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Saline-Filled Breast Implant Contamination with Curvularia Species among Women Who Underwent Cosmetic Breast Augmentation

  1. Marion A. Kainer1,2,5,a,
  2. Homa Keshavarz1,4,
  3. Bette J. Jensen2,
  4. Matthew J. Arduino2,
  5. Mary E. Brandt3,
  6. Arvind A. Padhye3,
  7. William R. Jarvis2,b and
  8. Lennox K. Archibald2,a
  1. 1Epidemic Intelligence Service, Division of Applied Public Health Training, Epidemiology Program Office, and Divisions of
  2. 2Healthcare Quality Promotion,
  3. 3Bacterial and Mycotic Diseases, and
  4. 4Public Health Surveillance and Informatics, Epidemiology Program Office, Centers for Disease Control and Prevention, Atlanta, Georgia;
  5. 5Department of Epidemiology and Preventive Medicine, Monash University, Melbourne, Australia
  1. Reprints or correspondence: Dr. Marion A. Kainer, Tennessee Dept. of Health, 4th Fl., Cordell Hull Bldg., 425 5th Ave. N, Nashville, TN 37247 (marion.kainer{at}state.tn.us)
 
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Abstract

BackgroundDuring December 2000–July 2001, black sediment was noted in saline-filled silicone breast implants of women who had undergone revision surgery at facility A. Curvularia fungus was isolated from implant saline

MethodsTo identify risk factors for contamination with Curvularia species, we performed case-control, retrospective cohort, and laboratory studies and conducted procedural reviews. A case patient was defined as any woman who underwent revision surgery at facility A between January 2000 and June 2001 and had black sediment in her implants

ResultsFive patients met the case definition. Contamination was associated with having had surgery performed in operating room (OR) 2 (4/88 vs. 1/140; P=.07) and a longer duration of surgery (P<.001). A longer duration spent in the OR was an additional risk factor (P=.005). Curvularia fungus was isolated from the sterile supply room, where saline bottles had been stored under a water-damaged ceiling, and from the corridor outside OR 2; it was also found more commonly from facility A personnel than from non–facility A personnel (12/34 vs. 4/60; P<.001). Saline was warmed in a cabinet opposite OR 2, which was maintained at negative pressure differentials, then was poured into bowls open to the OR 2 environment before injection into implants

ConclusionSurgeons should always use closed systems to inflate breast implants. Surgery center infection control measures must include moisture control and balanced ventilation systems

During 2000, 187,755 women underwent cosmetic breast augmentation (CBA) surgery in the United States, an increase of 476% compared with 1992 [1, 2]. Most augmentations (94%) used saline-filled silicone shell prosthetic breast implants (SALBIs) [1]. Recognized complications with SALBIs include leakage, capsular contracture, and infection [3]. The incidence of infection after CBA surgery is <2% [4 –7], and there have been few case reports of fungal contamination of SALBIs [8 –10]. In this article, we describe an investigation of an outbreak of Curvularia species contamination of SALBIs of women who had undergone CBA surgery

From 22 December 2000 through 21 July 2001, macroscopically visible black sediment was noted in the SALBIs in 5 women who had undergone revision surgery and SALBI removal. Curvularia fungus, a fast-growing dematiaceous fungus commonly found in soil, was cultured from the implant fluid in all 5 women. Two surgeons (surgeons X and Y) performed CBA procedures at a freestanding ambulatory surgical facility (facility A) and at medical center B, located 2 miles away. Surgeon X had performed all 5 initial CBAs at facility A during 1 June–12 September 2000. When preliminary investigations by facility A personnel did not identify a source of contamination, the Centers for Disease Control and Prevention (CDC) was invited to assist in an investigation. We report the findings of the outbreak investigation conducted in July–August 2001, which identified the source and risk factors for contamination with Curvularia species, and provide recommendations for the prevention of fungal contamination of operating rooms and SALBIs and future similar outbreaks

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Patients and Methods

To identify risk factors for contamination of SALBIs with Curvularia species, we conducted analytic epidemiologic (case-control and retrospective cohort) studies, review of practices and procedures at facility A, and laboratory studies

Case Definition and Ascertainment

A case patient was defined as any woman with macroscopic fungal contamination of ⩾1 of her SALBIs who previously underwent CBA surgery at facility A between 1 January 2000 and 28 June 2001. To ascertain case patients, we interviewed surgical and operating room (OR) staff and reviewed microbiology laboratory and patient medical records

Epidemiologic Studies

Case-control study A control patient was defined as a woman with 2 macroscopically clear SALBIs, as determined by direct visual inspection during revision surgery at facility A or medical center B. Both case and control patients had to have had a revision of a previous CBA procedure. Factors assessed included patient demographic data; indication for surgery; date, time, and duration of the surgical procedure; incision site; type of SALBI (manufacturer, lot number, style, and size); volume of saline injected; OR; operating staff; ancillary OR staff; and severity of illness, as measured by the American Society of Anesthesiologists (ASA) score. “OR time” was defined as the interval between arrival in the OR and incision closure

Cohort study Because the risk for fungal contamination might have been present only during May–September 2000 (i.e., the cohort study period), we conducted a cohort study of women whose original CBA surgery was performed by surgeon X during this period. Women who had had SALBIs but did not undergo revision surgery and remained asymptomatic were deemed noncase patients. We recognized a priori that misclassifying case patients as presumed noncase patients would bias our findings toward the null hypothesis that there was no difference between case and noncase patients. Because of this limitation, we also considered the direction and magnitude of statistical associations

Review of Practices and Procedures

Surgical procedures and practice review We interviewed the surgeons and OR ancillary staff and observed a CBA procedure performed by surgeon X. We reviewed facility A’s architectural plans and inspected the entire facility. We traced and recorded the path through which saline bottles and packaged SALBIs were transferred from storage in the sterile supply room to the OR

Health care worker assessment and survey We administered a questionnaire to facility A clinical and nonclinical staff. Information collected included history of sinus or skin problems, fungal infections, use of artificial fingernails, and exposure to plants or soil. We also examined the hands and fingernails of facility A staff

Facility A Review

We reviewed the layout of the ORs at facility A. In addition, we inspected the heating, ventilation, and air conditioning (HVAC) systems and the air duct interiors on 6 August 2001. We reviewed available engineering, general, and preventive maintenance records and specifications of the HVAC unit at facility A. Flutter strips were used to verify the direction of airflow from ORs to the corridor

Microbiologic Studies

Personnel cultures In August 2001, we cultured nasal mucus, fingernail clippings, and hands (by the Handiwipe method [11]) of facility A personnel. To determine the prevalence of nasal colonization by Curvularia species in this region of the United States, we obtained cultures from OR personnel at medical center B, none of whom had worked at facility A during the preceding 12 months

To establish whether colonized facility A staff could potentially shed Curvularia fungus, we placed settle plates at operating-table height in a small, designated room at another facility and left them for 20 min with the room empty. Next, the procedure was repeated with a person in the room; new settle plates were placed in the same format and for the same duration, within a 3-foot radius of the person being assessed

Environmental cultures In August 2001, we obtained targeted surface cultures of the sterile supply room, saline bottles, a saline bottle warmer, inlet and outlet ventilation grilles, air duct interiors, and moist or water-damaged walls and ceilings. We cultured water condensate specimens from OR portable dehumidifiers. Settle plates were placed in the sterile supply room and the saline warmer for 20 min. Air sampling was performed using an air sampler (SAS Super 90; International PBI)

Statistical Analysis

Data were collected on standardized forms and analyzed using Epi Info (version 6.04; CDC) and SAS statistical software (version 6.12; SAS Institute). The χ2 test or Fisher’s exact test, where appropriate, was used to compare categorical variables; the Kruskal-Wallis test was used to compare continuous variables. Because fungal contamination involving 2 SALBIs in the same patient were not independent events, analyses were performed at the patient level and not at the breast implant level

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Results

Case Patient Characteristics

Five patients met the case definition. Two were symptomatic, and 3 were asymptomatic—that is, SALBI fungal contamination was an incidental finding at revision surgery (table 1). The median age of case patients was 24 years (range, 21–49 years). The 5 explanted SALBIs were round and smooth; 3 were manufactured by the Mentor Corporation and 2 were manufactured by the McGhan Medical Corporation; the lot numbers for implants of each brand differed from one another. Normal sterile saline for irrigation (Baxter Healthcare Corporation) was used to fill the breast implants in the OR; lot and serial numbers were not available for the saline bottles

Figure 1
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Figure 1

A removed saline-filled silicone breast implant with black sediment that was later identified as Curvularia lunata

Figure 2
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Figure 2

Time line of key events for women (n=22) who had cosmetic breast augmentations with saline-filled silicone breast implants and subsequently underwent revision surgery, by month of procedure and surgeon, January 2000–June 2001

Table 1
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Table 1

Characteristics of case patients at facility A, 1 January 2000–28 June 2001

One woman had her initial CBA surgery in 1995 and underwent her first surgical revision in June 2000, to correct symmastia (i.e., medial confluence of the breasts producing a web across the midline). At her revision surgery in June 2000, both SALBIs were macroscopically clear. Saline was removed from each SALBI and replaced with fresh normal saline; the 2 SALBIs were then reimplanted. When this woman underwent further revision surgery, for cosmetic reasons, in July 2001, 1 of the 2 SALBIs contained black sediment that was macroscopically apparent and was later identified as Curvularia lunata (figure 1)

Epidemiologic Studies

Case-control study The 5 case patients and 17 control patients were similar in age, ASA score, volume of saline used to fill the breast implants, time of surgical procedure, and&amp;rank placement (e.g., first) on the operating list. In contrast, case patients were more likely than control patients to have undergone their operation on or after 1 May 2000 (5/5 vs. 5/17; odds ratio, undefined; P=.01) (figure 2), to have had their surgical procedure performed by surgeon X (5/5 vs. 4/17; odds ratio, undefined; P<.005), to have had a periareolar incision (4/5 vs. 2/17; odds ratio, 30.0 [95% confidence interval {CI}, 2.1–421]; P<.01), and to have undergone ⩾2 procedures at the same time as CBA (2/5 vs. 0/17; odds ratio, undefined; P<.05). In addition, case patients were significantly more likely than control patients to have had a longer duration of anesthesia (median, 82 vs. 62 min; P<.05) and duration of surgery (median, 66 vs. 45 min; P<.05) and to have a longer OR time (median, 107 vs. 67 min; P<.05)

Of the 5 case patients, 4 had surgery performed in OR 2, whereas 6 of 17 control patients had surgery performed in OR 2 (odds ratio, 7.3 [95% CI, 0.66–81.4]; P=.14). Compared with patients operated on by surgeon Y, patients operated on by surgeon X had significantly longer OR (median, 107 vs. 62 min; P<.001), anesthesia (median, 85 vs. 61 min; P<.001), and surgery (median, 66 vs. 40 min; P<.001) times. In addition, longer OR times were significantly associated with additional procedures, such as mastopexy (median, 191 vs. 67 min; P<.05) and periareolar incisions (median, 159 vs. 69 min; P < .001). The periareolar approach was used only by surgeon X (6/9 vs. 0/13; P=.001). When the analysis was restricted to surgeon X, 4 of 5 case patients versus 1 of 4 control patients had surgery performed in OR 2 (odds ratio, 25 [95% CI, 0.5–280.1]; P=.2). Indications for revision surgery for the 17 control patients included deflation (15), requesting larger implants (3), contracture (2), and bacterial infection (1)

Cohort study From 1 May through 30 September 2000, 121 women were operated on by surgeon X. Becoming a case patient was associated with OR time, time under anesthesia or surgery, having a periareolar incision, and undergoing additional surgical procedures. Women undergoing surgery in OR 2 were at a higher risk of contamination with Curvularia species (4/49 vs. 1/72; relative risk, 5.9 [95% CI, 0.7–51.0]; P=.16). When we conducted multivariate analyses of the data, independent risk factors associated with becoming a case patient included OR time (P=.005) and having surgery performed in OR 2 (adjusted OR, 5.2; P=.15)

Review of Practices and Procedures

Surgical procedures and practice review Before 1 February 2001, surgeons X and Y used the “open bowl” technique to fill the silicone shell of the inflatable saline breast implant. A sterile bowl was placed on the instrument tray before the woman arrived in the OR. Sterile saline for irrigation was poured from a bottle into the bowl, where it was exposed to the air and environment until it was drawn into a syringe and injected into the breast implant

After 31 January 2001, when the surgeons became aware of the first 2 case patients, surgeon X started using a closed system, whereas Surgeon Y began covering the open bowl with a sterile drape. Surgeon X transferred his practice to medical center B in April 2001, and surgeon Y retired on 28 June 2001 (figure 2)

Health care worker assessment and survey Nineteen (56%) of 34 staff members reported having sinus problems in August 2001; all but 1 had sinus problems during May–September 2000. Two staff members reported fungal infection of fingernails, and 3 reported fungal infection of toenails. Eight (24%) staff members wore artificial fingernails. Twenty-one (62%) were gardeners, and 24 (71%) had handled soil during leisure time

Facility A Review

Operating rooms Facility A contained 4 ORs. A warming cabinet for saline bottles was located directly opposite and 6 feet away from OR 2. This cabinet was opened 60–70 times per day

Sterile supply room Before 1 July 2001, saline bottles were stored in the sterile supply room on a metal grille shelf, directly under a portion of sheetrock ceiling that had sustained water damage in 1998 following a roof leak. Portions of the sheetrock ceiling had moisture content of 28%, probably because of an ongoing leak from the roof

Review of the HVAC system The HVAC system was replaced in late May/early June 2000. There was no moisture in the air ducts. According to the OR design specifications, return air should have had a flow rate of 800 cubic feet/min (cfm) and an exhaust air rate of 190 cfm, resulting in a net positive pressure in the OR. There was no documentation to demonstrate that the HVAC was balanced or to confirm the direction of airflow after the new HVAC was installed in June 2000. On 6 August 2001, the inflow rate of the supply air to OR 2 was 1235 cfm, and the outflow was 1520 cfm—a deficit of 285 cfm. Thus, OR 2 was maintained at negative pressure to the surrounding area; flutter strips demonstrated airflow from the corridor into the OR. OR 3 also was at negative pressure, whereas OR 1 and OR 4 were at positive pressure to the surrounding areas

Microbiologic Studies

Personnel cultures Cultures were obtained from 34 facility A and 60 medical center B staff members. C. lunata was isolated from nasal mucus in 12 (35%) facility A versus 4 (6.7%) medical center B staff members (prevalence ratio, 5.3 [95% CI, 1.9–15.1]; P<.001). One of 12 facility A staff members with positive nasal cultures also had hand cultures positive for C. lunata and another had a positive toenail clipping culture. Although C. lunata was isolated from the nasal mucus of surgeon X, his hand and settle plate cultures were negative. C. lunata was not isolated from surgeon Y. Isolation of C. lunata from facility A staff members was not statistically associated with sinus symptoms or exposure to plants or soil

Environmental cultures C. lunata was isolated from 2 of 18 air samples. One was obtained in the sterile supply room under the water-damaged ceiling, where the saline bottles were stored, and 1 was obtained from the corridor between OR 2 and the warming cabinet. Each air sample filtered 500 L of air. None of the other 179 environmental cultures grew Curvularia species. The number of fungal colony-forming units per cubic meter of air obtained in OR 2 was 66, versus 8 in OR 3; all other conditions were identical

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Discussion

The factors that contributed to contamination of SALBIs with Curvularia species among women who underwent CBA surgery at facility A included the open bowl method, which led to contamination of the saline, and engineering conditions that promoted fungal growth and contamination of the sterile supply room and ORs. Having surgery performed in OR 2 and OR time were associated with increased risk of contamination of implanted SALBIs with Curvularia species

The saline used to fill the silicone shells was likely contaminated while sitting in an open bowl before or during surgery. Our investigation suggests that the silicone shells themselves were not contaminated at the manufacturer for the following reasons: (1) the SALBI shells had different lot numbers and were produced by 2 manufacturers, and (2) the SALBI of the first case patient became infected only after the saline of 5-year-old, previously macroscopically clear SALBIs was replaced. In 1995, Young et al. were concerned that the open bowl method might have resulted in contamination of injectable saline [8]. Although both the McGhan and Mentor Corporations provide a closed filling system, such a system is not actively promoted

More than 7.4 million persons in the United States underwent cosmetic plastic surgery during 2000; 2.5% of these were women who underwent CBA surgery [1]. An additional 78,832 women underwent breast reconstructive surgery; 75% of implants used in these procedures were SALBIs [2]. This, however, might be an underestimate of the actual number of CBA surgical procedures performed annually, since increasing numbers of nonsurgeons are now performing cosmetic surgical procedures [12]. In most states today, increasing numbers of women are electing to have their CBA surgery performed under local anesthesia (e.g., intercostal nerve block) in outpatient clinics, ambulatory surgery centers, or physician offices, where one would expect the risks for complications, including infection, to be substantial. In fact, there have been a few case reports of fungal contamination involving SALBIs; these fungi include Aspergillus species, Curvularia species, and Paecilomyces species [8 –10]. In general, however, infection after augmentation mammoplasty remains uncommon

Our investigation showed that long OR time and duration of surgery were risk factors for contamination with Curvularia species. The surgical technique that uses the periareolar surgical incision approach takes longer than do other incisional approaches for CBA surgery. In addition, women who elected to undergo other procedures at the same time as their CBA surgery would have spent a longer time in the OR. Thus, undergoing CBA surgery involving the periareolar incision approach and undergoing additional procedures at the same time as CBA represent surrogate markers for a longer-than-anticipated OR time; hence, their significant association with SALBI contamination during the study period. The strong association with OR time, a marker for duration of exposure of saline in the open bowl to the environment, suggests that fungal spores in the OR air or environment extrinsically contaminated the saline

We constructed a hypothesis to explain the sequential mode of SALBI contamination: (1) the moist sheetrock ceiling in the sterile supply room provided favorable growth conditions for C. lunata; (2) fungal spores, via air currents, dust, or water droplets, settled from the ceiling onto the surface of the saline bottles stored directly under the water-damaged ceiling; and (3) the contaminated saline bottles then were placed into the warming cabinet, where the constant opening and closing of the cabinet door resulted in air drafts laden with fungal spores. The airborne fungal spores then were drawn into OR 2, which was at profound negative pressure and was located directly opposite the warming cabinet. This scenario would explain why women who underwent their surgical procedure in OR 2 were the ones most at risk of having their SALBIs contaminated with C. lunata. According to the American Institute of Architects Academy of Architecture for Health and the CDC’s guidelines for prevention of surgical site infections, air movement relative to surrounding areas should be outward from ORs [13, 14]. On the basis of the findings of the investigation and the plausibility of our hypothesis, we made several recommendations aimed at controlling the present outbreak and preventing recurrences (see the Appendix). These recommendations were immediately implemented by the facility A administration

In addition, facility A contacted 384 women by registered mail; all had SALBI insertions between April 2000 and January 2001 at facility A. Women were counseled and offered revision surgery at no cost. As of January 2005, 224 women had undergone revision surgery; implants were visually inspected, and implant fluid was sent to the CDC for fungal culture. Two contaminated breast implants were identified: 1 from the other breast of case patient 2 and 1 from a woman whose surgery was performed in October 2000. Curvularia species were not isolated from implant fluid that was macroscopically clear. The attack rate for SALBI contamination was 3.75% for the risk period of June 2000–January 2001

In this outbreak, personnel nasal cultures were a useful adjunct to high-volume air samplers, since each staff member’s nose effectively filtered 3000 L of air over an 8-h shift—that is, 6-fold the volume of 1 air sampler. Personnel cultures reflect the large volume of air filtered, as well as exposure to prior environmental conditions. There are no other published data on the prevalence or persistence of nasal colonization by Curvularia species in this region of the United States

Our investigation had some limitations. First, women who were asymptomatic and whose SALBI contamination status therefore was not known were presumed to be noncase patients for the cohort study analysis. This presumption resulted in potential misclassification of cases and reduced power. Second, the limited number of revision surgical procedures in women operated on by surgeon Y during May–September 2001 resulted in the potential for major case-ascertainment bias and prevented us from determining whether surgeon X was linked epidemiologically to the transmission of Curvularia species

In summary, a combination of factors, such as poor moisture control in the sterile supply room that facilitated Curvularia spores in the facility A environment, the maintenance of the OR at negative rather than positive air pressure differentials, and the absence of a closed-system protocol for injecting saline into SALBIs, all contributed to SALBI contamination with Curvularia species. These findings are in keeping with health care–associated outbreaks involving other fungi, such as Aspergillus species [15 –17]. Ambulatory or outpatient surgical centers need to (1) follow hospital recommendations for regular maintenance of HVAC systems and balancing of airflow in ORs; (2) follow infection control guidelines; and (3) include infection control staff in all stages of planning, construction, and renovation of health care facilities and HVAC systems. This outbreak investigation provides scientific evidence to support the recommendation that ORs should be at positive pressure relative to the surrounding areas and that a closed system should be used when injecting sterile saline into SALBIs

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Acknowledgments

We are grateful to the clinicians, patients, health care workers, and public health staff at facility A who assisted in this investigation. Also, we thank the facility A administration for implementing the recommendations that followed the investigation

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Footnotes

  • Presented in part: 40th Annual Meeting of the Infectious Diseases Society of America, Chicago, 24–27 October 2002 (abstract 416)

    Financial support: The investigation upon which this study is based was conducted while the authors were employees of the Centers for Disease Control and Prevention. The US Public Health Service underwrote all funding for this investigation

    Since submitting this manuscript, M.A.K. has provided professional clarification and interpretation on the results of this investigation to attorneys involved in pending court cases regarding this incident

    The use of trade names is for identification only and does not imply endorsement by the US Public Health Service or the US Department of Health and Human Services

  • ↵Present affiliations: Tennessee Department of Health, Nashville, Tennessee (M.A.K.); Regeneration Technologies, Inc., Alachua, Florida (L.K.A.)

  • ↵W.R.J. is now retired and in private practice

  • Received September 20, 2004.
  • Accepted January 28, 2005.
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Appendix

Recommendations

  • Use only a closed system to fill saline-filled silicone breast implants; do not use open systems, such as the “open bowl” method

  • Balance the heating, ventilation, and air-conditioning (HVAC) system in each operating room and provide infection control and administrative staff with documentation that balancing has been performed whenever adjustments to the air-handling unit are made or the operating rooms (ORs) undergo structural renovations [13]

  • Measure and document direction of airflow from the OR to the surrounding areas on a weekly basis and each time the HVAC system is balanced [13]. A flutter strip can be used to assess the direction of airflow across entrances to ORs

  • Remove and replace all water-damaged or moist building materials. Correct roof leaks and address any other causes of water damage

  • Involve infection control staff in all stages (including planning) of construction, demolition, and renovation of health care facility structures and the HVAC system [13]

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  1. J Infect Dis. (2005) 192 (1): 170-177. doi: 10.1086/430613
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