man who had dined in two different restaurants the day before hospitalization. The absence of a catheter line, which is usual in Acinetobacter spp. infections, led the researchers to suspect food as source of the infectious agent.

3. Arcobacter spp.

Arcobacter spp. is a genus of aerotolerant, Gram-negative bacteria of the class Epislonproteobacteria and the family Campylobacteraceae that can grow at temperatures higher than 30 °C and comprises more than 30 known species. Four of these have been reported to infect humans, namely Arcobacter butzleri, A. cryaerophilus, A. skirrowii, and A. thereius [15][16].
A. butzleri was first isolated in aborted bovine fetuses and was later linked to reproductive disorders and late-term abortions in cattle, pigs, and sheep. It can be present in a range of commonly consumed meat products [17] and bovine milk [18].
Arcobacter spp. was indicated by the European Food Safety Authority (EFSA) as “an issue that deserves further attention in terms of the burden of disease as it is most probably underreported”. It was mentioned for the first time in 2021 by the International Health Intelligence (IHI) platform for a prevalence study in bivalve mollusks carried out in Sardinia, Italy [19]. An infection cluster involved eight patients treated for acute diarrhea in a tertiary hospital in Cantabria, Northern Spain. The Arcobacter infection originated from different sources since the patients belonged to three categories, namely elderly persons, persons recently returned from journeys abroad, and persons with comorbidities. Fingerprinting methods indicated no clonal relationships among the isolates, which were all identified as A. butzleri. In this research, the possible dietary sources for A. butzleri were not investigated but the AR profiles were obtained, which indicated a resistance to cefazolin for all eight isolates. A resistance to amoxicillin–clavulanic acid and tetracycline was observed for five and four isolates, respectively [16].
Several sporadic outbreaks of A. butzleri gastroenteritis were observed in the U.S., Europe, and South Africa in the years 1990 to 2000. A. butzleri was identified as a causative organism for 24 out of 4636 cases of gastroenteritis in a prospective study in Germany, while several studies have identified A. butzleri to be among the most frequently isolated Campylobacteraceae in human clinical samples [15][17]. Persistent watery diarrhea is the main symptom of Arcobacter spp. infection, though bacteremia and septicemia were also reported. The prevalence of this emerging pathogen is not well documented due to the difficulty of its identification in clinical settings [15].
According to a phylogenetic analysis of the isolates from Thailand, the A. butzleri STs were defined by sequencing seven housekeeping genes, aspA, atpA, glnA, gltA, glyA, pgm, and tkt. Those that are more often involved in human infections are ST94 and ST166, which have been found in both human diarrheal stool samples and chicken offal or meat samples [20].
A case of pericarditis caused by Arcobacter spp. was reported for a 32-year-old male with a past medical history of well-controlled human immunodeficiency virus (HIV), antiviral therapy, and end-stage renal disease (ESRD) admitted to internal medicine for COVID-19 pneumonia. This patient presented worsening cardiac tamponade that was successfully managed with urgent pericardiocentesis, steroids, antibiotics, and pericardial drain. The patient reported that, about a month earlier, he had several episodes of diarrhea after consuming chicken from a local restaurant. The cultures of pericardial fluid and blood on aerobic blood agar were positive for Gram-negative rods identified by VITEK 2 as Arcobacter species. This case highlighted that COVID-19 infection can increase the risk and severity of secondary bacterial infections by damaging the respiratory tract and compromising the immune system [15].
A 38-year-old man with a history of HIV infection arrived at the hospital with symptoms of acute watery diarrhea lasting for two weeks. There was no recent travel history or intake of raw or uncooked food. The stool cultures were positive for A. butzleri. The infection was successfully treated with ciprofloxacin but, unfortunately, the patient passed away due to hospital-acquired severe pneumonia. The authors concluded that clinicians should recognize the pathogenicity of A. butzleri in immunocompromised hosts [17].

References

  1. Song, P.; Deng, J.; Hou, T.; Fu, X.; Zhang, L.; Sun, L.; Liu, Y. Aeromonas sobria peritonitis in a peritoneal dialysis (PD) patient: A case report and review of the literature. BMC Nephrol. 2019, 20, 180.
  2. Fernández-Bravo, A.; Figueras, M.J. An Update on the Genus Aeromonas: Taxonomy, Epidemiology, and Pathogenicity. Microorganisms 2020, 8, 129.
  3. Yasuda, T.; Yagi, N.; Nakahata, Y.; Kurobe, T.; Yasuda, Y.; Omatsu, T.; Obora, A.; Kojima, T. A case of phlegmonous gastritis with hepatic portal venous gas caused by Aeromonas hydrophila successfully treated with medication. Clin. J. Gastroenterol. 2020, 13, 281–286.
  4. Franco Abuín, C.M.; Calleja, C.A.; Escámez, P.F.; Moreno, V.; Arribas Moragas, G.S.; Díaz, A.V. Report of the Scientific Committee of the Spanish Agency for Food Safety and Nutrition (AESAN) on the prospection of biological hazards of interest in food safety in Spain. Food Risk Assess Eur. 2023, 1, 0003E.
  5. Malta, R.C.R.; de Paiva Anciens Ramos, G.L.; Nascimento, J.D.S. From Food to Hospital: We Need to Talk about Acinetobacter Spp. Germs 2020, 10, 210–217.
  6. Regalado, N.G.; Martin, G.; Antony, S.J. Acinetobacter lwoffii: Bacteremia Associated with Acute Gastroenteritis. Travel Med. Infect. Dis. 2009, 7, 316–317.
  7. Carvalheira, A.; Silva, J.; Teixeira, P. Acinetobacter Spp. in Food and Drinking Water—A Review. Food Microbiol. 2021, 95, 103675.
  8. Russo, A.; Gavaruzzi, F.; Ceccarelli, G.; Borrazzo, C.; Oliva, A.; Alessandri, F.; Magnanimi, E.; Pugliese, F.; Venditti, M. Multidrug-resistant Acinetobacter baumannii inections in COVID-19 patients hospitalized in intensive care unit. Infection 2022, 50, 83–92.
  9. Elwakil, W.H.; Rizk, S.S.; El-Halawany, A.M.; Rateb, M.E.; Attia, A.S. Multidrug-Resistant Acinetobacter baumannii Infections in the United Kingdom versus Egypt: Trends and Potential Natural Products Solutions. Antibiotics 2023, 12, 77.
  10. Rice, L.B. Federal Funding for the Study of Antimicrobial Resistance in Nosocomial Pathogens: No ESKAPE. J. Infect. Dis. 2008, 197, 1079–1081.
  11. Ayoub Moubareck, C.; Hammoudi Halat, D. Insights into Acinetobacter baumannii: A Review of Microbiological, Virulence, and Resistance Traits in a Threatening Nosocomial Pathogen. Antibiotics 2020, 9, 119.
  12. Yang, X.; Guo, C.; Wu, G.; Zhao, K.; Xiang, D.; Xu, D.; Liu, D.; He, Y. Treatment of Central Nervous System Infection Caused by Multidrug-Resistant Acinetobacter baumannii with Intravenous and Intraventricular Colistin Sulfate: A Case Report and Literature Review. Infect. Drug Resist. 2023, 16, 6029–6038.
  13. König, P.; Wilhelm, A.; Schaudinn, C.; Poehlein, A.; Daniel, R.; Widera, M.; Averhoff, B.; Müller, V. The VBNC State: A Fundamental Survival Strategy of Acinetobacter baumannii. MBio 2023, 14, e0213923.
  14. Umezawa, K.; Asai, S.; Ohshima, T.; Iwashita, H.; Ohashi, M.; Sasaki, M.; Kaneko, A.; Inokuchi, S.; Miyachi, H. Outbreak of Drug-Resistant Acinetobacter baumannii ST219 Caused by Oral Care Using Tap Water from Contaminated Hand Hygiene Sinks as a Reservoir. Am. J. Infect. Control 2015, 43, 1249–1251.
  15. Rathore, A.; Patel, F.; Gupta, N.; Asiimwe, D.D.; Rollini, F.; Ravi, M. First case of Arcobacter species isolated in pericardial fluid in an HIV and COVID-19 patient with worsening cardiac tamponade. IDCases 2023, 32, e01771.
  16. Ruiz de Alegría Puig, C.; Fernández Martínez, M.; Pablo Marcos, D.; Agüero Balbín, J.; Calvo Montes, J. Outbreak of Arcobacter butzleri? An Emerging Enteropathogen. Enferm. Infecc. Microbiol. Clin. 2023, 41, 169–172.
  17. Tan, T.H.Y.; Tham, S.M.; Tambyah, P.A. Arcobacter butzleri in an AIDS Patient. Case Rep. Infect. Dis. 2022, 2022, 6983094.
  18. Caruso, M.; Latorre, L.; Santagada, G.; Fraccalvieri, R.; Difato, L.M.; Miccolupo, A.; Capozzi, L.; Bonerba, E.; Mottola, A.; Parisi, A. Arcobacter Spp. in Bovine Milk: An Emerging Pathogen with Potential Zoonotic Risk. Ital. J. Food Saf. 2018, 7, 7685.
  19. Gkrintzali, G.; Georgiev, G.; Garcia Matas, R.; Maggiore, A.; Merten, C.; Rortais, A.; Giarnecchia, R.; Robinson, T.; Bottex, B. Technical report on EFSA’s activities on emerging risks in 2021. EFSA Support. Publ. 2023, 20, 8233E.
  20. Kietsiri, P.; Muangnapoh, C.; Lurchachaiwong, W.; Lertsethtakarn, P.; Bodhidatta, L.; Suthienkul, O.; Waters, N.C.; Demons, S.T.; Vesely, B.A. Characterization of Arcobacter Spp. Isolated from Human Diarrheal, Non-Diarrheal and Food Samples in Thailand. PLoS ONE 2021, 16, e0246598.
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