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*Corresponding Author: Alia A. ShoeibPlant Pathology Dept., Faculty of Agriculture, Alexandria University, Egypt.E-mail: [email protected]/[email protected]

Research Article Volume 2012, Article ID sjmb-112, 13 Pages, 2012. doi: 10.7237/sjmb/112

Science Journal of Microbiology Published By Science Journal PublicationISSN: 2276-626Xhttp://www.sjpub.org/sjmb.html© Author(s) 2012. CC Attribution 3.0 License.

A Study of Epidemiology and Etiology of Bacteremia Isolates fromPatients in Riyadh City of Saudi Arabia

Roua M. S. Alkufeidy 1

Alia A. Shoeib1, 2*

Ali M. Somily3

1 Botany and Microbiology Dept, College of Science, King Saud University, Saudi Arabia2 Plant Pathology Dept., Faculty of Agriculture, Alexandria University, Egypt3 Dept. of Pathology, College of medicine, King Saud University, Saudi Arabia

Accepted 27th November, 2012

ABSTRACT

Aim: Detection of the interface between etiological agents ofbacteremia and epidemiology.Methods: A total of 164 blood samples were collected frompatients infected by bacteremia in King Khalid UniversityHospital, Riyadh, Saudi Arabia. Special bottles of BACTEC/ALERTPF microbial detection System (BIOMÉRIEUX brand) were usedas blood culture bottles with antimicrobial removal systems.Bacterial species were identified using cultural, morphologicaland standard biochemical tests e.g. the oxidase, catalase andIndole tests.Results: Elderly category of age was the highest (38.3%),compared to the adult's category (33.2%), then came the othercategories (infants, pediatrics, teenagers) which werestatistically equal (13.2, 11.0, and 4.3% respectively). Theaverage of infected people in an Inpatient Departments (38.7%)was higher incorporeal than infected people in an OutpatientDepartments (11.3%). Identification of bacterial genus andspecies according to the biochemical definition prospects wascarried out in Hospital’s Bacteriology Lab. Pathogens wereidentified in 173 organisms of Gram Positive, Gram Negativebacteria and yeasts. The patients can be infected by one or morethan one pathogenic bacteria. The statistical analysis showed anon significant difference between the infected patients by eitherGــve or G+ve in both males and females.Conclusion: Patients can be infected by one bacterium, morethan one bacterium or yeast. E. coli and Staphylococcus sp.exhibited significant differences in comparison with other genera(G–ve and G+ve respectively) isolated from blood.KEYWORDS: Epidemiology, Etiology, age categories,Bacteremia, E. coli, StaphylococcusINTRODUCTIONBlood is still the richest environment for manybacteria to grow to cause bacteremia. It leads to thepossibility of microbial infection, serious blood

diseases which are incurable and sometimestransmitted in the present age through bloodtransfusions (Volk et al., 1986) and they commonlyspread in hospital (Mylonakis et al., 2006).For reviewing the present work, a variety of studieswas addressing the issue. Comparison betweenepisodes of bacteremia and fungemia in childrenand adults with cancer to assess differences inetiology (Rahbar et al., 2005), risk factors (Llop etal., 2001), outcome (Krupova et al., 1998) anddetermination whether the organisms in thebloodstream originated from the patient's own flora(von Eiff et al., 2001) were reported.Etiological agents of Bacteremia were studied bymany researchers, who confirmed that Neisseriameningitidis was the most common species incommunity-acquired infections, and staphylococcipredominated in hospital-acquired episodes (Grayet al., 2001), whereas Rahbar et al., (2005), reportedthat Gram+ve cocci, including coagulase-negativestaphylococci, Staph. aureus, Streptococcuspneumoniae and Gram-ve bacilli, particularly P.aeruginosa, were responsible of Bacteremia isolates.While, results from Berezin and Iazzetti (2006)showed that the most common etiologic agent wasS. pneumoniae.From previous studies the relationship betweenBacteremia and serious diseases with the causalagent was reported in Seydi et al., (2005) in cases ofE. coli bacteremia was associated with meningitisand AIDS, Ekkelenkamp et al., (2007) reported thatStaph. aureus bacteremia causes Staph. aureusbacteriuria, otherwise, Alamgir et al., (2006) found

Science Journal of Microbiology ISSN: 2276-626X 2

How to Cite this Article: Roua M. S. Alkufeidy, Alia A. Shoeib, Ali M. Somily, “A Study of Epidemiology and Etiology of Bacteremia Isolates from Patientsin Riyadh City of Saudi Arabia ” , Science Journal of Microbiology, Volume 2012, Article ID sjmb-112, 13 Pages, 2012. doi: 10.7237/sjmb/112

that gastrointestinal and genitourinary are sourcesfor E. coli bacteremia.The aim of this study is to detect the interfacebetween etiological agents of bacteremia andepidemiology. To reach the goal, we designed ourresearch through the study of the relationshipbetween bacteremia and neither category of ages inboth genders, Inpatient - Outpatients departmentsnor isolated gram negative and positive bacteriawith which of those isolates are dominant inbloodstream.MATERIALS AND METHODS

Samples CollectionsIn King Khalid University Hospital in Riyadh fromMarch to July 2007, a total of 164 blood sampleswere collected from community and hospitalizedpatients, as well as collected clinical data fromhospitalization files.Blood culture bottles with antimicrobial removalsystems were recommended for patients whodevelop fever while on antibiotics. Special bottles ofBACTEC/ALERT PF microbial detection System(BIOMÉRIEUX brand) were used, each bottlecontains suitable nutritional and environmentalconditions for organisms commonly encountered inblood infections, and each bottle was spiked with 10ml of patients’ blood, to determine ifmicroorganisms are present in blood taken from apatient suspected of having bacteremia/fungemia.Bottles were mixed and loaded onto their respectiveinstruments as per the manufacturer's instructions.Antimicrobial removal was evaluated on the basis oftime for detection of organism growth, for up to 7days of incubation.Specimens were cultured on blood agar; chocolateagar and MacCkonky in CO2, O2 incubators, and theplates were incubated overnight at 37Cْ.Identification of bacterial isolates: Identificationwas carried out in the clinical bacteriologylaboratory of the hospital. Bacterial species wereidentified using cultural, morphological andstandard biochemical tests e.g. the oxidase, catalaseand Indole tests were performed (Cheesbrough,2000, Holt, et al., 2000, Shehabi, et al., 2004 and AboEl-Dahab, et al., 2011). To support the identificationprocess, an automated system microscan was used,special panels for Gram+ve and Gram-ve (have 21wells and 34 wells respectively), some wells

dedicated to special biochemical reaction and somewells dedicated to some important antibiotics.Statistical analysisData was analyzed by (SPSS, 2006) Program:Frequencies and percentages, averages andstandard variations, variations analysis and Dunkintest.RESULTS

Identification of Bacteremia IsolatesAccording to the standard tests recommended forthe identification, the following Gram-ve bacteriagenera and species had been identified: Escherichiacoli, Pseudomonas aeruginosa, Klebsiellapneumoniae, Protus mirabilis, Acinetobacter lwoffi, A.baumannii/haemolyticus, Enterobacter agglomerans,En. cloacae, Citrobacter koseri, Citro. freundii,Alcaligenes sp., Alca. xylosoxidans subsp.xylosoxidans, Haemophilus influenzae, Moraxellacatarrhalis, Achromobacter xylosoxidans subsp.xylosoxidans, Brucella sp., Salmonella sp., S. serogroup D1, Ochrobactrum anthropi, Serratiamarcescens.The following Gram Positive bacteria genera andspecies had been identified: Streptococcuspneumonia, S. salivarius, S. viridans, S. mitis, S.sanguis, Streptococcus Group A, B and D,Staphylococcus aureus, Staph. simulans, Staph.hominis subsp. hominis, Staph. haemolyticus, Staph.epidermidis, Staph. auricularis, Staph. sciuri, Staph.xylosus, Staph. capitis subspecies ureolyticus, Staph.hominis subsp. novobiosepticus, MRSA, Enterococcusfaecalis, Bacillus spp., Diphtheroids sp., Micrococcussp. Also some isolates of yeast has been detected.Relationship between bacteremia and agecategoriesStatistical analysis illustrated that no significantdifferences (p<0.0001) between infected males andfemale with bacterimia, but there was a significanteffect in the age categories, in which the percentageof elderly was the highest (38.3%), compared to theadults category (33.2%), then came the othercategories (infants, pediatrics, teenagers) whichwere statistically equal (13.3, 11.0, 4.2%respectively), this means that there was nosignificant difference between them (Table 1, Figure1).



Table (1): The distribution of gender, males and females according to age categories and averages ofinfection (± standard variations) and variations analysis.ANOVA

*** P < 0.0001 NS = Non SignificantMeans with no common superscript are significantly different (p < 0.05) (SPSS, 2006)

Relationship between Bacteremia andDepartmentsThe percentage of infected males in an InpatientDepartment was more than the percentage ofinfected females, as much as 39.6%, and 37.8%respectively.In an Outpatients Department the percentage ofinfected male was 12.2%, while % of infectedfemale was 10.4%, so the total percentage of

infection in an Inpatient and Outpatientdepartments was 77.4%, 22.6% respectively.Table (2) and Figure (2) below illustrated thefollowing: the significant diversity (P < 0.0001) inthe percentage of infection by bacteremia betweenInpatient and Outpatient Departments, in which theaverage of infected people in an InpatientDepartment was higher incorporeal than infectedpeople in an Outpatient Departments 38.7% and11.3%respectively.

ElderlyAdultsTeenagersPediatricInfantAge CategoriesSex > or = 6122-6012-213-110-2 %No.%No.%No.%No.%No. 10.42 ± 4.9018.33012.2204.278139.716Male 9.59 ± 9.362033213400353.66Female 19.15a ± 0.9816.45a ± 4.902.25b ± 2.595.78b ± 2.456.4b±3.23Mean%± SDSOV df Mean Square F- value Sig.AgeSexError 4114 216.1983.44410.09 21.420.341 ****NS

Fig. (1): The percentage of patients infected by bacteremia according to age categories.

13.3%

11 %

4.2%

33.2%

38.3%InfantPediatricTeenagersAdultsElderly



Table (2): Relationship between numbers of infected males and females and Departments

ANOVA

**** P < 0.0001Means with no common superscript are significantly different (p < 0.05) (SPSS, 2006)

Fig. (2): Relationship between numbers of infected male and female and DepartmentsRelationship between Bacteremia and theInpatient DepartmentsThe statistical analysis of Bacteremia prevalencedemonstrated that the patients in an InpatientDepartments showed that ICU registered thehighest percentage of infection in as much as (35%),then the Peads Dept. (11%), then the EMD (9.7%),

followed by surgery Dept. (6.1%), thenHemat/oncol Dept. (4.8%), Nephrology Dept. (RDU,HDU) (4.2%), Gastro-Enterology Dept. (1.8%),Urology Dept. and I D had the same percentage(1.2%) Intraverto Fertilization, L/D, Thoracic Dept.and Cardiology Dept. had the same percentage(0.6%) (Table 3, Fig. 3)

Mean% ± SDFemaleMaleSexDepartment %No%No 38.70a ± 1.0337.86239.665Inpatient 11.28b ± 1.0610.41712.220Outpatient 24.08b ± 15.8425.90a ± 15.81Mean% ± SDSOV df Mean Square F- value Sig.SexDept.Error 115 6.6251503.7130.001 66251503.713 ********

65 62

127

20 17

37

0

10

20

30

40

50

60

70

80

No.

of p

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Inpatient OutpatientDepartment

MaleFemaleTotal



Table (3): Relationship between Bacteremia and Inpatient Departments

ANOVASOV df Mean Square F- value Sig.SexDept.Error 11238 0.31488.6682.796 0.11231.712 NS******** P < 0.0001 NS = Non SignificantMeans with no common superscript are significantly different (p < 0.05) (SPSS, 2006)

Fig. (3): The relationship between Bacteremia and numbers of infected males and females and the totalnumber of each sex in an Inpatient departments

Inpatient

SexDepartment Male Female Mean% ± SDNo. % No. %Intensive Care Unit (ICU) 34 21 23 14 17.50a ±4.04Nephrology Department (Nephrology Dept.) 4 2.4 3 1.8 2.10de ± .34Urology Department (Urology Dept.) 1 0.6 1 0.6 .60e ± .00Pediatric Department (Peads Dept.) 13 8 5 3 5.47b ± 2.80Surgery Department (Surgery Dept.) 3 1.8 7 4.3 3.05cd ± 1.44Infection Disease Department (ID) 1 0.6 1 0.6 .60e ± .00Hemato/oncology Department (Hemat/oncolDept.) 3 1.8 5 3 2.42de ± .72Emergency medicine Department (E M D) 4 2.4 12 7.3 4.85bc ± 2.83Gastro-Enterology Department (Gastro-EnterologyDept.) 2 1.2 1 0.6 .90e ± .35Intravetro Fertilization (Intravetro Fertilization) 0 0 1 0.6 .30e ± .35Labour/ Delivery (L/D) 0 0 1 0.6 .30e± .34Cardiology Department (Cardiology Dept.) 0 0 1 0.6 .30e± .34Thoracic Department (Thoracic Dept.) 0 0 1 0.6 .30e ± .34Mean% ± SD 3.05 ±5.67 2.90 ± 3.82



Relationship between Bacteremia and theOutpatients Departments

In an Outpatient Departments the DEM (Peads A/R)registered the highest percentage of infectionby bacteremia (20.8%), while PCC1, WBC andPediatric Clinic had registered the same percentage(0.6%) (Table 4 and Fig. 4).

Table (4): Relationship between Bacteremia and Outpatients Departments

Outpatient SexDepartment Male Female Mean% ± SDNo % No %DEM ( Paeds A/R)* 18 11 16 9.8 10.35a ± .635PCC1** 0 0 1 0.6 .30b ± .346WBC*** 1 0.6 0 0 .30b ± .346Pediatric clinic 1 0.6 0 0 .30b ± .346Mean% ± SD 3.025 ± 4.867 2.600 ± 4.451* Department of Emergency Medicine (DEM), Pediatric Emergency Department(Absolute Risk) (Paeds A/R).** Primary Care Clinic for Female (PCC1).***Pediatric Clinic, Well Baby Care/Clinic (WBC).

ANOVASOV df Mean Square F- value Sig.SexDept.Error 1311 0.7225101.00250.1523 4.744663.181 NS******** P < 0.0001 NS = Non SignificantMeans with no common superscript are significantly different (p < 0.05) (SPSS, 2006)

Fig. (4): The relationship between Bacteremia and numbers of infected Patients in an OutpatientsDepartmentRelationship between Bacteremia and IsolatedMicroorganisms

The results illustrated that the patients can beinfected by more than one microorganism causingbacteremia, in which there were 153 out of 164

1816

34

01 1 1

01 1

01

0

5

10

15

20

25

30

35

No.

of p

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emia

bact

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ia

DEM, Paeds A/R PCC1 WBC Pediatric clinicDepartment

MaleFemaleTotal



cases (93.3%) infected by one bacterium, 8/164cases (4.9%) were infected by more than one bacterium, and 3/164 cases (1.8%) were infectedby yeast (Table 5).Table (5): Numbers of cases infected by one or more than one microorganism

Relationship between Bacteremia with G-veBacteria and G+ve BacteriaThe statistical analysis in the Table below shows anon significant difference between the infected patients by either G–ve or G+ve in both males andfemales (Table 6).Table (6): Relationship between bacteremia and Gram Negative bacteria and Gram Positive bacteria

ANOVA

NS = Non significant (SPSS, 2006)Genera of Gram Negative Bacteria CausingBacteremiaThe Table below illustrates that there weresignificant differences (p<0.0001) between generaof G–ve bacteria which infected patients, where E.coli exhibited significant differences in comparison

with other genera isolated from blood, while therewere no significant differences between othertested genera. The statistical analysis showed thatthere was a non significant difference between thepercentage of infection by G–ve bacteria in malesand females (Table 7 and Figures 5 and 6).

TotalyeastMore than onebacteriumOnebacteriumMicroorganism %No.%No.%No.%No.Infected cases 1001641.834.9893.3153TotalyeastMore than onebacteriumOnebacteriumIsolatedMicroorganism ThreeisolatesTwoisolates %No.%No.%No.%No.%No. 1001731.730.619.21688.5153

Mean% ± SDG-veG+veBacteriaSex 43.00 ± 8.083649Male 42.50 ± 6.354738Female 42.00 ± 6.9243.50 ± 7.50Mean% ± SDSOV df Mean Square F- value Sig.Kinds of bacteriaSexError 115 4.5000.500312.50 0.014.713 NSNS



Table (7): Genus of Gram Negative Bacteria Causing BacteremiaMean% ± SDFemaleMaleSexBacteria

%No. ofIsolates%No. ofIsolatesSpeciesGenus of G-ve 11.35a ± 7.5617.9154.84E. coliEscherichia 7.70b ± 2.075.959.58P. aeruginosaPseudomonas 5.35bc ± .6354.845.95K. pneumoniaeKlebsiella .60d ± .691.2100Pro. mirabilisProteus

7.10b ± .007.167.16A. lwoffiA.baumannii/haemolyticus

Acinetobacter

2.40cd ± 1.383.631.21En. agglomeransEn. cloacae

Enterobacter 1.20d ± 1.38002.42Citro. koseriCitro. freundiiCitrobacter

1.20d ± 1.382.4200Alca. xylosoxidanssubsp. xylosoxidansAlcalignes sp.Alcalignes .60d ± .6921.2100Haem. influenzaHaemophilus .60d ±.692001.21M. catarrhalisMoraxella 1.80d ± .691.212.42Ach. xylosoxidans subsxylosoxidans

Achromobacter 4.75c ± 2.717.162.42Brucella sp.Brucella 3.55cd ± 2.711.215.95Salmonella sp.Salmonella sero groupD1Salmonella .60d ± .6921.2100Ochro. anthropiOchrobactrum 1.20d ± 001.211.21Ser. marcescensSerratia 3.73 ± 4.522.93 ± 2.94Mean% ± SD

ANOVASOV df Mean Square F- value Sig.SexGenusError 11444 9.642.9725.564 1.7257.723 NS******** P < 0.0001 NS = Non SignificantMeans with no common superscript are significantly different (p < 0.05) (SPSS, 2006)



Fig. 5: Number of isolated Gram Negative Bacteria of patients which are the most frequency causingbacteremia

Fig. 6: The relationship between numbers of isolated Gram Negative Bacteria of patients which are the mostfrequency causing bacteremia and number of infected males and females and their total.Genera of Gram Positive Bacteria CausingBacteremia

The Table below illustrates that there weresignificant differences (p<0.0001) between generaof G+ve bacteria which infected patients, whereStaphylococcus sp. exhibited significant differencesin comparison with other genera isolated from



blood, while there were no significant differencesbetween other tested genera. The statistical analysis showed that there was a non significant differencebetween the percentages of infection by G+vebacteria in males and females (Table 8, Figures 7 and 8).Table (8): Genus of Gram positive bacteria (G+ve) causing bacteremia

Mean% ± SDFemaleMaleSexBacteria%No. ofIsolates%No. ofIsolatesSpeciesGenus of G+ve

7.45b ± .63876.96S. pneumoniaeS. salivariusStreptococcus Group AS. viridansS. MitisS. sanguisStreptococcus Group DStreptococcus Group B

Streptococcus

31.55a ± 4.6727.52435.631

Staph. aureusStaph. simulansStaph. hominis subsp.hominisStaph. haemolyticusStaph. epidermidisStaph. auricularisStaph. sciuriStaph. xylosusStaph. Capitis subspeciesureolyticusStaph. hominis subsp.novobiosepticusMRSA

Staphylococcus

2.30c ± 2.65004.64Entero. faecalisEnterococcus 4.60bc ± 1.273.535.75Bacillus sp.Bacillus 3.50c ±.003.533.53Diphtheroids sp.Diphtheroids 0.60c ± .691.2100Micrococcus sp.Micrococcus 7.28 ± 9.799.38 ± 12.45Mean% ± SDANOVASOV df Mean Square F- value Sig.SexGenusError 1517 26.46538.6393.988 6.6355135.065 NS

******** P < 0.0001 NS = Non SignificantMeans with no common superscript are significantly different (p < 0.05) (SPSS, 2006)



Fig. (7): Number of isolated Gram Positive Bacteria of patients which are the most frequency causingbacteremia

Fig. (8): The relationship between numbers of isolated Gram Positive Bacteria of patients which are the mostfrequency causing bacteremia and number of infected males and females and their total.



DISCUSSIONSThe study discussed the relationship betweenbacteremia and age, which illustrated that thepercentage of elderly was the highest (38.3%),compared to the adults category (33.2%), thencame the other categories (infants, pediatrics,teenagers) which were statistically equal, (13.2, 11,4.3%) respectively. The prevalent bacteria whichwere associated with bacteremia wereStaphylococcus sp. as G+ve bacteria and E. coli as G-ve bacteria, which disagreed with Frederiksen et al.,(2007) who reported that the incidence ofbacteremia in an infant age group had greaterpercentage (73.9%) compared with other agestrata, and supports that Staph. aureus is dominantbacteria in bloodstream.Results obtained in our study showed that thehighest percentage of infections was in an IntensiveCare Unit (35%) for both genders, which wasopposed Juanjuan et al., (2007) who noted that thehighest percentage of infections was in theDepartment of Urological Surgery (48.1%).Results from the previous studies (Gray et al., 2001and Juanjuan et al., 2007) were consistent with thepresent result, which revealed that the percentageof patients in an Inpatients Departments (77.4%)was highly significant than the percentage ofinfected patients in an Outpatients Departments(22.6%). The present results supported Rahbar etal., (2005) who found that the percentage of G+veand G-ve bacteria causing bacteremia were equal,while, Espinosa et al., (1999) revealed that G-vebacteria were more than G+ve bacteria.It was worth mentioning, according to the cultural,morphological and physiological characters of theisolated bacteria from bloodstream, that 8 patientswere infected by more than one genus of bacterium(Gupta, et al., 2005), 153 patients were infected byone genus of bacterium and 3 patients were infectedby yeast. According to the available literatures, itseems that infection by more than one genus ofbacteria was considered as one of the first record inSaudi Arabia. To follow the differences in etiologyand outcome of bacteremia in Riyadh, city, SaudiArabia, a study at Security Forces Hospital, forSaudi's patients only, was carried out after 2 yearsfrom our study (Alsayed, M. F. S., 2010). Resultsobtained from 50 samples of blood were collectedfrom Inpatients and Outpatients departments,seems to be close to our findings this means thatoverview of bacterimia within 2 years didn't change

either in Saudi population or Saudi with foreignpopulation in Riyadh City.CONCLUSIONSOut of 164 samples, 20 species belonging to 15 G-vegenera and 23species belonging to 6 G+ve generawere isolated from blood stream infection.Statistical analysis illustrated the following: asignificant effect in the age categories, infectedpeople in an Inpatient Departments was higherincorporeal than infected people in an OutpatientDepartments. ICU and DEM (Peads A/R) registeredthe highest percentage of infection in an Inpatientand Outpatient Departments respectively.The results illustrated that the patients can beinfected by one bacterium, more than onebacterium or yeast.E. coli and Staphylococcus sp. exhibited significantdifferences in comparison with other genera (G–veand G+ve respectively) isolated from blood, whilethere were no significant differences between othertested genera. The statistical analysis showed a nonsignificant difference between the infected patientby either G–ve or G+ve in both males and females.ACKNOWLEDGEMENTThanks for King Abdulaziz City for Science andTechnology (KACST)) Contribution No. AT-18-75)and the Research Center in the Departments ofScience and Medical Studies in King Saud Universityfor its Grant to support this research project.REFERENCES

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