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[08/04/2005]
 Sudan
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Author: Dr Francis J. LOUIS, Yaounde, Cameroon
Acknowledgements: Mme Dominique LOUIS-LUTINIER, Yaounde, Cameroon




> General Statistics | > Epidemiological facies | > Parasites and Chemoresistance | > Vectors and the Fight for Vector control | > Advice to travelers | > Further reading: 67 Biliographical references

 General Statistics

Area: 2,505,810 km2
Population: 36,080,373 inhabitants (2001 estimation)
Official Language: Arabic
Currency: Soudanese Dinar
Bordering Countries: Egypt, Libya, Chad, C.A.R, .D.R. of Congo, Uganda, Kenya, Ethiopia, Eritrea

Sudan is the largest country in Africa and because of this there are huge variations in the climate. Going from the driest to most humid regions one notes a gradient of north-south and west-east. The climate is tropical in the south and arid desert in the north. 

Very few epidemiological studies have been conducted in Sudan.  
The majority of those available were carried out in the centre of the country, to the east in the Blue Nile region, and in Karthoum.   
This is largely due to the turmoil that has shook the country for the last 30 years, rendering virtually impossible any study in the south, despite the fact that this remains the region most affected by malaria.

 Epidemiological facies

With regard to the epidemiology of malaria in Sudan, the country can be split into four zones:
.    The North and north-west are arid desert regions with no malaria.
.   The central eastern region in the Blue Nile zone has a short rainy season from June to August. Malaria thrives mainly from September to November, and is unstable, without acquisition of relative immunity. Malaria attacks therefore occur essentially between September and November (19, 62, 66)
.   The White Nile zone in the southern part of the country has a longer rainy season from March to October, with maximum rainfall from May to October   (during which rainfall does not however surpass the 150 mm mark) Malaria here is also unstable with high seasonal outbreaks from September to December (15). During the rainy season, parasites are found in 62.5% of children in school and 58% of children with fevers (15). Relative immunity occurs at the age of about 10 years old.
.   Karthoum, between the White Nile and the Blue Nile, suffers from an urban   hypo-endemic malaria. The rainy season lasts from August to October and no relative immunity is developed. During the rainy season, parasites are found in 1.08% of school children, 43.8% of children with fevers (15), 0.8% of refuges (45) and 1% of hospitalized patients in Omdurman (50).

A study conducted by G. and W. Wernsdorfer in 1959 was based upon the climatology of 6 places in Sudan:- Wadi Haifa, Port Sudan, Wad Madani, El Obeid, Wau and Juba (01):

Rainfall

Temperature 

Rainy Season 

Peak months

Maximum rainfall

Range(°C)

Peak(s)

Wadi Haifa
Port Sudan
Wad Madani
El Obeid
Wau
Juba

-
Oct-Dec
June-Oct
May-Oct
Mar-Oct
Mar-Oct

-
Oct-Dec
July-Aug
Aug-Sept 
July-Aug
May-Oct

-
< 50
130
100
200
150

20-35
25-35
25-35
20-30
25-28
26-28

July-Aug
July-Aug
May & Oct
May & Oct
none
none

 

 Parasites and Chemoresistance

Parasites 
Sudan is one of the rare regions in Africa where the four plasmodium species are found. The relative frequency of the species varies according to different studies:

In Karthoum: 
Plasmodium falciparum: from 84.9% to 100% (02, 15, 67)  
Plasmodium vivax: from 4.5% to 6.9% (02, 67) 
Plasmodium ovale: from 0 to 8.2% (02, 67) 
Plasmodium malariae: from 0 to 4.1% (02, 69) 

In the centre and East:
Plasmodium falciparum: from 90 to 95% (57, 59) 
Plasmodium vivax: 5% (57) 
Plasmodium ovale: not stated 
Plasmodium malariae: not stated 

In the south:
Plasmodium falciparum: from 83.9% to 7% (02, 15, 17) 
Plasmodium vivax: from 0 to 6.8% (02, 15, 17)  
Plasmodium ovale: from 0 to 1.2% (02, 15, 17 
Plasmodium malariae: from 1.6% to 7.7% (02, 15, 17) 

Plasmodium ovale is documented for the first time in Karthoum in 2000 (67).

Chemoresistance 

This is a badly documented domain.

Chloroquine resistance:

In 1978 at Sennar, in the east of Sudan, RL Kouznetsov et al. suspected as much: they achieved 100% good results in vivo, but had doubts on those in vitro (04). In the same year in Al Jazirah, Abdel Hamid Sayed Omer recorded 0.4% of type RI resistance and 0.2% of type RII (03). 
In 1981 in Karthoum, on 16 patients treated with chloroquine, there were 9 occurrences of   type RI resistance and 7 of type RII (06).
In 1984 in the Blue Nile Province, no in vitro resistance was proved (10)
In 1987 in Gedaref, 30 cases of drug failure were noted out of 63 (47.6%)(31).
In Asar (East) in 1991, 8 strains of Plasmodium falciparum out of 26, were resistant in vitro (30.8%)(33).
In 1992 in Wad Medani, out of 140 children aged between 6 months and 16 years old, suffering from fever, 19% were recorded as being RI and RII resistant (37).
In 1996 in Daraweesh, (east) 20 patients were treated with chloroquine: no resistance was recorded (63). In Waat, the Upper Nile Province, 4% of RI and 6% of RII resistances were noted in the case of 56 children treated with chloroquine (52).

So we can say that although chloroquine resistance exists, there have been no cases of the type RIII, and with the exception of the Gedaref study in 1988 the levels of resistance are low.

Resistance to other antimalarial drugs:

Very few studies have been published on this area.
.   amodiaquine: no publications
.   quinine: in 1993, out of 18 patients treated, clinical and parasitic clearance was achieved in under   48 hours, but 1 patient still had parasites on day 14, one on day 21 and   1 on day 28 (39).
.   mefloquine: in 1984, in the Blue Nile Province, not one of the 66 strains of plasmodium falciparum tested were resistant to mefloquine (10), the same results were achieved in 1991 in Asar   where not one of the   26 strains of Plasmodium falciparum showed resistance (30.8%)(33).
.   pyrimethamine: in Asar in 1991, 3 strains of Plasmodium falciparum out of   26 were resistant in vitro (11.5%)(33).
.   Sulfadoxine-pyrimethamine combination: in a 1997 in Daraweesh, 17 patients were successfully treated (63).
.   clindamycine: in 1985, out 20 patients treated, 3 were still parasite carriers on day 17 and 2   on day 28 (14).
.   Artemether: 100% success rate in a 1993 study(39). 

 Vectors and the Fight for Vector control

In this domain too, there is very little published material.
Vectors 
In 1983 in the Blue Nile Province, Anopheles funestus was predominant during the dry season, and Anopheles arabiensis during the rainy season (05).
In Daraweesh, the exclusive vector is Anopheles arabiensis. It proliferates during the rainy season (July to September) and survives in wells during the dry season (October to May) (59).
Still in the east of the country, a year 2000 study conducted in 40 villages allowed the capture of 2,162 female mosquitoes: 93% were Anopheles arabiensis and 7% Anopheles gambiae s.s. (64).

Vector control 
Only a 1983 study showed the effectiveness of malathion (07).

 Advice to travelers

In the “recommandations sanitaires pour les voyageurs 2005” (sanitary recommendations for travellers 2005) : B.E.H.  n°24-25 of 14th june 2005, Sudan is classified under chemoresistance group III ; that is to say, it is considered as being a country with “Widespread high chloroquine-resistance”, which would indicate a chemoprophylaxis with Mefloquine or with Atovaquone-Proguanil combined treatment.
In practice many things must be taken into consideration before deciding upon a treatment: the length of the dry season, the fact that there is little malaria in the capital and the relatively low chloroquine-resistance in the country. For most cases, individual measures of protection against mosquito bites (skin creams, mosquito bed nets treated with a long lasting insecticide) should be more than sufficient.

 Further reading: 67 Biliographical references

01 Wernsdorfer G., Wernsdorfer W. – Malaria im mittleren Nilbecken und dessen Randgebieten.  Z.  Tropenmed. Parasit. 1959 ; 18: 17-44.
02 Omer AHS – Species prevalence of malaria in Northern and Southern Sudan, and control by mass chemoprophylaxis.  Am. J. Trop. Med. Hyg. 1978 ; 27: 858-63.
03 Omer AHS – Response of Plasmodium falciparum in Sudan to oral chloroquine.  Am. J. Trop.  Med. Hyg. 1978 ; 27: 853-7.
04 Kouznetsov RL, Rooney W, Wernsdorfer WH, El Gaddal AA, Payne D, Abdalla RE   - Use of the in vitro microtechnique for the assessment of drug sensitivity of Plasmodium falciparum in Sennar, Sudan. Bull. WHO. 1980 ; 58: 785-9.
05 Jensen JB, Boland MT, Hayes M, Akood MA – Plasmodium falciparum: rapid assay for in vitro inhibition due to human serum from residents of malarious areas. Exp. Parasitol. 1982 ; 54: 416-24.
06 Al Tawil N, Akood MA – Response of falciparum malaria to a standard regimen of chloroquine in Khartoum Province, Sudan. East Afr. Med. J. 1983 ; 60: 663-8. 
07 Hemingway J – Biochemical studies on malathion resistance in Anopheles arabiensis from Sudan.  Trans. R. Soc. Trop. Med. Hyg. 1983 ; 77: 477-80.
08 Woodruff AW, Adamson EA, El Suni A, Maughan TS, Kaku M, Bundru N – Infants in Juba, Southern Sudan: the first six months of life. Lancet  1983 ; ii: 262-4.
09 Vande Waa JA, Jensen JB, Akood MA, Bayoumi R – Longitudinal study on the in vitro immune response to Plasmodium falciparum in Sudan. Infect. Immun. 1984 ; 45: 505-10.
10 Carlin JM, Vande Waa JA, Jensen JB, Akood MAS – African serum interference in the determination of chloroquine sensitivity in Plasmodium falciparum.  Z. Parasitenkd. 1984 ; 70: 589-97.
11 Bambauer R, Jutzler GA – Therapeutischer plasma-austausch bei schwer verlaufender malaria tropica. Dtsch. Med. Wschr.  1985 ; 110: 1290-3.
12 Mahmoud AA – Mosquitofish Gambusia affinis holbrooki as a malaria vector control agent in Gezira irrigation canals of The Sudan.  J. Am. Mosq. Control Assoc. 1985 ; 1: 524-6.
13 Shears P, Berry AM, Murphy R, Nabil MA – Epidemiological assessment of the health and nutrition of Ethiopian refugees in emergency camps in Sudan, 1985. Br. Med. J. 1985 ; 295: 314-8.
14 El Wakeel ES, Homeida MM, Ali HM, Geary TG, Jensen JB – Clindamycin for the treatment of falciparum malaria in Sudan.  Am. J. Trop. Med. Hyg.  1985 ; 34: 1065-8.
15 Taha TET, Broadhead RL – A comparative epidemiological study of malaria between children of Northern and Southern SudanJ. Trop. Pediatr.   1986 ; 32: 117-9.
16 Taha TET, Wahab MMA, Wallace HM – Morbidity patterns in a new paediatric hospital in Juba, Sudan.   Child   care health   dev.  1986 ; 12: 111-20.
17 Taha TET, Broadhead RL – Malaria in primary school children in Juba, Southern Sudan. East Afr. Med. J. 1986 ; 63: 546-9.
18 Bayoumi RA, Bashir AH, Abdulhadi NH – Resistance to falciparum malaria among adults in central Sudan.  Am. J. Trop. Med. Hyg. 1986 ; 35: 45-55.
19 El Samani FZ, Willett WC, Ware JH – Nutritional and socio-demographic risk indicators of malaria in children under five: a cross-sectional study in a Sudanese rural community.  J.  Trop. Med. Hyg.  1987 ; 90: 69-78.
20 Homeida M, Ismail AA, El Tom I, Mahmoud B, Ali HM – Resistant malaria and the Sudan floods. Lancet 1988 ; 2: 912.
21 Novelli VM, El Tohami TA, Osundwa VM, Ashong F – Floods and resistant malaria. Lancet 1988 ; 2: 1367.
22 Londner MV, Revel A, Rosen G, Shehata MG, Kemawi MA, El Said S, Said M, Spira DT – Dot-ELISA, a potential immunoassay for the detection of Plasmodium falciparum antibodies.  Trans. R. Soc. Trop. Med. Hyg. 1988 ; 82: 686-8.
23 Kano S, Takagi T, El Gaddal AA, Suzuki M – A new method of plasma collection suitable for large scale seroepidemiological surveys of malaria in the tropics.  Trans. R. Soc. Trop. Med.  Hyg. 1989 ; 83: 304.
24 Lienhardt C, Ghebray R, Candolfi E – Does chloroquine resistance occur in refugee camps in eastern Sudan.  Trans. R. Soc. Trop. Med. Hyg. 1989 ; 83: 486-7.
25 Taha AZ, Merghani OA – Community health in a rural area of Sudan. J. Community Health 1990 ; 15: 267-74.
26 Hviid L, Theander TG, Jakobsen PH, Abu-Zeid YA, Abdulhadi NH, Saeed BO, Jepsen S, Bayoumi RAL, Bendtzen K, Jensen JB – Cell-mediated immune responses to soluble Plasmodium falciparum antigens in residents from an area of unstable malaria transmission in the Sudan. A.P.M.I.S. 1990 ; 98: 594-604.
27 Toole MJ, Waldman RJ – Prevention of excess mortality in refugee and displaced populations in developing countries. J.A.M.A. 1990 ; 263: 3296-302.
28 Atabani GS, Saeed BO, El Seed BA, Bayoumi MA, Hadi NH, Abu-Zeid YA, Bayoumi RA – Hypoglycaemia in Sudanese children with cerebral malaria. Postgrad. Med. J. 1990 ; 66: 326-7.
29 Theander TG, Hviid L, Abu-Zeid YA, Abdulhadi NH, Saeed BO, Jakobsen PH, Reimert CM, Jepsen S, Bayoumi RAL, Jensen JB – Reduced cellular immune reactivity in healthy individuals during the malaria transmission season. Immunol. Lett.  1990 ; 25: 237-42.
30 Bayoumi RA, Abu-Zeid YA, Abdulhadi NH, Saeed BO, Theander TG, Hviid L, Ghalib HW, Nugud AHD, Jepsen S, Jensen JB – Cell-mediated immune responses to Plasmodium falciparum purified soluble antigens in sickle-cell trait subjects. Immunol. Lett.  1990 ; 25: 243-9.
31 Saeed BO, Hassabalrasoul MA, Ibrahim KE, Abdel-Karim EI, Salih SA, Hassan IM, Khider S, Bayoumi RA – Plasma chloroquine measurement in the evaluation of Plasmodium falciparum  sensitivity.  J. Trop. Med. Hyg. 1990 ; 93: 393-6.
32 Lienhardt C, Ghebray R, Candolfi E, Kien T, Hedlin G – Malaria in refugee camps in eastern Sudan: a sero-epidemiological approach.  Ann. Trop. Med. Parasitol. 1990 ; 84: 215-22.
33 Babiker HA, Creasey AM, Bayoumi RA, Walliker D, Arnot DE – Genetic diversity of Plasmodium falciparum in a village in eastern Sudan. 2 – Drug resistance, molecular karyotypes and the mdr1 genotype of recent isolates.  Trans. R. Soc. Trop. Med. Hyg. 1991 ; 85: 578-83.
34 Ibrahim ME, Awad-El-Kariem FM, El Hassan IM, El Mubarak ER – A case of Plasmodium falciparum malaria sensitive to chloroquine but resistant to pyrimethamine/sulfadoxine in Sennar, Sudan.  Trans. R. Soc. Trop. Med. Hyg. 1991 ; 85: 446.
35 Karim EA, Ibrahim KE, Hassabalrasoul MA, Saeed BO, Bayoumi RA – A study of chloroquine and desethylchloroquine plasma levels in patients infected with sensitive and resistant malaria parasites. J. Pharm. Biomed. Anal. 1992 ; 10: 219-23.
36 Aguiar JC, Albrecht GR, Cegielski P, Greenwood BM, Jensen JB, Lallinger G, Martinez A, McGregor IA, Minjas JN, Neequaye J, Patarroyo ME, Sherwood JA, Howard RJ – Agglutination of Plasmodium falciparum-infected erythrocytes from east and west African isolates by human sera from distant geographic regions.  Am. J. Trop. Med. Hyg. 1992 ; 47: 621-32.
37 Ibrahim AM, Ali FR, Ali ME – Assessment of chloroquine resistance of Plasmodium falciparum in children of Wad Medani   (Central Sudan).  J. Trop. Pediatr.  1992 ; 38: 162-6.
38 Nur ET – The impact of malaria on labour use and efficiency in the Sudan.  Soc. Sci. Med. 1993 ; 37: 1115-9.
39 Elhassan IM, Satti GH, Ali AE, Fadul I, Elkhalifa AA, Abedelrahim AM, Ming C, Theander TG – The efficacy of artemether in the treatment of Plasmodium falciparum malaria in Sudan.  Trans. R. Soc. Trop. Med. Hyg. 1993 ; 87: 685-6.
40 Dar FK, Bayoumi R, Al Karmi T, Shalabi A, Beidas F, Hussein M – Status of imported malaria in a control zone of the United Arab Emirates bordering an area of unstable malaria.  Trans.  R. Soc. Trop. Med. Hyg. 1993 ; 87: 617-9.
41 Taha T el T, Gray RH, Mohamedani AA – Malaria and low birth weight in central Sudan.  Am.  J. Epidemiol.  1993 ; 138: 318-25.42 Taha TE, Gray RH, Abdelwahab MM – Determinants of neonatal mortality in central Sudan.  Ann. Trop. Paediatr.   1993 ; 13: 359-64.
42 Taha TE, Gray RH, Abdelwahab MM – Determinants of neonatal mortality in central Sudan.  Ann. Trop. Paediatr.   1993 ; 13: 359-64.
43 Taha T el-T, Gray RH – Malaria and perinatal mortality in central Sudan.   Am. J. Epidemiol.   1993 ; 138: 563-8
44 Taha TE, Gray RH, Abdelwahab MM, Abdelhafeez AR, Abdelsalam AB – Levels and determinants of perinatal mortality in central Sudan. Int. J. Gynecol. Obstet. 1994 ; 45: 109-15.
45 Slutsker L, Tipple M, Keane V, McCance C, Campbell CC – Malaria in east African refugees resettling to the United States: development of strategies to reduce the risk of imported malaria.  J.Infect. Dis. 1995 ; 171: 489-93.
46 Taha Tel-T, Gray RH, Abdelwahab MM, Abdelhafeez A – Distribution and determinants of low birthweight in central Sudan. Paediatr. Perinat. Epidemiol. 1995 ; 9: 185-200.
47 A/Rahman SH, Mohamedani AA, Mirgani EM, Ibrahim AM – Gender aspects and women’s participation in the control and management of malaria in central Sudan.  Soc. Sci. Med. 1995 ; 42: 1433-46.
48 Babiker HA, Satti G, Walliker D – Genetic changes in the population of Plasmodium falciparum  in a Sudanese village over a three-year period.  Am. J. Trop. Med. Hyg.  1995 ; 53: 7-15.
49 Elhassan IM, Hviid L, Jakobsen PH, Giha H, Satti GM, Arnot DE, Jensen JB, Theander TG – High proportion of subclinical Plasmodium falciparum infections in an area of seasonal and unstable malaria in Sudan.  Am. J. Trop. Med. Hyg. 1995 ; 53: 78-83.
50 McCarthy MC, Haberberger RL, Salib AW, Soliman BA, El-Tigani A, Khalid IO, Watts DM – Evaluation of arthropod-borne viruses and other infectious disease pathogens as the causes of febrile illnesses in the Khartoum Province of Sudan. J. Med. Virol. 1996 ; 48: 141-6.
51 Roper C, Elhassan IM, Hviid L, Giha H, Richardson W, Babiker H, Satti GM, Theander TG, Arnot DE – Detection of very low level Plasmodium falciparum infections using the nested polymerase chain reaction and a reassessment of the epidemiology of unstable malaria in Sudan.  Am. J. Trop. Med. Hyg. 1996 ; 54: 325-31.
52 Guthmann JP, Cetre C, Suzan F, Darovare S, Morin F – Field research, relief work and war: does chloroquine-resistance occur in displaced populations of southern Sudan?  Trop. Doct.  1996 Apr ; 26 (2): 89-90.
53 Elzubier AG, Ansari EH, El Nour MH, Bella H – Knowledge and misconceptions about malaria among secondary school students and teachers in Kassala, Eastern Sudan.  J. R.  Soc. Health 1997 ; 117: 381-5.
54 Bayoumi RA, Dar FK, Tanira MO, Stephen RS, Hussein MM, Hammo NE, Omer RI, Beidas MF, Shalabi A, El-Wasila M – Effect of previous chloroquine intake on in vivo P. falciparum drug sensitivity.  East Afr. Med. J. 1997 ; 74: 278-82.
55 Cavanagh DR, Elhassan IM, Roper C, Robinson VJ, Giha H, Holder AA, Hviid L, Theander TG, Arnot DE, McBride JS – A longitudinal study of type-specific antibody responses to Plasmodium falciparum merozoite surface protein-1 in an area of unstable malaria in Sudan. J. Immunol  1998 ; 161: 347-59.
56 Arnot D – Unstable malaria in Sudan: the influence of the dry season. Clone multiplicity of Plasmodium falciparum infections in individuals exposed to variable levels of disease transmission.  Trans. R. Soc. Trop. Med. Hyg.  1998 ; 92: 580-5.
57 Babiker HA – Unstable malaria in Sudan: the influence of the dry season. Plasmodium falciparum population in the unstable malaria area of eastern Sudan is stable and genetically complex.  Trans. R. Soc. Trop. Med. Hyg. 1998 ; 92: 585-9.
58 Theander TG – Unstable malaria in Sudan: the influence of the dry season. Malaria in areas of unstable and seasonal transmission. Lessons from Daraweesh.  Trans. R. Soc. Trop. Med.  Hyg. 1998 ; 92: 589-92.
59 Roper C, Richardson W, Elhassan M, Giha H, Hviid L, Satti GMH, Theander TG, Arnot DE – Seasonal changes in the Plasmodium falciparum  population in individuals and their relationship to clinical malaria: a longitudinal study in a Sudanese village. Parasitology 1998 ; 116: 501-10. 
60 Babiker HA, Abdel-Muhsin AM, Ranford-Cartwright LC, Satti G, Walliker D – Characteristics of Plasmodium falciparum parasites that survive the lengthy dry season in eastern Sudan where malaria transmission is markedly seasonal.  Am. J. Trop. Med. Hyg. 1998 ; 59: 582-90.
61 Giha HA, Staalsoe T, Dodoo D, Elhassan IM, Roper C, Satti GMH, Arnot DE, Theander TG, Hviid L – Nine-year longitudinal study of antibodies to variant antigens on the surface of Plasmodium falciparum-infected erythrocytes. Infect. Immunol. 1999 ; 67: 4092-8.
62 Babiker HA, Abdel-Muhsin AA, Hamad A, Mackinnon MJ, Hill WG, Walliker D – Population dynamics of Plasmodium falciparum in an unstable area of eastern Sudan. Parasitology 2000 ; 120: 105-11.
63 Hamad AA, El Hassan IM, El Khalifa AA, Ahmed GI, Abdelrahim SA, Theander TG, Arnot DE – Chronic Plasmodium falciparum infections in an area of low intensity malaria transmission in the Sudan. Parasitology 2000 ; 120: 447-56.
64 Petrarca V, Nugud AD, Elkarim Ahmed MA, Haridi AM, Di Deco MA, Coluzzi M – Cytogenetics of the Anopheles gambiae complex in Sudan, with special reference to An. arabiensis: relationships with East and West African populations. Med. Vet. Entomol. 2000 ; 14: 149-64.
65 Donnelly MG, Townson H – Evidence for extensive genetic differentiation among populations of the malaria vector Anopheles arabiensis in Eastern Africa. Insect. Molecular Biology 2000 ; 9: 357-67.
66 Giha HA, Rosthoj S, Dodoo D, Hviid L, Satti GMH, Scheike T, Arnot DE, Theander TG – The epidemiology of febrile malaria episodes in an area of unstable and seasonal transmission.  Trans. R. Soc. Trop. Med. Hyg. 2000 ; 94: 645-51.
67 El Sayed BB, Arnot DE, Mukhtar MM, Baraka OZ, Dafalla AA, Elnaiem DEA, Nugud AHD – A study of the urban malaria transmission problem in Khartoum. Acta Tropica 2000 ; 75: 163-71.

 

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