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Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome

Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome
Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome

L7 (5?-CACCCCAGTCTTTCTTGAAA-3?) for cohorts 5–7, according to the method of Peret and colleagues,17 with conventional and real-time PCR for cohort 8, with use of a family-specific primer pair according to Drosten and colleagues11for cohort 9, for cohort 10 with use of N and F gene-based primers, and by nested PCR with use of the outer primer pair P9 (5?-GATCAACATATCT TCAGTCCAGAC-3?) and P10 (5?-AAAAGCATGATC CGATATGAACCC-3?) and L6 and L7 as inner primer pair for cohorts 11 and 12. In addition, for cohort 8 samples were inoculated onto HeLa, human embryonic lung, LLC, Madin-Darby canine kidney, and Vero cell lines for 28 days at 33oC.

For cohort 4, nasopharyngeal aspirate samples were inoculated onto LLC-MK2 rhesus monkey kidney cell and human laryngeal carcinoma cell (HEp-2) monolayers and incubated at 37oC for 12–14 days (HEp-2 cells) or 21 days (LLC-MK2 cells) in a roller tube culture system. These cell lines were selected based on the results of an initial assessment.18Irrespective of the presence of cytopathic effect, cell culture supernatants were testd for human metapneumovirus by nested RT-PCR with use of the outer primer pair (5?-AGCTGTTCCATTGG CAGCA-3?) and (5?-ATGCTGTTCRCCYTCAAC TTT-3?; R=A or G, Y=C or T) and the inner primer pair (5?-GAGTAGGGATCATCAAGCA-3?) and (5?-GCT TAGCTGRTATACAGTGTT-3?). All PCR products were confirmed by nucleotide sequencing. In addition, all cell cultures positive for human metapneumovirus rtPCR were passaged on to another LLC-MK2 rhesus monkey kidney cell culture tube and incubated for 21 days. Randomly selected supernatants of cell cultures with cyopathic effect were examined by electron microscopy for the presence of virus particles.

Macaque investigations

We made the virus stock used to inoculate cynomolgus macaques from the fourth passage of a SARS-CoV isolate, obtained from patient 5688, who died of SARS, and inoculated it on to Vero 118 cells cultured in Iscove’s Modified Dulbeco’s Medium (Bio Whitaker, Walkersville, MD, USA). After centrifugation at 270 g for 5 min, 1 mL samples were made from the supernatant and from the pelleted cells, which were resuspended in 5 mL medium. The titre of this virus stock was 1?106median tissue

culture infectious dose (TCID

50) per mL. All cell cultures

were done under biosafety level 3 conditions.

Four adult cynomolgus macaques, two males and two females, were placed in negatively pressurised glove

boxes. They were infected with 1?106TCID

50of SARS-

CoV suspended in 5 mL phosphate-buffered saline. 4mL was applied intratracheally, 0·5 mL intranasally, and 0·25 mL on each conjunctiva. We checked the macaques daily for clinical signs. Just before infection and at days 2, 4, and 6 after infection, we anaesthetised the macaques with ketamine and collected 10 mL blood from inguinal veins, and took nasal, oral, pharyngeal, and rectal swabs, which were placed in 1 mL virus transport medium.19From macaques 3 and 4, we also collected sputum samples by use of swabs under the tongue and sponges placed in the buccal cavity during anaesthesia. We extracted fluid from the sponges by centrifugation. The macaques were euthanised 6 days after infection by exsanguination under ketamine anesthesia.

We did necropsies of the macaques according to a standard protocol. For histological examination we collected the following tissues: adrenal gland, aorta, axillary lymph node, brachial biceps muscle, brain stem, caecum, cerebellum, cerebrum, colon, duodenum, eye,

eyelid, femoral bone marrow, heart muscle (left and right), ileum, inguinal lymph node, jejunum, kidney, lung (inflated with 10% neutral-buffered formalin), liver, mandibular lymph node, mesenteric lymph node, nasal septum, oesophagus, pancreas, primary bronchus, ovary, prostate, salivary gland, skin, spleen, stomach, testis, thymus, thyroid gland, tongue, tonsil, trachea, tracheobronchial lymph node, urinary bladder, and uterus. Tissues for light-microscope examination were fixed in 10% neutral-buffered formalin, embedded in paraffin, and 4?m sections were stained with haematoxylin and eosin. Selected lung sections were stained with monoclonal antibody AE1/AE3 (Neomarkers, Fremont, CA, USA) for the identification of epithelial cells, and monoclonal antibody CD68 (Dako, Glostrup, Denmark) for the identification of macrophages according to standard immunohistochemical procedures.

We developed an immunohistochemical method for detecting SARS-CoV antigen. Duplicate sections of all tissue samples were stained with an avidin-biotin complex peroxidase method. Paraffin was removed from sections, which were rehydrated and pretreated with protease (Sigma, St Louis, MO, USA) for 10 min at 37oC. Endogenous peroxidase was revealed with 4-chloro-1-naphthol (Sigma). Endogenous biotin was blocked with an avidin-biotin blocking kit (Vector Laboratories, Burlingame, CA, USA). Slides were briefly washed with 0·05% phosphate-buffered saline Tween 20 (Fluka, Buchs, Switzerland) and incubated with biotinylated purified human IgG from a convalescent SARS patient, negative control biotinylated purified human IgG, or the dilution buffer (phosphate-buffered saline containing 1% bovine serum albumin) for 1h at room temperature. After washing, sections were incubated with avidin-biotin complex-horseradish peroxidase (Dako) for 1h at room temperature. Horseradish peroxidase activity was revealed by incubating slides in 3-amino-9-ethylcarbazole (Sigma) solution for 10 min, resulting in a bright red precipitate. Sections were counterstained with haematoxylin. Tissue sections from cynomolgus macaques that had not been infected with SARS-CoV were included as negative controls. We included formalin-fixed, paraffin-embedded SARS-CoV-infected or uninfected Vero 118 cells in each staining as positive and negative controls, respectively. For negative contrast electron microscopy, samples of tissue culture supernatants were centrifuged at 17000 g at 4oC, after which the pellet was resuspended in phosphate-buffered saline and stained with phosphotungstic acid. Samples of lung from macaque 3 were fixed for transmission electron microscopy in 4% formaldehyde and 1% glutar(di)aldehyde after brief fixation in 10% neutral-buffered formalin, and post-fixed in 1% osmium tetroxide. After embedding in epoxy resin, thin sections were prepared, stained with 6% saturated uranyl acetate and lead citrate, and examined with a Philips Morgagni 268D electron microscope.

Samples from lung, duodenum, jejunum, kidney, liver, and spleen were collected post mortem for virus isolation and RT-PCR. Additionally, we collected the following samples for RT-PCR only: cerebellum, cerebrum, ileum, intestinal contents from the colon, mesenteric lymph node, nasal septum, pancreas, skin, spleen, stomach, tonsil, trachea, tracheobronchial lymph node, urinary bladder, and urine. From macaques 3 and 4, samples of intestinal contents from the jejunum, ileum, and caecum were also collected for RT-PCR. Intestinal contents were pretreated with stool transport and recovery buffer (Roche Diagnostics, Mannheim, Germany) before further processing. Tissue samples were homogenised in 4 mL transport medium19with Polytron PT2100 tissue grinders (Kinematica, Littau-Lucerne, Switzerland). After low-speed centrifugation, the homogenates were frozen at –70oC until inoculation on Vero 118 cell cultures in logarithmic dilutions. The infectious virus titres were expressed as TCID

50

/g of tissue. The identity of the isolated virus was confirmed as SARS-CoV by RT-PCR of supernatant.

We developed an RT-PCR with primers and probe specific for the nucleoprotein gene of SARS-CoV because the nature of the coronavirus replication cycle20suggested that such an assay may be more sensitive than RT-PCRs based on the polymerase gene, which are currently in use for diagnostics. Nucleic acid isolation was done on the Magnapure LC automated nucleic acid isolation system (Roche Diagnostics). Swabs, faeces, and serum were processed with the Magnapure LC total nucleic acid serum plasma blood isolation kit. Postmortem tissue samples were processed with the Magnapure LC RNA isolation kit I on the Magnapure LC station using the external lysis protocol. SARS-CoV RNA was detected on the ABI prism 7700, with use of the EZ rTtH RNA amplification kit (Applied Biosystems, Foster City, CA, USA). Primers SARSNP fpr1 (5?-CAAACATTGGCCG CAAATT-3?), SARSNP rpr1 (5?-CAATGCGTGACA TTCCAAAGA-3?), and probe SARSNP prb1 (5?-CACAATTTGCTCCAAGTGCCTCTGCA-3?) (Eurogentec) specific for the nucleoprotein (NP) gene of SARS-CoV were used for amplification. Amplification parameters were 2min at 50oC, 30 min at 60oC, 5 min at 95oC, and 45cycles of 30 s at 95oC, and 1 min at 62oC. We compared the sensitivity of the SARS-CoV NP rtPCR with a SARS-CoV polymerase rtPCR that used essentially the same methods with primers and probe specific for the SARS-CoV polymerase (SARSTM fpr1 5?-T G T G C G C A A G T A T T A A G T G A G A T G-3?, SARSTM rpr1 5?-CACCGGATGATGTTCCACC-3?, SARSTM prb1 5?-FAMTCATGTGTGGCGGCTCA CTATATGTTAAACC-TAMRA-3?). Serial dilutions of the SARS-CoV virus stock and SARS-CoV-infected Vero cells from patient 5688 were made and tested with the NP and polymerase-specific RT-PCRs.

Samples from the respiratory tract (nasal swabs, pharyngeal swabs, postmortem trachea, and lung samples) were also monitored for influenza A and B virus, respiratory syncytial virus A and B, rhinovirus, coronavirus (OC43 and 229E), and human metapneu-movirus with use of essentially the same RT-PCR methods but with specific primers.

We detected antibody to SARS-CoV in macaque sera by use of an indirect immunofluorescence assay. SARS-CoV-infected Vero 118 cells that had developed cytopathic effect were used to coat microscope slides. After incubation of the serum for 30 min at 37oC, slides were washed with phosphate-buffered saline and incubated with antihuman IgG, IgA, and IgM, conjugated with fluorescein thiocyanate (Dako). After washing and drying, slides were examined with a fluorescence microscope (Zeiss Axioscope, Oberkochen, Germany). We tested lung swabs and blood samples for bacterial pathogens at the Department of Medical Microbiology and Infectious Diseases, Erasmus MC, Rotterdam, Netherlands, by routine bacteriological methods (with blood agar, chocolate agar, and MacConkey agar) under aerobic and anaerobic conditions. Lung-tissue homogenates were tested for the presence of Chlamydia pneumoniae with PCR using universal primers for Chlamydia sp21and specific primers for C pneumoniae.22

Figure 1: Histological lesions in lungs from cynomolgus macaques infected with SARS-CoV

A: Early changes of diffuse alveolar damage, characterised by disruption of alveolar walls and flooding of alveolar lumina with serosanguineous exudate admixed with neutrophils and alveolar macrophages. B: More advanced changes of diffuse alveolar damage, characterised by thickened alveolar walls lined by type 2 pneumocytes, and mainly alveolar macrophages in alveolar lumina. C: Arrows show hyaline membranes on surfaces of alveoli. D: A characteristic change is presence of syncytia (arrowhead), here in the lumen of bronchiole. All slides haematoxylin and eosin stained.Figure 2: Immunohistochemical identification of cells in lungs from cynomolgus macaques infected with SARS-CoV

A: Arrows show enlarged type 2 pneumocytes with abundant vesicular cytoplasm and large nucleus containing prominent nucleolus that frequently occur along alveolar walls; haematoxylin and eosin. B: Epithelial origin confirmed by positive staining with monoclonal antibody AE1/AE3, a pan-keratin marker; avidin-biotin complex immunoperoxidase with diaminobenzidine substrate and hematoxylin counterstain. C: Arrows show alveolar macrophages that are common in alveolar lumina; haematoxylin and eosin. D: Macrophage origin is confirmed by positive staining with monoclonal antibody CD68, a macrophage marker; avidin-biotin complex immunoperoxidase with diaminobenzidine substrate and haematoxylin counterstain.

The main lesion in the consolidated pulmonary tissue of macaques 2–4 involved the alveoli and bronchioles, and consisted of areas with acute or more advanced phases of diffuse alveolar damage.

In such areas the lumina of alveoli and bronchioles were variably filled with protein-rich oedema fluid, fibrin, erythrocytes, and cellular debris, a moderate number of alveolar macrophages, and fewer neutrophils and lymphocytes (figure 1). The cytoplasm of some of these macrophages contained erythrocytes or pools of oedema fluid. There was extensive loss of epithelium from alveolar and bronchiolar walls. In areas with more advanced diffuse alveolar damage, the alveolar walls were moderately thickened and lined by cuboidal epithelial cells (type 2 pneumocyte hyperplasia), and the alveolar lumina contained mainly alveolar macrophages (figure 1). Regeneration of epithelium was seen in some bronchioles, visible as one irregular layer of squamous to high cuboidal epithelial cells with hyperchromatic nuclei. In some areas, the alveolar walls were lined by deep eosinophilic hyaline membranes (figure 1). There were occasional multinucleated giant cells (syncytia) in bronchioles and alveoli, either attached to the wall or free in the lumen (figure 1). These syncytia had up to about 30 peripheral nuclei, abundant hyaline eosinophilic cytoplasm, and, based on positive CD68 staining and negative pan-keratin staining, originated from marcophages. Enlarged type 2 pneumocytes with large vacuolated nuclei, prominent nucleoli and abundant vesicular cytoplasm were frequently found attached to the alveolar walls (figure 2). The epithelial origin of these cells was confirmed by keratin expression (figure 2). By contrast, alveolar macrophages had smaller nuclei, less prominent nucleoli, and were generally loose in the alveolar lumina (figure 2). The identity of these cells as macrophages was confirmed by CD68 staining (figure 2). Alveolar and bronchiolar walls were thickened by oedema fluid, mononuclear cells, and neutrophils. There were aggregates of lymphocytes around small pulmonary vessels. Moderate numbers of lymphocytes and macrophages were present in the lamina propria and submucosa of the bronchial walls, and a few neutrophils in the bronchial epithelium.

Changes in other tissues of macaques 2–4 were diffuse lymphoid hyperplasia and sinus histiocytosis of the tracheobronchial lymph nodes. Macaques 2 and 3 also had diffuse intrafollicular hyalinosis of the spleen. There were minimum multifocal inflammatory lesions in the pulmonary tissue of macaque 1, consisting of increased numbers of alveolar macrophages (about ten per alveolus) and occasional syncytia in alveoli and bronchioles.

With use of a biotinylated IgG fraction from a SARS patient, SARS-CoV expression was detected in a few to moderate numbers of alveolar epithelial cells (type 2 pneumocytes; figure 3) and rare intrabronchiolar and intra-alveolar syncytia (figure 3) in inflamed lung tissue of macaques 2–4. Positive immunohistochemical staining for SARS-CoV was visible as diffuse red-brown staining in the cytoplasm. The character of the staining was similar to that in SARS-CoV-infected Vero 118 cells (positive control), whereas non-infected Vero 118 cells and lung tissue from non-infected macaques (negative controls) were negative on staining. The other tissues in these three macaques, as well as the lung and other tissues of macaque 1, showed no SARS-CoV expression by immunohistochemistry.

Figure 3: Immunohistochemical detection of SARS-CoV in lungs

from experimentally infected cynomolgus macaques

A: Expression of SARS-CoV antigen by two alveolar epithelial cells,

probably type 2 pneumocytes. Immunoglobulin G fraction of convalescent

serum of SARS patient was used as specific antibody; avidin-biotin

complex immunoperoxidase with diaminobenzidine substrate and

haematoxylin counterstain. B: Expression of SARS-CoV antigen by

syncytium in lumen of alveolar duct. Small cell along the duct wall also

stains positive; avidin-biotin complex immunoperoxidase with 3-amino-9-

ethylcarbazole substrate and haematoxylin counterstain.

Figure 4: Electron microscopy of SARS-CoV in inoculum,

clinical samples, and tissue samples of experimentally

infected cynomolgus macaques

A: Negative-contrast electron microscopy of virus stock used to inoculate

cynomolgus macaques shows the typical club-shaped surface projections

of coronavirus particles; negatively stained with phosphotungstic acid,

bar=100 nm. B: Morphologically identical particles isolated from nasal

swabs of infected macaques; negatively stained with phosphotungstic

acid, bar=100 nm. C: Transmission electron microscopy of infected Vero

118 cell shows viral nucleocapsids with variably electron-dense and

electron-lucent cores in smooth-walled vesicles in the cytoplasm; stained

with uranyl acetate and lead citrate, bar=500 nm. D: Morphologically

similar particles occur in pulmonary lesions of infected macaques, within

vesicles of the Golgi apparatus of pneumocytes; stained with uranyl

acetate and lead citrate; bar=500 nm.

swabs (figure 4) and closely resembled those in the virus stock used to infect the macaques (figure 4). Virus was not detected in rectal swabs. SARS-CoV was isolated

from the lung (1?105TCID

50/g tissue) and kidney

(1?103TCID

50/g tissue) of macaque 2, and from the

lung (1?104TCID

50/g tissue) of macaque 4. No virus

was isolated from the postmortem samples of macaques 1 or 3. Several other tissues were positive only by RT-PCR (table 4). No macaque had detectable antibody to SARS-CoV by day 6 after infection.

Virological examinations of nasal and pharyngeal swabs, and tracheal and lung samples from all four macaques by RT-PCR for influenza A and B virus, respiratory syncytial virus A and B, rhinovirus, coronavirus (OC43 and 229E) and human metapneumo-virus were negative.

No relevant pathogens were identified on bacterio-logical culture of lung and blood samples. The lung homogenates tested negative for Chlamydia sp and C pneumoniae by PCR.

Discussion

According to Koch’s postulates, as modified by Rivers for virus diseases,23six criteria need to be fulfilled for a particular micro-organism to be the causal agent of a disease. Laboratory investigations of clinical and postmortem samples from SARS patients, as presented here and in earlier studies2,5,7,11already fulfilled the first three criteria—isolation of the virus from diseased hosts, cultivation in experimental hosts or host cells, and proof of filterability (to exclude larger pathogens). The results of our studies on SARS-CoV-infected macaques fulfill the remaining postulates—production of a comparable disease in the original host or a related species, and reisolation of the virus. Detection of a specific immune response to the virus after experimental infection was already reported.12Together, these findings prove that SARS-CoV is the primary cause of SARS.

The primary role of SARS-CoV in the cause of SARS is suggested by the cumulative studies at WHO laboratories, in which most SARS patients were diagnosed as having SARS-CoV infection, frequently in the absence of other respiratory pathogens. The most common co-infection in SARS patients was with human metapneumovirus. The SARS patients in cohort 4 co-infected with human meta-pneumovirus were mostly health-care workers from the same ward and who shared resting areas. The circulation of this infection among them during the SARS outbreak probably explains the frequency of the infection in cohort 4. Similarly, four SARS patients from Canada were infected with SARS-CoV and human metapneumovirus.5 The clinical symptoms of human metapneumovirus infection vary from mild upper-respiratory-tract disease to severe bronchiolitis and pneumonia.24The possible role of human metapneumovirus infection in exacerbating SARS remains to be assessed.

Alternative diagnoses, such as influenza, were occasionally made among patients fitting the case definition of SARS but testing negative for SARS-CoV infection. On the basis of the current case definition, therefore, disease from SARS-CoV infection overlaps with respiratory illnesses of other causes. Alternative diagnoses are most likely in geographical areas where SARS is not endemic.

The pulmonary lesions in SARS-CoV-infected macaques are comparable to those in SARS patients,2,4,5,7,8 and to those in other respiratory coronavirus infections, such as sialodacryoadenitis virus infection in rats,25and porcine respiratory coronavirus infection in pigs.26

Syncytia were found commonly in bronchioles, and less frequently in alveolar ducts and alveoli, of SARS-CoV-infected macaques. Syncytia also were prominent in the alveoli of SARS patients.3,7,8Based on expression of CD68 and pan-keratin, the syncytia were of histiocytic origin in macaques (this study), and of histiocytic or epithelial origin in SARS patients.8The formation of syncytia in these macaques may have been induced by SARS-CoV infection, because some syncytia were positive for SARS-CoV by immunohistochemistry, and the spike protein of coronavirus induces cell to cell fusion.20Pneumocytes showing cytomegaly, enlarged nuclei, and prominent nucleoli were common both in SARS-CoV-infected macaques (this study) and in SARS patients.2,8Such enlargement and cytologic atypia of hyperplastic type 2 pneumocytes occurs commonly in organising diffuse alveolar damage, and is non-specific.27

The development of a specific immunohistochemical test to identify SARS-CoV antigen in histological samples allowed us to assess the cell tropism of SARS-CoV infection in macaques. Expression of SARS-CoV in the lung was restricted to pneumonic areas and localised to the cytoplasm of type 2 pneumocytes and syncytia. The infection of type 2 pneumocytes by coronavirus was confirmed by transmission electron microscopy. These findings correspond to the detection of coronavirus-like particles in pneumocytes of a postmortem lung sample of a SARS patient,8and with the tropism of respiratory coronaviruses in pigs and rats for respiratory epithelium, and occasionally alveolar macrophages.25,26

On the basis of histological changes, SARS-CoV infection in the macaques primarily affected the epithelium of alveoli and bronchioles. At the time of euthanasia, 6 days after infection, most pneumonic areas showed early to advanced type 2 pneumocyte hyperplasia, indicating repair of alveolar walls after loss of type 1 pneumocytes. The temporal sequence of the histological changes corresponds with that of experimental infection with porcine respiratory coronavirus in pigs, in which acute changes (loss of epithelium, presence of macrophages and fibrin in airway lumina) were seen at days 2–6 after infection, and more advanced changes (type 2 pneumocyte hyperplasia, interstitial mononuclear cell infiltration) were seen from days 7–11 after infection.26Because diffuse alveolar damage from different causes follows a common pathway,27,28more chronic changes in these macaques probably would have included organisation of the intra-alveolar exudate, resulting in alveolar fibrosis and bronchiolitis obliterans, as seen in SARS patients who died later in the course of disease.3–5The development of fibrosis is dependent on the deposition of fibrin in the alveoli rather than on the continued presence of virus infection. Onset of fibrosis is a critical feature of chronic diffuse alveolar damage, because it leads to loss of alveolar function and is irreversible.27

In respiratory coronavirus infections in pigs and rats, viral infection of respiratory epithelium is maximum at days 3–4 after infection, and is no longer measurable by days 6–9.25,29The rapid disappearance of infected cells after initial infection might explain why SARS-CoV was not found in type 1 pneumocytes, and was only occasionally found in type 2 pneumocytes in these macaques. It also might decrease the chance of detecting SARS-CoV by immunohistochemistry in postmortem lung tissue of SARS patients who die after a protracted course of disease.

The lymphoid depletion of splenic follicles in experimentally infected macaques corresponds to that seen in a SARS patient8and in pigs infection with porcine respiratory coronavirus.29Based on these findings, together with the leucopenia observed in SARS patients,2–5we speculate that SARS-CoV infection suppresses immunity and may predispose infected hosts to secondary infections, such as in measles virus infection.30

Virological examination of clinical and postmortem samples of experimentally infected macaques indicates that the respiratory tract was the most important source of virus, as is probably the case in human beings.13Unlike in SARS patients,13SARS-CoV was not detected in urine or faeces of these macaques, although faeces did test positive in a previous experiment.12This finding may be partly explained by the early cut-off point of the experiment (6 days after infection), because SARS-CoV RNA was detected in the faeces of SARS patients in the late convalescent phase.11The sporadic detection by RT-PCR of SARS-CoV in the urinary bladder, stomach, duodenum, cerebrum, and spleen in infected macaques in the absence of evidence of viral replication—based on virus culture or immunohistochemistry—suggests overspill from other tissues, for example via blood. The isolation of SARS-CoV from the kidney of one macaque suggests viral replication at that site, but this theory could not be confirmed by immunohistochemistry.

The RT-PCR based on nucleoprotein primers proved to be about 100-fold more sensitive than the existing RT-PCR, based on polymerase primers. Presumably, this difference is due to the gradient in the transcription of coronavirus RNA, with high concentrations of nucleoprotein RNA and low concentrations of polymerase RNA.20

Collectively, these results of laboratory studies of SARS patients and experimental infections of macaques prove that the newly discovered SARS-CoV is the primary causal agent of SARS. Based on histopathological and immunohistochemical analysis of postmortem tissues of these macaques, SARS-CoV infection primarily affects epithelium of the lower respiratory tract, with potentially severe consequences for respiratory function.

Conflict of interest statement

None declared.

Contributors

T Kuiken and R A M Fouchier participated in the joint planning and coordination of the study. T Kuiken wrote the report and supervised and interpreted the pathology, immunohistochemistry, and electron microscopy components of the experimental infections. R A M Fouchier and M Schutten developed, supervised, and assessed the RT-PCR for SARS-CoV. G F Rimmelzwaan and G van Amerongen planned and carried out the infection experiments. D van Riel and J D Laman were involved in the design, execution, and assessment of the immunohistochemistry test to detect SARS-CoV in tissues. T de Jong did the electron microscopy and detected SARS-CoV in pneumocytes.

G van Doornum supervised the virological analyses of samples from the experimental infections. K St?hr participated as secretary of the WHO laboratory network on SARS diagnosis and played a substantial part in the initiation of the study. A D M E Osterhaus was the principal investigator and was responsible for the overall planning and coordination of the study. All other researchers were involved in the development, application, assessment of diagnostic tests on samples from SARS patients, or a combination of these.

Acknowledgments

We thank, at the Erasmus Medical Centre, Rotterdam, the staff of the histology and immunohistochemistry laboratories of the Department of Pathology for technical assistance; Alewijn Ott and Arjen van Vliet, Diagnostic Unit, Department of Medical Microbiology and Infectious Diseases, for bacteriological examination of macaque tissues; and

Alex van Belkum and Liesbeth van der Zwaan, Department of Medical Microbiology and Infectious Diseases, for examination of macaque lung homogenates for chlamydia. We thank Theo Bestebroer,

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胁患者生命。)[目前在国内外有一种糖尿病既是心血管病的理念正在叫响] 临床证明,糖尿病的关键在于胰岛功能障碍,致使胰岛素的分泌量和效用活性减少和降低,摄入的葡萄糖不能被机体充分利用,积聚于血液中而出现高血糖。所以单纯降糖只是治标之法。虽起效快,但其降糖作用的前提是胰岛功能尚可。随着病程的延长,降糖药剂量越来越大其两大弊病就会突显出来,其一是:由于长期大量的使用降糖药最终导致胰岛功能衰竭。其二是:化学降糖药对肝肾胃肠等脏器的副用,进一步加重了合并症的发展。 以上是西医对糖尿病的诊断与治疗方法,但是对于大数人们而言真正的认识糖尿病和了解糖尿病的人并不多,人们往往是通过一些所谓的指标来界定自己是否患病,其发病的机理和形成的原因并不清楚。[一般普遍认为发病原因是:自身免疫缺陷,遗传,肥胖,和年龄等诱因]。日常生活中大家都会有一种想法就是认为我不吃糖了就不会得糖尿病了,另一种就是你到医院医生都会告诉你糖尿病没有治,终身携带。为什么这样没有人告诉你知道。导致我们常常陷入误区而不清楚。大家常会认为血糖高就是糖尿病,到医院化个验血糖高,完了就是糖尿病了,从此帽子就戴上,一辈子也摘不掉了。可是什么是血糖没有人了解。 什么是:[血糖]:在讲血糖之前我们要先了解一下我们人体的消化系统,糖尿病是属于消化系统出了毛病。人体的消化系统有两大组织一是脾与胃肠,另一个就是肝胆,那么肝胆是怎么样帮我们消化的呢?肝与胆主要是负责消化肉食类与蔬菜,水果类。肝脏分泌胆汁给胆,胆在分泌胆固醇到胃,变成胆酸,胆碱,胆盐等很复杂的。脾胃主要帮我们消化五谷类食物。 现在我们再来了解一下血糖吧,我们吃的任何食物都是有养分的,不管什么东西咀嚼完了吞到胃里以后全部有一个名词就是—糖类。然后同胃部消化,消化三四个小时,消化完了给小肠,由它吸收养分,这些养分的医学名词就是血糖。脾脏{胰

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一、什么是糖尿病? 由于胰岛素绝对不足和相对不足引起的以高血糖为主要特征的全身心的内分泌疾病。 糖尿病分为两种:I型和II型。 I型糖尿病:占总数量的5%~10%;特征:胰岛素分泌绝对不足;发病人群:多在幼少年,一发现就必须注射直接补充胰岛素不足。 II型糖尿病:占总数90%~95%;特征:胰岛素分泌相对不足(胰岛素抵抗,胰岛素β细胞部分分泌障碍),血糖无法充分地被细胞吸收利用堆积在血液中,血糖变高就形成了II型糖尿病(多发人群45岁左右),II型糖尿病开始并没有特别症状,所以往往被忽视,直到发病后通过偶然发现。 注意:糖尿病人根本不是体内的糖多了,而是胰岛素不够,糖分吸收不了导致高血糖。 二、什么是胰岛素? 胰岛素是一种由人体胰岛β细胞分泌的蛋白质激素(在人体的十二指肠旁边,有一条长形的器官叫做胰腺,在胰腺中散布着许许多多的细胞群,叫胰岛)。 三、胰岛素作用: 胰岛素是机体内唯一降低血糖的蛋白质激素也是唯一同时促进糖原、脂肪、蛋白质合成的激素。 人在进食后,小肠吸收食物中的糖并转化为葡萄糖进入血液,这时候人的胰岛马上分泌胰岛素,葡萄糖在胰岛素与受体的情况下,随着血液进入肌体组织细胞中,供细胞吸收利用,同时把多余的葡萄糖合成糖原储存起来。 当人在空腹的时候胰岛β细胞就分泌胰岛素将储存的糖原和脂肪分解成葡萄糖释放到血液给细胞提供营养维持血糖的稳定。 四、糖尿病的诊断 两种检测指标:①血糖检测②糖化血红蛋白的检测 1.正常的血糖范围:空腹 3.9~6.1毫摩尔 餐后两小时 3.9~7.8毫摩尔 不正常的血糖范围:空腹血糖≥7.0 餐后两小时血糖≥11.1 (注:连续三次测量达到此项标准才能有效反映) 2.糖化血红蛋白的检测可以检测到120天平均的血糖浓度 糖化血红蛋白的正常范围:3.8%~6.5% 不正常:≥6.5% 五、糖尿病的危害及其症状表现 胰岛素长期的分泌不足导致血糖升高,血液中过量的葡萄糖会逐渐腐蚀全身器官,特别的心脑血管和神经组织的病变。 症状: 1.(分早期症状和后期并发症)合并症 早期:三多一少(多食·多尿·多饮·体重减轻)

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