THE ANATOMICAL RECORD (NEW ANAT.) 269:194 –197, 2002
ARTICLE
Infective Agents in Fixed Human Cadavers:
A Brief Review and Suggested Guidelines
DENIZ DEMIRYU¨REK,* ALP BAYRAMOGˇ LU, AND S¸EMSETTIN USTAC¸ ELEBI
Cadavers remain a principal teaching tool for anatomists and medical educators teaching gross anatomy. Infectious
pathogens in cadavers that present particular risks include Mycobacterium tuberculosis, hepatitis B and C, the AIDS
virus HIV, and prions that cause transmissible spongiform encephalopathies such as Creutzfeldt-Jakob disease (CJD)
and Gerstmann-Straussler-Scheinker syndrome (GSS). It is often claimed that fixatives are effective in inactivation of
these agents. Unfortunately cadavers, even though they are fixed, may still pose infection hazards to those who
handle them. Specific safety precautions are necessary to avoid accidental disease transmission from cadavers
before and during dissection and to decontaminate the local environment afterward. In this brief review, we describe
the infectious pathogens that can be detected in cadavers and suggest safety guidelines for the protection of all who
handle cadavers against infectious hazards. Anat Rec (New Anat) 269:194 –197, 2002. © 2002 Wiley-Liss, Inc.
KEY WORDS: cadaver dissection; education; medical curriculum; gross anatomy; infection; mycobacterium tuberculosis;
hepatitis; AIDS; HIV; prion; spongiform encephalopathy; Creutzfeldt-Jakob Disease; CJD
INTRODUCTION encephalopathies (Weed and Bag- INFECTIOUS DISEASES AND
genstoss, 1951; Brown et al., 1986;
Like all other occupations, being a Roth et al., 1992; De Craemer, 1994; THEIR AGENTS
member of an anatomy department Healing et al., 1995; Kappel et al.,
has its own risks. The potential infec- 1996; Catteneo et al., 1999). The em- Tuberculosis
tion hazard of human cadavers is one balming fluid used in anatomy depart-
of them. Cadavers are the main study- ments contains fixatives, disinfec- Tuberculosis is a slowly progressive,
ing materials of anatomists (Aziz et tants, glycerol, salts, and water. There chronic infection usually of the
al., 2002) but may pose infection risks lungs, but many other organs can
to people who handle them during Like all other become affected. The infective
embalming procedures or dissections. occupations, being a agent, M. tuberculosis, is an acid-
Infectious pathogens in the cadavers member of an anatomy fast, slender, beaded bacillus and
that present particular risks include department has its own can be cultured on Lo¨ wenstein-
Mycobacterium tuberculosis, hepatitis Jensen medium as rough, dry, and
B and C viruses, HIV, and prions risks. The potential yellow colonies (Sleigh and Tim-
that cause transmissible spongiform infection hazard of burry, 1998). Tuberculosis was one
human cadavers is one of the biggest killers among the in-
Drs. Demiryu¨ rek and Bayramogˇ lu are in fectious diseases in the past. The an-
the Department of Anatomy, Hacettepe of them. nual number of tuberculosis cases
University Faculty of Medicine, Ankara, continues to increase due to its
Turkey. They are interested in the occu- are inadequate data in the literature emergence in HIV infections. The
pational diseases of anatomists and about the disinfectant efficiencies of risk of acquiring tuberculosis varies
those who work with cadavers. Dr. Us- fluids used for embalming. The pur- according to occupation, and anat-
tac¸ elebi, of the Department of Clinical pose of this review is to draw atten- omy department workers are at par-
Microbiology at Hacettepe University tion to the infective agents that can be ticularly risk of contracting tubercu-
Faculty of Medicine, has the special detected in fixed human cadavers and losis carried by cadavers (Smith,
study topic of prion diseases. to suggest safety guidelines for the 1953; Kappel et al., 1996; Sterling et
*Correspondence to: Deniz Demiryu¨ rek, protection of all who handle cadavers. al., 2000). Of particular concern is
M.D., Ph.D., Hacettepe University Fac- the growing number of multiple-
ulty of Medicine, Department of Anat- drug–resistant strains that have
omy, 06100, Ankara, Turkey. Fax: ؉90- evolved in recent years.
312-310-71-69; E-mail: [email protected] or
[email protected] Transmission of M. tuberculosis is
thought to occur primarily by expo-
DOI 10.1002/ar.10143 sure to aerosolized infectious bacilli.
Published online in Wiley InterScience
(www.interscience.wiley.com).
© 2002 Wiley-Liss, Inc.
ARTICLE THE ANATOMICAL RECORD (NEW ANAT.) 195
Infected particles and splashes con- availability of cadaveric tissue as a tients after storage at 2°C for up to
taining tuberculous material can be transplantation material is often lim- 16.5 days after death (Douceron et al.,
acquired during respiration (Sloan, ited by pathogenic organisms which it 1993). Viable HIV was also isolated
1942; Harrington and Shannon, may contain. Specific serologic mark- from bone fragments, spleen, brain,
1976). The increased risk of tubercu- ers of hepatitis B and C viruses can be bone marrow, and lymph nodes from
losis among employees who handle detected in cadaveric tissue banks a patient with AIDS at autopsy 6 days
cadavers was demonstrated through (hepatitis B surface ag 18.1% and hep- postmortem (Nyberg et al., 1990). Al-
tuberculin skin testing (McKenna et atitis C ab 14.3%) (Barnett et al., though in suspension tests, 25% etha-
al., 1996; Gershon et al., 1998). 2001) and in postmortem blood tests nol and 0.5% formaldehyde were
for body donation programs (Roth et shown to be effective against HIV
It is generally thought that the risk al., 1992; Watkins et al., 1998). The (Sattar and Springthorpe, 1991), it is
of transmission is decreased by fixa- prevalence of HIV and hepatitis C not clear whether these concentra-
tion, and some authors agree with a markers has been studied among a tions are also effective in cadavers (De
commonly held belief that formalin cadaver population, and the cases rep- Craemer, 1994). On the other hand,
is tuberculocidal (Weed and Bag- resented a high prevalence of sero- cadavers infected with HIV are often
genstoss, 1951; Johnson et al., 1953; logic markers for HIV and hepatitis C infected with opportunistic infec-
Smith, 1953). Although it was previ- virus infection (Catteneo et al., 1999). tions, such as tuberculosis, which
ously reported that tubercle bacilli It has been reported that organ trans- may be more infectious then HIV in-
from cadavers were not infectious plantation from cadavers can trans- fection itself (Healing et al., 1995).
(Meade and Steenken, 1949) and trials mit hepatitis (Lutwick et al., 1983).
for culturing M. tuberculosis from Workers in morbid anatomy also face Prion Diseases and
10% buffered formalin-fixed pulmo- risk of contamination (Smith,
nary autopsy tissues have been unsuc- 1953),which raises serious questions Transmissible Spongiform
cessful (Kappel et al., 1996), it has about the infective hazards of cadav-
been shown that bacilli remain viable Encephalopathies
and, therefore, infectious for at least Can an individual who
24 to 48 h after an infected cadaver died of AIDS still be The transmissible spongiform encepha-
has been embalmed (Weed and Bag- lopathies (TSEs) are degenerative dis-
genstoss, 1951). There is also a case infectious at the time of eases of the central nervous system.
report describing the transmission of arrival in the anatomy Two of these found in humans are
M. tuberculosis from a cadaver to an Creutzfeldt-Jakob disease (CJD) and
embalmer during the embalming pro- department as a Gerstmann-Straussler-Scheinker (GSS)
cess, with the subsequent develop- cadaver? Unfortunately, syndrome. GSS is distinct from CJD;
ment of active tuberculosis (Sterling GSS is thought to be familial but is
et al., 2000). Based on the contradic- the answer is YES. known to occur sporadically as well.
tory published data, the disinfection CJD is characterized by loss of motor
properties of fixatives for tuberculosis ers and the effectiveness of fixatives control, dementia, paralysis, and death
infected tissue remain unclear. against hepatitis viruses. secondary to pneumonia.
Viral Hepatitis AIDS The infectious agent that causes
CJD has been called a prion and can
Hepatitis can be seen in many viral HIV, the cause of AIDS, is one of the be defined as small proteinaceous in-
diseases such as yellow fever, cyto- most intensively investigated viruses. fectious particles resistant to inactiva-
megalovirus and Epstein-Barr infec- The cytopathic effect of HIV on T4 tion by procedures that modify nu-
tion, and congenital rubella. However, helper lymphocytes causes the failure cleic acids. It might be transmitted by
viral hepatitis is caused by infections of the immune system and results in diet or after medical procedures such
by viruses that primarily target the AIDS. Human immunodeficiency vi- as surgery, cadaver pituitary-derived
liver. There are six types of hepatitis rus is an RNA virus with typical retro- growth hormone injections, and ca-
viruses: A, B, C, D, E, and F types. virus structure, and it is transmitted daveric dural grafts or cornea trans-
Hepatitis A is transmitted by the oral by similar routes as hepatitis B (Tim- plants (Billette de Villemeur and
route by means of food contaminated burry, 1997). Pradel, 1994; Budka et al., 1995).
with fecal matter. Hepatitis B is ex-
tremely infectious. It might be trans- Can an individual who died of AIDS Prion is highly resistant to conven-
mitted by blood or blood products, still be infectious at the time of arrival tional methods of sterilization and
sexual transmission, and skin pene- in the anatomy department as a ca- disinfection (Brown et al., 1982). It
tration through contact with infected daver? Unfortunately, the answer is has been shown that a related agent
material. Hepatitis C is transmitted by YES. Infectious HIV has been re- that causes scrapie survived inter-
the same routes as hepatitis B but is ported in pleural fluid, pericardial ment for 3 years with infectivity
probably less infectious (Timburry, fluid, and blood of such deceased pa- (Brown and Gajdusek, 1991). The CJD
1997). agent has been shown to survive well
in formalinized tissue, and it has been
Most of the studies made on cadav- experimentally demonstrated that
eric tissue donors revealed that the transmission of prion from formalin-
ized brain tissue to mice is possible
(Brown et al., 1986). Also, the CJD
196 THE ANATOMICAL RECORD (NEW ANAT.) ARTICLE
causative agent has been shown to ination of the dissection table should In suspension tests, these fixatives
stay infective in ash at 360°C after be avoided by a nonpermeable, dis- and disinfectants were shown to be
formaldehyde fixation (Brown et al., posable plastic sheet or similar mate- effective against most of the bacteria
1990). The evidence of risk to those rial (Budka et al., 1995; Healing et al., and viruses (Rutala, 1996). However,
who handle infected tissue has been 1995). it is not clear whether they are also
supported by case reports of this dis- effective in cadavers, for several rea-
ease in morbid anatomy workers Embalming Chemicals sons. First, in suspension tests, the
(Miller, 1988). cell-free infectious agent is tested,
Although embalming is thought to re- whereas in humans, some infective
PROCEDURES AND duce the infectious risks, there is in- agents (such as HIV) can localize
adequate information about the disin- within cells. Second, the concentra-
PRECAUTIONS fectant properties of fluids commonly tion of the embalming fluid compo-
used to embalm cadavers. The em- nents decreases as they diffuse
The information given above indi- balming fluid used in anatomy depart- throughout the human body. Third,
cates that a cadaver might be still in- ments contains fixatives, disinfec- several classes of products, includ-
fectious at the time of arrival in an tants, surfactants, buffers, glycerol, ing formalin, alcohols, and phenolic
anatomy department for subsequent salts, and water. The most frequently agents, are partially inactivated by the
educational purposes. Therefore, spe- used fixatives and disinfectants are presence of protein. This sensitivity to
cific safety precautions are mandatory formalin, ethanol, and phenol. For- organic load suggests that the effi-
from the moment of the cadaver’s ar- malin, a 37% aqueous solution of ciency of the disinfectants will be
rival at the facility. formaldehyde gas, inactivates infec- much lower in cadavers than in vitro
tious agents by forming covalent tests (De Craemer, 1994). Fourth, al-
Preparation for Dissection cross-links with several organic func- though a certain fixative at certain lev-
tional groups on proteins. Although els may be cidal to a single agent or
The corpse must have a detailed file, formaldehyde is known to be a high- even a group or class of infectious
indicating the reason of death and level germicide that has the capacity agents, other agents that co-exist may
containing previous hospital records to kill all microbes and viruses, it is survive as mentioned above; thus,
if possible. Working on cases known ineffective against the CJD agent as complete disinfection may not be ac-
to be infectious with M. tuberculosis, mentioned above. complished.
hepatitis B and C, HIV, and prions
should be avoided. Every cadaver Every cadaver should Postdissection Decontamination
should be regarded as an infectious be regarded as an
material. During the transportation infectious material. After the dissection is completed, tis-
process, disposable body bags must sue remnants, cutting debris, the
be used. The risk to department per- Ethanol is one of the most com- sheet covering the table, and all the
sonnel of respiratory tract pathogens monly used alcohols to control micro- disposable material should be dis-
from the deceased is probably remote, bial growth. Its mechanism of action carded within a plastic container as
even from the single exhalation of air involves protein denaturation and infectious hospital waste. All instru-
that occurs when the body is first lipid dissolution. Ethanol can be used ments that came into contact with po-
moved. Covering the face of the body alone in concentrations of 60 to 95% tentially infectious material must be
with a cloth would be a simple precau- or in combination with other antimi- decontaminated. Although the con-
tion (Healing et al., 1995). crobial agents in lower concentra- ventional methods of sterilization and
tions. It is known to be effective disinfection are effective for most of
Proper protective clothing must be against bacteria and fungi but not en- the infective agents, they do not de-
used by the department personnel dospores, nonenveloped viruses, or contaminate prions (Miller, 1988).
for avoiding accidental transmission prions. Specific measures must be used for
(CDC, 1988). Single-use latex exami- prions, and these measures will also
nation gloves must be worn whenever Phenol and its derivative phenolics be adequate for other infective agents.
handling bodies; they should be used exert antimicrobial activity by inacti- One of the most effective procedures
once only and then discarded. Safety vating essential cell enzymes and in- is steam autoclaving (instruments,
gloves (e.g., Teflon-made from spec- juring lipid-containing plasma mem- safety gloves, etc.) at 134°C with 30 lbs
tra, or metallic gloves) should be worn branes, which results in leakage of psi for 60 min (Committee on Health
over examination gloves to protect cellular contents. At concentrations Care Issues, 1986). Chemical decon-
from longer term exposure to chemi- above 1%, phenol and phenolics have tamination with 2 N NaOH for 1 h or
cal hazards and accidental penetrat- an antibacterial effect. They have a 1 N NaOH for 2 h is an alternative for
ing wounds. Filter masks must be broad spectrum of activity against nonautoclavable materials and sur-
used for respiratory protection from bacteria, viruses, and fungi, but they faces. It is not recommended to use
specific hazards, such as lead dust, are ineffective against prions. NaOH for aluminium material. Boil-
fungal spores, and aerosols. Face vi- ing of instruments in 3% sodium do-
sors should be worn for protection decyl sulfate (SDS) at least 3 min is
against hazardous splashes to eyes, another option. Autoclaving can be
nose, and mouth. Disposable aprons
or gowns must be used for protection
against splashes to the body. Contam-
ARTICLE THE ANATOMICAL RECORD (NEW ANAT.) 197
used either alone or in combination Brown P, Gibbs CJ, Amyx HL, et al. 1982. fixed autopsy tissue: Review of literature
with using SDS or NaOH. Alterna- Chemical disinfection of Creutzfeldt-Ja- and brief report. Hum Pathol 27:1361–
tively, 5% NaOCl (at least 20,000 ppm kob disease virus. N Engl J Med 306: 1364.
free chloride) can be used for 2 h, but 1279 –1282.
this chemical is very irritating and Lutwick LI, Sywassink JM, Corry RJ, Sho-
corrosive to steel (Tateishi et al., Brown P, Gibbs CJ, Gajdusek DC, Cathala rey JW. 1983. The transmission of hepa-
1991). F, LaBauge R. 1986. Transmission of titis B by renal transplantation. Clin
Creutzfeldt-Jakob disease from forma- Nephrol 19:317–319.
The environment should be cleaned lin-fixed, paraffin embedded human
with a phenolic disinfectant (contain- brain tissue. N Engl J Med 315:1614 – McKenna MT, Hutton M, Cauthen G,
ing 3–5% active ingredient) daily. This 1615. Onarato IM. 1996. The association be-
method is preferred to hypochlorite for tween occupation and tuberculosis: A
several reasons: hypochlorite is a corro- Brown P, Liberski PP, Wolff A, Gajdusek population based survey. Am J Respir
sive chemical and may damage surfaces DC. 1990. Resistance of scrapie infectiv- Crit Care Med 154:587–593.
or instruments; cleaning large areas ity to steam autoclaving after formalde-
with hypochlorite may liberate unac- hyde fixation and limited survival after Meade GM, Steenken W Jr. 1949. Variabil-
ceptable amounts of chlorine; and ashing at 360°C: Practical and theoreti- ity of tubercle bacilli in embalmed hu-
formaldehyde reacts with hypochlorite cal implications. J Infect Dis 161:467– man lung tissue. Am Rev Tuberc 59:429 –
to produce a potent carcinogen, bis- 472. 437.
chloromethyl ether (Gamble, 1977).
Budka H, Aguzzi A, Brown P, et al. 1995. Miller DC. 1988. Creutzfeldt-Jakob disease
CONCLUSION Tissue handling in suspected Creutzfeldt- in histopathology technicians. N Engl
Jakob disease and other human spongio- J Med 318:853– 854.
The potential infection hazard from form encephalopathies (prion diseases).
human cadavers is one of the risks of Brain Pathol 5:319–322. Nyberg M, Suni J, Haltia M. 1990. Isola-
being a member of an anatomy de- tion of human immunodeficiency virus
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working conditions for handling ca- Prevalence of HIV and hepatitis C mark-
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