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The diffusion of influenza in sub-Saharan Africa during the 1918–1919 pandemic
SW. Sci. Med. Vol. 17, No. 17, pp. 1299-1307,
1983
PrInted in Great Britain. All rights reserved
Copyright 0
0277-9536/83 $3.00 + 0.00 1983 Pergamon Press Ltd
THE DIFFUSION OF INFLUENZA IN SUB-SAHARAN AFRICA DURING THE 1918-1919 PANDEMIC K. DAVID PATTERSON* and GERALD F. PYLE? Department
of History and Department of Geography Carolina at Charlotte, UNCC Station,
and Earth Science, The University Charlotte, NC 28213, U.S.A.
of North
Abstract-The focus of this study is the spread of influenza in Africa south of the Sahara during the pandemic of 1918-1919. Most known types of diffusion pattern. i.e. radial, wave-like and linear, have been identified; however, the disease spread so rapidly that four particularly devastating linear patterns stand out. One of the most incredible aspects of the regularity in epidemic velocity along these pathways was that the colonial transportation network was of fairly recent origin. Given modern transportation linkages, the ever-present danger of the resurgence of the agent or agents that caused the pandemic could result in a much greater disaster in Africa and other Third World areas if unabated by effective inoculation programs.
unexplainable and uncontrollable in Africa as it was on other continents. The viral agent was, of course, still unknown and many colonial physicians suspected Pfeiffer’s bacillus or some other bacterium [6]. Even if the etiology had been understood, there was neither therapy for influenza itself nor treatment for the secondary bacterial pneumonias which killed many influenza victims. There were no effective vaccines and, in Africa as elsewhere, quarantines and restrictions on markets and other public gatherings made little difference. Physicians could do nothing but order rest and symptomatic treatment and record the epidemic’s progress [7].
The influenza pandemic (global epidemic) of I91 8-1919 was one of the most pervasive and devastating biological disasters since the bubonic plague of the fourteenth century. The pandemic struck almost every colony and community in sub-Saharan Africa. This article describes the spread of the disease and how it was influenced by the transportation system developed by the recently established European colonial powers. This study focuses on Africa south of the Sahara, as the sparsely populated desert made North Africa a separate epidemiological entity. THE GENERAL PROBLEM AREA Jordan’s estimates of approx. 21 million dead worldwide and 1.35 million dead in Africa (including North Africa) [I] have been widely quoted, although both figures are based on official reports and hence are quite conservative. For example, authorities in the British colony of Gold Coast (Ghana) guessed that about 60,000 people died; the real figure was closer to 100,000 [2]. In sub-Saharan Africa alone, at least I .5-2 million people died, probably the greatest short-term demographic disaster in the history of the region. As elsewhere, young adults suffered the heaviest mortality [3], in contrast to the usual pattern of excess influenza deaths among the elderly and the very young. However, despite the importance of the subject, only a few social scientists have written on influenza in Africa [4]. Influenza was not unknown in Africa prior to 1918. At least some areas were touched by the 1889-1893 pandemic and scattered cases were reported annually by medical authorites throughout the continent. The usual smattering of cases occurred in the early months of 1918, but nothing like the ‘spring wave’ noted in the United States [5]. The devastation of late 1918 and early 1919 was as totally unexpected,
SOURCES OF INFORMATION Data for this study come primarily from published government reports and a few contemporary articles in the medical literature. Reporting was spotty, in part because some documents simply ignore times and places of outbreaks and, more importantly, because of the weaknesses of colonial medical services and of colonial governments in general. European rule and frontiers were generally no more than three decades old. Large regions were still almost unadministered and medical staffs were small everywhere. We have, for example (see Table l), extensive data for the Gold Coast and for sparsely-populated Mauritania, very little for Zaire or Angola and nothing at all for vast and populous Sudan [8]. In general, we have much more information on West Africa than for the rest of the continent. Also, it must be noted that reports are often vague as to when influenza reached a region (‘late October’) and, even when an exact date was given, it may not accurately represent the first few cases. Further research in archives of various African states might produce useful information, but will probably not greatly modify the conclusions presented here [9].
*A portion of this study was supported by the National Library of Medicine and the National Institute of Health (Grant No. LM-02517). PResearch was also conducted under the National Science Foundation grant, “Simulation of Influenza Diffusion” (Grant No. SES-8200901). 1299
COLONIAL CONDITIONS CONTRIBUTING TO DIFFUSION Two factors associated with colonial rule helped to spread the disease. First, wartime disruption and
1300
K. DAVID PATTER~N and GERALD F. PYLE Table Place Angola Luanda Basutoland (Lesotho) Bechuanaland (Botswana) Belgian Congo (Zaire) Elisabethville Stanleypool Area (Kinshasa) Boma Matadi British Somalia Berbera Cameroun Douala Edea Eseka Y aounde Bamenda Ngaoundere Maroua Garoua Lere Cape Verde Islands SBo Vincente Chad Fort-Lamy ‘South Waddai Dahomey (Benin) Porto Novo Cotonou Abomey Grand Popo Zaenando Parakou Kandi Atacora Eritrea ‘Western’ Ethiopia Addis Ababa Harrar Danakil region French Somalia Djibouti Gabon Port-Gentil Libreville ‘North’ Gold Coast (Ghana) Cape Coast Accra Koforidua Saltpond Kumasi Winnebah Axim Tarkwa Obuasi Yeji Keta Bole Wa Tamale Tumu Zuarungu Guinea Conakry Mamou
1. Temporal
and spatial Date of first cases
spread
of influenza
No. of weeks
after 22 August
Linear diffusion pathway
Late Nov. Early Oct. Early Oct.
14 7 I
IV IV
3rd week Oct. 11 Nov.
8 12
IV IV
Mid-Nov. Mid-Nov.
13 13
Early
11
Nov.
15 Oct. 29 Oct. 29 Oct. 8 Nov. 20 Nov. 21 Nov. 3 Dec. 13 Dec. 13 Dec.
8 10 10 12 13 13 15 17 I7
11 Sept.
3
14 Dec. Jan., 1919 Mar., 1919
18 20 30
I Oct. 15 Oct. 22 Oct. 22 Oct. 30 Oct. 20 Nov. 24 Nov. I1 Dec.
7 8 9 9 10 L3 14 16
2 Dec.
15
Mid-Oct. 11 Dec. 8 Feb., 1919
8 16 25
Early
Oct.
17 Nov. 26 Nov. Approx.
15 Dee
III III III III III III III III
I 13 14 17
31 Aug. 3 Sept. 19 Sept. 21 Sept. 23 Sept. 24 Sept. 25 Sept. 25 Sept. 1 Oct. 8 Oct. 12 Oct. 26 Oct. 7 Nov. 12 Nov. 16 Nov. 21 Nov.
2 2 4 5 5 5 5 5 6 I 8 10 11 12 13 14
10 Sept. 12 Sept.
3 3
I I I I I I I I I I I I I I I I
-
first cases
19 Sept. 25 Sept. IO Oct.
No. of weeks after 22 August
4 5 7
29 Sept. IO Oct. 21 Oct. 26 Oct. 31 Oct. 5-20 Nov.
6 7 9 IO IO 12
23 Sept. Late Sept. Early Nov.
5 6 I2
5 Apr., 1919 I8 Apr., 1919 25 July, 1919 2 Aug., 1919
34 36 49 50
I5 Sept.
Linear diffusion pathway
I I I I I
-
4
Late Sept. IO Oct. I6 Oct. 20 Oct. 20 Oct. Jan., 1919 Jan., 1919 Feb.. 1919 20 Mar., 1919 25 Mar., 1919
5 7 8 9 9 21 21 25 30 31
10 Nov. Early Dec.
12 15
20 Oct.
9
22 Oct. 14 Nov. 20 Nov. 25 Nov. 28 Nov. 28 Nov. 1 Dec. 28 Dec.
9 12 I3 I4 14 I4 I5 19
II
14 Sept. I Oct. 5 Oct. 14 Oct. I5 Oct. 17 Oct. 31 Oct. Late Nov.
4 6 7 8 8 8 IO I4
II 11 II II II II II II
25 Oct.
10
IV
5 Nov. 9 Nov. 9 Nov. I8 Nov. 3 Dec.
II 12 12 I3 I5
1302
K. DAVID PATTER~N and GERALD F. Table
1. cont.
Date of first cases
Place Oubangui-Chari (Central African Republic) Kouango Bangui Fort-Sibut Fort-de Posse1 Fort-Crampel Dekoa Marali Haut-M’boumou Senegal Dakar St Louis Senegal River Vallev Sierra Leone ’ Freetown South Africa Durban Rand area Cape Town Kimberley Southern Rhodesia (Zimbabwe) Bulawayo Salisbury (Harare) Inyanga Melsetter Togo Lomt Uganda Entebbe Upper Volta Southwestern area L&o Zanzibar
15 Nov.
25 Nov. 14 Dec. 16 Dec. 16 Dec. 24 Dec. 26 Dec. Apr., 1919
PYLE
No. of weeks after 22 August
13 14 17 17 17 18 18 33
24 Aug. I Sept. 16 Sept.
3 4
22 Aug.
0
14 18 23 23
Sept. Sept. Sept. Sept.
4 4 5 5
IV IV
9 Oct. Mid-Oct. Jan., 1919 Jan., 1919
7 8 21 21
IV IV
9
I
22 Oct. Late Oct.
10
Early Nov. 19 Nov. 28 Oct.
11 13 IO
The first outbreak was in Freetown, 22 August, 1918. If applicable, see Fig. 3 and Table, p. 1305 for Spearman Rank-Order II-Nigeria; III-Benin (Dahomey); IV-South Africa/Congo.
movements of troops and laborers, especially in and near German colonies and in areas of heavy recruitment of soldiers and porters, was often locally significant. A more important factor was the newlycreated colonial transportation network (see Fig. 1). Railway lines, built by Europeans to facilitate economic exploitation and administrative control, generally linked ports to colonial hinterlands. Lines from the coast of the Belgian Congo and in the interior of French West Africa provided access to the Congo (Zaire) and Niger Rivers, both of which were major communications arteries. The rail network was most fully developed in southern Africa, where lines beginning in Cape Town and Durban extended northward through the Rhodesias to connect with the Congo River in Katanga (Shaba). Motor vehicles were not yet in widespread use, but some lorries and buses already contended with bicycle and pedestrian traffic on the roads which radiated from the towns and railways [lo]. PATTERNS OF DIFFUSION
Studies
of the spatial
diffusion
Linear diffusion pathway
of infectious
dis-
IV
Tests: I-Gold
Coast;
eases reveal several common phenomena: (1) extremely virulent agents can penetrate areas rapidly (especially when there are low immunity levels) and linear pathways result [l 11; (2) radical spatial diffusion takes place from the onset, with the disease spreading to places adjacent to the major pathways and beyond [12]; and (3) these forms of diffusion often coalesce into ‘clinical fronts’ [13], and, in many instances, spatial-temporal diffusion waves can be identified. The nature of the 1918-1919 disease agent was such that influenza seemed to rage through sub-Saharan Africa as though the colonial transportation network had been planned in preparation for the pandemic. Linear penetration and diffusion were followed by radial expansion and successive waves of influenza built up to sweep the area within a few months. Most of the southern part of the continent had been enveloped by the spring of 1919. The primary linear pathways are depicted in Fig. 2 and the temporal waves are shown in Fig. 4. The first place in sub-Saharan Africa to be hit by the virulent ‘fall wave’ was the busy harbor of Freetown, Sierra Leone, where influenza broke out on 22 August. It was apparently introduced by a ship
Influenza
mMa~or asslsted 1918
Fig.
railway I”
the
(south
lines
dlffuslon
of the
that
in sub-Saharan
Africa
during
1918-1919
probably
of Influenza
I”
Sahara)
I. Africa (south of the Sahara) during the 1918-1919 influenza pandemic. have not been named
from England, although a local viral mutation cannot be ruled out. Interestingly and inexplicably, severe influenza outbreaks began almost simultaneously in Boston, Massachusetts, and Brest, France [ 141. Freetown was the focus from which the disease spread to
Fig. 2. Known
primary influenza 1918-I 919 epidemic.
for purposes
Note some political
entities
of clarity.
all of West Africa. It diffused relatively slowly into the Sierra Leone hinterland, but was spread rapidly to other ports by coastal shipping. As early as 24 August, a Brazrhan warshtp trom Freetown was thought to have brought the disease to
diffusion pathways within Africa south of the Sahara Cities shown are clearly documented points of entry.
during
the
1304
K. DAVID PATTERSON and GERALII F. PYLE
Dakar and the capital of French West Africa was thoroughly infected within 10 days. Dakar served as a diffusion point for the disease into the savanna country of the West African interior. The disease quickly spread by rail north to St Louis by 7 September and east to Thies and Kayes. Boat traffic on the Senegal River was also an important means of spread. Influenza diffused more slowly over the countryside of Senegal and thence to Gambia and Guinea. Mauritania was infected from the Senegal valley by early October; the disease did not reach some of the remote northern cercles until March 1919. Influenza reached western Mali via the Senegal-Bamako railroad by mid-September and thence spread slowly eastward along the Niger River and across the savanna, reaching Upper Volta by late October and Niger soon after. The remote Bilma area of northeastern Niger was one of the very few places in Africa to escape infection [15]. Liberian authorities proclaimed and enforced a maritime quarantine, but influenza struck overland from the hinterland, reaching Monrovia in mid-November [16]. Meanwhile, an American ship, the Shonga, carried the disease from Freetown to Cape Coast and Accra, Gold Coast, on 31 August and 3 September respectively. From the coast, influenza spread quickly up the rail line to Ashanti and thence, at pedestrian speed, reached the Northern Territories by early November, where it met the wave sweeping eastward from Senegal [17]. A ship from the Gold Coast brought the malady to Lagos on 14 September; the Gold Coast authorities had not even bothered to telegraph a warning to their colleagues in Nigeria [18]. Infection rapidly spread north and east along river, road, and rail routes, reaching the north by mid-October and the Kamerun (Cameroun) and Niger borders by early November [19]. Douala, the major port of Kamerun, was infected by ship in early October; virtually the entire country was covered within 6 weeks [20]. In Gabon, a maritime quarantine prevented ships from West Africa from introducing the virus, but passengers from Matadi (Belgian Congo) infected Port-Gentil on 17 November. The epidemic quickly spread up the Ogowe River and to Libreville. Northern Gabon was attacked by influenza brought south from Kamerun by traders [21]. Luanda, Angola was attacked in late November. The most striking pathway was from South Africa northward through the Rhodesias and thence along the Congo River system almost to the Atlantic coast. Influenza reached South Africa by ship in September. However, there had been an abnormal number of mild cases for several previous months, so it is possible the spring wave had also been introduced to the country by sea. Durban harbor was infected on 14 September, probably from Asia and the disease reached the Rand 4 days later. Numerous cases were reported among African mine workers, but most were mild. Indeed, it is possible that the deadly fall virus did not arrive in South Africa until 23 September, when a ship carrying members of the South African Native Labour Corps reached Cape Town from Europe. The vessel had called at Freetown during the epidemic there. Acute influenza spread rapidly along the rail line to Bloemfontein, Kimberley and points
beyond, diffusing into the countryside from towns along the railway [22]. The railroad network made it possible for influenza to advance with remarkable speed in central Africa. Basutoland and Bechuanaland were infected in October and by 9 October railway workers in Bulawayo. Southern Rhodesia were reporting sick [23]. By late October. influenza had traversed Northern Rhodesia’s rail system and had reached the Katanga mining area [24]. Once in the Belgian Congo, the virus was carried along the Lualaba and the Congo by river steamers. Leopoldville (Kinshasa) and Brazzaville were infected by &IO November respectively. At about the same time, ships from Europe infected the ports of Matadi and Boma in Belgian Congo and Point-Noire in French Congo. Remarkably, however, most of equatorial Africa, including points as near the sea as Brazzaville and Leopoldville, was infected via Cape Town, not from the Atlantic [25]. A steamer from Leopoldville introduced the disease to Bangui, Ubangui-Chari, on 25 November. From here the disease spread northward along French porterage routes through the savanna to southern Chad, where in early January it met the West African waves of influenza which had reached Chad from Niger. Nigeria and Kamerun. The remote eastern codes of Ubangui-Chari were not attacked until April 1919, when influenza was introduced from adjacent parts of Sudan and the Belgian Congo [26]. The East African coast was generally infected by shipping from Asia. Beira, Mozambique was attacked on 20 October; from there the disease advanced up the Zambezi and Shire, reaching southern Nyasaland on 5 November. Ships from Bombay brought influenza cases to Mombasa by 23 September and to Zanzibar by 28 October. By the last week of October, the disease had advanced across Kenya on the Uganda railroad and had reached Entebbe, Uganda [27]. Also in October, ships from Aden and India brought the infection to the coasts of British and French Somalia and to Eritrea [28]. Pankhurst reports a major outbreak in Addis Ababa, Ethiopia by late August; this is surprisingly early and almost certainly represents the continuing activity of the spring wave, which did afflict Ethiopia, and/or faulty diagnosis. The more serious fall epidemic after broke out in the city in mid-October, progressing up the rail line from the port of Djibouti, French Somalia [29]. Madagascar, defended by a rigorous quarantine, was not attacked until April 1919, when the virus reached the island on a ship from France [30]. SOME NON-PARAMETRIC TESTS OF EPIDEMIC VELOCITY
In spite of some recent contentions that influenza viruses spread in a radical fashion outward from outbreak epicenters [31], our findings clearly show how the disease diffused along transportation routes. Statistical tests have been done with time and distance data for four of the major diffusion routes. Spearman rank-order correlations were computed by first converting distances traveled and time of first reporting by place to ordinal vectors. A perfect statistic indicating time of infection as a function of
Influenza
in sub-Saharan
Africa
during
1305
1918-1919
30007
Origins/Pathways -------GOLD 2500-
COAST (RS =.9271 -.----.-NIGERIA (Rs =.867) l l l l lBENIN(Dahomey) (RS =.971
200°-
-SOUTH
c
6 6 j 1500-
j
AFRICA/CONGO (Rs =.91 1)
: z lODo-
500 -
1 August
1 September
Fig. 3. Time-distance
traverses
for selected
distance using this method would be + 1.00 [32]. The actual time-distance plots are shown in Fig. 3. While these interval-scaled time-distance plots indicate the velocity of movement along the South Africa/Congo pathway was much more rapid than the other three, the ordinal ranking process nonetheless resulted in the following Spearman rank-order correlations: Pathway South Africa/Congo Gold Coast Nigeria Benin (Dahomey)
Spearman Rank-Order Correlation (R,) 0.911 0.927 0.867 0.971
These statistics give a strong indication of the devastating nature of the 1918-1919 influenza epidemic within sub-Saharan Africa. In fact, the disease is known to have had such velocities worldwide. The overall pattern in Fig. 4 also offers further support to the conventional belief that the pandemic did not originate in Africa. West and East Africa were infected separately, and the disease was first introduced at major ports. As described above, the earliest contacts with the disease were in August in coastal West Africa, and it has been assumed by many researchers for more than a half-century that the disease was carried from either Europe, South America, or both. If the African strain (or strains) did not result from local genetic changes, then where were the geographical origins of the pandemic? Unfortunately, the results of this analysis offer few clues to that mystery. LINKAGES
TO RECENT KNOWLEDGE INFLUENZA
November
October
OF
Most of the conventional wisdom that has accumulated both before and after the 1918-1919 pandemic implies that the disease usually originates in China or
major
diffusion
December
pathways.
elsewhere in Central Asia. The contention is that there is something about the ecology of that part of the world that facilitates the genetic recombination of influenza viruses. Still, similar conditions could exist in North or South America. At times, these genetic shifts are signaled by springtime ‘herald waves’ [33] of abnormally high reporting of influenza. During the spring of 1918-1919, as already mentioned, such phenomena occurred in both the United States and India [34]. A massive shift to a virulent strain with subsequent worldwide diffusion took place during the middle of 1918. The shift could have taken place anywhere on the planet, including the southern hemisphere during the winter there. The passage of time seems to diminish the importance of such speculations about the geographical origins of the 1918-1919 pandemic, but recent fears of a ‘swine fu’ epidemic have led to the re-examination of many aspects of the event. While the agent(s) causing the 191&1919 pandemic are still not clearly known, many virologists have long suspected the strain of influenza that is annually responsible for the winter-spring deaths of many hogs to have been responsible for the World War I event. The 1976-1977 wintertime influenza inoculation program within the United States was based largely on that premise [35]. While the program was a qualified success with regard to the reduction of overall influenza mortality, the feared ‘swine flu’ epidemic fortunately never happened. Instead, a viral strain perhaps more distantly related to the 1918-1919 agent(s) surfaced in the late 1970s and early 1980s. The genetic shift was not massive and the prevailing strain is not particularly virulent. Comparisons of the diffusion of influenza during the earlier pandemic are still useful in determining the severity of influenza strains and the establishment of inoculation programs.
1306
K.
Months with documented
DAVID
PATTERSON and GERALD F. PYL.E
penetration
August
September
Fig. 4. Waves
pJ
October
pJ
November
q
December
of influenza
diffusion
in Africa
(south
REFERENCES
4.
5.
6.
7. 8.
9.
IO.
Jordan E. 0. Epidemic InJluenzu: A Survey, pp. 229-230. Chicago, 1927. Patterson K. D. The influenza epidemic of 1918 in the Gold Coast. To appear in J. Afr. Hist. Patterson K. D. The demographic impact of the 1918-1919 influenza pandemic in sub-Saharan Africa: a preliminary assessment. In African Historical Demography, II (Edited by Fyfe C. and McMaster D.). pp. 401433. Centre of African Studies, University of Edinburgh, I98 I. Phimster 1. R. The ‘Spanish’ influenza pandemic of I9 I8 and its impact on the Southern Rhodesian mining industry. Central Afr. J. Med. 19, 143-148, 1973; Pankhurst R. The ‘Hedar Basita’ of 1918. J. Ethiopian Stud. 13, 103-131, 1975; Ohadike D. H. The influenza pandemic of 1918-1919 and the spread of cassava cultivation on the Lower Niger: a study in historical linkages. J. A@. Hisr. 22, 379-391, 1981. Collins S. D. Age and sex incidence of influenza and pneumonia morbidity and mortality in the epidemic of 1928-29 with comparative data for the epidemic of 1918-1919. Publ. Hith Rep. 46, 1909, 1931. Burnet F. M. and Clarke E. Influenza: A Suwey qf the Last Fifty Years in the Light qf‘ Modern Work on the Virus of Epidemic Ifluenzu, pp. 69-99. Macmillan, Melbourne, 1942. See Refs [2] and [4]. The late Gerald W. Hartwig found no materials on influenza in the official archives in Khartoum. Ahmed Bayoumi does not mention the epidemic in his The History of Sudan Health Services, Nairobi, 1979. Relevant materials probably exist in some countries. as in Ghana. Marc Dawson of Union College and Rita Headrick of the University of Chicago generously provided archival data on Kenya and French Equatorial Africa respectively. Oliver R. and Atmore A. Afticrr Since 1800, pp. 18&200. Cambridge University Press. Cambridge, 1967.
of the Sahara)
II. 12. 13.
14.
I5
I6
I7 18 19 20
21
22. 23. 24.
25. 26. 21.
28. 29.
during
the latter
half of 1918
Pyle G. F. The diffusion of cholera in the United States in the nineteenth century. Geogr. Ano/. 1, 59-75. 1969. Stock R. Cholera in Africa. International African Institute, London. 1976. Brownlea A. A. An urban ecology of infectious disease: city of Greater Wollongong-Shell Harbour. Ausfr. Grogr. 10, 169-187. 1967. Crosby Jr A. W. Epidemic, and Puce. 1918, pp. 37-38. Greenwood Press, Westport, CT. 1976; Beveridge W. 1. B. Infiuenzu: Thr Lust Grear Plague: An Unfinished Story of Discowry, p. 40. New York, 1977. Gouzien P. La pandimic grlppale de I9 1% I9 I9 dans les colonies Franqaises, B~rll. ti~e,!s. Off: mf. H),,q. Pub/. 12, 686724. 1920. Great Britain, Ministry of Health. Report O,I /he Prrndemic of Infiuen;u 191%1919. London, 1920. The section on the Empire was prepared by S. P. James. Patterson K. D. Influenza in the Gold Coast. Annual Repor! of thr Medical Deportment. Southrrn Nigrriu, pp. 2% 29. I91 8. Ihid.. map pp. 2&27. Martin G. In P. Gouzien. L’Cpidtmie d’intluenza de 1918~1919 dans les colonies franCaises. Note pr& liminaire. Ann/s Mkd. Phorm. colon. 19, 294-296. I92 1. David. In Huot. L’ipidkmie d’influenza de 1918-1919 dans les colonies fraqaises (suite). Ann/.s MGd. Phnrm. wlon. 19, 45946 I, I92 I. Great Britain. Repor/. 362: Howard Phillips. personal communication, 29 September 1980. Great Britain. Report. pp. 367-368. Perrings C. Block Minaworkers in C’enrrol A,fircu: Industriul Strolegies and /he Ecolurion of on African Proletariuf in the Copperbelt 1911~ 1941, p. 171. London, 1979. Op. cit. [2l], pp. 443-444. Op. cir. [21], pp. 448-450. Annuul Mediul Repor/. East Africa Protectorate. p. 36. I91 8; Annuul Report oil %on;ihar. p. 9, 1918; Great Britain, Repor/. pp. 369 371. Great Britain. Report. p. 371; op. cir. [2l], pp. 476- 477. Pdnkhurst R. [4]. pp. 103-109.
Influenza
in sub-Saharan
30. Op. cit. [21], pp. 463465. 31. Fine P. Applications of mathematical models to the epidemiology of influenza: a critique. In InJi’uenza Models (Edited by Selby P.), pp. 5G-56. MTP Press, Lancaster, 1982. 32. Gibbons J. P. Nonparametric Methods for Quantitative Analysis, pp. 22-28; 273-284. Holt, Rinehart & Winston, New York, 1976.
Africa
during
1918-1919
1307
33. Glezen W. P., Couch R. B. and Six H. R. The influenza herald wave. Am. J. Epid. 116, 589-598, 1982. 34. Gill C. A. The Genesis of Epidemics and the Natural History of Disease, pp. 251-288. William Wood, New York, 1928. 35. Neustadt R. E. and Fineberg H. V. The Swine Flu Aflair. U.S. Public Health Service, Department of Health, Education and Welfare, Washington, DC, 1978.
1983
PrInted in Great Britain. All rights reserved
Copyright 0
0277-9536/83 $3.00 + 0.00 1983 Pergamon Press Ltd
THE DIFFUSION OF INFLUENZA IN SUB-SAHARAN AFRICA DURING THE 1918-1919 PANDEMIC K. DAVID PATTERSON* and GERALD F. PYLE? Department
of History and Department of Geography Carolina at Charlotte, UNCC Station,
and Earth Science, The University Charlotte, NC 28213, U.S.A.
of North
Abstract-The focus of this study is the spread of influenza in Africa south of the Sahara during the pandemic of 1918-1919. Most known types of diffusion pattern. i.e. radial, wave-like and linear, have been identified; however, the disease spread so rapidly that four particularly devastating linear patterns stand out. One of the most incredible aspects of the regularity in epidemic velocity along these pathways was that the colonial transportation network was of fairly recent origin. Given modern transportation linkages, the ever-present danger of the resurgence of the agent or agents that caused the pandemic could result in a much greater disaster in Africa and other Third World areas if unabated by effective inoculation programs.
unexplainable and uncontrollable in Africa as it was on other continents. The viral agent was, of course, still unknown and many colonial physicians suspected Pfeiffer’s bacillus or some other bacterium [6]. Even if the etiology had been understood, there was neither therapy for influenza itself nor treatment for the secondary bacterial pneumonias which killed many influenza victims. There were no effective vaccines and, in Africa as elsewhere, quarantines and restrictions on markets and other public gatherings made little difference. Physicians could do nothing but order rest and symptomatic treatment and record the epidemic’s progress [7].
The influenza pandemic (global epidemic) of I91 8-1919 was one of the most pervasive and devastating biological disasters since the bubonic plague of the fourteenth century. The pandemic struck almost every colony and community in sub-Saharan Africa. This article describes the spread of the disease and how it was influenced by the transportation system developed by the recently established European colonial powers. This study focuses on Africa south of the Sahara, as the sparsely populated desert made North Africa a separate epidemiological entity. THE GENERAL PROBLEM AREA Jordan’s estimates of approx. 21 million dead worldwide and 1.35 million dead in Africa (including North Africa) [I] have been widely quoted, although both figures are based on official reports and hence are quite conservative. For example, authorities in the British colony of Gold Coast (Ghana) guessed that about 60,000 people died; the real figure was closer to 100,000 [2]. In sub-Saharan Africa alone, at least I .5-2 million people died, probably the greatest short-term demographic disaster in the history of the region. As elsewhere, young adults suffered the heaviest mortality [3], in contrast to the usual pattern of excess influenza deaths among the elderly and the very young. However, despite the importance of the subject, only a few social scientists have written on influenza in Africa [4]. Influenza was not unknown in Africa prior to 1918. At least some areas were touched by the 1889-1893 pandemic and scattered cases were reported annually by medical authorites throughout the continent. The usual smattering of cases occurred in the early months of 1918, but nothing like the ‘spring wave’ noted in the United States [5]. The devastation of late 1918 and early 1919 was as totally unexpected,
SOURCES OF INFORMATION Data for this study come primarily from published government reports and a few contemporary articles in the medical literature. Reporting was spotty, in part because some documents simply ignore times and places of outbreaks and, more importantly, because of the weaknesses of colonial medical services and of colonial governments in general. European rule and frontiers were generally no more than three decades old. Large regions were still almost unadministered and medical staffs were small everywhere. We have, for example (see Table l), extensive data for the Gold Coast and for sparsely-populated Mauritania, very little for Zaire or Angola and nothing at all for vast and populous Sudan [8]. In general, we have much more information on West Africa than for the rest of the continent. Also, it must be noted that reports are often vague as to when influenza reached a region (‘late October’) and, even when an exact date was given, it may not accurately represent the first few cases. Further research in archives of various African states might produce useful information, but will probably not greatly modify the conclusions presented here [9].
*A portion of this study was supported by the National Library of Medicine and the National Institute of Health (Grant No. LM-02517). PResearch was also conducted under the National Science Foundation grant, “Simulation of Influenza Diffusion” (Grant No. SES-8200901). 1299
COLONIAL CONDITIONS CONTRIBUTING TO DIFFUSION Two factors associated with colonial rule helped to spread the disease. First, wartime disruption and
1300
K. DAVID PATTER~N and GERALD F. PYLE Table Place Angola Luanda Basutoland (Lesotho) Bechuanaland (Botswana) Belgian Congo (Zaire) Elisabethville Stanleypool Area (Kinshasa) Boma Matadi British Somalia Berbera Cameroun Douala Edea Eseka Y aounde Bamenda Ngaoundere Maroua Garoua Lere Cape Verde Islands SBo Vincente Chad Fort-Lamy ‘South Waddai Dahomey (Benin) Porto Novo Cotonou Abomey Grand Popo Zaenando Parakou Kandi Atacora Eritrea ‘Western’ Ethiopia Addis Ababa Harrar Danakil region French Somalia Djibouti Gabon Port-Gentil Libreville ‘North’ Gold Coast (Ghana) Cape Coast Accra Koforidua Saltpond Kumasi Winnebah Axim Tarkwa Obuasi Yeji Keta Bole Wa Tamale Tumu Zuarungu Guinea Conakry Mamou
1. Temporal
and spatial Date of first cases
spread
of influenza
No. of weeks
after 22 August
Linear diffusion pathway
Late Nov. Early Oct. Early Oct.
14 7 I
IV IV
3rd week Oct. 11 Nov.
8 12
IV IV
Mid-Nov. Mid-Nov.
13 13
Early
11
Nov.
15 Oct. 29 Oct. 29 Oct. 8 Nov. 20 Nov. 21 Nov. 3 Dec. 13 Dec. 13 Dec.
8 10 10 12 13 13 15 17 I7
11 Sept.
3
14 Dec. Jan., 1919 Mar., 1919
18 20 30
I Oct. 15 Oct. 22 Oct. 22 Oct. 30 Oct. 20 Nov. 24 Nov. I1 Dec.
7 8 9 9 10 L3 14 16
2 Dec.
15
Mid-Oct. 11 Dec. 8 Feb., 1919
8 16 25
Early
Oct.
17 Nov. 26 Nov. Approx.
15 Dee
III III III III III III III III
I 13 14 17
31 Aug. 3 Sept. 19 Sept. 21 Sept. 23 Sept. 24 Sept. 25 Sept. 25 Sept. 1 Oct. 8 Oct. 12 Oct. 26 Oct. 7 Nov. 12 Nov. 16 Nov. 21 Nov.
2 2 4 5 5 5 5 5 6 I 8 10 11 12 13 14
10 Sept. 12 Sept.
3 3
I I I I I I I I I I I I I I I I
-
first cases
19 Sept. 25 Sept. IO Oct.
No. of weeks after 22 August
4 5 7
29 Sept. IO Oct. 21 Oct. 26 Oct. 31 Oct. 5-20 Nov.
6 7 9 IO IO 12
23 Sept. Late Sept. Early Nov.
5 6 I2
5 Apr., 1919 I8 Apr., 1919 25 July, 1919 2 Aug., 1919
34 36 49 50
I5 Sept.
Linear diffusion pathway
I I I I I
-
4
Late Sept. IO Oct. I6 Oct. 20 Oct. 20 Oct. Jan., 1919 Jan., 1919 Feb.. 1919 20 Mar., 1919 25 Mar., 1919
5 7 8 9 9 21 21 25 30 31
10 Nov. Early Dec.
12 15
20 Oct.
9
22 Oct. 14 Nov. 20 Nov. 25 Nov. 28 Nov. 28 Nov. 1 Dec. 28 Dec.
9 12 I3 I4 14 I4 I5 19
II
14 Sept. I Oct. 5 Oct. 14 Oct. I5 Oct. 17 Oct. 31 Oct. Late Nov.
4 6 7 8 8 8 IO I4
II 11 II II II II II II
25 Oct.
10
IV
5 Nov. 9 Nov. 9 Nov. I8 Nov. 3 Dec.
II 12 12 I3 I5
1302
K. DAVID PATTER~N and GERALD F. Table
1. cont.
Date of first cases
Place Oubangui-Chari (Central African Republic) Kouango Bangui Fort-Sibut Fort-de Posse1 Fort-Crampel Dekoa Marali Haut-M’boumou Senegal Dakar St Louis Senegal River Vallev Sierra Leone ’ Freetown South Africa Durban Rand area Cape Town Kimberley Southern Rhodesia (Zimbabwe) Bulawayo Salisbury (Harare) Inyanga Melsetter Togo Lomt Uganda Entebbe Upper Volta Southwestern area L&o Zanzibar
15 Nov.
25 Nov. 14 Dec. 16 Dec. 16 Dec. 24 Dec. 26 Dec. Apr., 1919
PYLE
No. of weeks after 22 August
13 14 17 17 17 18 18 33
24 Aug. I Sept. 16 Sept.
3 4
22 Aug.
0
14 18 23 23
Sept. Sept. Sept. Sept.
4 4 5 5
IV IV
9 Oct. Mid-Oct. Jan., 1919 Jan., 1919
7 8 21 21
IV IV
9
I
22 Oct. Late Oct.
10
Early Nov. 19 Nov. 28 Oct.
11 13 IO
The first outbreak was in Freetown, 22 August, 1918. If applicable, see Fig. 3 and Table, p. 1305 for Spearman Rank-Order II-Nigeria; III-Benin (Dahomey); IV-South Africa/Congo.
movements of troops and laborers, especially in and near German colonies and in areas of heavy recruitment of soldiers and porters, was often locally significant. A more important factor was the newlycreated colonial transportation network (see Fig. 1). Railway lines, built by Europeans to facilitate economic exploitation and administrative control, generally linked ports to colonial hinterlands. Lines from the coast of the Belgian Congo and in the interior of French West Africa provided access to the Congo (Zaire) and Niger Rivers, both of which were major communications arteries. The rail network was most fully developed in southern Africa, where lines beginning in Cape Town and Durban extended northward through the Rhodesias to connect with the Congo River in Katanga (Shaba). Motor vehicles were not yet in widespread use, but some lorries and buses already contended with bicycle and pedestrian traffic on the roads which radiated from the towns and railways [lo]. PATTERNS OF DIFFUSION
Studies
of the spatial
diffusion
Linear diffusion pathway
of infectious
dis-
IV
Tests: I-Gold
Coast;
eases reveal several common phenomena: (1) extremely virulent agents can penetrate areas rapidly (especially when there are low immunity levels) and linear pathways result [l 11; (2) radical spatial diffusion takes place from the onset, with the disease spreading to places adjacent to the major pathways and beyond [12]; and (3) these forms of diffusion often coalesce into ‘clinical fronts’ [13], and, in many instances, spatial-temporal diffusion waves can be identified. The nature of the 1918-1919 disease agent was such that influenza seemed to rage through sub-Saharan Africa as though the colonial transportation network had been planned in preparation for the pandemic. Linear penetration and diffusion were followed by radial expansion and successive waves of influenza built up to sweep the area within a few months. Most of the southern part of the continent had been enveloped by the spring of 1919. The primary linear pathways are depicted in Fig. 2 and the temporal waves are shown in Fig. 4. The first place in sub-Saharan Africa to be hit by the virulent ‘fall wave’ was the busy harbor of Freetown, Sierra Leone, where influenza broke out on 22 August. It was apparently introduced by a ship
Influenza
mMa~or asslsted 1918
Fig.
railway I”
the
(south
lines
dlffuslon
of the
that
in sub-Saharan
Africa
during
1918-1919
probably
of Influenza
I”
Sahara)
I. Africa (south of the Sahara) during the 1918-1919 influenza pandemic. have not been named
from England, although a local viral mutation cannot be ruled out. Interestingly and inexplicably, severe influenza outbreaks began almost simultaneously in Boston, Massachusetts, and Brest, France [ 141. Freetown was the focus from which the disease spread to
Fig. 2. Known
primary influenza 1918-I 919 epidemic.
for purposes
Note some political
entities
of clarity.
all of West Africa. It diffused relatively slowly into the Sierra Leone hinterland, but was spread rapidly to other ports by coastal shipping. As early as 24 August, a Brazrhan warshtp trom Freetown was thought to have brought the disease to
diffusion pathways within Africa south of the Sahara Cities shown are clearly documented points of entry.
during
the
1304
K. DAVID PATTERSON and GERALII F. PYLE
Dakar and the capital of French West Africa was thoroughly infected within 10 days. Dakar served as a diffusion point for the disease into the savanna country of the West African interior. The disease quickly spread by rail north to St Louis by 7 September and east to Thies and Kayes. Boat traffic on the Senegal River was also an important means of spread. Influenza diffused more slowly over the countryside of Senegal and thence to Gambia and Guinea. Mauritania was infected from the Senegal valley by early October; the disease did not reach some of the remote northern cercles until March 1919. Influenza reached western Mali via the Senegal-Bamako railroad by mid-September and thence spread slowly eastward along the Niger River and across the savanna, reaching Upper Volta by late October and Niger soon after. The remote Bilma area of northeastern Niger was one of the very few places in Africa to escape infection [15]. Liberian authorities proclaimed and enforced a maritime quarantine, but influenza struck overland from the hinterland, reaching Monrovia in mid-November [16]. Meanwhile, an American ship, the Shonga, carried the disease from Freetown to Cape Coast and Accra, Gold Coast, on 31 August and 3 September respectively. From the coast, influenza spread quickly up the rail line to Ashanti and thence, at pedestrian speed, reached the Northern Territories by early November, where it met the wave sweeping eastward from Senegal [17]. A ship from the Gold Coast brought the malady to Lagos on 14 September; the Gold Coast authorities had not even bothered to telegraph a warning to their colleagues in Nigeria [18]. Infection rapidly spread north and east along river, road, and rail routes, reaching the north by mid-October and the Kamerun (Cameroun) and Niger borders by early November [19]. Douala, the major port of Kamerun, was infected by ship in early October; virtually the entire country was covered within 6 weeks [20]. In Gabon, a maritime quarantine prevented ships from West Africa from introducing the virus, but passengers from Matadi (Belgian Congo) infected Port-Gentil on 17 November. The epidemic quickly spread up the Ogowe River and to Libreville. Northern Gabon was attacked by influenza brought south from Kamerun by traders [21]. Luanda, Angola was attacked in late November. The most striking pathway was from South Africa northward through the Rhodesias and thence along the Congo River system almost to the Atlantic coast. Influenza reached South Africa by ship in September. However, there had been an abnormal number of mild cases for several previous months, so it is possible the spring wave had also been introduced to the country by sea. Durban harbor was infected on 14 September, probably from Asia and the disease reached the Rand 4 days later. Numerous cases were reported among African mine workers, but most were mild. Indeed, it is possible that the deadly fall virus did not arrive in South Africa until 23 September, when a ship carrying members of the South African Native Labour Corps reached Cape Town from Europe. The vessel had called at Freetown during the epidemic there. Acute influenza spread rapidly along the rail line to Bloemfontein, Kimberley and points
beyond, diffusing into the countryside from towns along the railway [22]. The railroad network made it possible for influenza to advance with remarkable speed in central Africa. Basutoland and Bechuanaland were infected in October and by 9 October railway workers in Bulawayo. Southern Rhodesia were reporting sick [23]. By late October. influenza had traversed Northern Rhodesia’s rail system and had reached the Katanga mining area [24]. Once in the Belgian Congo, the virus was carried along the Lualaba and the Congo by river steamers. Leopoldville (Kinshasa) and Brazzaville were infected by &IO November respectively. At about the same time, ships from Europe infected the ports of Matadi and Boma in Belgian Congo and Point-Noire in French Congo. Remarkably, however, most of equatorial Africa, including points as near the sea as Brazzaville and Leopoldville, was infected via Cape Town, not from the Atlantic [25]. A steamer from Leopoldville introduced the disease to Bangui, Ubangui-Chari, on 25 November. From here the disease spread northward along French porterage routes through the savanna to southern Chad, where in early January it met the West African waves of influenza which had reached Chad from Niger. Nigeria and Kamerun. The remote eastern codes of Ubangui-Chari were not attacked until April 1919, when influenza was introduced from adjacent parts of Sudan and the Belgian Congo [26]. The East African coast was generally infected by shipping from Asia. Beira, Mozambique was attacked on 20 October; from there the disease advanced up the Zambezi and Shire, reaching southern Nyasaland on 5 November. Ships from Bombay brought influenza cases to Mombasa by 23 September and to Zanzibar by 28 October. By the last week of October, the disease had advanced across Kenya on the Uganda railroad and had reached Entebbe, Uganda [27]. Also in October, ships from Aden and India brought the infection to the coasts of British and French Somalia and to Eritrea [28]. Pankhurst reports a major outbreak in Addis Ababa, Ethiopia by late August; this is surprisingly early and almost certainly represents the continuing activity of the spring wave, which did afflict Ethiopia, and/or faulty diagnosis. The more serious fall epidemic after broke out in the city in mid-October, progressing up the rail line from the port of Djibouti, French Somalia [29]. Madagascar, defended by a rigorous quarantine, was not attacked until April 1919, when the virus reached the island on a ship from France [30]. SOME NON-PARAMETRIC TESTS OF EPIDEMIC VELOCITY
In spite of some recent contentions that influenza viruses spread in a radical fashion outward from outbreak epicenters [31], our findings clearly show how the disease diffused along transportation routes. Statistical tests have been done with time and distance data for four of the major diffusion routes. Spearman rank-order correlations were computed by first converting distances traveled and time of first reporting by place to ordinal vectors. A perfect statistic indicating time of infection as a function of
Influenza
in sub-Saharan
Africa
during
1305
1918-1919
30007
Origins/Pathways -------GOLD 2500-
COAST (RS =.9271 -.----.-NIGERIA (Rs =.867) l l l l lBENIN(Dahomey) (RS =.971
200°-
-SOUTH
c
6 6 j 1500-
j
AFRICA/CONGO (Rs =.91 1)
: z lODo-
500 -
1 August
1 September
Fig. 3. Time-distance
traverses
for selected
distance using this method would be + 1.00 [32]. The actual time-distance plots are shown in Fig. 3. While these interval-scaled time-distance plots indicate the velocity of movement along the South Africa/Congo pathway was much more rapid than the other three, the ordinal ranking process nonetheless resulted in the following Spearman rank-order correlations: Pathway South Africa/Congo Gold Coast Nigeria Benin (Dahomey)
Spearman Rank-Order Correlation (R,) 0.911 0.927 0.867 0.971
These statistics give a strong indication of the devastating nature of the 1918-1919 influenza epidemic within sub-Saharan Africa. In fact, the disease is known to have had such velocities worldwide. The overall pattern in Fig. 4 also offers further support to the conventional belief that the pandemic did not originate in Africa. West and East Africa were infected separately, and the disease was first introduced at major ports. As described above, the earliest contacts with the disease were in August in coastal West Africa, and it has been assumed by many researchers for more than a half-century that the disease was carried from either Europe, South America, or both. If the African strain (or strains) did not result from local genetic changes, then where were the geographical origins of the pandemic? Unfortunately, the results of this analysis offer few clues to that mystery. LINKAGES
TO RECENT KNOWLEDGE INFLUENZA
November
October
OF
Most of the conventional wisdom that has accumulated both before and after the 1918-1919 pandemic implies that the disease usually originates in China or
major
diffusion
December
pathways.
elsewhere in Central Asia. The contention is that there is something about the ecology of that part of the world that facilitates the genetic recombination of influenza viruses. Still, similar conditions could exist in North or South America. At times, these genetic shifts are signaled by springtime ‘herald waves’ [33] of abnormally high reporting of influenza. During the spring of 1918-1919, as already mentioned, such phenomena occurred in both the United States and India [34]. A massive shift to a virulent strain with subsequent worldwide diffusion took place during the middle of 1918. The shift could have taken place anywhere on the planet, including the southern hemisphere during the winter there. The passage of time seems to diminish the importance of such speculations about the geographical origins of the 1918-1919 pandemic, but recent fears of a ‘swine fu’ epidemic have led to the re-examination of many aspects of the event. While the agent(s) causing the 191&1919 pandemic are still not clearly known, many virologists have long suspected the strain of influenza that is annually responsible for the winter-spring deaths of many hogs to have been responsible for the World War I event. The 1976-1977 wintertime influenza inoculation program within the United States was based largely on that premise [35]. While the program was a qualified success with regard to the reduction of overall influenza mortality, the feared ‘swine flu’ epidemic fortunately never happened. Instead, a viral strain perhaps more distantly related to the 1918-1919 agent(s) surfaced in the late 1970s and early 1980s. The genetic shift was not massive and the prevailing strain is not particularly virulent. Comparisons of the diffusion of influenza during the earlier pandemic are still useful in determining the severity of influenza strains and the establishment of inoculation programs.
1306
K.
Months with documented
DAVID
PATTERSON and GERALD F. PYL.E
penetration
August
September
Fig. 4. Waves
pJ
October
pJ
November
q
December
of influenza
diffusion
in Africa
(south
REFERENCES
4.
5.
6.
7. 8.
9.
IO.
Jordan E. 0. Epidemic InJluenzu: A Survey, pp. 229-230. Chicago, 1927. Patterson K. D. The influenza epidemic of 1918 in the Gold Coast. To appear in J. Afr. Hist. Patterson K. D. The demographic impact of the 1918-1919 influenza pandemic in sub-Saharan Africa: a preliminary assessment. In African Historical Demography, II (Edited by Fyfe C. and McMaster D.). pp. 401433. Centre of African Studies, University of Edinburgh, I98 I. Phimster 1. R. The ‘Spanish’ influenza pandemic of I9 I8 and its impact on the Southern Rhodesian mining industry. Central Afr. J. Med. 19, 143-148, 1973; Pankhurst R. The ‘Hedar Basita’ of 1918. J. Ethiopian Stud. 13, 103-131, 1975; Ohadike D. H. The influenza pandemic of 1918-1919 and the spread of cassava cultivation on the Lower Niger: a study in historical linkages. J. A@. Hisr. 22, 379-391, 1981. Collins S. D. Age and sex incidence of influenza and pneumonia morbidity and mortality in the epidemic of 1928-29 with comparative data for the epidemic of 1918-1919. Publ. Hith Rep. 46, 1909, 1931. Burnet F. M. and Clarke E. Influenza: A Suwey qf the Last Fifty Years in the Light qf‘ Modern Work on the Virus of Epidemic Ifluenzu, pp. 69-99. Macmillan, Melbourne, 1942. See Refs [2] and [4]. The late Gerald W. Hartwig found no materials on influenza in the official archives in Khartoum. Ahmed Bayoumi does not mention the epidemic in his The History of Sudan Health Services, Nairobi, 1979. Relevant materials probably exist in some countries. as in Ghana. Marc Dawson of Union College and Rita Headrick of the University of Chicago generously provided archival data on Kenya and French Equatorial Africa respectively. Oliver R. and Atmore A. Afticrr Since 1800, pp. 18&200. Cambridge University Press. Cambridge, 1967.
of the Sahara)
II. 12. 13.
14.
I5
I6
I7 18 19 20
21
22. 23. 24.
25. 26. 21.
28. 29.
during
the latter
half of 1918
Pyle G. F. The diffusion of cholera in the United States in the nineteenth century. Geogr. Ano/. 1, 59-75. 1969. Stock R. Cholera in Africa. International African Institute, London. 1976. Brownlea A. A. An urban ecology of infectious disease: city of Greater Wollongong-Shell Harbour. Ausfr. Grogr. 10, 169-187. 1967. Crosby Jr A. W. Epidemic, and Puce. 1918, pp. 37-38. Greenwood Press, Westport, CT. 1976; Beveridge W. 1. B. Infiuenzu: Thr Lust Grear Plague: An Unfinished Story of Discowry, p. 40. New York, 1977. Gouzien P. La pandimic grlppale de I9 1% I9 I9 dans les colonies Franqaises, B~rll. ti~e,!s. Off: mf. H),,q. Pub/. 12, 686724. 1920. Great Britain, Ministry of Health. Report O,I /he Prrndemic of Infiuen;u 191%1919. London, 1920. The section on the Empire was prepared by S. P. James. Patterson K. D. Influenza in the Gold Coast. Annual Repor! of thr Medical Deportment. Southrrn Nigrriu, pp. 2% 29. I91 8. Ihid.. map pp. 2&27. Martin G. In P. Gouzien. L’Cpidtmie d’intluenza de 1918~1919 dans les colonies franCaises. Note pr& liminaire. Ann/s Mkd. Phorm. colon. 19, 294-296. I92 1. David. In Huot. L’ipidkmie d’influenza de 1918-1919 dans les colonies fraqaises (suite). Ann/.s MGd. Phnrm. wlon. 19, 45946 I, I92 I. Great Britain. Repor/. 362: Howard Phillips. personal communication, 29 September 1980. Great Britain. Report. pp. 367-368. Perrings C. Block Minaworkers in C’enrrol A,fircu: Industriul Strolegies and /he Ecolurion of on African Proletariuf in the Copperbelt 1911~ 1941, p. 171. London, 1979. Op. cit. [2l], pp. 443-444. Op. cir. [21], pp. 448-450. Annuul Mediul Repor/. East Africa Protectorate. p. 36. I91 8; Annuul Report oil %on;ihar. p. 9, 1918; Great Britain, Repor/. pp. 369 371. Great Britain. Report. p. 371; op. cir. [2l], pp. 476- 477. Pdnkhurst R. [4]. pp. 103-109.
Influenza
in sub-Saharan
30. Op. cit. [21], pp. 463465. 31. Fine P. Applications of mathematical models to the epidemiology of influenza: a critique. In InJi’uenza Models (Edited by Selby P.), pp. 5G-56. MTP Press, Lancaster, 1982. 32. Gibbons J. P. Nonparametric Methods for Quantitative Analysis, pp. 22-28; 273-284. Holt, Rinehart & Winston, New York, 1976.
Africa
during
1918-1919
1307
33. Glezen W. P., Couch R. B. and Six H. R. The influenza herald wave. Am. J. Epid. 116, 589-598, 1982. 34. Gill C. A. The Genesis of Epidemics and the Natural History of Disease, pp. 251-288. William Wood, New York, 1928. 35. Neustadt R. E. and Fineberg H. V. The Swine Flu Aflair. U.S. Public Health Service, Department of Health, Education and Welfare, Washington, DC, 1978.