case study of gifted child

The case for gifted education

Editor’s note: This is an edition of “Advance,” a newsletter from the Thomas B. Fordham Institute written by Brandon Wright, our Editorial Director, and published every other week. Its purpose is to monitor the progress of gifted education in America, including legal and legislative developments, policy and leadership changes, emerging research, grassroots efforts, and more. You can subscribe on the Fordham Institute website and the newsletter’s Substack .

We have ample evidence that a number of education programs targeted at advanced students significantly improve their learning outcomes. Because of that, high-quality gifted education—or what would be better labeled “advanced education”—has two primary benefits. One, it helps maximize the potential of participating students, which is something every child deserves. And two, in better developing the talent of these advanced students, it supports America’s economic, scientific, and technological prowess in an increasingly competitive global market. It’s therefore important that more school leaders adopt these policies and implement them well.

As Jonathan Plucker, Julian C. Stanley Professor of Talent Development at Johns Hopkins University, explained in a Fordham Institute article a couple years ago, the two interventions with the most robust evidence behind them are acceleration and ability grouping—with enrichment, such as summer and residential programs, having generally positive results, too.

Acceleration is “an academic intervention that moves students through an educational program at a rate faster or at an age that is younger than typical,” reports the highly-respected Belin-Blank Center at the University of Iowa . It comes in at least twenty forms, with the most common being whole grade skipping and receiving higher-level instruction in a single subject. It is “one of the most-studied intervention strategies in all of education, with overwhelming evidence of positive effects on student achievement,” writes Plucker. One study that looked at approximately 100 years of research on the intervention’s impact on K–12 academic achievement, for example, found three meta-analyses showing that “accelerated students significantly outperformed their nonaccelerated same-age peers,” and three others showing that “acceleration appeared to have a positive, moderate, and statistically significant impact on students’ academic achievement.” The Belin-Blank Center also offers an excellent and thorough summary of the evidence related to acceleration.

Numerous high-quality studies have also found that flexible ability grouping—arranging students by academic achievement in the same or separate classrooms—is a net positive for advanced students and isn’t detrimental to their peers. The aforementioned review of a century of research, for example, looked at thirteen meta-analyses of ability grouping, and three models boosted outcomes: within-class grouping, cross-grade subject grouping, and special grouping for the gifted. Moreover, there seemed to be little downside for medium- and low-achieving students, and often upside . Research on curriculum models can also be placed under the ability-grouping umbrella, and “ those studies suggest that pre-differentiated, prescriptive curricula lead to significant growth in advanced learning,” writes Plucker.

Because these interventions work, we ought to use them. Why? Because doing so benefits both the individual students and the country in general. Each and every child deserves an education that meets their needs and enhances their futures, and advanced students are no different. They have their own legitimate claim on our conscience, our sense of fairness, our policy priorities, and our education budgets.

What’s more, many of them also face such challenges as disability, poverty, ill-educated parents, non-English-speaking homes, and tough neighborhoods. Many also attend schools awash in low achievement, places where all the incentives and pressures on teachers and administrators are to equip weak pupils with basic skills in reading, writing, and arithmetic. Such schools understandably invest their resources in boosting lower achievers. They’re also most apt to judge teachers by their success in doing that and least apt to have much to spare—energy, time, incentive, or money—for students already above the proficiency bar.

It’s advanced students from these disadvantaged and oft-marginalized backgrounds who most need these programs—but they’re also the least likely to have access to them. A Fordham study in 2018 called Is There A Gifted Gap? found, for example, that White students constitute 47.9 percent of the student population but 55.2 percent of those enrolled in advanced learning programs, while the comparable figures for Black students are 15.0 and 10.0 percent, and for Hispanic students, 27.6 and 20.8 percent. And these forces contribute to widening gaps as they progress through grades. Those latter student groups are 49 and 23 percent less likely, respectively, to participate in Advanced Placement than their peers, and 62 percent and 51 percent less likely, respectively, to take part in International Baccalaureate courses when attending a school that offers them. Better-designed programming for advanced students in more places, implemented well, would help change that.

The second big reason for more and better advanced education interventions is that the country needs these children to be highly educated to ensure its long-term competitiveness, security, and innovation. They’re the young people most apt to become tomorrow’s leaders, scientists, and inventors, and to solve our current and future critical challenges. The same point was framed in different words in the 1993 federal report titled National Excellence: A Case for Developing America’s Talent : “In order to make economic strides,” the authors wrote, “America must rely upon many of its top-performing students to provide leadership—in mathematics, science, writing, politics, dance, art, business, history, health, and other human pursuits.”

But the U.S. and its schools have long underperformed many of our competitor countries, according to two respected international metrics: the OECD’s Program for International Student Assessment (PISA) and the Trends in International Mathematics and Science Study (TIMSS) , in which dozens of countries participate. PISA tests fifteen-year-olds in math, science, and reading, and organizes its scores into seven levels, from 0 to 6, with high scorers generally being those who reach level 5 or 6. TIMMS assesses fourth and eighth graders in math and science and splits its scores into five levels, with a high achiever judged as one who reaches at least 625 on the relevant scales.

Using these cutoffs on the most recent math assessments—2018 for PISA and 2019 for TIMSS—illustrates the magnitude of the problem.

In the TIMSS results, the U.S. ranks eleventh in grade four and eighth in grade eight. In both, America landed behind Singapore, Taiwan, South Korea, Japan, Hong Kong, and Russia. Worse, the top-performing countries have two, three, and in the case of Singapore, almost four times the proportion of advanced students as does the U.S. The only silver lining is that many of these countries are small. America’s vast scale means that we have a decently large number of high achievers in raw numbers.

PISA paints an even worse picture for high-achieving high school students in the U.S., mirroring our dismal NAEP results for twelfth-graders . Rankings include all members of the OECD that took the assessment, plus Hong Kong, Macau, Taiwan, and a quartet of Chinese cities (Beijing, Shanghai, Jiangsu, and Zhejiang). That’s a total of forty jurisdictions. The United States comes in thirty-fourth, behind all participants in Asia and every participant in Europe except Spain, Turkey, and Greece.

The problem, of course, is not that the United States lacks smart children. It’s that such kids aren’t getting the education they need to realize their potential, allowing other countries like China to forge ahead. Using other international test data, for example, economists Eric Hanushek and Ludger Woessmann estimate that a “10 percentage point increase in the share of top-performing students” within a country “is associated with 1.3 percentage points higher annual growth” of that country’s economy, as measured in per-capita GDP. Which is to say, if the U.S. propelled more of its young people into the ranks of high achievers, it would be markedly more prosperous—with faster growth, higher employment, better wages, and all that comes with these. As the United States faces ever-steepening economic competition from China and elsewhere—not to mention mounting challenges to our national security and wellbeing, including climate change, intergenerational poverty, growing partisanship, and much more—the stakes are high and rising.

The good news is that we have evidence-based methods for reversing these trends: acceleration, ability grouping, and enrichment programs. When well-designed and carefully implemented, these interventions have long proven to boost the achievement of advanced students. This in turn gives these young people the education they deserve, and helps ensure American competitiveness, prosperity, and security for future generations. Sadly, far too many schools don’t offer these services or don’t implement them well, and there’s a misguided push to eliminate them in more places. Instead, more districts should adopt them—the sooner the better.

QUOTE OF NOTE

“A group of U.S. children could be set up for failure, despite the fact that they have a notable academic advantage over their peers. Gifted children fall victim to a belief shared by parents, educators, and legislators alike that they ‘will be fine on their own.’”

“ When the ‘gifted’ kids aren’t all right ,” Deseret News, Addison Whitmer, November 22, 2022

THREE STUDIES TO STUDY

“ Who Is Considered Gifted From a Teacher’s Perspective? A Representative Large-Scale Study ,” by Jessika Golle, Trudie Schils, Lex Borghans, and Norman Rose, Gifted Child Quarterly, Volume 67, Issue 1, 2023

“Teachers play important roles in identifying and promoting gifted students. An open question is: Which student characteristics do teachers use to evaluate whether a student is gifted or not? We used data from a representative sample of Dutch primary school teachers (N = 1,304) who were asked whether or not they thought the students (N = 26,720) in their class were gifted. We investigated students’ cognitive and noncognitive attributes as well as demographic factors that might be relevant for this judgment. In sum, the findings revealed that teachers considered students to be gifted when, in comparison with their peers, students were superior in cognitive domains, especially with respect to academic achievement, scored higher on openness to experience and lower on agreeableness, were male, were younger, and came from families with higher parental education.”

“ Promises, Pitfalls, and Tradeoffs in Identifying Gifted Learners: Evidence from a Curricular Experiment ,” by Angel H. Harris, Darryl V. Hill, and Matthew A. Lenard, Annenberg Institute at Brown University, July 2022

“Disparities in gifted representation across demographic subgroups represents a large and persistent challenge in U.S. public schools. In this paper, we measure the impacts of a school-wide curricular intervention designed to address such disparities. We implemented Nurturing for a Bright Tomorrow (NBT) as a cluster randomized trial across elementary schools with the low gifted identification rates in one of the nation’s largest school systems. NBT did not boost formal gifted identification or math achievement in the early elementary grades. It did increase reading achievement in select cohorts and broadly improved performance on a gifted identification measure that assesses nonverbal abilities distinct from those captured by more commonly used screeners. These impacts were driven by Hispanic and female students. Results suggest that policymakers consider a more diverse battery of qualifying exams to narrow disparity gaps in gifted representation and carefully weigh tradeoffs between universal interventions like NBT and more targeted approaches.”

“ The Experience of Parenting Gifted Children: A Thematic Analysis of Interviews With Parents of Elementary-Age Children ,” by Jodi L. Peebles, Sal Mendaglio, and Michelle McCowan, Gifted Child Quarterly, Volume 67, Issue 1, 2023

“This qualitative study aimed to delve deeply into the phenomenon by interviewing parents of elementary-age gifted children. We conducted 12 interviews with parents whose children attended gifted schools. The interview transcripts were analyzed using thematic analysis to identify key themes related to the experience of parenting gifted children. Themes identified included the parents’ description of a “child-driven” approach to parenting, experiencing social isolation due to a lack of understanding, and physical and emotional feelings of exhaustion. The findings are particularly important for parents of gifted children, and other professionals who would benefit from a better understanding of the day-to-day experience of raising gifted children.”

WRITING WORTH READING

“ Does growth mindset matter? The debate heats up ,” Hechinger Report, Jill Barshay, December 5, 2022

“ From a formerly gifted and talented kid, now burnt-out adult: Slow down and take care of yourself ,” The Flat Hat, Vivian Hoang, December 5, 2022

“ Teens embrace AP class featuring Black history, a subject under attack ,” Washington Post, Sydney Trent, December 2, 2022

“ NYC’s ‘gifted and talented’ application timeline moves up ,” Chalkbeat, Michael Elsen-Rooney, November 30, 2022

“ Should your child take AP or IB classes? It could save them thousands in tuition .” Green Bay Press-Gazette, Danielle DuClos, November 29, 2022

“ Schools for gifted students: What to know ,” U.S. News, Andrew Warner, November 29, 2022

“ Michigan to start notifying parents of AP eligibility ,” News-Herald, Matthew Fahr, November 24, 2022

“$1.5 million NSF award will power scholarships and support for high-achieving, low-income engineering students ,” Temple Now, Sarah Frasca, November 18, 2022

“ We need to rethink gifted and talented education in NC ,” The Daily Tar Heel, Georgia Roda-Moorhead, November 15, 2022

Brandon Wright is the Editorial Director of the Thomas B. Fordham Institute. He is the coauthor or coeditor of three books: Failing our Brightest Kids: The Global Challenge of Educating High-Ability Students  (with Chester E. Finn, Jr.), Charter Schools at the…

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The Young Gifted Learner: What We Know and Implications for Early Educational Practice

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Research into giftedness in early childhood has been a neglected area in gifted education studies, there being until relatively recently only a handful of older studies carried out in the USA (Gottfried, Gottfried, Bathurst, & Guerin, 1994 ; Robinson, 1993 ; Roedell, 1986 ). Over the last two decades, in the Asia-Pacific area research into giftedness and gifted education in the early years has become an area of relative strength. Some major areas of investigation have been gifted development from infancy to early school years, transition of gifted children into formal education settings, response of early childhood teachers to young gifted children, gifted early readers, and educational planning and practice with young gifted children (Grant, 2005; Hodge & Kemp, 2006; Margrain, 2010 ; Morrissey, 2007 ; Walsh, Bowes, & Sweller, 2017 ). However, the real value of a body of evidence-based information is in its application to educational practice to enable young gifted children to thrive in their educational program. While a reasonable body of evidence about early characteristics of giftedness is now available, there is less empirical detail about reliable educational practice. Nonetheless, these current findings about young gifted children can be applied to high-quality early educational practice with them, including across cultures. In this chapter, many research-based suggestions for effective practice will be provided, Towards the end, the implications for future research directions within the early childhood field are included.

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Gifted Education: Best Practices and Methods for Educating Gifted Youth from a Christian Perspective

Gifted education in the asia-pacific: from the past for the future: an introduction.

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Grant, A., Morrissey, AM. (2021). The Young Gifted Learner: What We Know and Implications for Early Educational Practice. In: Smith, S.R. (eds) Handbook of Giftedness and Talent Development in the Asia-Pacific. Springer International Handbooks of Education. Springer, Singapore. https://doi.org/10.1007/978-981-13-3041-4_57

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Intelligence

What a century of research reveals about gifted kids, what we've learned from 100 years of longitudinal research on the gifted.

Posted January 30, 2017

A recent article published by distinguished gifted education scholar David Lubinski of Vanderbilt University, “ From Terman to today: A century of findings on intellectual precocity ,” serves as an excellent resource for parents, students, and educators who are interested in the findings of two major longitudinal studies of the gifted which roughly span the last century, and more broadly the historical progression of research on the gifted. Here are brief descriptions of the longitudinal studies:

Lewis Terman’s Genetic Studies of Genius: Launched in the early 1920’s and included over 1,500 adolescents identified in the top 1% of general intellectual ability.

Julian Stanley’s longitudinal Study of Mathematically Precocious Youth (SMPY): Launched in the early 1970’s, now co-directed by Camilla P. Benbow and David Lubinski, and included over 5,000 adolescents identified in the top 1% of general intellectual ability.

The level and pattern of abilities matter

Terman’s study showed that top 1% individuals tended to be quite successful overall. SMPY findings also showed that top 1% individuals are quite successful then documented that more ability matters even within that highly select 1% and that one’s pattern of math, verbal, and spatial abilities over and above their general ability matters in the prediction of multiple educational, occupational and creative outcomes.

Ability level: SMPY findings have demonstrated that even within the top 1% of ability, more ability matters. Therefore the idea that beyond a certain ability threshold, say an IQ of 120, more ability doesn’t matter has been shown to be false.

Ability pattern: SMPY extended the findings of Terman by showing that in addition to general ability level, an individual’s level and pattern of math, verbal, and spatial ability all played an important role in the prediction of later outcomes. For example, individuals with relatively higher verbal compared to math/spatial talents tend to end up in humanities professions, whereas individuals with relatively higher math/spatial compared to verbal talents tend to end up in STEM professions.

Interests and values matter

Measured interests and values of gifted youth also predict later outcomes over and above ability level and pattern. Theoretical (the discovery of truth: empiricism, intellectualism), Economic (that which is useful: resourceful, practical affairs), Aesthetic (form and harmony: grace, artistry in life), Social (love of people: altruism , sympathy, caring), Political (power in all realms: influence, leadership ), and Religious (unity of life: comprehension of life’s meaning, holiness) values and their pattern all helped improve prediction of later outcomes.

Educational stimulation and hours devoted to talent development matters

Both the Terman study and SMPY study showed that advanced educational stimulation matters for gifted individuals to fully develop their talent and actualize their intellectual potential. One study from SMPY showed that grade skipping is a highly effective intervention on later achievement, and another study showed that it may not necessarily be one specific intervention that matters for the development of gifted youth but rather the right mix and intensity of interventions—the appropriate educational dosage—to keep them intellectually stimulated and engaged. Additionally, findings from SMPY have also shown that the willingness to work long hours varies greatly among the gifted population and thus is also likely connected to long-term development of expertise.

In general, gifted youth grow up to be highly accomplished and well-adjusted adults

In 1916, the predominant view of the gifted child was “early to ripe, early to rot,” including the idea that gifted kids were physically weak and emotionally unstable. However, Terman’s findings by the 1930’s had already shown this to be incorrect. Findings from SMPY indicate that, broadly, gifted youth grow up to be highly accomplished adults, achieving doctorates, a higher income, patents, publications, university tenure and other creative achievements at very high rates relative to the general population. Gifted youth also grow up to be no different from their same age peers in terms of reported broad life satisfaction regarding personal and family life.

Of course, this review of the research and highlights of key findings is based on gifted students overall, and the individual path through life for each gifted student is certainly not average but unique. However, these broad findings can be useful in understanding what longitudinal research across the last 100 years has demonstrated and should be known by parents, students, and educators who hope to help gifted youth develop to their fullest.

Lubinski, D. (2016). From Terman to today: A century of findings on intellectual precocity . Review of Educational Research, 86 , 900-944.

Jonathan Wai, Ph.D. , is Assistant Professor of Education Policy and Psychology and the 21st Century Endowed Chair in Education Policy at the University of Arkansas.

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Emotional and Behavioral Characteristics of Gifted Children and Their Families

1 Yıldırım Beyazıt University, Yenimahalle Training and research Hospital, Department of Child and Adolescent Mental Health and Disease, Ankara, Turkey

Ayla Ömerelli Çete

2 Gaziemir Nevvar Salih İşgören State Hospital, Emergency, İzmir, Turkey

Sibelnur Avcil

3 Medical Faculty of Adnan Menderes University, Department of Child and Adolescent Mental Health and Disease, Aydın, Turkey

Burak Baykara

4 Medical Faculty of Dokuz Eylül University, Department of Child and Adolescent Mental Health and Disease, İzmir, Turkey

Introduction:

To compare the quality of life, areas of social, emotional, behavioural and mental problems and family functionality of gifted children and children of normal intelligence.

The study included 49 gifted children aged 9-18 years and 56 age and gender-matched healthy children of normal intelligence. The Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL), and the Children’s Depression Rating Scale were applied to all the cases. The Quality of Life Scale for Children, the Depression Scale for Children, the Trait-State Anxiety Inventory, and the Strengths and Difficulties Questionnaire- Adolescent Form were completed by all the participants. All the parents completed the Family Evaluation Scale, the Strengths and Difficulties Questionnaire- Parents Form and the Parents Form of the Quality of Life Scale for Children.

Compared to children of normal intelligence, gifted children described themselves as more inattentive and lively, social functionality was reported to be low and they had a worse perception of their physical health status. Gifted boys were determined to have more depressive symptoms than gifted girls. The parents of boys of normal intelligence reported lower academic performance than the parents of giftedboys. This difference was not determined for girls between the cases and comparative groups.

Conclusion:

All the findings obtained in this study suggest that gifted children are at risk in respect of mental health. Therefore, to be able to become healthy adults in a biopsychosocial aspect, it is important for the future of gifted children that this status can be identified at an early age, that they can receive appropriate education, that support and counselling are provided for emotional needs and that parents and teachers are fully informed.

INTRODUCTION

The definition of giftedness comprises of superior intelligence level, superiority in academic field and leadership skills, creativity and artistic skills ( 1 ). For the full understanding of the potentials of gifted students, the using of multiple diagnostic tools gives more reliable results ( 2 ). In Turkey, in determining of gifted students, teacher notification, aptitude tests, individual intelligence tests are used generally ( 3 ).

The different social and emotional needs arising from the asynchronousity between the cognitive and physical development of gifted children and problems that may arise from them are a subject that has been studied for years ( 4 ). It is emphasized that when compared with their peers, gifted children emotionally and socially can have different needs in comparison with their peers ( 5 , 6 ). There are data about gifted children’s being socially more isolated, less sensitive to thoughts of their peers, less adapted to their environment and society ( 7 ).

Reasons such as extreme and unrealistic expectations of parents and teachers, their intense concerns, discordance between the child’s ability and teaching, difficulties in peer relationships, difficulty in understanding by the social environment, suggest that behavioral and emotional problems may occur more frequently in this group ( 8 - 10 ).

Beside these, in the gifted group; psychological problems such as inadequacy in learning ( 1 , 11 ), high test anxiety and general anxiety level ( 12 ), somatization ( 10 ), lack of self-confidence accompanied by depressive symptoms ( 13 ), attention deficit hyperactivity disorder were also found to accompany more frequently ( 1 ).

Therefore, it is important to assess gifted children in many dimensions such as academic field, self-perception, social skills, emotional and mental health ( 14 ).

Families with gifted children are reported to have higher levels of anxiety to meet the special needs of their children. These families feel themselves more inadequate and less equipped. It is reported that they are less permissive to their children and tend to use an authoritarian style. Because of these features, a gifted child is not only face difficulties in school functioning and peer relations; but also known to face difficulties in family relationships ( 15 ).

In the literature, there could not find any studies which had researched the quality of life of gifted children. In this study, it was also aimed to compare the quality of life of gifted children with those of normal intelligence. Besides; it is aimed to assess social, emotional, behavioral and family functionalities of a gifted child and to compare these functions with children with normal intelligence.

On the basis of the data in the literature; in this study, hypotheses were formed that by comparison to peers with normal intelligence, gifted child’s having exhibited anxiety and depressive mood in increased frequency; having had more problems on social, behavioral, and family functionalities, and for these reasons the quality of life of gifted children will be at a lower level.

The study was conducted with the participation of 49 gifted and 56 normal intelligent children and adolescents. Gifted and normal intelligent children and adolescents without chronic medical disease, aged 9-18 years, haven’t had a psychiatric diagnosis of axis I according to criteria DSM-IV-TR, who voluntarily accept to participate in the study, were compared in terms of quality of life by the Pediatric Quality of Life Inventory (PedsQL); social, emotional, behavioral, psychological problem areas by the Strength and Difficulties Questionnaire (SDQ), the State-Trait Anxiety Inventory for Children (STAI-C), the Child Depression Inventory (CDI) and the Children Depression Rating Scale Revised (CDRS-R), family functioning by the Family Assesment Device (FAD).

A sample group was created by choosing gifted children (Group I) who study at Izmir Narlıdere Sıdıka Akdemir Science Art Center (INSASAC), and choosing normal intelligent children (Group II) with total intelligence points ranged 90-109 in the Wechsler Intelligence Scale for Children (WISC-R) who study at Ertugrul Gazi Primary School (EGPS). The WISC-R is first applied to children who are guided by the thought of being gifted, so that they can gain the right to education at INSASAC. Secondly, the Primary Mental Abilities (PMAs) Test is applied to children with a total intelligence score of 130 or higher in WISC-R to analyze their skill areas. Group I in the study has been made up of gifted children studying in INSASAC. Therefore, the previously applied WISC-R and PMAs were not reapplied.

In order to ensure the equivalence of compared groups, family relationships and sociodemographic factors that may affect the mental state of children have been identified. These factors are scored in sociodemographic data form as education status, number of siblings in the family, birth order, number of people living in the family, mother’s age at birth, maternal education status, maternal employment status, paternal education status, paternal employment status, cohabitation of mother and father, family income, residing, family history of medical illness, family history of mental disorder, school success, and peer relationships. It was aimed to make the groups equivalent through the criteria. However, the unmatched factors were matched to the closest criteria (number of siblings, income status, birth order, education status of mother and father, mother’s age at birth).

Schedule for Affective Disorders and Schizophrenia for School Age Children-Present and Lifetime Version-Turkish Version (K-SADS-PL-T): The K-SADS-PL-T is a semi-structured interview form which is developed by Kaufman et al. (1997) in order to determine past and present psychopathologies of children and adolescents according to DSM-III-R and DSM-IV diagnostic criteria. The K-SADS-PL-T is applied through interviews with the parents and the child himself/herself ( 16 ). Validity and reliability study for the Turkish form was done by Gökler et al (2004)( 17 ).

Pediatric Quality of Life Inventory (PedsQL): The scale developed by Varni et al. in 1999 ( 18 ), aims to evaluate the general quality of life in the 2-18 age group. The scale consists of four sub-sections that question physical, emotional, social, and school-related functioning. Validity and reliability study for the Turkish form of the inventory, was done for 2–18 age group ( 19 ).

State-Trait Anxiety Inventory for Children (STAI-C): Turkish adaptation studies of the scale which is developed in order to determine the level of “trait and state anxiety” of the students, was done by Özusta (1993) ( 20 ).The adaptation studies of the scale demonstrate its applicability in the 9–16 age group.

Child Depression Inventory (CDI): The scale which adapted to Turkish in 1990 by Öy, is filled by the child ( 21 ).The maximum score on the twenty-seven-item scale is 54 and cut-off score is recommended as 19 ( 22 , 23 ).Elevation of total score points the severity of the depression level.

Strength and Difficulties Questionnaire (SDQ): For use in screening psychological problems in children and adolescents, SDQ was developed by Robert Goodman in 1997. The SDQ comprise of 25 questions, some of which question positive behavioral characteristics and some of which question negative ones. These questions were collected in five sub-headings. These headings are conduct problems, inattention and hyperactivity, emotional problems, peer problems and social behaviors ( 24 ). Scale which had adapted to Turkish was observed to be consistent and reliable ( 25 ).

Children Depression Rating Scale Revised (CDRS-R): The CDRS-R is a 17-item scale used in clinical trials to assess the severity of depression and alterations in depressive symptoms in depressed children and adolescents. Twenty-eight points and below indicate remission, and 40 points and above indicate depression. This scale was adapted to Turkish in 2012. As a result of the validity and reliability studies, the Turkish version of CDRS-R was found to have good psychometric properties ( 26 ).

Family Assesment Device (FAD): The scale was developed by Brown University and Butler Hospital in the US in 1983 ( 27 ). It was developed to evaluate whether the family fulfill their functions and to reveal the problems, it consists of 60 items. Turkish adaptation study was done by Bulut (1990) ( 28 ).

Primary Mental Abilities (PMAs) Test: The PMAs test was developed by T. G. Thurstone and L. L. Thurstone as three separate forms to be applied to 5–7, 7–11 and 11–17 age groups to identify mental ability fields. Adapting to Turkish was made in 1953 by the Ministry of National Education ( 29 ).

Sociodemographic data form: In the form of data, regarding child; date of birth, education status, school success, peer relationships, birth order, regarding parents; education levels, cohabitation status, occupational status and income levels, number of children, diagnosis of physical disease and/or mental disorder in parents/children are included.

Collection of Data

The study was found to be ethical in accordance with the decision of the Ethics Committee of Dokuz Eylul University dated 05.01.2012 and numbered 2012/01-23. On account of the decree of Ministry of National Education dated 04.04.2012 and numbered 21194, a permit has been issued in order to carry out the study in involved schools. Also obtaining permission from INSASAC and EGPS Directorates, all children were informed individually. Verbal approval was obtained from 105 students who met the participation criteria and accepted to participate. Written acknowledgment and scales which expected to be filled by the parents were sent to families of both groups and collected through their children. At this stage, verbal approvals were obtained through informing the family about the study and interviewing them by the telephone or face-to-face. The sociodemographic data form and the CDRS-R were filled in by the clinician for the students who were given an approval, and in order to exclude any psychiatric diagnosis that may be present in the children in both groups, the K-SADS-PL-T was applied in the parent-teacher interview room in their schools. By children individually, PedsQL 8–12, 13–18 age form; CDI, STAI-C, SDQ adolescent form were filled in respectively. The FAD, SDQ-parent form, PedsQL 8–12 or 13–18 age parent form were filled in by mothers and/or fathers of the students.

In order to evaluate their total intelligence score, The WISC-R psychometric intelligence test was applied to children in Group II by an experienced psychologist at Dokuz Eylul University Medical School Hospital. The WISC-R psychometric test, which was applied to the children in Group I at guidance and research center during the application to INSASAC was not reapplied to the students in the scope of the study.

Evaluation of Data

SPSS Windows 15.0 package program was used in statistical evaluation of the data obtained in study.

The mean age between group I and II was compared using t-test in independent groups, and gender distribution was compared using Pearson Chi-Square Test. T-test and two-way analysis of variance (two-way ANOVA) were used in the analysis of continuous data between the two groups. Two-way ANOVA was used to assess together the statistical significance of the differences in mean values over scale scores and the effects of the group (group I and group II) and gender (male and female) over averages of the scale scores. Statistical significance level was determined as p <0.05.

Group I and group II were matched in terms of gender ratios. Thus, gender distribution does not differ between group I and group II. There are 22 girls (45%), 27 boys (55%) in group I and 25 girls (45%), 31 males (55%) in group II. There was not also any significant difference between the age distributions of the groups (group I: 132.00 ± 16.26 months, group II: 131.78 ± 16.66 months, t =0.103, p =0.947, t-test in independent groups).

There was not any statistically significant difference between the group I and group II in terms of the scores which are taken in STAI-C for assessing their state and trait anxiety, CDI for assessing their depression levels, CDRS-R for assessing their depressive symptoms by the clinician (p>0.05) ( Table 1 ). In the CDRS-R, males in group I were found to have statistically significant higher depressive scores than females in group I (2x2 ANOVA, group I *gender, F=4.797, p=0.031, Partial η2=0.045) ( Figure 1 ). When the effect of the puberty on depressive scores in group I was examined, there was not any statistically significant difference in the mean of CDRS-R scores of boys who are in prepubertal and pubertal age range, in group I (Mann-Whitney U test, Z=-1.763, p=0.078).

Mean Scores of Children in Group I and Group II

CDI: Child Depression Inventory, CDRS-R: Children Depression Rating Scale Revised, SDQ: Strength and Difficulties Questionnaire, PedsQL: Pediatric Quality of Life Inventory

T Scores of Children Depression Rating Scale Revised (CDRS-R) in Group I and Group II According to Genders

*2 x 2 ANOVA case group*gender, F=4.797, p=0.031, Partial η2=0.045

In group I and group II, subtest scores of the SDQ child form which is applied for screening psychological problems were compared with the t-test in independent groups, and statistically significant differences were found only between the scores of inattention/hyperactivity subtest scores (p = 0.036) while there was no significant difference in other subtest scores ( Table 1 ). A statistically significant difference was found between the genders in the peer problems subtest of SDQ child form (2×2 ANOVA gender effect; F=5.038, p=0.027, partial η2=0.048) ( Table 2 ). Boys in both groups which participate to study, were found to have higher levels of peer relationship problems than girls at a statistically significant level, in peer problems subtest. A statistically significant interaction was found between gender and groups as a result of 2×2 ANOVA (gender × group) applied in the SDQ child form social behaviour subtest (F=4.821, p=0.004, partial η2=0.125) ( Table 2 ). Girls in both groups which participate to study were found to have higher social behaviors than boys at a statistically significant level in SDQ child form social behaviour subtest (2×2 ANOVA gender effect; F=12.024, p=0.001, partial η2=0.106) ( Table 2 ).

Mean Scores Between Genders in Peer Problems Subtest and Social Behaviour Subtest of Strength and Difficulties Questionnaire Child Form, Social Functioning Subtest of Pediatric Quality of Life Inventory Self-Assessment Form

GGA: Güçler Güçlükler Anketi, ÇİYKO: Çocuklar için Yaşam Kalitesi Ölçeği.

There was not any statistically significant difference between mean scores of the group I and group II, in the subtest scores of the SDQ- parental form, according to t-test results in independent groups (p >0.05) ( Table 3 ).

Mean Scores of Parents of Children in Group I and Group II

PedsQL: Pediatric Quality of Life Inventory, SDQ: Strength and Difficulties Questionnaire, FAD: Family Assesment Device

In order to evaluate the overall quality of life of Group I and Group II, PedsQL self-assessment scale was applied to children and adolescents. The average of Physical Health Total Score, a subtest of the PedsQL self-assessment scale, were found to be statistically significantly lower in Group I than Group II (p=0.037) ( Table 1 ). It was found that gender difference did not contribute to the difference between the groups (2×2 ANOVA gender effect; F=0.395, p=0.531, partial η2=0.004).

The average of PedsQL social functioning scores was found to be in a lower level close to statistically significantly lower level in group I than group II (F=3.898, p=0.051, partial η2=0.037) ( Table 1 ). When the effect of gender factor to social functioning subtest of PedsQL self-assessment scale was examined, boys participating in the study were seen to have statistically significantly lower PedsQL social functioning scores than girls participating in the study (2×2 ANOVA gender effect; F=5.559, p=0.020, partial η2=0.052) ( Table 2 ). In 2×2 ANOVA, statistically significantly low school functioning subtest scores of PedsQL parental assessment scale were obtained in group II males (F=2.732, p=0.048, partial η2=0.076) ( Table 4 ).

Mean Scores According to Groups and Genders in Children Depression Rating Scale Revised and School Functioning Subtest of Pediatric Quality of Life Inventory Parent Assessment Form

PedsQL: Pediatric Quality of Life Inventory

In “Affective Involvement” subtest of FAD, statistically significantly lower scores were obtained in group I than group II (p=0.035). There was not any significant difference between genders (2×2 ANOVA gender effect, F=0.024, p=0.877). In other FAD subtests, there was not found any statistically significant difference between groups ( Table 3 ).

In this study, gifted children were evaluated for depressive symptomatology. The depressive symptoms identified with CDRS-R by the clinician were found to be higher in gifted boys than in gifted girls. In conclusions of this study, gifted children have defined themselves more inattentive and hyperactive than children and adolescents with normal intelligence in SDQ self-report scale. In group I and group II, when their quality of life was compared, the gifted children were found to perceive their social functionalities and physical health statuses worse. Normal intelligent boys’ having been perceived as having low school functionalities by their parents is also one of the observed results. According to own evaluations of children and adolescents, another result obtained in the study is that boys participating in the study have reported lower social functioning and higher peer relationship problems than girls. In a way that supports this finding, according to their own evaluations, girls also assessed themselves more social than boys. When family functionalities was assessed with FAD, it was determined that family members of gifted children showed more interest, care and love for each other than group II.

In the literature, there are different datas about the anxiety level of children with high intelligence level. Some of the studies reports increased frequency of anxiety in individuals with high intelligence levels ( 10 , 12 , 30 – 33 ); while the other part reports that there is not any increased frequency of anxiety ( 34 – 38 ). Perfectionism ( 39 ), school changes, high academic expectations ( 40 ), future-related concerns, difficulties related to family and friends were often seen to be among sources of stress that can create anxiety complaints for gifted children ( 38 ). Good intelligence and problem-solving strategies are emerging as a protective factor against anxiety ( 35 ). This study supports the argument that anxiety is not seen at a higher level in gifted children than in children with normal intelligence.

In our study, while there was not any difference in depressive complaints according to self-report and clinical interview in most of all gifted children by comparison with group II, boys of gifted children group had high depressive scores in CDRS-R. In the literature, in some of the studies, it has been reported that increased frequency of depressive complaints are seen in gifted children ( 32 , 41 , 42 ), but in another studies, it is emphasized that gifted children show similar depressive symptoms like their peers with normal intelligence and ability level ( 43 – 46 ). This situation may be related to children’s having a chance to define existing depressive symptoms more easily in a clinical interview with CDRS-R. In relation to this finding, gifted children’s being able to hide their depression is indicated in the literature. This attitude may appear as a factor that makes it difficult to understand the frequency and extent of depression in gifted children. When the reason for increased depressive symptoms in boys of gifted group was considered, boys of group I were seen to have greatest difficulty score in SDQ emotional and total difficulty scores based on both self-report and parental reports.This increase in difficulty levels may be responsible for the increased frequency of depressive symptoms.

In our study, even though gifted children are not perceived inattentive and hyperactive by their families, they perceive themselves more inattentive and hyperactive than childrens in group II perceive themselves.

Inattention and hyperactivity are separate cognitive and behavioral processes. The SDQ applied in the study does not separately evaluate inattention and hyperactivity. Therefore, it is not clear whether this group perceived themselves as inattentive or hyperactive.

Due to their fast learning capacity, gifted children’s learning lessons easily and finding the curriculum boring is known ( 13 ). Since also hyperactivity symptoms of gifted children manifest especially in school during learning in the classroom, parents may not be able to observe inattention and hyperactivity symptoms in their children. When the literature is reviewed, it is reported that Attention Deficit Hyperactivity Disorder (ADHD) coexists in gifted children ( 47 – 49 ), and ADHD clinical features are similar to those of children with normal and low intelligence ( 50 , 51 ). However, Webb (2001) and Brazilian Council for Giftedness (CONBRASD) report that gifted children may misdiagnose with ADHD in an increasingly false positive ratio, even if they do not have ADHD ( 52 , 53 ). In the literature, it has been reported that inattention and hyperactivity symptoms can be seen in gifted children due to curriculum incompatibility or high creative ability features, which in turn can lead to false positive ADHD diagnosis ( 51 , 52 ). In our study, applying K-SADS-PL-T to both groups, ADHD and other axis I diagnoses were excluded. Inattention and hyperactivity complaints that gifted children have identified at increased frequency are thought to be related to giftedness. According to the results obtained from this study, when performing differential diagnosis of ADHD, it is necessary to consider giftedness. According to these results, gifted children’s perceiving themselves more problematic than group II in inattention and hyperactivity subtest of SDQ self-assestment scale suggests that they have difficulties in the classroom environment because of high skill level. On the other hand, according to the results of this study, gifted children’s attributing themselves more problems on inattention and hyperactivity than their parents is thought.

The quality of life is defined as the way in which an individual perceives their own situation within the culture and values system. This concept includes the physical health, mental health, level of independence, social relations, environmental factors and personal beliefs of the individual’s ( 54 ). The World Health Organization (1948) states that a multidimensional measure is necessary to assess health-related quality of life correctly and exactly, and this measure should at least include physical, psychological and social dimensions ( 55 ). In this study, group I perceived themselves more unhealthy than group II in terms of physical health quality of life. Gifted children mostly just focus on areas which they are capable of. Occupations which are related to outer world and are outside of their skill areas, mostly doesn’t motivate these children enough. Activities which outside of their skill areas remain at a restricted level. Assuming that out-of-school social and cultural activities are complementary to physical health, it can be supposed that the limitations in these areas lead to gifted children’s perceiving themselves physically more unhealthy. Besides, gifted children’s showing intense curiosity and interest to outer world is known ( 56 ). This intense curiosity and interest may also increase the awareness of these children to their bodies, as a result of this, normal physical difficulties which experienced may be reducing the perceived quality of life associated with physical health.

Furthermore, it is also known that gifted children can hide the depression which they are experiencing ( 41 ). In this respect, gifted children may tend to somatize their feelings, or may experience difficulty in the psychomotor field. In this study, although there were not determined any differences in the state-trait anxiety levels and depressive symptom levels of gifted children to group II, some studies in the literature reports increased somatization in gifted children ( 34 , 57 ). In this respect, the tendency of the gifted children to somatize their feelings may be the source of their feeling of being unhealthy. On the other hand, gifted children’s feeling themselves physically unhealthy may be arised from the greater number of adolescents in group I than in group II and also from physiological changes in adolescence.

It is known that the ability area of academically talented gifted children only includes one field like mathematics or language and these children generally have an avarage level of ability in other fields ( 3 ). Due to the fact that this study is made up of gifted children with talent in fields other than the psychomotor field and especially with talent in academic field, though this children demonstrate a superiority in their fields, their inability of demonstrating that superiority in the psychomotor field may have led them to perceive themselves more unhealthy. Therewithal, gifted children’s being at a less developed affective and psychomotor stage in proportion to their increased cognitive development stage is entitled as internal dyssynchrony. This internal dyssynchrony may have led them to perceive themselves physically more unhealthy.

When gifted children are examined regarding peer relationships, different results are observed. While some of the studies identify prominent problems in gifted children in peer relationships ( 58 – 60 ), some do not identify any problem ( 61 ). Also according to results of this study, giftedness negatively affects the quality of life in social functionalities. Especially in social-functioning quality of life subtest of PedsQL; given that gifted boys’ having had the lowest social-functioning quality of life points when they evaluate themselves, it can be predicted that the quality of life of gifted boys in social functionalities is at a risk. Moreover, depressive complaints which are seen in gifted boys more often than gifted girls may have negatively affect their quality of life in social functionalities. Because depressive disorder is a psychiatric disorder that increases the risk of medical disease and causes prominent problems in academic, work and social areas and in the family. On the other hand, gifted boy’s problems in the quality of life in social functioning may have led them to have higher depressive scores in the CDRS-R.

When academic achievement and school attendance are based as indicators of school functioning, it is reported that some of gifted children are successful, but the group experiencing difficulties in the emotional, behavioral, social, and psychological area that affect school life is unsuccessful ( 62 ). In addition; school success reduces in the presence of conditions like negative familial factors, comorbid learning disabilities, and ADHD ( 63 , 64 ). As a result of Matthews’ study (2006), it has been determined that about 10-20% of the group out of the education system is gifted children ( 65 ). In this study, presence of no difference in school functioning between gifted child and child with normal intelligence suggests that giftedness does not foresee a better school life. On the other hand, K-SADS-PL-T which is applied on this study, does not examine a diagnosis like learning disability which may affect school functioning, though it examine ADHD. Therefore, it could not determined that whether gifted children which involved in this study have a diagnosis of learning disability or not. Superior cognitive properties of gifted children may have hidden their learning disabilities and this situation may be the reason why they can not show better school functioning than children with normal intelligence.

In the literature, when strengths and difficulties which are seen in gifted children in social, emotional and behavioral areas are examined, while some of the studies reported that more problems were seen in gifted children in the social and emotional area ( 9 , 66 ); other studies emphasize that the level of social, emotional and behavioral problems of gifted children is similar to their peers with normal intelligence and ability level ( 35 , 67 , 68 ). In our study, apart from inattention and hyperactivity scores, there was not find any increased complaint in gifted children in other difficulty areas of SDQ. Also, when compared to group II, there was not determined any difference in social behaviour area as a strength area.

In terms of peer relationships, popularity can become a decisive factor in peer relationships of gifted children. Studies related to this subject have reported that gifted children are popular among their peers and no peer-related problems are identified ( 58 , 59 ). However, it is also reported in the literature that the qualities which enable gifted children to succeed and get ahead of others, can also lead them to be excluded from peer groups and social environments, and that these qualities may lead them to be alone in peer group ( 61 ).When the literature is reviewed on the difference between genders in peer relationships and social behaviour subtests of SDQ, it is generally seen that girls are better in peer relationships than boys. When the psychometric properties of strenghts and difficulties questionnaire are examined, it is reported that girls are more social than boys and although boys’ problems are not statistically significant, their problems in peer relationships are more prominent than girls ( 69 ). In this respect, also in our study, independently from the groups, findings that difficulties in peer relationships in girls are less than those in boys and strengths in social skills are better than those in boys, suggest that this is due to psychometric properties of SDQ.

In the quality of life scale, gifted children’s having fewer points than group II at a level close to statistically significant level in fields in which they assessed themselves, suggests that being gifted affects the quality of life negatively. Dauber and Benbow (1990) report that gifted children grow away from the normal population as their intelligence increases ( 70 ). In addition, they emphasize that their existing superiorities estrange them from the environment. Results obtained from this study support results of Dauber and Benbow (1990).

In the FAD which was given to families of groups in order to evaluate whether families fulfill their functions or not, and in order to reveal problem areas, in affective involvement subtest, group I scored statistically significant fewer points, but this difference was not observed among the genders. This finding points that family members of gifted children in group II show a sufficient level of interest, care, and love for each other. No significant difference was found with FAD in other subtests. This shows the similarity of families of group I and group II, and supports equivalence of families. The conclusion of our study is parallel to conclusions of Gubbins’ study (2002) which shows gifted childrens are encouraged and supported by their parents consistently.

In this study, due to the fact that problems emerging in social, emotional, behavioural areas and the decline in quality of life in gifted children carry a risk of arising from a psychological disorder, the exclusion of any mental disorder by the K-SADS-PL-T; group I and group II’s matching by sociocultural and sociodemographic aspects; having a heterogeneous sampling which represents gifted children in terms of various ability fields, are strengths of the study.

Small sample group and the inability of the K-SADS-PL-T to determine a diagnosis such as learning disorder which may affect school functioning, are limited aspects of the study.

All findings in this study suggest that gifted children are at risk for mental health. In terms of gifted children’s being at this risk, educational interventions and assists are needed psychologically and also those are needed so that they achieve their potential. Because of the risks which gifted children have in terms of their mental health, there is a need for longer surveillance studies which can be evaluated in more dimensions and have greater sample.

Ethics Committee Approval: Ethical approval was obtained from the Ethics Committee of Dokuz Eylül University (Decision No. 2012 / 01-23 dated 05.01.2012)

Informed Consent: Written informed consent form was obtained from all patients.

Peer-review: Externally peer-reviewed.

Author Contributions: Concept - FE, BB; Design - FE, BB; Supervision - BB, SA; Resource - FE, AÖÇ, SA; Materials - FE, BB; Data Collection and/ or Processing - FE, AÖÇ; Analysis and/or Interpretation - FE, BB, SA; Literature Search - FE, AÖÇ, SA, BB; Writing - FE, SA, BB; Critical Reviews - SA, BB.

Conflict of Interest: No conflict of interest was declared by the authors.

Financial Disclosure: The authors declared that this study has received no financial support.

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Dallas Cowboys owner Jerry Jones arrives at federal court Tuesday, June 18, 2024, in Los Angeles. Jones is testifying in a class-action lawsuit filed by "Sunday Ticket" subscribers claiming the NFL broke antitrust laws. (AP Photo/Damian Dovarganes)

LOS ANGELES – The federal judge presiding over the class-action lawsuit filed by “Sunday Ticket” subscribers against the NFL voiced frustrations Tuesday with the way the plaintiffs' attorneys have handled their side of the case.

Before Dallas Cowboys owner Jerry Jones took the stand Tuesday for a second day of testimony, U.S. District Judge Philip Gutierrez said the premise of the case was simple — who wouldn't see the frustration of a Seattle Seahawks fan living in Los Angeles not being able to see their favorite team without buying a subscription for all the Sunday afternoon out-of-market games.

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“The way you have tried this case is far from simple,” Gutierrez told attorneys representing the subscribers. “This case has turned into 25 hours of depositions and gobbledygook. ... This case has gone in a direction it shouldn't have gone."

The class-action, which covers 2.4 million residential subscribers and 48,000 businesses who paid for the package of out-of-market games from the 2011 through 2022 seasons, claims the league broke antitrust laws by selling its package of Sunday games aired on CBS and Fox at an inflated price. The subscribers also say the league restricted competition by offering “Sunday Ticket” only on a satellite provider.

The NFL maintains it has the right to sell “Sunday Ticket” under its antitrust exemption for broadcasting. The plaintiffs say that only covers over-the-air broadcasts and not pay TV.

If the NFL is found liable, a jury could award $7 billion in damages, but that number could balloon to $21 billion because antitrust cases can triple damages.

Tuesday was not the first time Gutierrez has expressed frustration with the plaintiffs' side. On Monday, he admonished their attorneys for repeatedly describing past testimony, which he considered a waste of time.

Before Jones resumed his testimony, Gutierrez expressed doubts about plaintiffs' attorneys citing Jerry Jones' lawsuit against the NFL in 1995, which challenged the league's licensing and sponsorship procedures.

“I don't know what you are doing, but marketing is not media,” Gutierrez said.

Later in his testimony, Jones said he sued the NFL because the league sued him. Both sides eventually settled out of court.

Jones' filing against the NFL in 1994 said he supported the league's model for negotiating television contracts and the revenue-sharing agreements in place.

When asked Tuesday if teams should be able to sell their out-of-market television rights, Jones said no because “it would undermine the free TV model we have now.”

Retired CBS Sports chairman Sean McManus also testified, reiterating during his testimony that he was a not fan of “Sunday Ticket” or the NFL's Red Zone channel because he believes it infringes on the exclusivity CBS has in local markets.

CBS and Fox both requested in negotiations that “Sunday Ticket” be sold as a premium package. DirecTV, and not the NFL, set the prices during the class-action period.

The league has language in television contracts with CBS and Fox that the “resale packages (Sunday Ticket) are to be marketed as premium products for avid league fans that satisfy complementary demand to the offering of in-market games.”

There is additional language that prohibits the selling of individual games on a pay-per-view basis.

The NFL received a rights fee from DirecTV for the package from 1994 through 2022. Google's YouTube TV acquired “Sunday Ticket” rights for seven seasons, beginning last year.

Jamie Dyckes, a DirecTV marketing official, said during a deposition that MLB, the NBA and the NHL had a suggested retail price for their out-of-market packages and that there was revenue sharing between the leagues and the carriers, since their packages were distributed on multiple platforms.

Testimony will continue Thursday, with closing statements scheduled early next week. Gutierrez said he would consider invoking a rule where the court can find that a jury does not have sufficient evidence to rule for a party in a case.

“I'm struggling with the plaintiffs' case,” he said.

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Open Access

Peer-reviewed

Research Article

Epidemiology and multiple colonization of gastrointestinal pathogens in rural Tanzanian children with and without diarrhea: A case-control study

Roles Formal analysis, Writing – original draft, Writing – review & editing

* E-mail: [email protected]

Affiliation One Health Bacteriology Group, Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany

Roles Formal analysis, Writing – review & editing

Affiliation Department of Infectious Disease Epidemiology, Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany

Roles Data curation, Writing – review & editing

Affiliation National Institute for Medical Research, Tanga Centre, Tanga, Tanzania

Roles Data curation

Roles Conceptualization, Investigation, Writing – review & editing

Roles Investigation, Writing – review & editing

Affiliation Department of Animal Health and Zoonoses, Central Institute of the Bundeswehr Medical Service, Kiel, Germany

Roles Conceptualization, Writing – review & editing

Affiliations Department of Infectious Disease Epidemiology, Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany, University Medical Centre Hamburg-Eppendorf (UKE), Tropical Medicine, Hamburg, Germany, German Centre for Infection Research (DZIF), Hamburg-Lübeck-Borstel-Riems, Germany

Roles Writing – review & editing

Roles Investigation

Affiliation Department of Microbiology and Hospital Hygiene, Bundeswehr Central Hospital, Koblenz, Germany

Roles Methodology

Roles Methodology, Writing – review & editing

Affiliations Department of Infectious Disease Epidemiology, Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany, German Centre for Infection Research (DZIF), Hamburg-Lübeck-Borstel-Riems, Germany, Institute of Medical Biostatistics, Epidemiology and Informatics, University Medical Centre of the Johannes Gutenberg University Mainz, Mainz, Germany

Roles Conceptualization, Writing – original draft

Affiliations Department of Microbiology and Hospital Hygiene, Bundeswehr Hospital, Hamburg, Germany, Department of Medical Microbiology, Virology and Hygiene, University Medicine, Rostock, Germany

•  [ ... ],

Roles Conceptualization, Writing – original draft, Writing – review & editing

• [ view all ]
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• Daniel Haile Chercos, 
• Solomon T. Wafula, 
• John P. A. Lusingu, 
• Daniel T. R. Minja, 
• Samwel Gesase, 
• Joyce R. Mbwana, 
• Ulrich Schotte, 
• Jürgen May, 
• Lea Mardeis, 

• Published: June 18, 2024
• https://doi.org/10.1371/journal.pone.0305469
• Reader Comments

Diarrheal diseases are important causes of morbidity and mortality, worldwide. The occurrence of multiple pathogens in stool samples of symptomatic and asymptomatic individuals in resource-limited countries have been repeatedly described. In this study, we assessed the differentiated effects of combined pathogen detections on recorded symptoms. A case-control study was conducted among 620 under-five-year-old children in rural northeastern Tanzania with emphasis of multiple detection. The median age of children was 11 months (IQR = 7, 20), and 52.1% were male. Cases (50.2%, n = 157) were less likely than controls (64.5%, n = 198) to have multiple colonization with gastrointestinal tract (GIT) pathogens. The children’s age was positively associated with the likelihood of harboring multiple GIT pathogens [OR, 1.02, 95% CI = 1.01, 1.04]. Shigella spp./enteroinvasive Escherichia coli (EIEC) [OR = 2.80, 95% CI 1.62, 4.83] and norovirus [OR = 2.04, 95% CI 1.23, 3.39] were more common in cases and were strongly associated with diarrhea, while enteroaggregative E . coli (EAEC) [OR = 0.23, 95%CI 0.17–0.33] were more common in controls. Diarrheal diseases in under-five children from rural Tanzania are likely to be due to infections with Shigella spp./EIEC, and norovirus with strongly age-dependent associations.

Citation: Chercos DH, Wafula ST, Lusingu JPA, Minja DTR, Gesase S, Mbwana JR, et al. (2024) Epidemiology and multiple colonization of gastrointestinal pathogens in rural Tanzanian children with and without diarrhea: A case-control study. PLoS ONE 19(6): e0305469. https://doi.org/10.1371/journal.pone.0305469

Editor: António Machado, Universidad San Francisco de Quito, ECUADOR

Received: January 3, 2024; Accepted: May 30, 2024; Published: June 18, 2024

Copyright: © 2024 Chercos et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the manuscript and its Supporting Information files.

Funding: This research was funded by the German Research Foundation as part of the SASSA Project DFG; project number 380545990) as well as by institutional funds of the Bernhard Nocht Institute for Tropical Medicine.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Diarrheal disease, particularly in children below the age of five, is among the leading causes of childhood mortality in resource-limited countries. In the year 2019 and thus before the SARS-CoV-2-pandemic-associated changes, approximately 1.6 million deaths were reported from diarrheal infections, mainly occurring in Africa and South-East Asia [ 1 ]. With few exemptions, however, microbial causes of infectious gastroenteritis are facultatively pathogenic, meaning that they can occur both as causative agents and as merely colonizing commensals in the enteric tract of human individuals. This is particularly true for tropical high endemicity, making assignments of etiological relevance to diagnostically detected microorganisms in stool samples challenging as summarized elsewhere [ 2 ]. However, reliable etiological assignments would be highly desirable to adequately consult the clinical management of patients with infectious gastroenteritis.

Large multicentric studies including the MAL-ED (malnutrition and enteric disease) study and others conducted in resource-limited countries have shown not only that the colonization with multiple gastroenteric pathogens is common in patients with diarrhea, but also demonstrated that multiple or individual pathogen species can be carried asymptomatically [ 1 , 3 , 4 ]. Asymptomatic infections are frequently overlooked, resulting in undetected but continued mild symptoms or colonization following a development of partial immunity. Recent studies among Tanzanian children with diarrhea not only showed that multiple detections of gastroenteric pathogens are frequent, but also that pathogens affect each other reciprocally regarding their etiological relevance in human disease [ 3 , 4 ]. Furthermore, there seems to be an age-dependent increased likelihood of pathogen-specific infections in children below the age of five years [ 5 ]. In patients with infectious gastroenteritis, a broad spectrum of possible causative pathogens has to be considered including rare parasites as well as antimicrobial-resistant bacteria such as Salmonella enterica and others [ 6 , 7 ]. Altogether, bacterial and protozoan pathogens quantitatively dominate in children with diarrhea in Tanzania.For instance among viral causative agents of gastroenteritis, rotavirus and norovirus have been most frequently implicated [ 8 , 9 ]. Nevertheless, their role in causing symptoms and hence disease is often unclear, especially in patients from which multiple pathogens have been isolated. To identify associations between multiple pathogens and the occurrence of diarrhea, a control group without diarrhea would be essential.

The etiology of diarrhea in some regions of sub-Saharan Africa is still poorly understood, although crucial to guide antimicrobial treatment when indicated and to support the implementation of preventive programs.

This study aimed to assess the role of different gastrointestinal pathogens alone or in the course of multiple colonization in children with and without diarrhea attending a rural hospital in Tanzania. Further possible associations with cumulative effects of multiple infections/colonization were assessed as well as the most frequently observed pathogen combinations and gastrointestinal clinical symptoms in children aged below five years. By doing so, a new piece in the puzzle hopefully leading to a better future understanding of etiological relevance assignment to enteric microorganisms detected in tropical high-endemicity settings was provided.

Material and methods

Study design, population and sample materials.

Unmatched case-control study was carried out from September 2017 to February 2019 among under-five years-old children at Korogwe District Hospital, in rural Northeastern Tanzania. Stool samples from 632 individuals with and without gastrointestinal symptoms were screened for bacterial, protozoan and viral pathogens with a focus on multiple pathogen detection. Symptomatic children presented to the outpatient department of Korogwe District Hospital were included in the study when they had diarrhea or a history of diarrhea in the past 72 hours (cases). Asymptomatic in the sense of the study approach were those children without diarrhea or a history of diarrhea in the past 72 hours before visiting the vaccinatinion clinic (controls). Clinical data such as vomiting and presence of diarrhea, as well as epidemiological data such as age, sex, and date of the year were also collected from the study participants. Cherry pit-sized stool volumes were collected and subjected to immediate nucleic acid extraction on site as well to storage at room temperature on Whatman FTA micro cards (Sigma Aldrich, Ulm, Germany, product number WHAWB120210) and on flocked swabs with an included proprietary drying system (GenoTube Livestock Swabs, Thermo Fisher Scientific Prionics AG, Schlieren, Switzerland) for later additional nucleic acid extraction after sample shipment to Germany for a methodical comparison reported elsewhere [ 10 ].

Nucleic acid extraction

All stool samples were subjected to nucleic acid extraction by applying the Invisorb Spin Universal Kit (INVITEK Molecular, Berlin, Germany) for RNA and DNA according to the manufacturer’s instructions in the Korogwe GCLP-compliant laboratory, Tanzania. Extracts were then stored at -80°C and shipped on dry ice to the Bernhard Nocht Institute for Tropical Medicine (BNITM) in Hamburg, Germany after the Material Transfer Agreement was approved by the Tanzania National Ethics Committee. From a subpopulation of 466 patients with and without diarrhea, additional nucleic acid extraction was performed from Whatman FTA micro cards (Sigma Aldrich, Ulm, Germany, product number WHAWB120210) and from flocked swabs with an included proprietary drying system (GenoTube Livestock Swabs, Thermo Fisher Scientific Prionics AG, Schlieren, Switzerland) in Kronshagen, Germany. Fragments from the Whatman papers and swabs were incubated at 56°C in 550 μL buffer ATL (Qiagen, Hilden, Germany) and centrifuged for 15 minutes at 1000 rev min -1 (revolutions per minute) [ 11 , 12 ]. Nucleic acid extraction was then performed automatically by applying a QIAsymphony automate (Qiagen; protocol “Complex_200_default_IC”, QIAsymphony DSP Virus/Pathogen Mini-Kit) as described by the manufacturer including the addition of carrier RNA. All extractions were stored at −80°C until further processing. In case of Polymerase Chain Reaction (PCR) assessments from multiple extractions from the same sample, the sample was considered as positive in case of at least one positive PCR signal from any extraction.

Real-time PCRs

The samples were subjected to PCR-based screening in Hamburg and Kronshagen including in-house real-time multiplex PCR targeting enteropathogenic Escherichia coli (EPEC) ( EAF , eae ), enterotoxigenic E . coli (ETEC) ( LT /ST ), and enteroaggregative E . coli (EAEC) ( aggR ) [ 13 ], entero-invasive Salmonella spp. ( ttrR ), Shigella spp./enteroinvasive E . coli (EIEC) ( ipaH ), Campylobacter jejuni (gyrA) , and Yersinia spp. ( ail ) [ 14 ], the enteropathogenic protozoa Entamoeba histolytica (SSU-rRNA) , Giardia duodenalis (SSU-rRNA) , Cyclospora spp. ( SSU-rRNA ), and Cryptosporidium parvum (138-bp fragment inside the C. parvum-specific 452-bp fragment), the enteric helminths Ancylostoma spp. ( ITS-2 ), Ascaris lumbricoides (ITS-1) , Enterobius vermicularis (ITS-1) , Hymenolepis nana (ITS-1) , Necator americanus (ITS-2) , Schistosoma spp. ( ITS-2) , Strongyloides stercoralis (18S-rRNA) , Taenia saginata (ITS-1) , Taenia solium (ITS-1) , Trichuris trichiura (18S-rRNA) [ 15 ], and hepatitis E-virus [ 16 ], respectively, as well as one commercial real-time PCR targeting norovirus and hepatitis A virus (SureFast® Norovirus/Hepatitis A 3plex assay, r-biopharm, Darmstadt, Germany) according to the manufacturer’s instructions. The in-house real-time PCRs and their performance characteristics are described in detail elsewhere [ 13 – 17 ]. Both qualitative PCR results and cycle threshold (Ct) values were recorded.

Statistical methods

Data were collected and managed using REDCap version 9.8.2 (Vanderbilt University, Nashville, USA) before being analyzed using R version 4.2.1 and RStudio version 2022.12.0+353 (Posit Software, Boston, Massachusetts). Categorical data were described as frequencies and percentages, and numerical data were summarized by calculating the median and interquartile range. The association between multiple colonization of gastrointestinal tract (GIT) pathogens and case-control status were estimated using ordinal logistic regression which is adjusted for sex, age and season. Binary logistic regression with interaction terms adjusted for sex, age, and season was also constructed to determine if there was a difference in the distribution of the most commonly reported combinations of gastrointestinal pathogens between cases and controls. Based on the p-value < 0.05 criterion, variables with significant associations were identified, and Benjamini and Hochberg correction was applied when multiple testing was conducted. Odds ratios (OR) with 95% confidence intervals (CI) were calculated to describe effect sizes.

Demographic characteristics of study participants

Of the 632 children enrolled, complete information were available for 620 children (313 cases and 307 controls). Approximately half (52%, n = 324) were male and the median age was 11 months (IQR = 7, 20). Among recorded symptoms, vomiting was more prevalent in cases (38%) than in controls (11%) (q<0.001) ( Table 1 ).

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https://doi.org/10.1371/journal.pone.0305469.t001

Common gastrointestinal pathogens isolated from rural Northeastern Tanzanian children

Among the 23 gastrointestinal pathogens considered in this study, G . duodenalis , enteropathogenic E . coli (EPEC), and enteroaggregative E . coli (EAEC) were the most frequently observed. Despite their low proportions, Shigella spp./enteroinvasive E . coli (EIEC), norovirus, and C . jejuni were more common in cases than in controls. EAEC, EPEC, and G . duodenalis were observed more often in controls than in cases ( Fig 1 ).

https://doi.org/10.1371/journal.pone.0305469.g001

Distribution of GIT pathogens in different age groups

Enteropathogenic E . coli and EAEC were the most frequent GIT pathogens found in rural Northeastern Tanzanian children with and without diarrhea under the age of two. Norovirus was more frequent in children under the age of two in the case group than in children of comparable age in the control group. C . jejuni was more frequent in children with diarrhea under the age of two, compared to children of similar age in the control group. Shigella spp . / EIEC were more frequent in children above one year of age in cases than in children of similar age in the control group. The graph below ( Fig 2 ) suggests that the frequency of any GIT pathogen decreases as children get older, with the exceptions of Shigella spp. / EIEC and G . duodenalis .

https://doi.org/10.1371/journal.pone.0305469.g002

Multiple GIT pathogens among rural Northeastern Tanzanian children

More than one GIT pathogen was isolated in 50.2% (n/N = 157/313) of cases and 64.5% (n/N = 198/307) of controls. On the other hand, more cases (33.5%, n/N = 105/313) than controls (25.4%, n/N = 78/307) had only a single GIT pathogen. More children tested negative for GIT pathogens (16.3%, n/N = 51/313) than the controls (10.1%, n/N = 31/307). Children with multiple colonization had up to five detected GIT pathogens. There were more controls than cases with two GIT pathogens (34.5%, n/N = 106/307 vs 29.1%, n/N = 91/313) and three GIT pathogens (23.4%, n/N = 72/307 vs 14.1%, n/N = 44/313). However, the proportion of children with four (5.55% n/N = 17/307 vs 5.54% n/N = 17/313) and five (0.98% n/N = 3/307 vs 1.6% n/N = 5/313) GIT pathogens in both groups was the same.

Common GIT pathogen co-infection among rural Northeastern Tanzanian children

The most common GIT combination found in rural northeastern Tanzanian children’s stool samples were EAEC and EPEC, which was more frequent in controls than in cases. In addition, the combined prevalence of EAEC, G . duodenalis , and EPEC in controls was more frequent than in cases ( Fig 3 ). In contrast, the combination of Shigella spp./EIEC and EPEC was more frequent in cases than in controls.

https://doi.org/10.1371/journal.pone.0305469.g003

Associations of GIT colonization in rural Northeastern Tanzanian children

There was a difference in the odds of having multiple GIT pathogenic organisms when comparing cases to controls. Adjusted regression results revealed that cases were 44% less likely than controls to have multiple GIT pathogenic organisms isolated in their stool samples [OR = 0.56, 95% CI = 0.41, 0.76]. Similarly, there appears to be a minor but statistically significant association between children’s age and the odds of harboring multiple GIT pathogens. The odds of harboring multiple GIT pathogens increased by 2% on average for every additional 1 month of child age [OR, 1.02, 95%CI = 1.01, 1.04]. In contrast, there was no significant differences in odds of multiple colonizations between different gender (of the child) and season of the year ( Table 2 ).

https://doi.org/10.1371/journal.pone.0305469.t002

Association between GIT pathogens and diarrhea in rural Northeastern Tanzanian children

According to logistic regression analysis adjusted for age, gender and season, cases were 2.80 times as likely than controls to be associated with Shigella spp./EIEC infection [OR = 2.80, 95% CI 1.62, 4.83]. In addition, norovirus was twice as likely to be detected among cases compared to controls [OR = 2.04, 95% CI 1.23, 3.39]. Cases also had lower odds for EAEC detection than controls [OR = 0.23, 95%CI 0.17–0.33]. We observed a marginally significant association between C . jejuni infection and diarrhea (case group) [OR = 1.77, 95%CI 0.99–3.16] ( Table 3 ).

https://doi.org/10.1371/journal.pone.0305469.t003

The effect of GIT pathogens and their combinations on the presence of diarrhea

According to a logistic regression analysis that accounted for age, sex, and season, the odds of finding EAEC in cases were significantly lower compared to controls. Furthermore, the odds of identifying Shigella spp . /EIEC in cases were significantly greater than in controls. Furthermore, while there is no statistically significant difference between cases and controls, the presence of EPEC appears to influence the odds of identifying norovirus, EAEC, Shigella spp . /EIEC , and Giardia duodenalis in cases or controls ( Fig 4 ).

https://doi.org/10.1371/journal.pone.0305469.g004

The study sought to understand the epidemiology of gastrointestinal pathogens among under five children with and without diarrhea in rural Tanzania. The groups were comparable regarding age and gender, more vomiting in the diarrhea group compared to the control group further confirmed clinically apparent gastroenteritis within the diarrheal group. Our findings confirmed a high prevalence of bacterial and protozoan intestinal infections previously reported in Tanzanians [ 18 , 19 ]. Among the identified enteropathogenic protozoa, G . duodenalis and–to a lesser extent– C . parvum were most frequent, which is in line with previous findings [ 20 , 21 ]. E . histolytica did not play a relevant role in contrast to what was described before [ 22 ]. This observed discrepancy as compared to other studies [ 22 ] that were done elsewhere in Tanzania suggests geographic disparities in E . histolytica prevalence in Tanzania. Diagnostic accuracy of the screening PCR applied (mean and 95% confidence interval) of 97.7% (94.0%, 99.1%) sensitivity and 99.4% (98.7%, 99.7%) as reported elsewhere [ 23 ] makes it unlikely that relevant proportions of E . histolytica -containing samples were overlooked in the present study. Focusing on detected enteropathogenic bacteria, there was a great majority of diarrheagenic E . coli and Shigella spp. followed by C . jejuni and Salmonella spp. This finding is in line with previous reports in Tanzanian context [ 18 , 19 , 24 ], although two-digit percentages of Salmonella spp.-infections like reported elsewhere [ 24 ] could not be confirmed in our study. The quantitatively relevant detection of norovirus in our study cohort matches previous results [ 9 ]. Quantitatively relevant helminthic infections could only be shown for S . stercoralis , for which regional differences were previously demonstrated in another study conducted in Northern Tanzania [ 25 ].

Multiple pathogen detections were not primarily associated with increased risk of clinical diarrhea but were more frequently observed in colonized individuals than in patients with diarrhea. Moreover, multiple colonization was associated with age, while–in contrast—age-dependent pathogenicity was only inconsistently recorded. Although the numbers of older children were low, these findings at least pointed into the direction of habituation phenomena as recently described for Tanzania [ 26 ], potentially resulting in a semi-immunity-like state without clinically apparent diarrhea. This likely immunity-associated habituation effect is supported by the finding that proportions of most pathogen detections dramatically declined with increasing age in spite of an obvious high colonization pressure. Interestingly, Shigella spp./EIEC detections in diarrheagenic children seemed to be an exemption from this rule.

In addition, associations of pathogen detection with diarrhea could be confirmed for a minority of pathogens only, while most pathogens were almost evenly distributed among both study groups. Shigella spp. or enteroinvasive E . coli , not discriminable with the applied PCR assay, as well norovirus detections were found to be associated with diarrhea, while there was an association of enteroaggregative E . coli and children without gastroenteric symptoms. Both observations match previous findings from other settings [ 26 , 27 ]. In a previous study in children in rural Ghana [ 28 ], Shigella spp./EIEC and norovirus were found to be more frequent in children with diarrhea compared to children without gastroenteric symptoms. In the same study, Cryptosporidium spp. and rotavirus were associated with diarrhea, the latter not examined and frequencies of Cryptosporidium spp. being low in this study, which makes it difficult to draw any conclusion. Focusing on the here-observed association of enteroaggregative E . coli and healthy individuals [ 29 ], a recent study on travelers’ diarrhea indicated the abundance of this microorganism in stool samples in general, considerably challenging its etiological relevance.

Of note, no conclusive information on the effect of pathogen combinations on etiological relevance could be obtained from this study. However, this may at least partly be due to the low sample size and so, future studies with a larger sample size would be required to draw definite conclusion from this.

The study has a number of limitations. First, the sample size is still fairly low, which makes any conclusions on rarely occurring pathogens difficult. Second, the applied real-time PCR assays comprise only a subset of microorganisms possibly associated with diarrhea in the study participants. Other pathogens such as rotavirus, which is strongly associated with diarrhea, were not screened. Accordingly, a lacking pathogen diagnosis does not necessarily mean the absence of an etiologically relevant microorganism not included in the real-time PCR panel. Finally, we abstained from including semi-quantification based on the cycle threshold values of real-time PCR in the assessments, which was decided for the following reasons. One reason is that Ct-value-based stratification would have made the compared populations too small and so, statistically meaningful results would have been unlikely. Also, Ct-value comparisons in a previous technical assessment with datasets from the same study population [ 10 ] had shown that Ct-values of individuals with and without diarrhea were virtually indistinguishable. Although complex pathogen interactions with microbial loads as a relevant influence cannot be excluded based on this previous experience, we feel justified to assume that semi-quantification is no reliable parameter by itself to assign etiological relevance to a detected microbial pathogen in the assessed population. For the assessment of complex interactions, however, future studies including higher sample sizes will be required.

Conclusions

In the presented study on the epidemiology of diarrhea in rural Tanzanian children, multiple PCR detections of pathogens were more likely to occur in children without diarrhea than in those with diarrhea. Multiple pathogens detection was also associated with the children’s age. Diarrhea was mainly associated with Shigella spp./EIEC either alone or in combination with other pathogens like, e.g., norovirus, while, in contrast, enteroaggregative E . coli were more frequently detected alone or in defined combinations with other enteropathogens in subjects without diarrhea. The study results underline the difficulties of assigning etiological relevance to pathogen detections in stool samples in high endemic settings. Further research is desired to support the diagnostic discrimination of etiologically relevant pathogen detections from the identification of harmlessly colonizing bystanders not requiring therapeutic intervention under such circumstances.

Supporting information

S1 data. anonymized raw data used for this manuscript..

https://doi.org/10.1371/journal.pone.0305469.s001

Acknowledgments

We are grateful to all the children who participated in this study and to their parents or guardians who consented to take part. Also thank you to the personnel at the Korogwe District Hospital. Without their efforts this research study would not have been possible.

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