CHILDHOOD URINARY TRACT INFECTION: CLINICAL SIGNS, BACTERIAL CAUSES AND ANTIBIOTIC SUSCEPTIBILITY

Abdulrahman A. Ishak1image, Abdulrahman M Alhadi1, Khaled Abdulkareem A Al-Moyed2image, 

Hassan A. Al-Shamahy2image

1Department of Pediatrics, Faculty of Medicine and Health Sciences, Sana’a University, Sana’a, Republic of Yemen.

2Medical Microbiology and Clinical Immunology Department, Faculty of Medicine and Health Sciences, Sana’a University, Republic of Yemen.

ABSTRACT 

Background and objective: Urinary tract infections (UTIs) are the neglected infection in children from the side of study its clinical symptoms, causative organisms and their antibiotic sensitivity. This investigation searches for determine clinical symptoms frequency, prevalence rate, bacterial features, and antibiotic sensitivity of bacterial urinary tract infection in children attending private children’s health center in Sana’a city.

Methods: In a prospective study carried out over a 24-month period, 1925 samples from children patients suspected of having a UTI were investigated, of which 175 were culture-positive. Clinical and demographic data were collected. Isolated bacteria were identified by standard tests, and antibiotic susceptibility was performed by the disk diffusion method.

Results: Fever was the most frequent symptom that occurred (88%) while other UTI symptoms were less frequent than that reported in adult patients for UTI. The most common etiological agent was Escherichia coli (89.7%), followed Staphylococcus aureus (3.4%), Klebsiella spp (2.9%), Proteus spp (2.3%), and beta haemolytic streptococci (1.7%).  Results of antimicrobial resistant for E. coli, as the most prevalent cause of UTI, to commonly used antibiotics are ranged from less than 3% for  levofloxacin, gentamicin,  amikacin and cefoxitin to more than 75% for  tetracycline, nalidixic acid,  doxycycline,  co-trimoxazol and amoxicillin .

Conclusions: The results show the most common  symptom of UTI are fever and lack of more obvious symptoms of UTI in adult patients. The antimicrobial resistance patterns of the causes of UTI are highly changeable and constant surveillance of trends in resistance patterns of uropathogens among children is essential. 

Keywords: antibiotic resistant, bacterial causes, children, Sana’a, UTI symptoms, UTI, Yemen.

 

INTRODUCTION

 

A urinary tract infection (UTI) is an infection that affects part of the urinary tract1. As the lower UTI, which is known as cystitis and as it affects the upper urinary tract, it is known as pyelonephritis2. As for the symptoms resulting from lower UTI, they include pain during urination, frequent urination, and the feeling of needing to urinate despite the presence of an empty bladder2,3. The symptoms of kidney infection include fever and flank pain and rarely, blood appears in the urine. In the elderly and the young, the symptoms are vague or non-specific1,4. In young children, researchers have found that the only symptom of UTI is fever5. Therefore, because there are no more obvious symptoms, when the fever appears in females under the age of two or in males less than a year old, it is recommended to do a bacterial culture of the child's urine. Also, one of the symptoms in children is that children feed poorly, vomit, sleep more than normal, or may show signs of jaundice. However, in older children, new onset of enuresis (loss of bladder control) may occur. Reports have documented that about 1 of 400 infants aged between 1 to 3 months having UTIs will develop bacterial meningitis5,6. Overall, urinary tract infections (UTIs) are one of the most common infectious diseases, and approximately 10% of people will likely develop a UTI during their lifetime7,8. It is known that UTIs are the most common after upper respiratory tract infections in humans9. 

This infection may be clinically symptomatic or asymptomatic, and upper or lower UTI infection may lead to serious consequences if left untreated10. Many different microorganisms can cause UTIs, consist of fungi and viruses, but bacteria are the main causative agents and cause more than 95% of UTI cases11. Since bacteria are the important cause of UTI, Escherichia coli is the most common UTI-causing bacterium and is exclusively responsible for more than 80% of these infections. Precise and rapid diagnosis of UTI is important in shortening the course of the disease and preventing transmission of infection to the upper urinary tract, which may lead to kidney failure12,13. The choice of antibiotics and the inappropriate dose leads to treatment failure and an increase in antibiotic resistance; and with recurrent UTIs, in particular, it may lead to permanent injuries such as renal parenchymal scarring, impaired renal function, high blood pressure, and chronic kidney disease14. In addition, frequent antibiotic use or urinary tract abnormalities are risk factors for developing resistance and although there are regional differences, resistance to antibiotics used in empirical therapy is gradually increasing worldwide and particularly in Yemen country15-17,18-32. 

An example of the importance of this topic in Sana'a and the situation where this information is useful in Sana'a as well. As the rates of antibiotic resistance are high, doctors depend on giving antibiotics experimentally without bacterial isolation and sensitivity testing to antibiotics18-32.  Treatment for UTIs often begins with an experiment. Treatment is derived from specific information from the antimicrobial resistance pattern of urinary pathogens. Nevertheless, due to the developing and persistent phenomenon of antibiotic resistance, regular monitoring of resistance patterns is essential to improve the guidelines for empirical antibiotic therapy 30-32. However, the availability of data about the type of isolated bacteria from childhood having UTIs and their antibacterial susceptibility profiles in Sana’a city, Yemen, are very limited.This study aimed to determine the frequency of clinical symptoms, prevalence, bacterial features, and antibiotic sensitivity of UTIs in children attending the private pediatric health center in Sana'a city, Yemen.

 

MATERIAL AND METHODS

 

Study design and area

This was a retrospective descriptive study. Clinical and microbiological data for the 2019-2020 bienniums were obtained from the Pediatric Department of Sam Medical Center (Private Childhood Hospital) in Sana'a City, Yemen. This time capsule was chosen for the completeness and correctness of the information, as it was reviewed and followed up by the first author. 

Data collection

Clinical and demographic data were collected in a pre-designed questionnaire. The data were filled in by physicians and assistants and reviewed by the study supervisor. 

 

Ethical approval 

The written consent in all cases were obtained. Approval was obtained from the participants prior to including in the study. Ethical approval was obtained from the Medical Research and Ethics Committee of the Faculty of Medicine and Health Sciences, Sana’a University with reference number (752) on 01/12/2018.

Inclusion and Exclusion criteria 

The study included outpatient children with suspected UTI, who had not received antimicrobials within the past 2 months, referred to NCPHL for urine culture and obtained written consent.

Sample collection

Cultivation and identification were performed at the Microbiology Department of the National Center of Public Laboratories (NCPHL), Sana'a City. Urine samples were collected from 1925 outpatient children with suspected UTI, who had not received antimicrobials within the past two months, and referred to theNCPHL for Urine Culture. There were 1459 (75.8%) samples of female patients and 466 (24.2%) of male patients. The patient's age ranged from 7 months to 13 years (mean age 7.7±5.2 years). Children older than 3 years were sampled with clean urine midstream, and children younger than 3 years old were sampled using sterile urine bags.

Isolation and identification of bacteria

 Urine samples were examined and cultured within an hour of sampling. All samples were inoculated on blood agar plus MacConkey agar and incubated at 37°C for 24 h, and for 48 h in negative cases. The sample was considered positive for urinary tract infection if a single organism was cultured at a concentration of 105 CFU/ml, or when a single organism was cultured at a concentration of 104 CFU/ml and 5 leukocytes per high-power field were observed on urine microscopy. The bacteria were identified on the basis of standard culture and biochemical characteristics of the isolates. Gram-negative bacteria were identified by standard biochemical tests11,12. Gram-positive bacteria were identified by the corresponding laboratory tests: catalase, coagulase, CAMP test (for Streptococcus agalactiae), and Esculin agar (for enterococci)33.

Susceptibility testing

The isolates were tested for antimicrobial susceptibility by disc diffusion method consistent with the approvals of the National Committee for Clinical Laboratory Standards (NCCLS), employing Muller-Hinton medium12. The antimicrobial agents tested were: amikacin, amoxicillin, ampicillin, ampicillin- sulbactam, augmentin, azithromycin, aztreonam, cefaclor, cefadroxam, cefepime, cefixime, cefotaxime, cefoxitin, ceftazidime, ceftriaxin, ceftriaxone, cefuroxime, ciprofloxacin, clarithromycin, clindamy-cin, co-trimoxazol, etrapenem, erythromycin, doxycy-cline,  gentamicin, fosfomycin, levafloxacin, lomeflox-acin moxifloxacin, nalidixic acid, nitrofurantoin, piperacillin/tazobactam, tetracycline and vancomycin (BD-BBL-TM-Sensi-Disc-TM).

Statistical analysis

Discrete variables were expressed as percentages and proportions were compared using the Chi-square test34.

Table 1: The age and sex distribution of children suffering from UTI.

*Mean±SD age=7.5±4.3 year, *Mean ±SD age=7.89±5.3 year, *Mean±SD age=7.7±5.2 year.

RESULTS

 

Over a 24-month, 1925 urine samples from children outpatients were analyzed, of which 175 (9.1%) had significant bacteriuria.  The rate of positive culture was 8.4% (124/1459) for female subjects and 10.9% (51/466) for male subjects (Table 1).  Table 2 shows the frequency of clinical signs of UTI among children. The usual clinical symptoms of upper and lower UTIs in the current study were significantly lower than those reported in adults, with the rate of pain above the pubic bone, lower back pain, flank pain, urine appearing bloody, and visible pus in urine <50 %. Whereas, the most important symptom was fever, which occurred in 88% of the children completely, followed by enuresis as a new onset (73.1%). 

Table 2: The frequency of clinical signs of UTI among children.

Also, the symptom of poorly nourished children occurred at 57.1% in children under the age of one year, vomiting was recorded in 14.3%, and the presentation of sleeping more than usual in 58.9% and burning during urination was recorded in 56%. Gram-negative bacilli were responsible for 94.9% of cases followed by Gram-positive bacteria responsible for 5.1% of cases. Analysis of the results according to patient gender indicated that although E. coli is the predominant pathogen isolated from both sexes, it occurs significantly in female children (91.8% for females compared to 84.9% for males; p<0.05), whereas. 

Table 3: The bacterial causes of  children UTI according to gender.

The prevalence of urinary tract infection due to Klebsiella species and Proteus species was 2.9% and 2.5%, respectively. The prevalence of UTI caused by S. aureus in males (5.7%) was higher than in females (2.5%) (Table 3). Table 4 shows the pattern of antibiotic resistance of microorganisms in children with UTI. The resistance rates of isolates to a group of antibiotics, including penicillins, cephalosporins, quinolones, aminoglycosides, and trimethoprim-sulfamethoxazole, that are routinely used to treat UTIs, are shown in Table 4. E. coli as the predominant cause of UTI, showed higher proportion of resistance to amoxicillin (91.5%), nalidixic acid (88.5%) and tetracycline (88.5%) while the least resistant to E. coli were to levafloxacin (1.9%), amikacin (2.5%), cefoxin (2.5%), gentamicin (2.5%), moxifloxacin (3.2%), lomefloxacin (3.8%), ertapenem (5.1%),  and aztreonam (6.4%). Klebsiella spp as the second predominant UTI pathogen showed a similar resistance pattern and was 100% resistant to amoxicillin, ampicillin and augmentin, while 80% of this bacterium was resistant to azithromycin, cefaclor, cefadroxam, nalidixic acid, tetracycline and doxycycline. Proteus species also showed a high rate of antibiotic resistance to many of the antibiotics tested (Table 4). S. aureus was 100% resistant to amoxicillin, ampicillin and azithromycin, while all isolates of S. aureus were sensitive to vancomycin.

Table 4: Bacterial antibiotic resistances pattern of children UTI.

 

DISCUSSION 

 

Urinary tract infection is a common disease in children, especially females, where in the current study 78.86% of cases were females, while only 21.24% of male cases, and this is similar to what was mentioned in the previous literature35-37. Infection generally occurs with the colonization of the lower urinary tract by bacteria, most of which are Gram-negative. The infection may extend from the bladder to the kidneys, depending on the characteristics of the pathogen. It is known that infection is rarely transmitted by the hematogenous route and may occur as a result of the transmission of the agent to the urinary tract through the blood during sepsis. Vesicoureteral reflux, voiding dysfunctions, neurogenic bladder, urinary incontinence, constipation, bladder neck obstruction, and the presence of a catheter are predisposing factors for UTI35. Another factor is familial and genetic predisposition36.

Clinical outcomes in pediatric UTI vary according to age, location in the urinary tract, and severity of infection37. In the neonatal and pediatric period, the signs are mostly nonspecific38. Diagnosis is based mostly on the patient's symptoms and results of the physical examination and urinalysis, and treatment generally begins empirically39. However, increasing antibiotic resistance nowadays leads to treatment failure and an increase in acute cases. It is now known that antibiotic resistance has become an important problem for hospital infections, and for community-acquired infections40. Therefore, it is recommended that the resistance rate does not exceed 10-20% to start experimental treatment in any region of the world41. For that reason, the American Infectious Diseases Society emphasizes that regional pathogenic agents and antibiotic sensitivities in UTIs should be known42. 

Microbial infection of the urinary tract is one of the most common diseases worldwide. In this study, of 1925 children clinically diagnosed with a UTI, samples were taken and only 9.1% had a UTI while the others gave negative culture results. This is probably because UTI symptoms are not a reliable indicator of infection and also that children under 5 years of age have nonspecific UTI symptoms. This is similar to that reported by Farajnias, et al., in Iran in their study, of the 5,136 patients from whom urine samples were taken; only 13.2% had a UTI1. In the current investigation, most urine samples were collected from pediatric patients who did not have a symptomatic group of UTI, and most of the subjects were referred by general practitioners and specialist physicians. These results indicate that urine culture is essential for the definitive diagnosis of urinary tract disease, and that empirical treatment should only be performed in the absence of urine culture examination7. The results of the current study show a higher number of females (124 females versus 51 males). This may be that males are less likely to develop UTIs due to the length of their urethra7.

Even though the prevalence of UTIs causative agents in diverse parts of the world is to some extent similar, the patterns of antimicrobial resistance reported from different areas are considerably different and antimicrobial resistance is increasing in the world. The results of the current study illustrate that among the heterogeneous causative bacteria for UTI, Enterobacteriaceae are the dominant pathogens, followed by Gram-positive cocci. These results are consistent with reports published in Yemen previously and from other countries around the world30-32,37,39. In UTI, the causative agent is generally Gram-negative bacteria. The main pathogen is E. coli, Klebsiella, Enterobacter and Proteus spp. It has been reported at lower rates37-39. Consistent with previous studies, we found that the most common causative agent was  E. coli, and the female sex was dominant in current study37-39. The highest resistances were found to amoxicillin (91.5%), ampicillin (90.7%), doxycycline (95.5%), trimethoprim-sulfamethoxazole (75.2%), and nalidixic acid (88.5%), while the least resistant to E. coli were to levofloxacin (1.9%), amikacin (2.5%), cefoxin (2.5%). %), gentamicin (2.5%), moxifloxacin (3.2%), lfomfloxacin (3.8%), Ertapenem (5.1%), aztronam (6.4%); these results are mainly consistent with other studies conducted previously in Yemen18-32,44 and around the world7-11. The present study, as with previous studies, shows that E. coli is the predominant etiology of UTI32,45,46 and also reveals a very high rate of bacterial resistance to antibiotics. This was particularly the case for the Klebbsilla species and Proteus sp. that were completely resistant to ampicillin, cephalexin, nitrofurantoin, nalidixic acid and trimethoprim-sulfamethoxazole; this resistance is higher than that of other reports32,46,47. Over the past decade, there has been a significant increase in the resistance of urinary pathogens to antibiotics. Resistance rates are increasing among strains of Staphylococcus aureus, and a significant portion of this species has become resistant to beta-lactamase-resistant penicillin48. For such resistant species, vancomycin is the effective drug choice. Vancomycin resistance has been reported among Enterococci48, but this resistance has also begun to develop among Staphylococci. In this study, we focused on vancomycin resistance and fortunately no vancomycin-resistant strains were observed, but 100% of cases were resistant to ampicillin, aztreonam, and azithromycin. The regional variations of resistance to antibiotics may be explained partly by distinct local antibiotic practices50. The pressure of unnecessary and/or inappropriate antibiotic use on the development of antibiotic-resistant strains, mostly broad-spectrum agents prescribed empirically, has been demonstrated. Reducing the number of prescriptions of a particular antibiotic can lead to a decrease in resistance rates. Transmission of resistant isolates between people and/or by consumption of foods originated from animals that have received antibiotics and greater mobility of individuals worldwide has also be a factor of the expansion of antibiotic resistance. Regional differences in antibiotic resistance may be partially explained by different local antibiotic practices50,51. The outcome of unnecessary and/or improper use of antibiotics on the expansion of antibiotic-resistant strains, especially of broad-spectrum agents described experimentally, has been demonstrated. Reducing the number of prescriptions for a particular antibiotic can lead to lower rates of resistance. Transmission of resistant isolates between people and/or by consumption of foods originating from animals that received antibiotics and greater movement of individuals around the world has also play a role on the expansion of antibiotic resistance50,52.

 

CONCLUSION

 

In conclusion, since the antibiotic susceptibility pattern of bacteria varies over time and in different geographic regions, antibiotic treatment of infection should be based on local experience of susceptibility and resistance patterns of culture and antibiotic susceptibility testing. In this study, it was found that  augmentin and aztreonam two most suitable oral antibiotics, amikacin and third-generation cephalosporins were the most suitable parenteral antibiotics, for the empirical treatment of urinary tract infection. Also, E. coli was the most common causative agent of childhood UTIs.

 

CONFLICT OF INTEREST 

 

No conflict of interest associated with this work. 

 

AUTHOR’S CONTRIBUTION

 

The first author presented the data and the first, and the rest authors analyzed the data and wrote, revised and edited the paper.

 

REFERENCES

 

  1. Farajnia S, Alikhani MY, Ghotaslou R, Naghili B, Nakhlband A. Causative agents and antimicrobial susceptibilities of urinary tract infections in the northwest of Iran. Int J Infect Dis 2009; 13(2):140-4. https://doi.org/10.1016/j.ijid.2008.04.014
  2. Lane DR, Takhar SS. Diagnosis and management of urinary tract infection and pyelonephritis.  Emerg Med Clin North America 2009; 29 (3): 539–52.https://doi.org/10.1016/j.emc.2011.04.001
  1. Salvatore S, Salvatore S, Cattoni E, Siesto G, Serati M, Sorice P, Torella M. Urinary tract infections in women. European J Obstet Gynecol Reprod Biol 2011; 156 (2):131-6. https://doi.org/10.1016/j.ejogrb.2011.01.028
  2. Woodford HJ, George J. Diagnosis and management of urinary infections in older people. Clinical Med 2011; 11 (1): 80–3.https://doi.org/10.7861/clinmedicine.11-1-80
  1. Bhat RG, Katy TA, Place FC. Pediatric urinary tract infections. Emerg Med Clin North America 2011; 29 (3): 637–53.https://doi.org/10.1016/j.emc.2011.04.004
  2. Nugent J, Childers M, Singh-Miller, et al. Risk of meningitis in infants aged 29 to 90 days with urinary tract infection: a systematic review and meta-analysis. The J Pediatrics 2019; 212: 102–110.e5.  https://doi.org/10.1016/j.jpeds. 2019.04.053
  1. Hoberman A, Wald ER. Urinary tract infections in young febrile children. Pediatr Infect Dis J 1997; 16(1):11-7.https://doi.org/10.1097/00006454-199701000-00004
  1. Delanghe JR, Kouri TT, Huber AR, Hannemann-Pohl K, Guder WG, Lun A, Sinha P, Stamminger G, Beier L. The role of automated urine particle flow cytometry in clinical practice. Clin Chim Acta 2000; 301(1-2):1-18.https://doi.org/10.1016/s0009-8981(00)00342-9
  1. Hryniewicz K, Szczypa K, Sulikowska A, Jankowski K, Betlejewska K, Hryniewicz W. Antibiotic susceptibility of bacterial strains isolated from urinary tract infections in Poland. J Antimicrob Chemother 2001; 47(6):773-80.https://doi.org/10.1093/jac/47.6.773
  1. Pezzlo M. Detection of urinary tract infections by rapid methods. Clin Microbiol Rev 1988; 1(3):268-80.https://doi.org/10.1128/CMR.1.3.268
  1. Bonadio M, Meini M, Spitaleri P, Gigli C. Current microbiological and clinical aspects of urinary tract infections. Eur Urol 2001; 40(4):439-44; discussion 445.https://doi.org/10.1159/000049813
  1. National Committee for Clinical Laboratory Standards. Performance standards for antimicrobial disc susceptibility tests. 7th Wayne, Pennsylvania, USA: NCCLS; 2000. M2-A7.
  2. Hsiao CY, Yang HY, Hsiao MC, Hung PH, Wang MC. Risk factors for development of acute kidney injury in patients with urinary tract infection. PLoS One. 2015; 10(7):e0133835.https://doi.org/10.1371/journal.pone.0133835
  3. Elder JS. Urinary tract infection and vesico ureteral reflux. In: Behrman RE, Kleigman RM, Jenson HB, editors. Nelson Textbook of Pediatrics. 19th Philadelphia: Saunders; 2011:1829–34.
  4. Peña C, Albareda JM, Pallares R, Pujol M, Tubau F, Ariza J. Relationship between quinolone use and emergence of ciprofloxacin-resistant Escherichia coli in bloodstream infections. Antimicrob Agents Chemother 1995; 39(2):520-4. https://doi.org/10.1128/AAC.39.2.520
  5. Ladhani S, Gransden W. Increasing antibiotic resistance among urinary tract isolates. Arch Dis Child 2003; 88:444–5.  https://doi.org/10.1136/adc.88.5.444
  6. Prais D, Straussberg R, Avitzur Y, Nussinovitch M, Harel L, Amir J. Bacterial susceptibility to oral antibiotics in community acquired urinary tract infection. Arch Dis Child 2003; 88:215–8.http://dx.doi.org/10.1136/adc.88.3.215 
  1. Abbas AM, Al-Kibsi TAM, Al-Akwa AAY, AL-Haddad KA, Al-Shamahy HA, Al-labani MA. Characterization and antibiotic sensitivity of bacteria in orofacial abscesses of odontogenic origin. Universal J Pharm Res 2020; 5(6):36-42. https://doi.org/10.22270/ujpr.v5i6.510 
  2. Al Hamzi MA, Al-Shamahy HA, Al jorany AA, Al Sharani AA. Phototoxic effect of visible blue light on Porphyromonas Gingivalis and Aggregatibacter Actinomycetemcomitans. On J Dent Oral Health. 2(3): 2019. http://dx.doi.org/10.33552/OJDOH.2019.02.000540
  3. Al-Akwa AAY, Zabara AQMQ, H. A. Al-Shamahy HA, et al. Prevalence of staphylococcus aureus in dental infections and the occurrence of MRSA in isolates. Universal J Pharm Res 2020; 5(2):1-6. https://doi.org/10.22270/ujpr.v5i2.384
  4. Al-Eryani SA, Alshamahi EYA, Al-Shamahy HA, Alfalahi GHA, Al-Rafiq AA. Bacterial conjunctivitis of adults: causes and ophthalmic antibiotic resistance patterns for the common bacterial isolates. Universal J Pharm Res 2021; 6(1):25-28. https://doi.org/10.22270/ujpr.v6i1.535
  5. AL-Haddad KA, Ali Al-Najhi MM, Al-Akwa AAY, et al. Antimicrobial susceptibility of Aggregatibacter actinomycetemcomitans isolated from Localized Aggressive Periodontitis (LAP) cases. J Dent Ora Heal Ad Re 2021:103. http://dx.doi.org/10.39127/2021
  6. Al-Haifi AY, Al Makdad ASM, Salah MK, Al-Shamahy, Al Shehari WAA. Epidemiology, bacterial profile, and antibiotic sensitivity of lower respiratory tract infections in Sana’a and Dhamar city, Yemen. Universal J Pharm Res 2020, 5(2):1-6. https://doi.org/10.22270/ujpr.v5i2.386
  7. Alhasani AH, Ishag RA, Yahya Al-Akwa AAY, Al Shamahy HA, Al-labani MA. Association between the Streptococcus mutans biofilm formation and dental caries experience and antibiotics resistance in adult females. Universal J Pharm Res 2020; 5(6):1-3.https://doi.org/10.22270/ujpr.v5i5.478
  1. Al-Hrazi RMA, Al-Shamahy HA, Jaadan BM. Determination of rifampicin mono-resistance Mycobacterium tuberculosis in the National tuberculosis control programme in Sana’a city-Yemen: a significant phenomenon in war region with high prevalence tubercloisis. Universal J Pharm Res 2019; 4(3):1-9. https://doi.org/10.22270/ujpr.v4i3.266
  1. Al-Safani AA, Al-Shamahy HA, and Al-Moyed KA. Prevalence, antimicrobial susceptibility pattern and risk factors of MRSA isolated from clinical specimens among military patients at 48 medical compounds in Sana’a city-Yemen. Universal J Pharm Research 2018; 3(3):40-44.https://doi.org/10.22270/ujpr.v3i3.165
  1. AL-Magrami RTF, Al-Shamahy HA. Pseudomonas aeruginosa skin-nasopharyngeal colonization in the in-patients: prevalence, risk factors and antibiotic resistance in tertiary hospitals in Sana’a city -Yemen. Universal J Pharm Res 2019; 3(6):1-9.https://doi.org/10.22270/ujpr.v3i6.219
  1. Alshamahi EYA, Al-Shamahy HA, Musawa YA. Bacterial causes and antimicrobial sensitivity pattern of external ocular infections in selected ophthalmology clinics in Sana’a city. Universal J Pharm Res 2020; 5(3):12-16.https://doi.org/10.22270/ujpr.v5i3.329
  1. Al-Shami IZ, Al-Hamzi MA, Al-Shamahy HA, et al. Efficacy of some antibiotics against Streptococcus mutans associated with tooth decay in children and their mothers. On J Dent Oral Health 2019;2(1): 1-6.https://doi.org/10.33552/OJDOH.2019.02.000530
  1. Alyahawi A, Alkaf A, Alnosary T. Current trend of resistant for the commonly prescribed new fluoroquinolones among hospitalised patients in Sana’a, Yemen. Universal J Pharm Res 2018; 3(5):1-6. https://doi.org/10.22270/ujpr.v3i5.197
  1. Alyahawi A, Alkaf A, Alnamer R, Alnosary T. Study of resistance for recently marketed carbapenem drug among hospitalised patients in Sana’a, Yemen. Universal J Pharm Res, 2018; 3(5): 1-6. https://doi.org/10.22270/ujpr.v3i5.203
  2. Saleh AAM, Al-Shamahy HA, Al-Hrazi RM, Jaadan BM,  AL-Magrami RTF, Al-Sharani AA. Biofilm formation and antibiotic susceptibility of uropathogens in patients with catheter associated urinary tract infections in Ibb city -Yemen. Universal J Pharm Res 2020; 4(6):1-6.https://doi.org/10.22270/ujpr.v4i6.329
  1. Magee JT, Pritchard EL, Fitzgerald KA, Dunstan FD, Howard AJ. Antibiotic prescribing and antibiotic resistance in community practice: retrospective study, 1996-8. BMJ. 1999; 319(7219):1239-1240.https://doi.org/10.1136/bmj.319.7219.1239
  1. Hulley S, Cummings S, Browner W. Designing clinical research. 2nd ed. Philadelphia, USA: Lippincott, Williams & Wilkins; 2001.
  2. Wald ER. Cystitis and pyelonephritis. In: Feigin RD, Cherry JD, Demler-Harrison GJ, editors. Textbook of pediatric infectious diseases. 6th edition. Philadelphia: Saunders; 2009:554–69.
  3. Zaffanello M, Malerba G, Cataldi L, Antoniazzi F, Franchini M, Monti E, Fanos V. Genetic risk for recurrent urinary tract infections in humans: a systematic review. J Biomed Biotechnol 2010; 2010:321082.https://doi.org/10.1155/2010/321082
  1. Jantausch B, Kher K. Urinary tract infection. In: Kher KK, Schnaper HW, Makker SP, editors. Clinical Pediatric Nephrology 2nd London: Informa Healthcare; 2006:553–73.
  2. Samancı S, Çelik M, Köşker M. Antibiotic resistance in childhood urinary tract infections: A single-center experience. Turk Pediatri Ars. 2020; 55(4):386-392.https://doi.org/10.14744/TurkPediatriArs.2020.22309
  1. Rosenberg M. Pharmacoeconomics of treating uncomplicated urinary tract infections. Int J Antimicrob Agents 1999; 11(3-4):247-51.https://doi.org/10.1016/s0924-8579(99)00024-2
  1. Ansbach RK, Dybus K, Bergeson R. Uncomplicated  coli urinary tract infection in college women: a follow-up study of E. coli sensitivities to commonly prescribed antibiotics. J Am Coll Health 2005; 54(2):81-4; discussion 85-6.https://doi.org/10.3200/JACH.54.2.81-84
  1. Rahn DD. Urinary tract infections: contemporary management. Urol Nurs 2008;28(5):333-41; quiz 342.PMID: 18980099
  1. Alós JI, Serrano MG, Gómez-Garcés JL, Perianes J. Antibiotic resistance of Escherichia coli from community-acquired urinary tract infections in relation to demographic and clinical data. Clin Microbiol Infect 2005; 11(3):199-203. https://doi.org/10.1111/j.1469-0691.2004.01057.x
  2. Edrees HW, Anbar AA. Prevalence and antibacterial susceptibility of bacterial uropathogens isolated from pregnant women in Sana'a, Yemen. PSM Biol Res. 2020; 5(4): 157-165.
  3. Al-Khawlany RS, Edrees WH, et al. Prevalence of methicillin-resistant Staphylococcus aureus and antibacterial susceptibility among patients with skin and soft tissue infection at Ibb City, Yemen. PSM Microbiol 2021; 6(1): 1-11.
  4. Sharifian M, Karimi A, Tabatabaei SR, Anvaripour N. Microbial sensitivity pattern in urinary tract infections in children: a single center experience of 1,177 urine cultures. Jpn J Infect Dis 2006; 59(6):380-2. PMID: 17186957
  5. Levtchenko E, Lahy C, Levy J, Ham H, Piepsz A. Treatment of children with acute pyelonephritis: a prospective randomized study. Pediatr Nephrol 2001; 16(11):878-84. https://doi.org/10.1007/s004670100690
  6. Kapoor H, Aggarwal P. Resistance to quinolones in pathogens causing urinary tract infections. J Commun Dis 1997; 29(3):263-7. PMID: 9465532
  7. Van den Bogaard AE, London N, Driessen C, Stobberingh EE. Antibiotic resistance of faecal Escherichia coli in poultry, poultry farmers and poultry slaughterers. J Antimicrob Chemother 2001; 47(6):763-71.https://doi.org/10.1093/jac/47.6.763
  1. Heidari H, Hasanpour S, Ebrahim-Saraie HS, Motamedifar M. High incidence of virulence factors among clinical Enterococcus faecalis isolates in Southwestern Iran. Infect Chemother 2017; 49(1):51-56.https://doi.org/10.3947/ic.2017.49.1.51
  1. Critchley IA, Cotroneo N, Pucci MJ, Mendes R. The burden of antimicrobial resistance among urinary tract isolates of Escherichia coli in the United States in 2017. PLoS ONE 2019; 14(12): e0220265.  https://doi.org/10.1371/journal.pone.0220265
  1. Edrees WH, Al-Asbahi AA, Al-Shehari WA, Qasem EA. Vulvovaginal candidiasis prevalence among pregnant women in different hospitals in Ibb, Yemen. Universal J Pharm Res 2020; 5(4):1-5.https://doi.org/10.22270/ujpr.v5i4.431
  1. Alhlale MF, Humaid A, Saleh AH, Alsweedi KS, Edrees WH. Effect of most common antibiotics against bacteria isolated from surgical wounds in Aden Governorate hospitals, Yemen. Universal J Pharm Res 2020; 5(1): 21-24. https://doi.org/10.22270/ujpr.v5i1.358