REFLECTIONS ON THE EPIDEMIOLOGY AND PREVENTION OF PLAGUE1

Dr. Celso Arcoverde de Freitas2 y,

In spite of the spectacular advances made in medicine, the ancient scourge of continues even today to be a constant threat to vast numbers of human beings in the underdeveloped areas of the world. The author traces its history, describes the cycle of transmission to humans through rodents and fleas, and furnishes data on its incidence.

Introduction Writing on the history of plague in in more recent times, Wu-Lien-Teh (1936) tells Plague, a disease caused by Pasteurella how in 1792 at Chaochow, in Province, pestis, is primarily and basically a zoonosis Shih-Tao-Nan wrote a poem “Tien Yii Cm,” a found in rodents, though human beings can section of which, entitled “Rat Death,” des- contract the disease if they live in the same cribes the scourge of plague in that area. The ecological environment as rodents that are poet died of the plague a short time afterward. reservoirs of the infection. Later on, as recently as the end of the 19th From time immemorial, plague has dogged century, a Moslem rebellion and troop move- man’s footsteps, and at various periods in ments in Yunnan Province brought the plague history it has taken a bitter toll of human lives. to Canton and Hong Kong in 1894, and the In some areas it has actually altered the social recent was propagated from that structure and upset the economic situation, and international port. It was not until the pan- it is the disease that perhaps more than any demic occurred, and obviously as a result of other has caught the imagination of poets and modern scientific development, that epide- writers and led them to depict its horrors. miological research brought a knowledge of Wu-Lien-Teh, reviewing the history of plague in all its aspects, including the reasons plague on the basis of Sticker’s researches, cites for its persistence in certain foci. the Bible (1 Samuel) as the earliest reference to In spite of the enormous body of knowledge the- occurrence of plague, which decimated the regarding plague and the technical resources Philistines in 1320 B. C. now available for its prevention, even today- Other references to the antiquity of plague when the degenerative diseases, industrial are found in the writings of the physician Rufus accidents, air pollution, and contamination of of Ephesus, who speaks of the existence of natural water sources are emerging as the major plague in the year 1000 B. C. in , , health problems-this communicable disease and . Another ancient historical reference continues to pose a permanent threat for vast to the disease is the account of the plague that population groups in developing areas. began at Pelusium in Justinian’s reign in the fifth century. Natural Foci of Plague

Natural Primary Foci ‘Paper read at the XVII Brazilian Hygiene Con- gress held in Salvador (Bahia) from 8 to 14 December 1968, and subsequently published in Spanish in The oldest and most active plague area in Boletin de la Oficina Sanitaria Panamericana, Vol. the world is the Central Asian Plateau, bounded LXVIII, No. 5 (May 1970), pp. 393-402. 2Public Health-Medical Officer in the National on the south by the Himalayas, on the east by Department of Rural Endemic Diseases. the Tien Shan mountain chain and Mount

39 40 BOLETIN DE LA OFICINA SANITARIA PANAMERICANA

Altay, and to the northeast by the Shing-Shan area coincides with the northern edge of the and Stanovoy ranges. desert region which is the habitat of the gerbil This area, regarded as the ancestral cradle of (Rhombomys opimus), the chief reservoir in plague, with the marmot as the primary reser- that part of the world (Petrov, 1967). voir, lies between parallels 30 and 50 south The plague area is bounded on the extreme latitude while in the east it stops short of the northwest by another focus, the Volga-Ural, Pacific coast, reaching the middle course of the less extensive in size (200,000 Km2), the Sungari. reservoirs here being Citellus pygmeus, Me- The area of the plague bacillus today in the riones m eridianus, and M. tamaricinus Eurasian continent as a whole extends north- (Mironov, 1967); and in the southwest it ward slightly beyond latitude 50 into the fringes the Asia Minor focus, where the reser- Transbaikal area, and in the extreme east to 51 voirs are Meriones Zibycus, M. persicus (highly degrees latitude, on the east bank of the Ural resistant), and M. tristami and M. vinogradovi River. (highly sensitive) (Baltazard, 1960). In this vast region there are many natural The world map (Figure 1) shows the natural foci (microfoci) where, as Kucheruk says foci plague areas in Eurasia, , and the (1967) the plague agent exists independently Americas. of human activity, being a normal and authentic member of the local biocenosis. The Secondary Natural Foci natural focus of the desert region of south- (Kazakhstan) alone is 2 million The area of distribution of P. pestis through- square kilometers in area, stretching from the out the world comprises at the present time not Ural River to the north of the Aral Sea, and only the vast primary natural focus of Eurasia, ending at the western end of Lake Balkash. This but the new areas of “sylvatic” or wild-rodent

FIGURE 1 -Natural foci of plague in Eurasia, Africa, and the Americas.

450 .~ - ~~ -~___ liiiiil NATURAL FOCI OF PLAGUb ” m DESERT H STEPPE

Source: V. V. Kucheruk. “Un the Paleogenels of Natural FOCI of Plague ” F’roceedmgs of a Symposium. Prague, 1963. Arcoverde de Freitas . PLAGUE 41 plague in Africa and the Americas, of recent mediaries are Mastomys coucha and origin. These foci, which have emerged since Rhabdomys pumilio (Jorge, 1928). the recent pandemic, have come about as a North America. The North American focus result of the transference of the plague bacillus comprises approximately 40 per cent of the from common rats and mice to the indigenous land area of the United States of America, wild rodents. embracing 131 counties in 15 of the western AjYica. The natural foci here are situated in states (Figure 2). Ground squirrels of the the southern part of the continent, in the species CitelZus are the main reservoirs, but 10 Republic of South Africa, South West Africa, wild rodent species and two Lagomorpha have and Botswana, and also in the areas around been found infected: Citellus, Neotoma, Lakes Victoria, Albert, and Edward, in the Peromyscus, Eufamias, Tamiasciurus, Congo, Uganda, Kenya, and Tanzania. Claucomys, Marmota, Thomomys, Microtus, In the African foci the primary reservoir is Reithrodon tomys, Lepus, and Silvilagus the gerbil (Tatera lobengulae) and inter- (Kartman, 1958).

FIGURE 2-Distribution of Pasteurella pestis infection in wild rodents and fleas in the United States of America,by counties, 1908-1964.

q$5 NEGATIVE COUNTIES

Source: Reproduction of figure in Plague Epidemiology, 1966. H. E. Stark, B. W. Hudson, and B. Pittman. National Communicable DiseaseCenter, Atlanta, Georgia, 1967.

the Paleogenesis 42 BOLETIN DE LA OFICINA SANITARIA PANAMERICANA

In 1939 plague was detected in Canada in Kucheruk (1963), studying the paleogenesis areas bordering on the United States, and also of the natural foci, gives his opinion that the in northern Mexico (Coahuila State) close to North American focus is likewise primary, the U. S. border. dating from a remote geological age, and related South America. The plague foci in South to the appearance of reservoir rodents of the America, all of them independent, are situated same family (Sciuridae and Cricetidae) and also in the following regions: to the chief vector (Oropsyllus) in both con- a) Venezuela. The focus covers a small area tinents. The distribution of the natural foci of dry Savannah in Miranda and Aragua States. follows the desert and semiarid lands, the same Plague has been detected in Sigmodon hirsutus being true of the foci of Africa and South and Heteromys anomalus (De la Barrera, America. Other authors (Jorge, 1928; Macchia- quoted in Plague in the Americas, PAHO, vello, 1941; Pollitzer, 1954) consider that the 1965). foci in the Americas and in Africa originated b) -Ecuador. The focus is located in a with the pandemic that occurred at the begin- continuous zone between northern Peru ning of the present century when plague-ridden (Ayabaca and Huancabamba, Departments of from the synanthropic fauna were Piura and Cajamarca) and southern Ecuador transported by the sea route (Rattus nor- (Loja, El Oro, and Chimborazo a little farther vegicus, R. rattus, R. alexandrinus, R. fru- north). The reservoirs are Akodon, Sigmodon, givorus, Mus musculus). Oryzomys, and Sciureus (Macchiavello, 1955). If in fact the plague agent reached North It is noteworthy that plague originating in America on earlier occasions via the Bering this focus, situated in the mountainous inter- Strait, presumably it would first have infected Andine region, has already reached the Amazon the fauna of Canada (Pollitzer, 1954). Another Basin, and in 1963 and 1964 cases occurred in point worth considering is the biochemical humans in Bagua Province on the right bank of composition of the strains of P. pestis. The the Maration River. American race is glycerol-negative and of c) Argentina-Bolivia. The focus extends “oceanic” race (Berlin and Borzenkov, quoted from northern Argentina (Santiago de1 Estero, by Korobkova, 1967) whereas the strain found C6rdoba, Tucuman, Salta, Jujuy) as far as in the Asian foci is of the “continental” race Bolivia (Tarija, Chuquisaca, Santa Cruz). The which acidifies glycerol media. reservoirs are Caviidae and Graomys (De la Barrera, 1965). StructureandDynamics ofthe Natural Foci d) . There are two independent areas The research conducted by Pavlov&i3 on of foci: the northeast focus, running along the natural foci of communicable diseases has arid zone of Bahia as far as northern Minas suggested new directions, since 1939, for the Gerais; and the Terezopolis focus, isolated and study of the structure and dynamic evolution covering a small area of the Serra do Mar, in the of plague foci; and it has been demonstrated districts of Terez6polis and Nova Friburgo. that the pathogenic agent, the reservoir, and the Plague has already been found in the follow- vector have a biological kinship in their bio- ing wild rodents in Brazil: Zigodentomys types, since they exist permanently in natural pixuna, Cercomys cunicularius laurentius, conditions as co-members of the local bio- Cercomys cunicularius inermis, Galea spixii, cenosis. Hesperomys tener, Kerodon rupestris, Holo- If we apply Pavlovski’s theory to the study chilus sciureus, Oryzomys subflavus, Thoma- of the ecology-epidemiology of plague foci, in somys pirrhorhinus, Silvilagus brasiliensis, Cavia aperea (Silva , 1938; Macchiavello, 1941; 3PavIovski, E. N. “On theTheory of Natural Foci Simond, 1951; Neves, 1956; De la Barrera, of Diseases Communicable to Man.” J Gen Biol 1965). (Moscow) 7:3-33, 1946. Arcoverde de Freitas . PLAGUE 43

other words, if we investigate thoroughly all the The theory of the perpetuation of plague in ecological factors involved, we can learn some- a poly-host focus was launched in in thing of the laws governing the process by 1949 by Kalabukhov, who stressed the impor- which plague is perpetuated and propagated in tance of this focus for the maintenance of the nature, and thus acquire the necessary basic enzootic, since the varying degree of suscep- knowledge for combating and controlling the tibility in the different rodent species furnishes disease. the plague agent with sensitive elements at all The mechanism by which P. pestis survives times (Kalabukhov, 1965). in the interepizootic periods is still an unknown The studies conducted by Baltazard et al. in factor. There are various hypotheses to explain the Kurdistan focus interpret the perennial the phenomenon, the one most commonly nature of plague in foci of long standing as accepted being the permanent propagation of being the result of “the presence of the the plague agent through sporadic cases of resistant rodent/susceptible rodent complex.” acute and subacute infection, following the The perpetuation of P. pestis demanded a dense rodent-flea-rodent chain of transmission, with a population of highly resistant rodents capable more prolonged sojourn in the organism of the of surviving the most virulent plague epizootic flea, especially during the cold season. in large numbers, sedentary rodents capable of Petrov (1967), writing about the conserva- maintaining the infection of fleas in their tion of plague in fleas, says that they preserve warrens deep underground, which are perma- the bacillus in their organism during the cold nent structures with a favorable microclimate winter months and actively transmit it to (Baltazard, 1960). animals during the hot season. He also says that Recently, in 1964, still researching in the bacillus can be kept alive inside the rodent Kurdistan, Baltazard noted that P. pestis as well, and he demonstrated that “the process survives in the soil of rodents’ warrens for a of infection among gerbils (il4. libycus) can long time following an epizootic. become chronic when the plague agent is kept In 1967 Mollaret succeeded experimentally for several months, without losing its virulence, in keeping the plague bacillus alive in earth, in inside the parenchyma, enclosed in a capsule of conditions similar to those of the microclimate adipose abscess tissue. In due course, for of rodent warrens, and recorded P. pestis as unknown reasons the capsule disintegrates, and surviving for more than seven months. the process of general infection takes place, Experiments carried out by Baltazard’s team with growth of bacteria. This leads to the (1964), in an attempt to reproduce the telluric infection of the fleas and reactivation of the cycle of plague, demonstrated the importance epizootic process.” of the “burrowing of meriones in soil contami- The work of the Soviet researchers shows nated with a culture; they were literally that “in a natural focus of plague the fleas are stricken with plague.” not only responsible for the transmission of the plague agent; they also help it to survive over a IncidenceofPlague throughout theWorld long period... adult fleas contaminated in natural conditions have been found to stay alive Following ‘the epidemic outbreaks in the for a long time, up to 210 days being recorded early decades of this century, urban plague has in the warrens of the larger gerbils” (Bibikova, receded everywhere, as a result no doubt of 1967). Under experimental conditions, even development, more hygienic housing, the dying- longer periods have been observed (Golov and out of plague in urban areas, and modem Yoffe, 1928, and Mikulin, quoted by Bibikova, methods of reservoir and vector control. 1967). Macchiavello (1941) mentions the flea In South America, urban plague had as a temporary reservoir in the Brazilian north- practically disappeared, but its incidence has east. been on the increase since 1960. Tables 1, 2, 44 BOLE’PIN DE LA OFICINA SANITARIA PANAMERICANA _..

TABLE l-Reported cases of plague in Africa, 1950-1967.a

country 1950-1954 1955-1959 1960 1961 1962 1963 1964 1965 1966 1967

Botswana 5s - - Cameroon - ;:::rr7 Congo 172 102 26 3 4 4 2 16 8 7

GhanaKenya 766 127 36- 3 3 ; 1 I 7 1 Lesotho 11 - - - 834 120 a 4 28 9 6 38 9 8 Malawi 29 - - - 30 - - - - Mauritania i - - - Namibiab - - 9 80 4 1; 1 z I South Africa 90 26 1 1 7 - 1 - - - Tanzania 848 10 - - 2 - 513 1 - - Uganda 30 - - - Upper Volta - - - - - 1 1 Zambia 10 29 ------

aWorld Health Organization. Epidemiological and Vital Statistics Report No. 20(S), 1967. World Health Statistics Report No. 21(4), 1968. bFormerly South West Africa. and 3 show (a) a falling-off in the incidence of provides highly favorable conditions for the plague in African and Asian countries, except in reservoir fauna that breed in the environment Vietnam, where 5,574 cases were recorded in surrounding human dwellings. This has become 1967; and (b) an increase in the frequency of the ideal “habitat,” man-made for wild rodents, casesin the South American foci since 1960. which find food in abundance in the harvested Plague in South America today is essentially crops and shelter in the stone walls separating rural; it is linked with the primitive type of the fields. rural dwelling, but it is widespread in the In conditions so favorable for the propaga- cultivated areas. The way of life of the rural tion of the zoonoses, it is surprising that the dweller, engaged in tilling the earth and living in endemic index is not even higher. The annual precarious housing built of materials that offer variation of incidence depends on many factors- no protection against ’ rodent infestation, density of the rodent and flea population, “‘!y. L-r.,

TABLE 2-Eeported cases of plague in Asia.a ), c i. 9.

Country i&To-l-G&. 1955-1959 1960 1961 1962 1963 1964 1965 1966 1967 . -__ Burma 3,488 887 22 41 73 34 11 36 48 117 Cambodia 38 15 - 22,450 891 78 404 686 205 109 14 1T 6 Indonesia 11,444 520 ------Iran 50 12 ------Laos 2 26 _ _ _ - Philippines ; ---_---- Thailand 71 - .i Vietnam 205 53 14 s 29 11; 297 374 2,843 5,574

aWorld Health Organization. Epidemiologicai and Vital Statistics Rep& 40. 20(5), 1967. ~k’grlcj-&k% StatisticalReport No. 21(4), 1968. ,‘_ ; i. i -,., *, ’ Arcoverde de Freitus - PLAGUE 45

TABLE 3-Reported cases of plague in the Americas, 1950-1967.a

country 1950-1954 1955-1959 1960-1964 1965-1967

Argentina 4 1 - - Bolivia 96 48 134 155 Brazil 156 109 494 324 Ecuador 276 218 960 559 Peru 238 151 568 903 United States of America 4 6 6 16 Venezuela 14 3 7 -

aWorld Health Organization. Epidemiological and Vital Statistics Report No. 20(5), 1967. World HeaZth Statistical Report No. 21(4), 1968. previous epizootics, meteorological conditions, Arapiraca, Santana Ipanema, Mata Grande. agricultural production, etc.-which affect the Bnhiar Regions of Senhor do Bon&n, Feira deSantana, Jequie, Vitbria da Conquista. reservoirsand/or vectors. Minas Gerais: Medina, Pedra Azul, Salinas, IncidenceofPlague inBrazil Tumiritinga, Itanhemi. Terez@olis Focus. This is an isolated focus, There is no record of the occurrence of confined to a small area in the Serra do Mar, plague in Brazil prior to the year 1899, when it within the boundaries of the districts of invaded the country via the port of Santos. Terezopolis and Nova Friburgo. It covers a After infecting many cities along the coast, the tropical forest area where the rainfall is more disease reached the interior, especially the than 1,000 mm (Figure 3). northeast, and gradually spread through the The present endemic area covers approxi- rural areas, where it found favorable conditions mately 230,000 km2 with a rural population of for survivaland propagation in the fauna of more than 3 million and including 189 muni- indigenous rodents. Thus two independent cipalities in eight states (Table 4). Between plague foci were formed: the northeast and 1935 and 1967, 4,213 cases of plague were Terezopolis.

Northeast focus. This covers a wide area FIGURE 3-Present endemic plague areas in Brazil. centered around the semiarid zone with a rainfall of under 1,000 mm, and stretches over the dry region into Bahia, as far as northern Minas Gerais. The area is literally dotted with apparently independent foci, mostly located in the oro- graphic system of the region, where conditions suit this particular zoonosis. The foci areas include the following: Cearci: Regions of Serra de Ibiapaba, Serra deBaturitB, Chapada do Araripe (north slope). : Chapada do Araripe (south slope), , Exu, Bodoc6, Serra do Triunfo, Serra de , Born Conselho, Aguas Belas, , SZo Caetano, Pesqueira. : Serra da Borborema, Umbuzeiro, Campina Grande, Cuite, Cel. Ezequiel (R.N.). AZagoas: Palmeira dos Indios, Quebrangulo, 46 BOLETIN DE LA OFICINA SANITARIA PANAMERICANA

TABLE 4-Endemic plague area in Brazil, foci in 1958-1967.a

Municipalities Rural Area 2 Focus State with plague population in Km centers foci (1960) (1960)

Cear& 27 462,340 21,907 186 Rio G. do Norte 5 48,670 922 21 Paraiba 9 147,857 5,195 Pernambuco 813,764 34,323 2;: f&y= 2”: 271,183 8,561 68 1,180,668 129,066 3;; Minas Gerais 14 188,396 28,154 75 *- Rio de Janeiro 2 37,052 1,858 2 Total 189 3,149,930 229,986 971

L-. aProphylaxis Division, National Department of Rural Endemic Diseases. I

TABLE S-Reported human cases of plague, by state, Brazil, 1935-1967.

States

1935 148 - 571 1936 16 146 - 72 359 1937 - - 5 1938 - 1: - - 12 13466 1939 - - 2 - 111 1940 - 1: - 255 1941 - :i 7 302 1942 - i - - - 3 1943 - 22 - - 2 - - - 2’6 27 - - - 154 :g’:; - 3”; - 1 - 192 1946 = 175 - 19 36 - - 34 333 1947 - - 4 :0 - 7 1948 - 3: - 257 - 388: 1949 - 10 52 9 96 - 1950 - r 17 - - C’ 1951 - 2 - - 4 - - g 1952 - - - - - 1 4 - - 1953 ------10 c 1954 - - - : - - - 6 1955 - 4 20 - - - 27 c- 1956 - - - - - 4 1957 - - 5 - 20 - - - 1958 - - - - - 25 - - - ;; - - - 1959 - - - - 16 4’ 1960 - - - :: -T - - 1961 - 31 39 :: 15 - z 102: * 1962 - 3 13 - - - 36 1963 - ; : - 14 - - - 1964 - 2 6: 60 - - - 2:; + 1965 - Is 3 23 4 - :s - - r 119 1966 - 3 13 - 1967 - 7 2: -2 10 --i - % 1:; Total 16 1043 21 85 1580 553 1 785 34 38 57 4213 Arcoverde de Freitas . PLAGUE 47

TABLE (j-Reported cases of plague, decade practical, particularly as it would have to cover 1958-1967.a 90 per cent of the population to be effective. Positive Suspected Control measures are nearly always carried State out late, generally after the epizootic has Case Death Case Death broken out, in other words, at the development stage. Cearir 353 15 49 4 Rio Grande Failure to take control measures in good do Norte 2 Paraiba f:. :‘6 time is the consequence of lack of field Pernambuco 174 180 1; research, which can help to detect plague Alagoas before the epizootic process is under way. Bahia 1;; 42 91 Minas Gerais 4 160 6 It should be pointed out that in the foci of Rio de Janeiro li - - underdeveloped areas today, antiplague cam- Total 859 89 873 134 paign laboratories tend to be staffed and equipped for diagnosis only, not for research. aprophylaxis Division, National Department of Rural Endemic Diseases. Yet systematic field investigations are essential for detecting plague before its epizootic mani- festations appear and determining where and reported in 11 states (Table 5). During the when to take control measures. IO-year period 1958 to 1967, 859 cases were reported, with 89 deaths, or a case-death rate of Summary 10.4 per cent (Table 6). The author outlines the geographic distribu- tion of the primitive or “natural” foci of plague, and discussesthe spread of the zoonosis SomeAspects ofPlague Prevention to rodent reservoirs in new areas. Emphasis is laid on the importance of the study of the The objectives of programs to combat epidemiological peculiarities of a particular plague are: (a) to reduce mortality (prompt plague focus, on the need to determine its treatment); (b) to prevent secondary cases structure and dynamics by means of research (chemoprophylactic treatment of contacts); (c) into the ecological environment in which P. pestis thrives, as a basis for the control of the to interrupt the domestic transmission cycles disease. Data are given on the incidence of rodent-flea-man, rodent-flea-rodent, man-flea- plague throughout the world during the period man, and man-flea-rodent (disinsecting); (d) to 1950-1967, and particularly in Brazil between carry out deratization (where possible with 1935 and 1967,with special reference to the rodenticides); (e) to improve housing (health area where it is endemic, describing the larger education measures). and more important foci and giving corrobo- rative data in a series of tables and figures. Immunization is the measure recommended Various preventive measures that can be taken for preventing man from being infected in the in underdeveloped areas are discussed, espe- fields in the event of a wild animal epizootic; cially prompt treatment, interruption of the but at present there is no vaccine of high transmission cycles, destruction of the rodent immunizing potency available. and flea vectors, and improved housing. Immunization is recommended as the answer to The vaccine considered to be the best is that many of these problems, together with system- prepared with the EV strain, but inoculation atic research on vaccines and field investigations has to be repeated every year, which is not for the early detection of plague. 0

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