Bacteremia

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Bacteremia
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Bacteremia (also bacteraemia) is the presence of bacteria in the blood. Blood is normally a sterile environment, [1] so the detection of bacteria in the blood (most commonly accomplished by blood cultures [2] ) is always abnormal. It is distinct from sepsis, which is the host response to the bacteria. [3]

Contents

Bacteria can enter the bloodstream as a severe complication of infections (like pneumonia or meningitis), during surgery (especially when involving mucous membranes such as the gastrointestinal tract), or due to catheters and other foreign bodies entering the arteries or veins (including during intravenous drug abuse). [4] Transient bacteremia can result after dental procedures or brushing of teeth. [5]

Bacteremia can have several important health consequences. The immune response to the bacteria can cause sepsis and septic shock, which has a high mortality rate. [6] Bacteria can also spread via the blood to other parts of the body (which is called hematogenous spread), causing infections away from the original site of infection, such as endocarditis or osteomyelitis. [7] Treatment for bacteremia is with antibiotics, and prevention with antibiotic prophylaxis can be given in high risk situations. [8]

Presentation

Bacteremia is typically transient and is quickly removed from the blood by the immune system. [5]

Bacteremia frequently evokes a response from the immune system called Sepsis, which consists of symptoms such as fever, chills, and hypotension. [9] Severe immune responses to bacteremia may result in septic shock and multiple organ dysfunction syndrome , [9] which are potentially fatal.

Causes

Bacteria can enter the bloodstream in a number of different ways. However, for each major classification of bacteria (gram negative, gram positive, or anaerobic) there are characteristic sources or routes of entry into the bloodstream that lead to bacteremia. Causes of bacteremia can additionally be divided into healthcare-associated (acquired during the process of receiving care in a healthcare facility) or community-acquired (acquired outside of a health facility, often prior to hospitalization).

Gram positive bacteremia

Gram positive bacteria are an increasingly important cause of bacteremia. [10] Staphylococcus, streptococcus, and enterococcus species are the most important and most common species of gram-positive bacteria that can enter the bloodstream. These bacteria are normally found on the skin or in the gastrointestinal tract.

Staphylococcus aureus is the most common cause of healthcare-associated bacteremia in North and South America and is also an important cause of community-acquired bacteremia. [11] Skin ulceration or wounds, respiratory tract infections, and IV drug use are the most important causes of community-acquired staph aureus bacteremia. In healthcare settings, intravenous catheters, urinary tract catheters, and surgical procedures are the most common causes of staph aureus bacteremia. [12]

There are many different types of streptococcal species that can cause bacteremia. Group A streptococcus (GAS) typically causes bacteremia from skin and soft tissue infections. [13] Group B streptococcus is an important cause of bacteremia in neonates, often immediately following birth. [14] Viridans streptococci species are normal bacterial flora of the mouth. Viridans strep can cause temporary bacteremia after eating, toothbrushing, or flossing. [14] More severe bacteremia can occur following dental procedures or in patients receiving chemotherapy. [14] Finally, streptococcus bovis is a common cause of bacteremia in patients with colon cancer. [15]

Enterococci are an important cause of healthcare-associated bacteremia. These bacteria commonly live in the gastrointestinal tract and female genital tract. Intravenous catheters, urinary tract infections and surgical wounds are all risk factors for developing bacteremia from enterococcal species. [16] Resistant enterococcal species can cause bacteremia in patients who have had long hospital stays or frequent antibiotic use in the past. [17]

Gram negative bacteremia

Gram negative bacterial species are responsible for approximately 24% of all cases of healthcare-associated bacteremia and 45% of all cases of community-acquired bacteremia. [18] [19] In general, gram negative bacteria enter the bloodstream from infections in the respiratory tract, genitourinary tract, gastrointestinal tract, or hepatobiliary system. Gram-negative bacteremia occurs more frequently in elderly populations (65 years or older) and is associated with higher morbidity and mortality in this population. [20]

E.coli is the most common cause of community-acquired bacteremia accounting for approximately 75% of cases. [21] E.coli bacteremia is usually the result of a urinary tract infection. Other organisms that can cause community-acquired bacteremia include Pseudomonas aeruginosa , Klebsiella pneumoniae , and Proteus mirabilis . Salmonella infection, despite mainly only resulting in gastroenteritis in the developed world, is a common cause of bacteremia in Africa. [22] It principally affects children who lack antibodies to Salmonella and HIV+ patients of all ages.

Among healthcare-associated cases of bacteremia, gram negative organisms are an important cause of bacteremia in the ICU. [23] Catheters in the veins, arteries, or urinary tract can all create a way for gram negative bacteria to enter the bloodstream. [13] Surgical procedures of the genitourinary tract, intestinal tract, or hepatobiliary tract can also lead to gram negative bacteremia. [13] Pseudomonas and Enterobacter species are the most important causes of gram negative bacteremia in the ICU. [23]

Bacteremia risk factors

There are several risk factors that increase the likelihood of developing bacteremia from any type of bacteria. [10] [24] These include:

Mechanism

Bacteremia can travel through the blood stream to distant sites in the body and cause infection (hematogenous spread). Hematogenous spread of bacteria is part of the pathophysiology of certain infections of the heart (endocarditis), structures around the brain (meningitis), and tuberculosis of the spine (Pott's disease). Hematogenous spread of bacteria is responsible for many bone infections (osteomyelitis). [26]

Prosthetic cardiac implants (for example artificial heart valves) are especially vulnerable to infection from bacteremia. [27]

Prior to widespread use of vaccines, occult bacteremia was an important consideration in febrile children that appeared otherwise well. [28]

Diagnosis

Bacteremia is most commonly diagnosed by blood culture, in which a sample of blood drawn from the vein by needle puncture is allowed to incubate with a medium that promotes bacterial growth. [29] If bacteria are present in the bloodstream at the time the sample is obtained, the bacteria will multiply and can thereby be detected.

Any bacteria that incidentally find their way to the culture medium will also multiply. For example, if the skin is not adequately cleaned before needle puncture, contamination of the blood sample with normal bacteria that live on the surface of the skin can occur. [30] For this reason, blood cultures must be drawn with great attention to sterile process. The presence of certain bacteria in the blood culture, such as Staphylococcus aureus, Streptococcus pneumoniae , and Escherichia coli almost never represent a contamination of the sample. On the other hand, contamination may be more highly suspected if organisms like Staphylococcus epidermidis or Cutibacterium acnes grow in the blood culture.

Two blood cultures drawn from separate sites of the body are often sufficient to diagnose bacteremia. [30] Two out of two cultures growing the same type of bacteria usually represents a real bacteremia, particularly if the organism that grows is not a common contaminant. [30] One out of two positive cultures will usually prompt a repeat set of blood cultures to be drawn to confirm whether a contaminant or a real bacteremia is present. [30] The patient's skin is typically cleaned with an alcohol-based product prior to drawing blood to prevent contamination. [30] Blood cultures may be repeated at intervals to determine if persistent — rather than transient — bacteremia is present. [30]

Prior to drawing blood cultures, a thorough patient history should be taken with particular regard to presence of both fevers and chills, other focal signs of infection such as in the skin or soft tissue, a state of immunosuppression, or any recent invasive procedures. [29]

Ultrasound of the heart is recommended in all those with bacteremia due to Staphylococcus aureus to rule out infectious endocarditis. [31]

Definition

Bacteremia is the presence of bacteria in the bloodstream that are alive and capable of reproducing. It is a type of bloodstream infection. [32] Bacteremia is defined as either a primary or secondary process. In primary bacteremia, bacteria have been directly introduced into the bloodstream. [33] Injection drug use may lead to primary bacteremia. In the hospital setting, use of blood vessel catheters contaminated with bacteria may also lead to primary bacteremia. [34] Secondary bacteremia occurs when bacteria have entered the body at another site, such as the cuts in the skin, or the mucous membranes of the lungs (respiratory tract), mouth or intestines (gastrointestinal tract), bladder (urinary tract), or genitals. [35] Bacteria that have infected the body at these sites may then spread into the lymphatic system and gain access to the bloodstream, where further spread can occur. [36]

Bacteremia may also be defined by the timing of bacteria presence in the bloodstream: transient, intermittent, or persistent. In transient bacteremia, bacteria are present in the bloodstream for minutes to a few hours before being cleared from the body, and the result is typically harmless in healthy people. [37] This can occur after manipulation of parts of the body normally colonized by bacteria, such as the mucosal surfaces of the mouth during teeth brushing, flossing, or dental procedures, [38] or instrumentation of the bladder or colon. [32] Intermittent bacteremia is characterized by periodic seeding of the same bacteria into the bloodstream by an existing infection elsewhere in the body, such as an abscess, pneumonia, or bone infection, followed by clearing of that bacteria from the bloodstream. This cycle will often repeat until the existing infection is successfully treated. [32] Persistent bacteremia is characterized by the continuous presence of bacteria in the bloodstream. [32] It is usually the result of an infected heart valve, a central line-associated bloodstream infection (CLABSI), an infected blood clot (suppurative thrombophlebitis), or an infected blood vessel graft. [32] Persistent bacteremia can also occur as part of the infection process of typhoid fever, brucellosis, and bacterial meningitis. Left untreated, conditions causing persistent bacteremia can be potentially fatal. [14]

Bacteremia is clinically distinct from sepsis, which is a condition where the blood stream infection is associated with an inflammatory response from the body, often causing abnormalities in body temperature, heart rate, breathing rate, blood pressure, and white blood cell count. [39]

Treatment

The presence of bacteria in the blood almost always requires treatment with antibiotics. This is because there are high mortality rates from progression to sepsis if antibiotics are delayed. [23]

The treatment of bacteremia should begin with empiric antibiotic coverage. Any patient presenting with signs or symptoms of bacteremia or a positive blood culture should be started on intravenous antibiotics. [20] The choice of antibiotic is determined by the most likely source of infection and by the characteristic organisms that typically cause that infection. Other important considerations include the patient's past history of antibiotic use, the severity of the presenting symptoms, and any allergies to antibiotics. [40] Empiric antibiotics should be narrowed, preferably to a single antibiotic, once the blood culture returns with a particular bacteria that has been isolated. [40]

Gram positive bacteremia

The Infectious Disease Society of America (IDSA) recommends treating uncomplicated methicillin resistant staph aureus (MRSA) bacteremia with a 14-day course of intravenous vancomycin. [41] Uncomplicated bacteremia is defined as having positive blood cultures for MRSA, but having no evidence of endocarditis, no implanted prostheses, negative blood cultures after 2–4 days of treatment, and signs of clinical improvement after 72 hrs. [41]

The antibiotic treatment of choice for streptococcal and enteroccal infections differs by species. However, it is important to look at the antibiotic resistance pattern for each species from the blood culture to better treat infections caused by resistant organisms. [10]

Gram negative bacteremia

The treatment of gram negative bacteremia is also highly dependent on the causative organism. Empiric antibiotic therapy should be guided by the most likely source of infection and the patient's past exposure to healthcare facilities. [42] In particular, a recent history of exposure to a healthcare setting may necessitate the need for antibiotics with pseudomonas aeruginosa coverage or broader coverage for resistant organisms. [42] Extended generation cephalosporins such as ceftriaxone or beta lactam/beta lactamase inhibitor antibiotics such as piperacillin-tazobactam are frequently used for the treatment of gram negative bacteremia. [42]

Catheter-associated infections

For healthcare-associated bacteremia due to intravenous catheters, the IDSA has published guidelines for catheter removal. Short term catheters (in place <14 days) should be removed if bacteremia is caused by any gram negative bacteria, staph aureus, enterococci or mycobacteria. [43] Long term catheters (>14 days) should be removed if the patient is developing signs or symptoms of sepsis or endocarditis, or if blood cultures remain positive for more than 72 hours. [43]

See also

Related Research Articles

Lemierres syndrome Human disease: infectious thrombophlebitis of the internal jugular vein

Lemierre's syndrome refers to infectious thrombophlebitis of the internal jugular vein. It most often develops as a complication of a bacterial sore throat infection in young, otherwise healthy adults. The thrombophlebitis is a serious condition and may lead to further systemic complications such as bacteria in the blood or septic emboli.

<i>Staphylococcus aureus</i> Species of Gram-positive bacterium

Staphylococcus aureus is a Gram-positive, round-shaped bacterium that is a member of the Firmicutes, and it is a usual member of the microbiota of the body, frequently found in the upper respiratory tract and on the skin. It is often positive for catalase and nitrate reduction and is a facultative anaerobe that can grow without the need for oxygen. Although S. aureus usually acts as a commensal of the human microbiota it can also become an opportunistic pathogen, being a common cause of skin infections including abscesses, respiratory infections such as sinusitis, and food poisoning. Pathogenic strains often promote infections by producing virulence factors such as potent protein toxins, and the expression of a cell-surface protein that binds and inactivates antibodies. The emergence of antibiotic-resistant strains of S. aureus such as methicillin-resistant S. aureus (MRSA) is a worldwide problem in clinical medicine. Despite much research and development, no vaccine for S. aureus has been approved.

Sepsis Life-threatening organ dysfunction triggered by infection

Sepsis is a life-threatening condition that arises when the body's response to infection causes injury to its tissues and organs. This initial stage is followed by suppression of the immune system. Common signs and symptoms include fever, increased heart rate, increased breathing rate, and confusion. There may also be symptoms related to a specific infection, such as a cough with pneumonia, or painful urination with a kidney infection. The very young, old, and people with a weakened immune system may have no symptoms of a specific infection, and the body temperature may be low or normal instead of having a fever. Severe sepsis is sepsis causing poor organ function or blood flow. The presence of low blood pressure, high blood lactate, or low urine output may suggest poor blood flow. Septic shock is low blood pressure due to sepsis that does not improve after fluid replacement.

Methicillin-resistant <i>Staphylococcus aureus</i> Bacterium responsible for difficult-to-treat infections in humans

Methicillin-resistant Staphylococcus aureus (MRSA) refers to a group of Gram-positive bacteria that are genetically distinct from other strains of Staphylococcus aureus. MRSA is responsible for several difficult-to-treat infections in humans. MRSA is any strain of S. aureus that has developed, through horizontal gene transfer and natural selection, multiple drug resistance to beta-lactam antibiotics. Beta-lactam (β-lactam) antibiotics are a broad-spectrum group that include some penams and cephems such as the cephalosporins. Strains unable to resist these antibiotics are classified as methicillin-susceptible S. aureus, or MSSA.

<i>Klebsiella pneumoniae</i> Species of bacterium

Klebsiella pneumoniae is a Gram-negative, non-motile, encapsulated, lactose-fermenting, facultative anaerobic, rod-shaped bacterium. It appears as a mucoid lactose fermenter on MacConkey agar.

Septic arthritis arthritis that involves infection by a pathogen located in joint syaptic

Septic arthritis, also known as joint infection or infectious arthritis, is the invasion of a joint by an infectious agent resulting in joint inflammation. Symptoms typically include redness, heat and pain in a single joint associated with a decreased ability to move the joint. Onset is usually rapid. Other symptoms may include fever, weakness and headache. Occasionally, more than one joint may be involved.

Infective endocarditis endocarditis that is characterized by inflammation of the endocardium caused by infectious agents.

Infective endocarditis is an infection of the inner surface of the heart, usually the valves. Symptoms may include fever, small areas of bleeding into the skin, heart murmur, feeling tired, and low red blood cell count. Complications may include backward blood flow in the heart, the heart struggling to pump a sufficient amount of blood to meet the body's needs, abnormal electrical conduction in the heart, stroke, and kidney failure.

Osteomyelitis bone inflammation disease that has material basis in infection located in bone or located in bone marrow

Osteomyelitis (OM) is an infection of bone. Symptoms may include pain in a specific bone with overlying redness, fever, and weakness. The long bones of the arms and legs are most commonly involved in children, while the feet, spine, and hips are most commonly involved in adults.

Cefazolin chemical compound

Cefazolin, also known as cefazoline and cephazolin, is an antibiotic used for the treatment of a number of bacterial infections. Specifically it is used to treat cellulitis, urinary tract infections, pneumonia, endocarditis, joint infection, and biliary tract infections. It is also used to prevent group B streptococcal disease around the time of delivery and before surgery. It is typically given by injection into a muscle or vein.

Hospital-acquired infection Infection that is acquired in a hospital or other health care facility

A hospital-acquired infection (HAI), also known as a nosocomial infection, is an infection that is acquired in a hospital or other health care facility. To emphasize both hospital and nonhospital settings, it is sometimes instead called a health care–associated infection. Such an infection can be acquired in hospital, nursing home, rehabilitation facility, outpatient clinic, diagnostic laboratory or other clinical settings. Infection is spread to the susceptible patient in the clinical setting by various means. Health care staff also spread infection, in addition to contaminated equipment, bed linens, or air droplets. The infection can originate from the outside environment, another infected patient, staff that may be infected, or in some cases, the source of the infection cannot be determined. In some cases the microorganism originates from the patient's own skin microbiota, becoming opportunistic after surgery or other procedures that compromise the protective skin barrier. Though the patient may have contracted the infection from their own skin, the infection is still considered nosocomial since it develops in the health care setting.

<i>Haemophilus influenzae</i> Species of bacterium

Haemophilus influenzae is a Gram-negative, coccobacillary, facultatively anaerobic pathogenic bacterium of the family Pasteurellaceae. H. influenzae was first described in 1892 by Richard Pfeiffer during an influenza pandemic.

Bacterial pneumonia is a type of pneumonia caused by bacterial infection.

Boil deep folliculitis, infection of the hair follicle

A boil, also called a furuncle, is a deep folliculitis, infection of the hair follicle. It is most commonly caused by infection by the bacterium Staphylococcus aureus, resulting in a painful swollen area on the skin caused by an accumulation of pus and dead tissue. Boils which are expanded are basically pus-filled nodules. Individual boils clustered together are called carbuncles. Most human infections are caused by coagulase-positive S. aureus strains, notable for the bacteria's ability to produce coagulase, an enzyme that can clot blood. Almost any organ system can be infected by S. aureus.

Vancomycin-resistant <i>Staphylococcus aureus</i>

Vancomycin-resistant Staphylococcus aureus (VRSA) are strains of Staphylococcus aureus that have become resistant to the glycopeptide antibiotic vancomycin.

Blood culture To find organisms in blood

A blood culture is a medical laboratory test used to detect bacteria or fungi in a person's blood. Blood is normally sterile, and the presence of microorganisms in the blood often indicates a serious infection.

Carbapenem group of β-lactam antibiotics

Carbapenems are a class of highly effective antibiotic agents commonly used for the treatment of severe or high-risk bacterial infections. This class of antibiotics is usually reserved for known or suspected multidrug-resistant (MDR) bacterial infections. Similar to penicillins and cephalosporins, carbapenems are members of the beta lactam class of antibiotics, which kill bacteria by binding to penicillin-binding proteins, thus inhibiting bacterial cell wall synthesis. However, these agents individually exhibit a broader spectrum of activity compared to most cephalosporins and penicillins. Furthermore, carbapenems are typically unaffected by emerging antibiotic resistance, even to other beta-lactams.

Community-acquired pneumonia (CAP) refers to pneumonia contracted by a person outside of the healthcare system. In contrast, hospital-acquired pneumonia (HAP) is seen in patients who have recently visited a hospital or who live in long-term care facilities. CAP is common, affecting people of all ages, and its symptoms occur as a result of oxygen-absorbing areas of the lung (alveoli) filling with fluid. This inhibits lung function, causing dyspnea, fever, chest pains and cough.

Pseudomonas oryzihabitans, also known as Flavimonas oryzihabitans, is a nonfermenting yellow-pigmented, gram-negative, rod-shaped bacterium that can cause sepsis, peritonitis, endophthalmitis, and bacteremia. It is an opportunistic pathogen of humans and warm-blooded animals that is commonly found in several environmental sources, from soil to rice paddies. They can be distinguished from other nonfermenters by their negative oxidase reaction and aerobic character. This organism can infect individuals that have major illnesses, including those undergoing surgery or with catheters in their body. Based on the 16S RNA analysis, these bacteria have been placed in the Pseudomonas putida group.

Ecthyma gangrenosum skin lesion

Ecthyma gangrenosum is a type of skin lesion characterized by vesicles or blisters which rapidly evolve into pustules and necrotic ulcers with undermined tender erythematous border. "Ecthyma" means a pus forming infection of the skin with an ulcer, "gangrenosum" refers to the accompanying gangrene or necrosis. It is classically associated with Pseudomonas aeruginosa bacteremia, but it is not pathognomonic. Pseudomonas aeruginosa is a gram negative, aerobic bacillus.

Staphylococcal infection Human disease

A staphylococcus infection or staph infection is an infection caused by members of the Staphylococcus genus of bacteria. These bacteria commonly inhabit the skin and nose where they are innocuous, but may enter the body through cuts or abrasions which may be nearly invisible. Once inside the body, the bacterium may spread to a number of body systems and organs, including the heart, where the toxins produced by the bacterium may cause cardiac arrest. Once the bacterium has been identified as the cause of the illness, treatment is often in the form of antibiotics and, where possible, drainage of the infected area. However, many strains of this bacterium have become antibiotic resistant; for those suffering these kinds of infection, the body's own immune system is the only defense against the disease. If that system is weakened or compromised, the disease may progress rapidly. Anyone can contract Staph, but pregnant women, children, and people with chronic diseases or who are immuno-deficient are often more susceptible to contracting an infection.

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  28. ↑ "Fever without a source in children 3 to 36 months of age".
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  30. 1 2 3 4 5 6 Hall, Keri K.; Lyman, Jason A. (2016-12-16). "Updated Review of Blood Culture Contamination". Clinical Microbiology Reviews. 19 (4): 788–802. doi:10.1128/CMR.00062-05. ISSN   0893-8512. PMC   1592696 . PMID   17041144.
  31. ↑ Holland, TL; Arnold, C; Fowler VG, Jr (1 October 2014). "Clinical management of Staphylococcus aureus bacteremia: a review". JAMA. 312 (13): 1330–41. doi:10.1001/jama.2014.9743. PMC   4263314 . PMID   25268440.
  32. 1 2 3 4 5 Seifert, Harald (2009-05-15). "The Clinical Importance of Microbiological Findings in the Diagnosis and Management of Bloodstream Infections". Clinical Infectious Diseases. 48 (Supplement 4): S238–S245. doi: 10.1086/598188 . ISSN   1058-4838. PMID   19374579.
  33. ↑ "IDP200 Pathophysiology of Infectious Diseases, Fall 2004/2005 - Tufts OpenCourseWare". ocw.tufts.edu. Retrieved 2016-12-07.
  34. ↑ "IDP200 Pathophysiology of Infectious Diseases, Fall 2004/2005 - Tufts OpenCourseWare". ocw.tufts.edu. Retrieved 2016-12-07.
  35. ↑ Medical Microbiology, 27e. New York: McGraw-Hill Education. 2016. pp. Chapter 9. ISBN   9780-0-71-82498-9 – via http://accessmedicine.mhmedical.com/content.aspx?bookid=1551&Sectionid=94106209.
  36. ↑ Sherris Medical Microbiology, 6e. New York: McGraw-Hill. 2014. pp. Infectious Diseases: Syndromes and Etiologies. ISBN   9780-0-7-181821-6 – via http://accessmedicine.mhmedical.com/content.aspx?bookid=1020&Sectionid=56968846.
  37. ↑ Cohen-Poradosu, Ronit (2015). Harrison's Principles of Internal Medicine, 19e. New York: McGraw-Hill. pp. Chapter 201. ISBN   978-0-07-180215-4 – via http://accessmedicine.mhmedical.com/content.aspx?bookid=1130&Sectionid=79736907.
  38. ↑ Forner, Lone; Larsen, Tove; Kilian, Mogens; Holmstrup, Palle (2006-06-01). "Incidence of bacteremia after chewing, tooth brushing and scaling in individuals with periodontal inflammation". Journal of Clinical Periodontology. 33 (6): 401–407. doi:10.1111/j.1600-051X.2006.00924.x. ISSN   1600-051X. PMID   16677328.
  39. ↑ Kaplan, MD, Lewis (2016-08-16). "Systemic Inflammatory Response Syndrome: Background, Pathophysiology, Etiology". Medscape.
  40. 1 2 Hooper, David (2016). Harrison's Principles of Internal Medicine 19th Edition. New York: McGraw Hill. pp. Chapter 170. ISBN   978-0-07-180215-4.
  41. 1 2 Liu, Catherine; Bayer, Arnold; Cosgrove, Sara E.; Daum, Robert S.; Fridkin, Scott K.; Gorwitz, Rachel J.; Kaplan, Sheldon L.; Karchmer, Adolf W.; Levine, Donald P. (2011-02-01). "Clinical practice guidelines by the infectious diseases society of America for the treatment of methicillin-resistant Staphylococcus aureus infections in adults and children". Clinical Infectious Diseases. 52 (3): e18–55. doi: 10.1093/cid/ciq146 . ISSN   1537-6591. PMID   21208910.
  42. 1 2 3 Russo, Thomas (2016). Harrison's Principles of Internal Medicine 19th Edition. New York: McGraw Hill. pp. Chapter 186. ISBN   978-0-07-180215-4.
  43. 1 2 Mermel, Leonard A.; Allon, Michael; Bouza, Emilio; Craven, Donald E.; Flynn, Patricia; O'Grady, Naomi P.; Raad, Issam I.; Rijnders, Bart J. A.; Sherertz, Robert J. (2009-07-01). "Clinical practice guidelines for the diagnosis and management of intravascular catheter-related infection: 2009 Update by the Infectious Diseases Society of America". Clinical Infectious Diseases. 49 (1): 1–45. doi:10.1086/599376. ISSN   1537-6591. PMC   4039170 . PMID   19489710.
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