Generalized Adaptation Syndrome: A Case Study

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General Adaptation Syndrome

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Following title and abstract screening, articles remained for full text review from the original search, and 47 articles remained for full text review from the updated search. In full text review, remaining articles were screened for relevant information for the purpose of this study. Articles were included if full text was available in English and contained both a denominator of total severe YF cases and a numerator of deaths among the severe cases. Articles that did not report a numerator and denominator, but did report a denominator and fatality proportion for YF cases, were included. While some studies reported that YF cases were laboratory confirmed, others did not report laboratory confirmation and classified identified YF cases by symptoms.

Articles that were not included most commonly included editorials, single case reports, reporting of cases in nonhuman primates, reports of capacity building, or laboratory detection methods. Of the articles undergoing full text review from the original search, 14 were not available in full text, seven were not available in English, and focused on YF topics, but did not include a specific denominator of cases or numerator of fatal cases.

During full text review from the original search, four articles were added from the references of the articles read, yielding 30 articles in total. From the updated search, one article was retained from full text review, and another was added from references of the 47 articles. Following these steps, the 32 total articles were reread to validate the data extracted. Following data extraction from the 32 articles, those that did not specifically report severe cases were removed. In this study, severe YF cases were defined by having a fever and at least one of jaundice or hemorrhaging.

Studies that did not state that YF cases were defined by having fever as well as at least one of jaundice of hemorrhaging were removed. During the updated search, this criterion was applied during full text review. These symptoms were typically reported at the study level, where the authors of the studies stated broadly the symptoms used in identifying YF cases in the main text. Many studies only included fever and jaundice in the definition of severe YF, while others included hemorrhaging and other symptoms including organ failure Additional file 2 : Table S2.

A total of 14 studies contained explicit numbers for fatal and nonfatal severe cases through these definitions Fig. In order to incorporate data from the recent YF outbreak in Brazil, four studies from the updated search that specified severe YF cases through healthcare use, but did not explicitly state the symptom definition outlined previously as inclusion criteria, were added. These studies stated that some patients showed symptoms such as fever, jaundice, and hemorrhaging, but the numbers of fatal and total cases did not exclusively consist of cases meeting the symptom definition.

Flow diagram for screening and including articles in systematic literature review and meta-analysis for case fatality risk of severe Yellow Fever cases. Publication years of articles ranged between and In addition to the numbers of total and fatal severe cases, descriptive information was collected for each study. Data collected included country, continent, year, symptoms, applied case definitions, and research methods for each study. Case definition and symptoms in the main text were used to confirm that cases listed were severe cases. While, for the purposes of this study, fever as well as either jaundice or hemorrhaging were required for inclusion as severe YF cases, some included studies considered other symptoms as well in their case definitions, including abdominal pain and organ failure Additional file 2 : Table S2.

It also was noted whether the authors were active in recruiting YF patients or stating numbers from reported case data. All studies were classified as either an investigative or reporting study Table 1. Also collected was whether the cases in each study were confirmed or suspected for YF. Cases were considered confirmed if the articles stated laboratory diagnostic confirmation for YF. Studies that specified a specific laboratory diagnosis, such as through polymerase chain reaction PCR , or stated lab confirmed cases without specifying a specific type of test, were included as laboratory confirmed cases. Cases were considered suspect if the article explicitly stated cases were suspect.

Probable cases, where symptoms are observed without a guaranteed laboratory result, were considered suspect cases in this study. If the article did not state whether cases were confirmed or suspect, then cases were assumed to be suspect Table 1. All included studies list total and fatal counts of severe YF cases without the CFR being the primary focus of the study. Therefore, the sources of bias in the individual studies remained consistent. Two possible major sources of bias are underreporting of cases within studies and deaths occurring after followup [ 14 ]. Underreported cases, if nonfatal, would lead to a smaller denominator and an overestimated CFR. If the underreported cases were as fatal as reported cases, no bias would be observed.

Deaths occurring after followup would lead to fatal cases being classified as nonfatal, and lead to an underestimate of CFR. Despite these two potential sources of bias, publication bias, where tests of statistical significance affect reporting of results [ 33 ], is not likely to be present in this study. Because the primary focus of the studies was not to estimate the CFR of YF, issues of publication bias are less likely since no included articles used statistical significance tests for CFR estimates. Therefore, the proportions of fatal cases within studies are unlikely to affect whether the studies were published.

Collected data were inputted into a Microsoft Excel spreadsheet during full text review, with information to be collected determined prior to data collection. Case fatality risk was estimated using a meta-analysis for proportions. Only proportions not equal to zero or one were included in the meta-analysis, as these would produce standard errors of zero. They are, however, included in Table 1. Stratified CFRs were estimated for differences by continent South America or Africa , by study type investigative or reporting, as defined previously and by symptoms reported fever and jaundice or fever, jaundice, and other severe symptoms.

Values of the I 2 statistic were calculated to describe heterogeneity [ 35 ]. Analyses were run separately to include and exclude the four recent studies added to show whether results are sensitive to the inclusion of studies containing data likely to be useful, but not meeting the strict inclusion criteria. A total of 18 studies were found through the literature review reporting a CFR for severe YF, three of which were added from the references of the articles that underwent full-text screening and four of which underwent full text screening and were included due to their relevance to the recent Brazilian outbreak.

The 18 papers contained a total of 36 proportions of fatal severe cases; 30 of these, present in 17 studies, were not equal to zero or one Table 1 and therefore included in the meta-analysis. The six proportions that equaled zero or one were instances where only one severe YF case was reported in the denominator. Of the 30 proportions included in the meta-analysis, 14 articles provided 16 proportions of CFR among confirmed severe cases of YF, and another three articles provided 14 proportions among severe suspected cases.

Articles included in analyses reported cases in both Africa and South America Fig. The countries with more than one study or more than one fatality proportion found through the literature review were Brazil 7 papers, 8 proportions , Nigeria 3 papers, 9 proportions , Ghana 1 paper, 6 proportions , Cameroon 2 papers, 2 proportions , and Democratic Republic of Congo 2 papers, 2 proportions Fig. Articles reporting multiple proportions in the same country during the same year s reported different proportions for different locations within countries.

Articles from the updated search ranged between and , with the article added from references in full text review, which did not appear in the initial search, published in Of these, four papers are clustered between and , another four are clustered between and , seven are clustered between and , and the remaining three are interspersed outside these time clusters. Among the 36 fatality proportions for severe YF found in literature, 21 represented fatality proportions among laboratory confirmed severe cases Table 1 , though the laboratory test used was not always specified in the text.

The remaining 15 represented proportions from suspect severe cases, where laboratory confirmation was not stated. From assessing the study methods, 22 proportions were found from investigative studies as described previously, with the remaining 14 presented in reporting studies. All proportions, with the exception of those from recent clinical investigations in Brazil, explicitly stated use of both fever and jaundice in their case definitions, and some studies also included other symptoms as well in YF case diagnosis.

These included hemorrhaging 15 proportions , abdominal pain 13 proportions , or organ failure 2 proportions Additional file 2 : Table S2. Travel to a YF endemic region was a criterion included in eight proportions. Numbers of articles found through systematic literature review reporting case fatality risk data for severe Yellow Fever cases for each nation. Some articles contained data for multiple nations. Numbers of proportions for case fatality risk among severe Yellow Fever cases found through systematic literature review by nation. Numbers of proportions are separated by a confirmed and b suspect severe Yellow Fever cases. Forest plots are shown in Fig.

The individual numerators and denominators in each study are shown in Table 1. Forest plots of case fatality risk estimates among severe a laboratory confirmed and b suspect Yellow Fever cases found through literature review. Only risk estimates not equal to zero are included. Including or excluding the four recent clinical studies from Brazil also did not lead to substantial differences in CFR estimates Table 2. Much heterogeneity was seen among studies, as indicated by I 2 values. The CFRs for severe YF cases were stratified by characteristics of the articles to account for potential heterogeneities in either YF dynamics or data collection and reporting. First, CFRs were stratified by continent.

This study aimed to systematically evaluate the CFR for severe YF cases, defined as cases showing fever with either jaundice or hemorrhaging. A systematic literature review was conducted in order to find reported proportions of fatal cases of severe YF. Separating the CFR by continent showed a notably higher CFR in South America compared to Africa, separating the CFR among severe cases by article type showed no difference in CFR between investigative studies and passively reported cases, and separating by inclusion of symptoms beyond fever and jaundice showed no difference in CFR estimates. The drastic difference in estimated CFR between South America and Africa may potentially result from differences in data collection as well as differences in YF dynamics.

The differences seen across geographic locations in these studies were less pronounced than the difference in CFR between continents found in this study. Different strains of YF are found between South America and Africa [ 56 , 57 ] as well as different primary mosquito vectors and nonhuman primate reservoirs [ 58 ]. Clinical care also differs across countries. Though International Health Regulations require reporting of YF cases [ 59 ], implementation and surveillance quality may differ between the two continents, as well as differences in healthcare seeking behaviors, which can lead to differences in severe cases represented across each continent.

The small number of proportions representing CFR in South America may also account for the difference in estimated CFR across continents, as having eight South American proportions makes the CFR estimate more sensitive to any single study providing a non-representative sample of severe YF cases. Across studies, there was significant heterogeneity among the CFRs reported Fig. Among other reviews estimating CFR for other infectious diseases, high heterogeneities have also been seen [ 55 , 60 , 61 ].

Potential sources of heterogeneity across the different studies include differences in surveillance resources as well as differences in healthcare infrastructure across the various settings of the studies. This does not, however, suggest that the estimated CFR from this study will apply to every outbreak situation. The CFRs of other diseases have been seen to change over time [ 13 ] and may differ in relation to industrialization [ 62 ]. The estimate yielded in this study should be used as an average CFR and broad recommendation.

It is important to note that the interpretation of the estimated CFR in this study is based on the case definition used. A CFR among all YF cases, which would commonly include all symptomatic cases beyond the definition imposed in this study, would be lower. Further, an estimate of the infection fatality ratio IFR would represent risk of fatality among all infections, which includes asymptomatic infections, and be even lower than the CFR for all YF cases.

Relaxing the symptomatic definition to include cases of confirmed YF presenting in healthcare settings did not lead to notable differences in CFR estimates Table 2. Other studies using systematic review methods to estimate the CFR of other diseases commonly have more available papers relevant to the study aims [ 16 , 55 , 60 ], though others have had similarly lower article counts [ 54 , 61 , 64 ].

Many of these studies also used the I 2 statistic to consider heterogeneity, with many of them similarly showing high heterogeneity [ 20 , 21 , 22 ]. Stratification by geography was also seen in other studies [ 54 , 55 ]. This study benefits from the use of a comprehensive strategy for literature review, which maximizes the completeness of data available for analysis. Conducting a literature review rather than estimating CFR solely from surveillance data allowed multiple outbreak investigations to contribute to the data analysis.

As a result, studies with researchers playing a more active role in surveillance of YF cases, which may have greater accuracy, were included. This study also stratified CFR by the methods of the individual studies into investigative and reporting studies. Both types of studies could experience different limitations to accuracy. Following the updated search strategy results, the similarity between the two estimates can demonstrate consistency, and potentially validity, in these two types of surveillance.

The analyses in this study included CFR estimates for confirmed and suspected severe YF cases separately as well as combined. Because YF can present similar symptoms and be misdiagnosed for other diseases such as dengue [ 65 ], there is less certainty of whether suspected YF cases in this study are true YF cases. However, the similarity in stratified results comparing laboratory confirmed and suspected YF cases shows that excluding the suspected cases from analyses would not lead to a substantial change in conclusions.

An initial aim of this study was to use the systematic review to also collect data to estimate total cases through estimating proportions of cases that are asymptomatic and mild, similarly to the study by Johansson et al. There were insufficient studies from the literature review to reliably generate these estimates due to inconsistency of study results and few studies reporting such information. This is evidence of the challenges inherent to collecting highly detailed data, particularly in less affluent nations, which typically experience higher burdens of YF and other vector-borne diseases.

However, having a reliable estimate for CFR, as generated in this study, can prove useful for attempting to quantify underreporting of YF cases. Case reports with higher proportions of fatal cases may suffer from underreporting under the assumption that the CFR found in this study is broadly applicable to other incidence of YF. For example, using data provided from the Pan American Health Organization and the Brazilian Ministry of Health, fatal among confirmed cases of YF were reported via surveillance in Brazil between and , which may include non-severe cases.

By multiplying the fatal cases by the inverse of the estimated CFR, an estimate of severe YF cases is obtained. This serves as a minimum proportion of underreported cases rather than an estimate [ 15 ] since this assumes all fatal cases were observed and all reported cases were severe. Through the literature search, 14 studies were identified to fit the defined criteria for severe YF, 13 of which were suitable to be used in meta-analysis. The requirement that studies must indicate that cases present fever as well as either jaundice or hemorrhaging for inclusion in this study led to several studies to be excluded.

Many studies stated numbers of cases and fatalities without specifying symptoms [ 44 , 66 , 67 , 68 , 69 , 70 , 71 ], which included studies from the recent outbreak in Angola [ 66 , 67 ]. Studies representing cases from the recent YF outbreak in Brazil, though not stating that all cases reported showed the symptoms, were added to the analyses to show whether inclusion of confirmed cases from a clinical setting might impact substantive results [ 50 , 51 , 52 , 53 ]. While the symptom requirements in this study led to potentially useful sources of information to be excluded from analysis, they do increase confidence that the CFR estimated applies directly to severe YF cases by not including potentially mild cases.

Similarity in results when including four studies of YF cases seeking healthcare increase confidence that the results may be more broadly applicable. The results of this study rely on the reported data from the 17 studies used in the meta-analysis. Because the purpose of these articles was not necessarily to offer estimates of the CFR for YF, it is possible that maximizing the accuracy of fatal and nonfatal case counts was not the highest priority.

The studies detailing outbreak investigations do report numbers of severe and fatal cases, but the purpose was not to assure generalizable accuracy of the CFR. This possibility is even stronger among reporting studies. Since underreporting of infectious disease cases is a well established issue [ 72 ], it is likely that the proportions used in this analysis may also be subject to issues of data quality.

Within this review, the results are limited by the heterogeneity in studies and the assumption that different world regions are expected to have similar CFRs. In combining the studies across nations in South America and Africa, where stratified CFRs differed notably, it is assumed that the differences observed are artifacts of the individual studies rather than indicative of actual differences in CFR across the two continents. Heterogeneity likely exists within continents as well, as the nations represented in this study include both East and West Africa Fig.

This heterogeneity may result from actual differences in probability of fatality; risk of fatality may differ by population demographics [ 1 , 73 ] or national industrialization [ 62 ], as seen in other diseases. This is lower than the frequently cited CFR for severe cases, indicating that the previous estimate is either a cautious estimate or based on underreported data. However, these results indicate high fatality among severe YF cases, demonstrating the public health importance of this disease.

Preventative measures such as vaccination and diagnosis methods are of importance for reducing deaths from YF. Use of systematic reviews for estimating CFR has been seen for other diseases, and this method can be extended to further characteristics of various diseases beyond CFR. Further research is needed to distinguish among asymptomatic, mild, and severe YF infections in order to most accurately estimate the total burden of disease. The estimate of CFR found in this study can be used to estimate potential mortality in future YF outbreaks.

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