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Am. J. Trop. Med. Hyg., 69(3), 2003, pp. 284-287
Copyright © 2003 by The American Society of Tropical Medicine and Hygiene

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SHORT REPORT: CRIMEAN-CONGO HEMORRHAGIC FEVER OUTBREAK IN RAWALPINDI, PAKISTAN, FEBRUARY 2002

MUHAMMAD NAUMAN ATHAR, HAIDER ZAIGHAM BAQAI, MASOOD AHMAD, MOHAMMAD ALI KHALID, NAGHMAN BASHIR, AHSAN MAQBOOL AHMAD, ABBAS HAYAT BALOUCH, AND KAUKAB BASHIR
Department of Medicine, and Department of Pathology, Holy Family Hospital, Rawalpindi Medical College, Rawalpindi, Pakistan; Department of Community Health Sciences, The Aga Khan University, Karachi, Pakistan

 

ABSTRACT

A nosocomial outbreak of Crimean-Congo hemorrhagic fever occurred in Rawalpindi, Pakistan in February 2002. The identified index case died shortly after admission to a hospital. Two of the health care workers became secondary cases; one of them died on day 13 after coming in contact with the index case. The other secondary case was successfully treated with oral ribavirin.

 

INTRODUCTION

Crimean-Congo hemorrhagic fever (CCHF) is endemic in Pakistan with sporadic outbreaks. The virus is one of the five genera in the family Bunyaviridae and mainly affects mono-nuclear phagocytes, endothelial cells, and hepatocytes, causing a severe hemorrhagic fever.1

It was first described in Crimea in the Soviet Union in 1944.2 In Pakistan, it was initially reported in 1976, when a laparotomy was performed on a patient with abdominal pain, hematemesis, and malena in a general hospital in Rawalpindi.3 Since then 12 outbreaks, mainly in western and north western regions of the country, have been reported.4 Outbreaks have also been reported from western province of Saudi Arabia,5 the United Arab Emirates,6 Kuwait,7 and Iraq.8 Case fatality is reported between 15% and 100%.1,9–11 Nosocomial outbreaks have been reported with a high mortality rate.3,6,8,12,13 Treatment of CCHF is with oral/intravenous ribavirin.14–21 Because of its transmissibility from domestic ruminant animals such as cattle, sheep, and goats, prevention is best achieved by educating the farming community and hospital staff.22 Duration of contact and type of exposure determine transmissibility.23

 

INDEX CASE

On February 12, 2002, a 25-year-old Kashmiri woman from Bagh in Azad Jammu and Kashmir, 100 km northwest of Rawalpindi/Islamabad, presented at a local health outlet with high grade fever accompanied with chills, rigors, and severe myalgias persisting for one week. Two days later, following the initial symptoms, she developed features of generalized coagulopathy with vaginal bleeding, hematemesis, and melena. After admission to a local hospital, her condition deteriorated and she was referred to Holy Family Hospital, a tertiary care center in Rawalpindi. At the time of her presentation, she was drowsy and febrile (temperature = 102°F), tachypneic with a respiration rate of 44/min, and hypotensive (blood pressure = 90/50 mm of Hg). There were multiple petechiae on her body, especially around the intravenous access sites and purpuric rashes on both forearms. A chest examination revealed bilateral coarse crepitations extending up to mid chest with decreased air entry at the bases. She responded only to painful stimulus (grade III coma) with no focal neurologic signs. Laboratory investigations revealed pancytopenia with a platelet count of 12 x 109/L (normal = 150–300 x 109/L), a serum urea level of 60 mg/dL (normal = 8–20 mg/dL), marked derangement of coagulation profile (prothrombin time [PTT] = 25 seconds [control = 13 seconds]; activated partial thromboplastin time [aPTT] = 78 seconds, [control = 26 seconds]; fibrinogen = 100 mg/dL [normal = 200–400 mg/dL]; and fibrin degradation products [FDPs] = 40 µg/mL [normal = <10 µg/mL]), and normal serum electrolytes. A chest radiograph was reported as normal and peritoneal ascites was seen on an abdominal ultrasonogram.

A provisional diagnosis of septicemia leading to disseminated intravascular coagulation (DIC) was made and the subject was treated accordingly. After transfusions of fresh frozen plasmas (FFPs), platelets, and red blood cell concentrates, her platelet count improved to 29 x 109/L. However, no improvement was observed in the coagulation profile (PTT, aPTT, fibrinogen, and FDPs). Twenty four hours after admission, the patient developed respiratory arrest and was placed on artificial ventilation, but four hours later she died. Since no suspicion of CCHF arose for this patient, no sample of serum was saved for retrospective detection of antibodies against CCHF virus.

 

SECONDARY CASE 1

During the period of stay of the index case in the intensive care unit, an attending intern physician, a 25-year-old woman, looked after the patient. At the time of respiratory arrest on the evening of February 12, the index case was revived successfully, during which time the intern also administered mouth-to-mouth resuscitation. She also had multiple contacts with blood and vomitus of the patient, but no needle stick injury was reported. The intern spent rest of the evening and night managing the patient until her death on the morning of February 13. She remained generally asymptomatic for the next four days except for mild fatigue. On the morning of February 18, she developed fever, shivering, and generalized weakness. She was taken to the emergency room and on suspicion of an acute malarial episode, was prescribed a course of an antimalarial and then discharged. Throughout the night she vomited and complained of mild generalized abdominal pain. In the early hours of February 19, she developed drowsiness and was admitted to the isolation room with a provisional diagnosis of enteric fever leading to septicemia.

At the time of admission, her clotting profile, liver functions (bilirubin = 0.3 mg/dL, alanine aminotransferase [ALT] = 32 units/L, and aspartate aminotransferase [AST] = 48 units/L), and platelet count (170 x 109/L) were within normal ranges. Vomiting improved by evening and she slept well throughout the night. A repeat of the coagulation profile on February 20 revealed deranged PT, aPTT (42 seconds and 45 seconds more than the controls, respectively), and a low platelet count (80 x 109/L). Levels of FDPs were elevated (28 µg/mL); however, the fibrinogen level was normal (250 mg/dL). Ten bags (each bag contains approximately 70–80 mL) of FFPs were transfused over the next 24 hours to correct the biochemical coagulation abnormalities. She remained afebrile, but by the evening of February 21 she started bleeding from multiple sites. Family attendants also reporting a single episode of aggressive behavior. The coagulation profile carried out on that day showed further derangements (PT = 64 seconds [control = 12 seconds]; aPTT = 77 seconds [control = 32 seconds]; platelet count = 28 x 109/L; FDPs = 1000 µg/mL; and fibrinogens = 100 mg/dL). Ultrasonography of the lower pelvis and abdomen showed peritoneal ascites and multiple cysts in the adenexae. Subsequent abdominal paracentesis revealed hemorrhagic fluid, and based on this evidence viral hemorrhagic fever was now thought of as a strong possibility. On the morning of February 22, she developed respiratory difficulty and marked drowsiness. She was shifted to the intensive care unit of the Pakistan Institute of Medical Sciences, an advanced tertiary care center, and intravenous ribavirin therapy was initiated after consultation with the epidemic investigation cell of the National Institutes of Health of Pakistan.20 The intern remained on an artificial respirator in critical condition and died on the morning of February 25, 2002 from hemorrhagic complications of CCHF infection. Blood samples of the patient were sent to the National Institute of Virology in Johannesburg, South Africa for serologic testing by an enzyme-linked immunosorbent assay (ELISA). The test results were positive for IgM antibodies against CCHF virus and were confirmed by a polymerase chain reaction for this virus.

 

SECONDARY CASE 2

Before the transfer of the index case to the intensive care unit from the general ward, she had profuse bleeding from oral cavity, rectum, vagina, and nasal orifices. An intern physician, a 27-year-old man, looked after the index case in the general ward, where he performed gastric lavage on her. The intern used latex gloves, but no face mask or eye shields were used. He reported contact with respiratory secretions of index case over his face while performing this procedure, which took approximately 45 minutes. He also reported soaking of sleeves of his white coat with patient’s blood. On February 17 (five days after initial contact with the index case), he developed generalized aches, pain, and malaise. A day later, he reported weakness, exhaustion, and severe generalized lower limb pain. By February 19, he had a fever (temperature = 101°F) and an episode of epistaxis, followed by severe drenching sweats four hours later. These symptoms persisted from February 19 to February 22, and during this whole period he remained on a liquid diet. Baseline investigations showed a total leukocyte count (TLC) of 2.3 x 109/L (neutrophils = 54%, lymphocytes = 41%) and a platelet count of 80 x 109/L. A coagulation screening was done at that time, which revealed a normal PTT and aPTT. He remained in state of fatigue and exhaustion from February 23 to February 26. He also reported bleeding gums on awakening in the morning. Further coagulation profiles done on February 26 showed a TLC of 3.7 x 109/L, a platelet count of 87 x 109/L, a prolonged aPTT of 50 seconds (control = 32 seconds), and a normal PTT.

Crimean-Congo hemorrhagic fever was suspected, and antiviral therapy (oral ribavirin) was started on February 26 and continued for 10 days (a loading dose of 2 grams, followed by 4 grams/day for 4 days and 2 grams/day for 6 days).9 The family effectively isolated the intern at home. Investigations done on day 7 of the treatment showed normalization of the TLC, platelet counts, and coagulation abnormalities. Samples dispatched to the National Institute of Virology in Johannesburg, South Africa tested positive for IgM and IgG antibodies to CCHF virus. The male intern is the only known secondary case of CCHF who survived this outbreak.

 

DISCUSSION

Crimean-Congo hemorrhagic fever virus can infect a wide range of domestic and wild animals, including sheep and cattle. Animals are infected with CCHF virus from the bite of infected ticks. Seroprevalence has been observed to be between 13% and 36% among animals.24,25 A number of tick genera are capable of becoming infected with CCHF virus, but the most efficient and common vectors for CCHF appear to be members of the genus Hyalomma.26 The most important source for acquisition of the virus by ticks is believed to be infected small vertebrates on which immature Hyalomma ticks feed. Once infected, the tick remains infected throughout its life, and the mature tick may transmit the infection to large vertebrates, such as livestock. Domestic ruminant animals, such as cattle, sheep, and goats remain viremic for one week after becoming infected. Humans may become infected with CCHF through transmission of virus from direct contact with blood or other infected tissues of livestock or from an infected tick bite. The majority of human cases have occurred in workers associated with livestock industry, agriculture, slaughterhouses, and veterinary practice. Seroprevalence is reported to be 13.1% among rural farmers in the northern Senegal22 and South Africa.27

Thirteen outbreaks of CCHF have been previously reported in Pakistan (Figure 1Go).3,4 The presently reported cases represent the fourteenth (eighth nosocomial) outbreak of CCHF in Pakistan and the second in Rawalpindi. Since January 1976, CCHF has caused 43 reported deaths.4 Rarely diagnosed, CCHF is known and feared among the medical staff in Pakistan.3



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  		    FIGURE 1. Crimean-Congo hemorrhagic fever (CCHF) in Pakistan, 1976–2002: Infected and fatal cases.4

 
The index case spent 36 hours in our hospital. There was no reported history of tick bite; however, she was a member of a shepherd’s family. The possibility of a Hyalomma tick bite or contact with infected animal blood cannot be ruled out. The patient may also have contracted the virus by handling infected meat of livestock. Blood samples of the index case for CCHF antibody testing were not taken since there was no suspicion of CCHF. Since viremia is more profound and intense in fatal cases, they have the greatest potential for nosocomial transmission.28,29 The secondary cases were most likely exposed to the index case in the hospital. Both of the secondary cases became symptomatic within five days of the exposure to index case. From her admission until her death, the index case was looked after by 12 health care workers. The physical contact of the female secondary case with the index case was of longer duration than any other.

Deaths have been reported to occur on days 5–14 of CCHF fever.30 The onset of DIC is unique to CCHF among the viral hemorrhagic fevers.31 The index case died of DIC-related complications on day 8 of the illness and both secondary cases developed DIC early in their disease.

During the first five days of illness, occurrence of any of the following clinical pathology values is >=90% predictive of a fatal outcome as calculated by method of Galen and Gambino:32 TLC >=10 x 109/L, platelet count <=20 x 109/L, AST >=200 units/L, ALT >=150 units/L, aPTT >=60 seconds, and fibrinogen <=110 mg/dL.30

Almost all pathologic parameters of the first secondary case had reached critical levels by day 5 of her illness. In comparison, these parameters for the other secondary case remained within normal limits during the same period (Table 1Go).


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TABLE 1
Predictors of fatal outcome within five days of onset of Crimea-Congo hemorrhagic fever (CCHF)30
 
An ELISA is currently the most sensitive test for the detection of antibodies against CCHF virus. However, it is cumbersome and time-consuming, which make it unsuitable for rapid diagnosis.33 We collected 50 samples from high-risk contacts of the index and secondary cases and sent them to the National Institute of Virology in Johannesburg, South Africa for detection of antibodies against CCHF virus. Two samples turned out to be positive for IgG and IgM antibodies against CCHF virus. No secondary cases were seen in the index case family. There were no tertiary cases noted.

In our experience, the post-exposure prophylaxis and treatment with oral/intravenous ribavirin in recommended doses has been found to be effective. Surveillance of cattle, control of ticks, rapid identification and isolation of cases, barrier nursing of the cases, and tracing and surveillance of contacts are necessary for best achieving prevention. There is a need to estimate the seroprevalence of CCHF among herds and shepherds because they have a high probability of being involved in an outbreak.

Received September 30, 2002. Accepted for publication June 4, 2003.

Acknowledgments: We are grateful to Samina Satti and Raja Mohammad Babar Akram (Department of Medicine, Holy Family Hospital, Rawalpindi, Pakistan) for reviewing the manuscript, and to Hamayun Asghar, Athar Saeed Dil (Public Health Division, National Institute of Health, Islamabad, Pakistan), and the staff of National Institute of Virology (Johannesburg, South Africa) for invaluable technical assistance. The authors are proud to be associated with Farzana Altaf, house physician at Holy Family Hospital, whose energy in improving standards was in the best traditions of our profession.

Authors’ addresses: Muhammad Nauman Athar, 436 South Lansdowne Avenue, Apartment # E-104, Yeadon, PA 19050, Telephone/ Fax: 610-394-6331, E-mail: drnaumanathar{at}yahoo.com. Haider Zaigum Baqai, Masood Ahmad, Mohammad Ali Khalid, Naghman Bashir, and Kaukab Bashir, Medical Unit II, Department of Medicine, Holy Family Hospital and Rawalpindi Medical College, Satellite Town, Rawalpindi, Pakistan, Telephone: 92-51-929-0321-27 extensions 272 and 277, Fax: 92-51-929-0518. Ahsan Maqbool Ahmad, Department of Community Health Sciences, Second Floor, Ibn-e-Ridwan Building, The Aga Khan University, Stadium Road, Karachi, Pakistan, Telephone: 92-21-4859-4923, Fax: 92-21-493-4294 and 92-21-493-2095. Abbas Hayat Balouch, Department of Pathology, Holy Family Hospital and Rawalpindi Medical College, Satellite Town, Rawalpindi, Pakistan, Telephone: 92-51-929-0321-27, Fax: 92-51-929-0518.

 

REFERENCES

  1. Burt FJ, Swanepoel R, Shieh WJ, Smith JF, Leman PA, Greer PW, Coffield LM, Rollin PE, Ksiazek TG, Peters CJ, Zaki SR, 1997. Immunohistochemical and in situ localization of Crimean-Congo hemorrhagic fever (CCHF) virus in human tissues and implications for CCHF pathogenesis. Arch Pathol Lab Med 1219: 839–846.
  2. Leshchinskaya EV, 1965. Crimean hemorrhagic fever (in Russian). Trudy Inst Polio Virus Entsef Akad Med Nauk SSSR 7: 226–236.
  3. Burney MI, Ghafoor A, Saleen M, Webb PA, Casals J, 1980. Nosocomial outbreak of viral hemorrhagic fever caused by Crimean Hemorrhagic fever-Congo virus in Pakistan, January 1976. Am J Trop Med Hyg 29: 941–947.
  4. Bosan AH, Kakar F, Dil AS, Asghar H, Zaidi S, 2000. Crimean-Congo hemorrhagic fever (CCHF) in Pakistan. Dis Surveillance 2: 4–5.
  5. Scrimgeour EM, 1995. Communicable diseases in Saudia Arabia; an epidemiological review. Trop Dis Bull 92: R79–R95.
  6. Suleiman MN, Muscat-Baron JM, Harries JR, Satti AG, Platt GS, Bowen ET, Simpson DI, 1980. Congo/Crimean haemorrhagic fever in Dubai. An outbreak at the Rashid Hospital. Lancet 2: 939–941.[Web of Science][Medline]
  7. Al-Nakib W, Lloyd G, El-Mekki A, Platt G, Beeson A, Southee T, 1984. Preliminary report on arbovirus-antibody prevalence among patients in Kuwait: evidence of Congo/Crimean virus infection. Trans R Soc Trop Med Hyg 78: 474–476.[Web of Science][Medline]
  8. Al-Tikriti SK, Al-Ani F, Jurji FJ, Tantawi H, Al-Moslih M, Al-Janabi N, Mahmud MI, Al-Bana A, Habib H, Al-Munthri H, Al-Janabi S, AL-Jawahry K, Yonan M, Hassan F, Simpson DI, 1981. Congo/Crimean haemorrhagic fever in Iraq. Bull World Health Organ 59: 85–90.[Web of Science][Medline]
  9. Fisher-Hoch SP, Khan JA, Rehman S, Mirza S, Khurshid M, McCormick JB, 1995. Crimean Congo-haemorrhagic fever treated with oral ribavirin. Lancet 346: 472–475.[Web of Science][Medline]
  10. el-Azazy OM, Scrimgeour EM, 1997. Crimean-Congo haemorrhagic fever virus infection in the western province of Saudi Arabia. Trans R Soc Trop Med Hyg 91: 275–278.[Web of Science][Medline]
  11. Khan AS, Maupin GO, Rollin PE, Noor AM, Shurie HH, Shalabi AG, Wasef S, Haddad YM, Sadek R, Ijaz K, Peters CJ, Ksiazek TG, 1997. An outbreak of Crimean-Congo hemorrhagic fever in the United Arab Emirates, 1994–1995. Am J Trop Med Hyg 57: 519–525.
  12. van de Wal BW, Joubert JR, van Eeden PJ, King JB, 1985. A nosocomial outbreak of Crimean-Congo haemorrhagic fever at Tygerberg Hospital. Part IV. Preventive and prophylactic measures. S Afr Med J 68: 729–732.[Web of Science][Medline]
  13. van Eeden PJ, Joubert JR, van de Wal BW, King JB, de Kock A, Groenewald JH, 1985. A nosocomial outbreak of Crimean-Congo haemorrhagic fever at Tygerberg Hospital. Part I. Clinical features. S Afr Med J 68: 711–717.[Web of Science][Medline]
  14. Watts DM, Ussery MA, Nash D, Peters CJ, 1989. Inhibition of Crimean-Congo hemorrhagic fever viral infectivity yields in vitro by ribavirin. Am J Trop Med Hyg 41: 591–595.
  15. Tignor GH, Hanham CA, 1993. Ribavirin efficacy in an in vivo model of Crimean-Congo hemorrhagic fever virus (CCHF) infection. Antiviral Res 22: 309–325.[Web of Science][Medline]
  16. Huggins JW, 1989. Prospects for treatment of viral hemorrhagic fevers with ribavirin, a broad-spectrum antiviral drug. Rev Infect Dis 11 (Suppl 4): S750–S761.
  17. McCormick JB, King IJ, Webb PA, Scribner CL, Craven RB, Johnson KM, Elliott LH, Belmont-Williams R, 1986. Lassa fever. Effective therapy with ribavirin. N Engl J Med 314: 20–26.[Abstract]
  18. Huggins JW, Hsiang CM, Cosgriff TM, Guang MY, Smith JI, Wu ZO, LeDuc JW, Zheng ZM, Meegan JM, Wang QN, 1991. Prospective, double-blind, concurrent, placebo-controlled clinical trial of intravenous ribavirin therapy of hemorrhagic fever with renal syndrome. J Infect Dis 164: 1119–1127.[Web of Science][Medline]
  19. Swanepoel R, Leham P, Abbott JC, Burt FJ, Grobbelaar AA, 1990. Epidemiology, diagnosis, clinical pathology and treatment of Crimean-Congo Hemorrhagic Fever (CCHF) in South Africa. Proceedings and Abstracts of the VIIth International Congress of Virology. Berlin, West Germany.
  20. CDC, 1988. Management of patients with suspected viral hemorrhagic fever. MMWR Morb Mortal Wkly Rep 37: 1–16.
  21. Fisher-Hoch SP, Price ME, Craven RB, Price FM, Forthall DN, Sasso DR, Scott SM, McCormick JB, 1985. Safe intensive-care management of a severe case of Lassa fever with simple barrier nursing techniques. Lancet 2: 1227–1229.[Medline]
  22. Chapman LE, Wilson ML, Hall DB, LeGuenno B, Dykstra EA, Ba K, Fisher-Hoch SP, 1991. Risk factors for Crimean-Congo hemorrhagic fever in rural northern Senegal. J Infect Dis 164: 686–692.[Web of Science][Medline]
  23. Altaf A, Luby S, Ahmed AJ, Zaidi N, Khan AJ, Mirza S, McCormick J, Fisher-Hoch S, 1998. Outbreak of Crimean-Congo haemorrhagic fever in Quetta, Pakistan: contact tracing and risk assessment. Trop Med Int Health 3: 878–882.[Web of Science][Medline]
  24. Gonzalez JP, LeGuenno B, Guillaud M, Wilson ML, 1990. A fatal case of Crimean-Congo haemorrhagic fever in Mauritania: virological and serological evidence suggesting epidemic transmission. Trans R Soc Trop Med Hyg 84: 573–576.[Web of Science][Medline]
  25. Morrill JC, Soliman AK, Imam IZ, Botros BA, Moussa MI, Watts DM, 1990. Serological evidence of Crimean-Congo haemorrhagic fever viral infection among camels imported into Egypt. J Trop Med Hyg 93: 201–204.[Web of Science][Medline]
  26. Hoogstraal H, 1979. The epidemiology of tick-borne Crimean-Congo hemorrhagic fever in Asia, Europe, and Africa. J Med Entomol 15: 307–417.[Web of Science][Medline]
  27. Fisher-Hoch SP, McCormick JB, Swanepoel R, Van Middlekoop A, Harvey S, Kustner HG, 1992. Risk of human infections with Crimean-Congo hemorrhagic fever virus in a South African rural community. Am J Trop Med Hyg 47: 337–345.
  28. Shepherd AJ, Swanepoel R, Leman PA, Shepherd SP, 1986. Comparison of methods for isolation and titration of Crimean-Congo hemorrhagic fever virus. J Clin Microbiol 24: 654–656.[Abstract/Free Full Text]
  29. Shepherd AJ, Swanepoel R, Gill DE, 1988. Evaluation of enzyme-linked immunosorbent assay and reversed passive hemagglutination for detection of Crimean-Congo hemorrhagic fever virus antigen. J Clin Microbiol 26: 347–353.[Abstract/Free Full Text]
  30. Swanepoel R, Gill DE, Shepherd AJ, Leman PA, Mynhardt JH, Harvey S, 1989. The clinical pathology of Crimean-Congo hemorrhagic fever. Rev Infec Dis 11 (Suppl 4): S794–S800.
  31. Fischer-Hoch SP, 1983. The haemostatic defect in viral haemorrhagic fevers. Br J Haematol 55: 565–571.[Web of Science][Medline]
  32. Galen RS, Gambino SR, 1975. Beyond Normality: The Predictive Value and Efficiency of Medical Diagnosis. New York: John Wiley and Sons.
  33. Shepherd AJ, Swanepoel R, Leman PA, 1989. Antibody response in Crimean-Congo hemorrhagic fever. Rev Infect Dis 11 (Suppl 4): S801–S806.



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M. N. ATHAR, M. A. KHALID, A. M. AHMAD, N. BASHIR, H. Z. BAQAI, M. AHMAD, A. H. BALOUCH, and K. BASHIR
CRIMEAN-CONGO HEMORRHAGIC FEVER OUTBREAK IN RAWALPINDI, PAKISTAN, FEBRUARY 2002: CONTACT TRACING AND RISK ASSESSMENT
Am J Trop Med Hyg, April 1, 2005; 72(4): 471 - 473.
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