Prostate cancer (PCa) is the most prevalent cancer in males in Western countries. In Europe, an incidence of 450,000 new cases and a mortality of 107,000 cancer deaths per year have been estimated for 2018 . Prostate-specific antigen (PSA) remains as the most used biomarker in the detection of early PCa. However, since 2009, PSA usefulness in PCa screening has been widely argued following the opposite results obtained in the two largest randomized screening studies. The European Randomized Study of Screening for Prostate Cancer (ERSPC), enrolling 162,387 men between 50 and 74 years old from seven European countries, found a PCa-specific mortality reduction of 20% in the screened group after a median follow-up of 9 years . In evident contrast, the Prostate, Lung, Colorectal, and Ovarian (PLCO) Screening Trial, based on 76,693 men, found no differences in the PCa-specific mortality after 7 years of follow-up between the screened group and the control group . Furthermore, these opposite results were confirmed by both groups increasing the time of follow-up and differences were confirmed by the ERSPC trial .
In 2011 the United States Preventive Services Task Force (USPSTF) strongly advise against PSA screening based on a review of six well-done trials, underlying harms related to subsequent evaluation and treatments . Nevertheless, several studies showed the evidence that screening reduces the risk of metastasis both at diagnosis and during follow-up , . Furthermore, Gulati et al.  suggested that discontinuing PSA screening for all men may generate many avoidable cancer deaths in the next years. On the other hand, Stephan et al.  remarked on methodological limitations in the meta-analysis showing no evidence of a PCa-specific mortality reduction, suggesting the value of multivariable risk-prediction tools to select appropriate treatment or active surveillance. Additionally, in a recent review, Carlsson and Roobol  underlined data emerging in last years that suggest a new approach to PCa screening according to PSA-based risk stratification at an early age. Similarly, Eapen et al.  postulated in favor of a smarter screening approach, based on relatively infrequent PSA testing, consistent use of multivariable risk stratification, and selective treatment focused on patients with high grade PCa.
Clinical practice guidelines (CPGs) are produced to facilitate incorporation of evidence into clinical practice. This is particularly useful when PCa screening remains controversial and guidelines diverge among different medical institutions. Ideally CPGs from different organizations should be based on high quality methodology to achieve similar clinical recommendations. Unfortunately, despite of the enormous energies invested in its realization, the value of CPGs varies considerably. Clinicians should consider recommendations of varying evidence levels differently. A multidisciplinary approach, the description of the sources of information used, and recommendations graded according to level of evidence are necessary items to be considered in a high-quality CPG.
The evidence-based laboratory medicine commission of the Spanish Society of Laboratory Medicine (SEQC-ML) has observed that, despite the obvious involvement of the clinical laboratory in the PCa screening using PSA, some technical aspects have been unremarked among clinicians .
We critically review the characteristics of guidelines about PCa detection, focusing the attention on the laboratory issues considered. In addition, we propose a checklist including several laboratory issues related to PSA measurement that in our opinion should be considered during the development of clinical practice guidelines.
Materials and methods
Information sources, search strategy and study selection
A systematic search was undertaken using several electronic databases: Medline/PubMed, Web of Science and Scopus. A strategic search was done by one reviewer looking for combinations of the following search terms: as publication type (“Guideline”, “Practice Guideline”), as medical subject heading MeSH (“Guidelines as Topic”, “Prostatic Neoplasms”, “Prostate-Specific Antigen”, “Mass Screening”, “Early Detection of Cancer”, “Diagnosis”) and as free search terms (“guideline”, “prostate cancer”, “prostate specific antigen”, “screening”, “diagnosis”). Guidelines published since 2008 were included in this study. The most updated version of these CPGs was used for the evaluation. This scientific literature search was complemented with three international guideline websites: National Guidelines Clearinghouse , Guidelines International Network Web site  and National Institute for Health and Care Excellence (NICE) .
All the guidelines were considered eligible for inclusion if they met the following criteria: publication type guideline, published in the last 10 years, written in English language.
Data collection process
Two of the authors participated in the final process of guideline selection. The main information, overall recommendation and remarkable quality information of each guideline was extracted by two researcher and independently checked for accuracy by the other researchers. Disagreements between researchers were resolved by discussion.
Each CPG was assessed using a checklist of laboratory issues following the criteria described by Aakre et al. . These criteria were adapted for the PSA assay. Previous versions of the selected GPCs were also checked for this purpose.
The Appraisal of Guidelines Research and Evaluation II (AGREE II) instrument was used to assess the quality of guidelines. This tool has 23 items distributed in six domains: scope and purpose (1), stakeholder involvement (2), rigor of development (3), clarity of presentation (4), applicability (5) and editorial independence (6). Each guideline was rated by four independent appraisers trained using the online training tools recommended by the AGREE collaboration. We also followed the AGREE II instrument guideline to calculate all the scores.
The study selection process is summarized in Figure 1.
A summary of the most relevant characteristics of the 22 selected PCa guidelines are shown in Table 1 , , , , , , , , , , , , , , , , , , , , , , including information concerning, among others, overall recommendation, laboratory issues considered, the description of the sources of information used, and recommendations graded according to the level of evidence. Shared decision considering benefits and harms of PCa screening is a frequent criterion in the evaluated guidelines, while mass screening is not recommended in any guideline. Differences among guidelines go from the non-restricted criteria counseled by the Canadian Urological Association to the recommendation against screening counseled by the American College of Physicians or the Australian Government National Health and Medical Research Council. Furthermore, in the majority of CPGs, screening is explicitly not recommended for men higher than 70 years old or with a life expectancy <10 years.
Table 2 shows a list of laboratory issues that should be examined for PSA measurement. CPGs should report information about these laboratory requirements for high quality results. The list was adapted from Aakre et al.  but modified according to the specific criteria for PSA . The issues were classified following three categories: pre-analytical, analytical and post-analytical phases. Specifically, guidelines should report information about the standard reference material used in the measurement of PSA and how reference ranges were established.
We found data concerning consequences of the adoption of the standard reference material from the World Health Organization (WHO) in PSA testing in only two of 22 CPGs evaluated in this study, the National Academy of Clinical Biochemistry (NACB) and the National Comprehensive Cancer Network (NCCN) guidelines. Also, the guideline of the Canadian Urological Association informs of 20%–25% differences in the concentration of PSA among laboratories.
Previous versions of the selected GPCs were also checked for this purpose. We found relevant data in previous versions of American Urological Association (AUA) guidelines, corresponding to 2009, and the European Association of Urology (EAU) guidelines, corresponding to 2013 and 2015, respectively.
Three of the six CPGs considering laboratory issues remark that assays using the WHO standard offer results 20%–25% lower than those using the initial Hybritech© standard. The other three guidelines only refer that results between different PSA assays are not interchangeable. A summary of these characteristics is shown in Table 3 , , , , . The references cited in these guidelines about PSA standardization are also indicated.
We used the AGREE II instrument to evaluate the quality of the guidelines (Table 4). The overall assessment score ranged from 39.5% to 97% and 13 (59%) of the 22 guidelines obtained an overall assessment score higher to 70%. The highest score was reached by the NICE, the Canadian Task Force on Preventive Health Care and the AUA guidelines.
The usefulness of PSA as a screening test for reducing PCa mortality has been an area of intense controversy. Nowadays, PCa guidelines recommend against routine PSA testing or emphasize that the decision to undergo early PSA testing should be a shared decision between the patient and his physician, considering potential benefits and harms. Nonetheless, discussion about the opportunity of screening remains. Actually, a balance between benefits and harms is the key point to decide to screen. So, active surveillance has been proposed to mitigate harms related with overtreatment in patients with indolent PCa. On the other hand, recently, several studies have noted a reduction in PSA screening rates following the USPSTF ,  recommendation against systematic PSA screening in general population , , . Fleshner et al.  have recently remarked that the withdrawal of PSA screening would prevent all cases of overdiagnosis, but would fail to prevent 100% of avoidable deaths, leading to a 13%–20% increase in PCa-related deaths. These data demonstrate that harms associated with no screening must be also considered and suggest that the process of reviewing evidences and updating recommendations must be continuous. This is reflected in the remarkable changes in the recommendations of the US Preventive Services Task Force along the last decade. In 2008, the panel indicated for men younger than 75 years old that current evidence was insufficient to assess the balance of benefits and harms of PCa screening . Later on, in 2012, the group recommended against PCa screening , but, more recently, in 2018, the panel recommends a shared decision considering benefits and harms for men aged from 55 to 69 years .
On the other hand, additional reflex tests in blood (Prostate Health Index, 4Kscore) or urine (PCA3) has been proposed by several guidelines , , , , , ,  to increase PSA specificity and potentially to decrease the overdiagnosis of indolent PCa. Furthermore, recent data have demonstrated that these biomarkers can also improve the cost-effectiveness of PCa screening , , showing that is more cost-effective the use and development of screening tests than the use of tests after a negative biopsy .
The quality of PCa CPGs is heterogeneous according to published data. Heterogeneity of results has been emphasized by Gupta et al.  using the AGREE II instrument to assess the quality of 13 CPGs selected from 1999 to 2014. The authors showed that the guidelines from the NICE and AUA had the best scores in most domains using this tool. We share the same conclusion, remarking the heterogeneity of quality in guidelines and having obtained a high overall score for NICE and AUA guidelines, as well. In contrast, Qaseem et al.  gave a low overall quality rate to the AUA guideline, remarking the high quality of the American Cancer Society (ACS) guideline. All these results show the need for improving CPGs methodology and quality.
In our study, we found that recommendations were graded according to the level of evidence only in 12 of 22 guidelines evaluated and clear algorithms were only provided for four CPGs. On the other hand, we reviewed the sources of information used in every guideline evaluated in this study. It is remarkable that only one of 22 guidelines was not based on a wide review of data (Table 1). This procedure was specifically discarded by Vickers et al. , focusing their attention on three well-known screening high quality studies (ERSPC, the Prostate Cancer Prevention Trial and the Malmö Project Study), and arguing that regarding to other questions (frequency of PSA testing, indications for biopsy) a systematic review of the literature would be uninformative.
Finally, we found that laboratory issues are frequently (86%) omitted in GPCs. In our opinion, the no inclusion of laboratory medicine specialists in the development process of the guidelines is the main reason for it. The laboratory medicine experts can provide the perspective of the clinical laboratory that sometimes goes unmarked among clinicians .
We found that laboratory medicine specialists participate in only two of the 22 CPGs reviewed in our study, one of them corresponding to the NACB guideline. This guideline widely considers factors in the pre-analytical, analytical and post-analytical phases, which can affect the clinical interpretation of PSA results. We suggest a list of laboratory issues for PSA assays (Table 2) that should be examined in the CPGs, following Aakre et al.  and the specific criteria for PSA reported by Schmeller .
The lack of harmonization of the assays is a major problem in the interpretation of PSA results. The establishment of the 1st International Standard for PSA (World Health Organization 96/670) in 2000 and its adoption as primary calibrator by most manufacturers of PSA assays decreases differences between assays, but concordance has not yet been achieved . Additionally, the reference cut-off of 4 μg/L used to select patients for biopsy was obtained using the traditional Hybritech© standard. Information concerning the influence of WHO standard in the PSA cut-off was directly or indirectly reported by six guidelines (Table 3). Furthermore, the NACB, the 2009 AUA and the 2013 EAU guidelines explain that the initial Hybritech© PSA values are about 20% higher than the assays using the WHO 96/670 standard. The information furnished by the Canadian Urological Association guidelines is less precise, only reporting a 20%–25% variation among laboratories. In consequence, it would be necessary to change the cut-off of 4 μg/L for a cut-off of 3.1 μg/L to obtain similar clinical results. However, published data show that this is not absolutely true. Initial results comparing Access© PSA test using WHO and Hybritech© standards showed that PSA serum levels were 20%–25% lower when WHO standard is adopted . Similar results have been observed for other assays using the reference material from WHO, but there are assays were the differences with the Hybritech© PSA assay are minimal despite the fact that the WHO standard is used. This point was remarked by Stephan et al.  showing that PSA serum levels measured with Elecsys© (using the WHO standard) were very similar to the Hybritech© PSA values. More recently, Foj et al.  compared different assays calibrated against the WHO standard in relation to the Hybritech© PSA values. The authors showed lower PSA results when Advia Centaur©, and Architect© were used, but results for Elecsys©, Lumipulse G 1200©, and Immulite 2000© were substantially similar to the Hybritech© PSA values.
Despite the availability of numerous CPGs considering PCa screening, consensus is currently lacking among them, although opportunistic screening is not recommended. Discrepant methodologies have been applied in the development of these CPGs, even in one case a systematic review of the literature has been explicitly rejected. Also, differences in the quality of the CPGs available have been reported by several authors. We focused our attention on the laboratory issues, because they are frequently omitted in the development of GPCs. The mechanical transfer of the established Hybritech© reference range of <4.0 μg/L to other assays could lead to clinical mistakes in the selection of patients for biopsy. Differences between assays in the measurement of PSA serum levels are not taken into account by the majority of these guidelines. Furthermore, we detected some errors in three of the CPGs about the consequences of the calibration of PSA assays against the WHO. In conclusion, in our opinion, the quality of PCa early detection guidelines could be adequately improved considering the laboratory issues in their development.
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About the article
Published Online: 2019-05-23
Published in Print: 2019-09-25
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: None declared.
Employment or leadership: None declared.
Honorarium: None declared.
Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.