PREVALENCE, BIOTYPING, AND ANTIBIOTIC SUSCEPTIBILITY PROFILES OF AEROMONAS SPECIES ISOLATED FROM DIARRHOEAL PATIENTS IN SANA'A CITY, YEMEN 

Sami Sultan Ahmed Abdu1image, Sami Mohammed Abdo Hassan2image, Hassan Abdulwahab Al-Shamahy3*image, Ibrahim Mohammed Amed Nahshal3, Ibrahim Ali Al-Arashi4, Amirh Abdullah Sa'aed Aljabri5,

Ahmed Mohammed Al-Haddad6image, Naif Mohammed Al-Haidary7image

1Medical Microbiology and Clinical Immunology Department, Faculty of Medicine and Health Sciences, Sana’a University, Yemen. 2Medical Microbiology and Clinical Immunology Department, Faculty of Medical Sciences, Al-Nasser University, Yemen.

3Medical Microbiology and Clinical Immunology Department, Faculty of Medicine and Health Sciences, Sana’a University.

4Medical Microbiology and Clinical Immunology Department, Faculty of Health Sciences, Thamar University, Yemen.

5Medical Microbiology and Clinical Immunology Department, Faculty of Medical Sciences, Al-Nasser University, Yemen.

6Department of Medical Laboratories, College of Medicine and Health Sciences, Hadhramout University, Al-Mukalla, Yemen.

7Medical Microbiology and Clinical Immunology Department, Faculty of Medicine and Health Sciences, Sana’a University.

 

Abstract

Background and Aims: The genus Aeromonas is one of new and increasingly important bacterial genera which have been included as a cause of human gastritis.  The aims of the study include determination of the prevalence of Aeromonas species among diarrhoeal patients, as well as biotyping, and studying the antibiotic susceptibility of the isolates.

Methods: Initially patients suffering from diarrhoea were selected from patients who attended the main hospitals in Sana'a and sent to NCPHL for stool culture. A total of 1991 diarrheal stool specimens were collected during the period of two-year period (2023–2024). In order to identify Aeromonas the stool specimens were inoculated into alkaline peptone water, Aeromonas agar and TCBS agar, and then the isolates were identified by the relevant biochemical tests. 

Results:   Presents data on 1,991 diarrhea patients, predominantly children aged 2 months to 9 years (34.0%). There was a slight male predominance (52.9%). The mean age was 22.4 years, with a range of 2 months to 75 years. The leading bacterial causes were non-Salmonella typhoid serogroups (25.0%), Shigella serogroups (13.0%), and Vibrio cholerae (7.7%). Moderate to low prevalence included enteropathogenic E. coli (5.1%) and Aeromonas (1.9%). Resistance rates for Aeromonas were 100% for PG-penicillin, Ampicillin-sulbactam, Oxacillin, and Ampicillin, with high resistance to nalidixic acid (84.2%).

Conclusion:    Diarrheal illness in this study population heavily burdens young children and is primarily driven by non-Salmonella typhoid and Shigella serogroups. 

Keywords: Aeromonas, antibiotic susceptibility, diarrhea, gastritis, Yemen. 

INTRODUCTION

 

Members of the genus Aeromonas as human and animal pathogens have attracted a great deal of scholarly attention in the last ten years, and the number of scientific and medical publications on the genus has increased significantly1. The Gram-negative bacillus's link to human gastrointestinal disorders is mostly responsible for increased attention, but other areas of growing significance included the genus's complex taxonomy and virulence-related variables in infections in humans and animals2. Because there are few long-term investigations and it is difficult to distinguish between pathogenic and non-pathogenic strains, the involvement of Aeromonas species in bacterial gastroenteritis remains unclear3. There are two main types of serious human infections linked to Aeromonas. One of these is gastroenteritis, which primarily affects young children or the elderly, although it can also strike travellers and patients with weakened immune systems4,5. In addition to gastroenteritis, adults can get extra-intestinal infections. The Mesophile groups of motile Aeromonas species are considered to be potential human pathogens, but A. salmaonicida, the only member, which has not been recovered from humans6. Aeromonas species infections are contracted through ingestion, and in a few documented cases, refrozen or undercooked shellfish and oysters have been strongly suspected of causing food-borne gastroenteritis7. Additionally, contact of damaged skin or mucosal surfaces to contaminated water or soil can result in extraintestinal infections8. Due to years of civil conflict, widespread population displacement, economic collapse, and the deterioration of water, sanitation, and hygiene (WASH) infrastructures, Yemen is experiencing a serious public health crisis caused by bacterial and parasite illnesses9-14. These preventable and treatable diseases spread quickly, especially among vulnerable rural communities and internally displaced persons (IDP) camps, because less than half of the country's healthcare facilities are completely operational15,16.
 About 26% of Yemen's reported neglected infectious diseases are caused by bacterial infections, which are closely associated with tainted food and water sources9. Cholera epidemics in Yemen have historically been unusual12. The aims of the study include determination of the prevalence of Aeromonas species among diarrhoeal patients, as well as bio-typing, and studying the antibiotic susceptibility of the Aeromonas  isolates.

 

MATERIAL AND METHODS

 

Sample size and patient selection

Study population and sample size: A total of 1,991 patients presenting with diarrheal symptoms were enrolled in this study. The sample size reflects the total volume of symptomatic individuals who met the inclusion criteria during the designated study timeframe.

Selection criteria and study period

Participants were selected based on the following criteria: Patients presenting with acute or chronic diarrhea symptoms. Clinical cases were consecutively accumulated over a two-year period (from 1st January, 2022, to 31st December, 2023).

Study setting: The selection was restricted to patients who actively sought medical attention or were referred directly to the National Central Public Health Laboratory (NCPHL).

Fecal specimens: The stool specimens from selected diarrhoeal patients were collected according to the standard method of Bialy and Scott Diagnostic Microbiology17. Each stool specimen was collected in a sterile disposable 25 ml container.  Loose stools were collected only.  All stool specimens were transported within two hours of collection to the National Central Public Health Laboratory (NCPHL) for processing, culture and identification.  A transport medium (Cary-Blair) was used when stool specimens were not delivered within two hours to the National Central Public Health Laboratory (NCPHL).

Data collection:   A full history was taken from each patient.  The findings were recorded in a predesigned questionnaire which included sex, age, risk factors of contracting gastritis.

Culture and identification: All stool specimens were inoculated into alkaline peptone water, TCBS18 and Aeromonas agar then incubated aerobically at 37oC for 48 hours19. The suspected colonies then picked for bacterial identification by microscopy, Gram-stain reaction, and biochemical tests, and bio-typing was done by API.

Sensitivity test:  Stoke disc diffusion sensitivity test was used to test the isolates for 13 different antibiotics. Both the test and control (S. aureus NCTC6571) organisms were inoculated onto Muller Hinton agar (Oxoid), the same plate using an inoculum which gives semi confluent growth. This means that the activity of each disc is controlled, the inhibition zone size of the test organism can be compared directly with that of the control, and errors due to using too heavy or too light an inoculum would be detected.

 

RESULTS

 

Table 1 illustrates the distribution by age and gender of 1,991 patients suffering from diarrhoea who visited the central laboratory for stool culture testing in Sana'a, Yemen, over a two-year period (2023–2024). Regarding age distribution, children and young people constituted the majority of cases; the 2-month to 9-year age group recorded the highest prevalence, accounting for 34.0% (677 patients) of the total. As for gender distribution, a slightly higher proportion of males (52.9%) were observed compared to females (47.1%).

Analysis of the age statistics reveals a mean patient age of 22.4 years, with significant age variation (a standard deviation of 18.8 years); the most frequent age (mode) among patients seeking treatment was one year, while ages ranged from a minimum of two months to a maximum of 75 years. Table 2 shows that the most common cause of diarrhoea, in which parasitic causes were the most frequently isolated, accounted for 31.0% (617 cases) of the total. Considering the leading bacterial causes among the pathogenic bacteria, non-Salmonella typhoid serogroups were the most prevalent at 25.0% (498 cases), followed by Shigella serogroups at 13.0% (259 cases) and Vibrio cholerae at 7.7% (153 cases).  

Considering moderate to low prevalence: Entero-pathogenic E. coli serogroups made up 5.1% (101 cases), while Aeromonas species were found in 1.9% (38 cases) of patients. Considering rare pathogens, several organisms were extremely rare in this sample, each appearing in less than 1% of the cases. These include Campylobacter jejuni, Bacillus cereus, and Clostridium perfringens, which were each isolated in only 2 patients (0.1%). Furthermore, Other Isolates: Non-pathogenic bacterial isolates accounted for 13.1% (261 cases) of the total findings. Table 3 outlines the prevalence rate of different isolated Aeromonas species collected from 38 specimens of diarrheal patients. Aeromonas hydrophila is the most prevalent species found in the specimens, accounting for 17 cases (44.7%); Aeromonas sobria is the second most common species, closely following at 16 cases (42.1%); and Aeromonas caviae is the least prevalent species isolated, representing only 5 cases (13.2%). Table 4 displays the antibiotic susceptibility patterns of 38 Aeromonas species isolates collected from patients experiencing diarrhea in Sana’a, Yemen. It categorizes the bacteria's response to 13 different antibiotics into three levels: sensitivity, intermediate, and resistant, showing both the raw count and the percentage. The Aeromonas isolates showed 100% resistance (38 out of 38 isolates) to four specific antibiotics, including PG-penicillin, Ampicillin-sulbactam, Oxacillin, and Ampicillin. 

Several other antibiotics faced high rates of bacterial resistance, including nalidixic acid (84.2%, 32 isolates), ofloxacin (76.3%, 29 isolates), trimethoprim (57.9%, 22 isolates), and gentamicin (57.9%, 22 isolates). The antibiotics that successfully inhibited the highest percentage of isolates were chloramphenicol (60.5%, 23 isolates), nitrofurantoin (57.9% sensitive, 22 isolates), and cefotaxime (57.9% sensitive, 22 isolates). Ciprofloxacin showed a highly divided split, with 42.1% sensitivity, 28.9% intermediate, and 28.9% resistance. Gentamicin showed 57.9% resistance; the remaining 42.1% fell entirely into the intermediate category, leaving 0% fully sensitive. Clindamycin showed a relatively even spread across sensitivity (31.6%), intermediate (26.3%), and resistance (42.1%).

 

DISCUSSION

 

The findings of this study provide a detailed epidemiological insight into the etiology of diarrheal illness within the studied cohort. A striking observation is that parasitic pathogens emerged as the primary cause of diarrhea, accounting for 31.0% (617 cases) of the total sample. This exceptionally high burden of parasitic isolates highlights a significant public health concern. Globally, intestinal protozoa and helminths remain deeply endemic in areas constrained by poor sanitation infrastructure, compromised water safety, and inadequate personal hygiene. 

The predominant isolation of parasites over viral or bacterial agents in this study underscores the critical necessity for localized targeted interventions, such as enhanced water treatment systems and aggressive health sanitation campaigns15,16.

Among the pathogenic bacteria isolated, non-Salmonella typhoid serogroups were identified as the most prevalent bacterial etiology, comprising 25.0% (498 cases) of the sample. This high frequency indicates substantial fecal-oral contamination routes, likely tied to contaminated food or municipal water networks. Following closely, Shigella serogroups accounted for 13.0% (259 cases). This finding aligns robustly with global data, including the Global Burden of Diseases Study, which consistently positions Shigella as a leading bacterial driver of moderate-to-severe diarrheal morbidity and mortality worldwide, particularly due to its low infectious dose and high transmissibility. The detection of V. cholerae at 7.7% (153 cases) further signifies an active risk of acute secretory diarrheal outbreaks within the community, reinforcing the demand for rapid diagnostic tracking and immediate rehydration protocols9,20,21.

Pathogens exhibiting a moderate-to-low prevalence included Enteropathogenic E. coli (EPEC) serogroups (5.1%, 101 cases) and Aeromonas species (1.9%, 38 cases). EPEC pathotypes are well-documented contributors to persistent infantile and childhood diarrhoea via the disruption of intestinal microvilli. Meanwhile, Aeromonas species, though less frequently discussed, are increasingly recognized as opportunistic aquatic pathogens capable of inducing gastroenteritis following the consumption of untreated well water or contaminated seafood15,16.

Conversely, certain classic bacterial Enteropathogens were exceptionally rare in this population. Campylobacter jejuni, Bacillus cereus, and Clostridium perfringens were each isolated in a mere 0.1% (2 cases) of patients. While Campylobacter stands as a dominant cause of bacterial foodborne diarrhea in high-income, developed countries, its sparse distribution in this sample suggests variations in regional livestock exposure, dietary habits, or potential under-isolation due to strict microaerophilic culture requirements. The low incidence of B. cereus and C. perfringens indicates that acute, toxin-mediated food poisoning outbreaks were not the driving factor behind the steady burden of diarrheal presentations during the study period9,15,16.

Finally, non-diagnostic cases constituted 13.1% (261 cases) of the total findings. This subset represents instances where standard laboratory diagnostic workflows failed to identify a definitive pathogen. This diagnostic gap can reasonably be attributed to several factors: viral etiologies (such as Rotavirus or Norovirus) that may not have been screened for in the baseline panel, preceding self-medication with over-the-counter antimicrobials by patients prior to sample collection, or non-infectious causes of acute diarrhea such as dietary intolerances and functional bowel disorders. Implementing molecular multi-pathogen testing, such as multiplex polymerase chain reaction (PCR) assays, in future surveillance could significantly reduce this undiagnosed fraction and improve therapeutic precision15,16.

No surveys, have been performed in Yemen to determine the prevalence of Aeromonas species as a cause of diarrhoea, nor have any cases been reported. However, Aeromonas gastritis has been reported from areas in Europe, America, and Asia4,5,22.   This study has demonstrated that human gastritis due to Aeromonas species is currently 1.9% from Yemen, while in India the prevalence of Aeromonas was (3.1%)23, in Bangladesh 7%24, and in Africa 2.7%, in Latin America 1.8%, and 2.3% in Asia as whole2,3,22. The low rate in our study might be due the facts, First, Aeromonas species are significant pathogens of animals, and cause serious opportunistic infection only in immune-compromised individuals3,25.  The second point is that there is no association between Aeromonas species and gastroenteritis in Yemen because Aeromonas species  are found everywhere in the environment, so most people in Yemen may be immunized against Aeromonas species, due to the high frequency of exposure to these species resulting from poor environmental hygiene. This is converse of the situation in developed countries where it is less frequent, so that the chance to develop immunity among the general population against Aeromonas species is rare; most probably for this reason accidental exposure to Aeromonas species leads to clinical infections.  This hypothesis is supported by the findings of Kirov et al. and Jiang et al.25,26. A third key factor involves the bacteria themselves: identifying Aeromonas as a definitive cause of diarrhea is challenging because the genus is highly heterogeneous, and only specific subgroups may be pathogenic27. Furthermore, although various virulence factors have been identified in Aeromonas species such as enterotoxins, cytotoxins, hemolysins, aerolysins, proteases, hemagglutinins, and tissue-culture adherence or invasion capabilities a clear link between these factors and actual diarrheagenic ability remains unproven28,29.

The fourth point is related to the diagnostic method, since the ability of most commercial identification systems to accurately identify Aeromonas species to the species level is limited and uncertain, and some kits have trouble separating Aeromonas species from Vibrio species30,31. The fifth point is due to the unrecognized short-duration diarrhoea which is caused by Aeromonas species, and the quick recovery without antibiotics32,33.

Furthermore, the global clinical burden of Aeromonas in human gastroenteritis remains undefined. Nevertheless, its prevalence fluctuates geographically, peaking in areas with poor sanitation34-36. Diverse global literature reports Aeromonas species isolation rates ranging from 0.6% to 7.2% among diarrheal patients, with the highest frequency observed in pediatric populations37,38. Meanwhile, in North America and Europe, the bacterium is implicated in approximately 2% of traveler’s diarrhea cases39,40. By comparison, Aeromonas species represent the third most common cause of bacterial gastroenteritis among Spanish children, comprising 2.5 to 4% of diagnosed cases41-43. A similar incidence rate of 2.5% has been documented in American children suffering from diarrhea43. In the current study, Aeromonas spp. was detected in 0.61% of diarrheal stool samples. This finding aligns with earlier literature and reinforces the established understanding that in industrialized nations, Campylobacter species remain the dominant bacterial pathogens, accounting for 1.32% of the cases in this cohort44.

Aeromonas species were unexpectedly the second most frequent intestinal pathogen found in stool samples within our study, outnumbering Salmonella enterica (which stood at 0.46%). This highlights that Aeromonas species should be recognized as significant human intestinal pathogens, much like Campylobacter and Salmonella species. Furthermore, relying on traditional stool culture techniques without specific selective media may cause health professionals to underestimate how often this pathogen actually occurs, even in developed nations45. Aeromonas spp. infection was monomicrobial in most of our cases (93%). This contrasts with previous studies on traveler’s or children’s diarrhoea, which reported a higher prevalence of co-infections46 a discrepancy likely driven by differences in study populations. Because our survey avoids patient recruitment bias, it reveals a bimodal distribution: one peak in children under 15 years old and a second, substantial peak in individuals over 45. Consistent with prior literature, 30% of the patients in our cohort were infants and children40.

The findings of this study outline a highly concerning antibiotic susceptibility profile among the 38 Aeromonas species isolates retrieved from diarrheic patients in Sana’a, Yemen. The absolute resistance (100%) observed against ampicillin, ampicillin-sulbactam, oxacillin, and penicillin G aligns closely with established microbiological paradigms. Virtually all Aeromonas species naturally harbor chromosomal beta-lactamase genes, including classical penicillinases and cephalosporinases, which render standard and inhibitor-assisted penicillins therapeutically useless47.

A critical concern raised by these results is the high level of resistance to nalidixic acid (84.2%) and ofloxacin (76.3%), alongside an unstable split in susceptibility to ciprofloxacin (42.1% sensitive, 28.9% intermediate, 28.9% resistant). Fluoroquinolones have historically served as the cornerstone empirical therapy for severe, persistent gastroenteritis caused by Gram-negative pathogens like Aeromonas. The severe drop in ciprofloxacin efficacy, alongside the failure of earlier-generation quinolones, signals a profound shift. This shift points to the rapid acquisition of target-site mutations (such as in the gyrA or parC genes) or plasmid-mediated quinolone resistance (PMQR) factors. This alarming pattern restricts oral outpatient treatment choices for severe cases in the region47.

The 57.9% resistance rate observed for both trimethoprim and gentamicin further highlights a multidrug-resistance (MDR) crisis in Yemen49-51. In Yemen, public health infrastructure challenges combined with easy, unregulated access to over-the-counter medications have historically driven the overuse of broad-spectrum agents like trimethoprim-sulfamethoxazole. While aminoglycosides like gentamicin are normally reserved for systemic or severe infections, the 0% full sensitivity noted in this cohort where the remaining 42.1% of isolates fell entirely into the intermediate range suggests widespread adaptation to aminoglycoside-modifying enzymes49,50-54. Conversely, chloramphenicol (60.5% sensitive), nitrofurantoin (57.9% sensitive), and cefotaxime (57.9% sensitive) achieved the highest rates of bacterial inhibition. The relative efficacy of chloramphenicol and nitrofurantoin may stem from their less frequent use in routine diarrheal management due to toxicity concerns and localized prescription habits54. The 57.9% sensitivity to cefotaxime indicates that a narrow majority of strains remain vulnerable to third-generation cephalosporins. However, the remaining resistant fraction indicates the encroaching presence of extended-spectrum beta-lactamases (ESBLs) or AmpC overproduction within the local microbial reservoir54. Ultimately, the diverse responses seen across antibiotics like clindamycin (31.6% sensitive, 26.3% intermediate, 42.1% resistant) reflect an increasingly unpredictable resistance landscape. These dynamics necessitate rapid diagnostic profiling and stringent antibiotic stewardship policies across clinical centers in Sana'a to preserve the few remaining viable therapies53,54.

Limitations of the study

First, there is a geographical bias; although the study claims to address the situation in Yemen comprehend-sively, the selection of patients was limited exclusively to major hospitals in Sana'a. A second limitation stems from the study’s “cross-sectional” design and its reliance on a single center as sample collection was confined to one urban hub or specific medical facility which may fail to account for seasonal variations or population dynamics in rural regions across Yemen.

 

CONCLUSIONS

 

In conclusion, diarrheal disease primarily affects young children (aged two months to nine years), although it impacts a broad age range, extending up to 75 years. Non-typhoidal Salmonella and Shigella serogroups are the most significant bacterial causes of diarrhea identified in this study, followed by V. cholerae. Aeromonas species, while less frequent, exhibit high levels of drug resistance; they show complete (100%) resistance to common antibiotics such as penicillin, ampicillin-sulbactam, oxacillin, and ampicillin as well as high resistance to nalidixic acid. The use of beta-lactam antibiotics and fluoroquinolones (e.g., ciprofloxacin) should be avoided in treating Aeromonas infections, given their variable susceptibility profiles. 

 

ACKNOWLEDGEMENTS

 

The authors express their gratitude to The National Centre of Public Health Laboratories (NCPHL), Sana'a, Yemen for their kind assistance.

 

 

AUTHOR’S CONTRIBUTIONS

 

Abdu SSA: formal analysis, conceptualisation, data organisation, writing original draft. Hassan SMA: data analysis, manuscript writing.  Al-Shamahy HA: data analysis, manuscript writing. Nahshal IMA: literature survey. Al-Arashi IA: critical review. Aljabri AAS: data analysis, manuscript writing. Al-Haddad AM: critical review, editing. Al-Haidary NM: literature survey, editing.   Final manuscript was checked and approved by all authors. 

 

DATA AVILIABILITY

 

The data will be available to anyone upon request from the corresponding author.

 

CONFLICT OF INTEREST

 

None to declare.

 

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