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研究生：	曾進忠 Tseng, Chin-Chung
論文名稱：	宿主和大腸桿菌毒性因素在上泌尿道感染以及氣腫性腎盂腎炎致病角色之研究 The Roles of Host and Escherichia coli Virulence Factors in the Development of Upper Urinary Tract Infection and Emphysematous Pyelonephritis
指導教授：	吳俊忠 Wu, JiunnJong 黃建鐘 Huang, Jeng-Jong
學位類別：	博士 Doctor
系所名稱：	醫學院 - 臨床醫學研究所 Institute of Clinical Medicine
論文出版年：	2005
畢業學年度：	93
語文別：	英文
論文頁數：	115
中文關鍵詞：	大腸桿菌、泌尿道阻塞、毒性因素、泌尿道感染、宿主因素、同源性突變
外文關鍵詞：	emphysematous, virulence, E. coli, host factors, urinary tract infection
相關次數：	點閱：140 下載：1
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　　研究背景: 上泌尿道感染(急性腎臟感染)是造成人類罹病率及死亡率的重要原因之一，大腸桿菌則是上泌尿道感染最常見的菌種。許多的研究顯示造成泌尿道感染的大腸桿菌比從健康人分離出的大腸桿菌，帶有更多種的毒性相關因子。而在這些毒性因子中，有些與上泌尿道感染有顯著的相關性，如：P型繖毛，溶血素與嗜鐵因子等，其中以P型繖毛與上泌尿道感染的發生最為相關。P繖毛的頂端有黏著蛋白，可與泌尿道上皮細胞的受體相結合，而黏附於上皮細胞上；近年來發現P型繖毛上的黏著蛋白可分成三型，然而大腸桿菌的P繖毛黏著蛋白亞型及其它的繖毛或非繖毛性黏著蛋白，或是其他毒性因素在上泌尿道感染的致病角色仍不清楚，而且也很少有學者研究宿主致病因素與大腸桿菌毒性因素彼此間的相關性。
　　氣腫性腎盂腎炎是一種少見但嚴重的化膿壞死性急性腎臟感染，此病與其它急性腎盂腎炎不同之地方在於其有較嚴重的腎臟組織壞死而且併發氣體聚積在腎臟實質或腎周圍組織。我們曾對成大醫院十年內48位氣腫性腎盂腎炎的病例作單一醫院最大的回顧性臨床研究並發表於內科學重要雜誌-內科學檔案（Archies of Internal Medicine）上；而氣腫性腎盂腎炎的致病機轉，雖有學者提出不同的假設，然而因缺乏控制性研究來比較其宿主因素和其致病細菌之毒性因素與其它非氣腫性腎盂腎炎間之差異，所以其確定的致病機轉仍不清楚。
　　研究目的: (1) 找出與上泌尿道感染有關之宿主及大腸桿菌毒性因子；(2) 探討宿主易感因素與大腸桿菌毒性因素間的相關性；(3) 探討P繖毛黏著蛋白變異型中之第二型黏著蛋白基因與上泌尿道感染的相關性；(4) 將帶有P繖毛第二型型黏著蛋白基因之大腸桿菌加以突變，使其不表現P繖毛第二型黏著蛋白，比較野生株與突變株造成BALB/c老鼠的腎臟感染能力之差異，以探討其在上泌尿道感染的致病角色；(5) 研究氣腫性腎盂腎炎的宿主因素及細菌的致病因子。
　　研究方法: 我們收集由大腸桿菌造成泌尿道感染之病患，回顧其宿主因素，包括：年齡、性別、糖尿病史、免疫力是否低下和泌尿道是否有功能性或結構性的阻塞等因素。抽取致病菌株的染色體基因，設計具專一性探測某毒性基因的引子，以多聚合酶鏈反應的方式來偵測大腸桿菌毒性因素之存在與否。進一步比較上和下泌尿道感染菌株的毒性因素之差異，並將宿主因素納入考慮，作多重因子分析比較，以找出獨立之致病因子。而為了進一步證實大腸桿菌P繖毛第二型黏著蛋白在上泌尿道感染之致病角色，我們將帶有插入性突變之P繖毛第二型黏著蛋白基因之pCVD442自殺性質體送入致病性野生株細胞內，分別在含有安比西林(ampicillin)和5%的蔗糖培養液中進行兩次同源性基因交換，製造失去正常P繖毛第二型黏著蛋白基因及其蛋白表現之突變株，然後再比較野生株與突變株造成腎臟感染能力之差異。BALB/c老鼠的泌尿道上皮細胞已證實帶有P繖毛第二型黏著蛋白的受體，因此我們以BALB/c老鼠上行性泌尿道感染的模式作實驗。對於氣腫性腎盂腎炎致病機制之研究，比較氣腫性腎盂腎炎與非氣腫性腎盂腎炎間的宿主因素與大腸桿菌毒性因素之差異，並且比較造成氣腫性腎盂腎炎與非氣腫性腎盂腎炎之致病性大腸桿菌培養在含有不同濃度之葡萄糖，但未含其他醣類的厭氧培養液中，在培養24和48小時後的產氣量之差異。
　　研究結果: 大腸桿菌P繖毛第二型黏著蛋白基因是造成具有正常泌尿道患者發生上泌尿道感染的顯著危險因素，當病患的泌尿道有阻塞時此基因的重要性便相對下降。而泌尿道阻塞、糖尿病患者的血糖控制不良以及宿主免疫能力低下是與上泌尿道感染相關之三種宿主危險因素；當宿主有泌尿道阻塞或以上三項宿主危險因子中之兩項以上時，其致病性大腸桿菌帶有第二型P繖毛黏著蛋白的顯著性會降低；進一步的動物實驗結果顯示P繖毛第二型黏著蛋白突變株對老鼠腎臟的感染能力，在老鼠接受經由尿道將細菌送入膀胱後的第三天明顯低於野生株。對於氣腫性腎盂腎炎致病機制之研究顯示若宿主為糖尿病血糖控制不良者(醣化血色素大於11%)和有泌尿道阻塞併發水腎者為與氣腫性腎盂腎炎有關之兩項宿主因素；此外，氣腫性腎盂腎炎的致病大腸桿菌帶有iroN及usp基因的比例有顯著增加。在病菌之產氣能力方面，則無明顯的差異；但當培養液中之葡萄糖濃度上升至250 mg/dl時，不管是氣腫性腎盂腎炎或非氣腫性腎盂腎炎菌株的產氣量皆明顯大於含100 mg/dl及180 mg/dl的葡萄糖培養液。
　　結論: 宿主及細菌毒性因素為造成上泌尿道感染的危險因子，但在宿主有易感因子存在時，即使較不具毒性的菌株仍可能造成上泌尿道感染。大腸桿菌P繖毛第二型黏著蛋白確實可以強化細菌對腎臟感染的初期建立，而當阻斷大腸桿菌之P繖毛第二型黏著蛋白之正常表現時，其對腎臟感染的能力會受到影響。宿主為糖尿病血糖控制不良者，或有泌尿道阻塞併發水腎以及致病大腸桿菌帶有iroN或usp等毒性基因是造成氣腫性腎盂腎炎的危險因子。

　　Background: Upper urinary tract infection (UTI) is one of the major causes of morbidity and mortality for human. Escherichia coli is the most common pathogen for upper UTI. The putative virulence factors of E. coli include P-fimbriae, hemolysin and aerobactin; and the P-fimbriae is most frequently associated with upper UTI. The PapG adhesins at the tip of P-fimbriae mediate the binding with receptors on the uroepithelial cells. Recent studies have shown there are three variants of PapG adhesins. However, the roles of PapG adhesins subtypes, other fimbrial or non-fimbrial adhesins and toxins of E. coli in the development of upper UTI (i.e. acute renal infection ) are still unclear. In addition, only rare studies have examined these virulence factors concurrently with host factors that also may contribute to renal infection. Emphysematous pyelonephritis (EPN) is the most severe form of upper UTI. We have published a study on the clinical manifestations, radiological classification, pathogenesis, and outcome of EPN in “Archives of Internal Medicine”. However, there has been no control study of investigating the host and bacterial factors predisposing to the development of EPN and, thus, the precise pathogenesis remains obscure.
　　Aims: (1) to identify the host and E. coli virulence factors associated with upper UTI; (2) to investigate the interaction between host and E. coli virulence factors in upper UTI; (3) to investigate the association between P-fimbrial adhesin II (PapG II) and upper UTI; (4) to determine the role of PapG II adhesin in the development of upper UTI; (5) to identify the host and bacterial factors predisposing to the development of EPN.
　　Materials and Methods: Patients who fulfilled the diagnostic criteria for upper or lower UTI caused by E. coli were enrolled into this study. Availability of a stock of causative E. coli is prerequisite for inclusion. The prevalence of host factors and E. coli virulence factors was compared between lower and upper UTI groups. The prevalence of potential virulence genes of E. coli isolate was determined by polymerase chain reaction (PCR) method. To determine the importance of the papG II gene in the development of upper UTI, we constructed an isogenic mutant, deficient in PapG II adhesin phenotype, and compared the phenotypes of this mutant with its parental strain, a clinical isolate from a pyelonephritis patients, including its colonization ability in kidney in the ascending UTI model of BALB/c mouse. For investigation of the pathogenesis of EPN, we identified the host and bacterial factors by comparing with analogs in non-gas-forming renal infections (i.e. non-EPN) and determined the role of bacterial gas-producing capacity by comparison for the gas volumes produced by EPN and non-EPN E. coli strains, cultured in broths with different glucose concentrations.
　　Results: Diabetes with poor blood glucose control, immunosuppression, urinary tract obstruction, and papG II gene were independently associated with upper UTI. However, the papG II gene was less prevalent in strains isolated from patients with upper UTI with urinary tract obstruction or with two of the three predisposing host factors. The results of ascending BALB/c mice model of renal infection showed that the geometric means of quantitative bacterial counts in mice kidney were significantly decreased when challenged with mutant strain, which was mutated in the papG II gene, than with wild type strain on day 3 after inoculation, at both low and high inoculation dose (P < 0.05). The results of EPN pathogensis showed diabetic mellitus with poor glycemic control (i.e. HbA1C level > 11%) was the only host factor independently associated with EPN. Higher prevalence of the iroN and usp genes was demonstrated in the EPN strains. The gas volumes produced by E. coli were significantly increased only when the glucose concentrations of broths were elevated to 250 mg/dl in both groups.
　　Conclusion: This study contributes to a further understanding of the roles of hosts and bacterial factors in the pathogenesis of upper UTI and EPN. It demonstrated that both the hosts and bacterial factors can contribute to the development of upper UTI, and less virulent strains can cause upper UTI in hosts with predisposing factors. The papG II gene plays an important role in the development of upper UTI, and blocking the normal expression of papG II gene by mutation can inhibit the early establishment of E. coli in the kidney. Diabetes mellitus with poor glycemic control, major urinary tract obstruction, and more virulent strain are the factors predisposing to EPN.

English Abstract 1
中文摘要 4
General Introduction 7
Chapter 1. Host and E. coli virulence factors and their
interactions in the development of upper
urinary tract infection (UTI) 16
Introduction 16
Study objects 17
Materials and Methods 18
 Bacterial isolates 18
 Diagnostic criteria and patients selection 18
 Definition and classification of host factors   predisposing
to UTI 19
 Detection of E. coli virulence determinants 20
 PCR primers 20
 Amplification procedures 21
 Determination of nucleotide sequence 21
Results 22
 Influences of urinary tract abnormalities on the
 virulence characteristics of E. coli strains  causing upper UTI 22
 Comparisons of host and E. coli virulence factors
 between patients with upper and lower UTI 23
 Comparison of the Prevalence of papG II Gene of E. coli in upper and lower UTI patients with and
without predisposing host factors 25
 Host and bacterial factors associated with  bacteremia in patients with upper UTI 25
Discussion 26
Chapter 2. Role of PapG II adhesin in pathogenesis
of upper UTI : Isogenic papG II mutant
in mouse model of ascending renal
infection 34
Introduction 34
Study object 34
Materials and Methods 35
 Bacterial strains and media 35
 Determination of virulence genes 36
 Test for P-fimbrial phenotype 36
 DNA purification and transformation 36
 Construction of pMW353 containing papG II mutant 37
 Mating and selection of papG II mutant 37
 PCR analysis and nucleotide sequencing for PCR
 products 38
 Southern blot hybridization 39
 Complementation 40
 Mouse model of ascending UTI 40
 Histological examination 41
Results 42
 Selection of a strain for mutation 42
 Construction of pMW353 containing a papG II
 fragment with insertion mutation 43
 Construction of papG II insertion mutant 43
 Genetic analysis 43
 Phenotypes of the isogenic mutants 44
 Virulence in BALB/c mouse model of ascending UTI 44
 Results of Renal Biopsy 45
Discussion 46
Chapter 3. Host and E. coli virulence factors in the
development of EPN 50
Introduction 50
Study object s 50
Materials and Methods 51
 Patients 51
 Diagnostic criteria 51
 Definition and classification of host factors 52
 Bacterial isolates and detection of E. coli  virulence factors 52
 Comparison of gas production 53
Results 54
Discussion 55
Conclusions 59
Future work 60
References 61
Tables
Table 1. The sequences of primer pairs 74
Table 2. Comparisons of virulence factors of E. coli and underlying
medical diseases between upper UTI and Lower UTI
patients with a normal urinary tract 75
Table 3. Comparison of the prevalence of underlying medical
diseases and papG genes of E. coli between the three
groups of patients with Upper UTI 76
Table 4. Comparisons of host factors and urovirulence genes of E.
coli between patients with upper and lower UTI 77
Table 5. Comparisons of the prevalence of papG II gene of E. coli
in upper and lower UTI groups with and without
predisposing host factors 78
Table 6. Comparisons of host factors and E. coli virulence genes in
upper UTI groups with and without bacteremia 79
Table 7. Association of papG II gene of E. coli and predisposing
host factors in upper UTI patients with bacteremia 80
Table 8. Comparison of clinical characteristics in EPN and
non-EPN groups 81
Table 9. Comparison of host factors in EPN and non-EPN groups 82
Table 10. Comparisons of E. coli virulence genes in strains isolated
from EPN and non-EPN patients 83
Table 11. Comparisons of mean gas volumes for E. coli cultured in
different glucose broths for 24 and 48 h. 84
Figures
Figure 1. Electron micrography of E. coli fimbriae 85
Figure 2. Composition and subunits of P-fimbriae 86
Figure 3. The pap gene cluster 87
Figure 4. Construction of mutant papG II fragment 88
Figure 5. Construction of pMW353 89
Figure 6A. Mating and selection of papG II insertion mutants
(1st homologous recombination). 90
Figure 6B. Mating and selection of papG II insertion mutants
(2nd homologous recombination). 91
Figure 7. PCR analysis and southern hybridization test for
confirmation the insertion mutation in the papG II gene
of MEC114 92
Figure 8. Phenotype characteristics of wild type EC114, mutant
strain MEC114, and complementation strain 93
Figure 9. Rate of successful colonization and geometric means of
quantitative bacterial counts in BALB/c mice kidney 94
Figure 10. Rate of successful colonization and geometric means of
quantitative bacterial counts in BALB/c mice bladder 95
Figure 11. Renal pathological scores obtained from histological
evaluation of mice kidney 96
Figure 12. Histological examination of the mice kidney infected
with EC114 or MEC114 97
Curriculum vitae 98
                                    

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