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系統識別號 U0026-2208201221394800
論文名稱(中文) 由流行病學及in vitro的研究探討B群鏈球菌之生物膜與表面蛋白質
論文名稱(英文) Biofilm and surface proteins of Group B streptococci: implications from epidemiology and in vitro studies
校院名稱 成功大學
系所名稱(中) 基礎醫學研究所
系所名稱(英) Institute of Basic Medical Sciences
學年度 100
學期 2
出版年 101
研究生(中文) 何月仁
研究生(英文) Yueh-Ren Ho
學號 S58921125
學位類別 博士
語文別 英文
論文頁數 132頁
口試委員 指導教授-吳俊忠
口試委員-何漣漪
口試委員-林以行
口試委員-劉清泉
口試委員-鄧景浩
口試委員-鄧麗珍
口試委員-賴信志
口試委員-胡小婷
中文關鍵字 B群鏈球菌  生物膜  Rib蛋白質  環境因子  酸性環境  移生  原子力顯微鏡 
英文關鍵字 Group B streptococcus  GBS  Rib protein  Biofilm  environmental factors  Vaginal pH  Colonization  AFM 
學科別分類
中文摘要 B群鏈球菌是常見於懷孕婦女陰道的移生菌,可以經過羊水或生產過程中傳播給胎兒,或者經由其他路徑,伺機性地造成新生兒的肺炎、腦膜炎和敗血症;近幾年來,罹患慢性疾病的成人,尤其是高年齡族群,受到B群鏈球菌的感染案例也逐漸增加,對於B群鏈球菌在這些好發族群的感染或移生,都是值得追蹤探討的重要議題。細菌的生物膜是細菌受到酸性、溫度、營養、及滲透壓等外在環境的變化,所因應而釋放出多醣體的黏液來保護菌體,時常造成環境清除與抗生素抗性的困擾,也是醫療上急待解決的問題。近年來,細菌的生物膜被認為與細菌在宿主的移生以及致病機轉有關,但截至目前,對於B群鏈球菌生物膜的產生了解並不多,而對於其影響因子所知更有限,因此,本研究主要針對B群鏈球菌的好發族群進行流行病學的研究,並探討B群鏈球菌生物膜的特性及其形成有關的影響因子,藉此建立一套B群鏈球菌生物膜形成的模式。此外,檢視由懷孕的婦女所採檢到之移生的B群鏈球菌,探討它們形成生物膜的能力,以了解B群鏈球菌在懷孕的婦女的移生所扮演的角色。
由流行病學的研究發現,B群鏈球菌在懷孕婦女的攜帶率是19.6%;在新生兒檢出的B群鏈球菌中,來自晚期發作疾病 (69%) 明顯地高於早期發作疾病 (31%)。在B群鏈球菌已知的血清型中,type III與type V是台灣血液培養最常見的;其中type III (79%) 是造成新生兒B群鏈球菌感染主要的血清型,而type V 則主要發生在成人的感染(26%)以及懷孕婦女的移生(26%)。由GBS之Alp表面蛋白質的分析,顯示在所有156株菌株中,所表現之Alp表面蛋白質基因以bca、alp2/3與 rib為主,共占86 %,其中又以rib最顯著,在新生兒的感染族群,所佔比例高達69 %;而成人B群鏈球菌感染方面則以bca (31%)、alp2/3 (29-33%)為最多。研究也發現在造成新生兒腦膜炎的B群鏈球菌中,有高達78%帶有rib,因此推論Rib蛋白質可能在造成新生兒的腦膜炎中扮演重要的角色。由於rib基因的構造中有80 %具有tandem repeat的特性,研究結果顯示rib的tandem repeat數目的不同與感染的年齡層有顯著的關係,新生兒感染的B群鏈球菌,通常是帶有低數目的tandem repeat,反之,成人的tandem repeat多是較高的,這種rib低tandem repeat的數目的特性可能與B群鏈球菌在感染新生兒時較容易躲避母親宿主的免疫攻擊有關。
由B群鏈球菌的生長研究顯示,此菌可以存活在營養有限並且酸性的環境下,維持107-8 CFU/ml菌數至少24小時。而生物膜的研究也發現,B群鏈球菌生物膜的產生與細菌的生長速率沒有絕對的關係,但與環境的酸鹼值有顯著關係,也證實在酸性的環境的確可以產生生物膜,這是過去的研究尚未證實的。此外,也會受到環境中之培養基、葡萄糖、酪蛋白胺基酸的濃度影響。在酸性的環境下,B群鏈球菌在營養有限的培養基M9YE,不論加或不加葡萄糖,都可以產生生物膜,但在營養相對豐富的THB環境則無法產生。反之,在中性環境下,B群鏈球菌只有在THB外加0.4%葡萄糖的培養下,可以產生生物膜,但M9YE則不能;另外,酪蛋白胺基酸對B群鏈球菌生物膜的產生都有提昇的作用,尤其在THB的培養下。此外,細菌培養的成長期與接種量也會對B群鏈球菌生物膜的產生造成影響,本研究發現當細菌經過4小時的再新培養之後,即生長穩定期前的B群鏈球菌才能產生生物膜;而且,起始的菌量至少需要107 CFU/ml以上。由以上的結果顯示,B群鏈球菌在營養豐富與有限的環境下都可以形成生物膜,但須結合環境的酸鹼值才有決定性的影響。另外,由原子力拓樸形貌與彈性力學的研究結果也發現,在不同條件下,B群鏈球菌生物膜的表面有很明顯的差異,生物膜產生能力愈強的,其軟度愈高,而且表面愈多不定形的顆粒,其緻密度也愈高。
另外,利用營養豐富與營養有限的二種產生生物膜的模式,針對懷孕的婦女陰道採檢到之B群鏈球菌,進行生物膜的分析,結果也證實B群鏈球菌的確在營養有限且酸性的模式培養下, 96%都會產生生物膜;而在中性的環境之下,只有10%會產生;相反的,在營養豐富且中性的模式下,有67%會形成生物膜,相對的在酸性下則完全無法產生;也進一步發現在酸性的模式下,所產生的生物膜顯著地比在中性的模式下所產生的多。此外,也發現B群鏈球菌生物膜的產生與其血清型有關,由懷孕婦女陰道所收集的菌株,第III以及V血清型總合起來,明顯地比Ia及 Ib行容易產生生物膜。
總結,B群鏈球菌在人體的感染與移生,以及造成的疾病,與宿主的年齡、細菌的血清型及表面蛋白質分佈有顯著的關係;而在營養有限並且酸性的環境,很明顯地會促進B群鏈球菌產生生物膜,這種模式很可能就是造成B群鏈球菌容易在生育期婦女的陰道移生的主要原因,而相對的在營養豐富且中性下的環境也能產生生物膜,意味著B群鏈球菌在新生兒及成人感染中形成生物膜的可能性。
英文摘要 Group B streptococcus (GBS) is a common asymptomatic colonizer in acidic vagina of pregnant women and can transmit to newborns, causing neonatal pneumonia and meningitis. GBS is also important pathogens in adult patients with underlying diseases, especially in elderly. Biofilm is a sessile community of bacteria, encapsulated in a self-produced extracellular matrix in response to stressful environments; it usually posts serious challenge in detachment and antibiotic resistance. Recently, biofilm formation has been reported to associate with bacterial colonization and pathogenesis. Still, little is known about GBS biofilm and the effect of environmental stimuli on biofilm formation. The objective of this study was to investigate the epidemiology of invasive GBS strains isolated from neonates and adults, and colonizing GBS from pregnant women. Further aims were to characterize GBS biofilm, and biofilm formation including its affecting factors; in order to construct an ideal biofilm formation model, and eventually apply to screen the capability of biofilm formation on the colonizing GBS strains.
The surveillance has unveiled 19.6% carrier rate of colonizing GBS from pregnant women, high incidence rate of late-onset disease (LOD; 69%) rather than early-onset disaease (EOD; 31%), and the most prevalent serotypes III and V among invasive GBS strains. In particular, serotype III (79%) dominated in neonatal infection, however, type V dominated in adults (26%) and pregnant women (26%). Surface protein profile showed that the most common protein genes were bca, alp2/3 and rib, totally accounting for 86%. Furthermore, the rib gene was significantly dominant in invasive neonates, while bca (31%) and alp2/3 (29-33%) were dominant in adults. Interestingly, 78% of isolates from neonatal meningitis harbored the rib gene, implying that Rib protein plays a critical role in neonatal meningitis. Tandem repeats study of the rib gene revealed that the variation of repeat numbers in the rib gene was age related; variants with few repeats were more often collected from neonates than adults. GBS isolates from neonates with few repeats of the rib gene might reflect their advantage to escape the pressure of maternal immunity.
The growth study showed that GBS could survive in M9YE and THB medium, with cell density above 107-8 CFU/ml. In GBS biofilm study indicates that biofilm formation of GBS was growth rate-independent, but strongly associated with pH conditions. One of the innovative discoveries was acidic condition could enhance biofilm formation in GBS. Also, GBS biofilm production was influenced by environmental factors e.g., pH, growth medium, and glucose. At acidic condition, GBS biofilm formation favored in M9YE medium, in contrast, THB supplemented with 0.4% glucose favored biofilm production at neutral pH. Further, biofilm formation by GBS favored bacterial culture of early stationary phase relative to overnight cultures, and with minimum inoculum cell density of 107 CFU/ml. The atomic force microscope (AFM) study of topography of GBS biofilm showed amorphous material on the surface of biofilm and the quantity was increased along with ascending of inoculum size and incubation time. Mechanical force measurement by AFM demonstrated that low elastic modulus on the high biofilm sample, approving the softness of biofilm; in contrast, a high elastic modulus as measured on low or non-biofilm sample. The screening of biofilm formation in colonizing GBS strains using two GBS biofilm models, confiirmed their efficiency in biofilm formation, but with higher production in M9YE rather than in THB model. Further, the predominant serotypes, III and V combined, showed significant difference in biofilm formation than type Ia and Ib combined.
In conclusion, the clinical manifestations and colonization of GBS were associated with disease, age, bacterial serotype and surface proteins. The capability of forming biofilm at acidic and nutrition-limited conditions may provide GBS a potential advantage to colonize its natural habitats, such as vagina of reproductive women; while establishing biofilm at nutrient-rich at neutral pH model, indicate the possibility of biofilm formation of GBS in neonatal and adult infections.
論文目次 Table of Contents

Abstract---------------------------------------------------i
Acknowledgements------------------------------------------vi
Table of contents-------------------- --vii
List of tables----------------------------------------xiii
List of figures---------------------------------------xiv
List of abbreviations----------------------------xvi

CHAPTER 1 Introduction------------------------------------1
1.1. Epidemiology of GBS------------------------------1
1.1.1. General aspects----------------------------------1
1.1.2. GBS infection in neonates-------------------------1
1.1.3. GBS infection in non-pregnant adults--------------2
1.1.4. GBS colonization in pregnant women---------------3
1.2. Molecular basis of GBS virulence------------------3
1.2.1. General aspects----------------------------------3
1.2.2. Serotype of GBS----------------------------4
1.2.3. Surface proteins--------------------------4
1.2.4. Pili---------------------------------------------6
1.2.5. Alp family proteins------------------------7
1.2.6. Virulence factors involving cellular adherence and invasion-------------8
1.2.7. Virulence factors involving immune evasion-------10
1.2.8. Virulence factors involving resistance to host antimicrobial peptides-----------------10
1.2.9. Other virulence factors contributing GBS pathogenesis-----------------------11
1.3. Growth and killing of GBS------------------11
1.4. Microbial biofilms--------------------------12
1.4.1. General aspects---------------------------12
1.4.2. Biofilm development------------------13
1.4.3. Extracellular matrix of biofilm--------------13
1.4.4. Environmental factors affecting biofilm formation-----------------------------------------14
1.4.4.1. pH-----------------------------------------14
1.4.4.2. Nutrients----------------------------------15
1.4.4.2.1. carbon source---------------------------15
1.4.4.3. Osmolarity---------------------------------17
1.4.4.4. Quorum sensing-----------------------17
1.4.5. Differences between biofilm and planktonic cells------------------------------------------18
1.4.6. Antibiotic resistance of biofilm-----------------19
1.4.7. Biofilm and infectious diseases-----------------19
1.4.8. Animal models of bacterial biofilm formation-----20
1.5. Biofilm formation by GBS------------------21
1.5.1. Serotype, pili and biofilm formation-------------22
1.6. AFM technology---------------------------------23
1.7. Aims of the work-------------------------------24

CHAPTER 2 Materials and Methods-------------------------26
2.1. Clinical presentation--------------------------26
2.2. Bacterial strains----------------------------26
2.3. Bacterial media and growth conditions------------27
2.3.1. Media--------------------------------------------27
2.3.2. Growth conditions-----------------------27
2.4. DNA manipulation and analysis------------------28
2.4.1. Preparation of chromosomal DNA-------------------28
2.4.2. Polymerase chain reaction (PCR)------------------28
2.4.3. GBS Serotyping-------------------------------28
2.4.4. Pilus typing------------------------------------29
2.4.5. Surface protein gene profiles--------------------29
2.4.6. Determination of the number of tandem repeats in the rib gene----------------------30
2.5. Antibiotic susceptibility-----------------------30
2.6. Growth rate determination---------------------31
2.7. Killing rate determination--------------32
2.8. Growth and survival experiment-----------32
2.9. Biofilm assay-------------------------------33
2.9.1. Influence of pH on biofilm formation---------34
2.9.2. Influences of glucose, casamino acid, and NaCl on biofilm formation----------------34
2.9.3. Influence of inoculum cell density on biofilm formation---------------------------------34
2.9.4. Influence of growth phase on biofilm formation-------------------------------------------35
2.10. Measurement of metabolic activity---------35
2.11. Scanning electron microscopy (SEM)----------35
2.12. Atomic force microscopy (AFM)--------36
2.12.1. Mechaincal force measurement---------36
2.12.2. Topography AFM scanning--------------37
2.13. Measurements and statistical analysis-----------37

CHAPTER 3 Results-------------------38
Part I Epidemiology of GBS-------------------38
3.1.1. Epidemiology of invasive GBS strains----------38
3.1.1.1. General aspects---------------------------38
3.1.1.2. Clinical manifestations---------------38
3.1.1.3. Serotyping---------------------------39
3.1.1.4. Surface protein gene profile----------39
3.1.1.5. Antibiotic susceptibility-------------40
3.1.1.6. Repeat number of the rib gene---------------40
3.1.2. Epidemiology of GBS colonization on pregnant women----------------------------------41
3.1.2.1. General aspects-----------------------41
3.1.2.2. Serotyping------------------------------41
3.1.2.3. Surface protein gene profile----------41
3.1.2.4. Pilus typing-----------------------------42
3.1.2.5. Antibiotic susceptibility-------------42
3.1.2.6. Repeat number of the rib gene----------43
3.1.3. Correlation between invasive neonates, nonpregnant adults and pregnant women--------------------------------43

Part II GBS growth and survival in vitro-----------------44
3.2.1. General aspects--------------------------44
3.2.2. Growth rate in pH gradient----------44
3.2.3. Killing rate in pH gradient-------------44
3.2.4. Growth and survival in different media-----------45
3.2.4.1. In THB medium------------------------45
3.2.4.2. In M9YE medium-------------------45
3.2.4.3. In SVF medium------------------------46

Part III Biofilm formation of GBS-----------47
3.3.1. General aspects--------------------------47
3.3.2. Biofilm formation-----------------------47
3.3.2.1. Environmental factors affecting GBS biofilm formation---------------------------------47
3.3.2.1.1. pH-------------------------------47
3.3.2.1.2. Carbon source--------------------48
3.3.2.1.2.1. Glucose------------------------------48
3.3.2.1.2.2. Different carbon sources--------49
3.3.2.1.3. Growth medium---------------------50
3.3.2.1.4. Casamino acid (CA)----------------50
3.3.2.1.5. NaCl----------------------------------50
3.3.2.1.6. Inocula of culture-------------------51
3.3.2.1.7. Growth phase of culture-----------51
3.3.2.2. Metabolic activity---------------------52

Part IV Ultrastructure analysis of GBS biofilms-----------53
3.4.1. General aspects------------------------------53
3.4.2. SEM study---------------------------------53
3.4.3. AFM study----------------------------------53
3.4.3.1. General aspects---------------------------53
3.4.3.2. Mechanical force measurement-------------54
3.4.3.3. Topography scanning----------------54

Part V Investigation of biofilm formation in clinical isolates-------------------------------------56
3.5.1. General aspects-------------------------56
3.5.2. Screening of biofilm formation--------56
3.5.3. Serotype and biofilm formation-----------57
3.5.4. Pilus and biofilm formation------------57

CHAPTER 4 Discussion--------------------59
4.1. Epidemiology of GBS-------------------------59
4.2. GBS growth and survival in vitro---------62
4.3. Biofilm formation of GBS ---------------64
4.4. Ultrastructure analysis of GBS biofilm-----------68
4.5. Inveatigation of biofilm formation in clinical isolates----------------------------------------69

CHAPTER 5 Conclusion and Future Perspective-------------------------------------------71

References-----------------------------------------------------------------------------------------------------76
Tables-----------------------------------------------------------------------------------------------------------96
Figures----------------------------------------------------------------------------------------------------------99
Appendix-----------------------------------------------------------------------------------------------------128
List of original publications------------------------------------------------------------------------------132
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