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Received: 9 June 2021 Revised: 29 July 2021 Accepted: 3 August 2021

DOI: 10.1111/jep.13612

COMPREHENSIVE REVIEW

Quality of clinical practice guidelines for gestational

and congenital toxoplasmosis: A systematic review
of the literature

Ginna Cabra-Bautista MD, MSc1 | Beatriz E. Paz-Cordoba MD | 1 |

1
Tatiana Henao-Pabon MD Ana Milena Bravo MD1 |
Ivan D. Florez MD, MSc, PhD2,3 | Mario Delgado-Noguera MD, MSc, PhD1 | Jose
Andrés Calvache MD, MSc, PhD4

1
Department of Pediatrics, School of Health
Sciences, Universidad del Cauca, Popayán,
Colombia
two
Department of Pediatrics, University of
Antioquia, Medellin, Colombia
3
School of Rehabilitation Science, McMaster
University, Hamilton, Canada
4
Anesthesiology Department, School of Health
Sciences, Universidad del Cauca, Popayán,
Colombia
Correspondence
Ginna Cabra-Bautista, Department of
Pediatrics, School of Health Sciences,
Universidad del Cauca, Popayán, Colombia.
Email: ginnapcabrab@unicauca.edu.co
Abstract
Objective: To evaluate the methodological quality and transparency of the clinical
practice guidelines (CPGs) for the prevention, diagnosis, and treatment of pregnancy
and congenital toxoplasmosis (CT).
Methods: Systematic review of the literature on gestational and CT CPGs conducted
in the MEDLINE, Embase, TripDatabase, Biblioteca Virtual en Salud databases and
extensive manual searches in 19 CPG repositories. The characteristics of each of the
guidelines were extracted using My AGREE PLUS online. Three reviewers assessed
overall quality using the Appraisal of Guidelines for Research and Evaluation II
(AGREE II) tool.
Results: The combined systematic review found 8651 citations. Of them 46 full texts
were reviewed, and eight documents were finally included: four toxoplasmosis CPGs,
three prenatal care CPGs that included recommendations on toxoplasmosis, and one
pregnancy infection guideline that also included recommendations on toxoplasmosis.
The AGREE II domains found to have the highest scores were 'clarity of presenta-
tion' (85%; [37%-100%]), followed by 'scope and purpose' (73%; [33%-98%]), and
'editorial independence' (51%; [3%-94%]); the domains with the lowest scores were
'rigour of development' (36%; [11%-79%]), 'stakeholder involvement' (34%;
[24%-85%]), and 'applicability' (17%; [6%-83%]). The Colombian and Spanish-
Agencia de Evaluacion de Tecnologías Sanitarias de Andalucía (AETSA) CPGs had the
highest global AGREE II scores. Absolute interter agreement was good to excellent.
Conclusion: Substantial quality variation was found among CPGs, which provided
recommendations in accordance with the context of the disease in the corresponding
country or region. Only two of the CPGs approved obtained a good score and are
classified as 'recommended'.

KEYWORDS
AGREE, evidence-based practice, practice guidelines as topic, quality of health care,
toxoplasmosis, congenital toxoplasmosis

J Eval Clin Pract. 2021;1–7. wileyonlinelibrary.com/journal/jep © 2021 John Wiley & Sons, Ltd. 1
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two
1 | INTRODUCTION
Toxoplasmosis is a zoonosis caused by various serotypes of Toxo-
plasma gondii, an intracellular parasite that produces manifestations in
humans ranging from mild and self-limiting to severe ocular and
neurological involvement, leaving significant sequelae.1
With a global incidence of 190 100 cases per year and a more
aggressive behavior in South America, CT is one of the forms of
greatest concern from the public health perspective.2,3
Toxoplasmosis being a preventable and treatable disease, a world
initiative has been created with the aim of identifying the current situation
action in the most affected countries. This initiative calls for work on
the design, development, and implementation of clinical practice
guidelines (CPGs) for the detection of the infection in pregnant women
women, prevention of vertical transmission, treatment of foetal and
neonatal infection, and as guidance for follow-up in children with confirmed
CT.1
CPGs have been developed as a strategy to improve healthcare
by reducing clinical variability and providing more rational care
through the implementation of evidence-based recommendations that
allow for a critical assessment of the risks and benefits of existing
options.4,5 CPG development requires a rigorous methodological process
carried out by multidisciplinary teams, designed to incorporate
the evidence found in the literature, expert opinions, patient values
and preferences, needs, and priorities of the population, taking into
account costs within each health system.4-6
Gestational toxoplasmosis exposes the fetus to the risk of con-
genital infection. Therefore, an early approach during pregnancy
reduces neonatal mortality, neurological and ophthalmological
sequelae, improving the quality of life of patients and their families,
and may reduce the economic burden on health systems.1,2 CPGs
contain evidence-based recommendations useful for providing better
patient care, helping the physicians and the patients to make the best
decisions for the prevention, diagnosis, and treatment of diseases during
clinical practice.5 However, there is wide variability in their devel-opment
that may result in varying degrees of quality of the process
itself and the quality of the recommendations provided. Therefore, it
is necessary to know the methodological rigor and transparency during
the development process of CPGs and their recommendations.7-10
Our objective was to identify and evaluate the methodological quality
and transparency of CPGs for the prevention, diagnosis, and treatment of
gestational and CT.
2 | METHODS
A systematic review of the existing CPGs on congenital and gestational
toxoplasmosis or the approach to prenatal and postnatal care
was carried out, which included recommendations on the diagnosis
and management of congenital and neonatal toxoplasmosis. Individual
CPGs were considered if they reported a systematic search strategy
or contained recommendations. In those cases, in which there was
more than one version of the same CPG, the most updated version by
CABRA-BAUTISTA ET AL.
a single work group or organization, or partial later publications of the
same CPG were included. CPGs in progress, published by a single
author, based on formal or informal consensus, and duplicate publica-
tions were excluded.
A systematic search was conducted in MEDLINE (PubMed),
Embase, TripDatabase and Virtual Health Library (VHL). Addition-
ally, extensive manual searches were conducted in 19 CPG reposito-
ries and webpages of CPG producing agencies as Emergency Care
Research Institute (ECRI) Guidelines Trust, National Guidelines Clear-
ingHouse, The National Institute for Health and Care Excellence
(NICE), Scottish Intercollegiate Guideline Network (SIGN), GIN Guide-
lines International Network, National Health and Medical Research
Council (NHMRC)-Australian Clinical Practice Guidelines, Clinical
Practice Guidelines (Canadian Medical Association), New Zealand
Guidelines Group, BIGG International database of GRADE Guidelines,
BMJ Best Practice, Guíasalud (España), CENETEC Maestro Catalog
of Clinical Practice Guides (Mexico), Ministry of Health Protocols
Clinicians and Therapeutic Guidelines (Brazil), Clinical Practice Guides
Ministry of Health and Social Protection (Colombia), Clinical Guides
AUGE (Chile), Technical Guides (Perú), Ministerio de Salud (Nicaragua),
Ministry of Public Health (Uruguay) and Ministry of Health
(Argentina).
The search was adapted according to the indications for each
database, using medical subject headings, keywords, and boolean
connectors to combine the terms used. Terms that included toxoplasmo-
sis were taken into consideration to improve the sensitivity of the
strategy, and because of the possibility of finding sections on toxo-
plasmosis for appraisal as part of the prenatal care CPGs, the term
'prenatal care' was also used. The search was conducted until
31 October 2020, with no publication date or language restrictions.
After eliminating duplicates, three reviewers (BP, TH and GC)
working independently selected all titles and abstracts for inclusion
and exclusion criteria application. Full texts were then obtained for
the final decision on inclusion. Disagreements were resolved by consensus
in online meetings; when needed, a fourth reviewer (JAC)
participated in the discussion until agreement was reached. The rea-
sounds for excluding papers were documented.
The three reviewers (BP, TH and GC) conducted an independent
dent assessment of the quality of each of the CPGs. To that end, My
AGREE PLUS (https://www.agreetrust.org/), the official online platform of
the AGREE collaboration was used to apply the AGREE II
appraisal either individually or as a group.11 The reviewers were pae-
diatrics' residents and one paediatrician who received training from an
expert in the tool. Also, before initiating the process, a pilot study of
the appraisal was also conducted using three CPGs not related to the
study subject.
The AGREE II tool consists of 23 items grouped into six qualities
domains: 1. scope and purpose (items 1-3), 2. stakeholder involvement
(items 4-6), 3. rigor of development (items 7-14), 4. clarity of presentation
(items 15-17), 5. applicability (items 18-21), and 6. editorial
independence (items 22 and 23). Each item is given a score on a
seven-point Likert scale, where 1 is the 'totally disagree' and 7 is the
'totally agree'. This tool also includes two global appraisal items:
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CABRA-BAUTISTA ET AL.
1. global guideline quality, also on a seven-point Likert scale, where 1 is the
'lowest possible quality' and 7 is the 'highest possible quality'; and 2.
recommendation of the guideline for use, rated as 'recommended',
12
'recommended with modifications', or 'not recommended'.
After domain appraisal, overall confidence of each CPG was rated
as follows: 'recommended' (four out of six domains ÿ60%); 'rec-
ommended with modifications' (at least two domain scores >60%);
and 'not recommended' (three out of six domain scores <30% or no domain
>60%).13,14 Mean scores of the domains are classified as good (ÿ80%),
acceptable (60%-79%), moderate (40%-59%) or low (<40%).13,14
The protocol for this review was reviewed and approved by the
vice-rector for research at Universidad del Cauca, registered under number
5221 on 12 March 2020. This systematic review is reported
according to the preferred reporting items for systematic review and meta-
analyses (PRISMA) statement (Table S1),15 and was classified as a no-
risk observational study.16
2.1 | Statistical analysis
Each appraisal was documented in My AGREE PLUS and the ratings by
each of the three reviewers were then exported to an Excel
spreadsheet which was delivered to a fourth researcher (JAC) who
conducted the analysis to obtain the score for each domain and determine-
mine the degree of appraisal agreement. A standardized score with a range
between 0% and 100% was calculated for each domain. The score for each
of the six domains was calculated by adding all
FIGURE 1 Search and selection
of CPGs for the prevention,
diagnosis, and treatment of
gestational and congenital
toxoplasmosis
3
the corresponding scores for the individual items in the domains, and the
total was standardized as a percentage over the maximum possible score
for each domain. The following formula was applied for that purpose: (score
obtained minimum possible score)/(maximum
score minimum possible score) 100. The score obtained was the
sum of the scores given to the domain by each of the reviewers: mini-mum
possible score = 1 (strongly disagree) number of items 3 reviewers, and
maximum score = 7 (strongly agree) number of items 3 reviewers.12
Absolute interterter agreement was evaluated using the intraclass
correlation coefficient (ICC) with a 95% confidence interval (CI), based
on a mean rating (k = 3), using a random bidirectional effect model. A
separate standardized score for each of the six domains was calculated
lated and classified as poor (<0.50), moderate (0.50-0.75), good (0.75-0.90)
and excellent agreement (>0.90).17 Data were analyzed using the RStudio
software package.18
3 | RESULTS
A total of 8678 references were identified: 744 toxoplasmosis CPGs
and 7899 prenatal care CPGs in the databases, plus 39 toxoplasmosis
CPGs identified in the repositories included in the search. After
removing duplicates, 8651 single citations were screened, of which 46 were
retrieved for full text review, resulting in eight eligible CPGs Figure 1.19-26
The complete search strategy is shown in Table S2. The CPGs were
published between 2013 and 2019. The characteristics of
the eligible guidelines are shown in Table S3.
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4 CABRA-BAUTISTA ET AL.

TABLE 1 AGREE II domain scores for the eight CPGs included

AGREE II domains

Scope and Stakeholder Rigor of Clarity of Editorial

purpose involvement development presentation Applicability independence Recommended
CPG evaluation (%) (%) (%) (%) (%) (%) for future use

SEIP 2013 33 31 11 85 13 31 At the

Spain-AETSA 98 81 75 100 50 81 R
2014

SOGC 2018 63 30 21 87 13 33 RM

Colombia 2013 91 85 79 98 83 94 R

France-Peyron 81 30 38 70 14 72 RM
et al. 2019

AAP 2017 57 24 34 37 19 69 At the

ACOG 2015 65 37 24 44 6 3 At the

AGDH 2019 98 70 57 85 24 17 RM

Median score 73 34 36 85 17 51 —

Abbreviations: AAP, American Academy of Pediatrics; ACOG, American College of Obstetricians and Gynaecologists; AETSA, Agencia de Evaluacion de Tecnologías
Sanitarias de Andalucía; AGDH, Australian Government Department of Health; R, recommended; RM, recommended with modifications; SEIP,
Spanish Society of Pediatric Infectious Diseases; SOGC, Society of Obstetricians and Gynecologists of Canada.

The approved CPGs included four exclusively for toxoplasmosis

(one for gestational toxoplasmosis, two for CT and one that included
both gestational as well as CT), three prenatal care guidelines and one
guideline for pregnancy infections that included recommendations on
toxoplasmosis.
About the recommendations presented in the CPGs, Australia-
AGDH issues a recommendation on primary prevention, while Spain-
AETSA and the Canadian guide SOGC 2018 contains recommendations
on primary prevention and gestational screening. The Colombian
guideline includes recommendations on primary prevention,
preconceptional and gestational screening (using the IgG avidity test
and IgA serology), diagnosis, and treatment of gestational toxoplasmosis
and foetal infection and diagnosis and treatment of CT. However,
the last two guidelines have not been recently updated.
Regarding recommendations on the treatment of gestational toxo-
plasmosis, France-Peyron et al recommend treatment according to the
trimester in which the maternal infection is documented. Concerning the
treatment of CT, the Spanish CPG (SEIP) provides an approach related to FIGURE 2 Median scores of CPGs appraised against six domains
the classification of the infection (symptomatic, symptomatic with the of the AGREE II instrument (n = 8)
central nervous system and/or ocular involvement, asymptomatic, and
doubtful). In relation to the follow-up, CPG France (Peyron et al) and
Spanish CPG (SEIP) recommend subsequent serological monitoring to (17%; [6%-83%]) and 'stakeholder involvement' (34%; [24%-85%])
the patient until the end of treatment and guarantee ophthalmological domains (Table 1 and Figure 2).
and neurological surveillance until adulthood. These recommendations Of the eight CPGs approved, two are 'recommended', both of
and their reported levels of evidence are presented in Table S4. them developed by government agencies: those published by Colom-bia
The highest scores for all the guidelines were observed in the (all domains >60%) and Spain-AETSA (with five of the six domains
'clarity of presentation' (85%; [37%-100%]) and 'scope and purpose' with scores >60%). Three are 'recommended with modifications'
(73%; [33%-98%]) domains. The score for the 'rigour of development' (SOGC, France-Peyron et al, AGDH), with at least two domains with
domain was 36% with a range between 11% and 79%; the CPGs with scores of 60% or more. Three are 'not recommended' (SEIP, AAP, and
the highest scores in this domain came from Spain-AETSA (75%) and ACOG) because of scores under 30% in three domains Table 1. Abso-
Colombia (79%). The lowest scores were found in the 'applicability' lute interter agreement was rated as moderate for the 'scope and
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CABRA-BAUTISTA ET AL. 5

TABLE 2 Interrater agreement of

Interrater agrees
AGREE II domains of eight CPGs
Intraclass correlation 95% CI of Degree of
Domain coefficient (ICC) the ICC correlation

Scope and purpose 0.70 0.12-0.93 Moderate

Stakeholder involvement 0.85 0.52-0.96 Good

Rigor of development 0.91 0.71-0.98 Excellent

Clarity of presentation 0.90 0.69-0.97 Excellent

Applicability 0.89 0.65-0.97 Good

Editorial independence 0.88 0.64-0.97 Good

The

Intraclass correlation coefficient. Poor (<0.50), moderate (0.50-0.75), good (0.75-0.90), and excellent
(>0.90) agreement.

purpose' domain, and good-to-excellent for the remaining domains to specific guideline information.8,28 The 'applicability' domain
(Table 2). obtained the lowest score (17%); low scores have a strong relationship

with the developers of CPGs. It is expected that any development

team has support from certain governmental institutions or agencies

4 | DISCUSSION with detailed knowledge of the barriers, costs and adherence measurement to the

recommendations, allowing the development of

In this systematic review we found eight CPGs relevant to the prevention, diagnosis, implementable and sustainable CPGs.8,28-30

and treatment of gestational and CT after a careful sea-rch and selection process. In the CPGs developed by scientific societies (SEIP, ACGO,

Most of the CPG included recommendations France-Peyron et al, AAP, and SOGC), the weakest domains were 'rig-our of

based on the prevalence and regional impact of the disease. Two of the development' and 'applicability'. It has been previously

CPGs obtained a rating above 60% in more than four domains and then reported that guidelines developed by scientific societies have a lower
were classified as 'recommended' for its use19,20; this CPGs were developed and probability of being recommended due to their low scores. This could

endorsed by government agencies. From the remaining CPGs, be attributed to less diverse development groups (same specialty) and
three were classified as 'recommended with modifications', 23,24,26 and less interest in implementation.8,28 Additionally, a study that assessed
three (37.5%) were 'not recommended'. 21,22,25 the quality of CPG recommendations reported lower statistically significant scores in

The 'rigour of development' domain is considered the most several aspects of the recently developed AGREE-REX tool, in CPGs developed by

important to assess methodological quality. Some authors have rec- scientific societies.31
recommended the use of a 75% threshold in this domain to rate a CPG Among the strengths of our work, we highlight the use of AGREE II,

as high quality.27 This domain includes a detailed review of the considered a valid and reliable tool for this type of assessment.9 The system-atic

methods employed during evidence search and selection, methods review included explicit eligibility criteria and a comprehensive search in

used in formulating recommendations, considerations about health four databases and repositories, appraisals were carried out independently

benefits and risks, external expert audits and update procedures.27 by three reviewers previously trained in the use of the tool, who also conducted a

Likewise, this domain requires development teams to have sufficient pilot test to address any issues before the assessment.11 More-over, our interter

resources and experts in methodology.28 In this study, only the agreement was found to be good to excellent.

Colombian (79%) and Spanish-AETSA (75%) CPGs, developed by government The AGREE II tool appraises the quality of the methodological

agencies, achieved a score ÿ 75% for this domain.27 development of the CPGs but not so the content or the described rec-

Exploration of the 'rigour of development' domain in the ommendations.28 This is a limitation, considering that the healthcare

remaining six CPGs (SEIP, SOGC, France-Peyron et al, AAP, ACOG, practitioner who uses the toxoplasmosis CPGs is required to use

and AGDH) revealed that three of them lacked methodological information regarding his/her critical judgment when applying the recommendations, based

literature search, while one lacked clear information on disease prevalence, public health conditions and access to health

on that point. Although they all describe a methodology to assess evidence quality services in each country.

and issue a recommendation, one does not apply the We found patterns of clinical significance for treatment according

proposed methodology, and four do not establish an explicit link to the clinical classification of the patient and the long-term follow-up

between the recommendations and the existing evidence. Four fail to of the infected child. These patterns were included in CPGs classified

mention review by external peers before publication; three CPGs fail in this study as not recommended or recommended with modification

to mention a procedure for updating the guidelines. This finding contributed to the tions. Further research may appraise the quality of those

great variation in scores among the CPGs. recommendations—in detail—by using the AGREE-REX tool.31,32 In

Regarding the remaining domains, 'clarity of presentation' and addition, further developments of CPGs in this area must ensure a

'scope and purpose' received the highest scores, both directly related minimum of the 11 key components for high-quality and trustworthy
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6 CABRA-BAUTISTA ET AL.
guidelines, as recommended by The Guidelines International Network
(GIN),33 and also improve the use of the Grading of Recommendations,
Assessment Development and Evaluation (GRADE) system to assess
the quality of the included evidence.34
5 | CONCLUSIONS
Toxoplasmosis is prevalent in many countries, hence the need for
physicians and decision makers to identify the best-quality-published
CPGs pertaining to this disease. Eight toxoplasmosis CPGs were
identified, with a significant variation found in terms of methodological
quality. CPGs developed by government agencies (Colombia and Spain-
AETSA) were 'recommended' for use. The recommendations of
These guidelines are presented according to the context of the disease
in the respective countries but need to be updated. The toxoplasmosis
Guidelines developed by scientific societies require stronger
methodological rigor, and development groups must take into
consideration CPG implementation and sustainability.
CONFLICT OF INTEREST
Ivan D. Florez was the coordinator of the Colombian CPGs program at
the IETS from 2012 to 2014. The other authors declare no conflict of
interest.
AUTHOR CONTRIBUTIONS
Ginna Cabra-Bautista, Beatriz E. Paz-Cordoba, Tatiana Henao-Pab on:
conceptualized the study, developed the search strategy, evaluated the
methodological quality of included studies, data management, drafted
the manuscript, provided content expertise, provided feedback on man-
uscript drafts, and read and approved the final manuscript. Ivan
D. Florez and Mario Delgado-Noguera: conceptualized the study,
developed the search strategy, provided content expertise, wrote
sections of the paper, provided feedback on manuscript drafts, and read
and approved the final manuscript. Jose Andrés Calvache: conceptual-
ized the study, developed the search strategy, data management and
statistical analysis, provided content expertise, wrote sections of the
paper, provided feedback on manuscript drafts, and read and approved
the final manuscript. Ana Milena Bravo: conceptualized the study, pro-
vided content expertise, wrote sections of the paper, provided feed-
back on manuscript drafts, and read and approved the final manuscript.
DATA AVAILABILITY STATEMENT
Data are available on request from the authors.
ORCID
Ginna Cabra-Bautista https://orcid.org/0000-0002-4134-100X Beatriz
E. Paz-Cordoba https://orcid.org/0000-0002-2282-6044 Tatiana
Henao-Pabon https://orcid.org/0000-0002-6002-3584 Ana Milena
Bravo https://orcid.org/0000-0002-9020-1353 Ivan D. Florez
https://orcid.org/0000-0002-0751-8932 Mario Delgado-
Noguera https://orcid.org/0000-0002-1163-2041 Jose Andrés Calvache
https://orcid.org/0000-0001-9421-3717
REFERENCES
1. El Bissati K, Levigne P, Lykins J, et al. Global initiative for congenital
toxoplasmosis: an observational and international comparative clinical
analysis. Emerg Microbes Infect. 2018;7:165. https://doi.org/10.1038/
s41426-018-0164-4
2. de-la-Torre A, Sauer A, Pfaff AW, et al. Severe South American ocular toxoplasmosis
is associated with decreased Ifn-ÿ/Il-17a and increased Il-6/Il-13 intraocular levels.
PLoS Negl Trop Dis. 2013;7(11):e2541. https://doi.org/10.1371/journal.pntd.0002541
3. Behnke MS, Khan A, Wootton JC, Dubey JP, Tang K, Sibley LD. Viru-
lence differences in toxoplasma mediated by amplification of a family
of polymorphic pseudokinases. Proc Natl Acad Sci. 2011;108(23):
9631-9636. https://doi.org/10.1073/pnas.1015338108
4. Lohr KN, Field MJ. (eds). Institute of Medicine (US) Committee to
Advise the Public Health Service on Clinical Practice Guidelines
Clinical Practice Guidelines: Directions for a New Program [Internet].
Washington (DC): National Academies Press; 1990. https://doi.org/
10. 17226/1626
5. Lenzer J, Hoffman J, Furberg C, Loannidis J, Guideline Panel Review
Working Group. Ensuring the integrity of clinical practice guidelines: a
tool for protecting patients. BMJ. 2013;347:f5535. https://doi.org/ 10.1136/
bmj.f5535 6.
Organizacion Panamericana de la salud. Guideline for strengthening national
guide programs informed by evidence. A tool for adapting and
implementing guides in the Americas. Washington, DC: OPS; 2018. http://
iris.paho. org/xmlui/bitstream/handle/123456789/49145/9789275320167_
spa.pdf?sequence=5&isAllowed=y
7. Mejia-Oquendo M, Marulanda-Ibarra E, Gomez-Marin JE. Evaluation of
the impact of the first evidence-based guidelines for congenital
toxoplasmosis in Armenia (Quindío) Colombia: an observational retro-
spective analysis. Lancet Reg Heal Am. 2021;100010. https://
linkinghub.elsevier.com/retrieve/pii/S2667193X21000028 8.
Alonso-Coello P, Irfan A, Sola I, et al., eds. The quality of clinical practice
tice guidelines over the last two decades: a systematic review of guideline
appraisal studies. Which Saf Heal Care. 2010;19(6):e58. https://doi.org/
10.1136/qshc.2010.042077 9. Brouwers MC,
Kho ME, Pt B, et al. AGREE next steps consortium.
Development of the AGREE II, part 1: performance, usefulness and
areas for improvement. Cmaj. 2010;182(10):1045-1052. https://doi. org/
10.1503/cmaj.091714 10.
Brouwers MC, Kho ME, Browman GP, et al. AGREE next steps con-
sortium. Development of the AGREE II, part 2: assessment of validity of
items and tools to support application. CMAJ. 2010;182(10):E472- E478.
https://doi.org/10.1503/cmaj.091716
11. AGREE Next Steps Consortium My AGREE PLUS Canada: Canadian
Institutes of Health Research; 2010. http://www.agreetrust.org/resource-
centre/agree-plus/ 12. AGREE
Next Steps Consortium The AGREE II Instrument [Electronic version] ; 2017.
13. Yan J, Min J, Zhou B. Diagnosis of pheochromocytoma: a clinical practice
tice guideline appraisal using AGREE II instrument. J Eval Clin Pract.
2013;19(4):626-632.
14. Lam WMJ, Al-Khalifah R, Florez ID, et al. Management of type 2 day-
betes using non-insulin glucose-lowering therapies: a critical appraisal of
clinical practice guidelines with the AGREE II instrument. Diabet Med.
2020;37(4):636-647.
15. Von Elm E, Altman DG, Egger M, et al. The strengthening the
reporting of observational studies in epidemiology (STROBE)
statement: guidelines for reporting observational studies. Int J Surg.
2014;12(12):1495-1499. https://doi.org/10.1016/j.ijsu.
2014.07.013
16. Colombia Ministerio de Salud Resolucion 8430 [Internet]. 1993. https://
www.minsalud.gov.co/sites/rid/Lists/BibliotecaDigital/RIDE/DE/DIJ/
RESOLUCION-8430-DE-1993.PDF . Accessed April 30, 2021
Machine Translated by Google
CABRA-BAUTISTA ET AL.
17. Koo TK, Li MY. A guideline of selecting and reporting Intraclass correlation
coefficients for reliability research. J Chiropr Med 2016;15(2): 155-163.
https://doi.org/10.1016/j.jcm.2016.02.012 18. RStudio
Team (2020). RStudio: Integrated Development for R. RStudio,
PBC. http://www.rstudio.com/
19. Colombia Ministry of Health and Social Protection - Colciencias.
SECTION 4. INFECTIONS IN EMBARAZO: toxoplasmosis. Clinical
Practice Guide for prevention, early detection and treatment of
ÿ
embarassment, childbirth or postpartum [Internet]; Bogotá. Colombia:
Ministry of Health and Social Protection - Colciencias; 2013:369-398. http://
gpc.minsalud.gov.co/gpc_sites/Repositorio/Conv_500/GPC_embarazo/
gpc_embarazo.aspx _
20. Working group for the Clinical Practice Guide for postpartum and postpartum
care. Screened for toxoplasmosis. Clinical practice guide for emergency
and postpartum care Ministry of Health, Social Services and Equality
Agencia de Evaluacion de Tecnologías Sanitarias de Andalucía [Internet];
Ministry of Health, Social Services and Equality; 2014:104-109. https://
portal.guiasalud.es/wp-content/uploads/2018/12/GPC_533_Embarazo_
AETSA_compl.pdf 21. American College of Obstetricians and Gynecologists.
Practice bulletin
no. 151: cytomegalovirus, parvovirus B19, varicella zoster, and toxoplasmosis
in pregnancy. Note Gynecol. 2015;125(6):1510-1525. https://www.acog.org/
clinical/clinical-guidance/practice-bulletin/articles/ 2015/06/cytomegalovirus-
parvovirus-b19-varicella-zoster-and-toxoplas mosis-in-pregnancy 22.
Baquero-Artigao F , Del Castillo MF, Fuentes Corripio I, et al.
Congenital and Perinatal Infection Working Group of the Spanish
Sociedad de Infectología Pediátrica (SEIP). Guide from the Spanish
Society of Pediatric Infectology for the diagnosis and treatment of
congenital toxoplasmosis. An Pediatr. 2013; 79(2):116.e1-116.e16. https://
doi.org/10.1016/j.anpedi.2012. 12,001
23. Paquet C, Yudin MH. No. 285-toxoplasmosis in pregnancy: prevention,
screening, and treatment. J Obs Gynaecol Can. 2018;40(8):e687- e693.
https://doi.org/10.1016/j.jogc.2018.05.036 24. Peyron
F, L'ollivier C, Mandelbrot L, et al. Maternal and congenital toxoplasmosis:
diagnosis and treatment recommendations of a French multidisciplinary
working group. Pathogens. 2019;8(1):1-15. https:// doi.org/10.3390/
pathogens8010024
25. Maldonado YA, Read JS, AAP Committee on Infectious Diseases.
Diagnosis, treatment, and prevention of congenital toxoplasmosis in the
United States. Pediatrics. 2017;139(2):e20163860. https://doi. org/
10.1542/peds.2016-3860
26. Department of Health. Clinical Practice Guidelines: Pregnancy Care.
Canberra: Australian Government Department of Health; 2020. https://
www.health.gov.au/resources/pregnancy-care-guidelines
7
27. Brouwers MC, Spithoff K, Lavis J, Kho ME, Makarski J, Florez ID.
What to do with all the AGREEs? The AGREE portfolio of tools to
support the guideline enterprise. J Clin Epidemiol. 2020;125:191-197.
https://doi.org/10.1016/j.jclinepi.2020.05.025
28. Armstrong JJ, Goldfarb AM, Instrum RS, MacDermid JC. Improve-
ment evident but still necessary in clinical practice guideline quality: a
systematic review. J Clin Epidemiol. 2017;81:13-21. https://doi.org/10.1016/
j.jclinepi.2016.08.005 _
29. Cabra-Bautista G, Florez ID, Calvache JA. Clinical practice guidelines in low
and middle income countries: experiences from Colombia.
J Clin Epidemiol. 2021;(21):S0895-S4356. https://doi.org/10.1016/j.
jclinepi.2021.05.024
30. Browman GP, Somerfield MR, Lyman GH, Brouwers MC. When is good,
good enough? methodological pragmatism for sustainable guideline
development. Implement Sci. 2015;10:28. https://doi.org/
10.1186/s13012-015-0222-4
31. Florez ID, Brouwers MC, Kerkvliet K, et al. Assessment of the quality of
recommendations from 161 clinical practice guidelines using the appraisal
of guidelines for research and evaluation-recommendations excellence
(AGREE-REX) instrument shows there is room for improvement.
Implement Sci. 2020;15(1):79. https://doi.org/10.1186/s13012-020-01036-5
32. Brouwers M, Spithoff K, Kerkvliet K, et al. Development and validation of
a tool to assess the quality of clinical practice guideline recommendations.
JAMA Netw Open. 2020;3(5):e205535. https://doi.org/10.1001/
jamanetworkopen.2020.5535 _
33. Qaseem A, Forland F, Macbeth F, Ollenschläger G, Phillips S, van der
Wees P. Guidelines international network: toward international standards
for clinical practice guidelines. Ann Intern Med. 2012;156(7):525- 531.
https://doi.org/10.7326/0003-4819-156-7-201204030-00009
34. Guyatt G, Oxman AD, Akl EA, et al. GRADE guidelines: 1. Introduction—
GRADE evidence profiles and summary of findings tables. J Clin
Epidemiol. 2011;64(4):383-394. https://doi.org/10.1016/j.jclinepi.2010.04.026
SUPPORTING INFORMATION
Additional supporting information may be found in the online version
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How to cite this article: Cabra-Bautista G, Paz-Cordoba BE,
Henao-Pabon T, et al. Quality of clinical practice guidelines for
gestational and congenital toxoplasmosis: A systematic review
of the literature. J Eval Clin Pract. 2021;1-7. https://doi.org/
10.1111/jep.13612