Loading...
English Term 4
Quiz by Cheryl Anne Villapando
Customize this quiz to suit your class
Instantly translate to 100+ languages
Tag the questions with any skills you have. Your dashboard will track each student's mastery of each skill.
Give this quiz to my class
Words with Diphthongs: ou, ow, oi and oy
Direction: Choose the word with the diphthongs (ou, ow, oi or oy) in the sentence.
Destroy the breeding places of mosquitos.
Words with Diphthongs: ou, ow, oi and oy
Direction: Choose the word with the diphthongs (ou, ow, oi or oy) in the sentence.
The ball bounces non-stop.
Words with Diphthongs: ou, ow, oi and oy
Direction: Choose the word with the diphthongs (ou, ow, oi or oy) in the sentence.
Destroy the breeding places of mosquitos.
Words with Diphthongs: ou, ow, oi and oy
Direction: Choose the word with the diphthongs (ou, ow, oi or oy) in the sentence.
The ball bounces non-stop.
Words with Diphthongs: ou, ow, oi and oy
Direction: Choose the word with the diphthongs (ou, ow, oi or oy) in the sentence.
She wants to wear the purple gown.
Words with Diphthongs: ou, ow, oi and oy
Direction: Choose the word with the diphthongs (ou, ow, oi or oy) in the sentence.
I am loyal to my friends and family.
Words with Diphthongs: ou, ow, oi and oy
Direction: Choose the word with the diphthongs (ou, ow, oi or oy) in the sentence.
What is the point of all this?
Words with Diphthongs: ou, ow, oi and oy
Direction: Choose the word with the diphthongs (ou, ow, oi or oy) in the sentence.
The Banawe Rice terraces is known all over the world.
Choose the best answer from the questions in the story, "A Boy Against Odds."
What work did Fredo's father do for a living?
Choose the best answer from the questions in the story, "A Boy Against Odds."
When Fredo graduated, what was the highest honor he received?
Choose the best answer from the questions in the story, "A Boy Against Odds."
Where did Fredo and his family lived?
Choose the best answer from the questions in the story, "A Boy Against Odds."
Do you think Fredo is hardworking and persevering? Why?
Choose the best answer from the questions in the story, "A Boy Against Odds."
How did Fredo go to the village school?
Choose the best answer from the questions in the story, "A Boy Against Odds."
During weekends, what does Fredo do?
Making Inferences on Character traits:
Direction: Choose the character trait expressed in the situation.
When the children returned to their rooms after the fire drill, Marcus saw a purse on the stairway. He picked it up and brought it to the Principal's office. Marcus is ____________.
Making Inferences on Character traits:
Direction: Choose the character trait expressed in the situation.
Fredo trekked three miles everyday from his home to his village. Fredo is _____________.
Making Inferences on Character traits:
Direction: Choose the character trait expressed in the situation.
Von always comes too early. He does his assigned classroom task for the day right away. Von is _________.
Making Inferences on Character traits:
Direction: Choose the character trait expressed in the situation.
Carla meets the school principal and greets her, "Good morning, Mrs. Suarez!" Carla is ___________.
Making Inferences on Character traits:
Direction: Choose the character trait expressed in the situation.
Please accept my apology. I didn't mean what I said.
Making Inferences on Character traits:
Direction: Choose the character trait expressed in the situation.
Ate Yuki practiced hard for the singing contest. She slept early in the evening and avoided food and drinks that might cause discomfort to her throat. She told herself, "I will do my best, win or lose." Ate Yuki is quite ______________.
Recognizing Descriptive Adjectives
Direction: Choose the descriptive adjective in the sentence.
Who is the fairest of them all?
Recognizing Descriptive Adjectives
Direction: Arrange the determiners and adjectives in the sentence.
The show's episode is interesting
Recognizing Descriptive Adjectives
Direction: Choose the descriptive adjective in the sentence.
You were amazing during the competition.
Recognizing Descriptive Adjectives
Direction: Choose the descriptive adjective in the sentence.
I have great games in my IPad.
Recognizing Descriptive Adjectives
Direction: Choose the descriptive adjective in the sentence.
The plane flew over a wide valley.
Recognizing Descriptive Adjectives
Direction: Choose the descriptive adjective in the sentence.
Grizz is a thoughtful dog
Recognizing Descriptive Adjectives
Direction: Choose the descriptive adjective in the sentence.
The weather was calm when we arrived in Boracay.
Recognizing Descriptive Adjectives
Direction: Choose the descriptive adjective in the sentence.
Rapunzel has long, beautiful hair.
Recognizing Descriptive Adjectives
Direction: Choose the descriptive adjective in the sentence.
We went to a grassy field last weekend.
Recognizing Descriptive Adjectives
Direction: Choose the descriptive adjective in the sentence.
Our kitchen sink is full of dirty dishes
Using Degrees of Comparison
Direction: Choose the best answer.
Spiderman is the _______ superhero of all time!
Using Degrees of Comparison
Direction: Choose the best answer.
Tenzing Norgay was a _________ climber.
Using Degrees of Comparison
Direction: Choose the best answer.
Grizz is _________ than Snowball.
Using Degrees of Comparison
Direction: Choose the best answer.
Fortnite is the ________ PS game I have ever played!
Using Degrees of Comparison
Direction: Choose the best answer.
Ayee is the _________ girl in our class
Using Degrees of Comparison
Direction: Choose the best answer.
Mommy is __________ to her family.
Using Degrees of Comparison
Direction: Choose the best answer.
Daddy is _________ than Mommy.
Using Degrees of Comparison
Direction: Choose the best answer.
Zach is _______ at drawing stick man.
Using Degrees of Comparison
Direction: Choose the best answer.
Snowball is ________ than Icy.
Using Degrees of Comparison
Direction: Choose the best answer.
The series Amazing World of Gumball is ________ than the Beyblade.
Using Degrees of Comparison
Direction: Choose the best answer.
Our house is _________.
Using Degrees of Comparison
Direction: Choose the best answer.
Binangonan Province is ___________ than Angono.
English Term 4 QuizEnglish Term 4 Quiz 2English Term 4 Quiz 1QUIZ 2 TERM 1 English 4 Naturalism- A term often used as a synonym for realism; also a view of experience that is generally characterized as bleak and pessimistic; characters within this type of work often struggle unsuccessfully to exercise free will. Non Sequitur- A statement or idea that fails to follow logically from the one before Novel of Manners- A novel focusing on and describing the social customs and habits of a particular social group Novella- A work of fiction of roughly 20,000 to 50,000 words-longer than a short story, but shorter than a novel Ode -A lyric poem usually marked by serious, respectful, and exalted feelings toward the subject Old English- The Anglo-Saxon language spoken in what is now English from approximately 450 to 1150 A.D. Omniscient Narrator- A narrator with an unlimited awareness, understanding, and insight of characters, setting, background, and all other elements of the story Ottava Rima- An eight-line rhyming stanza of a poem Myth- An imaginary story that has become an accepted a part of the cultural or religious tradition of a group or society; often used to explain natural phenomena. Narrative - A form of verse or prose that tells a storyCan you make a multiple choice of test questions regarding this information given which is Curriculum from Different Points of View There are many definitions of curriculum. Because of this, the concept of curriculum is sometimes characterized as fragmentary, elusive and confusing. However, the numerous definitions indicate dynamism that connotes diverse interpretations of what curriculum is all about. The definitions are influenced by models of thought, pedagogies, political as well as cultural experiences. Let us study some of these definitions. 1. Traditional Points of View of Curriculum In early years of the 20th century, the traditional concepts held of the “curriculum is that it is a body of subjects or subject matter prepaid by the teachers for the student’s to learn”. It was synonymous to the “course of study” and “syllabus” Robert M. Hutchins views curriculum as “permanent studies” where the rules of grammar, reading, rhetoric and logic and mathematics for basic education are emphasized. Basic education should emphasize the 3 Rs and college education should be grounded on liberal education. On the other, Arthur Bestor as an essentialist, believes that the mission of the school should be intellectual training, hence curriculum should focus on the fundamental intellectual disciplines of grammar, literature and writing. It should also include mathematics, science, history and foreign language. The definition leads us to the view of Joseph Schwab that discipline is the sole source of curriculum. Thus in our education system, curriculum is divided into chunks of knowledge we call subject areas in basic education such as English, Mathematics, Science, Social Studies and others. In college, discipline may include humanities, sciences, language and many more. To Phoenix, curriculum should consist entirely of knowledge which comes from various disciplines. Academic discipline became the view of what curriculum is after the cold war and the race to space. Joseph Schwab, a leading curriculum theorist coined the term discipline as a ruling doctrine for curriculum development. Curriculum should consist only of knowledge which comes from disciplines which is the sole source. Thus curriculum can be viewed as a field of study. It is made up of its foundations (philosophical, historical, psychological and social foundations); domains of knowledge as well as its research theories and principles. Curriculum is taken as scholarly and theoretical. It is concerned with broad historical, philosophical and social issues and academics. Most of the traditional ideas view curriculum as written documents or a plan of action in accomplishing goals. 2. Progressive Points of View of Curriculum On the other hand, to a progressivist, a listing of school subjects, syllabi, course of study, and a list of courses or specific discipline do not make a curriculum. These can only be called curriculum if the written materials are actualized by the learner. Broadly speaking, curriculum is defined as the total learning experiences of the individual. This definition is anchored on John Dewey’s definition of experience and education. He believed that reflective thinking is a means that unifies curricular elements. Thought is not derived from action but tested by application. Caswell and Campbell viewed curriculum as “all experiences children have under the guidance of teachers”. This definition is shared by Smith, Stanley and Shores when they defined “curriculum as a sequence of potential experiences set up in the schools for the purpose of disciplining children and youth in group ways of thinking and acting”. Marsh and Willis on the other hand view curriculum as all the “experiences in the classroom which are planned and enacted by the teacher, and also learned by the students”. Points of View on Curriculum Development From the various definitions and concepts presented, it is clear that curriculum is a dynamic process. Development connotes changes which are systematic. A change for the better means any alteration, modification or improvement of existing condition. To produce positive changes, development should be purposeful, planned and progressive. This is how curriculum evolves. Let us look at the two models of curriculum development and concepts of Ralph Tyler and Hilda Taba. Ralph Tyler Model: Four Basic Principles. This is also popularly known as Tyler’s Rationale. He posited four fundamental questions or principles in examining any curriculum in schools. These four fundamental principles are as follows: 1. What educational purposes should the school seek to attain? 2. What educational experiences can be provided that are likely to attain these purposes? 3. How can these educational experiences be effectively organized? 4. How can we determine whether these purposes are being attained or not? In summary, Tyler’s Model show that in curriculum development, the following considerations should be made: (1) Purpose of the school, (2) Educational experiences related to the purposes, (3) Organization of the experiences, and (4) Evaluation of the experiences. On the other hand, Hilda Taba improved on Tyler’s Rationale by making a linear model. She believed that teachers who teach or implement the curriculum should participate in developing it. Her advocacy was commonly called the grassroots approach. She presented seven major steps to her model where teachers could have a major input. These steps are as follows: 1. Diagnosis of learner’s needs and expectations of the larger society. 2. Formulation of learning objectives. 3. Selection of learning content. 4. Organization of learning content. 5. Selection of learning experiences. 6. Organization of learning activities. 7. Determination of what to evaluate and the means of doing it. Thus as you look into curriculum models, the three interacting processes in curriculum development are planning, implementing and evaluating. Types of Curriculum Operating in Schools From the various concepts given, Allan Glatthorn(2000) describes seven types of curriculum operating in the schools. These are (1) Recommended curriculum- proposed by scholars and professional organizations. (2) Written Curriculum- appears in school, district, division or country documents. (3) Taught Curriculum- what teacher’s implement or deliver in the classrooms and schools. (4) Supported Curriculum- resources-textbooks, computers, audio- visual materials which support and help in the implementation of the curriculum. (5) Assessed Curriculum- that which is tested and evaluated. (6) Learned Curriculum- which the students actually learn and what is measured and (7) Hidden Curriculum- the unintended curriculum. 1. Recommended Curriculum- Most of the school curricula are recommended. The curriculum may come from a national agency like the Department of Education, Commission on Higher Education (CHED), Department of Science and Technology (DOST) or any professional organization who has stake in education. For example the Philippine Association for Teacher Education (PAFTE) or the Biology Teacher Association (BIOTA) may recommend a curriculum to be implemented in the elementary or secondary education. 2. Written Curriculum- This includes documents, course of study or syllabi handed down to the schools, districts, division, departments or colleges for implementation. Most of the written curricula are made by curriculum experts with participation of teachers. These were pilot-tested or tried out in sample schools or population. Example of this is the Basic Education Curriculum (BEC). Another example is the written lesson plan of each classroom teacher made up of objectives and planned activities of the teacher. 3. Taught Curriculum- The different planned activities which are put into action in the classroom compose the taught curriculum. These are varied activities that are implemented in order to arrive at the objectives or purposes of the written curriculum. These are used by the learners with the guidance of teachers. Taught curriculum varies according to the learning styles of students and the teaching styles of teachers. 4. Supported Curriculum- In order to have a successful teaching, other than the teacher, there must be materials which should support or help in the implementation of a written curriculum. These refer to the support curriculum that includes material resources such as textbooks, computers, audio-visual materials, laboratory equipment, playgrounds, zoos and other facilities. Support curriculum should enable each learner to achieve real and lifelong learning. 5. Assessed Curriculum- This refers to a tested or evaluated curriculum. At the duration and end of the teaching episodes, series of evaluations are being done by the teachers to determine the extent of teaching or to tell if the students are progressing. This refers to the assessed curriculum. Assessment tools like pencil-and-paper tests, authentic instruments like portfolio are being utilized. 6. Learned Curriculum- This refers the learning outcomes achieved by the students. Learning outcomes are indicated by the results of the tests and changes in behavior which can either be cognitive, affective or psychomotor. 7. Hidden Curriculum- This is the unintended curriculum which is not deliberately planned but may modify behavior or influenced learning outcomes. There are lots of hidden curricula that transpire in the schools. Peer influence, school environment, physical condition, teacher-learner interaction, mood of the teachers and many other factors made up the hidden curriculum.ILLINOIS PROFESSIONAL TEACHING STANDARDS (2013) Standard 1 - Teaching Diverse Students – The competent teacher understands the diverse characteristics and abilities of each student and how individuals develop and learn within the context of their social, economic, cultural, linguistic, and academic experiences. The teacher uses these experiences to create instructional opportunities that maximize student learning. Knowledge Indicators – The competent teacher: 1A) understands the spectrum of student diversity (e.g., race and ethnicity, socioeconomic status, special education, gifted, English language learners (ELL), sexual orientation, gender, gender identity) and the assets that each student brings to learning across the curriculum; 1B) understands how each student constructs knowledge, acquires skills, and develops effective and efficient critical thinking and problem-solving capabilities; 1C) understands how teaching and student learning are influenced by development (physical, social and emotional, cognitive, linguistic), past experiences, talents, prior knowledge, economic circumstances and diversity within the community; 1D) understands the impact of cognitive, emotional, physical, and sensory disabilities on learning and communication pursuant to the Individuals with Disabilities Education Improvement Act (also referred to as “IDEA”) (20 USC 1400 et seq.), its implementing regulations (34 CFR 300; 2006), Article 14 of the School Code [105 ILCS 5/Art.14] and 23 Ill. Adm. Code 226 (Special Education); 1E) understands the impact of linguistic and cultural diversity on learning and communication; 1F) understands his or her personal perspectives and biases and their effects on one’s teaching; and 1G) understands how to identify individual needs and how to locate and access technology, services, and resources to address those needs. Performance Indicators – The competent teacher: 1H) analyzes and uses student information to design instruction that meets the diverse needs of students and leads to ongoing growth and achievement; 1I) stimulates prior knowledge and links new ideas to already familiar ideas and experiences; 1J) differentiates strategies, materials, pace, levels of complexity, and language to introduce concepts and principles so that they are meaningful to students at varying levels of development and to students with diverse learning needs; 1K) facilitates a learning community in which individual differences are respected; and 1L) uses information about students’ individual experiences, families, cultures, and communities to create meaningful learning opportunities and enrich instruction for all students. Standard 2 - Content Area and Pedagogical Knowledge – The competent teacher has in-depth understanding of content area knowledge that includes central concepts, methods of inquiry, structures of the disciplines, and content area literacy. The teacher creates meaningful learning experiences for each student based upon interactions among content area and pedagogical knowledge, and evidence-based practice. Knowledge Indicators – The competent teacher: 2A) understands theories and philosophies of learning and human development as they relate to the range of students in the classroom; 2B) understands major concepts, assumptions, debates, and principles; processes of inquiry; and theories that are central to the disciplines; 2C) understands the cognitive processes associated with various kinds of learning (e.g., critical and creative thinking, problem-structuring and problem-solving, invention, memorization, and recall) 2 and ensures attention to these learning processes so that students can master content standards; 2D) understands the relationship of knowledge within the disciplines to other content areas and to life applications; 2E) understands how diverse student characteristics and abilities affect processes of inquiry and influence patterns of learning; 2F) knows how to access the tools and knowledge related to latest findings (e.g., research, practice, methodologies) and technologies in the disciplines; 2G) understands the theory behind and the process for providing support to promote learning when concepts and skills are first being introduced; and 2H) understands the relationship among language acquisition (first and second), literacy development, and acquisition of academic content and skills. Performance Indicators – The competent teacher: 2I) evaluates teaching resources and materials for appropriateness as related to curricular content and each student’s needs; 2J) uses differing viewpoints, theories, and methods of inquiry in teaching subject matter concepts; 2K) engages students in the processes of critical thinking and inquiry and addresses standards of evidence of the disciplines; 2L) demonstrates fluency in technology systems, uses technology to support instruction and enhance student learning, and designs learning experiences to develop student skills in the application of technology appropriate to the disciplines; 2M) uses a variety of explanations and multiple representations of concepts that capture key ideas to help each student develop conceptual understanding and address common misunderstandings; 2N) facilitates learning experiences that make connections to other content areas and to life experiences; 2O) designs learning experiences and utilizes assistive technology and digital tools to provide access to general curricular content to individuals with disabilities; 2P) adjusts practice to meet the needs of each student in the content areas; and 2Q) applies and adapts an array of content area literacy strategies to make all subject matter accessible to each student. Standard 3 - Planning for Differentiated Instruction – The competent teacher plans and designs instruction based on content area knowledge, diverse student characteristics, student performance data, curriculum goals, and the community context. The teacher plans for ongoing student growth and achievement. Knowledge Indicators – The competent teacher: 3A) understands the Illinois Learning Standards (23 Ill. Adm. Code 1.Appendix D), curriculum development process, content, learning theory, assessment, and student development and knows how to incorporate this knowledge in planning differentiated instruction; 3B) understands how to develop short- and long-range plans, including transition plans, consistent with curriculum goals, student diversity, and learning theory; 3C) understands cultural, linguistic, cognitive, physical, and social and emotional differences, and considers the needs of each student when planning instruction; 3D) understands when and how to adjust plans based on outcome data, as well as student needs, goals, and responses; 3E) understands the appropriate role of technology, including assistive technology, to address student needs, as well as how to incorporate contemporary tools and resources to maximize student learning; 3 3F) understands how to co-plan with other classroom teachers, parents or guardians, paraprofessionals, school specialists, and community representatives to design learning experiences; and 3G) understands how research and data guide instructional planning, delivery, and adaptation. Performance Indicators – The competent teacher: 3H) establishes high expectations for each student’s learning and behavior; 3I) creates short-term and long-term plans to achieve the expectations for student learning; 3J) uses data to plan for differentiated instruction to allow for variations in individual learning needs; 3K) incorporates experiences into instructional practices that relate to a student’s current life experiences and to future life experiences; 3L) creates approaches to learning that are interdisciplinary and that integrate multiple content areas; 3M) develops plans based on student responses and provides for different pathways based on student needs; 3N) accesses and uses a wide range of information and instructional technologies to enhance a student’s ongoing growth and achievement; 3O) when planning instruction, addresses goals and objectives contained in plans developed under Section 504 of the Rehabilitation Act of 1973 (29 USC 794), individualized education programs (IEP) (see 23 Ill. Adm. Code 226 (Special Education)) or individual family service plans (IFSP) (see 23 Ill. Adm. Code 226 and 34 CFR 300.24; 2006); 3P) works with others to adapt and modify instruction to meet individual student needs; and 3Q) develops or selects relevant instructional content, materials, resources, and strategies (e.g., project-based learning) for differentiating instruction. Standard 4 - Learning Environment – The competent teacher structures a safe and healthy learning environment that facilitates cultural and linguistic responsiveness, emotional well-being, self-efficacy, positive social interaction, mutual respect, active engagement, academic risk-taking, self-motivation, and personal goal-setting. Knowledge Indicators – The competent teacher: 4A) understands principles of and strategies for effective classroom and behavior management; 4B) understands how individuals influence groups and how groups function in society; 4C) understands how to help students work cooperatively and productively in groups; 4D) understands factors (e.g., self-efficacy, positive social interaction) that influence motivation and engagement; 4E) knows how to assess the instructional environment to determine how best to meet a student’s individual needs; 4F) understands laws, rules, and ethical considerations regarding behavior intervention planning and behavior management (e.g., bullying, crisis intervention, physical restraint); 4G) knows strategies to implement behavior management and behavior intervention planning to ensure a safe and productive learning environment; and 4H) understands the use of student data (formative and summative) to design and implement behavior management strategies. Performance Indicators – The competent teacher: 4I) creates a safe and healthy environment that maximizes student learning; 4J) creates clear expectations and procedures for communication and behavior and a physical setting conducive to achieving classroom goals; 4K) uses strategies to create a smoothly functioning learning community in which students assume responsibility for themselves and one another, participate in decision-making, work collaboratively and independently, use appropriate technology, and engage in purposeful learning activities; 4 4L) analyzes the classroom environment and makes decisions to enhance cultural and linguistic responsiveness, mutual respect, positive social relationships, student motivation, and classroom engagement; 4M) organizes, allocates, and manages time, materials, technology, and physical space to provide active and equitable engagement of students in productive learning activities; 4N) engages students in and monitors individual and group-learning activities that help them develop the motivation to learn; 4O) uses a variety of effective behavioral management techniques appropriate to the needs of all students that include positive behavior interventions and supports; 4P) modifies the learning environment (including the schedule and physical arrangement) to facilitate appropriate behaviors and learning for students with diverse learning characteristics; and 4Q) analyzes student behavior data to develop and support positive behavior. Standard 5 - Instructional Delivery – The competent teacher differentiates instruction by using a variety of strategies that support critical and creative thinking, problem-solving, and continuous growth and learning. This teacher understands that the classroom is a dynamic environment requiring ongoing modification of instruction to enhance learning for each student. Knowledge Indicators – The competent teacher: 5A) understands the cognitive processes associated with various kinds of learning; 5B) understands principles and techniques, along with advantages and limitations, associated with a wide range of evidence-based instructional practices; 5C) knows how to implement effective differentiated instruction through the use of a wide variety of materials, technologies, and resources; 5D) understands disciplinary and interdisciplinary instructional approaches and how they relate to life and career experiences; 5E) knows techniques for modifying instructional methods, materials, and the environment to facilitate learning for students with diverse learning characteristics; 5F) knows strategies to maximize student attentiveness and engagement; 5G) knows how to evaluate and use student performance data to adjust instruction while teaching; and 5H) understands when and how to adapt or modify instruction based on outcome data, as well as student needs, goals, and responses. Performance Indicators – The competent teacher: 5I) uses multiple teaching strategies, including adjusted pacing and flexible grouping, to engage students in active learning opportunities that promote the development of critical and creative thinking, problem-solving, and performance capabilities; 5J) monitors and adjusts strategies in response to feedback from the student; 5K) varies his or her role in the instructional process as instructor, facilitator, coach, or audience in relation to the content and purposes of instruction and the needs of students; 5L) develops a variety of clear, accurate presentations and representations of concepts, using alternative explanations to assist students’ understanding and presenting diverse perspectives to encourage critical and creative thinking; 5M) uses strategies and techniques for facilitating meaningful inclusion of individuals with a range of abilities and experiences; 5N) uses technology to accomplish differentiated instructional objectives that enhance learning for each student; 5O) models and facilitates effective use of current and emerging digital tools to locate, analyze, evaluate, and use information resources to support research and learning; 5P) uses student data to adapt the curriculum and implement instructional strategies and materials according to the characteristics of each student; 5 5Q) uses effective co-planning and co-teaching techniques to deliver instruction to all students; 5R) maximizes instructional time (e.g., minimizes transitional time); and 5S) implements appropriate evidence-based instructional strategies. Standard 6 - Reading, Writing, and Oral Communication – The competent teacher has foundational knowledge of reading, writing, and oral communication within the content area and recognizes and addresses student reading, writing, and oral communication needs to facilitate the acquisition of content knowledge. Knowledge Indicators – The competent teacher: 6A) understands appropriate and varied instructional approaches used before, during, and after reading, including those that develop word knowledge, vocabulary, comprehension, fluency, and strategy use in the content areas; 6B) understands that the reading process involves the construction of meaning through the interactions of the reader's background knowledge and experiences, the information in the text, and the purpose of the reading situation; 6C) understands communication theory, language development, and the role of language in learning; 6D) understands writing processes and their importance to content learning; 6E) knows and models standard conventions of written and oral communications; 6F) recognizes the relationships among reading, writing, and oral communication and understands how to integrate these components to increase content learning; 6G) understands how to design, select, modify, and evaluate a wide range of materials for the content areas and the reading needs of the student; 6H) understands how to use a variety of formal and informal assessments to recognize and address the reading, writing, and oral communication needs of each student; and 6I) knows appropriate and varied instructional approaches, including those that develop word knowledge, vocabulary, comprehension, fluency, and strategy use in the content areas. Performance Indicators – The competent teacher: 6J) selects, modifies, and uses a wide range of printed, visual, or auditory materials, and online resources appropriate to the content areas and the reading needs and levels of each student (including ELLs, and struggling and advanced readers); 6K) uses assessment data, student work samples, and observations from continuous monitoring of student progress to plan and evaluate effective content area reading, writing, and oral communication instruction; 6L) facilitates the use of appropriate word identification and vocabulary strategies to develop each student’s understanding of content; 6M) teaches fluency strategies to facilitate comprehension of content; 6N) uses modeling, explanation, practice, and feedback to teach students to monitor and apply comprehension strategies independently, appropriate to the content learning; 6O) teaches students to analyze, evaluate, synthesize, and summarize information in single texts and across multiple texts, including electronic resources; 6P) teaches students to develop written text appropriate to the content areas that utilizes organization (e.g., compare/contrast, problem/solution), focus, elaboration, word choice, and standard conventions (e.g., punctuation, grammar); 6Q) integrates reading, writing, and oral communication to engage students in content learning; 6R) works with other teachers and support personnel to design, adjust, and modify instruction to meet students’ reading, writing, and oral communication needs; and 6S) stimulates discussion in the content areas for varied instructional and conversational purposes. Standard 7 - Assessment – The competent teacher understands and uses appropriate formative and summative assessments for determining student needs, monitoring student progress, measuring student 6 growth, and evaluating student outcomes. The teacher makes decisions driven by data about curricular and instructional effectiveness and adjusts practices to meet the needs of each student. Knowledge Indicators – The competent teacher: 7A) understands the purposes, characteristics, and limitations of different types of assessments, including standardized assessments, universal screening, curriculum-based assessment, and progress monitoring tools; 7B) understands that assessment is a means of evaluating how students learn and what they know and are able to do in order to meet the Illinois Learning Standards; 7C) understands measurement theory and assessment-related issues, such as validity, reliability, bias, and appropriate and accurate scoring; 7D) understands current terminology and procedures necessary for the appropriate analysis and interpretation of assessment data; 7E) understands how to select, construct, and use assessment strategies and instruments for diagnosis and evaluation of learning and instruction; 7F) knows research-based assessment strategies appropriate for each student; 7G) understands how to make data-driven decisions using assessment results to adjust practices to meet the needs of each student; 7H) knows legal provisions, rules, and guidelines regarding assessment and assessment accommodations for all student populations; and 7I) knows assessment and progress monitoring techniques to assess the effectiveness of instruction for each student. Performance Indicators – The competent teacher: 7J) uses assessment results to determine student performance levels, identify learning targets, select appropriate research-based instructional strategies, and implement instruction to enhance learning outcomes; 7K) appropriately uses a variety of formal and informal assessments to evaluate the understanding, progress, and performance of an individual student and the class as a whole; 7L) involves students in self-assessment activities to help them become aware of their strengths and needs and encourages them to establish goals for learning; 7M) maintains useful and accurate records of student work and performance; 7N) accurately interprets and clearly communicates aggregate student performance data to students, parents or guardians, colleagues, and the community in a manner that complies with the requirements of the Illinois School Student Records Act [105 ILCS 10], 23 Ill. Adm. Code 375 (Student Records), the Family Educational Rights and Privacy Act (FERPA) (20 USC 1232g) and its implementing regulations (34 CFR 99; December 9, 2008); 7O) effectively uses appropriate technologies to conduct assessments, monitor performance, and assess student progress; 7P) collaborates with families and other professionals involved in the assessment of each student; 7Q) uses various types of assessment procedures appropriately, including making accommodations for individual students in specific contexts; and 7R) uses assessment strategies and devices that are nondiscriminatory, and take into consideration the impact of disabilities, methods of communication, cultural background, and primary language on measuring knowledge and performance of students. Standard 8 - Collaborative Relationships – The competent teacher builds and maintains collaborative relationships to foster cognitive, linguistic, physical, and social and emotional development. This teacher works as a team member with professional colleagues, students, parents or guardians, and community members. Knowledge Indicators – The competent teacher: 8A) understands schools as organizations within the larger community context; 7 8B) understands the collaborative process and the skills necessary to initiate and carry out that process; 8C) collaborates with others in the use of data to design and implement effective school interventions that benefit all students; 8D) understands the benefits, barriers, and techniques involved in parent and family collaborations; 8E) understands school- and work-based learning environments and the need for collaboration with all organizations (e.g., businesses, community agencies, nonprofit organizations) to enhance student learning; 8F) understands the importance of participating on collaborative and problem-solving teams to create effective academic and behavioral interventions for all students; 8G) understands the various models of co-teaching and the procedures for implementing them across the curriculum; 8H) understands concerns of families of students with disabilities and knows appropriate strategies to collaborate with students and their families in addressing these concerns; and 8I) understands the roles and the importance of including students with disabilities, as appropriate, and all team members in planning individualized education programs (i.e, IEP, IFSP, Section 504 plan) for students with disabilities. Performance Indicators – The competent teacher: 8J) works with all school personnel (e.g., support staff, teachers, paraprofessionals) to develop learning climates for the school that encourage unity, support a sense of shared purpose, show trust in one another, and value individuals; 8K) participates in collaborative decision-making and problem-solving with colleagues and other professionals to achieve success for all students; 8L) initiates collaboration with others to create opportunities that enhance student learning; 8M) uses digital tools and resources to promote collaborative interactions; 8N) uses effective co-planning and co-teaching techniques to deliver instruction to each student; 8O) collaborates with school personnel in the implementation of appropriate assessment and instruction for designated students; 8P) develops professional relationships with parents and guardians that result in fair and equitable treatment of each student to support growth and learning; 8Q) establishes respectful and productive relationships with parents or guardians and seeks to develop cooperative partnerships to promote student learning and well-being; 8R) uses conflict resolution skills to enhance the effectiveness of collaboration and teamwork; 8S) participates in the design and implementation of individualized instruction for students with special needs (i.e., IEPs, IFSP, transition plans, Section 504 plans), ELLs, and students who are gifted; and 8T) identifies and utilizes community resources to enhance student learning and to provide opportunities for students to explore career opportunities. Standard 9 - Professionalism, Leadership, and Advocacy – The competent teacher is an ethical and reflective practitioner who exhibits professionalism; provides leadership in the learning community; and advocates for students, parents or guardians, and the profession. Knowledge Indicators – The competent teacher: 9A) evaluates best practices and research-based materials against benchmarks within the disciplines; 9B) knows laws and rules (e.g., mandatory reporting, sexual misconduct, corporal punishment) as a foundation for the fair and just treatment of all students and their families in the classroom and school; 9C) understands emergency response procedures as required under the School Safety Drill Act [105 ILCS 128/1], including school safety and crisis intervention protocol, initial response 8 actions (e.g., whether to stay in or evacuate a building), and first response to medical emergencies (e.g., first aid and life-saving techniques); 9D) identifies paths for continuous professional growth and improvement, including the design of a professional growth plan; 9E) is cognizant of his or her emerging and developed leadership skills and the applicability of those skills within a variety of learning communities; 9F) understands the roles of an advocate, the process of advocacy, and its place in combating or promoting certain school district practices affecting students; 9G) understands local and global societal issues and responsibilities in an evolving digital culture; and 9H) understands the importance of modeling appropriate dispositions in the classroom. Performance Indicators – The competent teacher: 9I) models professional behavior that reflects honesty, integrity, personal responsibility, confidentiality, altruism and respect; 9J) maintains accurate records, manages data effectively, and protects the confidentiality of information pertaining to each student and family; 9K) reflects on professional practice and resulting outcomes; engages in self-assessment; and adjusts practices to improve student performance, school goals, and professional growth; 9L) communicates with families, responds to concerns, and contributes to enhanced family participation in student education; 9M) communicates relevant information and ideas effectively to students, parents or guardians, and peers, using a variety of technology and digital-age media and formats; 9N) collaborates with other teachers, students, parents or guardians, specialists, administrators, and community partners to enhance students’ learning and school improvement; 9O) participates in professional development, professional organizations, and learning communities, and engages in peer coaching and mentoring activities to enhance personal growth and development; 9P) uses leadership skills that contribute to individual and collegial growth and development, school improvement, and the advancement of knowledge in the teaching profession; 9Q) proactively serves all students and their families with equity and honor and advocates on their behalf, ensuring the learning and well-being of each child in the classroom; 9R) is aware of and complies with the mandatory reporter provisions of Section 4 of the Abused and Neglected Child Reporting Act [325 ILCS 5/4]; 9S) models digital etiquette and responsible social actions in the use of digital technology; and 9T) models and teaches safe, legal, and ethical use of digital information and technology, including respect for copyright, intellectual property, and the appropriate documentation of sources. Received: 26 November 2019 Revised: 10 January 2020 Accepted: 19 January 2020 DOI: 10.1111/obr.13005 PEDIATRICS/PHYSIOLOGY Adipokines: A gear shift in puberty Desirée Nieuwenhuis | Natàlia Pujol-Gualdo Amanda J. Kiliaan Department of Anatomy, Radboud university medical center, Donders Institute for Brain, Cognition and Behaviour, Preclinical Imaging Center PRIME, Nijmegen, The Netherlands Correspondence Amanda J. Kiliaan, PhD, Associate Professor, Department of Anatomy, Donders Institute for Brain, Cognition, and Behaviour, Preclinical Imaging Center PRIME, Radboud university medical center, 6500 HB Nijmegen, Geert Grooteplein 21N 6525 EZ Nijmegen, The Netherlands. Email: amanda.kiliaan@radboudumc.nl Funding information Europees Fonds voor Regionale Ontwikkeling (EFRO), Grant/Award Number: BriteN 2016 1 | INTRODUCTION The prevalence of obesity in adolescents and children is increasing in | Ilse A.C. Arnoldussen | Summary In this review, we discuss the role of adipokines in the onset of puberty in children with obesity during adrenarche and gonadarche and provide a clear and detailed overview of the biological processes of two major players, leptin and adiponectin. Adipokines, especially leptin and adiponectin, seem to induce an early onset of puberty in girls and boys with obesity by affecting the hypothalamic-pituitary- gonadal (HPG) axis. Moreover, adipokines and their receptors are expressed in the gonads, suggesting a role in sexual maturation and reproduction. All in all, adipokines may be a clue in understanding mechanisms underlying the onset of puberty in child- hood obesity and puberty onset variability. KEYWORDS adipokines, obesity, puberty 1,2 the age of 5 years were overweight or were with obesity in 2016, and 3 Obesity is defined by an excessive accumulation of white adipose tissue (WAT), and it is often indicated by a body mass index (BMI) 4 above 30. Two main types of adipose tissue were described: WAT and brown adipose tissue (BAT), which differ in morphology and func- 5-7 Ilse A.C. Arnoldussen and Amanda J. Kiliaan contributed equally to this work. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2020 The Authors. Obesity Reviews published by John Wiley & Sons Ltd on behalf of World Obesity Federation Obesity Reviews. 2020;21:e13005. wileyonlinelibrary.com/journal/obr 1 of 10 https://doi.org/10.1111/obr.13005 alarming rates. Specifically, worldwide, 41 million children below this number is expected to increase to 70 million in 2025. obesity is associated with various severe health complications, includ- ing increased risk of diabetes mellitus type 2, hypertension, heart dis- eases, and disturbances in sex hormone levels. 5,6 and mitochondria and plays a role in thermogenesis. Adipocytes in tion. BAT consists of adipocytes containing multiple lipid droplets WAT contain only a few mitochondria and a single lipid droplet. Adipose tissue has several functions including the storage of energy, thermogenesis, and the production and secretion of adipokines Generally, two physiological processes, adrenarche and gonadarche, 11,24 Childhood 5,7,8 a key role in puberty onset. Puberty is known as a period through which the body changes physically, being a physiological process resulting in the maturation of children, i.e. they develop sexual characteristics and obtain reproduc- 9,11 Adipokines are involved in a number of physiological processes including blood pressure, metabo- lism, glucose, and vascular homeostasis and may play amongst others 8-10 (hormones, cytokines, and peptides). tive functions. between obesity and puberty,2,12-23 the biological mechanisms under- lying obesity and puberty onset remain unclear. Hereafter, we review in detail the role of adipokines in the onset of puberty in childhood obesity. Although many studies have shown associations 2 | INITIATION OF PUBERTY PHYSIOLOGICAL PROCESSES IN THE interact to regulate the onset of puberty. During adrenarche, the adrenal cortex secretes steroid hormones (including 2 of 10 NIEUWENHUIS ET AL. androstenedione, dehydroepiandrosterone, dehydroepiandrosterone sulfate (DHEAS), androstenedione, and cortisol), insulin-like growth factor, and growth hormone, which contribute to the pubertal insights on new genetic loci (e.g. melanocortin-4 receptor, mitochon- drial carrier 2, and mitogen-activated protein kinase 13) and on sev- eral pathways that regulate the timing of puberty; however, it partly 34 9,24,25 Both adrenarche and gonadarche are involved in the development growth spurt, body odor, skin oiliness, and skeletal maturation. explains puberty timing variation. Thereby, defining the role of 25 adipokines is of importance in elucidating the variability in puberty as the expression of adipokines is sex-specific and is altered with body composition, adiposity, and during growth spurts. Moreover, adipokines and their receptors are expressed in gonads and several brain regions suggesting involvement in the onset of puberty and sex- ual maturation. Lastly, adipokines interfere in processes regulating timing and duration of puberty, for instance in the HPA and HPG axes which are both key players during adrenarche and gonadarche. Involvement of adipokines in the onset of puberty and specifically in individuals with obesity will be further reviewed in the next 2,24 3 | Puberty onset in girls is assessed using different markers, such as thelarche (breast development), menarche (the start of of pubic hair. pituitary-gonadal (HPG) axis is activated,2,26 and several hormones have been identified to participate in the activation of the HPG axis During gonadarche (Figure 1), the hypothalamic- 2,27 Kisspeptin, neurokinin B, and dynorphin are released by specialized including kisspeptin, neurokinin B, dynorphin, leptin, and ghrelin. 28 key regulator of the pulsatile secretion of gonadotropin releasing neurons, the KNDy neurons in the hypothalamus. Kisspeptin is a 29,30 B stimulates, and dynorphin inhibits the release of kisspeptin, which hormone (GnRH) from the hypothalamus. In addition, neurokinin implies that both coordinate a pulsatile release of kisspeptin. 31 Sub- sections. sequently, the activated HPG axis induces the pituitary gland to secrete luteinising hormone (LH) and follicle stimulating hormone (FSH). As a result, gametogenesis occurs, and the gonads will release sex hormones. Consequently, secondary sex characteristics develop including breast development in girls and an increased testicular vol- 2,26,32 is possibly due to differences in levels of body fat, hypothalamic-pitui- THE ONSET OF PUBERTY IN GIRLS ume in boys. The age at puberty onset varies greatly among individuals, which 19 35 menstruation), and pubic hair development. 33 genome-wide association studies have provided important new tary-adrenal (HPA) axis activity, and genetic background. Recent The average age of However, this age differs between cultures and ethnicities, and since 1980, age at menarche is girls at start of menarche is 12.4 years. 36 significantly decreasing. 36-39 F I G U R E 1 Hormonal regulation in the initiation of puberty in boys and girls. The secretion of kisspeptin, neurokinin B, and dynorphin from KNDy neurons initiate the release of gonadotropin releasing hormone (GnRH) from the hypothalamus. This activates the pituitary gland to produce and secrete luteinising hormone (LH) and follicle stimulating hormone (FSH), which in turn stimulate the gonads to produce estrogen and testosterone in girls and boys, respectively 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License NIEUWENHUIS ET AL. 3 of 10 T A B L E 1 Summary of included studies Authors Year Country Study Design Primary Outcome Sex Sample Size (n) Age (y) Data Collection Lian et al21 2019 China Cross-sectional Puberty starts earlier in Chinese Han girls with obesity compared with Chinese Han girls with normal weight. Girls 2996 9-19 2012 and 2013 Biro et al12 Lazzeri et al20 2018 USA 2018 Italy Longitudinal Cross-sectional Body mass index had a greater effect on age at menarche than did race and ethnicity. Girls 946 6-16 2004-2014 Li et al23 2018 China Longitudinal For both, boys and girls, a higher BMI (ie, overweight and obese) is associated with earlier onset of puberty Girls Girls Boys Girls 542 Deng et al22 Flom et al15 2017 China Cross-sectional Increased BMI is associated with early timing spermarche and menarche. Boys Girls Girls 1278258 9-15 2005-2012 He et al24 Holmgren et al17 2017 China 2017 Sweden Cross-sectional Longitudinal Onset of puberty is not related to obesity in boys. Boys Boys Girls Girls 782 7-17 972 929 5839 Kelly et al19 2017 UK 2016 Brazil 2016 USA Longitudinal prospective cohort Higher BMI in girls is associated with the onset of menstruation at an earlier age. 11 10-18 11-17 Barcellos Gemelli et al25 Cross-sectional Longitudinal Excess weight is associated with early age of menarche. Girls 727 2014 2003-2009 Glass et al16 Lee et al26 In girls, but not in boys, greater adiposity is associated with the earlier onset of puberty. Boys Girls 135 Cabrera et al27 Leonibus et al14 2014 USA 2013 Italy Cross-sectional Longitudinal Thelarche occurred earlier than recently reported, while age of menarche remained unchanged. Girls 610 3-17.9 2007 2005-2012 Currie et al13 2012 Europe, USA, Canada Cross-sectional Overweight/obesity during childhood predicts the early onset of puberty in girls. Girls 20410 11, 13, 15 2005-2006 2017 USA Prospective birth cohort Overweight/obese status at the age of 7 ye was associated with increased risk of early menarche 788 From birth to menarche occurred Pregnancies 1959-1966 2016 USA Cross-sectional Boys with overweight enter puberty earlier compared with boys with normal weight or obesity, while puberty starts later in boys with obesity compared with boys with normal weight and overweight. Boys 3872 6-16 2005-2010 Overweight during childhood shows a relation with the early onset of puberty in girls. 6535 4259 695 11 15 5.8-12.2 2009/2010 2013/2014 2014-2017 Higher BMI during childhood is associated with early puberty. 2008 and 2009 2000-2002 Obesity during childhood is related to the earlier onset of puberty. Boys Girls 84 123 71 (Continues) 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 4 of 10 NIEUWENHUIS ET AL. 3.1 | Fat storage For the initiation of puberty, the timing of stimulation and/or inhibi- tion of different hormones is important, and additionally, a certain amount and distribution of body fat is needed in order to start menar- che, which emphasizes the importance of body fat. From an evolution- ary point of view, body fat increases in mammalian females during puberty onset, and it highlights the need to guarantee a healthy preg- 40 women with anorexia nervosa. particularly body fat localized predominantly on the gluteofemoral fat depots, is profoundly associated with start of menarche, more than nancy, offspring, and maternal survival. fat, sex-hormones, and neuroendocrine alterations can evolve in men- strual dysfunction, for instance, in women with severe obesity or in 41-43 44-46 to gluteofemoral fat depots suggesting that leptin may convey infor- amount of total body fat. mation on body fat distribution to the hypothalamus during puberty. An improper level of body Importantly, body fat distribution, Blood leptin levels are strongly related 45 3.2 | HPG axis The HPG axis is activated by the release of kisspeptin resulting in the release of GnRH from the hypothalamus, and LH and FSH from the pituitary gland. In girls, FSH is involved in the development of the folli- cles in the ovaries, and it promotes the secretion of estrogen. LH stim- ulates the production of androgen hormones and induces ovulation 48 9,47 the release of kisspeptin and neurokinin B, and kisspeptin thereby (Figure 1). The secretion of estrogen has an inhibitory effect on inhibits the GnRH release from the hypothalamus. pattern of GnRH is important for the regulation of the menstrual cycle. This roughly 28-day-cycle comprises several phases, including the follicular phase and luteal phase. During the follicular phase, increasing levels of FSH stimulate the maturation of follicles and the production of estrogen from the ovaries. This in turn inhibits the release of FSH from the pituitary gland. A high level of estrogen will induce the production of LH by the pituitary gland, resulting in ovula- tion. The matured follicle secretes progesterone thereby inhibiting the release of GnRH. When the corpus luteum is demolished, there is less 48 3.3 | Adipokines According to results from studies reported in Table 1, girls with obe- sity enter puberty earlier compared with girls with normal higher leptin concentrations inhibit the intake of food and increases inhibition of GnRH. As a consequence, the cycle will start again. whole process, starting from the activated HPG axis, results in the development of the secondary sex characteristics in girls including 9,47 thelarche and menarche. 13,14,16-23,49-51 weight. these girls might be found in the secretion of adipokines. For instance, leptin is positively associated with the amount of body fat. Generally, energy expenditure. 9,52-54 An explanation for the early onset of puberty in The expression This TABLE 1 (Continued) Authors Year Country Study Design Primary Outcome Sample Sex Size (n) Age (y) Data Collection Herman-Giddens et al28 2012 USA Cross-sectional Observed mean ages of beginning genital and pubic hair growth and early testicular volumes were earlier than in past studies, depending on the characteristic and race/ethnicity. Boys 4131 6-16 2005-2010 Sorensen et al29 Aksglaede et al30 2010 2009 Denmark Denmark Cross-sectional/longitudinal Longitudinal Puberty onset at earlier ages was associated with an increased BMI in boys. Boys 1528 5.8-19.9 1991-1993/2006-2008 1930-1969 Juul et al31 Ribeiro et al32 2007 2006 Denmark Portugal Retrospective cohort Cross-sectional Higher BMI is associated with early voice break. 11-15 10-15 1990-1999 Kaplowitz et al18 Abbreviation: BMI, body mass USA Cross-sectional The early onset of puberty in Caucasian girls is likely related to an increased BMI. 5-12 1992-1993 2001 index. The higher BMI in boys and girls at 7 y of age, the earlier they enter puberty. Boys 21 612 Girls 135 223 Boys 463 Boys 382 Girls 437 Girls 10 750 Early sexual maturation in boys and girls is associated with overweight. 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License NIEUWENHUIS ET AL. 5 of 10 Leptin may possibly play a role in adrenarche as its plasma level increases with higher levels of body fat and as it can modulate both girls. 33 ing adrenarche. In coherence, in children with obesity, the androgen These findings suggested that lower reproductive status was associated with higher total adiponectin concentrations and that a higher reproductive status was related to higher HMW adiponectin the HPA and HPG axes. These axes are functionally integrated dur- DHEAS was positively associated with leptin levels. Nevertheless, concentrations in girls. In addition, individuals with obesity often another study showed that enhanced adrenal androgen secretion in girls with premature adrenarche was not explained by leptin or BMI 55 ated with androgen levels in girls ; however, it was not related to levels. and IL-6. TNF-α alters, and IL-6 inhibits the expression of 56 8 In addition, the adipokine adiponectin was negatively associ- 57 differences of adiponectin seem to develop during the progression of 56 adiponectin (Figure 2). Thereby, a low level of total adiponectin and/or high levels of inflammatory cytokines in individuals with obe- sity can promote the onset of puberty. Many more adipokines are secreted by WAT including omentin, 52,65-67 9,36,62,68 adrenarche in girls with Prader-Willi syndrome. Interestingly, sex puberty. adrenarche; however, both are not required factors. Thus, leptin and adiponectin might be able to influence In gonadarche, leptin can stimulate the secretion of kisspeptin, and subsequently activation of the HPG axis, which eventually increases the expression of estrogen and androstenedione in the ova- 58 2,60 65-67 The expression of these ries (Figure 2). Ob gene in WAT, resulting in the synthesis and secretion of leptin. Thus, high levels of leptin promote onset of puberty in girls via secre- tion of kisspeptin, and estrogen stimulates leptin secretion addition- ally. Moreover, adiponectin can affect the HPG axis due to the expression of adiponectin receptors in the hypothalamus, pituitary In return, estrogen stimulates the expression of the 59 gland, and gonads. onset as it inhibits the secretion of kisspeptin and GnRH in the hypo- thalamus and the release of GH and LH in the pituitary gland, and 2,60-62 52,60 63 girls with central precocious puberty (CPP). Moreover, total adiponectin had negative correlations with progression of puberty in girls (defined by Tanner stages), whereas HMW adiponectin had FIGURE 2 Adipokinesaffectingthe initiation of puberty in girls. Leptin stimulates the release of kisspeptin in KNDy neurons, which activates the hypothalamus to produce gonadotropin releasing hormone (GnRH). In response to the release of GnRH, the pituitary gland secretes follicle stimulating hormone (FSH) and luteinising hormone (LH), which stimulates the ovaries to release estrogen resulting in the formation of secondary sex characteristics in girls. Estrogen stimulates the production of leptin. Adiponectin inhibits GnRH release resulting in reduced levels of GnRH and thereby a delayed onset of puberty. TNF- α and IL-6 inhibit the production of adiponectin and therefore stimulate the onset of puberty In detail, adiponectin is a regulator of puberty thereby inhibiting the onset of puberty (Figure 2). with obesity often have low levels of adiponectin. et al. showed that total adiponectin was significantly lower, whereas high molecular weight (HMW) adiponectin was significantly higher in ment. 55 63 develop a chronic low-grade inflammatory state, which can be indi- cated by a high level of circulating inflammatory cytokines like TNF-α 64 Individuals Sitticharoon positive associations with LH levels and the progression of puberty in 63 visfatin, resistin, and chemerin. and visfatin are expressed in the ovaries. adipokines in the ovaries suggests a role within the reproductive sys- tem; however, the exact biological processes have to be examined. Thus, specifically leptin, adiponectin, and inflammatory cytokines pro- duced by WAT could be permissive key players during an early onset of puberty in girls with obesity. As an exception, HMW adiponectin seems to have a stimulatory effect on peripheral repro- ductive function as HMW is not able to cross the blood brain 63 barrier. 4 | Markers that are used to assess puberty onset in boys are THE ONSET OF PUBERTY IN BOYS spermarche, voice break, testicular volume, and pubic hair develop- 35 spermarche develop in the early stages of puberty onset, voice In women, omentin, chemerin, While pubic hair development, larger testicular volume, and 69 testicular volume increases, which occurs at an average age of break usually appears in later stages of puberty. Generally, first 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 6 of 10 NIEUWENHUIS ET AL. 11.9 years, followed by the development of pubic hair at 12.2 years of average, and lastly, boys experience spermarche around an aver- 55 related with leptin levels. Thereby, leptin plausibly has a minor impact in adrenarche in boys. Since leptin receptors are found in the hypothalamus, pituitary gland, and testes, they might be involved in the onset of puberty by affecting the HPG axis during gonadarche. Leptin stimulates the release of kisspeptin and GnRH, and as a consequence, it accelerates the onset of puberty (Table 1, Figure 3). In contrast, adiponectin inhibits the secretion of GnRH, GH, LH, and FSH therewith delaying the onset of puberty. However, adiponectin levels are generally lower in men compared with women and even lower in men with obe- age age of 13.4 years. 70 4.1 | Fat storage Many aspects of the reproductive physiology are energetically demanding,71 and therefore, an adequate energy level is necessary. In boys, a dynamic change in body composition occurs around the age of 10 to 13 years, in which they gain approximately 40% of sity. culating inflammatory cytokines. levels can stimulate the HPG axis and therewith an early onset of puberty in boys. Nevertheless, leptin can inhibit the production of tes- 72 mostly consisting of lean mass, which causes exhaustion of most of fat. Subsequently, a growth spurt follows in which they gain tissue 72 in boys, an adequate amount of body fat is important in the onset of their body fat. These alterations in amount of body fat indicate that 4.2 | Puberty in boys is initiated by the release of kisspeptin. As mentioned before, this activates the HPG axis, resulting in the release of GnRH from the hypothalamus, and consequently the release of LH and FSH 9,74 puberty. tosterone from the testes, to estrogen (Figure 3). of the development of secondary sex characteristics in boys. Additionally, leptin can affect fertility in men as it can modulate the nutritional support of spermatogenesis, and moreover, dysfunction of spermatogenesis is associated with an increased leptin level and 73 58 2,60-62 HPG axis from the pituitary gland (Figure 1). and LH stimulates the secretion of testosterone from the testes, which inhibits the release of kisspeptin from the KNDy neurons and 9,48 in men, the release of kisspeptin is more consistent, causing a con- 29,48 subsequently GnRH from the hypothalamus. receptors expressed on KNDy neurons. In humans, KNDy neurons Contrarily to women, LH-induced testosterone levels lead to the stant release of LH. development of secondary sex characteristics in boys. differences between sexes in kisspeptin release are related to a sex- specific and sex steroid-dependent kisspeptin system as estrogen and progesterone modulate kisspeptin activity through the sex-steroid 48 in the infundibular nucleus are involved in negative and positive sex- 48 tal exposure to sex steroids and result in sex-specific differences in steroid feedbacks. kisspeptin release. These sexual dimorphisms are induced by perina- 75,76 4.3 | Adipokines The association between obesity and puberty onset in boys is rather controversial compared with findings in girls. Most studies reported an early onset of puberty in boys associated with increased ate adipose tissue from actual breast tissue. stages are more difficult to assess than female stages as boys lack a more determined marker such as menarche. Thirdly, puberty onset can be indicated by the activation of the HPG axis, and the presence of these secondary sex characteristics is the result of hormonal 2 14,17,22,23,50,51,77,78 BMI, 20,49 all while others reported no associations at Current markers used 79 16,80 or a delayed onset of puberty (Table 1). The presence of excessive adipose tissue can be involved in puberty onset in boys as the secretion of adipokines can modulate both adrenarche and gonadarche. Leptin can affect adrenarche by modulating both the HPG and HPA axes,33 and moreover, androgen levels were positively 55 nal androgen secretion in boys with premature adrenarche was not associated with plasma leptin levels. Nevertheless, enhanced adre- 9 In more detail, 61,62 adiponectin, and individuals with obesity often have high levels of cir- Moreover, inflammatory cytokines, TNF-α, and IL-6, inhibit expression of the leptin receptor in the testis. FSH induces spermatogenesis, too. function and role still have to be examined. 64 High leptin and low adiponectin and fat tissue can convert testosterone Both processes might result in the delay 29,61,79 81,82 In men, other adipokines like chemerin are found in the gonads 65 Thus, particularly high leptin and low adiponectin levels stimulate the HPG axis and thereby accelerate the onset of puberty in boys. Additionally, leptin can dysregulate the development of secondary sex characteristics and spermatogenesis by affecting testosterone levels and nutritional sup- port of spermatogenesis. 5 | LIMITATIONS AND FUTURE RESEARCH DIRECTIONS Even though multiple epidemiological studies have shown the link between puberty onset and obesity, there are some important limita- tions. Firstly, determining both the onset and stage of puberty is rather difficult. For instance, assessing the stage of breast develop- ment in girls with obesity is complicated as clinicians should differenti- 2 changes in response to the activated HPG axis. to determine the onset of puberty refer to secondary sex characteris- tics, such as testicular volume in boys and breast development in girls. A more accurate measurement of puberty onset would be to combine secondary sex characteristics with plasma or serum hormone level measurements such as LH, FSH, adipokines, e.g. leptin. Thereby, differences in puberty measurements could explain variations in the age of puberty onset between boys and girls within different Thereby, resistin is expressed in the testes of rats, but its exact 83 Secondly, male pubertal 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License NIEUWENHUIS ET AL. 7 of 10 FIGURE 3 Adipokines affecting the initiation of puberty in boys. Leptin activates kisspeptin secretion in KNDy neurons, this activates the production of gonadotropin releasing hormone (GnRH) from the hypothalamus. GnRH stimulates the pituitary gland to secrete follicle stimulating hormone (FSH) and luteinising hormone (LH), activating the production of testosterone from the testes allowing the development of secondary sex characteristics. Leptin also inhibits the production of testosterone, which may cause a delayed onset of puberty. Adiponectin inhibits GnRH release. Low levels of adiponectin, as a result of TNF-α and IL-6 expression, lead to a reduced inhibition of GnRH. In response to GnRH release, the pituitary gland will secrete FSH and LH, and the testes will produce testosterone resulting in the development of secondary sex characteristics in boys countries, and In addition, the inclusion of a of puberty. ferent time points is complicated, as subjects examined several decades ago presented pronounced differences concerning lifestyle patterns such as nutrition and exercise habits. Lastly, obesity or over- weight is often determined by BMI, a classification based on weight and height measurements. Additionally, it is important that all studies studies or across continents, ethnicities proper age range (8-16 years) is important when assessing the onset (Figure 4). 12-15,17,20-23,49,77-79,84,85 30,47 Furthermore, comparison between studies from dif- 86 Specifically in children, BMI is often dependent on age and growth use the same anthropometric standards and sex-specific cut-offs. 13,14,16-23,49-51,77-80 fat and would represent a more accurate measurement in its regard. Based on this review, several suggestions can be made for further research. Firstly, the roles of adipokines like resistin, chemerin, visfatin, and omentin in puberty onset, fertility, and sexual maturation should be examined in detail. Secondly, future research examining the onset of puberty should combine indicators of puberty onset (e.g. breast development or testicular volume) with plasma or serum hor- mone measurements such as LH, FSH, sex-steroids, adipokines (e.g. spurts. ment in case of growth spurts. distribution of body fat should be taken into account in determining puberty and obesity in children. For instance, the body adiposity index (BAI), which was introduced in 2011 by Bergman et al.,87 uses hip cir- cumference and height in order to estimate the percentage of body 87 Thereby, BMI is a less accurate measure- F I G U R E 4 87,88 Therefore, both percentage and Average age of puberty onset in Europe, China, and the United States according to several studies from Table 1. Age of puberty onset ranges from 8.47 to 13.33 years in girls and from 8.63 leptin), and body fat distribution (e.g. BAI,87 waist-hip ratio's and/or dual-energy X-ray absorptiometry (DXA)2). Additionally, defining con- sistent and general measurements of puberty in both boys and girls, combined with a proper age range (8-16 years), would facilitate the comparisons between different studies and their results. 12-15, 17, 20-23, 25-29, 31 to 13.7 years in boys. included if average age of markers used to assess puberty was not reported. Pink: girls. Blue: boys Studies (Table 1) were not 39, 56 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 8 of 10 NIEUWENHUIS ET AL. 6 | CONCLUSION In conclusion, epidemiological data regarding obesity and puberty onset in girls show similar outcomes as adiposity results in the early onset of puberty in girls. The majority of the studies examining boys with obesity indicate an early onset of puberty, while not all reported an earlier onset of puberty. In detail, high leptin, TNF-α, and IL-6 levels combined with low adiponectin levels stimulate the activation of the HPG axis in girls and boys with obesity, and 5, 45, 50, 51 REFERENCES 1. Kumar S, Kelly AS. Review of childhood obesity: from epidemiology, etiology, and comorbidities to clinical assessment and treatment. May- o Clin Proc. 2017;92(2):251-265. 2. Reinehr T, Roth CL. Is there a causal relationship between obesity and puberty? The Lancet Child & adolescent health. 2019;3(1):44-54. 3. WorldHealthOrganization. Facts and figures on childhood obesity. 2017. 4. Guglielmi V, Sbraccia P. Obesity phenotypes: depot-differences in adipose tissue and their clinical implications. Eat Weight Disord. 2018; 23(1):3-14. 5. Gomez-Hernandez A, Beneit N, Diaz-Castroverde S. Escribano O. Dif- ferential role of adipose tissues in obesity and related metabolic and vas- cular complications. 2016;2016:1-15, 1216783. 6. Zwick RK, Guerrero-Juarez CF, Horsley V, Plikus MV. Anatomical, physiological, and functional diversity of adipose tissue. Cell Metab. 2018;27(1):68-83. 7. Gulyaeva O, Dempersmier J, Sul HS. Genetic and epigenetic control of adipose development. Biochimica et Biophysica Acta (BBA)— Molecular and Cell Biology of Lipids. 2019;1864:3-12. 8. Khan M, Joseph F. Adipose tissue and adipokines: the association with and application of adipokines in obesity. Forensic Sci. 2014;2014: 711-724, 328592. 9. Alotaibi MF. Physiology of puberty in boys and girls and pathological disorders affecting its onset. J Adolesc. 2019;71:63-71. 10. Cousminer DL, Stergiakouli E, Berry DJ, et al. Genome-wide associa- tion study of sexual maturation in males and females highlights a role for body mass and menarche loci in male puberty. Hum Mol Genet. 2014;23(16):4452-4464. 11. Ahmed ML, Ong KK, Dunger DB. Childhood obesity and the timing of puberty. Trends in endocrinology and metabolism: TEM. 2009;20(5): 237-242. 12. Biro FM, Pajak A, Wolff MS, et al. Age of menarche in a longitudinal US cohort. J Pediatr Adolesc Gynecol. 2018;31(4):339-345. 13. Currie C, Ahluwalia N, Godeau E, Nic Gabhainn S, Due P, Currie DB. Is obesity at individual and national level associated with lower age at menarche? Evidence from 34 countries in the Health Behaviour in School-aged Children Study. The Journal of adolescent health: official publication of the Society for Adolescent Medicine. 2012;50(6): 621-626. 14. De Leonibus C, Marcovecchio ML, Chiavaroli V, de Giorgis T, Chiarelli F, Mohn A. Timing of puberty and physical growth in obese children: a longitudinal study in boys and girls. Pediatr Obes. 2014; 9(4):292-299. 15. Flom JD, Cohn BA, Tehranifar P, et al. Earlier age at menarche in girls with rapid early life growth: cohort and within sibling analyses. Ann Epidemiol. 2017;27(3):187-93.e2. 16. Glass NA, Torner JC, Letuchy EM, et al. The relationship between greater prepubertal adiposity, subsequent age of maturation, and bone strength during adolescence. Journal of bone and mineral research: the official journal of the American Society for Bone and Min- eral Research. 2016;31(7):1455-1465. 17. Holmgren A, Niklasson A, Nierop AF, et al. Pubertal height gain is inversely related to peak BMI in childhood. Pediatr Res. 2017;81(3): 448-454. 18. Kaplowitz PB, Slora EJ, Wasserman RC, Pedlow SE, Herman- Giddens ME. Earlier onset of puberty in girls: relation to increased body mass index and race. Pediatrics. 2001;108(2):347-353. 19. Kelly Y, Zilanawala A, Sacker A, Hiatt R, Viner R. Early puberty in 11-year-old girls: Millennium Cohort Study findings. Arch Dis Child. 2017;102(3):232-237. 20. Lazzeri G, Tosti C, Pammolli A, et al. Overweight and lower age at menarche: evidence from the Italian HBSC cross-sectional survey. BMC Womens Health. 2018;18(1):168-174. thereby an early onset of obesity. leptin can inhibit the production of testosterone in boys and subse- quently inhibit the development of secondary sex characteristics affecting spermatogenesis. for other adipokines, like resistin and omentin, are present in the testes and ovaries suggesting a role in puberty or reproduction; 58, 71 however, their plausible function is still unknown. that adipokines may be key regulators in an early onset of puberty in both girls and boys with obesity, specifically by affecting the HPG axis during gonadarche. Future research should focus on assessing puberty onset by measuring consistent puberty markers and determine the percentage of body fat and its distribution and adipokines and hormone serum levels particularly involved in the HPG axis. CONFLICTS OF INTEREST The authors declare no conflict of interest. FUNDING INFORMATION This research was funded by Europees Fonds voor Regionale Ontwikkeling (EFRO), project BriteN 2016. ORCID Ilse A.C. Arnoldussen Amanda J. Kiliaan https://orcid.org/0000-0002-7395-5284 https://orcid.org/0000-0002-2158-6210 13, 14, 16-26, 29-32 Furthermore, several receptors Nevertheless, We conclude Search strategy We searched PubMed for articles published before Novem- ber 15th, 2019 using relevant keywords, including ‘onset of puberty and adiposity/obesity’, ‘onset of puberty’, ‘children with obesity’, ‘adipose tissue’, ‘childhood obesity’, ‘adiposity’, ‘obesity’, ‘adipokine(s)’, ‘HPG axis’, ‘adipokines ovary/ova- ries’, or ‘adipokines testes’, either alone or in combination. Selection criteria used were English language, longitudinal or cross-sectional studies assessing the onset of puberty, including menarche, thelarche, spermarche, or voice break, combined with high BMI or obesity/adiposity, and articles assessing or reviewing adipokines and its effects on the reproductive system. 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License NIEUWENHUIS ET AL. 9 of 10 21. Lian Q, Mao Y, Luo S, et al. Puberty timing associated with obesity and central obesity in Chinese Han girls. BMC Pediatr. 2019; 19(1):1-7. 22. Deng Y, Liang J, Zong Y, et al. Timing of spermarche and menarche among urban students in Guangzhou, China: trends from 2005 to 2012 and association with Obesity. Sci Rep. 2018;8(1):263-270. 23. Li W, Liu Q. Association of prepubertal obesity with pubertal devel- opment in Chinese girls and boys: a longitudinal study. 2018;30: e23195. 24. Mendle J, Beltz AM, Carter R, Dorn LD. Understanding puberty and its measurement: ideas for research in a new generation. Journal of research on adolescence: the official journal of the Society for Research on Adolescence. 2019;29(1):82-95. 25. Pagani S, Meazza C, Gertosio C, Bozzola E, Bozzola M. Growth hor- mone receptor gene expression in puberty. Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et metabolisme. 2015;47:581-584. 26. Abreu AP, Kaiser UB. Pubertal development and regulation. Lancet Diabetes Endocrinol. 2016;4(3):254-264. 27. Aguirre RS, Eugster EA. Central precocious puberty: from genetics to treatment. Best Pract Res Clin Endocrinol Metab. 2018;32(4): 343-354. 28. Sultan C, Gaspari L, Maimoun L, Kalfa N, Paris F. Disorders of puberty. Best Pract Res Clin Obstet Gynaecol. 2018;48:62-89. 29. Skorupskaite K, George JT, Anderson RA. The kisspeptin-GnRH path- way in human reproductive health and disease. Hum Reprod Update. 2014;20(4):485-500. 30. Dahl SK, Amstalden M, Coolen L, Fitzgerald M, Lehman M. Dynorphin immunoreactive fibers contact GnRH neurons in the human hypothal- amus. Reprod Sci. 2009;16(8):781-787. 31. Navarro VM, Gottsch ML, Chavkin C, Okamura H, Clifton DK, Steiner RA. Regulation of gonadotropin-releasing hormone secretion by kisspeptin/dynorphin/neurokinin B neurons in the arcuate nucleus of the mouse. J Neurosci. 2009;29(38):11859-11866. 32. Zhai L, Liu J, Zhao J, et al. Association of obesity with onset of puberty and sex hormones in chinese girls: a 4-year longitudinal study. PLoS ONE. 2015;10(8):1-12, e0134656. 33. Cizza G, Dorn LD, Lotsikas A, Sereika S, Rotenstein D, Chrousos GP. Circulating plasma leptin and IGF-1 levels in girls with premature adrenarche: potential implications of a preliminary study. Horm Metab Res. 2001;33(3):138-143. 34. Cousminer DL, Widén E, Palmert MR. The genetics of pubertal timing in the general population: recent advances and evidence for sex-spec- ificity. Curr Opin Endocrinol Diabetes Obes. 2016;23(1):57-65. 35. Marshall WA, Tanner JM. Variations in pattern of pubertal changes in girls. Arch Dis Child. 1969;44(235):291-303. 36. Lacroix AE, Whitten R. Physiology. Treasure Island (FL): Menarche. StatPearls. StatPearls Publishing; 2018. 37. McDowell MA, Brody DJ, Hughes JP. Has Age at Menarche Chan- ged? Results from the National Health and Nutrition Examination Sur- vey (NHANES) 1999–2004. J Adolesc Health. 2007;40(3):227-231. 38. de Muinich Keizer SM, Mul D. Trends in pubertal development in Europe. Hum Reprod Update. 2001;7(3):287-291. 39. Talma H, Schönbeck Y, van Dommelen P, Bakker B, van Buuren S, Hirasing RA. Trends in menarcheal age between 1955 and 2009 in the Netherlands. PLoS ONE. 2013;8:e60056-e60056. 40. Kaplan HS, Lancaster JB. An evolutionary and ecological analysis of human fertility, mating patterns, and parental investment. Off- spring: Human fertility behavior in biodemographic perspective. 2003;1: 170-223. 41. Mitan LA. Menstrual dysfunction in anorexia nervosa. J Pediatr Adolesc Gynecol. 2004;17(2):81-85. 42. Xu H, Li P-H, Barrow TM, et al. Obesity as an effect modifier of the association between menstrual abnormalities and hypertension in young adult women: Results from Project ELEFANT. PLoS ONE. 2018; 13(11):e0207929-e0207929. 43. Tauqeer Z, Gomez G, Stanford FC. Obesity in women: insights for the clinician. J Womens Health (Larchmt). 2018;27(4):444-457. 44. de Ridder CM, Thijssen JH, Bruning PF, Van den Brande JL, Zonderland ML, Erich WB. Body fat mass, body fat distribution, and pubertal development: a longitudinal study of physical and hormonal sexual maturation of girls. J Clin Endocrinol Metab. 1992;75(2): 442-446. 45. Lassek W, Gaulin S. Brief communication: menarche is related to fat distribution. Am J Phys Anthropol. 2007;133(4):1147-1151. 46. Loomba-Albrecht LA, Styne DM. Effect of puberty on body composi- tion. Curr Opin Endocrinol Diabetes Obes. 2009;16:10-15. 47. Simonneaux V, Bahougne T. A multi-oscillatory circadian system times female reproduction. Front Endocrinol. 2015;6:1-15. 48. Marques P, Skorupskaite K, George JT, Anderson RA. Physiology of GNRH and gonadotropin secretion. In: Feingold KR, Anawalt B, Boyce A, et al., eds. Endotext. Endotext.org: South Dartmouth (MA); 2000. 49. Barcellos Gemelli IF, Farias EDS, Souza OF. Age at menarche and its association with excess weight and body fat percentage in girls in the Southwestern Region of the Brazilian Amazon. J Pediatr Adolesc Gynecol. 2016;29(5):482-488. 50. Aksglaede L, Juul A, Olsen LW, Sorensen TI. Age at puberty and the emerging obesity epidemic. PLoS ONE. 2009;4:1-6, e8450. 51. Ribeiro J, Santos P, Duarte J, Mota J. Association between over- weight and early sexual maturation in Portuguese boys and girls. Ann Hum Biol. 2006;33(1):55-63. 52. Budak E, Fernandez Sanchez M, Bellver J, Cervero A, Simon C, Pellicer A. Interactions of the hormones leptin, ghrelin, adiponectin, resistin, and PYY3-36 with the reproductive system. Fertil Steril. 2006;85(6):1563-1581. 53. Castellano JM, Tena-Sempere M. Metabolic control of female puberty: potential therapeutic targets. Expert Opin Ther Targets. 2016; 20(10):1181-1193. 54. Venancio JC, Margatho LO, Rorato R, et al. Short-term high-fat diet increases leptin activation of CART neurons and advances puberty in female mice. Endocrinology. 2017;158(11):3929-3942. 55. l'Allemand D, Schmidt S, Rousson V, Brabant G, Gasser T, Gruters A. Associations between body mass, leptin, IGF-I and circulating adrenal androgens in children with obesity and premature adrenarche. Eur J Endocrinol. 2002;146(4):537-543. 56. Böttner A, Jr K, Müller G, et al. Gender Differences of adiponectin levels develop during the progression of puberty and are related to serum androgen levels. J Clin Endocrinol Metabol. 2004;89(8):4053- 4061. 57. Unanue N, Bazaes R, Iñiguez G, Cortes F, Avila A, Mericq V. Adre- narche in Prader-Willi syndrome appears not related to insulin sensi- tivity and serum adiponectin. Horm Res. 2007;67(3):152-158. 58. Michalakis K, Mintziori G, Kaprara A, Tarlatzis BC, Goulis DG. The complex interaction between obesity, metabolic syndrome and repro- ductive axis: a narrative review. Metabolism: clinical and experimental. 2013;62(4):457-478. 59. Machinal-Quelin F, Dieudonne MN, Pecquery R, Leneveu MC, Giudicelli Y. Direct in vitro effects of androgens and estrogens on ob gene expression and leptin secretion in human adipose tissue. Endo- crine. 2002;18(2):179-184. 60. Dobrzyn K, Smolinska N, Kiezun M. Adiponectin: A new regulator of female reproductive system. Int J Endocrinol. 2018;2018:1-12, 7965071. 61. Martin LJ. Implications of adiponectin in linking metabolism to testic- ular function. Endocrine. 2014;46(1):16-28. 62. Mathew H, Castracane VD, Mantzoros C. Adipose tissue and repro- ductive health. Metabolism: clinical and experimental. 2018;86:18-32. 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 10 of 10 NIEUWENHUIS ET AL. 63. Sitticharoon C, Sukharomana M, Likitmaskul S, Churintaraphan M, Maikaew P. Corrigendum to: Increased high molecular weight adiponectin, but decreased total adiponectin and kisspeptin, in central precocious puberty compared with aged-matched prepubertal girls. Reprod Fertil Dev. 2017;29:2506-2517. 64. Das UN. Is obesity an inflammatory condition? Nutrition. 2001; 17(11-12):953-966. 65. Comninos AN, Jayasena CN, Dhillo WS. The relationship between gut and adipose hormones, and reproduction. Hum Reprod Update. 2014; 20(2):153-174. 66. Singh A, Choubey M, Bora P, Krishna A. Adiponectin and chemerin: contrary adipokines in regulating reproduction and metabolic disor- ders. Reproductive sciences (Thousand Oaks, Calif). 2018;25:1462- 1473. 67. Tsatsanis C, Dermitzaki E, Avgoustinaki P, Malliaraki N, Mytaras V, Margioris AN. The impact of adipose tissue-derived factors on the hypothalamic-pituitary-gonadal (HPG) axis. Hormones (Athens). 2015; 14:549-562. 68. Kang MJ, Oh YJ, Shim YS, Baek JW, Yang S. Hwang IT. The usefulness of circulating levels of leptin, kisspeptin, and neurokinin B in obese girls with precocious puberty. 2018;34:627-630. 69. Lee J, Song J, Hootman JM, et al. Obesity and other modifiable fac- tors for physical inactivity measured by accelerometer in adults with knee osteoarthritis: data from the osteoarthritis initiative (OAI). Arthritis Care Res (Hoboken). 2012;53-61. 70. Bramswig J, Dubbers A. Disorders of pubertal development. Deutsches Arzteblatt international. 2009;106:295-303. quiz 04 71. Elias CF, Purohit D. Leptin signaling and circuits in puberty and fertil- ity. Cell Mol Life Sci. 2013;70(5):841-862. 72. Riumallo J, Durnin JV. Changes in body composition in adolescent boys. Eur J Clin Nutr. 1988;42(2):107-112. 73. Siervogel RM, Demerath EW, Schubert C, et al. Puberty and body composition. Horm Res. 2003;60(Suppl 1):36-45. 74. Zhang J. Gong M. Andrologia: Review of the role of leptin in the regu- lation of male reproductive function; 2018. 75. Kauffman AS, Gottsch ML, Roa J, et al. Sexual differentiation of Kiss1 gene expression in the brain of the rat. Endocrinology. 2007;148(4): 1774-1783. 76. Zeydabadi Nejad S, Ramezani Tehrani F, Zadeh-Vakili A. The role of kisspeptin in female reproduction. Int J Endocrinol Metab. 2017;15:1- 11, e44337. 77. Sorensen K, Aksglaede L, Petersen JH, Juul A. Recent changes in pubertal timing in healthy Danish boys: associations with body mass index. J Clin Endocrinol Metab. 2010;95(1):263-270. 78. Juul A, Magnusdottir S, Scheike T, Prytz S, Skakkebaek NE. Age at voice break in Danish boys: effects of pre-pubertal body mass index and secular trend. Int J Androl. 2007;30(6):537-542. 79. Lee JM, Wasserman R, Kaciroti N, et al. Timing of puberty in overweight versus obese boys. Pediatrics. 2016;137(2):137-146, e20150164. 80. He F, Guan P, Liu Q, Crabtree D, Peng L, Wang H. The relationship between obesity and body compositions with respect to the timing of puberty in Chongqing adolescents: a cross-sectional study. BMC Pub- lic Health. 2017;17:664-673. 81. Ishikawa T, Fujioka H, Ishimura T, Takenaka A, Fujisawa M. Expres- sion of leptin and leptin receptor in the testis of fertile and infertile patients. Andrologia. 2007;39(1):22-27. 82. Martins AD, Moreira AC, Sa R, et al. Leptin modulates human Sertoli cells acetate production and glycolytic profile: a novel mechanism of obesity-induced male infertility? Biochim Biophys Acta. 1852;2015: 1824-1832. 83. Morash BA, Willkinson D, Ur E, Wilkinson M. Resistin expression and regulation in mouse pituitary. FEBS Lett. 2002;526(1-3):26-30. 84. Cabrera SM, Bright GM, Frane JW, Blethen SL, Lee PA. Age of thelarche and menarche in contemporary US females: a cross- sectional analysis. Journal of pediatric endocrinology & metabolism: JPEM. 2014;27(1-2):47-51. 85. Herman-Giddens ME, Steffes J, Harris D, et al. Secondary sexual characteristics in boys: data from the Pediatric Research in Office Settings Network. Pediatrics. 2012;130(5):e1058-e1068. 86. WHO. Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Committee. World Health Organ Tech Rep Ser. 1995;854:1-452. 87. Akin I, Tolg R, Hochadel M, et al. No evidence of “obesity paradox” after treatment with drug-eluting stents in a routine clinical practice: results from the prospective multicenter German DES.DE (German Drug-Eluting Stent) Registry. JACC Cardiovasc Interv. 2012;5(2): 162-169. 88. Marcovecchio ML, Chiarelli F. Obesity and growth during childhood and puberty. World Rev Nutr Diet. 2013;106:135-141. How to cite this article: Nieuwenhuis D, Pujol-Gualdo N, Arnoldussen IAC, Kiliaan AJ. Adipokines: A gear shift in puberty. Obesity Reviews. 2020;21:e13005. https://doi.org/ 10.1111/obr.13005 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are gover