Case-control studies in neurosurgery

A review

Full access

Object

Observational studies, such as cohort and case-control studies, are valuable instruments in evidence-based medicine. Case-control studies, in particular, are becoming increasingly popular in the neurosurgical literature due to their low cost and relative ease of execution; however, no one has yet systematically assessed these types of studies for quality in methodology and reporting.

Methods

The authors performed a literature search using PubMed/MEDLINE to identify all studies that explicitly identified themselves as “case-control” and were published in the JNS Publishing Group journals (Journal of Neurosurgery, Journal of Neurosurgery: Pediatrics, Journal of Neurosurgery: Spine, and Neurosurgical Focus) or Neurosurgery. Each paper was evaluated for 22 descriptive variables and then categorized as having either met or missed the basic definition of a case-control study. All studies that evaluated risk factors for a well-defined outcome were considered true case-control studies. The authors sought to identify key features or phrases that were or were not predictive of a true case-control study. Those papers that satisfied the definition were further evaluated using the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) checklist.

Results

The search detected 67 papers that met the inclusion criteria, of which 32 (48%) represented true case-control studies. The frequency of true case-control studies has not changed with time. Use of odds ratios (ORs) and logistic regression (LR) analysis were strong positive predictors of true case-control studies (for odds ratios, OR 15.33 and 95% CI 4.52–51.97; for logistic regression analysis, OR 8.77 and 95% CI 2.69–28.56). Conversely, negative predictors included focus on a procedure/intervention (OR 0.35, 95% CI 0.13–0.998) and use of the word “outcome” in the Results section (OR 0.23, 95% CI 0.082–0.65). After exclusion of nested case-control studies, the negative correlation between focus on a procedure/intervention and true case-control studies was strengthened (OR 0.053, 95% CI 0.0064–0.44). There was a trend toward a negative association between the use of survival analysis or Kaplan-Meier curves and true case-control studies (OR 0.13, 95% CI 0.015–1.12). True case-control studies were no more likely than their counterparts to use a potential study design “expert” (OR 1.50, 95% CI 0.57–3.95). The overall average STROBE score was 72% (range 50–86%). Examples of reporting deficiencies were reporting of bias (28%), missing data (55%), and funding (44%).

Conclusions

The results of this analysis show that the majority of studies in the neurosurgical literature that identify themselves as “case-control” studies are, in fact, labeled incorrectly. Positive and negative predictors were identified. The authors provide several recommendations that may reverse the incorrect and inappropriate use of the term “case-control” and improve the quality of design and reporting of true case-control studies in neurosurgery.

Abbreviation used in this paper:STROBE = Strengthening the Reporting of Observational Studies in Epidemiology.

Abstract

Object

Observational studies, such as cohort and case-control studies, are valuable instruments in evidence-based medicine. Case-control studies, in particular, are becoming increasingly popular in the neurosurgical literature due to their low cost and relative ease of execution; however, no one has yet systematically assessed these types of studies for quality in methodology and reporting.

Methods

The authors performed a literature search using PubMed/MEDLINE to identify all studies that explicitly identified themselves as “case-control” and were published in the JNS Publishing Group journals (Journal of Neurosurgery, Journal of Neurosurgery: Pediatrics, Journal of Neurosurgery: Spine, and Neurosurgical Focus) or Neurosurgery. Each paper was evaluated for 22 descriptive variables and then categorized as having either met or missed the basic definition of a case-control study. All studies that evaluated risk factors for a well-defined outcome were considered true case-control studies. The authors sought to identify key features or phrases that were or were not predictive of a true case-control study. Those papers that satisfied the definition were further evaluated using the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) checklist.

Results

The search detected 67 papers that met the inclusion criteria, of which 32 (48%) represented true case-control studies. The frequency of true case-control studies has not changed with time. Use of odds ratios (ORs) and logistic regression (LR) analysis were strong positive predictors of true case-control studies (for odds ratios, OR 15.33 and 95% CI 4.52–51.97; for logistic regression analysis, OR 8.77 and 95% CI 2.69–28.56). Conversely, negative predictors included focus on a procedure/intervention (OR 0.35, 95% CI 0.13–0.998) and use of the word “outcome” in the Results section (OR 0.23, 95% CI 0.082–0.65). After exclusion of nested case-control studies, the negative correlation between focus on a procedure/intervention and true case-control studies was strengthened (OR 0.053, 95% CI 0.0064–0.44). There was a trend toward a negative association between the use of survival analysis or Kaplan-Meier curves and true case-control studies (OR 0.13, 95% CI 0.015–1.12). True case-control studies were no more likely than their counterparts to use a potential study design “expert” (OR 1.50, 95% CI 0.57–3.95). The overall average STROBE score was 72% (range 50–86%). Examples of reporting deficiencies were reporting of bias (28%), missing data (55%), and funding (44%).

Conclusions

The results of this analysis show that the majority of studies in the neurosurgical literature that identify themselves as “case-control” studies are, in fact, labeled incorrectly. Positive and negative predictors were identified. The authors provide several recommendations that may reverse the incorrect and inappropriate use of the term “case-control” and improve the quality of design and reporting of true case-control studies in neurosurgery.

Observational epidemiological studies have long been used as evidence-based tools for assessing disease risk and improving patient outcomes. Observational studies are defined as etiologic or effectiveness studies using various study designs, such as cross-sectional design, case series, case-control design, design with historical controls, or cohort design. They are ideal for research in surgery, in which inclusion of a placebo or no-treatment group is often not possible due to safety risk or ethical concerns, or when randomized controlled trials (the gold standard in trial design) are logistically too complex, expensive, time consuming, and may not be the ideal tool to answer a clinical question.80

A case-control study compares a group with a known disease status (or other well-defined outcome) to a control group without the disease status and looks back in time to identify whether the presence or absence of a disease attribute(s) differs between these 2 groups (Fig. 1). Case-control studies are most useful in instances where prospective studies are too inefficient or costly, such as in rare diseases and diseases with a long latency period. They are cheap and efficient but susceptible to recall bias, selection bias, and confounding and, therefore, rely heavily on sound study design.50,91 Cohort studies, on the other hand, compare a group of individuals exposed to a factor(s) hypothesized to influence the probability of disease occurrence or other outcome. Cohort studies may be designed as prospective (the investigator begins the study before the disease develops), retrospective (the investigator begins the study after the disease has developed), or ambispective (studying a disease state both before and after a disease develops). They are useful for studying common diseases and rare exposures but are susceptible to selection bias and loss to follow-up. Cohort studies also clearly define the temporal sequence of events leading to the disease or outcome and allow for calculation of disease incidence and relative risk or risk ratios.33,50

Fig. 1.
Fig. 1.

Case-control versus cohort study design. Case-control studies are designed to assess differences in risk between 2 or more groups with a known disease status. Cohort studies assess differences in outcome between 2 or more groups with a known risk status.

Case-control studies that are incorrectly designed or interpreted can easily lead to erroneous conclusions about disease causation or treatment efficacy. A review of case-control studies in the surgery literature by Mihailovic et al.65 shows that many articles reported as “case-control” are in fact not case-control studies but instead atypical or misreported case series and cohort studies. Such mistakes in research design, interpretation, or reporting have led some journals to implement checklists to standardize the reporting of research studies. The journal Neurosurgery, for example, now requires the authors of all observational epidemiological studies to submit a completed checklist from the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) consortium, a group of biostatisticians, epidemiologists, and other methodological experts who devised standardized guidelines for the reporting of epidemiological studies in medicine.5,107 Nevertheless, there remains no standardized method for evaluating the basic design of observational epidemiological studies in medicine, and no one has yet addressed this issue in the neurosurgical literature.

The primary aim of this study was to determine whether studies reported as “case-control” in the JNS Publishing Group Journals (Journal of Neurosurgery, Journal of Neurosurgery: Pediatrics, Journal of Neurosurgery: Spine, and Neurosurgical Focus) or Neurosurgery met a standard definition. The secondary aims of the study were to determine key characteristics of a study that were predictive of true case-control design and to evaluate the reporting of true case-control studies using the STROBE checklist.

Methods

Search Criteria

A PubMed/MEDLINE search was performed for all articles in the JNS Publishing Group journals (Journal of Neurosurgery, Journal of Neurosurgery: Pediatrics, Journal of Neurosurgery: Spine, and Neurosurgical Focus) and Neurosurgery through July 2013 with the terms “case control,” “case-control,” or “case-controlled” anywhere in the text. Inclusion criteria restricted our analysis to only original research articles and use of the phrase “case-control” in reference to the study being presented. Editorials, review articles, meta-analyses, and cost-effectiveness analyses were excluded. An article was likewise excluded if the text did not contain the phrase “case-control” or if this term was used in reference to another study.

Definition

A study was considered a true case-control study if it included 3 basic components: 1) a group of patients with a disease or who have experienced some event are compared with a control group without the disease or event; 2) a retrospective evaluation from the time point of a known outcome is made; and 3) the focus of the study is on identifying disease or event risk factors/associations/causality. This is consistent with multiple classic definitions of an epidemiological case-control study1,14,50 and expands the definition to include the smaller study types that are common to neurosurgery. Each study was independently evaluated by 2 authors (C.L.N. and P.K.) as having met or missed this definition.

A nested case-control study is one in which cases and controls are drawn from a cohort study population; time-matching is an essential feature of a nested case-control study. Controls are matched to cases on age, date of entry into the cohort, length of time in the cohort, or a combination of these measures, thus allowing for the potential confounding effect of time in the analysis.26,57 For those studies that did satisfy the case-control definition, we recorded whether matching was used and whether the case-control analysis was part of a formal (true-nested) or nonformal (pseudo-nested) longitudinal observational study. The studies that did not meet our definition of a case-control study were further assessed as to whether they were actually retrospective cohort studies, with or without matching (Fig. 2).

Fig. 2.
Fig. 2.

Study design flow chart. A literature search using PubMed/MEDLINE for case-control studies in the JNS Publishing Group journals (Journal of Neurosurgery, Journal of Neurosurgery: Pediatrics, Journal of Neurosurgery: Spine, and Neurosurgical Focus) and Neurosurgery through July 2013 produced 182 hits. Of these publications, 67 explicitly referred to the study as “case-control” in the text and met the inclusion criteria. Thirty-two of these 67 studies met the basic definition of a case-control study.

Data Collection

The following data points were collected independently by 2 authors (C.L.N. and P.K.) for each paper that was analyzed: year of publication; journal (JNS Publishing Group journal or Neurosurgery); topic (spine, trauma, vascular, functional/epilepsy, neurooncology, pediatrics, and other); number of authors; whether the focus of the paper was on a procedure or disease/event causation, risk or association; country of origin (classified as “United States” or “other” based on where the study took place; the country of the lead author was used when study location was not specified); whether it satisfied our definition of a case-control study; presence or acknowledgment of one or more individuals identified in the paper who conceivably had additional training in case-control techniques, such as a biostatistician, epidemiologist, or one with a master's degree in public health; use of odds ratios or logistic regression analysis; and presence of blinding (as specifically stated within the manuscript). We evaluated whether the authors attempted to control for confounding through use of matching, multivariate logistic regression, or stratified analysis and noted whether the authors actually used the word “confound” or “confounding” anywhere in the text of their study. We also recorded whether certain key words or phrases were used in the article: “prospective case-control”; “cohort” in the Methods, Results, or Discussion section; and “outcome” in the Results section. Finally, we noted if Kaplan-Meier curves/survival analysis or propensity-score matching was conducted.

True case-control studies were further evaluated using the 22-point STROBE checklist (see Appendix) and the accompanying Explanation and Elaboration article.107,110 The STROBE checklist actually consists of 33 individual criteria grouped together by topic; each study we analyzed was assigned a 0, 1, or “not-applicable” (NA) for each of the 33 items. Each article was given a score calculated as the number of applicable STROBE criteria that were successfully met divided by the number of applicable STROBE criteria. For example, if a study did not use matching, this criterion was not factored into the denominator and the maximum score was 32, not 33. Two authors (C.L.N. and P.K.) independently evaluated every article, and disagreements were addressed by consensus.

Questions

We sought to identify features of an article that were predictive of whether it was truly a case-control study. We also sought to determine the proportion of true case-control studies over time. Year of publication was divided into 4 groups for comparisons: those published before 2000, from 2000 to 2004, from 2005 to 2009, and from 2010 to 2013.

Statistical Methods

Bivariate logistic regression models were generated to assess the associations between select parameters and the dichotomous variable indicating whether a study was a true case-control study (yes/no). All p values are 2-sided, and p < 0.05 was considered significant. Stata/SE 11.2 (StataCorp) was used for all analyses.

Results

Search Results

An initial PubMed/MEDLINE search for articles containing “case control,” “case-control,” or “case-controlled” in the JNS Publishing Group journals or Neurosurgery through July 2013 produced 182 articles. One hundred six search results did not include any of the search phrases in the article text. Nine additional articles were excluded: one was a cost-effectiveness analysis,29 and the rest were meta-analyses or literature reviews.6,23,30,31,34,45,61,98 Thus, 67 articles were included for analysis (Fig. 2).4,7,8,10,13,16–19,21,22,24,25,27,28,32,35,36,38–44,47,49,51,54–56,58–60,62,63,66–73,76,77,79,81,82,84,86–89,92–96,100–104,106,108,109 Forty-one (61%) were published in The Journal of Neurosurgery or one of its subsidiaries.

Features of Our 67 Articles

Descriptive characteristics are shown in Table 1. The mean and median number of authors was 6 (range of 1–12). Almost half of the articles (30 [45%]) had as a coauthor or acknowledged a potential case-control study design expert. Thirty-eight studies (57%) focused on disease causation, risk, or association, while 25 (37%) focused on evaluating a surgical procedure or other medical intervention. Twenty-eight (42%) used odds ratios and 24 (36%) used logistic regression as part of the data analysis. Forty-three papers (64%) potentially addressed confounding through matching, stratified analysis, or multivariate logistic regression, but only 14 (21%) actually used the word “confound” or “confounding” anywhere in the text of their study. Six studies (9%) attempted some form of blinding. Thirty-two papers (48%) met our definition of a true case-control study.

TABLE 1:

Characteristics of the 67 case-control studies in the neurosurgical literature

DescriptionResult (%)
year of publication
 <20006 (9)
 2000–200410 (15)
 2005–200926 (39)
 >200925 (37)
journal
 JNS Publishing Group journals*41 (61)
 Neurosurgery26 (38)
topic
 vascular4,16,28,38,39,40,42,47,49,54,55,60,77,84,89,103,104,106,108,10920 (30)
 neurooncology8,17,19,35,36,43,56,58,59,79,92–94,101,10215 (22)
 pediatric7,21,22,44,72,73,967 (10)
 spine10,24,27,51,62,68,69,76,81,8610 (15)
 trauma13,67,82,95,1005 (7)
 functional/epilepsy25,32,633 (4)
 other18,41,66,70,71,87,887 (10)
case-control expert
 studies acknowledging study design expert30 (45)
country of origin
 US42 (63)
 other25 (37)
study design characteristics
 focus on procedure/intervention evaluation25 (37)
 focus on disease or event causation/risk/association38 (57)
 attempted blinding6 (9)
 addressed confounding43 (64)
 used logistic regression analysis24 (36)
 used odds ratio (OR)28 (42)
 used propensity score matching3 (4)
 used survival analysis/Kaplan-Meier curves8 (12)
terminology in reference to the study
 used the word “confounding”14 (21)
 used the word “cohort” in the Methods, Results, Discussion32 (48)
 used the word “outcome” in Results31 (46)
 used the phrase “prospective case-control”8 (12)
studies that met the definition of a case-control study
 studies that met case-control definition32 (48)
 utilized matching14 (44)
 true nested case-control studies4 (13)
 pseudo-nested case-control studies7 (22)
studies that did not meet the definition of a case-control study
 studies that did not meet case-control definition35 (52)
 retrospective cohort study w/ matching15 (43)
 retrospective cohort study w/o matching8 (23)

Journal of Neurosurgery, Journal of Neurosurgery: Pediatrics, Journal of Neurosurgery: Spine, and Neurosurgical Focus.

Predictors of True Case-Control Studies

Ten potential predictors underwent bivariate testing, the results of which are shown in Table 2. There were 3 strong positive predictors of a true case-control study: 1) focus on disease/event causation, risk, or association (all true case-control studies satisfied this, so an odds ratio could not be calculated); 2) use of odds ratios (OR 15.33, 95% CI 4.52–51.97); and 3) use of logistic regression analysis (OR 8.77, 95% CI 2.69–28.56). There were 2 statistically significant negative predictors of true case-control studies: focus on a procedure or evaluation (OR 0.35, 95% CI 0.13–0.998) and use of the word “outcome” or “outcomes” in the Results section (OR 0.23, 95% CI 0.082–0.65). There was a trend toward a negative association between use of survival analysis or Kaplan-Meier curves and true case-control studies (OR = 0.13, 95% CI, 0.015–1.12). There was no association between true case-control study design and time of publication, whether the study was performed in the United States, or whether a potential expert was used.

TABLE 2:

Experimental statistics: exponentiated coefficients with 95% confidence intervals from logistic regression analysis

ParameterTrue Case-Control (Yes/No)False Case-Control (Yes/No)Odds Ratio (95% CI)
study from the US18/1424/110.59 (0.22–1.60)
focus on procedure/intervention8/2417/180.35 (0.13–0.0998)*
focus on disease event causation, risk, or association32/06/29n/a
use of logistic regression analysis19/135/308.77 (2.69–28.56)
used an odds ratio23/95/3015.33 (4.52–51.97)
used a potential “expert”16/1614/211.50 (0.57–3.95)
used the word “cohort” in the Methods, Results, or Discussion14/1818/170.74 (0.28–1.92)
used the word “outcome” in Results9/2322/130.23 (0.082–0.65)§
used survival analysis or Kaplan-Meier curves1/317/280.13 (0.015–1.12)
publication date vs <20003/293/32
 2000–20047/253/322.33 (0.29–18.96)
 2005–200912/2014/210.86 (0.15–5.06)
 2010–201310/2215/200.67 (0.11–3.99)

p < 0.05.

Focus on disease event causation, risk, or association was found in all articles that met the definition of the case-control study.

p < 0.001.

p < 0.01.

Sensitivity Analysis

After removal of the 11 nested and pseudo-nested case-control studies, we repeated statistical testing on the following parameters: focus on procedure/intervention evaluation; use of the word “cohort” in the Methods, Results, or Discussion section; and use of survival analysis or Kaplan-Meier curves. When these 11 studies were excluded, the negative correlation between true case-control studies and procedure/intervention evaluation was strengthened (OR 0.053, 95% CI 0.0064–0.44). True and false case-control studies were still not significantly different in use of survival analysis or Kaplan-Meier curves (OR 0.20, 95% CI 0.023–1.76) or use of the word “cohort” (OR 0.38, 95% CI 0.12–1.20).

STROBE Checklist

Figure 3 depicts the number of case-control studies that received a “yes” response to each of the 33 questions in the STROBE checklist. (Note: For those papers that did not receive a “yes” answer, either the question was not applicable or it was not addressed in that study.) The average STROBE score for the 32 true case-control studies was 72% (range 50%–86%). There were 17 questions (52%) that were applicable and satisfactorily answered by 21 or more papers. The other 16 questions were answered by 16 or fewer papers. Less than half of true case-control studies (28%) described any efforts to address potential bias (as described by Item 9 of the STROBE checklist); 27% described methods to examine subgroups and interactions (Item 12b); and only 44% gave any source of funding (Item 22). Of note, only 3 (9%) described how the study size was derived (Item 10), and none of the studies reported the number of individuals at each stage of the study, gave reasons for nonparticipation at each stage, or used a flow diagram (Items 13a–c). The Discussion sections were generally well reported. All studies adequately summarized key results (Item 18); 91% gave a cautious overall interpretation of the results (Item 20); 94% discussed the generalizability of the study (Item 21); and 75% provided information on study limitations (Item 19).

Fig. 3.
Fig. 3.

STROBE evaluation of true case-control studies. Item 1 (Q1) of the STROBE checklist refers to the title and Abstract, Items 2–3 (Q2–3) refer to the Introduction, Items 4–12 (Q4–12) refer to Methods, Items 13–17 (Q13–17) refer to Results, and Items 18–22 (Q18–22) refer to the Discussion.

Discussion

So-called case-control studies are appearing with increasing frequency in the neurosurgical literature. Our study indicates that case-control studies are not well understood within the academic neurosurgical community. Over half of the studies that were reviewed incorrectly or inappropriately used the term “case-control.” Many of these were, in fact, retrospective cohort studies. The authors of 8 studies used the phrase “prospective case-control” to describe their study, which is a complete misnomer as all case-control studies are, by definition, retrospective. A recent study by Hatlen et al. on the use of programmable versus nonprogrammable shunts incorrectly recommended the need for “prospective case-control studies to confirm these data” in their abstract.37 Incorrect terminology use also occurs in other neurosurgical journals.12 Some experts, including the AANS/CNS Joint Guidelines Committee, view well-designed case-control and cohort studies as comparable in terms of strength of evidence, which highlights the fact that high-quality results can be obtained from rigorous retrospective research.64,83 Additionally, well-designed observational studies have been shown to closely approximate the treatment effect magnitudes obtained in randomized controlled trials.20 This underscores the value of conducting and correctly labeling well-designed case-control and cohort studies in a field in which randomized controlled trials are often not possible due to ethical, logistical, and financial limitations.

Predictors of True Case-Control Studies

Three factors were strongly and positively associated with a study being a true case-control study: focus on disease causation or risk, use of odds ratios, and use of logistic regression analysis. Focus on disease causation or risk is the foundation of a case-control study. The latter two factors form the statistical backbone of case-control study analysis and, thus, one would expect that true case-control studies are more likely to use them.1,50,85,90

Focus on a procedure or evaluation and use of the word “outcome” in the Results section proved to be statistically significant negative predictors of true case-control design. The strength of the negative association between focus on a procedure and true case-control study design was increased upon removal of the nested case-control studies (sensitivity analysis). An “outcome” is a specified event that occurs with the passage of time and is a key feature of cohort and randomized controlled studies.20,33 In a case-control study, the outcome has already occurred and the focus is on events or exposures that led to the development of the event.50,91 Therefore, unless the case-control study is part of a larger cohort study (that is, “nested”), any description of “outcomes” in the Results section should alert the reader or reviewer that the study is likely not a true case-control study.

Lack of a negative association between the use of the word “cohort” and true case-control design is likely due to the fact that some authors use this word incorrectly. It is often used to identify a group of patients when it should be used to identify a group of patients that are followed in time for the development of one or more prespecified outcome(s).1,33,50 Additionally, survival analysis or presentation of Kaplan-Meier curves details the development of an outcome—such as death or treatment failure within a cohort of patients—and, thus, should not be part of a true case-control analysis.9,48 Therefore, use of the word “cohort” or survival analysis should at least raise a reviewer's suspicion as to the true study design.

Interestingly, we found no correlation between the use of a plausible “expert” and true case-control design. This is contrary to our recent study evaluating meta-analyses in the neurosurgical literature, in which we did find a strong positive correlation.53 We offer 4 possible explanations: 1) our study was underpowered to detect a positive impact; 2) experts were not consistently acknowledged in true case-control studies; 3) acknowledged experts did not consistently participate in either the design or reporting of the study, but only performed statistical analysis; and 4) some individuals considered experts may not be able to distinguish between study designs. Several prominent epidemiologists have commented on the final point. David Sackett, undoubtedly with some element of tongue-in-cheek, stated that he would trust only 6 people in the world to conduct a proper case-control study.91 Kenneth Rothman commented, “…many studies have been conducted by would-be investigators who lack even a rudimentary appreciation for epidemiologic principles.”85 Despite the lack of association between true case-control design and use of a potential expert, it is only logical that clinicians should partner with or seek advice from someone who has additional knowledge in the design, analysis, and reporting of case-control studies.

Mihailovic et al.65 performed a study similar to ours and searched 6 general surgery journals over a 5-year period and found 55 reported case-control studies, of which only 19 (35%) met their definition. They too found that use of odds ratios and logistic regression analysis were positive predictors of true case-control study design (OR 15.3 for odds ratios and OR 3.6 for logistic regression analysis). They also found that if the focus of the study was on the evaluation of a surgical procedure, the odds of that study being a true case-control study was five times less likely.

We found that a mere 14 (21%) of 67 papers even used the words “confound” or “confounding” in their studies, but we generously credited 43 papers (64%) with a potential attempt to control for it by use of matching, Mantel-Haenszel methods, or multivariate logistic regression. Confounding is an important aspect of case-control studies and can be thought of as a mixing of effects. The study exposure may appear to elevate or reduce the risk of disease because the effect of extraneous factors is mistaken for—or mixed with—the actual exposure effect.85,90 From an epidemiological standpoint, a confounder must be an extraneous risk factor for the disease and associated with the exposure, but not affected by the exposure or the disease.85 Thorough knowledge of the study topic and inclusion of relevant covariates in the data analysis are the best means to control for known and unknown confounders.50

STROBE

The STROBE Initiative began in 2004 and culminated with the STROBE Statement in October 2007. Since its inception, STROBE has been well received and accepted by numerous peer-reviewed journals. With few exceptions, case-control studies in neurosurgery are adequately reporting the title, abstract, and introduction sections and sufficiently discussing the results. However, only 3 (9%) of the 32 studies calculated the number of participants needed to detect a specific difference between cases and controls (Item 10), only 14 papers (44%) gave any source of funding or described the role of the funders in the study (Item 22), and only 9 papers (28%) mentioned any effort to control for potential bias (Item 9).

Bias refers to any systematic error in the design, conduct, or analysis of a study that results in a mistaken estimate of an exposure's effect on the risk of disease or other outcome.3 Selection bias may be decreased by selecting controls from the same population as cases so that both groups have the same potential for exposure during the time period of risk under consideration.99 Recall and observer or information bias may be mitigated by selecting variables that do not rely on a subject's memory and blinding data gatherers to the disease status of each participant, a practice that was exercised in only 5 studies analyzed here.

The average STROBE score of 72% (range 50%–86%) obtained in our study is on par or higher than that reported in family medicine,52 periodontology,105 oncology,78 and gastroenterology.75 The reporting of bias, missing data, the reasons for and the timeline of data exclusion, funding sources, and explanations of study size have been identified by multiple groups as major weaknesses of observational studies in other fields of medicine.46,52,78,105 These are not unique problems to those using the STROBE checklist, as other groups have identified reporting of bias and funding as substandard and have used other criteria, such as the Standards for the Reporting of Diagnostic Accuracy (STARD) and custom checklists.11,15,97 The STROBE Statement was originally designed to give “guidance to authors about how to improve reporting of observational studies and [facilitate] critical appraisal and interpretation of studies by reviewers, journal editors and readers.”107 It should not be viewed as a set of absolute rules.

Our findings suggest that a reporting checklist, such as STROBE or the United Kingdom's National Health Institute Critical Appraisal Skills Program (available at: http://www.casp-uk.net/wp-content/uploads/2011/11/CASP-Case-Control-Study-Checklist-31.05.13.pdf), may also be used as a guide when designing a case-control study, which is a practice that was not reported in any of the papers in our study. It is likely that the more items on the checklist that a study adequately satisfies, the higher the level of quality of the study will be.2 Authors should be aware of and use the benefits of the EQUATOR (Enhancing the QUAlity and Transparency Of health Research) network (http://www.equator-network.org), a multidisciplinary organization whose goal is to improve the quality of research publications and of research itself.

Study Limitations

We admit that our use of the phrase “neurosurgical literature” is imprecise as we limited our search to only the Journal of Neurosurgery and Neurosurgery, the two dedicated neurosurgical publications with the highest impact factors (3.148 and 2.532, respectively, for 2012) and the Journal of Neurosurgery's sister publications. Studies in the field reported as “case control” surely exist elsewhere,12 and it is unknown whether expanding our search to other journals would have changed our results. Our initial search strategy may have missed self-identified “case-control” studies within these journals, as well as case-control studies that were not identified as such; however, 63% of the studies identified by our initial search did not explicitly identify themselves as case-control studies, suggesting that our search terms cast a broad net and identified nearly all eligible papers for the study in these journals. Finally, there is an element of subjectivity with several STROBE checklist items that required deliberation and judgment. We attempted to minimize this limitation by often giving authors the benefit of the doubt, consulting the Explanation and Elaboration article107 frequently, and reaching consensus opinion with each item.

Recommendations

Based on the results of our study, we offer the following recommendations.

  1. A clear definition of a case-control study should be adopted and understood by authors and reviewers. We have identified several key phrases and components that may help to distinguish a case-control study from others.

  2. Clinicians should attempt to work with someone who conceivably has additional knowledge of a case-control design, such as an epidemiologist or biostatistician.

  3. The JNS Publishing Group and other publishers of neurosurgical publications should require authors to use the STROBE checklist as Neurosurgery already does. Reviewers also need to be familiar with the checklist or given training to understand it better so they can recognize whether the items have been fulfilled or not.

  4. We encourage researchers to consult the STROBE checklist when designing their case-control studies.

Conclusions

As Newman et al. state, “Case-control studies are the ‘house red' on the research design wine list: more modest and a little riskier than the other selections but much less expensive and sometimes surprisingly good.”74 They have many positive attributes, can be viewed as a more efficient version of a corresponding cohort study, and are appearing with greater frequency in the leading neurosurgical publications. Rothman stated that, “the bad reputation once suffered by case-control studies stems more from instances of poor conduct and overinterpretation of results than from any inherent weakness in the approach.”85 The challenges with case-control studies—notably bias and confounding—can be overcome with a solid foundation of knowledge, thoughtful design, and data analysis. Our work has demonstrated that many studies are incorrectly labeled as “case-control,” and bona fide case-control studies often lack rigor in reporting. Journals need to validate those studies that use evidenced-based medicine terminology to ensure the highest level of quality.

Acknowledgment

We thank Andrew J. Gienapp for technical and copy editing, preparation of the manuscript and figures for publishing, and publication assistance with this manuscript.

Disclosure

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author contributions to the study and manuscript preparation include the following. Conception and design: Klimo, Nesvick. Acquisition of data: Klimo, Nesvick. Analysis and interpretation of data: Klimo, Nesvick, Thompson. Drafting the article: Nesvick. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Klimo. Statistical analysis: Thompson.

References

  • 1

    Armenian HK: The Case-Control Method: Design and Applications New YorkOxford University Press2009

  • 2

    Arrese ISarabia RPintado RDelgado-Rodriguez M: Flow-diverter devices for intracranial aneurysms: systematic review and meta-analysis. Neurosurgery 73:1932002013

  • 3

    Aydin DFeychting MSchüz JAndersen TVPoulsen AHProchazka M: Predictors and overestimation of recalled mobile phone use among children and adolescents. Prog Biophys Mol Biol 107:3563612011

  • 4

    Badjatia NFernandez LSchmidt JMLee KClaassen JConnolly ES: Impact of induced normothermia on outcome after subarachnoid hemorrhage: a case-control study. Neurosurgery 66:6967012010

  • 5

    Barker FG IIOyesiku NM: The Registrar. Improving the quality of research reports in Neurosurgery: the CONSORT, PRISMA, MOOSE, STARD, STROBE statements and the EQUATOR network. Neurosurgery 68:152011

  • 6

    Barnes BAlexander JTBranch CL Jr: Postoperative Level 1 anticoagulation therapy and spinal surgery: practical guidelines for management. Neurosurg Focus 17:4E52004

  • 7

    Berger RPAdelson PDPierce MCDulani TCassidy LDKochanek PM: Serum neuron-specific enolase, S100B, and myelin basic protein concentrations after inflicted and noninflicted traumatic brain injury in children. J Neurosurg 103:1 Suppl61682005

  • 8

    Bergsneider MXue KSuh JDWang MB: Barrier-limited multimodality closure for reconstruction of wide sellar openings. Neurosurgery 71:1 Suppl Operative68762012

  • 9

    Bland JMAltman DG: Survival probabilities (the Kaplan-Meier method). BMJ 317:157215801998

  • 10

    Börm WKast ERichter HPMohr K: Anterior screw fixation in type II odontoid fractures: is there a difference in outcome between age groups?. Neurosurgery 52:108910942003

  • 11

    Bossuyt PMReitsma JBBruns DEGatsonis CAGlasziou PPIrwig LM: The STARD statement for reporting studies of diagnostic accuracy: explanation and elaboration. Ann Intern Med 138:W1W122003

  • 12

    Brandão RACosta BSDellaretti MAde Carvalho GTFaria MPde Sousa AA: Efficacy and safety of a porcine collagen sponge for cranial neurosurgery: a prospective case-control study. World Neurosurg 79:5445502013

  • 13

    Bratton SLDavis RL: Acute lung injury in isolated traumatic brain injury. Neurosurgery 40:7077121997

  • 14

    Breslow NEDay NE: The Analysis of Case-Control Studies. Statistical Methods in Cancer Research 1:LyonIARC Press1980

  • 15

    Brophy RHGardner MJSaleem OMarx RG: An assessment of the methodological quality of research published in The American Journal of Sports Medicine. Am J Sports Med 33:181218152005

  • 16

    Brott TMandybur TI: Case-control study of clinical outcome after aneurysmal subarachnoid hemorrhage. Neurosurgery 19:8918951986

  • 17

    Chaichana KLZadnik PWeingart JDOlivi AGallia GLBlakeley J: Multiple resections for patients with glioblastoma: prolonging survival. Clinical article. J Neurosurg 118:8128202013

  • 18

    Chin LSMa LDiBiase S: Radiation necrosis following gamma knife surgery: a case-controlled comparison of treatment parameters and long-term clinical follow up. J Neurosurg 94:8999042001

  • 19

    Claus EBCalvocoressi LBondy MLSchildkraut JMWiemels JLWrensch M: Family and personal medical history and risk of meningioma. Clinical article. J Neurosurg 115:107210772011

  • 20

    Concato JShah NHorwitz RI: Randomized, controlled trials, observational studies, and the hierarchy of research designs. N Engl J Med 342:188718922000

  • 21

    Cress MKestle JRHolubkov RRiva-Cambrin J: Risk factors for pediatric arachnoid cyst rupture/hemorrhage: a case-control study. Neurosurgery 72:7167222013

  • 22

    Dadmehr MNejat FEl Khashab MAnsari SBaradaran NErtiaei A: Risk factors associated with occipital encephalocele: a case-control study. Clinical article. J Neurosurg Pediatr 3:5345372009

  • 23

    Dias MS: Neurosurgical causes of scoliosis in patients with myelomeningocele: an evidence-based literature review. J Neurosurg 103:1 Suppl24352005

  • 24

    Elder JBHoh DJLiu CYWang MY: Postoperative continuous paravertebral anesthetic infusion for pain control in posterior cervical spine surgery: a case-control study. Neurosurgery 66:3 Suppl Operative991072010

  • 25

    Englot DJRolston JDWang DDHassnain KHGordon CMChang EF: Efficacy of vagus nerve stimulation in posttraumatic versus nontraumatic epilepsy. Clinical article. J Neurosurg 117:9709772012

  • 26

    Ernster VL: Nested case-control studies. Prev Med 23:5875901994

  • 27

    Fairholm DLee STLui TN: Fractured odontoid: the management of delayed neurological symptoms. Neurosurgery 38:38431996

  • 28

    Fontanella MRainero IGallone SRubino ERivoiro CValfrè W: Lack of association between the apolipoprotein E gene and aneurysmal subarachnoid hemorrhage in an Italian population. J Neurosurg 106:2452492007

  • 29

    Garton HJKestle JRCochrane DDSteinbok P: A cost-effectiveness analysis of endoscopic third ventriculostomy. Neurosurgery 51:69782002

  • 30

    Gautschi OPSchatlo BSchaller KTessitore E: Clinically relevant complications related to pedicle screw placement in thoracolumbar surgery and their management: a literature review of 35,630 pedicle screws. Neurosurg Focus 31:4E82011

  • 31

    Gnanalingham KKTysome JMartinez-Canca JBarazi SA: Quality of clinical studies in neurosurgical journals: signs of improvement over three decades. J Neurosurg 103:4394432005

  • 32

    Gorgulho AJuillard CUslan DZTajik KAurasteh PBehnke E: Infection following deep brain stimulator implantation performed in the conventional versus magnetic resonance imaging-equipped operating room. Clinical article. J Neurosurg 110:2392462009

  • 33

    Grimes DASchulz KF: Cohort studies: marching towards outcomes. Lancet 359:3413452002

  • 34

    Haines SJ: Efficacy of antibiotic prophylaxis in clean neurosurgical operations. Neurosurgery 24:4014051989

  • 35

    Han YYBerkowitz OTalbott EKondziolka DDonovan MLunsford LD: Are frequent dental x-ray examinations associated with increased risk of vestibular schwannoma? Clinical article. J Neurosurg 117:Suppl78832012

  • 36

    Hardy SJNowacki ASBertin MWeil RJ: Absence of an association between glucose levels and surgical site infections in patients undergoing craniotomies for brain tumors. Clinical article. J Neurosurg 113:1611662010

  • 37

    Hatlen TJShurtleff DBLoeser JDOjemann JGAvellino AMEllenbogen RG: Nonprogrammable and programmable cerebrospinal fluid shunt valves: a 5-year study. Clinical article. J Neurosurg Pediatr 9:4624672012

  • 38

    Henderson RDPhan TGPiepgras DGWijdicks EF: Mechanisms of intracerebral hemorrhage after carotid endarterectomy. J Neurosurg 95:9649692001

  • 39

    Hoh BLSistrom CLFirment CSFautheree GLVelat GJWhiting JH: Bottleneck factor and height-width ratio: association with ruptured aneurysms in patients with multiple cerebral aneurysms. Neurosurgery 61:7167232007

  • 40

    Hui FKSchuette AJLieber MSpiotta AMMoskowitz SIBarrow DL: ɛ-Aminocaproic acid in angiographically negative subarachnoid hemorrhage patients is safe: a retrospective review of 83 consecutive patients. Neurosurgery 70:7027062012

  • 41

    Huttner HBKöhrmann MBerger CGeorgiadis DSchwab S: Influence of intraventricular hemorrhage and occlusive hydrocephalus on the long-term outcome of treated patients with basal ganglia hemorrhage: a case-control study. J Neurosurg 105:4124172006

  • 42

    Inagawa T: Risk factors for aneurysmal subarachnoid hemorrhage in patients in Izumo City, Japan. J Neurosurg 102:60672005

  • 43

    Jeswani SNuño MFolkerts VMukherjee DBlack KLPatil CG: Comparison of survival between cerebellar and supratentorial glioblastoma patients: surveillance, epidemiology, and end results (SEER) analysis. Neurosurgery 73:2402462013

  • 44

    Jhawar BSRanger ASteven DDel Maestro RF: Risk factors for intracranial hemorrhage among full-term infants: a case-control study. Neurosurgery 52:5815902003

  • 45

    Julien TDFrankel BTraynelis VCRyken TC: Evidence-based analysis of odontoid fracture management. Neurosurg Focus 8:6E12000

  • 46

    Kang DCHardee MJFesperman SFStoffs TLDahm P: Low quality of evidence for robot-assisted laparoscopic prostatectomy: results of a systematic review of the published literature. Eur Urol 57:9309372010

  • 47

    Kano HKondziolka DFlickinger JCPark KJIyer AYang HC: Stereotactic radiosurgery for arteriovenous malformations after embolization: a case-control study. Clinical article. J Neurosurg 117:2652752012

  • 48

    Kaplan ELMeier P: Nonparametric estimation from incomplete observations. J Am Stat Assoc 53:4574811958

  • 49

    Kassam ABHorowitz MChang YFPeters D: Altered arterial homeostasis and cerebral aneurysms: a molecular epidemiology study. Neurosurgery 54:145014622004

  • 50

    Kelsey JLWhittemore ASEvans ASThompson WD: Methods in Observational Epidemiology ed 2New YorkOxford University Press1996

  • 51

    Kim KAMcDonald MPik JHKhoueir PWang MY: Dynamic intraspinous spacer technology for posterior stabilization: case-control study on the safety, sagittal angulation, and pain outcome at 1-year follow-up evaluation. Neurosurg Focus 22:1E72007

  • 52

    Kim MRKim MYKim SYHwang IHYoon YJ: The quality of reporting of cohort, case-control studies in the Korean Journal of Family Medicine. Korean J Fam Med 33:79882012

  • 53

    Klimo P JrThompson CJRagel BTBoop FA: Methodology and reporting of meta-analyses in the neurosurgical literature. A review. J Neurosurg 120:7968102014

  • 54

    Komotar RJRansom ERMocco JZacharia BEMcKhann GM IIMayer SA: Critical postcraniotomy cerebrospinal fluid hypovolemia: risk factors and outcome analysis. Neurosurgery 59:2842902006

  • 55

    Krex DKotteck KKönig IRZiegler ASchackert HKSchackert G: Matrix metalloproteinase-9 coding sequence single-nucleotide polymorphisms in Caucasians with intracranial aneurysms. Neurosurgery 55:2072132004

  • 56

    La Torre DMaugeri RAngileri FFPezzino GConti ACardali SM: Human leukocyte antigen frequency in human high-grade gliomas: a case-control study in Sicily. Neurosurgery 64:108210892009

  • 57

    Langholz BThomas DC: Nested case-control and case-cohort methods of sampling from a cohort: a critical comparison. Am J Epidemiol 131:1691761990

  • 58

    Lin NDunn IFGlantz MAllison DLJensen RJohnson MD: Benefit of ventriculoperitoneal cerebrospinal fluid shunting and intrathecal chemotherapy in neoplastic meningitis: a retrospective, case-controlled study. Clinical article. J Neurosurg 115:7307362011

  • 59

    Mahajan AMcCutcheon IESuki DChang ELHassenbusch SJWeinberg JS: Case-control study of stereotactic radiosurgery for recurrent glioblastoma multiforme. J Neurosurg 103:2102172005

  • 60

    Marbacher SSchläppi JAFung CHüsler JBeck JRaabe A: Do statins reduce the risk of aneurysm development? A case-control study. Clinical article. J Neurosurg 116:6386422012

  • 61

    McColgan PThant KZSharma P: The genetics of sporadic ruptured and unruptured intracranial aneurysms: a genetic meta-analysis of 8 genes and 13 polymorphisms in approximately 20,000 individuals. Clinical article. J Neurosurg 112:7147212010

  • 62

    McLain RFKalfas IBell GRTetzlaff JEYoon HJRana M: Comparison of spinal and general anesthesia in lumbar laminectomy surgery: a case-controlled analysis of 400 patients. J Neurosurg Spine 2:17222005

  • 63

    Merello MNouzeilles MICammarota ABetti OLeiguarda R: Comparison of 1-year follow-up evaluations of patients with indication for pallidotomy who did not undergo surgery versus patients with Parkinson's disease who did undergo pallidotomy: a case control study. Neurosurgery 44:4614681999

  • 64

    Methodology of guideline development. Neurosurgery 50:3 SupplS2S62002

  • 65

    Mihailovic ABell CMUrbach DR: Users' guide to the surgical literature. Case-control studies in surgical journals. Can J Surg 48:1481512005

  • 66

    Mollman HDHaines SJ: Risk factors for postoperative neurosurgical wound infection. A case-control study. J Neurosurg 64:9029061986

  • 67

    Mondello SLinnet ABuki ARobicsek SGabrielli ATepas J: Clinical utility of serum levels of ubiquitin C-terminal hydrolase as a biomarker for severe traumatic brain injury. Neurosurgery 70:6666752012

  • 68

    Mu JGe WZuo XChen YHuang C: Analysis of association between IL-1β, CASP-9, and GDF5 variants and low-back pain in Chinese male soldier. Clinical article. J Neurosurg Spine 19:2432472013

  • 69

    Nakano MHirano NIshihara HKawaguchi YWatanabe HMatsuura K: Calcium phosphate cement-based vertebroplasty compared with conservative treatment for osteoporotic compression fractures: a matched case-control study. J Neurosurg Spine 4:1101172006

  • 70

    Narotam PKPuri VRoberts JMTaylon CVora YNathoo N: Management of hypertensive emergencies in acute brain disease: evaluation of the treatment effects of intravenous nicardipine on cerebral oxygenation. Clinical article. J Neurosurg 109:106510742008

  • 71

    Narotam PKReddy KFewer DQiao FNathoo N: Collagen matrix duraplasty for cranial and spinal surgery: a clinical and imaging study. J Neurosurg 106:45512007

  • 72

    Nejat FKazmi SSHabibi ZTajik PShahrivar Z: Intelligence quotient in children with meningomyeloceles: a case-control study. J Neurosurg 106:2 Suppl1061102007

  • 73

    Nejat FRadmanesh FAnsari STajik PKajbafzadeh AEl Khashab M: Spina bifida occulta: is it a predictor of underlying spinal cord abnormality in patients with lower urinary tract dysfunction?. J Neurosurg Pediatr 1:1141172008

  • 74

    Newman TBBrowner WSCummings SRHulley SBDesigning cross-sectional and case-control studies. Hulley SBCummings SRBrowner WS: Designing Clinical Research ed 3PhiladelphiaLippincott Williams & Wilkins2007. 109126

  • 75

    Olmos MAntelo MVazquez HSmecuol EMauriño EBai JC: Systematic review and meta-analysis of observational studies on the prevalence of fractures in coeliac disease. Dig Liver Dis 40:46532008

  • 76

    Olsen MAMayfield JLauryssen CPolish LBJones MVest J: Risk factors for surgical site infection in spinal surgery. J Neurosurg 98:2 Suppl1491552003

  • 77

    Pannu HKim DHSeaman CRVan Ginhoven GShete SMilewicz DM: Lack of an association between the angiotensin-converting enzyme insertion/deletion polymorphism and intracranial aneurysms in a Caucasian population in the United States. J Neurosurg 103:92962005

  • 78

    Papathanasiou AAZintzaras E: Assessing the quality of reporting of observational studies in cancer. Ann Epidemiol 20:67732010

  • 79

    Patil CGYi AElramsisy AHu JMukherjee DIrvin DK: Prognosis of patients with multifocal glioblastoma: a case-control study. Clinical article. J Neurosurg 117:7057112012

  • 80

    Peipert JFPhipps MG: Observational studies. Clin Obstet Gynecol 41:2352441998

  • 81

    Platzer PThalhammer GSarahrudi KKovar FVekszler GVécsei V: Nonoperative management of odontoid fractures using a halothoracic vest. Neurosurgery 61:5225302007

  • 82

    Polin RSShaffrey MEBogaev CATisdale NGermanson TBocchicchio B: Decompressive bifrontal craniectomy in the treatment of severe refractory posttraumatic cerebral edema. Neurosurgery 41:84941997

  • 83

    Preventative Services Task Force: Guide to Clinical Preventative Services: Report of the United States Preventative Services Task Force ed 2BaltimoreLippincott Williams & Wilkins1996

  • 84

    Qureshi AISuri MFYahia AMSuarez JIGuterman LRHopkins LN: Risk factors for subarachnoid hemorrhage. Neurosurgery 49:6076132001

  • 85

    Rothman KJGreenlan SLash TL: Case-control studies. Modern Epidemiology ed 3PhiladelphiaLippincott Williams & Wilkins2008. 111127

  • 86

    Ruban DO'Toole JE: Management of incidental durotomy in minimally invasive spine surgery. Neurosurg Focus 31:4E152011

  • 87

    Rughani AILin CDumont TMPenar PLHorgan MATranmer BI: A case-comparison study of the subdural evacuating port system in treating chronic subdural hematomas. Clinical article. J Neurosurg 113:6096142010

  • 88

    Schade RPSchinkel JRoelandse FWGeskus RBVisser LGvan Dijk JM: Lack of value of routine analysis of cerebrospinal fluid for prediction and diagnosis of external drainage-related bacterial meningitis. J Neurosurg 104:1011082006. (Erratum in J Neurosurg 106: 941 2007)

  • 89

    Schievink WIMaya MM: Frequency of intracranial aneurysms in patients with spontaneous intracranial hypotension. Clinical article. J Neurosurg 115:1131152011

  • 90

    Schlesselman JJ: Case-Control Studies: Design Conduct Analysis New YorkOxford University Press1982

  • 91

    Schulz KFGrimes DA: Case-control studies: research in reverse. Lancet 359:4314342002

  • 92

    Sedney CLNonaka YBulsara KRFukushima T: Microsurgical management of jugular foramen schwannomas. Neurosurgery 72:42462013

  • 93

    Semmler ASimon MMoskau SLinnebank M: Polymorphisms of methionine metabolism and susceptibility to meningioma formation. Laboratory investigation. J Neurosurg 108:99910042008

  • 94

    Semrad TJO'Donnell RWun TChew HHarvey DZhou H: Epidemiology of venous thromboembolism in 9489 patients with malignant glioma. J Neurosurg 106:6016082007

  • 95

    Shamim MSQadeer MMurtaza GEnam SAFarooqi NB: Emergency department predictors of tracheostomy in patients with isolated traumatic brain injury requiring emergency cranial decompression. Clinical article. J Neurosurg 115:100710122011

  • 96

    Shore PMJackson EKWisniewski SRClark RSAdelson PDKochanek PM: Vascular endothelial growth factor is increased in cerebrospinal fluid after traumatic brain injury in infants and children. Neurosurgery 54:6056122004

  • 97

    Smidt NRutjes AWvan der Windt DAOstelo RWReitsma JBBossuyt PM: Quality of reporting of diagnostic accuracy studies. Radiology 235:3473532005

  • 98

    Soults CBCanute GSRyken TC: Evidence-based review of the role of reoperation in the management of malignant glioma. Neurosurg Focus 4:6E111998

  • 99

    Stolley PDSchlesselman JJPlanning and conducting a study. Schlesselman JJ: Case-Control Studies: Design Conduct Analysis New YorkOxford University Press1982. 69104

  • 100

    Straume-Næsheim TMAndersen TEHolme KMorten IMcIntosh ASDvorak J: Do minor head impacts in soccer cause concussive injury? A prospective case-control study. Neurosurgery 64:7197252009

  • 101

    Sughrue MEKaur RKane AJRutkowski MJYang IPitts LH: Intratumoral hemorrhage and fibrosis in vestibular schwannoma: a possible mechanism for hearing loss. Clinical article. J Neurosurg 114:3863932011

  • 102

    Sughrue MERutkowski MJChang EFShangari GKane AJMcDermott MW: Postoperative seizures following the resection of convexity meningiomas: are prophylactic anticonvulsants indicated? Clinical article. J Neurosurg 114:7057092011

  • 103

    Taylor CLSteele DKopitnik TA JrSamson DSPurdy PD: Outcome after subarachnoid hemorrhage from a very small aneurysm: a case-control series. J Neurosurg 100:6236252004

  • 104

    Teo KChoy DKLwin SNing CYeo TTShen L: Cerebral hyperperfusion syndrome after superficial temporal artery-middle cerebral artery bypass for severe intracranial steno-occlusive disease: a case control study. Neurosurgery 72:9369432013

  • 105

    Tomasi CDerks J: Clinical research of peri-implant diseases—quality of reporting, case definitions and methods to study incidence, prevalence and risk factors of peri-implant diseases. J Clin Periodontol 39:Suppl 122072232012

  • 106

    van Dijk JMTerBrugge KGVan der Meer FJWallace MCRosendaal FR: Thrombophilic factors and the formation of dural arteriovenous fistulas. J Neurosurg 107:56592007

  • 107

    Vandenbroucke JPvon Elm EAltman DGGøtzsche PCMulrow CDPocock SJ: Strengthening the Reporting of Observational Studies in Epidemiology (STROBE): explanation and elaboration. PLoS Med 4:e2972007

  • 108

    Vannemreddy PCaldito GWillis BNanda A: Influence of cocaine on ruptured intracranial aneurysms: a case control study of poor prognostic indicators. J Neurosurg 108:4704762008

  • 109

    Varelas PNRickert KLCusick JHacein-Bey LSinson GTorbey M: Intraventricular hemorrhage after aneurysmal subarachnoid hemorrhage: pilot study of treatment with intraventricular tissue plasminogen activator. Neurosurgery 56:2052132005

  • 110

    von Elm EAltman DGEgger MPocock SJGøtzsche PCVandenbroucke JP: The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. PLoS Med 4:e2962007

Appendix

STROBE Statement—checklist of items that should be included in reports of case-control studies

SectionItem No.Recommendation
Title & Abstract1
  • a) Indicate the study's design with a commonly used term in the title or the abstract.

  • b) Provide in the abstract an informative and balanced summary of what was done.

Introduction
 Background/rationale2Explain the scientific background and rationale for the investigation being reported.
 Objectives3State specific objectives, including any prespecified hypotheses.
Methods
 Study design4Present key elements of study design early in the paper.
 Setting5Describe the setting, locations, and relevant dates, including periods of recruitment, exposure, follow-up, and data collection.
 Participants6
  • a) Give the eligibility criteria, and the sources and methods of case ascertainment and control selection. Give the rationale for the choice of cases and controls.

  • b) For matched studies, give matching criteria and the number of controls per case.

 Variables7Clearly define all outcomes, exposures, predictors, potential confounders, and effect modifiers. Give diagnostic criteria, if applicable.
 Data sources/measurement8For each variable of interest, give sources of data and details of methods of assessment (measurement). Describe comparability of assessment methods if there is more than one group.
 Bias9Describe any efforts to address potential sources of bias.
 Study size10Explain how the study size was arrived at.
 Quantitative variables11Explain how quantitative variables were handled in the analyses. If applicable, describe which groupings were chosen and why.
 Statistical methods12
  • a) Describe all statistical methods, including those used to control for confounding.

  • b) Describe any methods used to examine subgroups and interactions.

  • c) Explain how missing data were addressed.

  • d) If applicable, explain how matching of cases and controls was addressed.

  • e) Describe any sensitivity analyses.

Results
 Participants13
  • a) Report numbers of individuals at each stage of study—e.g., numbers potentially eligible, examined for eligibility, confirmed eligible, included in the study, completing follow-up, and analyzed.

  • b) Give reasons for non-participation at each stage.

  • c) Consider use of a flow diagram.

 Descriptive data14
  • a) Give characteristics of study participants (e.g., demographic, clinical, social) and information on exposures and potential confounders.

  • b) Indicate number of participants with missing data for each variable of interest.

 Outcome data15Report numbers in each exposure category, or summary measures of exposure.
 Main results16
  • a) Give unadjusted estimates and, if applicable, confounder-adjusted estimates and their precision (e.g., 95% confidence interval). Make clear which confounders were adjusted for and why they were included.

  • b) Report category boundaries when continuous variables were categorized.

  • c) If relevant, consider translating estimates of relative risk into absolute risk for a meaningful time period.

 Other analyses17Report other analyses done—e.g., analyses of subgroups and interactions, and sensitivity analyses.
Discussion
 Key results18Summarize key results with reference to study objectives.
 Limitations19Discuss limitations of the study, taking into account sources of potential bias or imprecision. Discuss both direction and magnitude of any potential bias.
20Give a cautious overall interpretation of results, considering objectives, limitations, multiplicity of analyses, results from similar studies, and other relevant evidence.
21Discuss the generalizability (external validity) of the study results.
Other information
 Funding22Give the source of funding and the role of the funders for the present study and, if applicable, for the original study on which the present article is based.

If the inline PDF is not rendering correctly, you can download the PDF file here.

Article Information

Address correspondence to: Paul Klimo Jr., M.D., M.P.H., Semmes-Murphey Neurologic & Spine Institute, 6325 Humphreys Blvd., Memphis, TN 38120. email: pklimo@semmes-murphey.com.

Please include this information when citing this paper: published online June 20, 2014; DOI: 10.3171/2014.5.JNS132329.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Case-control versus cohort study design. Case-control studies are designed to assess differences in risk between 2 or more groups with a known disease status. Cohort studies assess differences in outcome between 2 or more groups with a known risk status.

  • View in gallery

    Study design flow chart. A literature search using PubMed/MEDLINE for case-control studies in the JNS Publishing Group journals (Journal of Neurosurgery, Journal of Neurosurgery: Pediatrics, Journal of Neurosurgery: Spine, and Neurosurgical Focus) and Neurosurgery through July 2013 produced 182 hits. Of these publications, 67 explicitly referred to the study as “case-control” in the text and met the inclusion criteria. Thirty-two of these 67 studies met the basic definition of a case-control study.

  • View in gallery

    STROBE evaluation of true case-control studies. Item 1 (Q1) of the STROBE checklist refers to the title and Abstract, Items 2–3 (Q2–3) refer to the Introduction, Items 4–12 (Q4–12) refer to Methods, Items 13–17 (Q13–17) refer to Results, and Items 18–22 (Q18–22) refer to the Discussion.

References

1

Armenian HK: The Case-Control Method: Design and Applications New YorkOxford University Press2009

2

Arrese ISarabia RPintado RDelgado-Rodriguez M: Flow-diverter devices for intracranial aneurysms: systematic review and meta-analysis. Neurosurgery 73:1932002013

3

Aydin DFeychting MSchüz JAndersen TVPoulsen AHProchazka M: Predictors and overestimation of recalled mobile phone use among children and adolescents. Prog Biophys Mol Biol 107:3563612011

4

Badjatia NFernandez LSchmidt JMLee KClaassen JConnolly ES: Impact of induced normothermia on outcome after subarachnoid hemorrhage: a case-control study. Neurosurgery 66:6967012010

5

Barker FG IIOyesiku NM: The Registrar. Improving the quality of research reports in Neurosurgery: the CONSORT, PRISMA, MOOSE, STARD, STROBE statements and the EQUATOR network. Neurosurgery 68:152011

6

Barnes BAlexander JTBranch CL Jr: Postoperative Level 1 anticoagulation therapy and spinal surgery: practical guidelines for management. Neurosurg Focus 17:4E52004

7

Berger RPAdelson PDPierce MCDulani TCassidy LDKochanek PM: Serum neuron-specific enolase, S100B, and myelin basic protein concentrations after inflicted and noninflicted traumatic brain injury in children. J Neurosurg 103:1 Suppl61682005

8

Bergsneider MXue KSuh JDWang MB: Barrier-limited multimodality closure for reconstruction of wide sellar openings. Neurosurgery 71:1 Suppl Operative68762012

9

Bland JMAltman DG: Survival probabilities (the Kaplan-Meier method). BMJ 317:157215801998

10

Börm WKast ERichter HPMohr K: Anterior screw fixation in type II odontoid fractures: is there a difference in outcome between age groups?. Neurosurgery 52:108910942003

11

Bossuyt PMReitsma JBBruns DEGatsonis CAGlasziou PPIrwig LM: The STARD statement for reporting studies of diagnostic accuracy: explanation and elaboration. Ann Intern Med 138:W1W122003

12

Brandão RACosta BSDellaretti MAde Carvalho GTFaria MPde Sousa AA: Efficacy and safety of a porcine collagen sponge for cranial neurosurgery: a prospective case-control study. World Neurosurg 79:5445502013

13

Bratton SLDavis RL: Acute lung injury in isolated traumatic brain injury. Neurosurgery 40:7077121997

14

Breslow NEDay NE: The Analysis of Case-Control Studies. Statistical Methods in Cancer Research 1:LyonIARC Press1980

15

Brophy RHGardner MJSaleem OMarx RG: An assessment of the methodological quality of research published in The American Journal of Sports Medicine. Am J Sports Med 33:181218152005

16

Brott TMandybur TI: Case-control study of clinical outcome after aneurysmal subarachnoid hemorrhage. Neurosurgery 19:8918951986

17

Chaichana KLZadnik PWeingart JDOlivi AGallia GLBlakeley J: Multiple resections for patients with glioblastoma: prolonging survival. Clinical article. J Neurosurg 118:8128202013

18

Chin LSMa LDiBiase S: Radiation necrosis following gamma knife surgery: a case-controlled comparison of treatment parameters and long-term clinical follow up. J Neurosurg 94:8999042001

19

Claus EBCalvocoressi LBondy MLSchildkraut JMWiemels JLWrensch M: Family and personal medical history and risk of meningioma. Clinical article. J Neurosurg 115:107210772011

20

Concato JShah NHorwitz RI: Randomized, controlled trials, observational studies, and the hierarchy of research designs. N Engl J Med 342:188718922000

21

Cress MKestle JRHolubkov RRiva-Cambrin J: Risk factors for pediatric arachnoid cyst rupture/hemorrhage: a case-control study. Neurosurgery 72:7167222013

22

Dadmehr MNejat FEl Khashab MAnsari SBaradaran NErtiaei A: Risk factors associated with occipital encephalocele: a case-control study. Clinical article. J Neurosurg Pediatr 3:5345372009

23

Dias MS: Neurosurgical causes of scoliosis in patients with myelomeningocele: an evidence-based literature review. J Neurosurg 103:1 Suppl24352005

24

Elder JBHoh DJLiu CYWang MY: Postoperative continuous paravertebral anesthetic infusion for pain control in posterior cervical spine surgery: a case-control study. Neurosurgery 66:3 Suppl Operative991072010

25

Englot DJRolston JDWang DDHassnain KHGordon CMChang EF: Efficacy of vagus nerve stimulation in posttraumatic versus nontraumatic epilepsy. Clinical article. J Neurosurg 117:9709772012

26

Ernster VL: Nested case-control studies. Prev Med 23:5875901994

27

Fairholm DLee STLui TN: Fractured odontoid: the management of delayed neurological symptoms. Neurosurgery 38:38431996

28

Fontanella MRainero IGallone SRubino ERivoiro CValfrè W: Lack of association between the apolipoprotein E gene and aneurysmal subarachnoid hemorrhage in an Italian population. J Neurosurg 106:2452492007

29

Garton HJKestle JRCochrane DDSteinbok P: A cost-effectiveness analysis of endoscopic third ventriculostomy. Neurosurgery 51:69782002

30

Gautschi OPSchatlo BSchaller KTessitore E: Clinically relevant complications related to pedicle screw placement in thoracolumbar surgery and their management: a literature review of 35,630 pedicle screws. Neurosurg Focus 31:4E82011

31

Gnanalingham KKTysome JMartinez-Canca JBarazi SA: Quality of clinical studies in neurosurgical journals: signs of improvement over three decades. J Neurosurg 103:4394432005

32

Gorgulho AJuillard CUslan DZTajik KAurasteh PBehnke E: Infection following deep brain stimulator implantation performed in the conventional versus magnetic resonance imaging-equipped operating room. Clinical article. J Neurosurg 110:2392462009

33

Grimes DASchulz KF: Cohort studies: marching towards outcomes. Lancet 359:3413452002

34

Haines SJ: Efficacy of antibiotic prophylaxis in clean neurosurgical operations. Neurosurgery 24:4014051989

35

Han YYBerkowitz OTalbott EKondziolka DDonovan MLunsford LD: Are frequent dental x-ray examinations associated with increased risk of vestibular schwannoma? Clinical article. J Neurosurg 117:Suppl78832012

36

Hardy SJNowacki ASBertin MWeil RJ: Absence of an association between glucose levels and surgical site infections in patients undergoing craniotomies for brain tumors. Clinical article. J Neurosurg 113:1611662010

37

Hatlen TJShurtleff DBLoeser JDOjemann JGAvellino AMEllenbogen RG: Nonprogrammable and programmable cerebrospinal fluid shunt valves: a 5-year study. Clinical article. J Neurosurg Pediatr 9:4624672012

38

Henderson RDPhan TGPiepgras DGWijdicks EF: Mechanisms of intracerebral hemorrhage after carotid endarterectomy. J Neurosurg 95:9649692001

39

Hoh BLSistrom CLFirment CSFautheree GLVelat GJWhiting JH: Bottleneck factor and height-width ratio: association with ruptured aneurysms in patients with multiple cerebral aneurysms. Neurosurgery 61:7167232007

40

Hui FKSchuette AJLieber MSpiotta AMMoskowitz SIBarrow DL: ɛ-Aminocaproic acid in angiographically negative subarachnoid hemorrhage patients is safe: a retrospective review of 83 consecutive patients. Neurosurgery 70:7027062012

41

Huttner HBKöhrmann MBerger CGeorgiadis DSchwab S: Influence of intraventricular hemorrhage and occlusive hydrocephalus on the long-term outcome of treated patients with basal ganglia hemorrhage: a case-control study. J Neurosurg 105:4124172006

42

Inagawa T: Risk factors for aneurysmal subarachnoid hemorrhage in patients in Izumo City, Japan. J Neurosurg 102:60672005

43

Jeswani SNuño MFolkerts VMukherjee DBlack KLPatil CG: Comparison of survival between cerebellar and supratentorial glioblastoma patients: surveillance, epidemiology, and end results (SEER) analysis. Neurosurgery 73:2402462013

44

Jhawar BSRanger ASteven DDel Maestro RF: Risk factors for intracranial hemorrhage among full-term infants: a case-control study. Neurosurgery 52:5815902003

45

Julien TDFrankel BTraynelis VCRyken TC: Evidence-based analysis of odontoid fracture management. Neurosurg Focus 8:6E12000

46

Kang DCHardee MJFesperman SFStoffs TLDahm P: Low quality of evidence for robot-assisted laparoscopic prostatectomy: results of a systematic review of the published literature. Eur Urol 57:9309372010

47

Kano HKondziolka DFlickinger JCPark KJIyer AYang HC: Stereotactic radiosurgery for arteriovenous malformations after embolization: a case-control study. Clinical article. J Neurosurg 117:2652752012

48

Kaplan ELMeier P: Nonparametric estimation from incomplete observations. J Am Stat Assoc 53:4574811958

49

Kassam ABHorowitz MChang YFPeters D: Altered arterial homeostasis and cerebral aneurysms: a molecular epidemiology study. Neurosurgery 54:145014622004

50

Kelsey JLWhittemore ASEvans ASThompson WD: Methods in Observational Epidemiology ed 2New YorkOxford University Press1996

51

Kim KAMcDonald MPik JHKhoueir PWang MY: Dynamic intraspinous spacer technology for posterior stabilization: case-control study on the safety, sagittal angulation, and pain outcome at 1-year follow-up evaluation. Neurosurg Focus 22:1E72007

52

Kim MRKim MYKim SYHwang IHYoon YJ: The quality of reporting of cohort, case-control studies in the Korean Journal of Family Medicine. Korean J Fam Med 33:79882012

53

Klimo P JrThompson CJRagel BTBoop FA: Methodology and reporting of meta-analyses in the neurosurgical literature. A review. J Neurosurg 120:7968102014

54

Komotar RJRansom ERMocco JZacharia BEMcKhann GM IIMayer SA: Critical postcraniotomy cerebrospinal fluid hypovolemia: risk factors and outcome analysis. Neurosurgery 59:2842902006

55

Krex DKotteck KKönig IRZiegler ASchackert HKSchackert G: Matrix metalloproteinase-9 coding sequence single-nucleotide polymorphisms in Caucasians with intracranial aneurysms. Neurosurgery 55:2072132004

56

La Torre DMaugeri RAngileri FFPezzino GConti ACardali SM: Human leukocyte antigen frequency in human high-grade gliomas: a case-control study in Sicily. Neurosurgery 64:108210892009

57

Langholz BThomas DC: Nested case-control and case-cohort methods of sampling from a cohort: a critical comparison. Am J Epidemiol 131:1691761990

58

Lin NDunn IFGlantz MAllison DLJensen RJohnson MD: Benefit of ventriculoperitoneal cerebrospinal fluid shunting and intrathecal chemotherapy in neoplastic meningitis: a retrospective, case-controlled study. Clinical article. J Neurosurg 115:7307362011

59

Mahajan AMcCutcheon IESuki DChang ELHassenbusch SJWeinberg JS: Case-control study of stereotactic radiosurgery for recurrent glioblastoma multiforme. J Neurosurg 103:2102172005

60

Marbacher SSchläppi JAFung CHüsler JBeck JRaabe A: Do statins reduce the risk of aneurysm development? A case-control study. Clinical article. J Neurosurg 116:6386422012

61

McColgan PThant KZSharma P: The genetics of sporadic ruptured and unruptured intracranial aneurysms: a genetic meta-analysis of 8 genes and 13 polymorphisms in approximately 20,000 individuals. Clinical article. J Neurosurg 112:7147212010

62

McLain RFKalfas IBell GRTetzlaff JEYoon HJRana M: Comparison of spinal and general anesthesia in lumbar laminectomy surgery: a case-controlled analysis of 400 patients. J Neurosurg Spine 2:17222005

63

Merello MNouzeilles MICammarota ABetti OLeiguarda R: Comparison of 1-year follow-up evaluations of patients with indication for pallidotomy who did not undergo surgery versus patients with Parkinson's disease who did undergo pallidotomy: a case control study. Neurosurgery 44:4614681999

64

Methodology of guideline development. Neurosurgery 50:3 SupplS2S62002

65

Mihailovic ABell CMUrbach DR: Users' guide to the surgical literature. Case-control studies in surgical journals. Can J Surg 48:1481512005

66

Mollman HDHaines SJ: Risk factors for postoperative neurosurgical wound infection. A case-control study. J Neurosurg 64:9029061986

67

Mondello SLinnet ABuki ARobicsek SGabrielli ATepas J: Clinical utility of serum levels of ubiquitin C-terminal hydrolase as a biomarker for severe traumatic brain injury. Neurosurgery 70:6666752012

68

Mu JGe WZuo XChen YHuang C: Analysis of association between IL-1β, CASP-9, and GDF5 variants and low-back pain in Chinese male soldier. Clinical article. J Neurosurg Spine 19:2432472013

69

Nakano MHirano NIshihara HKawaguchi YWatanabe HMatsuura K: Calcium phosphate cement-based vertebroplasty compared with conservative treatment for osteoporotic compression fractures: a matched case-control study. J Neurosurg Spine 4:1101172006

70

Narotam PKPuri VRoberts JMTaylon CVora YNathoo N: Management of hypertensive emergencies in acute brain disease: evaluation of the treatment effects of intravenous nicardipine on cerebral oxygenation. Clinical article. J Neurosurg 109:106510742008

71

Narotam PKReddy KFewer DQiao FNathoo N: Collagen matrix duraplasty for cranial and spinal surgery: a clinical and imaging study. J Neurosurg 106:45512007

72

Nejat FKazmi SSHabibi ZTajik PShahrivar Z: Intelligence quotient in children with meningomyeloceles: a case-control study. J Neurosurg 106:2 Suppl1061102007

73

Nejat FRadmanesh FAnsari STajik PKajbafzadeh AEl Khashab M: Spina bifida occulta: is it a predictor of underlying spinal cord abnormality in patients with lower urinary tract dysfunction?. J Neurosurg Pediatr 1:1141172008

74

Newman TBBrowner WSCummings SRHulley SBDesigning cross-sectional and case-control studies. Hulley SBCummings SRBrowner WS: Designing Clinical Research ed 3PhiladelphiaLippincott Williams & Wilkins2007. 109126

75

Olmos MAntelo MVazquez HSmecuol EMauriño EBai JC: Systematic review and meta-analysis of observational studies on the prevalence of fractures in coeliac disease. Dig Liver Dis 40:46532008

76

Olsen MAMayfield JLauryssen CPolish LBJones MVest J: Risk factors for surgical site infection in spinal surgery. J Neurosurg 98:2 Suppl1491552003

77

Pannu HKim DHSeaman CRVan Ginhoven GShete SMilewicz DM: Lack of an association between the angiotensin-converting enzyme insertion/deletion polymorphism and intracranial aneurysms in a Caucasian population in the United States. J Neurosurg 103:92962005

78

Papathanasiou AAZintzaras E: Assessing the quality of reporting of observational studies in cancer. Ann Epidemiol 20:67732010

79

Patil CGYi AElramsisy AHu JMukherjee DIrvin DK: Prognosis of patients with multifocal glioblastoma: a case-control study. Clinical article. J Neurosurg 117:7057112012

80

Peipert JFPhipps MG: Observational studies. Clin Obstet Gynecol 41:2352441998

81

Platzer PThalhammer GSarahrudi KKovar FVekszler GVécsei V: Nonoperative management of odontoid fractures using a halothoracic vest. Neurosurgery 61:5225302007

82

Polin RSShaffrey MEBogaev CATisdale NGermanson TBocchicchio B: Decompressive bifrontal craniectomy in the treatment of severe refractory posttraumatic cerebral edema. Neurosurgery 41:84941997

83

Preventative Services Task Force: Guide to Clinical Preventative Services: Report of the United States Preventative Services Task Force ed 2BaltimoreLippincott Williams & Wilkins1996

84

Qureshi AISuri MFYahia AMSuarez JIGuterman LRHopkins LN: Risk factors for subarachnoid hemorrhage. Neurosurgery 49:6076132001

85

Rothman KJGreenlan SLash TL: Case-control studies. Modern Epidemiology ed 3PhiladelphiaLippincott Williams & Wilkins2008. 111127

86

Ruban DO'Toole JE: Management of incidental durotomy in minimally invasive spine surgery. Neurosurg Focus 31:4E152011

87

Rughani AILin CDumont TMPenar PLHorgan MATranmer BI: A case-comparison study of the subdural evacuating port system in treating chronic subdural hematomas. Clinical article. J Neurosurg 113:6096142010

88

Schade RPSchinkel JRoelandse FWGeskus RBVisser LGvan Dijk JM: Lack of value of routine analysis of cerebrospinal fluid for prediction and diagnosis of external drainage-related bacterial meningitis. J Neurosurg 104:1011082006. (Erratum in J Neurosurg 106: 941 2007)

89

Schievink WIMaya MM: Frequency of intracranial aneurysms in patients with spontaneous intracranial hypotension. Clinical article. J Neurosurg 115:1131152011

90

Schlesselman JJ: Case-Control Studies: Design Conduct Analysis New YorkOxford University Press1982

91

Schulz KFGrimes DA: Case-control studies: research in reverse. Lancet 359:4314342002

92

Sedney CLNonaka YBulsara KRFukushima T: Microsurgical management of jugular foramen schwannomas. Neurosurgery 72:42462013

93

Semmler ASimon MMoskau SLinnebank M: Polymorphisms of methionine metabolism and susceptibility to meningioma formation. Laboratory investigation. J Neurosurg 108:99910042008

94

Semrad TJO'Donnell RWun TChew HHarvey DZhou H: Epidemiology of venous thromboembolism in 9489 patients with malignant glioma. J Neurosurg 106:6016082007

95

Shamim MSQadeer MMurtaza GEnam SAFarooqi NB: Emergency department predictors of tracheostomy in patients with isolated traumatic brain injury requiring emergency cranial decompression. Clinical article. J Neurosurg 115:100710122011

96

Shore PMJackson EKWisniewski SRClark RSAdelson PDKochanek PM: Vascular endothelial growth factor is increased in cerebrospinal fluid after traumatic brain injury in infants and children. Neurosurgery 54:6056122004

97

Smidt NRutjes AWvan der Windt DAOstelo RWReitsma JBBossuyt PM: Quality of reporting of diagnostic accuracy studies. Radiology 235:3473532005

98

Soults CBCanute GSRyken TC: Evidence-based review of the role of reoperation in the management of malignant glioma. Neurosurg Focus 4:6E111998

99

Stolley PDSchlesselman JJPlanning and conducting a study. Schlesselman JJ: Case-Control Studies: Design Conduct Analysis New YorkOxford University Press1982. 69104

100

Straume-Næsheim TMAndersen TEHolme KMorten IMcIntosh ASDvorak J: Do minor head impacts in soccer cause concussive injury? A prospective case-control study. Neurosurgery 64:7197252009

101

Sughrue MEKaur RKane AJRutkowski MJYang IPitts LH: Intratumoral hemorrhage and fibrosis in vestibular schwannoma: a possible mechanism for hearing loss. Clinical article. J Neurosurg 114:3863932011

102

Sughrue MERutkowski MJChang EFShangari GKane AJMcDermott MW: Postoperative seizures following the resection of convexity meningiomas: are prophylactic anticonvulsants indicated? Clinical article. J Neurosurg 114:7057092011

103

Taylor CLSteele DKopitnik TA JrSamson DSPurdy PD: Outcome after subarachnoid hemorrhage from a very small aneurysm: a case-control series. J Neurosurg 100:6236252004

104

Teo KChoy DKLwin SNing CYeo TTShen L: Cerebral hyperperfusion syndrome after superficial temporal artery-middle cerebral artery bypass for severe intracranial steno-occlusive disease: a case control study. Neurosurgery 72:9369432013

105

Tomasi CDerks J: Clinical research of peri-implant diseases—quality of reporting, case definitions and methods to study incidence, prevalence and risk factors of peri-implant diseases. J Clin Periodontol 39:Suppl 122072232012

106

van Dijk JMTerBrugge KGVan der Meer FJWallace MCRosendaal FR: Thrombophilic factors and the formation of dural arteriovenous fistulas. J Neurosurg 107:56592007

107

Vandenbroucke JPvon Elm EAltman DGGøtzsche PCMulrow CDPocock SJ: Strengthening the Reporting of Observational Studies in Epidemiology (STROBE): explanation and elaboration. PLoS Med 4:e2972007

108

Vannemreddy PCaldito GWillis BNanda A: Influence of cocaine on ruptured intracranial aneurysms: a case control study of poor prognostic indicators. J Neurosurg 108:4704762008

109

Varelas PNRickert KLCusick JHacein-Bey LSinson GTorbey M: Intraventricular hemorrhage after aneurysmal subarachnoid hemorrhage: pilot study of treatment with intraventricular tissue plasminogen activator. Neurosurgery 56:2052132005

110

von Elm EAltman DGEgger MPocock SJGøtzsche PCVandenbroucke JP: The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. PLoS Med 4:e2962007

TrendMD

Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 300 300 40
PDF Downloads 386 386 48
EPUB Downloads 0 0 0

PubMed

Google Scholar