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Acosta J, Meneses C, Arévalo
V, Altamirano J, Gonzáles M.
Molecular diagnosis of
polymicrobial sepsis in pediatric
patient: a case report. Scientic
Magazine INSPILIP. 2022; 6 (1)
The author declares to be free of any
personal or commercial association
that could suppose a conict of
interest in connection with the article,
as well as having respected the
ethical principles of research, such as
having requested the authorizations
of the institution where the study
was carried out. , permission to use
the data, informed consent and in
the case of observational studies and
clinical trials, authorization from
a CEISH, ARCSA, Environment,
among others, according to the
category. In addition, the license
to publish images of the person or
persons that appear in the manuscript.
For this reason, INSPILIP is not
responsible for any aectation to
third parties, neither is INSPI as the
publishing entity, nor the Editor, the
responsibility of the publication is
the absolute responsibility of the
authors.
Jaime David Acosta España
a, b, c, d
, jdae_14@hotmail.com
Carolina Ximena Meneses Cañizares
e
, caroximeneses@yahoo.es
Víctor Manuel Arévalo Méndez
f
, pepito53@hotmail.com
Jenny Belén Altamirano Jara
g
, belen.medaltamirano93@gmail.com,
Mabel González Alemán
h
, gonzalezalemanmabel@yahoo.com
a Department of Medical Microbiology, Vozandes Hospital, 170521 Quito, Ecuador
b School of Medicine, Universidad de las Américas, 170124 Quito, Ecuador.
c Jena Microbial Resource Collection, Leibniz Institute for Natural Product Research and Infection
Biology—Hans Knöll Institute (HKI), 07745 Jena, Germany
d Institute of Microbiology, Friedrich Schiller University Jena, 07743 Jena, Germany
e Department of Pediatrics, Pediatric Gyneco-Obstetric Hospital “Luz Elena Arizmendi” Nueva
Aurora, 170146 Quito, Ecuador.
f Health Center “A” Military Fort Marco Aurelio Subía, Armed Forces of Ecuador, Quito, Ecuador.
g Professor, Instituto Técnico Superior Cruz Roja Ecuatoriana, Quito, Ecuador.
h Advisor for Infectious Diseases of the Secretary of Health of Mexico City, Mexico City, Mexico.
Correspondence: Jaime Acosta Email: jdae14@hotmail.com
Identication of the responsibility and contribution of the authors: The conception of the
article was carried out by (CM, JA). All authors collaborated equally in the writing of this
manuscript (CM, JA, VA, JA, MA). They reviewed and approved the manuscript (CM, MG).
Date of admission: 22/2/2022. Approval date: 05/04/2022. Publication date: 05/05/2022.
Molecular diagnosis of polymicrobial sepsis in pediatric patient: a case report
Diagnóstico molecular de sepsis polimicrobiana en paciente pediátrico: reporte de un caso
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DOI: https://doi.org/ 10.31790/inspilip.v6i1.265
Case report
Open access
Abstract
Citation
Polymicrobial sepsis is a controversial diagnosis, being feasible in patients
with a history of surgical interventions, and abdominal sepsis, among other
risk factors. The case of a pediatric patient with multiple hospitalizations and
surgical interventions due to an underlying diagnosis of type IV multiple
jejunal atresia that produced polymicrobial sepsis conrmed by molecular
biology and traditional cultures is described below. It is important to consider
polymicrobial sepsis in blood cultures taken with the correct technique, since
the identication of pathogens leads to targeted treatment, increasing the
probability of survival of these patients.
Keywords: Sepsis. Coinfection. Pediatrics. Molecular Diagnostic Techniques.
Ecuador.
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Resumen
El diagnóstico de sepsis polimicrobiana es
controvertido, se ha considerado factible en
pacientes con antecedentes de intervenciones
quirúrgicas, sepsis abdominal, entre otros factores
de riesgo. A continuación, se describe el caso de un
paciente pediátrico con múltiples hospitalizaciones e
intervenciones quirúrgicas por el diagnóstico de base
de atresia yeyunal múltiple tipo IV que produjo sepsis
polimicrobiana conrmada por biología molecular
y cultivos tradicionales. Es importante considerar
la sepsis polimicrobiana en hemocultivos tomados
con la técnica correcta, ya que la identicación
de patógenos conduce al tratamiento dirigido,
aumentando la probabilidad de supervivencia de
estos pacientes.
Palabras clave: Sepsis. Coinfección. Pediatría.
Técnicas de Diagnóstico Molecular. Ecuador,
Introduction
Conrmed polymicrobial sepsis is rare in pediatrics
and is associated with factors such as underlying
medical conditions, gastrointestinal problems,
malignancies, or a central venous access device
1-4
.
Thus, here we present a rare case of a pediatric
patient with sepsis with abdominal focus with
molecular and phenotypic detection of Acinetobacter
baumannii, Klebsiella pneumoniae producing
serinecarbapenemase (KPC), Enterococcus faecalis,
and Staphylococcus epidermidis MRSA and
constitutive MLSb.
Case report
An 11-month-old infant, the product of the rst
pregnancy of an adolescent mother (16 years old),
whose pregnancy was uneventful. This patient was
born by cephalo-vaginal delivery, APGAR 9 at
1 minute and APGAR 10 at 5 minutes of life, and
anthropometric measurements within normal limits.
Initially, on examination, the patient’s general
condition was good.
There was no obvious congenital anomaly, later in
the neonatology room, the patient presented bilious
vomiting 12-15 episodes/24 hours in the absence of
abdominal distension.
For this clinical presentation, abdominal radiography
and ultrasonography were requested and showed
dilated small bowel loops. This patient received a
diagnosis of intestinal atresia and was transferred to
a third-level pediatric hospital, where an exploratory
laparotomy was performed, which conrmed
multiple type IV jejunal atresia, for which a proximal
end resection + ileostomy was performed.
After this, the patient was hospitalized on 2 previous
occasions in the same hospital, due to diarrhea,
severe dehydration, and malnutrition. At 7 months
of age, he presented with sepsis of an abdominal
focus, secondary to a procedure to restore intestinal
transit, and received a non-detailed broad-spectrum
antibiotic treatment.
At 10 months of age on February 20, 2019, he
was admitted to a third-level public hospital. He
was admitted for new sepsis of abdominal focus,
pneumonia, urinary tract infection (UTI) by E. coli
and Candida sp., hydro electrolytic disorder, chronic
malnutrition, and cardiorespiratory arrest on 2
occasions.
For the management of his infectious etiologies, this
patient was treated with:
• ampicillin (200 mg/kg/day),
• amikacin (15 mg/Kg/day),
• metronidazole (30 mg/Kg/dose),
• fluconazole (6 mg/Kg/dose),
• ceftriaxone (40 mg/Kg/ day),
• linezolid and meropenem (40 mg/Kg/day).
During this condition, he remained hospitalized
for 29 days and was discharged due to a favorable
evolution.
Ten days later he went to a dierent pediatric hospital
with 10 months and 28 days of life. He was admitted
to the emergency room with a clinical history of 12
hours, characterized by: vomiting, hyporexia, and
decay.
On physical examination: the patient was asthenic,
irritable, pale, crying without tears, with cold skin and
dry oral mucous membranes, sunken eyes, moderate
nasal discharge, capillary lling for 3 seconds,
abdomen with increased air-uid noises, ileostomy
sheath with 20 mL of fecal uid content.
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vancomycin at 45 mg/Kg/day.
At 6 hours after incubation in semi-automated
equipment for blood cultures (BD Bactec Fx 40)
the two bottles were positive, and gram-negative
bacilli were observed in the stain. Due to the torpid
evolution of this patient, real-time multiplex PCR was
performed for sepsis using the BioFire FilmArray
blood culture panel (BioFire Diagnostics LLC, Salt
Lake City, UT).
In the blood culture panel for sepsis, genes were
detected of Acinetobacter baumannii, Klebsiella
pneumoniae resistance gene KPC, Enterococcus,
Staphylococcus mecA resistance gene (Figure 1).
For this reason, he was admitted with a diagnosis of
moderate dehydration, protein-calorie malnutrition,
ileostomy carrier, uid and electrolyte disorder,
prerenal renal failure, and oral candidiasis. In an
emergency, dehydration and electrolyte imbalance
were immediately corrected.
On the same day, antibiotic therapy was started
with ceftriaxone at 100 mg/kg/day and they were
impregnated with uconazole at 6 mg/kg due to their
history of previous fungal infection.
Patient with apparent clinical improvement,
however, on the seventh day of hospitalization,
presented temperature increase with the presence of
leukocytes of 18,000/mm3, C-reactive protein of 500
mg/dL, procalcitonin of 14 ng/dL, 2 new peripheral
blood cultures were taken under aseptic conditions
and empirically covered for Gram positives with
Figura 1. Resultados de hemoculvo
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Subsequently, in cultures, microbiology reported:
Acinetobacter baumannii, Klebsiella pneumoniae
producer of serinecarbapenemases with
susceptibility to colistin, Enterococcus faecalis,
and Staphylococcus epidermidis resistant to
cefoxitin and constitutive MLSb (Figure 2).
Therefore, the pediatric infectious disease specialist
established intravenous treatment for 14 days with
colistin
• (activity of 15 colistin base (AUC)/kg/day),
• and amikacin (20 mg/kg/day),
• meropenem (40 mg/kg/day). dose every 8 hours)
• and vancomycin (40 mg/Kg/day).
• The patient remained stable during his 14 days of
intravenous antibiotics.
Based on the pediatric infectious disease request
by the criterion that repeating blood cultures may
increase the diagnostic yield for conditions such as
infective endocarditis and may have implications
for the duration of antibiotic therapy, two peripheral
blood cultures were performed under aseptic
conditions on the fth day of antibiotic therapy,
which were negative.
After arduous management by a multidisciplinary
team, the patient was discharged, having overcome
his polymicrobial sepsis of abdominal origin after 32
days of hospitalization.
Discussion
Sepsis has a worldwide relevance in all ages, risk
factors include the extremes of age, abdominal
comorbidities, abdominal surgeries, etc.
Thus, the case analyzed presented a sum of these risk
factors characterized by age, congenital jejunal atresia,
multiple abdominal interventions, and malnutrition.
In addition, the multiple hospitalizations predisposed
this patient even to infections associated with health
services
1,3-6
.
It is important to mention that initially the patient
was treated in another hospital for his surgical needs,
where he received various cycles of broad-spectrum
antibiotics. Unfortunately, it was not possible to
obtain a detailed history of which antibiotics, dosage,
and the number of cycles he had previously received.
This background is crucial because it disrupts the gut
microbiome and increasingly recognized modulator
of the immune system and outcomes in sepsis
7
.
Previously, there was the criterion that an infection
could be produced only by a pathogen supported by
Koch’s postulates, but currently, it has been shown
that infections can be polymicrobial as in the case
presented, being important to highlight that the
multiple hospitalizations where he received several
antibiotics of dierent spectra made the traditional
microbiological diagnosis dicult
7
.
The use of antibiotics tends to inhibit the growth of
infection-producing pathogens in articial cultures.
Because the therapeutic spectrum was reduced in the
emergency of the last hospitalization to ceftriaxone
and uconazole, a window was produced where the
diagnosis was achieved by traditional and molecular
microbiology
8-10
.
In septic patients, the culture of blood, urine,
cerebrospinal uid, or other tissues is essential to
detect infection. Microbiological analysis is the gold
standard despite its limitations regarding response
time and the ability to detect only culturable
pathogens
2,6,7
.
In this way, molecular methods can shorten the
identication time helping to establish therapies based
on the microorganisms detected and their resistance
mechanisms, if any, thus there is a methodology
with multiplex PCR (Polymerase Chain Reaction)
in real-time that allows the detection of several
pathogens in a simultaneous test that even contain
Figura 2. Reporte de microbiología
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resistance genes such as MRSA, KPC, VAN A for
the most frequent resistance mechanisms, which are
a very helpful tool in polymicrobial sepsis
5,6,8
.
Usually, whenever more than two pathogens
are detected in blood cultures, contamination is
suspected. Therefore, the diagnosis of polymicrobial
sepsis is controversial.
The detection of real cases in pediatrics is rare and is
associated with factors such as underlying medical
conditions, patients with gastrointestinal problems,
malignancies, or a central venous access device
3-5
.
In this patient, a sum of criteria supported sepsis
as polymicrobial, such as leukocytosis, increased
C reactive protein, increased procalcitonin, and
fever The advantage of molecular microbiology
is that it searches for sequences of the pathogen’s
genetic material as well as resistance genes that
have an important impact on therapeutics. Based
on the long-standing clinical history, with previous
hospitalizations, multidrug-resistant pathogens of
hospital origin were suspected, so multiplex real-time
PCR was recommended for sepsis.
This allowed, in 7 hours after taking 2 peripheral
blood cultures in sterile conditions, to cover with
antibiotics that improved the spectrum such as
amikacin and colistin.
The association of meropenem, amikacin, colistin,
and vancomycin had a good clinical course in this
patient. Based on what has been discussed, it is
essential to analyze all risk factors in pediatric
patients with previous hospitalizations, it is important
to suspect multidrug-resistant pathogens, especially
if there is a history of previous infections, the use
of broad-spectrum antibiotics, invasive devices, and
long-term hospitalization.
There are new diagnostic tools that allow us to detect
pathogens in sepsis and medical scientic evidence
recommends the use of these as they can directly
inuence antibiotic therapy and patient survival,
especially in patients with septic shock where the
establishment of an early eective antibiotic therapy
decreases the risk of mortality
1,4,6
.
Conclusions
It is essential to individually evaluate each patient
who has criteria for sepsis with special attention
to risk factors as they will allow a more focused
diagnosis and management. The blood culture
collection technique in septic patients is essential to
ensure the reliability of the results, especially in those
cases where there are risk factors for polymicrobial
sepsis
11
.
In patients hospitalized for more than 3 days or with a
history of previous hospitalizations in the last month,
there is the possibility of infections by nosocomial
microorganisms, and this can represent a challenge
for diagnosis and antimicrobial therapy
12.
Although traditional blood cultures continue to be
the gold standard, it is interesting to consider the
new molecular diagnostic tools that can shorten
waiting times for results and can help guide initial
antimicrobial therapy. Despite this, traditional
cultures are essential since they are the only ones
that can show the results of bacterial susceptibility to
dierent antibiotics.
On the other hand, molecular techniques for the
syndromic diagnosis of sepsis with panels that
detect several microorganisms are more susceptible
to detecting false positives, for which these results
must always be correlated with the clinical status of
each patient, and it is also important to know that
only is possible apply these panels in positive blood
cultures
13-15
.
Special attention should be paid to pediatric patients
because their management is dierent from adults.
An example of this is the dose of antibiotics,
which must be adjusted to various factors, such as
weight
16
.
Recommendations
Specialized management by pediatricians with training
in pediatric sepsis management or subspecialists in
pediatric infectious disease is recommended for this
type of patient
16
.
It is always necessary to request cultures in pediatric
patients with sepsis since this can help us identify
the site of infection, the pathogen, and its resistance
mechanisms that directly impact the choice of
antimicrobial
16,17
.
There is an urgent need to train laboratory personnel
and physicians in the new diagnostic techniques in
sepsis since they can improve survival after an early
diagnosis.
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It is critical to adjust the dose of antibiotics in
pediatrics to weight, since many patients may have
changed during hospitalization, also to preserve renal
and hepatic function
18
.
If antimicrobial therapy has no clinical eect
after 72 hours of administration, it is important to
consider whether the dose is correct, whether other
drugs are interfering with the antibiotics, whether
the site of infection and my chosen drug have
adequate penetrance, whether the nursing sta is
carrying out a correct dilution and administration
of the medication, and in cases that warrant,
multi-resistant microorganisms should be considered
and the therapy should be escalated based on the
epidemiology or the microbiological surveillance
chart of your hospital
19
.
Finally, it is essential to have a doctor or laboratory
personnel with training in medical microbiology with
a clinical approach, which can be a great help for
clinicians who, in case of doubts or diculties in the
microbiological diagnosis of sepsis, can consult with
personnel trained in the subject
20-23
.
Conicts of Interest: The authors declare no conict
of interest.
Acknowledgments
The authors would like to acknowledge the teaching
department and the authorities of the Pediatric
Obstetrics and Gynecological Hospital “Nueva
aurora” for the authorization to access the data for
the publication of this case.
Funding: The research did not receive any
specic grant funding from agencies in the public,
commercial, or not-for-prot sectors.
Reference
1. T. Kawasaki, Update on pediatric sepsis: a review,
Journal of Intensive Care 2017 5:1. 5 (2017) 1–12.
https://doi.org/10.1186/S40560-017-0240-1.
2. K.J. Downes, J.P. Metlay, L.M. Bell, K.L. McGowan,
M.R. Elliott, S.S. Shah, Polymicrobial bloodstream
infections among children and adolescents with
central venous catheters evaluated in ambulatory care,
Clinical Infectious Diseases : An Ocial Publication
of the Infectious Diseases Society of America. 46
(2008) 387–394. https://doi.org/10.1086/525265.
3. L.S. al Yazidi, P. Britton, A. Kesson,
POLYMICROBIAL BACTEREMIA SECONDARY
TO FABRICATED OR INDUCED ILLNESS IN
A CHILD BY A CARER, Journal of Paediatrics
and Child Health. 56 (2020) 1660–1661. https://doi.
org /10.1111/J PC.15173.
4. M.H. Tsai, S.M. Chu, J.F. Hsu, R. Lien, H.R. Huang,
M.C. Chiang, R.H. Fu, C.W. Lee, Y.C. Huang,
Polymicrobial Bloodstream Infection in Neonates:
Microbiology, Clinical Characteristics, and Risk
Factors, PLoS ONE. 9 (2014). https://doi.org/10.1371/
JOURNAL.PONE.0083082.
5. K.J. Downes, J.P. Metlay, L.M. Bell, K.L. McGowan,
M.R. Elliott, S.S. Shah, Polymicrobial bloodstream
infections among children and adolescents with
central venous catheters evaluated in ambulatory care,
Clinical Infectious Diseases : An Ocial Publication
of the Infectious Diseases Society of America. 46
(2008) 387–394. https://doi.org/10.1086/525265.
6. M. Sinha, J. Jupe, H. Mack, T.P. Coleman, S.M.
Lawrence, S.I. Fraley, Emerging Technologies for
Molecular Diagnosis of Sepsis, (2018). https://doi.
org/10.1128/CMR.00089-17.
7. C. Rhee, S.S. Kadri, J.P. Dekker, R.L. Danner,
H.C. Chen, D. Fram, F. Zhang, R. Wang, M.
Klompas, Prevalence of Antibiotic-Resistant
Pathogens in Culture-Proven Sepsis and Outcomes
Associated With Inadequate and Broad-Spectrum
Empiric Antibiotic Use, JAMA Network Open. 3
(2020) e202899–e202899. https://doi.org/10.1001/
JAMANETWORKOPEN.2020.2899.
8. N. Mancini, S. Carletti, N. Ghidoli, P. Cichero, C.M.
Ossi, R. Ieri, E. Poli, R. Burioni, M. Clementi, Letters
to the editor molecular diagnosis of polymicrobial
sepsis, Journal of Clinical Microbiology. 47 (2009)
1274–1275. https://doi.org/10.1128/JCM.00011-09/AS-
SET/33CE489D-D445-4452-9F8E-41C51F40222C/
ASSETS/GRAPHIC/ZJM0040987920001.
JPEG.
9. A.L. Byrd, J.A. Segre, Adapting Koch’s postulates,
Science. 351 (2016) 224–226. https://doi.org/10.1126/
SCIENCE.AAD6753.
10. J. Cohen, The Evolution of Koch’s Postulates,
Infectious Diseases. (2017) 1-3.e1. https://doi.
org/10.1016/B978-0-7020-6285-8.00001-0.
Molecular diagnosis of polymicrobial sepsis in pediatric patient
Acosta España J
9
Código ISSN 2588-0551
144
https://www.inspilip.gob.ec
6
Magazine INSPILIP - V 6 - Number 1 - May 2022
6
6
11. J.L. Vincent, M. Singer, S. Einav, R. Moreno, J.
Wendon, J.L. Teboul, J. Bakker, G. Hernandez, D.
Annane, A.M.E. de Man, X. Monnet, V.M. Ranieri, O.
Hamzaoui, J. Takala, N. Juermans, J.D. Chiche, S.N.
Myatra, D. de Backer, Equilibrating SSC guidelines
with individualized care, Critical Care. 25 (2021)
1–4. https://doi.org/10.1186/S13054-021-03813-0/
TABLES/1.
12. K.M. Demerle, S.C. Royer, M.E. Mikkelsen,
H.C. Prescott, Readmissions for Recurrent
Sepsis: New or Relapsed Infection?, Critical Care
Medicine. 45 (2017) 1702. https://doi.org/10.1097/
CCM.0000000000002626.
13. S. Kim, J. Kim, H.Y. Kim, Y. Uh, H. Lee, Ecient
Early Diagnosis of Sepsis Using Whole-Blood
PCR–Reverse Blot Hybridization Assay Depending
on Serum Procalcitonin Levels, Frontiers in
Medicine. 7 (2020) 390. https://doi.org/10.3389/
FMED.2020.00390/BIBTEX.
14. T.E. Sweeney, O. Liesenfeld, L. May, Diagnosis
of bacterial sepsis: why are tests for bacteremia not
sucient?, Https://Doi.Org/10.1080/14737159.2019.
1660644. 19 (2019) 959–962. https://doi.org/10.1080/
14737159.2019.1660644.
15. R. Rule, F. Paruk, P. Becker, M. Neuho, J. Chausse,
M. Said, Clinical utility of the BioFire FilmArray
Blood Culture Identication panel in the adjustment
of empiric antimicrobial therapy in the critically
ill septic patient, PLOS ONE. 16 (2021) e0254389.
https://doi.org/10.1371/JOURNAL.PONE.0254389.
16. T. Lancet Child, A. Health, Paediatric sepsis:
timely management to save lives, The Lancet Child
& Adolescent Health. 4 (2020) 167. https://doi.
org/10.1016/S2352-4642(20)30032-8.
17. J.M. Miller, M.J. Binnicker, S. Campbell, K.C. Carroll,
K.C. Chapin, P.H. Gilligan, M.D. Gonzalez, R.C.
Jerris, S.C. Kehl, R. Patel, B.S. Pritt, S.S. Richter, B.
Robinson-Dunn, J.D. Schwartzman, J.W. Snyder, S.
Telford, E.S. Theel, R.B. Thomson, M.P. Weinstein,
J.D. Yao, A Guide to Utilization of the Microbiology
Laboratory for Diagnosis of Infectious Diseases: 2018
Update by the Infectious Diseases Society of America
and the American Society for Microbiology, Clinical
Infectious Diseases. 67 (2018) e1–e94. https://doi.
org/10.1093/CID/CIY381.
18. J. Le, J.S. Bradley, Optimizing Antibiotic Drug
Therapy in Pediatrics: Current State and Future Needs,
The Journal of Clinical Pharmacology. 58 (2018)
S108–S122. https://doi.org/10.1002/JCPH.1128.
19. K. Chiotos, J.S. Gerber, A.S. Himebauch, How can we
optimize antibiotic use in the pediatric intensive care
unit?, Pediatric Critical Care Medicine : A Journal of
the Society of Critical Care Medicine and the World
Federation of Pediatric Intensive and Critical Care
Societies. 18 (2017) 903. https://doi.org/10.1097/
PCC.0000000000001261.
20. G.M. Scott, Clinical microbiology—the UK model,
Clinical Microbiology and Infection. 6 (2000) 402–404.
https://doi.org/10.1046/J.1469-0691.2000.00114.X.
21. L.P. Samuel, G.T. Hansen, C.S. Kraft, B.S. Pritt, The
Need for Dedicated Microbiology Leadership in the
Clinical Microbiology Laboratory, Journal of Clinical
Microbiology. 59 (2021). https://doi.org/10.1128/
JCM.01549-19.
22. N.J. Beeching, H. Rautelin, J.P. Stahl, T.M. Leegaard,
Training and assessment of medical specialists
in clinical microbiology and infectious diseases
in Europe, Clinical Microbiology and Infection.
27 (2021) 1581–1588. https://doi.org/10.1016/J.
CMI.2021.07.009.
23. The Complete Guide To Becoming a Medical
Microbiologist/Virologist, (n.d.). https://www.bmj.
com/careers/article/the-complete-guide-to-beco-
ming-a-medical-microbiologist-virologist/ (accessed
March 18, 2022).
