June 27, 2014 — In late May, 2014, officials of the Greenville Health System in South Carolina identified a number of patients infected with an “unusual” type of organism.
The first infected patient was identified in March, 2014. Since then, 14 more patients who underwent surgery at Greenville Memorial Hospital have tested positive for an atypical mycobacterium called Mycobacterium abscesses.
Of these 15 infected (or colonized) patients, 12 had undergone cardiac surgery, two abdominal surgery, and one a neurological procedure.
Four patients die
In June, 2014, a local news source reported that hospital officials had linked this hospital’s outbreak to three patient deaths. One month later, a second news source reported that officials had linked a 4th patient’s death to this outbreak, too.
Hospital officials acknowledge that this outbreak may have been an important contributing factor to the death of the four infected patients, adding, however, that these patients also had other serious underlying health problems at the time of their infection.
Update: October 2015 — Wellspan York Hospital (York, PA) identified a similar type of deadly mycobacterial outbreak that infected 8 patients, 4 of whom died. This outbreak was linked to a heater-cooler device used during open-heart surgery. And in February 2016, University of Iowa Hospitals and Clinics linked a mycobacterial infection to the same type of heater-cooler device.
Update: November 28, 2016 — The CDC has told The Daily Beast that contamination of the Sorin 3T heater-cooler device used by Greenville Memorial Hospital (Greenville, SC) could have contributed to some of the hospital’s deadly mycobacterial infections. This outbreak was publicly disclosed in the summer of 2014.
Hospital officials notified approximately 180 patients who may have been exposed to this organism, in addition to temporarily closing the operating room.
This hospital’s investigation of the cause of this outbreak is being assisted by the Centers for Disease Control and Prevention (CDC) and the South Carolina Department of Health and Environmental Control (DHEC).
Greenville Memorial Hospital (GMH) is managed by the Greenville Health System (GHS), which oversees 6 other hospitals and 5 other campuses.
Two TV interviews, Comment: Two WPSA News 7 television aired two interviews of this article’s author (Dr. Lawrence F Muscarella) discussing Greenville Memorial Hospital’s deadly outbreak. Read his comments in WPSA’s July, 2014, article “GHS Infection Investigation Zeros In On Tap Water.”
Implicated medical equipment
Officials of GHS had acknowledged that, based on the preliminary results of their investigation, the outbreak may be related to a specific “piece of equipment,” which was removed from the operating room in June, 2014.
According to a hospital statement, officials have disclosed more facts about the originally suspected medical equipment.
Since this equipment’s removal, no new infections of this rare type of organism have been identified.
- Read GHS’s “Update on Infection Outbreak Investigation.”
- Also read the recommendations published by the DHEC in response to Greenville Memorial Hospital’s deadly mycobacterial outbreak in 2014.
According to a local news source, however, on July 21, 2014 — just a few weeks after having seemingly linked contaminated medical equipment to these 15 patient infections (or colonizations) and 4 deaths — Greenville Memorial officials appear to have come to a different conclusion.
Namely, several news source reported that the hospital could not formally link its deadly mycobacterial outbreak in 2014 to any one piece of contaminated equipment used in the operating room — its original, preliminary conclusion notwithstanding.
Although initially suspected by officials to have contributed to the outbreak, both an ice machine and a cardiac perfusion machine (a heater-cooler device) were subsequently both exonerated, according to hospital officials.
It is not entirely clear why officials first implicated this medical equipment as having contributed to this outbreak, only to conclude a few weeks later, to the contrary, that no specific medical equipment could be linked to these 15 patient infections.
Quality and Safety Services for Hospitals, Manufacturers, Patients: Click here to read about Dr. Muscarella’s quality and safety services committed to reducing the risk of healthcare-associated infections, including CRE outbreaks linked to contaminated endoscopes and other reusable medical equipment.
Mycobacterium abscessus, the cause of Greenville Memorial’s outbreak, may be found naturally in water, soil and dust. It is a slow growing organism, and because its incubation period is long, infected patients may not display symptoms until weeks or even months after exposure.
Healthy patients are usually not affected by M. abscessus, which generally only causes infection in patients who are ill or immuno-suppressed. This organism is therefore termed “opportunistic.”
M. abscessus is not transmitted from patient to patient, meaning it is not contagious. Rather, direct contact with a contaminated environmental source is required for infection.
UPDATE – An FDA Alert: On October 15, 2015, the FDA published the safety communication, “Nontuberculous mycobacterium infections associated with heater-cooler devices.”
On the same date, the CDC published the notice, “Non-tuberculous mycobacterium infections and heater-cooler devices.” Both articles bring attention to factors that could have contributed to GMH’s deadly mycobacterial outbreak.
The mycobacteria’s source, mode of transmission
Officials of GMH have reported that the source of its atypical mycobacterial outbreak was the facility’s tap water.
Suggesting mycobacteria in tap water poses a more widespread, national concern for U.S. hospitals, a CDC official investigating the cause of this hospital’s outbreak stated:
“We wouldn’t be surprised if we could find these bacteria or similar bacteria in the water supply going to any U.S. hospital.”
Hospital officials had originally suspected that contaminated surgical equipment used in the operating room was responsible for the outbreak.
“Rare” infection a contributing factor
Officials of GMH have maintained that this outbreak likely contributed to the death of the four infected patients, adding that, “We regret that any patient within our care could possibly be affected by this situation. Our thoughts are with those involved.”
Later, hospital officials issued another statement that read, in part: “Just as Greenville Health System (GHS) elected a transparent approach in communicating to the public and to our patients that a potential infection outbreak was being investigated, we anticipate continuing that transparency. … We believe in doing right by all of our patients, and we will continue to work with them moving forward.”
The originally suspected equipment
Although originally confused about the likely source of GMH’s mycobacterial outbreak, hospital officials are no longer blaming medical equipment, instead implicating the hospital’s tap water.
How, exactly, the 15 infected patients became exposed to the contaminated water during their surgical procedures, however, remains a mystery.
As they acknowledge, officials had originally suspected that medical equipment used in the operating room during open-chest surgeries, possibly the heater-cooler device or an ice machine, both of which may use tap water, contributed to this outbreak.
Unless all of this outbreak’s causes and potential contributing factors are not identified, U.S. acute-care hospitals will be precluded from implementing all of the necessary corrective and preventive actions to ensure that their own surgical patients are not at risk of this specific type of deadly mycobacterial infection. — Lawrence F Muscarella PhD
The initial suspicion by GMH’s officials that a heater-cooler device or ice machine might have played a critical role in causing this M. abscessus outbreak is understandable.
Indeed, previously published reports have linked other, unrelated outbreaks of atypical mycobacteria to ice (and ice dispensing machines) used in the healthcare setting and specifically during cardiac bypass surgery.(1-6)
Health officials also appear to have initially suspected that a heater-cooler machine used to perform cardiac surgery might have contributed to its mycobacterial outbreak.
But, the initial suspicions about these three types of machines used during cardiac surgery would not seem to explain how the other three patients who instead underwent abdominal surgery (2 patients) or a neurological operation (1 patient) in this same operating room also became infected with the outbreak’s strain of M. abscessus. This remains a mystery, too.
Contaminated tap water
If health officials are no longer implicating any medical equipment as a cause of this outbreak, they certainly are now blaming Greenville Memorial’s tap water.
A report, dated July 22, 2014, notes that hospital officials have cited tap water as the likely source of GMH’s mycobacterial outbreak.
One local newspaper reported investigators of the federal CDC as (correctly) saying:
- “Any piece of equipment in the surgical environment that could have contact with water has to be looked at very carefully.” (Author’s note: This equipment would include the ice machine and a heater-cooler device used by the hospital during cardiac surgery.)
- “Appropriately processed surgical instruments and equipment should undergo sterilization so that it isn’t exposed to un-sterile water before it comes into contact with the patient.”
- “When we hear about surgical site infections involving these organisms (atypical mycobacteria), we’re thinking water sources.”
- “Only sterile water (should be) used on the patient.”
To be sure, the use of non-sterile water in the operating room is a risk factor for mycobacterial outbreaks following cardiac bypass surgery.(1) And, tap water used to make ice to cool cardioplegia solutions has been previously identified as a source of infection due to atypical mycobacteria.
Other environmental surfaces in the healthcare setting that, like tap water, are prone to contamination with waterborne organisms, including sinks, shower-heads and faucet aerators, similarly have been linked to outbreaks of atypical mycobacteria (and other types of waterborne microorganisms).(7,8)
Indeed, whether safe or not, heater-cooler device used during cardiopulmonary bypass surgery may be filled with tap water.
Still more unanswered questions
But, in addition to what exactly were the causes and potential contributing factors of GMH’s mycobacterial outbreak, a number of other questions remain unanswered, including:
— Does the CDC consider this deadly outbreak to be confined to this one hospital in South Carolina, or it is a national concern? (Update: This question takes or greater concern after Wellspan York Hospital identified a similar type of outbreak in October 2015.)
— How thoroughly did the DHEC investigate the possible contribution of a heater-cooler to GMH’s outbreak?
— Will the CDC advise all U.S. hospitals to implement, too, the same corrective actions that both GMH and the South Carolina DHEC recently published, to ensure patient safety?
— Why have no state or federal health officials, or representatives of GHS, publicly disclosed that Greenville Memorial Hospital’s heater-cooler device was sampled and found to be contaminated with mycobacteria if it is true that the three aforementioned medical device reports filed with the FDA (see above) describe this hospital’s deadly outbreak in 2014?
A puzzle to solve: The outbreak’s cause
Details about the cause of GMH’s outbreak remain relatively scant, other than that contaminated tap water appears to be the outbreak’s source and the medical equipment, originally suspected of being the outbreak’s mode of transmission, has since been seemingly exonerated.
To summarize, what’s known so far is this, however:
1. Hospital officials had originally implicated medical equipment — an ice dispenser and heater-cooler device — as playing a significant role in this outbreak, but then they concluded otherwise, claiming instead that the hospital’s tap water was responsible for the outbreak;
2. The tap water in one of GMH’s several operating rooms was determined to be contaminated with M. abscessus. (The tap water in each of the other operating rooms was tested and was reportedly found not to be contaminated with mycobacteria);
3. This outbreak appears to be limited to a single operating room (the one that officials have temporarily closed) in which three different types of surgical procedures — cardiac surgery, abdominal surgery and neurosurgery — were performed; and
4. Three medical device reports filed with the FDA and appearing to describe Greenville Memorial’s outbreak in 2014 found the Sorin 3T heater-cooler device to be contaminated with mycobacteria — the same organism that caused the outbreak.
So, what caused Greenville Memorial’s mycobacterial outbreak?
Update: Based on a deadly mycobacterial outbreak that Wellspan York Hospital linked in October 2015 to a heater-cooler device, a reassessment of the potential contribution of this device to GMH’s outbreak a year earlier seems warranted.
According to officials, GHS began installing a new water filtration system on all of its campuses in the summer of 2014 to prevent another outbreak of atypical mycobacteria.
Indeed, installing this new filtration system is “an extraordinary measure,” as stated by hospital officials, who added that: “This is a very unusual thing for organizations to do. It’s not standard by any means, (but) we’ve taken that on so as to protect our patients.”
While on its face this seems like a proactive action, GHS’s installation of a new water filtration system raises at least one important question:
Should every acute-case hospital also install a similar type of water filtration system in its respective operating rooms, to avoid being blamed if it were itself to encounter an atypical mycobacterial outbreak following a surgical procedure?
Whether GHS’s installation of this filtration system on all of its campuses was necessary or superfluous is a fair issue to raise.
Indeed, GHS performed this measure as a comprehensive corrective action, even though only the tap water leading into one operating room of one of GHS’s hospitals (i.e., Greenville Memorial Hospital) was reported to be contaminated with the outbreak’s mycobacteria.
Greenville Health System’s recent installation of a new water filtration system throughout all of its campuses to prevent another mycobacterial outbreak would appear proactive, but, depending on the outbreak’s true cause and mode of transmission, this expensive measure could be unnecessary, which is why determining the precise cause of this outbreak, like the cause of any hospital’s outbreak, is so important. — Lawrence F Muscarella PhD
If this action is necessary to protect all of GHS’s patients, it would certainly seem that the installation of a new water filtration system would be required of every acute-care U.S. hospital to protect all open-chest surgery patients.
This action might not be necessary, however, if there was a specific piece of equipment that was responsible for infecting Greenville Memorial’s 15 patients with mycobacteria. Removing the contaminated equipment from the operating room, instead of installing a water filtration system on all of GHS’s campuses, might cost less and be more effective.
If there was a piece of equipment used in Greenville Memorial Hospital’s one implicated operating room that was contaminated with the outbreak’s mycobacteria, then its removal — not the installation of a water filtration system throughout all of Greenville Health System’s other campuses, per se — would seem to be the more appropriate and cost-effective corrective action to ensure patient safety. — Lawrence F Muscarella, PhD
Might the outbreak’s cause never be known?
Hospital officials recently stated that, “We don’t really know how it got transmitted from what we think is our water source, which is the most common place for the organism to be, into a patient (and) we probably never exactly will know that answer.”
The public-health implications of not determining the precise cause of GMH’s outbreak, however, are far-reaching.
Revisiting Greenville Memorial Hospital’s one operating room to isolate and identify how precisely its tap water infected these 15 patients is urged to ensure that hospitals do not employ unnecessary corrective actions in response to this mycobacterial outbreak. — Lawrence F Muscarella, PhD
Other reports of mycobacterial infections following surgery
While infections of atypical mycobacteria following surgery are uncommon, cases similar to GMH’s outbreak of M. abscessus have been previously reported.
For example, Wallace et al. (1989) studied, in part, the sources of strains of atypical mycobacteria linked to outbreaks of infection following cardiac bypass surgery, reporting that that environmental contamination was responsible for most of these infections.(1)
Cardiac bypass surgery was one of the three types of surgical procedures that Greenville Memorial Hospital linked to its outbreak of M. abscessus.
Wallace et al. (1989) state that the use of non-sterile water in the operating room — Note: officials have suggested this could be the cause of Greenville Memorial Hospital’s outbreak — may be an important contributor to mycobacterial outbreaks following cardiac bypass surgery.(1)
The conclusions and findings of a number of other similar types of reports are provided in Box A, which is appended to this article.
These outbreaks of atypical mycobacteria are only a few examples, and the extent to which the cause of either is similar to (or different from) and applies to GMH’s outbreak of M. abscessus is unclear.
These outbreak reports indicate that infections of atypical mycobacteria, like Greenville Memorial Hospital’s, are often due to the improper disinfection or sterilization of surgical instruments. — Lawrence F Muscarella PhD
A national concern?
Greenville Memorial Hospital’s mycobacterial outbreak is likely to have national implications.
As previously noted, atypical mycobacteria may be identified in the tap water of any hospital in the U.S. There remains the possibility, therefore, that other hospitals across the U.S., too, may be susceptible to this same type of deadly mycobacterial infection.
Moreover, this risk may not have been adequately mitigated, because all of the causes of (and contributing factors to) GMH’s outbreak have not been identified and published by hospital officials, the CDC or the DHEC.
Consequently, implementation by GMH or another hospital of all of the corrective and preventive actions necessary to prevent this outbreak’s recurrence would seem improbable.
Some recommendations intended to prevention transmission of atypical mycobacteria in the healthcare setting are listed, below. Additional recommendations are provided in an accompanying article by Dr. Muscarella entitled “Recommendations to prevent atypical mycobacterial infections following surgical procedures.”
UPDATE (October 15, 2015): Recommendations are also provided in in the FDA’s safety communication, “Nontuberculous mycobacterium infections associated with heater-cooler devices” and the CDC published notice, “Non-tuberculous mycobacterium infections and heater-cooler devices.”
1. Rigorously practice Standard Precautions and, if required, Contact Precautions to prevent disease transmission.
2. Ensure that any equipment used during cardiac surgery — including ice machines and heater-cooler devices — are properly maintained, serviced and periodically decontaminated, as required, in accordance with the manufacturer’s most up-to-date instructions.
- Update: As recommended in a 2015 FDA alert, establish regular cleaning, disinfection and maintenance schedules for heater-cooler devices according to the manufacturers’ instructions to minimize the risk of bacterial growth and subsequent patient infection.
- Update: Also as recommended in this 2015 FDA alert, direct the heater-cooler’s vent exhaust away from the surgical field to mitigate the risk of aerosolizing heater-cooler tank water into the sterile field and exposing the patient.
3. The use of point-of-use filters may be recommended to improve the quality of the tap water used by ice machines and heater-cooler devices. (Refer to each device’s respective operating manual for more information.)
- Properly maintain and replace any installed water filters, to ensure none become colonized with bacteria and themselves a source of infection.
- Depending on the model, heater-cooler devices might require not only the use of filtered tap water but also possibly the water’s dilution with a disinfectant. Routine decontamination of these machines’ internal water tanks may also be necessary, even though the water these machines use does not contact the patient. (Refer to the device’s operating manual for more information.)
4. Although it would require additional time and resources, an independent review of GMH’s mycobacterial outbreak, like that of any hospital’s outbreak, may be necessary to identify this outbreak’s precise cause(s) and, therefore, to prevent its recurrence — the claim by hospital officials that the cause of its atypical mycobacterial outbreak may never be known notwithstanding.
- Unless every cause and factor that contributed to the adverse event is identified, not all of the corrective and preventive actions necessary to prevent additional infections will be implemented, raising the specter of the outbreak’s recurrence.
5. Update: As recommended in a 2015 FDA alert, do not use tap water to rinse, fill, refill or top-off water tanks since this may introduce mycobacteria.
- Use only sterile water or water that has been passed through a filter of less than or equal to 0.22 microns.
- When making ice needed for patient cooling during surgical procedures use only sterile water or water that has been passed through a filter of less than or equal to 0.22 microns.
First, the original source of this outbreak’s M. abscessus is reported to be GMH’s tap water. Exactly how this water came into contact with the 15 patients’ sterile tissues has yet to be determined.
But, based on the deadly mycobacterial outbreak that Wellspan York Hospital linked in October 2015 to a heater-cooler device — and the mycobacterial infection that the University of Iowa Hospitals and Clinics linked in early 2016 to its heater-cooler device, — a reassessment of the potential contribution of this device to GMH’s outbreak a year earlier seems warranted.
Second, although 15 patients of GMH were infected with the outbreak strain, the possibility cannot be ruled out that other patients of this hospital who also underwent surgery might, too, have been infected, not necessarily with this same organism, but by the hospital’s contaminated tap water.
Third, the importance of determining the precise cause of GMH’s mycobacterial outbreak (or of any hospital’s outbreak), even if additional time, research, and resources are required, cannot be overstated, to prevent this type of outbreak’s recurrence.
Indeed, the failure to identify this outbreak’s cause, like that of any type of adverse event, poses an increased risk of its recurrence. It also increases the likelihood of limited funds being misallocated, and U.S. hospitals unnecessarily implementing expensive actions that, although intended to correct for and to prevent this type of outbreak’s recurrence, may miss their mark.
Article by: Lawrence F Muscarella, PhD; posted 6-27-2014.
Note: Dr. Muscarella is the president of LFM Healthcare Solutions, LLC, an independent quality improvement company. Click here for a discussion of his quality healthcare improvement services.
1. Wallace RJ, Musser JM, Hull SI, et al. Diversity and sources of rapidly growing mycobacteria associated with infections following cardiac surgery. J Infect Dis 1989 Apr;159(4):708-16.
2. Laussucq S, Baltch A, Smith RP, et al. Nosocomial Mycobacterium fortuitum colonization from a contaminated ice machine. Am Rev Respir Dis 1988; 138:891–4.
3. Kuritsky IN, Bullen MG, Broome CV, et al. Sternal wound infections and endocarditis due to organisms of the Mycobacterium fortuitum complex. Ann Intern Med 1983;98:938-939.
4. Fábregas L Smeltz A. Legionella bacteria found in hospital ice machines at UPMC Presbyterian. Pittsburgh Tribune‑Review May 2, 2014.
5. Brown-Elliott BA, Wallace RJ, Tichindelean C, et al. Five-year outbreak of community- and hospital-acquired Mycobacterium porcinum infections related to public water supplies. J Clin Microbiol 2011 Dec;49(12):4231-38.
6. Phillips MS, von Reyn CF. Nosocomial infections due to non-tuberculous mycobacteria. Clin Infect Dis 2001; 33:1363–74. (Click here)
7. Burns DN, Wallace RJ Jr, Schultz ME, et al. Nosocomial outbreak of respiratory tract colonization with Mycobacterium fortuitum: demonstration of the usefulness of pulsed-field gel electrophoresis in epidemiologic investigation. Am Rev Respir Dis 1991; 144:1153–9.
8. Hota S, Hirji Z, Stockton K, et al. Outbreak of multidrug-resistant Pseudomonas aeruginosa colonization and infection secondary to imperfect intensive care unit room design. Infect Control Hosp Epidemiol 2009 Jan;30(1):25-33.
9. Muscarella LF. Déjà vu … all over again? The importance of instrument drying. Infect Control Hosp Epidemiol 2000 Oct;21(10):628-9.
10. Muscarella LF. Inconsistencies in endoscope-reprocessing and infection-control guidelines: The importance of endoscope drying. Am J Gastroenterol 2006;101:2147-2154.
11. Dorozynski A. Poor sterilisation of instruments leads to infection outbreak in Paris. BMJ 1997 Sep 20;315:699.
12. Chaudhuri S, Sarkar D, Mukerji R. Diagnosis and management of atypical mycobacterial infection after laparoscopic surgery. Indian J Surg Dec 2010; 72(6): 438–442.
13. Muscarella LF. The importance of bronchoscope reprocessing guidelines: Raising the standard of care. Chest 2004 Sep;126(3):1001-2.
14. Centers for Disease Control and Prevention. Guidelines for environmental infection control in health-care facilities, 2003.
15. Vijayaraghavan R, Chandrashekhar R, Sujatha Y, et al. Hospital outbreak of atypical mycobacterial infection of port sites after laparoscopic surgery. J Hosp Infect 2006 Dec;64(4):344-7.
BOX A: Other atypical mycobacterial outbreaks
As discussed in the main article, while infections of atypical mycobacteria following surgery are uncommon, cases similar to GMH’s outbreak of M. abscessus have been previously reported.
1. Wallace et al. (1989) studied, in part, the sources of strains of atypical mycobacteria linked to outbreaks of infection following cardiac bypass surgery, reporting that that environmental contamination was responsible for most of these infections.(1)
Cardiac bypass surgery was one of the three types of surgical procedures that Greenville Memorial Hospital linked to its outbreak of M. abscessus.
Adding that extensive environmental culturing may be necessary to identify the source of a healthcare-associated atypical mycobacterial outbreak, Wallace et al. (1989) state that the use of non-sterile water in the operating room — officials have suggested this could be the cause of GMH’s outbreak — may be an important contributor to mycobacterial outbreaks following cardiac bypass surgery.(1)
2. A clinic in France reported an outbreak of spinal infections caused by M. xenopi, which is an atypical mycobacterium that is similar to M. abscessus; is also usually harmless although is resistant to the usual regimen of antibiotics; and may be found, too, in the water supply.(11,15)
According to this report published in 1997, the primary factor responsible for this outbreak infecting 31 patients was “poor sterilization” of arthroscopes.
These instruments used during spinal surgery had been “cold sterilized” using a liquid disinfectant (not sterilized using a steam autoclave) and then were rinsed with water contaminated with M. xenopi.
Whether the improper reprocessing of rigid endoscopes (e.g., laparoscopes) could have played a role in causing some of GMH’s infections is unclear.
3. A report documents atypical mycobacterial infections affecting 19 patients at the laparoscopic port site following laparoscopic surgery.(12) (The specific strain is not named in the report.)
Linking this outbreak, too, likely to the inadequate reprocessing of surgical instruments, this report recommends proper sterilization and storage of instruments to prevent the transmission of these organisms during surgery.
4. A report documents surgical site infections in 35 patients due to M. chelonae following laparoscopy performed at one hospital. The source of this organism was determined to be the water used to rinse the instruments after chemical disinfection.(15)
Like M. abscessus and M. xenopi, M. chelonae is an atypical mycobacterium.
These outbreaks of atypical mycobacteria are only three examples, and the extent to which the cause of either is similar to (or different from) and applies to GMH’s outbreak of M. abscessus remains unclear.
Indeed, the cause of GMH’s outbreak could be due less to the processing of surgical instruments than to one or more other factors, too.
No matter, the improper sterilization of surgical instruments remains a potential contributor to any outbreak of atypical mycobacteria following surgery until objective findings reasonably exclude it from consideration.
5. Documenting its aerosolized transmission, a report implicates a hospital’s shower as the source of an outbreak of atypical mycobacterium (i.e., M. fortuitum).(7)
6. Considered, but then seemingly ruled out, by officials of GMH as a potential contributor to its mycobacterial outbreak in 2014, another hospital’s ice machine was found to be colonized with the same strain of M. fortuitum as had been isolated from the sputum samples of 30 patients during a 5-month period, in 1988.(2)