On the function and origin of the avian renal portal shunt and its potential significance throughout evolution

IF 11 1区 生物学 Q1 BIOLOGY
Kobe Buyse, Koen Stein, Ward De Spiegelaere, Pieter Cornillie, Marcus Clauss, Geert P.J. Janssens
{"title":"On the function and origin of the avian renal portal shunt and its potential significance throughout evolution","authors":"Kobe Buyse, Koen Stein, Ward De Spiegelaere, Pieter Cornillie, Marcus Clauss, Geert P.J. Janssens","doi":"10.1111/brv.13144","DOIUrl":null,"url":null,"abstract":"All birds possess a unique venous architecture surrounding the kidneys known as the renal portal system. In veterinary medicine, this system is well known for causing a first‐pass effect when medication is administered parenterally <jats:italic>via</jats:italic> the leg veins, that is venous blood from the leg is filtered before entering general circulation, thus possibly compromising adequate dosage. Additionally, bilateral valves are present in these veins, and it has been hypothesized that they play a crucial role in regulating flow through the kidneys to protect them against increases in blood pressure. While this hypothesis has been acknowledged, it has not been thoroughly explored. We propose that the function of the renal portal valve extends beyond its significance for kidney function, potentially impacting general hemodynamics. Examining anatomical similarities with extant non‐avian reptiles, which lack the renal portal shunt with valve, could reveal additional functionalities of this system in birds. Given the endothermic metabolism and the energetically expensive locomotor activity of birds, the resistance of the hepatic and renal portal system might constrain the blood flow from splanchnic to non‐splanchnic blood vessels necessary for (sustained) peak performance. Therefore, diverting blood from the renal portal system using the renal portal valve as a regulatory structure might represent a key adaptation to facilitate sustained peak performance. In addition, we hypothesize that this shunt and valve represents a very early adaptation in amniotes, possibly lost in extant non‐avian reptiles but enhanced in birds, with a pivotal role in maintaining hemodynamic homeostasis to support the high metabolic rates characteristic of birds.","PeriodicalId":133,"journal":{"name":"Biological Reviews","volume":"21 1","pages":""},"PeriodicalIF":11.0000,"publicationDate":"2024-09-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Biological Reviews","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1111/brv.13144","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

All birds possess a unique venous architecture surrounding the kidneys known as the renal portal system. In veterinary medicine, this system is well known for causing a first‐pass effect when medication is administered parenterally via the leg veins, that is venous blood from the leg is filtered before entering general circulation, thus possibly compromising adequate dosage. Additionally, bilateral valves are present in these veins, and it has been hypothesized that they play a crucial role in regulating flow through the kidneys to protect them against increases in blood pressure. While this hypothesis has been acknowledged, it has not been thoroughly explored. We propose that the function of the renal portal valve extends beyond its significance for kidney function, potentially impacting general hemodynamics. Examining anatomical similarities with extant non‐avian reptiles, which lack the renal portal shunt with valve, could reveal additional functionalities of this system in birds. Given the endothermic metabolism and the energetically expensive locomotor activity of birds, the resistance of the hepatic and renal portal system might constrain the blood flow from splanchnic to non‐splanchnic blood vessels necessary for (sustained) peak performance. Therefore, diverting blood from the renal portal system using the renal portal valve as a regulatory structure might represent a key adaptation to facilitate sustained peak performance. In addition, we hypothesize that this shunt and valve represents a very early adaptation in amniotes, possibly lost in extant non‐avian reptiles but enhanced in birds, with a pivotal role in maintaining hemodynamic homeostasis to support the high metabolic rates characteristic of birds.
禽类肾门分流术的功能和起源及其在整个进化过程中的潜在意义
所有鸟类的肾脏周围都有一个独特的静脉结构,称为肾门系统。在兽医领域,众所周知,当通过腿部静脉进行肠外给药时,该系统会产生首过效应,即来自腿部的静脉血在进入血液循环之前会被过滤,从而可能影响足够的剂量。此外,这些静脉中还存在双侧瓣膜,据推测,它们在调节流经肾脏的血流以保护肾脏免受血压升高的影响方面起着至关重要的作用。虽然这一假设已得到认可,但尚未得到深入探讨。我们提出,肾门瓣膜的功能超出了其对肾脏功能的意义,有可能影响整个血液动力学。现存的非鸟类爬行动物缺乏带瓣的肾门分流管,研究它们在解剖学上的相似性可以揭示该系统在鸟类中的其他功能。鉴于鸟类的内热代谢和高能耗的运动活动,肝门和肾门系统的阻力可能会限制从脾脏到非平滑肌血管的血流,而(持续的)高峰表现是必要的。因此,利用肾门瓣膜作为调节结构将血液从肾门系统分流出来,可能是促进持续峰值表现的关键适应措施。此外,我们假设这种分流和瓣膜代表了羊膜动物的早期适应,可能在现存的非鸟类爬行动物中已经消失,但在鸟类中得到了加强,在维持血液动力学平衡以支持鸟类特有的高代谢率方面起着关键作用。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Biological Reviews
Biological Reviews 生物-生物学
CiteScore
21.30
自引率
2.00%
发文量
99
审稿时长
6-12 weeks
期刊介绍: Biological Reviews is a scientific journal that covers a wide range of topics in the biological sciences. It publishes several review articles per issue, which are aimed at both non-specialist biologists and researchers in the field. The articles are scholarly and include extensive bibliographies. Authors are instructed to be aware of the diverse readership and write their articles accordingly. The reviews in Biological Reviews serve as comprehensive introductions to specific fields, presenting the current state of the art and highlighting gaps in knowledge. Each article can be up to 20,000 words long and includes an abstract, a thorough introduction, and a statement of conclusions. The journal focuses on publishing synthetic reviews, which are based on existing literature and address important biological questions. These reviews are interesting to a broad readership and are timely, often related to fast-moving fields or new discoveries. A key aspect of a synthetic review is that it goes beyond simply compiling information and instead analyzes the collected data to create a new theoretical or conceptual framework that can significantly impact the field. Biological Reviews is abstracted and indexed in various databases, including Abstracts on Hygiene & Communicable Diseases, Academic Search, AgBiotech News & Information, AgBiotechNet, AGRICOLA Database, GeoRef, Global Health, SCOPUS, Weed Abstracts, and Reaction Citation Index, among others.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信