Epidemiologic Notes and Reports Update: Transmission of HIV Infection during an Invasive Dental Procedure -- Florida

Possible transmission of human immunodeficiency virus (HIV) infection during an invasive dental procedure was previously reported in a young woman (patient A) with acquired immunodeficiency syndrome (AIDS) (1). Patient A had no identified risk factor for HIV infection and was infected with a strain of HIV closely related to that of her dentist as determined by viral DNA sequencing. A follow-up investigation has identified four additional patients of the dentist who are infected with HIV. Laboratory and epidemiologic investigation has been completed on three of these patients (Table 1); two are infected with strains closely related to those of the dentist and patient A but not to strains from other persons residing in the same geographic area as the dental practice. The follow-up investigation included review of medical records of the dentist and interviews of former staff on the infection-control procedures of the dental practice. This report summarizes the findings of the investigation.* Epidemiologic Investigation of the Dentist's Patients

Following the initial report (1), the dentist wrote an open letter to his former patients, which prompted 591 persons to be tested for HIV antibody at the Florida Department of Health and Rehabilitative Services (HRS) county public health units; two (patients B and C) were seropositive. In addition, one infected patient (patient D) was identified by HRS by matching the list of available names of the dentist's former patients with the state's AIDS surveillance records, and another (patient E) contacted CDC to report that she was HIV-infected and a former patient of this dentist. Although the exact number of patients in this dental practice is unknown, approximately 1100 additional persons who may have been patients of the dentist and who could be located have been contacted by HRS to offer counseling and HIV-antibody testing; of these persons, 141 have been tested, and all are seronegative.

Patient B is an elderly woman for whom no risk factor for HIV infection could be established. She did not report intravenous (IV)-drug use or sexual contact with persons at risk for HIV infection. Based on interviews and review of her medical records, she had no history of transfusion, receipt of blood products, or illness compatible with an acute retroviral syndrome. Serologic tests for syphilis and hepatitis B virus (HBV) were negative. The patient's spouse, to whom she has been married greater than 25 years, tested negative for HIV antibody.

Patient C is a young man who has reported multiple heterosexual partners and a history of non-IV-drug use, including one hospitalization for toxicity caused by an illicit drug. Other risk factors for HIV infection were suggested by secondary sources but were not corroborated by the patient. He had no history of transfusion, receipt of blood products, or illness compatible with an acute retroviral syndrome; serologic tests for syphilis and HBV were negative. His wife and other female sexual contacts who were tested were HIV seronegative.

Patient D is a man with AIDS with established risk factors for HIV infection. Patient E is a woman with HIV infection whose epidemiologic and laboratory investigation has not yet been completed. All patients (A-E) denied sexual contact with the dentist, and they did not name each other as sex partners.

From 1984 through 1989, patients A, B, and C made numerous visits to this dentist (Table 1) for a variety of procedures: patient A--extractions, prophylaxis (cleaning), and cosmetic bonding; patient B--extractions, prophylaxis, periodontal scaling and root planing, and fixed and removable prosthodontics; and patient C--extractions, prophylaxis, periodontal scaling and root planing, and restorative fillings.

On two occasions, two of these three patients had appointments on the same day: in 1987, patient B was examined for a toothache the same day patient A had two maxillary third molars extracted; in 1989, patients B and C had prophylaxes performed on the same day. Neither the order nor the time of day of their appointments could be determined because appointment books could not be located; also, whether the dentist provided dental care for patients B and C during their appointments for prophylaxes is unknown.

To examine the likelihood that patients shared visit days, two conditional probabilities were calculated based on the number of visits made by each patient (six for patient A, 21 for patient B, and five for patient C) from November 1987 through the closure of the practice in July 1989**. These probabilities were calculated assuming visits occurred at random over the interval during days the dentist's office was open, without allowing multiple visits for the same patient on the same day. Given these assumptions, the probability of each of these patients having shared at least 1 day with another is 0.17; the probability of patients A and B having shared at least 1 day and patients B and C having shared at least 1 day is 0.13. These probabilities suggest that the shared visit days may have been chance events. Laboratory Investigation

To determine the relatedness of the HIV strains from patients B, C, and D to those of the dentist and patient A, blood specimens were obtained from these patients and from eight HIV-infected persons (controls 1-8) randomly selected from two HIV clinics located within 90 miles of the dental practice. Six of the eight controls were men; the sex of the other two controls was not known. Most men in these clinics were either homosexual/bisexual or IV-drug users. Because the blood samples from the controls were collected anonymously, details of their sexual and dental histories were not available.

Sequencing of the HIV proviral DNA present in these specimens was performed at CDC using previously described methods (1-4).*** The sequences included an approximately 300-base-pair variable region (V3) and/or an approximately 350-base-pair region, consisting of variable regions (V4 and V5) and a constant region (C3), encoding the amino acids of gp120. From one to 25 molecular clones obtained from each specimen were sequenced.****

In collaboration with Los Alamos National Laboratory, computer-based methods were used to analyze the relationships of HIV DNA sequences from the dentist, the four dental patients (A-D), and the eight control patients and from 21 other North American isolates (5). Because of the sequence variation between multiple molecular clones of HIV DNA obtained from the same person, consensus sequences were derived to represent the major viral strain present in each person. For four persons (the dentist, patients A and D, and one of the control patients), two consensus sequences were created to encompass the range of their HIV sequence variation.

Sequence variation can be depicted by tree analysis (5). The viruses of the dentist and patients A, B, and C are closely related in their V3 sequences (Figure 1), with an average difference of 3.4%. This degree of sequence relatedness has been reported only for multiple HIV strains obtained from a single person or for HIV strains from persons whose infections were epidemiologically linked (3,4). In contrast, the V3 sequences from the dentist and patients A, B, and C were not closely related to the viral sequences from patient D, seven control patients, and the 21 other North American isolates. Furthermore, the average viral sequence difference for patient D and seven control patients was approximately 13% (range: 8%-15%), suggesting that no particular HIV strain predominates in the geographic area in which the dentist practiced and indicating that no other instance of comparable viral sequence relatedness was identified.

In a separate analysis of a relatively conserved portion of the V4-C3-V5 region, including sequences from the eighth control, the viruses from the dentist and patients A, B, and C had an average difference of 1.8%, whereas the average difference of viruses from the local controls was 4.8%.

The low probability (p=0.006, Wilcoxon rank-sum statistic) that the HIV DNA sequences from patients A, B, and C would be closer by chance alone to the sequence from the dentist than to the sequences from the eight controls indicates that the viruses from patients A, B, and C are significantly more similar to the dentist's virus than to the viruses of the controls.

In addition, the HIV strains of the dentist and patients A, B, and C shared a unique pattern (or "signature sequence") of amino acids encoded by V3 nucleotides. This pattern was absent in the other sequences analyzed. This signature sequence provides additional evidence for the close relation among the viruses from the dentist and the three patients. Medical History of the Dentist

Review of the dentist's medical records revealed that he was diagnosed with symptomatic HIV infection in late 1986, and AIDS in September 1987. At the time of the AIDS diagnosis, his CD4 lymphocyte count was less than 200/mm3; zidovudine therapy was begun, discontinued for a short period in late 1987, then restarted and continued until after the practice closed in 1989. In 1988, he received radiation therapy for Kaposi's sarcoma of the palate. He performed invasive procedures on patients A and B after he was diagnosed with AIDS, including the brief period when he was not receiving antiretroviral therapy, and on patient C both before and after he was diagnosed with symptomatic HIV infection. While the dentist was in practice, he had no record of peripheral neuropathy, dementia, thrombocytopenia or other bleeding disorder, hand dermatitis, or injury. Investigation of the Dental Practice

The office employees of the dentist were interviewed regarding infection-control and other work practices of the dental office. Of the 14 employees, eight have been tested for HIV antibody; all were negative, including the dental hygienists who could have performed prophylaxes on patients A, B, and C. Interviews revealed that no written policy or training course on infection-control principles or practice was provided for staff by the dentist and that no office protocol existed for reporting or recording injuries, such as needlesticks or other percutaneous injuries involving sharp instruments or devices. Anesthetic needles were either recapped by the dentist using a two-handed technique** or left uncapped and recapped by the assistant using a two-handed technique on completion of the dental treatment procedure. One seronegative staff person recalled sustaining an injury while washing sharp instruments, but no other specific incidents were reported by the staff. In addition, neither patient B nor patient C recalled, nor did review of the dental records indicate, any specific incidents that would have exposed them to the dentist's blood (i.e., an injury to the dentist, such as a needlestick or cut with a sharp instrument); however, no injury log was kept. The dentist could not be interviewed before his death regarding his care of these patients.

Staff members reported that barrier precautions had been introduced into the practice by early 1987 and that all staff, including the dentist, wore latex gloves and surgical masks for patient-care activities. Staff reported that they changed gloves and washed their hands between most patient contacts; occasionally, however, they washed gloves rather than changed them between patient contacts. Masks reportedly were changed infrequently. Staff reported that the dentist's use of gloves and mask and handwashing practices were similar to their own. None of the staff reported a history of dermatitis.

Staff reported that by 1987 all surgical instruments were autoclaved. Nonsurgical heat-tolerant instruments (e.g., dental mirrors) were autoclaved when practice conditions, such as time and instrument supply, allowed or were immersed in a liquid chemical germicide for varying lengths of time. Tests of the autoclave in October 1990 demonstrated that it was functioning properly. Dental equipment, such as handpieces, prophylaxis angles, and air/water syringe tips, were not autoclaved but were either wiped with alcohol or immersed in a liquid chemical germicide at irregular intervals. Some disposable items (e.g., saliva ejectors, high-speed evacuation tubes, and prophylaxis cups) occasionally were reused after being immersed in a liquid chemical germicide for varying lengths of time. Germicides known to be available in the dental office were isopropyl alcohol and 2% glutaraldehyde. The dental practice had no written protocol or consistent pattern for operatory cleanup and instrument reprocessing.

Office staff also reported that the dentist occasionally received prophylactic treatment from the hygienists; at least one hygienist topically treated an oral lesion of the dentist on one occasion in 1987. Reported by: JJ Witte, MD, Florida Dept of Health and Rehabilitative Svcs. Div of HIV/AIDS and Hospital Infections Program, Center for Infectious Diseases; Dental Disease Prevention Activity, Center for Prevention Svcs; National Institute for Occupational Safety and Health, CDC.

Editorial Note

Editorial Note: Based on the following considerations, this investigation strongly suggests that at least three patients of a dentist with AIDS were infected with HIV during their dental care: 1) the three patients had no other confirmed exposures to HIV; 2) all three patients had invasive procedures performed by an HIV-infected dentist; and 3) DNA sequence analyses of the HIV strains from these three patients indicate a high degree of similarity of these strains to each other and to the strain that had infected the dentist--a finding consistent with previous instances in which cases have been linked epidemiologically (3,4). In addition, these strains are distinct from the HIV strains from patient D (who had known behavioral risks for HIV infection), from the strains of the eight HIV-infected persons residing in the same geographic area, and from the 21 other North American isolates.

Because the dentist had known behavioral risk factors for HIV, his infection was probably not occupationally acquired. The precise mode of HIV transmission to patients A, B, and C remains uncertain. All three patients had invasive dental procedures performed by the dentist at times when he was known to be HIV-infected, with patients B and C each having multiple invasive procedures. Multiple opportunities existed for the dentist to sustain needlestick injuries (e.g., during administration of local anesthetics, two-handed needle-recapping procedures, and suturing) or cuts with a sharp instrument, particularly in poorly visualized operative sites. Although barrier precautions were reportedly used, these techniques were not always consistent or in compliance with recommendations. Furthermore, barrier precautions do not prevent most sharps injuries (e.g., puncture or cut wounds); therefore, the occurrences of puncture or cut wounds during treatment may have allowed the dentist's blood to enter an open wound or contact mucous membranes of a patient directly. Objective assessment of sharps injuries, beyond self-reports by the staff and a previous report by the dentist, was not possible (1).

Patients A, B, and C had invasive dental procedures performed after the dentist's diagnosis of AIDS, and two of the patients did not receive dental care from this dentist until after he had been diagnosed with AIDS and had evidence of severe immunosuppression (i.e., CD4 lymphocyte count less than 200/mm3). At this time, higher titers of virus may have been present in the dentist's blood and he may have been more likely to transmit virus than earlier in the course of his HIV disease (6).

Transmission might also have occurred by the use of instruments or other dental equipment that had been previously contaminated with blood from either the dentist or a patient already infected by the dentist. The office did not have a written policy for reprocessing dental instruments and equipment and reportedly did not consistently adhere to all recommended guidelines (7-11). However, this mode of transmission may be less likely than direct blood-blood transfer during an invasive procedure because HIV is present in blood at low concentrations, does not survive in the environment for extended periods, and has not demonstrated resistance to heat or to commonly used chemical germicides (7). The investigation suggested that the instances in which two of the three patients had appointments on the same day may have been chance occurrences. In addition, no invasive procedure was documented for patient B on the day both she and patient A visited the office, and the HIV status of patients A, B, and C is unknown for the days of their shared visits.

The precise risk for HIV transmission to patients during invasive procedures is not known but is most likely very low (1). Although AIDS has been recognized in the United States since 1981, the cases described here are the first in which such transmission has been reported.

Guidelines for prevention of transmission of HIV and other bloodborne pathogens in health-care settings have been published by CDC and others (7-12); these guidelines promote adherence to universal precautions, including prevention of blood contact between health-care workers and patients, and proper cleaning and sterilization or disinfection of instruments and other patient-care equipment.

CDC will convene a meeting in Atlanta on February 21-22 to review current information on risks of transmission of HIV and HBV to patients during invasive procedures and to assess the implications of these risks. Information regarding this meeting can be obtained from the meeting organizers, PACE Enterprises, at (404) 633-8610.

References

1. CDC. Possible transmission of human immunodeficiency virus to

a patient during an invasive dental procedure. MMWR 1990;39:489-93.

2. Ou CY, Kwok S, Mitchell SW, et al. DNA amplification for direct detection of HIV-1 in DNA of peripheral blood mononuclear cells. Science 1988;239:295-7.

3. Burger H, Gibbs R, Nguyen PN, et al. HIV-1 transmission within a family: generation of viral heterogeneity correlates with duration of infection. In: Brown F, Chanock RM, Ginsberg HS, Lerner RA, eds. Vaccines 90: modern approaches to new vaccines including prevention of AIDS. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory, 1990:255-62.

4. Balfe P, Simmonds P, Ludlam CA, Bishop JO, Brown AJL. Concurrent evolution of human immunodeficiency virus type 1 in patients infected from the same source: rate of sequence change and low frequency of inactivating mutations. J Virol 1990;64:6221-33.

5. Myers G, Rabson AB, Berzofsky JA, Smith TF, Wong-Staal F. Human retroviruses and AIDS, 1990. Los Alamos, New Mexico: Los Alamos National Laboratory, 1990.

6. Ho DD, Moudgil T, Alam M. Quantitation of human immunodeficiency virus type 1 in the blood of infected persons. N Engl J Med 1989;321:1621-5.

7. CDC. Recommendations for prevention of HIV transmission in health-care settings. MMWR 1987;36(no. 2S).

8. American Dental Association. Infection control recommendations for the dental office and the dental laboratory. J Am Dent Assoc 1988;116:241-8.

9. CDC. Recommended infection control practices for dentistry. MMWR 1986;35:237-42. 10. CDC. Guidelines for prevention of transmission of human immunodeficiency virus and hepatitis B virus to health-care and public safety workers. MMWR 1989;38(no. S-6). 11. CDC. Update: universal precautions for prevention of transmission of human immunodeficiency virus, hepatitis B virus, and other bloodborne pathogens in health-care settings. MMWR 1988;37:377-82,387-8. 12. Association for Practitioners in Infection Control/Society of Hospital Epidemiologists of America. Position paper: the HIV-infected healthcare worker. Infect Control Hosp Epidemiol 1990;11:647-55.

• Single copies of this article will be available free until

January 18, 1992, from the National AIDS Information Clearinghouse, P.O. Box 6003, Rockville, MD 20850; telephone (800) 458-5231. ** The interval during which at least two of these HIV-infected persons (patients A, B, and C) were patients of this dentist.

*** HIV exhibits considerable genetic variability, particularly in the gene for its envelope glycoprotein (gp120), and analyses of DNA sequences of this gene can be used to determine the relations of viruses infecting different persons. Analyses of multiple molecular clones of HIV obtained from an infected person can also define the range of genetic variation in the virus infecting that person. Sequence differences are least for viral clones obtained from a single infected person, intermediate for viruses from persons whose infections are epidemiologically linked, and greatest for viruses from persons whose infections are epidemiologically unrelated (5). **** To assure that no laboratory error occurred, DNA sequences from patients B, C, and D encoding the human leukocyte antigen DQ alpha were amplified by the polymerase chain reaction. The lengths of the sequences from these specimens were distinct from each other and from the sequence lengths found for the dentist and patient A (1), confirming that each of the samples represented a different person. As an additional verification of the source of each set of DNA sequences, DNA oligonucleotides corresponding to short sequences unique to the HIV strains from each of these three persons were used as hybridization probes. The probes hybridized only with DNA from the person from whose virus the probe was derived. ***** Needle-recapping procedure in which the syringe with exposed needle is held in one hand and the needle cap or sheath is held in the other hand.

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