Home A case of pulmonary embolism with bad warfarin anticoagulant effects caused by E. coli infection
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A case of pulmonary embolism with bad warfarin anticoagulant effects caused by E. coli infection

  • Weifeng Huang , Qingqing Cai , Yan Huo , Jin Tang , Yan Chen , Yuan Fang and Yihan Lu EMAIL logo
Published/Copyright: January 24, 2023
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Open Life Sciences
From the journal Open Life Sciences Volume 18 Issue 1

Abstract

Warfarin is an anticoagulant commonly used as an oral drug in preventing and treating thromboembolic diseases. The international normalized ratio (INR) is a clinical monitoring anticoagulation intensity index that adjusts the dose based on important references. In particular, INR value must be strictly monitored when warfarin is used for anticoagulation therapy in infected patients. Herein, we report a 54-year-old female patient diagnosed with pulmonary embolism and venous thrombosis of the lower limbs. After the warfarin administration, the INR was always substandard. The patient did not take other warfarin-interacting drugs or foods during the hospital stay. Metagenome next-generation sequencing suggested a bloodstream infection caused by Escherichia coli, which was further confirmed by blood culture. After meropenem administration for anti-infective treatment, the INR value rose rapidly to a standard level. Considering the lack of relevant reports, this case is the first report of potential interaction between E. coli and warfarin. Further, in patients with thromboembolic diseases complicated by infection, antibiotics should be chosen reasonably with close monitoring of the INR to avoid the interaction of warfarin and antibiotics and to ensure the effectiveness and safety of warfarin treatment.

Keywords: warfarin; anticoagulation; Escherichia coli ; infection; metagenomic next-generation sequencing

1 Introduction

Pulmonary embolism is a frequent cardiovascular disease. It is mainly a pathological syndrome of respiratory dysfunction. Ninety percent of the emboli in acute pulmonary embolism are venous thrombosis of the lower limbs. Pulmonary infection is the most common complication of pulmonary embolism [1,2]. Warfarin is an oral drug commonly used for preventing and treating thromboembolic diseases. It acts as an anticoagulant by inhibiting the activity of vitamin K oxidoreductase (VKOR) and inhibiting the mutual conversion of vitamin K and 2,3-epoxides [3]. The treatment window of this drug is relatively narrow, and excessive use can easily cause bleeding and other adverse reactions. The anticoagulant effect of warfarin may be affected by anti-infective agents in patients with thromboembolism and infection, such as ciprofloxacin and miconazole are highly likely to increase the anticoagulant effect of warfarin, thereby increasing the international normalized ratio (INR) value and the risk of bleeding in patients [4,5]. On the contrary, griseofulvin, nafcillin, ribavirin, and rifampicin may inhibit the anticoagulant effects of warfarin [6,7].

The interaction of warfarin with other drugs has been studied extensively and showed that carbapenem antibiotics (meropenem, imipenem) have little effect on the anticoagulant effect of warfarin without liver enzyme metabolization. Therefore, carbapenem is the antibiotic of choice in infectious patients who need to use warfarin [8,9]. There is no interaction with warfarin reported for meropenem that was used in the present case. Simultaneously, considering the lack of relevant data on the interaction between microorganisms and warfarin, the possibility of interaction between Escherichia coli and warfarin was explored in this case study.

2 Case presentation

The patient, a 54-year-old female, admitted to the hospital on May 26, was diagnosed with pulmonary embolism and venous thrombosis of the lower limbs mainly due to sudden shortness of breath and chest tightness for 1 day while getting up. Physical examination of the patient upon admission revealed no abnormalities. Pulmonary artery computed tomography angiography showed extensive embolisms in each branch of the two pulmonary arteries. Lower extremity color doppler ultrasound showed hypoechoic muscular venous plexus in both legs and possible thrombosis.

On admission, the patient was administered warfarin for thrombosis in the upper and lower pulmonary artery branches and between the calf muscles, and the INR was 1.13 (Figure 1). Meanwhile, as gene polymorphism significantly affects the dose of warfarin, among which CYP2C9 (1075 A > C rs1057910) and VKORC1 (1639G > A rs9923231) are the most significant [10,11], the key loci of CYP2C9 and VKORC1 genes were tested to guide warfarin administration. On the second day of admission (May 27), the INR was 1.06 (Figure 1), and the gene test results showed that the CYP2C9 activity of the patient was regular and the expression level of VKORC1 enzyme was decreased. According to the international warfarin pharmacogenomics consortium warfarin dose prediction model [12], we calculated the dose of warfarin, including load dose and maintenance dose: the patient was administered an initial 2-day dose of 6.25 mg, followed by a maintenance dose of 3.75 and 5.0 mg administered alternatively. Meanwhile, she was administered nadroparin 0.6 mL q12 h. In the following 2 days, the INR value of warfarin was still lower than 2.00, even after administering a higher dose of warfarin. Warfarin did not show the expected anticoagulant effect. To reduce the risk of bleeding and achieve an anticoagulant effect, the patient was administered nadroparin 0.6 mL q12 h and warfarin 5 mg q.d.

Figure 1 Timeline of this case and diagnostic workup. (a) The INR increases with the control of infection. (b) The timeline recorded essential events of the patient during hospitalization.
Figure 1

Timeline of this case and diagnostic workup. (a) The INR increases with the control of infection. (b) The timeline recorded essential events of the patient during hospitalization.

Worse still, 2 days after admission (May 29), the patient had a fever with a body temperature of 39.4°C (Figure 1). Blood cell analysis on May 29 showed a neutrophil ratio (NEU%) of 75.7% and C-reactive protein at 42.1 mg/mL (Figure 1), indicating infection based on the hemogram. Therefore, vulvar secretions, urine, and blood samples were collected and cultured, but the test results were all negative. In the next few days, the patient had persistent fever, accompanied by a poor anticoagulant effect (INR < 2.00) (Figure 1). On May 31, routine blood testing showed that the percentage of human neutrophils increased to 83.5%, still indicating apparent infection. The culture smears of peripheral blood were then obtained for a second time and metagenomic next-generation sequencing (mNGS) was performed. E. coli was detected in the peripheral blood in mNGS (242 unique reads) (Figure 2). Then, meropenem (1 g q8 h) was administered as an empirical anti-infective therapy on June 1 for 4 days. E. coli was detected in the blood culture on June 4, and a bloodstream infection caused by E. coli was confirmed.

Figure 2 Data from mNGS. The location of the detected nucleic acid sequences of E. coli in blood, which yielded a total coverage of 7.2%.
Figure 2

Data from mNGS. The location of the detected nucleic acid sequences of E. coli in blood, which yielded a total coverage of 7.2%.

After starting meropenem treatment with warfarin, with the neutrophils and C-reactive protein levels of the patient returned to normal levels, the INR value of the patients also increased gradually from 1.36 (June 1) to 2.11, maintaining the best anticoagulant effect of warfarin on June 4 (Figure 1). After excluding the interaction between warfarin and the drugs or food used during hospitalization, interaction with E. coli infection was speculated to cause a decrease in the anticoagulant effect of warfarin, indicated by a reduction in the INR of patients.

  1. Informed consent: Informed consent has been obtained from all individuals included in this study.

  2. Ethical approval: The research related to human use has been complied with all the relevant national regulations, institutional policies and in accordance the tenets of the Helsinki Declaration, and has been approved by the authors’ institutional review board or equivalent committee.

3 Discussion

In this case, a 54-year-old female patient with pulmonary embolism and venous thrombosis of the lower limbs was treated with warfarin; while, at the recommended dose, the anticoagulant effect of warfarin was poor. During this period, the patient showed fever symptoms, and the mNGS and the blood culture results revealed E. coli bloodstream infection. Meropenem was immediately used as anti-infective treatment along with warfarin for 4 days. After starting meropenem, the INR increased from 1.36 to 2.11. The INR remained at approximately 2.00 after the infection index decreased and after stopping the meropenem used, indicating a time correlation between the efficacy of meropenem and INR. The time in the therapeutic range (TTR) can reflect the quality of anticoagulation of warfarin in clinical practice. A study predicted that a TTR of 58% would be considered as beneficial for anticoagulation treatment [13]. In this case, a TTR of 35.7% according to the Rosendaal method [14] was relatively low, indicating the poor anticoagulation effect of warfarin, which could be caused by the accompanied infectious condition.

In this case, under the suggestion of personal medication, the expected anticoagulation effect was not achieved until meropenem was used along with warfarin. The anticoagulant effect of warfarin and the side effects of bleeding are mainly caused by many factors such as disease, dietary vitamin K intake, genetic factors, and drugs [5,15–18]. Other factors that could affect the efficacy and pharmacokinetics of warfarin except for infection could be excluded, and no data indicate that meropenem is related to the enhanced anticoagulant effect of warfarin. Therefore, the interaction between E. coli infection and warfarin was speculated to inhibit the anticoagulant effect of warfarin.

Vitamin K antagonists such as warfarin have been applied in the anticoagulation treatment of thrombosis diseases for decades. In recent years, direct oral anticoagulants (DOACs), including rivaroxaban, edoxaban, apixaban, and dabigatran, have been developed to offer efficient anticoagulation [19–23], and have been increasingly applied in the clinical management of thrombosis diseases. However, in patients with severe renal insufficiency or inability to cover the costs of DOACs, warfarin remains a critical option for treatment. In our country, due to the relatively high price of DOACs, warfarin is still the first choice of anticoagulation treatment and DOACs would be applied in the conditions of warfarin intolerance.

Warfarin acts as an anticoagulant by inhibiting the activity of VKOR in human bodies. VKOR homologues are also found in some bacteria. It is reported that warfarin can inhibit the growth of customarily conjugated mycobacteria after VKOR knockout in mycobacteria, and inhibit bacterial disulfide bond formation [24]. Thus, the homolog of bacterial VKOR may be the target of warfarin. Disulfide bond formation protein B (DsbB) is necessary for the formation of disulfide bonds in E. coli. Follow-up studies have shown that DsbB and VKOR expressed by E. coli have no apparent homology at the primary sequence level. Still, both can catalyze the formation of disulfide bonds, a structure of the bacterial homolog of vitamin K epoxide reductase [25]. Therefore, we speculated that the DsbB protein expressed in E. coli has an antagonistic effect similar to that of VKORC1. During warfarin use, the DsbB protein expressed by E. coli in the patient’s blood may have interacted with warfarin, resulting in a low INR in the patient.

To further explore whether the interaction exist between warfarin and E. coli, the whole genome of the clinical isolates of E. coli obtained from the patient’s blood culture was sequenced. After the DsbB gene was sequenced, the protein structures of DsbB and VKORC1 were predicted. Although they both possess oxidoreductase activity, the result shows that the similarity of the three-dimensional structure between DsbB and VKORC1 is low (Figure A1). Further experiments like the competitive binding of the VKORC1 protein and E. coli with warfarin are needed to directly verify whether E. coli can interact with warfarin. Simultaneously, substances interacting with E. coli can be determined by combining a proteomics approach.

To conclude, this case was the first to suggest that E. coli infection may interact with warfarin. The use of warfarin is complicated because of its narrow treatment window, considerable individual differentiation, and interaction with many foods, drugs, and diseases, thus requiring close monitoring. So when patients are in thromboembolic conditions complicated by infection, we should closely monitor the INR to apply the proper dose of warfarin and to prevent the influence of pathogenic microorganisms on warfarin.

  1. Funding information: This work was supported by the Shanghai Three-year Action Plan (2020–2022) for Public Health (Grant No. GWV-10.1-XK03), Science and Technology Commission of Shanghai Municipality (Grant No. 20Y11901000), and Shanghai Municipal Health Commission (Project No. 202140105).

  2. Author contributions: W.H. was responsible for the idea conception, study design, and manuscript writing. Q.C. contributed to data analysis. Y.H., J.T., and Y.C. collected the clinical information of the patient and contributed to the study selection. Y.F. drafted the manuscript. Y.L. conceived this study, drafted the manuscript text and revised the finalized manuscript. All authors read and approved the final manuscript.

  3. Conflict of interest: Authors state no conflict of interest.

  4. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Appendix

Figure A1 Three-dimensional structure of VKORC1 and DsBb. The similarity of the three-dimensional structure between DsbB and VKORC1 is low. The whole genome of the clinical E. coli isolate obtained from the patient’s blood culture was sequenced, and the result showed a DsbB gene on the genome.
Figure A1

Three-dimensional structure of VKORC1 and DsBb. The similarity of the three-dimensional structure between DsbB and VKORC1 is low. The whole genome of the clinical E. coli isolate obtained from the patient’s blood culture was sequenced, and the result showed a DsbB gene on the genome.

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Received: 2022-08-03
Revised: 2022-10-25
Accepted: 2022-11-23
Published Online: 2023-01-24

© 2023 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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  266. Erratum
  267. Erratum to “Protein Z modulates the metastasis of lung adenocarcinoma cells”
  268. Erratum to “BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells”
  269. Retraction
  270. Retraction to “Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats”
https://doi.org/10.1515/biol-2022-0539
Keywords for this article
warfarin; anticoagulation; Escherichia coli; infection; metagenomic next-generation sequencing
Creative Commons
BY 4.0

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  173. Acute lupus pneumonitis resembling miliary tuberculosis: A case-based review
  174. Plasma levels of CD36 and glutathione as biomarkers for ruptured intracranial aneurysm
  175. Fractalkine modulates pulmonary angiogenesis and tube formation by modulating CX3CR1 and growth factors in PVECs
  176. Novel risk prediction models for deep vein thrombosis after thoracotomy and thoracoscopic lung cancer resections, involving coagulation and immune function
  177. Exploring the diagnostic markers of essential tremor: A study based on machine learning algorithms
  178. Evaluation of effects of small-incision approach treatment on proximal tibia fracture by deep learning algorithm-based magnetic resonance imaging
  179. An online diagnosis method for cancer lesions based on intelligent imaging analysis
  180. Medical imaging in rheumatoid arthritis: A review on deep learning approach
  181. Predictive analytics in smart healthcare for child mortality prediction using a machine learning approach
  182. Utility of neutrophil–lymphocyte ratio and platelet–lymphocyte ratio in predicting acute-on-chronic liver failure survival
  183. A biomedical decision support system for meta-analysis of bilateral upper-limb training in stroke patients with hemiplegia
  184. TNF-α and IL-8 levels are positively correlated with hypobaric hypoxic pulmonary hypertension and pulmonary vascular remodeling in rats
  185. Stochastic gradient descent optimisation for convolutional neural network for medical image segmentation
  186. Comparison of the prognostic value of four different critical illness scores in patients with sepsis-induced coagulopathy
  187. Application and teaching of computer molecular simulation embedded technology and artificial intelligence in drug research and development
  188. Hepatobiliary surgery based on intelligent image segmentation technology
  189. Value of brain injury-related indicators based on neural network in the diagnosis of neonatal hypoxic-ischemic encephalopathy
  190. Analysis of early diagnosis methods for asymmetric dementia in brain MR images based on genetic medical technology
  191. Early diagnosis for the onset of peri-implantitis based on artificial neural network
  192. Clinical significance of the detection of serum IgG4 and IgG4/IgG ratio in patients with thyroid-associated ophthalmopathy
  193. Forecast of pain degree of lumbar disc herniation based on back propagation neural network
  194. SPA-UNet: A liver tumor segmentation network based on fused multi-scale features
  195. Systematic evaluation of clinical efficacy of CYP1B1 gene polymorphism in EGFR mutant non-small cell lung cancer observed by medical image
  196. Rehabilitation effect of intelligent rehabilitation training system on hemiplegic limb spasms after stroke
  197. A novel approach for minimising anti-aliasing effects in EEG data acquisition
  198. ErbB4 promotes M2 activation of macrophages in idiopathic pulmonary fibrosis
  199. Clinical role of CYP1B1 gene polymorphism in prediction of postoperative chemotherapy efficacy in NSCLC based on individualized health model
  200. Lung nodule segmentation via semi-residual multi-resolution neural networks
  201. Evaluation of brain nerve function in ICU patients with Delirium by deep learning algorithm-based resting state MRI
  202. A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis
  203. Markov model combined with MR diffusion tensor imaging for predicting the onset of Alzheimer’s disease
  204. Effectiveness of the treatment of depression associated with cancer and neuroimaging changes in depression-related brain regions in patients treated with the mediator-deuterium acupuncture method
  205. Molecular mechanism of colorectal cancer and screening of molecular markers based on bioinformatics analysis
  206. Monitoring and evaluation of anesthesia depth status data based on neuroscience
  207. Exploring the conformational dynamics and thermodynamics of EGFR S768I and G719X + S768I mutations in non-small cell lung cancer: An in silico approaches
  208. Optimised feature selection-driven convolutional neural network using gray level co-occurrence matrix for detection of cervical cancer
  209. Incidence of different pressure patterns of spinal cerebellar ataxia and analysis of imaging and genetic diagnosis
  210. Pathogenic bacteria and treatment resistance in older cardiovascular disease patients with lung infection and risk prediction model
  211. Adoption value of support vector machine algorithm-based computed tomography imaging in the diagnosis of secondary pulmonary fungal infections in patients with malignant hematological disorders
  212. From slides to insights: Harnessing deep learning for prognostic survival prediction in human colorectal cancer histology
  213. Ecology and Environmental Science
  214. Monitoring of hourly carbon dioxide concentration under different land use types in arid ecosystem
  215. Comparing the differences of prokaryotic microbial community between pit walls and bottom from Chinese liquor revealed by 16S rRNA gene sequencing
  216. Effects of cadmium stress on fruits germination and growth of two herbage species
  217. Bamboo charcoal affects soil properties and bacterial community in tea plantations
  218. Optimization of biogas potential using kinetic models, response surface methodology, and instrumental evidence for biodegradation of tannery fleshings during anaerobic digestion
  219. Understory vegetation diversity patterns of Platycladus orientalis and Pinus elliottii communities in Central and Southern China
  220. Studies on macrofungi diversity and discovery of new species of Abortiporus from Baotianman World Biosphere Reserve
  221. Food Science
  222. Effect of berrycactus fruit (Myrtillocactus geometrizans) on glutamate, glutamine, and GABA levels in the frontal cortex of rats fed with a high-fat diet
  223. Guesstimate of thymoquinone diversity in Nigella sativa L. genotypes and elite varieties collected from Indian states using HPTLC technique
  224. Analysis of bacterial community structure of Fuzhuan tea with different processing techniques
  225. Untargeted metabolomics reveals sour jujube kernel benefiting the nutritional value and flavor of Morchella esculenta
  226. Mycobiota in Slovak wine grapes: A case study from the small Carpathians wine region
  227. Elemental analysis of Fadogia ancylantha leaves used as a nutraceutical in Mashonaland West Province, Zimbabwe
  228. Microbiological transglutaminase: Biotechnological application in the food industry
  229. Influence of solvent-free extraction of fish oil from catfish (Clarias magur) heads using a Taguchi orthogonal array design: A qualitative and quantitative approach
  230. Chromatographic analysis of the chemical composition and anticancer activities of Curcuma longa extract cultivated in Palestine
  231. The potential for the use of leghemoglobin and plant ferritin as sources of iron
  232. Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM
  233. Bioengineering and Biotechnology
  234. Biocompatibility and osteointegration capability of β-TCP manufactured by stereolithography 3D printing: In vitro study
  235. Clinical characteristics and the prognosis of diabetic foot in Tibet: A single center, retrospective study
  236. Agriculture
  237. Biofertilizer and NPSB fertilizer application effects on nodulation and productivity of common bean (Phaseolus vulgaris L.) at Sodo Zuria, Southern Ethiopia
  238. On correlation between canopy vegetation and growth indexes of maize varieties with different nitrogen efficiencies
  239. Exopolysaccharides from Pseudomonas tolaasii inhibit the growth of Pleurotus ostreatus mycelia
  240. A transcriptomic evaluation of the mechanism of programmed cell death of the replaceable bud in Chinese chestnut
  241. Melatonin enhances salt tolerance in sorghum by modulating photosynthetic performance, osmoregulation, antioxidant defense, and ion homeostasis
  242. Effects of plant density on alfalfa (Medicago sativa L.) seed yield in western Heilongjiang areas
  243. Identification of rice leaf diseases and deficiency disorders using a novel DeepBatch technique
  244. Artificial intelligence and internet of things oriented sustainable precision farming: Towards modern agriculture
  245. Animal Sciences
  246. Effect of ketogenic diet on exercise tolerance and transcriptome of gastrocnemius in mice
  247. Combined analysis of mRNA–miRNA from testis tissue in Tibetan sheep with different FecB genotypes
  248. Isolation, identification, and drug resistance of a partially isolated bacterium from the gill of Siniperca chuatsi
  249. Tracking behavioral changes of confined sows from the first mating to the third parity
  250. The sequencing of the key genes and end products in the TLR4 signaling pathway from the kidney of Rana dybowskii exposed to Aeromonas hydrophila
  251. Development of a new candidate vaccine against piglet diarrhea caused by Escherichia coli
  252. Plant Sciences
  253. Crown and diameter structure of pure Pinus massoniana Lamb. forest in Hunan province, China
  254. Genetic evaluation and germplasm identification analysis on ITS2, trnL-F, and psbA-trnH of alfalfa varieties germplasm resources
  255. Tissue culture and rapid propagation technology for Gentiana rhodantha
  256. Effects of cadmium on the synthesis of active ingredients in Salvia miltiorrhiza
  257. Cloning and expression analysis of VrNAC13 gene in mung bean
  258. Chlorate-induced molecular floral transition revealed by transcriptomes
  259. Effects of warming and drought on growth and development of soybean in Hailun region
  260. Effects of different light conditions on transient expression and biomass in Nicotiana benthamiana leaves
  261. Comparative analysis of the rhizosphere microbiome and medicinally active ingredients of Atractylodes lancea from different geographical origins
  262. Distinguish Dianthus species or varieties based on chloroplast genomes
  263. Comparative transcriptomes reveal molecular mechanisms of apple blossoms of different tolerance genotypes to chilling injury
  264. Study on fresh processing key technology and quality influence of Cut Ophiopogonis Radix based on multi-index evaluation
  265. An advanced approach for fig leaf disease detection and classification: Leveraging image processing and enhanced support vector machine methodology
  266. Erratum
  267. Erratum to “Protein Z modulates the metastasis of lung adenocarcinoma cells”
  268. Erratum to “BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells”
  269. Retraction
  270. Retraction to “Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats”
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