Infection with Gram-negative Bacteria among Children at a Tertiary Hospital in Jeddah, Saudi Arabia

   Abstract 


Resistant Gram-negative bacteria (GNB) constitute a severe threat to public health by becoming increasingly prevalent worldwide; they are challenging to treat and highly adaptive pathogens that develop resistance to antibiotics through several mechanisms with high morbidity and mortality rates. This study aimed to determine the incidence and outcome of children with GNB infections at a tertiary hospital in Jeddah, Saudi Arabia. A retrospective cohort study was done in 2019 on a total of 278 patients aged from one month to 16 years. Data were collected from patient medical records by using a data collection sheet without exclusion criteria. Among patients with GNB, more than half were males with 57.9% (161), while 42.1% (117) were females. However, the most GNB isolated were Staphylococcus in 31.7% (88) of the patient then Klebsiella in 18% (50). Organisms isolated from urine were 46.1% (117), which was the primary site of isolation, where blood was 26.6% (74). About 20.1% (56) were primarily diagnosed with sepsis. The length of stay was around one month or less, with more than half of patients 56.5% (157). The mortality rate was 9.4% (26/278). A patient between one and 5 years of age was the most age affected by multidrug-resistant (MDR) (11/16). No statistically significant differences were observed between the MDR and non-MDR patients with GNB infections concerning age, length of stay, and mortality rate. Conversely, there were statistically significant differences in primary diagnosis, isolated organisms, and site of isolation with MDR and non-MDR. Staphylococcus and Klebsiella were the most abundant GNB, and the mortality rate was 9.4%. However, additional studies in other settings with a larger sample size are needed to compare between different healthcare facilities.

How to cite this article:
Bamshmous Y, Alwagdani S, Albarakati M, Alkouwait M, AlThwebi S. Infection with Gram-negative Bacteria among Children at a Tertiary Hospital in Jeddah, Saudi Arabia. Saudi J Kidney Dis Transpl 2021;32:1593-9
How to cite this URL:
Bamshmous Y, Alwagdani S, Albarakati M, Alkouwait M, AlThwebi S. Infection with Gram-negative Bacteria among Children at a Tertiary Hospital in Jeddah, Saudi Arabia. Saudi J Kidney Dis Transpl [serial online] 2021 [cited 2022 Aug 10];32:1593-9. Available from: 
https://www.sjkdt.org/text.asp?2021/32/6/1593/352420    Introduction Top

Resistant Gram-negative bacteria (GNB) constitute a severe threat to public health by becoming increasingly prevalent all over the world; they are challenging to treat and highly adaptive pathogens that develop resistance to antibiotics through several mechanisms with high morbidity and mortality rates.[1] Sepsis is defined as a life-threatening organ dysfunction caused by a dysregulated host response to infection, leading to morbidity and mortality in children worldwide.[2],[3] The most common resistance mechanism for these bacteria is the production of beta-lactamases that hydrolyze the beta-lactam ring in beta-lactam antibiotics.[1] The multiresistant GNB frequency of both community and hospital-acquired varying by the type of medical device and region.[4] They can cause infections throughout the body. Common infection sites include the lungs, urinary tract, bloodstream, nervous system, and soft tissues. Surgical wounds can also become infected with GNB.[5] The most GNB and the infections they cause include: Escherichia coli: food poisoning, urinary tract infections (UTIs), gastroenteritis, and newborn meningitis, Pseudomonas aeruginosa: lung and UTIs, Klebsiella: meningitis, and lung, urinary tract, and bloodstream infections, Acinetobacter baumannii: several types of infections in wounded soldiers, Neisseria gonorrhoeae: a sexually transmitted disease, Enterobacteriaceae: urinary tract, lung, and bloodstream infections, and food poisoning (includes carbapenem-resistant Enterobacteria-ceae, which are very resistant to antibiotics).[5]

A prospective study was done on 158 neonates in Yemen, aged from 0 to 28 days. The study showed that GNB was the most frequent causative agent of bacterial sepsis. The Klebsiella pneumonia was the predominant organism (36.7%).[6]

Another prospective observational study was done in 2017, conducted on two pediatric intensive care units (PICUs) at Cairo University Hospitals to determine the incidence and outcome of GNB infections over one year on 1420 patients aged from 22 to 80 months, 291 developed GNB infections. Organisms were isolated from blood in the majority (86.6%) of patients, with Klebsiella (36.0%) being the most frequently isolated organism. Among patients with GNB infection, 235 patients, one had a multidrug-resistant (MDR) infection. The mortality rate was 37.1%.[7]

Another retrospective study performed between 2012 and 2017 in Turkey had a total of 302 patients with gram-negative bacteremia (90.7%) or meningitis (9.3%). Klebsiella spp. was the most frequent causative agent (39.4%) followed by E. coli (22.2%), Acinetobacter spp. (13.9%), Pseudomonas spp. (13.6%), and Enterobacter spp. (10.9%). In total, 115 isolates (38.1%) were MDR, 63 (20.9%) were extensively drug-resistant and 6 (2.0%) were pandrug-resistant.[8]

A cross-sectional survey was performed between 2014 and 2017 using electronic data on neonatology intensive care unit (NICU) and PICU patients in Brazil, included between (0 and 18) years. A total of 10,210 MDR bacteria cases, including 9261 colonizations and 949 infections, were reported. ESBL producing Klebsiella spp. and E. coli were the most reported colonization-causing agents in NICUs (36.9%) and PICUs (38.5%). The main causing bacteria reported in catheter-associated bloodstream infection, ventilator-associated pneumonia, and catheter-associated UTI in NICUs were Klebsiella spp. and E. coli (35.9%), carbapenem-resistant GNB (CRGNB) (33.9%), and CRGNB (30.6%) respectively, while in PICUs, they were Methicillin-resistant Staphylococcus aureus (31.4%), CRGNB (57.4%), Klebsiella spp. and E. coli (34.6%), respectively.[9]

There was a study in Cairo conducted on 86 pediatric patients; their age ranged from one to 156 months. They found that gram harmful bacteria were the most common group, while Staphylococcus was the most common micro-organism.[10]

There were not enough studies in Saudi Arabia about the incidence and outcome of infection among hospitalized patients with GNB. This study aimed to determine the incidence and outcome of children with GNB infections at a tertiary hospital in Jeddah, Saudi Arabia.

   Methods Top

This study aimed to determine the incidence and outcome of children with GNB infections at a tertiary hospital in Jeddah, Saudi Arabia. A noninterventional retrospective cohort study was done in 2019 on a total of 278 patients aged from one month to 16 years with GNB infection without exclusion criteria. Data have been collected from patients’ medical records kept confidential which include age, gender, length of hospitalization, mortality rate, primary diagnosis, site of isolation, isolated organisms, MDR, non-MDR, and antibiotic that was given. Data entered using Microsoft Excel and IBM SPSS Statistics version 21.0 (IBM Corp., Armonk, NY, USA) was used for statistical analysis.

   Results Top

This study aimed to determine the incidence and outcome of children with GNB infections at a tertiary hospital in Jeddah, Saudi Arabia. Around 278 children who included in this study were between one month and 16 years old. Most of them (70.5%, 196) were one to five years old. More than half were males with 57.9% (161), while 42.1% (117) were females.

The most recurrent Gram-negative organisms were Staphylococcus in 31.7% (88) then Klebsiella 18% (50). Organisms isolated from urine were 46.1% (117), which was the primary site of isolation, where blood was 26.6% (74). 20.1% (56) were primary diagnosed with sepsis. The length of stay was around one month or less, with more than half of patients, 56.5% (157), where only 30.9% (86) stayed for more than one month. The mortality rate was 9.4% (26/278) [Table 1]. Further, Staphylococcus was appearing as the most GNB organism in the one- to five-year-old patients [Table 2].


Table 1. Clinical characteristics of the enrolled Gram-negative bacteria patients at King Abdulaziz University Hospital in Jeddah (n=278).

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In [Table 3], the antibiotic susceptibility pattern to the most abundant GNB, there were about 34 with E. coli infection, 33 with Klebsiella, and 27 with Staphylococcus. Mainly, patients with Staphylococcus infection, 47 out of 88 received glycopeptide. Aminoglycoside given to (42/50) patients with Klebsiella infection (37/40) with E. coli and (23/26) with Pseudomonas infection. There statistically were significant differences between the isolated organism and the antibiotic used except with tetracycline and quinolone (P = 0.97 and 49), respectively.


Table 3. Antibiotic susceptibility pattern of the most abundant Gram-negative isolates.
E. coli: Escherichia coli, H. influenzae: Haemophilus influenzae, M. morgani: Morganella morgana.

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The most affected age by MDR was between one and five years of age (11/16). Staphylococcus was the more abundant in the non-MDR patient than from MDR patients (86/278).

Further, Klebsiella was more in non-MDR than MDR (47/278). No statistically significant differences were observed between the MDR and non-MDR patients with GNB infections concerning age, LOS, and mortality rate. Conversely, there were statistically significant differences in primary diagnosis, isolated organisms, and site of isolation with MDR and non-MDR [Table 4].


Table 4. Demographic data, clinical characteristics and outcome of multidrug-resistant and nonmultidrug-resistant patients at King Abdulaziz University Hospital in Jeddah (n=278).

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In summary, we found the incidence of Staphylococcus and Klebsiella more in children aged from one to five years. The mortality rate was 9.4%.

   Discussion Top

This study aimed to determine the incidence and outcome of children with GNB infections, including both MDR and non-MDR patients. Our result showed that Staphylococcus spp. was the most common GNB compared to another similar review from eight Arab countries on 2308 newborns with sepsis revealed that in Saudi Arabia, Bahrain, and Kuwait, the Gram-positive microorganisms, coagulase-negative staphylococci, and S. aureus were taking the lead (64–75%).[11] This finding was similar to those of a study conducted among 586 patients with GNB in Nigeria, which S. aureus, E. coli, and Klebsiella pneumonia.[12]

Another study was done in Cairo University Children’s Hospital conducted on 291/1420 who developed GNB infections in PICU. The mortality rate in their study was 37.1% higher than our result which was 9.4% (26/278). Furthermore, their organisms were isolated from blood in the majority (86.6%) of their patients but in our study was isolated more from a urine culture, 46.1% (117) than blood 26.6% (74), and Klebsiella being the most frequently isolated organism (36.0%). However, the most GNB isolated in our study were staphylococcus 31.7% (88/278) then Klebsiella 18% (50/278). Their study revealed that the mortality rate was 37.4%, which was markedly higher than that was found in our study (9.4%).[7]

A retrospective study was carried out of GNB isolates from the 800 adults in ICU at King Fahad National Guard Hospital (KFNGH) between 2004 and 2009. The most frequently isolated organism was A. baumannii (31.7%), followed by Pseudomonas aeruginosa, E. coli, Klebsiella pneumonia, Stenotrophomonas maltophilia, and Enterobacter.[13] Conversely, in our study A. baumannii was (1.8%). In our study, the more frequent diagnosis was sepsis (20.1%). But in another study was performed in Riyadh among 250 patients included in their study was demonstrated that bloodstream infection was the most common hospital-acquired infection (47.2%).[14]

The main limitations of this study were small sample sizes represent a single center and could not be generalized to other medical settings. Furthermore, the sample was included patients with GNB infection regardless of the patient stay department or either if critically ill or not. However, we suggest to increase the sample size and included more centers to get more precise finding. Furthermore, we recommended determining the antibiotics susceptibility for MDR and non-MDR GNB.

   Conclusion Top

This study aimed to determine the incidence and outcome of children with GNB infections. Staphylococcus and Klebsiella were the most abundant GNB, and the mortality rate was 9.4%. Comparing to studies done in Cairo on patients who developed GNB infection with Klebsiella being the most frequently isolated organism, 36.0% and mortality rate 37.1% and Nigeria, which S. aureus was the most isolated GNB organism.

Conflict of interest: None declared.

 

   References Top
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    2.Singer M, Deutschman CS, Seymour CW, et al. The third international consensus definitions for sepsis and septic shock (Sepsis-3). JAMA 2016;315:801-10.  Back to cited text no. 2
    3.World Health Organization Global Health Observatory. Causes of Child Mortality; 2013. Available from: http://www.who.int/gho/ child_health/mortality/causes/en/.  Back to cited text no. 3
    4.Berezin EN, Solórzano F; Latin America Working Group on Bacterial Resistance. Gram-negative infections in pediatric and neonatal Intensive Care Units of Latin America. J Infect Dev Ctries 2014;8:942-53.  Back to cited text no. 4
    5.Levineson W. Review of Medical Microbiology. 14th ed. McGraw Hill; 2016.  Back to cited text no. 5
    6.Al-Shamahy HA, Sabrah AA, Al-Robasi AB, Naser SM. Types of Bacteria associated with Neonatal Sepsis in Al-Thawra University Hospital, Sana'a, Yemen, and their Antimicrobial Profile. Sultan Qaboos Univ Med J 2012;12:48-54.  Back to cited text no. 6
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    8.Aykac K, Ozsurekci Y, Tanir Basaranoglu S, et al. Current epidemiology of resistance among Gram-negative bacilli in paediatric patients in Turkey. J Glob Antimicrob Resist 2017;11:140-4.  Back to cited text no. 8
    9.Oliveira PM, Buonora SN, Souza CL, et al. Surveillance of multidrug-resistant bacteria in pediatric and neonatal Intensive Care Units in Rio de Janeiro State, Brazil. Rev Soc Bras Med Trop 2019;52:e20190205.  Back to cited text no. 9
    10.El-Sahrigy SA, Shouman MG, Ibrahim HM, et al. Prevalence and anti-microbial susceptibility of hospital acquired infections in two pediatric Intensive Care Units in Egypt. Open Access Maced J Med Sci 2019;7:1744-9.  Back to cited text no. 10
    11.Tosson AM, Speer CP. Microbial pathogens causative of neonatal sepsis in Arabic countries. J Matern Fetal Neonatal Med 2011; 24:990-4.  Back to cited text no. 11
    12.Odusanya OO. Antibiotic susceptibility of microorganisms at a general hospital in Lagos, Nigeria. J Natl Med Assoc 2002;94:994-8.  Back to cited text no. 12
    13.Al Johani SM, Akhter J, Balkhy H, El-Saed A, Younan M, Memish Z. Prevalence of antimicrobial resistance among gram-negative isolates in an adult Intensive Care Unit at a tertiary care center in Saudi Arabia. Ann Saudi Med 2010;30:364-9.  Back to cited text no. 13
    14.Al-Hazmi HH, Al-Zahrani T, Elmalky AM. Hospital acquired blood stream infection as an adverse outcome for patients admitted to hospital with other principle diagnosis. Saudi J Anaesth 2014;8:S84-8.  Back to cited text no. 14
    

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Correspondence Address:
Yaser Saleh Bamshmous
Department of Pediatrics, King Abdulaziz University Hospital, Jeddah, Saudi Arabia.
Saudi Arabia
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Source of Support: None, Conflict of Interest: None

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DOI: 10.4103/1319-2442.352420

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  [Table 1], [Table 2], [Table 3], [Table 4]

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