http://www.annals.org/cgi/content/full/121/11/855

ARTICLE

Lack of HIV Transmission in the Practice of a Dentist with AIDS
Harold W. Jaffe; Joyce M. McCurdy; Marcia L. Kalish; Thomas Liberti;
Georges Metellus; Barbara H. Bowman; Sonia B. Richards; Annie R.
Neasman; and John J. Witte

1 December 1994 | Volume 121 Issue 11 | Pages 855-859

Objective: To determine whether dentist-to-patient or
patient-to-patient transmission of human immunodeficiency virus (HIV)
occurred in the practice of a dentist who had the acquired
immunodeficiency syndrome (AIDS).

Design: Retrospective epidemiologic investigation supported by
molecular virology studies.

Setting: The practice of a dentist with AIDS in an area with a high
AIDS prevalence.

Participants: A dentist with AIDS, his former employees, and his
former patients, including 28 patients with HIV infection.

Measurements: Identification of potential risks for acquisition of HIV
infection, genetic relatedness among HIV strains, and
infection-control practices.

Results: A dentist with known behavioral risks for HIV infection, who
was practicing in an area of Miami, Florida, that had a high rate of
reported AIDS cases, disclosed that he frequently did invasive
procedures and did not always follow recommended infection-control
procedures. Of 6474 patients who had records of receiving care from
the dentist during his last 5 years of practice, 1279 (19.8%) were
known to have been tested for HIV infection and 24 of those (1.9%)
were seropositive. Four other patients with HIV infection were
identified through additional case-finding activities. Of these 28
patients with HIV infection, all but 4 had potential behavioral risk
factors for infection. Phylogenetic tree analysis of HIV genetic
sequences from the dentist and 24 of the patients with HIV infection
showed an absence of strong bootstrap support for any grouping and
therefore did not indicate that the virus strains were linked.

Conclusions: Despite identifying numerous patients with HIV infection,
we found no evidence of dentist-to-patient or patient-to-patient
transmission of HIV during dental care. Our findings are consistent
with those of all previous studies in this area, with the exception of
one that did identify such transmission.

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The Florida Department of Health and Rehabilitative Services (HRS) and
the Centers for Disease Control and Prevention (CDC) have previously
described six patients who acquired human immunodeficiency virus (HIV)
infection while receiving care from a dentist with HIV infection
[1,2,3,4,5,6]. To date, this dentist's practice is the only practice
of a health care worker with HIV infection in which HIV transmission
to patients has occurred and has been reported. The events that
resulted in the infection of these patients remain unknown; however,
the available evidence suggests that HIV was transmitted from dentist
to patient rather than from patient to patient [7].
In July 1991, Miami newspapers published the name of another dentist
who had been diagnosed with the acquired immunodeficiency syndrome
(AIDS). This dentist had closed his practice 2 months earlier because
of ill health. To determine whether HIV had been transmitted to
patients during receipt of care in this practice, we investigated the
dentist's medical history, his dental practice, and his former
patients.

Methods  

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Discussion
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Epidemiologic Investigation

Information about the dentist's health was obtained from his available
medical records. Because the dentist was too ill to be interviewed,
information about his practice was obtained by interviewing his two
former employees, a dental assistant and an office manager.

The dentist's spouse provided HRS with the names and addresses of
those persons who had been patients of the dentist during the last 5
years of his practice; HRS sent a letter to each of these patients
telling them that they had received care from a dentist with HIV
infection and providing them with information about HIV counseling and
testing services. We reviewed the available dental and medical records
of all patients with HIV infection, and we interviewed all living
patients infected with HIV to determine whether they had behavioral or
transfusion risk factors for HIV infection.

Laboratory Investigation

We obtained a blood sample from the dentist with his consent. Blood
samples were also collected from all consenting patients with HIV
infection and from those of the patient's sexual partners who were
known to be infected with HIV. Mononuclear cells were separated from
the samples and DNA was extracted as previously described [8].

The primers MK603 and CO602 were used in a polymerase chain reaction
for primary amplification of approximately 1500 nucleotides of the C1
to gp41 domain of the HIV-1 envelope gene [9]. The primary amplified
DNA was then diluted 50-fold and used in a nested polymerase chain
reaction with the primers CL207 and CO72 to reamplify approximately
700 nucleotides of the C2 to C5 region [4]. The reamplified DNA was
purified by the Qiagen PCR Purification Spin Kit (Qiagen Inc.,
Chatsworth, California), and approximately 300 nucleotides of the V3
and flanking regions were sequenced in an automated DNA sequencer
(Applied Biosystems Inc., Foster City, California), either directly or
after being cloned into an M13 vector [4,9].

Genetic analysis was done on direct sequences from the dentist, 21
patients, and 2 sexual partners of patients. Direct sequencing of DNA
from its polymerase chain reaction product identifies the most common
nucleotide at each position from all the variants present within a
person. Only cloned sequences could be obtained from patients R, L,
and P. A consensus sequence was generated for patients L (10 clones)
and R (5 clones) based on the nucleotide present at each position in
at least 50% of the clones. Because patient P had only three clones,
it was difficult to generate a consensus sequence; thus, the longest,
most representative clone sequence was chosen for analysis.

Sequences were aligned by hand using ESEE2.00B [10]; sequence
positions that could not be aligned, as well as those in which one
sequence had an undetermined base, were eliminated from the analysis.
Two hundred fifteen alignable positions were used in phylogenetic
analysis. We calculated the number of base substitutions between each
of the sequences being compared to obtain a measure of the pairwise
genetic distances between the viruses of the persons studied. These
distances were used to construct a phylogenetic tree. Programs from
the PHYLIP suite, version 3.4, for Unix were used to construct the
neighbor-joining bootstrap tree shown in Figure 1RF 11 *. SEQBOOT was
used to create 1000 subreplicate sequence files; DNADIST returned a
distance matrix from each file, using a maximum-likelihood
multiple-hit correction; NEIGHBOR was used to construct a
neighbor-joining distance tree from each distance matrix; and CONSENSE
determined the percentage of replicate trees in which each internal
branch was present. This percentage, or bootstrap proportion, shows
how strongly phylogenetic analysis supports a particular grouping of
sequences.

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  Figure 1. Unrooted phylogenetic tree illustrating the relations
among HIV sequences obtained from the dentist, 24 of his former dental
patients, and 2 sexual partners of patients. Genetic distance
bootstrap results support only one pairing of sequences, that of O and
O-1, so the other branches are shown as a "star phylogeny." Branch
lengths are arbitrary





Results  

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The dentist was a man in his 60s who had known behavioral risk factors
for HIV infection and had had a positive HIV antibody test in June
1988. The reason for testing at that time is not known; the dentist
had no record of an earlier negative test. In November 1989, he was
asymptomatic and had a CD4+ T-lymphocyte count of 206
cells/microliters. By May 1990, his CD4 (+) lymphocyte count had
dropped to 69 cells/microliters and therapy with zidovudine and
aerosol pentamidine was started. In March 1991, he was hospitalized
with pneumonia of unknown cause that responded to therapy with dapsone
and trimethoprim. Human immunodeficiency virus encephalopathy was also
diagnosed, although a magnetic resonance imaging scan was normal. In
May 1991, the dentist was hospitalized after a syncopal episode in his
office. At admission, he stated that he had retired 3 months earlier,
but he apparently continued to provide care for a small number of
patients. According to his medical records, his recent memory was
impaired; a magnetic resonance imaging scan done at this time was
normal. After he was discharged from the hospital, he closed the
remainder of his practice. A month later, he was hospitalized with
diagnoses of staphylococcal sepsis, anemia, and HIV encephalopathy. He
died in a hospice in August 1991.

The dentist had practiced in the Liberty City area of Miami, Florida,
for almost 30 years and primarily served an indigent patient
population. According to his staff, he saw approximately 15 to 20
patients on a typical day and did extractions for about 5 patients per
day. Since 1986 or 1987, he had routinely worn gloves, a mask, and eye
protection. He recapped needles using a two-handed technique. Surgical
instruments were autoclaved and other instruments, such as curettes
and instruments used in restorative dentistry, were immersed in a
liquid chemical germicide called Cetylcide, which is a quaternary
ammonium compound (use of trade names is for identification only and
does not imply endorsement by the Public Health Service or the U.S.
Department of Health and Human Services). Dental handpieces were wiped
with alcohol but were not autoclaved.

Single-use, disposable pieces of equipment, such as prophylaxis cups,
were occasionally reused after being immersed in Cetylcide. Handpiece
and dental unit water lines were not flushed. Both staff members
reported that they had tested negative for HIV infection.

Of the 6474 letters sent to former patients of the dentist, 5469
(84.5%) were delivered. As a result of these letters and of newspaper
articles and other media coverage about the dentist, 1279 patients
were found to have been tested for HIV infection. Of these patients,
24 (1.9%) were seropositive. Additional case-finding activities
identified another 4 former patients who were infected with HIV or who
had AIDS. Thus, a total of 28 former dental patients with HIV
infection (designated A, B, D, E, F, G, H, I, J, K, L, M, N, O, P, Q,
R, S, T, U, V, W, X, Y, Z, BB, CC, and DD) were identified.

Sixteen of the 28 infected patients (57%) were female. The patients
ranged in age from 17 to 69 years (median, 35 years); 26 were
African-American, 1 was Hispanic, and 1 was Caucasian. Five patients
(H, U, X, CC, and DD) died of AIDS before or during the investigation.

Based on interviews with the patients and review of their medical
records, we placed patients in a mutually exclusive hierarchy of
potential risk categories for HIV infection Table 1. Although none of
the men acknowledged having practiced homosexual or bisexual
behaviors, 19 patients had engaged in drug use or in sexual behaviors
that could have resulted in HIV infection. An additional 5 patients
had had one or more sexually transmitted diseases. Only 4 patients
could not be placed in a potential risk category.

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  Table 1. Potential Risk Factors among Patients with HIV Infection
in a Florida Dental Practice





According to dental records, which were available for 22 patients, or
self-report, all but 4 of the 28 patients infected with HIV had
received care from the dentist in l988 or later, years during which
the dentist was known to have had HIV infection. During this time, 18
of the patients infected with HIV had a total of 24 invasive
procedures documented in their dental records Table 2. In most cases,
the invasive procedure was extraction or alveoplasty; none of the
documented procedures required the intraoral use of a dental
handpiece. In March 1988, patients Z and BB had extractions done on
the same day; this was the only common visit day recorded.

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  Table 2. Dates on Which Invasive Procedures Were Documented in
Patient Dental Records





Blood samples were obtained from the dentist and 24 of his former
patients. One of these patients, patient H, died during the
investigation, after a blood sample was collected. Three other
patients (X, CC, and DD) died before their blood samples could be
collected. The blood sample from patient U was broken in transit and
this patient died before another sample could be obtained. Samples
were also taken from the sexual partners of patients O and CC
(designated O-1 and CC-1, respectively); neither of these partners had
been a patient of the dentist.

The mean genetic distances between the viruses of the dentist and his
patients and between the viruses of the patients were 13.0% and 12.1%,
respectively Table 3, suggesting that these viral strains were not
similar. The smallest genetic distance, 5.8%, occurred between the
viral strains of patients K and Q; the dental visits of these patients
were separated by at least 5 years. On the other hand, the viruses of
patient O and her sexual partner, O-1, had a distance of 4.0%.

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  Table 3. Human Immunodeficiency Virus Nucleotide Diversity in the
V3 and Flanking Regions of the Envelope Glycoprotein gp120





The results of the genetic distance analysis were consistent with
those of the phylogenetic tree analysis, which indicated a lack of
similar viral sequences, with the exception of the sequences from O
and O-1 Figure 1. Support for phylogenetic relatedness can be
estimated by calculating bootstrap proportions Table 3. A bootstrap
proportion above 95%, such as that uniting the viral sequences of O
and O-1 (97.6%), indicates strong support for linkage between the
viruses. However, bootstrap proportions below 65%, which were found
for all other sequences including those from patients K and Q,
indicate that any similarity between these sequences may be the result
of chance alone [12].

For patients X, CC, DD, and U, no blood samples were available for HIV
DNA sequencing Table 4. Patient X had an ex-husband who was infected
with HIV and who was an injecting drug user. The viral strain of CC-1,
a woman infected with HIV who had been a regular sexual partner of
patient CC and who reported no other risk factors, differed from the
viruses infecting the dentist and his patients. If we assume that she
had been infected by patient CC, we may infer that patient CC was not
infected by the dentist. The medical records of patient DD show that
the patient's husband had had sexual contacts with prostitutes.
Patient DD's death certificate indicates that she was widowed. Her
dental records showed visits for construction and relining of
dentures, procedures that do not involve the intraoral use of sharp
instruments. Patient U died before she could be interviewed; no
information about her potential risk factors for HIV infection is
available. Her husband was located but failed to keep his appointment
for HIV testing.

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  Table 4. Characteristics of Patients with HIV Infection for Whom No
HIV DNA Sequences Were Available





Discussion  

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Discussion
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We found no evidence for dentist-to-patient or patient-to-patient
transmission of HIV infection during dental care, despite breaches in
recommended infection-control practices. Although we identified 28
patients with HIV infection who had been cared for by the dentist,
most of these patients had sexual or drug-related behaviors that
placed them at risk for HIV infection. The identification of numerous
persons infected with HIV in the practice of this dentist is not
surprising because the dentist worked in an area with a high rate of
reported AIDS cases (HRS. Unpublished data). Analysis of HIV
nucleotide sequences from the dentist and 24 of the patients infected
with HIV indicated that each was infected with a distinct viral
strain. This finding was consistent with epidemiologic data suggesting
that HIV transmission occurred in the community rather than in the
dental practice.

We must, however, acknowledge several limitations of our study.
Although the dentist cared for more than 6000 patients during the last
5 years of his practice, we obtained HIV antibody test results for
only 1279 of these patients. Other patients may have sought testing
from their own physicians or may have been tested anonymously at
public facilities. Given the intense publicity that accompanied this
case, we believe that most dental patients with HIV infection would
have been reported to HRS. However, we can exclude neither the
possibility that some patients with HIV infection were not tested for
HIV nor the possibility that some patients with positive test results
were not reported. Additionally, we could not obtain HIV sequence data
for four of the patients known to be infected with HIV, which
precluded us from definitively identifying the source of their
infections. However, one of these four patients had known behavioral
risk factors for HIV infection, one had a sexual partner whose HIV
strain was not similar to the strains infecting the dentist and other
patients, and one had had no invasive dental procedures.

Nucleotide sequence analysis was a powerful tool in the study of this
dental practice. Given the number of infected patients, which was
larger than that reported for any other practice, this analysis was
essential to the determination of whether the patients were infected
while receiving dental care. Because of the high mutation rate of HIV,
strains from epidemiologically unrelated persons are genetically
distinct. As we reported in the study of another Florida dental
practice, the presence of similar HIV sequences in different persons
implies an epidemiologic relation between those persons [4].
Conversely, in the present study, the lack of similar HIV sequences in
the dentist and his former patients implies that these persons
acquired their infections independent of one another. The only persons
with similar HIV strains were patient O and her sexual partner O-1, a
finding that validates our other sequencing results.

We found no evidence of patient-to-patient transmission of HIV within
this dental practice, but several of the dentist's infection-control
procedures, particularly his instrument reprocessing techniques, did
not accord with recommended practices [13]. If reusable dental
instruments contaminated with the blood or tissue of patients with HIV
infection are not appropriately cleaned and disinfected or sterilized
between uses, HIV can be transmitted to subsequent patients. In this
practice, for example, the dentist used a quaternary ammonium compound
to disinfect curettes, which cut soft tissues, and other nonsurgical
instruments used intraorally. Quaternary ammonium compounds are
low-level disinfectants and are not recommended for use on any
instrument used in the mouth [14]. In addition, between patients, the
dentist wiped the external surfaces of handpieces with alcohol but did
not autoclave them. Handpiece and dental unit water lines were not
flushed. Because the internal surfaces of handpieces may become
contaminated with patient material during use, retained patient
material can be expelled intraorally during use on subsequent patients
[15].

Recently, investigators from Australia reported patient-to-patient
transmission of HIV in the outpatient practice of a surgeon who was
not infected with HIV [16]. Four women were apparently infected on the
same day, while having skin lesions removed; the most likely source of
infection was a homosexual man who had also had a skin lesion removed
on the day the women were treated. Although the precise route of
transmission could not be determined, a failure of infection control
most likely resulted in transmission of HIV from the man to the four
women. No similar cases have been reported from the United States.

Results of this investigation and others indicate that the risk for
HIV transmission from an infected health care worker to his or her
patients is very small. In addition to this study, investigations
involving 12 499 patients of 32 dentists and dental students infected
with HIV have failed to document HIV transmission in the practice
setting (17-24; CDC. Unpublished data). No HIV transmission from
surgeons or obstetrician-gynecologists to patients has been reported.
Nonetheless, all health care workers infected with HIV should be
familiar with recommendations for preventing HIV transmission to
patients and should follow the specific guidelines that have been
implemented by their state or territorial health departments [25,26].

Acknowledgments: The authors thank Stacy Bourgeois, Mercedes
Escalante, Carol Trotter, Charlene Gilbert, Charlotte Gloster, and Tom
Walch for epidemiologic assistance; Claudiu Bandea, Chi-Ching Luo,
Nick De la Torre, and Jennifer Rapier for laboratory assistance; and
Robert Dumbaugh, Alan Lasch, and Donald Marianos for reviewing the
dental aspects of the investigation.

Author and Article Information  

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From the Centers for Disease Control and Prevention, Atlanta, Georgia.
The Florida Department of Health and Rehabilitative Services,
Tallahassee, Florida, and Miami, Florida. Roche Molecular Systems,
Alameda, California.
Requests for Reprints: Harold W. Jaffe, MD, Division of HIV/AIDS
(G29), Centers for Disease Control and Prevention, Atlanta, GA 30333.

References  

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Methods
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Discussion
Author & Article Info
References


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