Draper, C.C.

Lelijveld, J.L.M.

Matola, Y.G.

White, G.B

English

Digital Library of the Tanzania Health Community

TRANSACTIONS  OF  THE ROYAL  SOCIETY OF 
TROPICAL  MEDICINE  AND  HYGIENE. 
Vol. 66.  No. 6.  1972. 
905 
MALARIA  IN  THE  PARE  AREA  OF  TANZANIA. 
IV.  MALARIA  IN  THE  HUMAN  POPULATION  11  YEARS  AFTER  THE 
SUSPENSION  OF  RESIDUAL  INSECTICIDE  SPRAYING,  WITH  SPECIAL 
REFERENCE  TO  THE  SEROLOGICAL  FINDINGS 
C.  C.  DRAPER, 
London School of Hygiene and Tropical Medicine 
J.  L.  M.  LELIJVELD, Y.  G.  MATOLA AND  G.  B.  WHITE 
E. African Institute of Malaria and Vector-borne Diseases 
The South Pare area was  one of two areas  selected for special study within the 
Pare-Taveta Malaria Scheme, described by WILSON (1960).  In this, spraying of homes 
with the residual insecticide dieldrin, at intervals of 8 months for 3 years from 1956 to 
1959, caused a dramatic reduction in the transmission of malaria. Malaria in the South 
Pare area before, during, and after the spraying has been described in a series of previous 
papers by DRAPER and SMITH (1957 and  1960) and by PRINGLE (1967 and  1969).  The 
last author recorded observations made during the period from the suspension of the 
spraying in  1959 until  1966.  During this time there was  a surprisingly slow return of 
`4nopheles gambiae, with evidence of continuing reduced longevity, and an even greater 
delay in that of the other main vector in the area, Anophelesfunestus type form which, 
unlike the former, had been completely eradicated by the spraying. Factors in this slow 
return were thought to have been a prolonged residual insecticide effect of the dieldrin 
and, particularly in the case of A. funestus, competition by replacement species. Hence, 
it was only by 1966 that densities of`4. gambiae near to those found before the spraying 
were observed, while the ,4. funestus type form was  only then beginning to reappear. 
The resurgence of malaria in the human population appeared to be similarly delayed; 
a  contributory factor in this  was  thought to be an increase in the use of anti-malaria 
drugs. 
This paper describes malaria in the human population as found in surveys done in 
February and March 1970, that is almost exacdy 11 years after the last round of  insecticide 
spraying.  In addition to the standard maiariometric methods, a serological survey was 
done to determine whether this would give any further information on human infections, 
and a repeat survey of haemoglobin levels was  also done. 
Entomological  background 
From  1968 onwards densities of A. gambiae and A. funestus  were similar to those 
before spraying (WHITE and MAGAYUKA, 1968). The Human Blood Index (HBI) of re- 
established ,4. funestus females was about 90~o indoors as in pre-spray years, while the 
HBI of//. gambiae had risen by about 25% in certain villages between 1955 and 1968, 
We owe many thanks to Mr. Sherali Thaver and to Mr. Kassu Hassanali who carried 
out the IFA tests in London and East Africa respectively. 906  MALARIA  IN  THE  PARE  AREA  OF  TANZANIA 
apparently in  consequence  of the  reduction  of the  availability of cattle  as  alternative 
hosts (Wnxx~.,  1971)*.  Table I  shows the theoretical annual human malaria inoculation 
rates based on entomological data, calculated by the standard  methods  (WHO,  1963). 
Throughout the  series of papers  describing malaria in the Pare area a  distinction  was 
made between the swamp and the roadside villages and this is continued here. Because 
of the technical and statistical inaccuracies inevitable when the vectors have a very low 
sporozoite rate (less than  1% both before spraying and subsequently) such calculations 
can be no more than approximate. They suggest, however, that by the start of 1970 the 
risk of malaria was approaching that before spraying. 
TABLE I.  Approximate theoretical  human  malaria  inoculation  rates  (infective bites  per 
individual per year) in the South Pare area, based on entomological data. Range and (means). 
Swamps villages 
Roadside villages 
Year 
1954-55" 
1967-68 
1968-69 
1969-70 
1954-55" 
1967-68 
1968-69 
1969-70 
A. gambiae 
10-15  (11.9) 
1-20  (5.7) 
2-11  (4.8) 
10--34  (19-4) 
11-22  (20.3) 
1-21  (5-9) 
1-  8  (3.5) 
7-24  (13.9) 
A. fugleStU$ 
26-40  (29.8) 
2-35  (12-2) 
3-24  (9.5) 
15-54  (30-3) 
1-10  (4.6) 
1-13  (4.4) 
1-  7  (2.9) 
5-18  (10.1) 
Total 
27-53  (42) 
3-55  (18) 
5-35  (14) 
25-88  (50) 
13-27  (25) 
2-34  (10) 
2-15  (6) 
12-42  (24) 
*  before spraying 
Malaria  in  the  human  population 
An attempt was made to examine people from exactly the same villages and hamlets 
as had been examined during the main part of the scheme from 1954 to 1959.  This was 
not  altogether  possible because  of some rebuilding,  in  particular  an  extension  of the 
rice  growing  areas  in  some parts  having  caused  the  abandonment  of hamlets  in  the 
swamps and the migration of their people to the roadside villages. However, a differen- 
tiation  between  swamps  and  villages  has  been  maintained  and  this  is  justified  by 
differences in their malaria indices. These are shown in Table II while in Figure  1 the 
parasite rates for the swamp villages are compared with those before and at the suspension 
of spraying. For 1966 PaINGLE (1969) gave parasite rates for the swamp villages of 23% 
for the combined age groups under 2 years, of 39% for the 2 to 9 years combined groups, 
of 22% for the 10 to 19 years combined groups, and of 18% for the over 20 years groups. 
His figures for the roadside groups were 28,  23, 27 and  15% respectively. Despite the 
return of the vectors the indices for 1970  do not show more than a small increase over 
those for  1966  and  are still  considerably below those before spraying. 
*.Note : Since the present survey was conducted in early 1970 an epidemic of East Coast 
Fever during mid 1970 has eliminated perhaps three-quarters of the cattle from South 
Pare, causing greater man dependence of anophelines and a striking rise in sporozoite- 
rates. C.  C.  DRAPER, J.  L.  M.  LELIJVELD, Y.  G.  MATOLA AND  G.  B.  WHITE  907 
TABLE II.  Spleen and  parasite rates  in  S.  Pare area February to March  1970. 
Age groups  Swamp  villages  Roadside villages 
0-11 months 
12-23 months 
2-  4 years 
5-  9 years 
10-14 years 
15-19 years 
20-39 years 
Over 40 years 
No. examined 
Spleen rate 
Parasite rate 
No. examined 
Spleen rate 
Parasite rate 
No. examined 
Spleen rate 
Parasite rate 
No. examined 
Spleen rate 
Parasite rate 
No. examined 
Spleen rate 
Parasite rate 
No. examined 
Spleen rate 
Parasite rate 
No. examined 
Spleen rate 
Parasite rate 
No. examined 
Spleen rate 
Parasite rate 
68 
16 
24 
69 
37 
30 
187 
40 
32 
227 
54 
51 
106 
46 
47 
46 
31 
41 
159 
38 
24 
111 
38 
9 
33 
9 
6 
42 
12 
17 
90 
26 
28 
283 
35 
38 
291 
23 
28 
41 
14 
29 
33 
24 
33 
23 
30 
0 
89%  of infections were with Plasmodium falciparum,  10.2%  with P. malariae, and 
0.8%  with P. ovale, similar proportions to those before spraying. The mean  densities 
of P. faldparum  infections, when  compared with those before spraying, showed a  rise 
in those of the 5 to 9 years and 10 to 14 years of age groups, compatible with a delay in 
the acquisition of immunity. This can be seen also in Figure 1 where the peak prevalence 
of parasitaemia in  1970  has  been  shifted  towards  the  older school age  children.  The 
peak prevalence rate  of gametocytes (13%  in  1970,  compared with  30%  in  1955  and 
5%  in  1959)  still occurred in the  1 to 2  year age group. 
Serological studies 
While films were made blood was also collected into heparirfized capillary tubes for 
serology as  described  by  OTIENO  et  al.  (1971).  Several tubes  were  taken  from  each 908  MALARIA IN  THE  PARE  AREA  OF  TANZANIA 
person and after separation the sera were stored frozen. One set of samples was examined 
for malaria antibodies in East Africa using the indirect fluorescent antibody test (IFAT) 
with P. fiddi in a thin film (OTIENO et al., 1971). Another set was examined in London 
by the IFAT with P. faldparum in a thick film following, with minor modifications, the 
method of StlLZER et al. (1969).  The prevalence of antibodies by age groups, as  deter- 
mined by these two methods, is shown in Figure 2, where swamp and roadside villages 
have been combined and the parasite and spleen rates are given for comparison. Figure 
3 shows the geometric mean reciprocal titres (GMT) of the antibodies. The heterologous 
P. fieldi  antigen is  almost as  sensitive  as  the  P. falciparum in  this  community, the 
prevalence rates detected by the two methods being usually fairly close to each other. 
The greater sensitivity of the homologous P. falciparum antigen is, however, shown by a 
comparison of the GMT's of the antibodies detected by the two methods, those with 
P. falciparum being far higher. 
100 
80 
70 
60 
Parasite 
Rate %  50 
40  - 
0 
O-ll  12-23  2",4  5-0  Age Groups  < 
Months ---~ "  ,c 
~  March-June  1955 
October 1958  to Januaw 1959 
February - March 1970 
10-14  15-19  20-39  over 40 
Years  '  '  > 
FIG. 1. Parasite rates in S. Pare swamp villages before and after spraying. 
A  large proportion of the antibodies detected in the infants under one year old 
would be congenitally transmitted. The falls in the prevalence rates, and more particularly 
in the GMT's, at the age of about one year suggests that these congenital antibodies 
have begun to decrease by this time, after which the prevalence begins to rise again 
following the acquisition of malaria infections. A  similar picture in an area of hyper- 
endemic malaria was originally reported by MCGREGOR et al. (1965). 
The sharply rising curve of antibody prevalence rates in young children suggests 
that more malaria infection was  occurring than might be  deduced from the  parasite 
rates  alone.  For example, of the  1 to 2  years age group 84%  show antibodies to P. 
falciparum while only 24% show parasites, and in the 2 to 4 years age group the figures 
are 99  and 30%  respectively: Omitting the figures for the age groups under one year 
with congenital antibodies, it has been possible to fit a  curve to the figures for older 
children, by the method given by DRAPER et  al.  (1972),  corresponding to an annual 
successful inoculation rate with malaria of 0.72  or 72%  of the population (95%  con- 
fidence limits from 65 to 78).  This shows the usual discrepancy  with  the  theoretical 
inoculation rate calculated from entomological data, which has been remarked by several 
authors (e.g:, Dr.Ar~R and SMITH, 1957). C.  C.  DRAPER,  J.  L.  M.  LELIJVELD,  Y.  G.  MATOLA  AND  G.  B,  WHITE  909 
IFAT  with P.falciparum 
qO  ~~.  P.fieldi 
80  \\  //  v' 
70  \s~ 
6O 
~,  5O 
Of sera  /-~  Spleen Rate  reacting 40 
j,,a"  P ........ 
4 
2O 
Parasite Rate 
0  I  I  I  I  I  I  I  I  I  I  lover 40 I  AgeGroups:  0-2  3-5  6-8  9-11  12-23  2.4  5..9  10-14  15-19 20-39 
kz  Months  -~',:  Years  •1  No's.examlned  for antibodies: 
With P, fok:lparum  antigen  7  23  24  30  99  218  129  22  31  23  29 
With P.fleldi  antigen  7  16  22  19  97  197  140  129  58  65  40 
FIG. 2. Malaria antibodies and parasite and spleen rates for  S.  Pare  swamp and roadside 
villages combined, 1970. 
14.0 
10.012"0  ~  ~parum 
/  IFAT with P.fieldi 
Log  2 of  ~  //f~  ~-." 
titre  8.0  /f~ 
/ 
ss,~  .j 
6.0  ....... 
i  i  I  I  i  i  i  i  I 
4.0  I  0.  2  I  3-5  '  6-8  9-1!  12-23  2-4  5-9  10-14  15-19  20-39 Over40 
Age Groups  I,  Months  ~l,  Years 
FIG. 3. Geometric mean positive titres of malaria antibodies for S. Pare swamp and road- 
side villages combined, 1970. 
Measurement  of haemoglobin  levels 
One of the few positive observations made during attempts to assess the effects of 
the successful  1954-1959  Scheme on the general health of the population was a rise in 
levels of haemoglobin. This occurred at all ages but there was a particular improvement 
amongst the younger age groups (DRAPER, 1960).  In 1970 haemoglobin levels were again 
measured in the  South Pare  on a  sample  drawn from the  same swamp and roadside 
areas  as  in  1954-1959,  using the  same method of estimation (the M.R.C.  grey-wedge 
photometer). The results are given in Table  III, together with those at the beginning 
and end of the  Scheme.  The  latter included also measurements made on a  sample of 
people  from  Taveta,  who  were  not  examined  again  in  1970,  but  their  haemoglobin 
levels  at previous  times  were similar to those in  South Pare.  With  the resurgence of 
malaria there has  been  a  general  deterioration  of haemoglobin levels  although this  is 910  MALARIA IN  THE  PARE AREA OF TANZANIA 
significant only in the younger age groups, but they are still above the levels found in 
1955 before any malaria control. 
TABLE III. Mean haemoglobin levels in g. per 100 ml. 
Sex and age group 
Both sexes: 
2-11 months 
12-23 months 
2-  4 years 
5-  9 years 
Males: 
10-14 years 
15-19 years 
20-39 years 
Feb-Mar  1970 
No. ex.  Mean 
Aug. 1958-Feb. 1959 
No. ex.  Mean 
88  9.7  ~k 
104  9"9  :k 
226  11-6  :k 
1.4  106 
1 "4  87 
1 "5  102 
Over 40 years 
250 
10"9  ±  1-2 
11"2  4-  1"1 
12"2  ±  1"4 
12-9  ±  1"1 
Females: 
10-14 years 
15-19 years 
20-39 years 
Over 40 years 
227  12.1  4-  1-3 
83  12.5  4-  1.3 
30  12.9  :k  1.7 
58  13.8  ~:  1.7 
56  13.2  4-  1.7 
90  12.6  ±  1.3 
44  12-3  ±  1-7 
99  11.8  ±  1.6 
47  12.4  4-  1.8 
132  13.1  ±  1.2 
63  14-8  ±  1.7 
121  15-2  4-  1.5 
133  14.5  ±  1.5 
87  13.2  ±  1.1 
57  13.0  ±  1.5 
182  12.9  ±  1.4 
92  13-4  ±  1-4 
Feb.-June  1955 
No. ex.  Mean 
40  9.2  ±  1-6 
40  8"9  ±  1.8 
108  10.4  ±  1"5 
245  11.6  4-  1.6 
156  12"0  ±  1.5 
44  12-9  ±  1.5 
182  13.5  ±  1.8 
163  12.6  ±  1.9 
104  12.3  ±  1"6 
82  12.0  ±  1-9 
215  11.6  -k  1'8 
130  11.6  ~:  1"6 
Discussion 
Although the densities of the vectors and the theoretical malaria inoculation rates 
in the  South Pare area have almost returned to the levels found before the insecticide 
spraying, there has not been a similar resurgence of overt malaria in the human population 
as judged by standard malaria indices. One factor in this is probably because the older 
members of the population, of 14 years and over, still possess immunity acquired before 
the relatively short  period of malaria control.  The  high  incidence of congenital anti- 
bodies in children born of mothers  who  were alive in the previously highly malarious 
era, has been pointed out.  The serological findings, however, suggest that considerably 
more human infections may have been occurring and that many parasitaemias were being 
suppressed to submicroscopic levels. A  dissociation between the parasite rates and the 
theoretical malaria inoculation rates  was  noted also by PRmGLE (1967  and  1969),  who 
ascribed it to widespread use of small doses of antimalaria drugs. Following the cessation 
of spraying this was  encouraged in the population, and additionally there has been in 
Tanzania in recent years considerable national propaganda, commercial and government, 
for the use of these drugs. During the visit in 1970 an enquiry was made of all shops and C.  C.  DRAPER,  J.  L.  M.  LELIJVELD,  Y.  G.  MATOLA  AND  G.  B.  WHITE  911 
of the dispensary in the Gonja roadside area to discover how many antimalaria drugs 
had been sold and given out during the preceding year. A total of about 60,000 tablets 
of chloroquine, 2000 ml.  of chloroquine solution for injection, and 400 ml. of quinine 
solution  had  been  disbursed.  This  was  for  a  total  population  of between  5,000  and 
10,000.  This amount, even if reduced to a per caput consumption, could be expected to 
have some effect on the prevalence of parasites in the blood. Other recent surveys else- 
where in Tanzania by OTIS.NO et al.  (1971), and by VOLLER et al.  (1971), have shown 
falling malaria indices in places where these were formerly high, with similar dissociation 
from the antibody prevalence rates. These findings have been ascribed also to the increas- 
ing use of antimalaria  drugs.  In  such  conditions  the use of serological methods may 
give a more accurate measurement of the amount of transmission occurring. 
The last two authors mentioned above used P. fieldi as their only antigen in the 
IFAT. As shown here, this is almost as sensitive as P. falciparum in communities which 
are exposed to a considerable weight of  malaria transmission, and which could be expected 
to develop heterologous antibodies reacting with a  simian parasite as  well as  with the 
homologous human parasite.  However, in  a  less  exposed community, with antibodies 
of lower titre and with less cross reaction, a greater proportion than recorded here might 
be missed by using P. fieldi alone. This might be significant if, for example, the IFAT 
was  being used to search for small  residual  foci of transmission  in  a  malaria  control 
scheme. 
Although pre-existing immunity and the use of drugs have helped to mitigate the 
full resurgence of malaria in the Pare area, this has already been sufficient to reverse the 
improvement in  haemoglobin  levels  previously found  with  malaria  control.  PRINGLE 
(1969) has already noted the reversal of downward trends in the death rates of infants 
and young children. It is tempting to speculate what would have occurred if some degree 
of residual  insecticide spraying had been maintained  over the  last  11  years, together 
with  the  increasing  availability,  awareness  of,  and  use  of  antimalaria  drugs.  Such 
combined measures may provide the pattern for malaria control, as opposed to eradi- 
cation, in many parts of rural tropical Africa in the future. 
Summary 
A parasitological and serological survey was made in the South Pare area in 1970, 
where a residual insecticide spraying campaign had previously caused a great reduction 
in the transmission of malaria. Although the densities of the vectors and the theoretical 
inoculation rates had almost returned to pre-spraying levels the prevalence of malaria 
parasites in the human population was still significantly less  than formerly. Serological 
findings, however, suggested that more transmission was  occurring than was shown by 
the parasite rates. As well as pre-existing immunity, an important factor in the delayed 
resurgence of malaria,  and in the dissociation between parasite rates  on the one hand 
and inoculation and antibody prevalence rates on the other, was  the widespread use of 
antimalaria drugs. There was an indication of a fall in mean haemoglobin levels towards 
those of the period before malaria control. 
REFERENCES 
DRAPER, C. C. (1960). Br. reed. J., 1, 1480. 
& SMITH,  A. (1957).  Trans. R. Soc. trop. Med. Hyg., 51, 137. 
& ~  (1960).  Ibid., 54, 342. 
~,  VOLLER, A. & CARI'ENTER, R. G. (1972). Am. J. trop Med. Hyg. 21, 696. 
MCGREGOR, I. A., WILLIAMS, K., VOLL~R, A. & BILLEWlCZ,  W. Z. (1965).  Trans.  R. Soc. 
trop. Med. Hyg., 59, 395. 912  MALARIA  IN  THE  PARE  AREA  OF  TANZANIA 
OTIENO, L. H., LELIJVELD,  J., MEUWISSEN, J. H. E. TH., VERBEEK, A. M. J. A. & DOESBURG, 
W. H. (1971).  Trop. geogr. Med., 23, 369. 
PRINGLE, G. (1967).  Trans. R. Soc. trop. Med. Hyg., 61~ 69. 
(1969).  Ibid.,  63, 2. 
StrLZER, A. J., WILSON, M. & HALL, E. C. (1969).  Am. J. trop. Med. Hyg., 18~ 199. 
VOLLER, A., LELIJVELD,  J. & MATOLA, Y. G. (1971). J. trop. Med. Hyg., 74~ 45. 
WHITE, G. B. (1971).  E. Afr. med. J., 48,  122. 
& MAGAYUKA, S.  A.  (1968).  In Annual Report  1968  of East African  Institute  of 
Malaria and Vector-borne Diseases. 
WILSON, D. B. (1960).  Report on the Pare Taveta Malaria Scheme. Dares Salaam: Govern- 
ment Printer. 
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Parts  1 and  2.  Mimeographed document.  Geneva: W.H.O. 

Report on the Pare Taveta Malaria Scheme. Dares Salaam: Government Printer.

Malaria in the Pare Area of Tanzania:Malaria in the Human Population 11 Years After the Suspension of Residual Insecticide Spraying, with Special Reference to the Serological Findings

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Malaria in the Pare Area of Tanzania:Malaria in the Human Population 11 Years After the Suspension of Residual Insecticide Spraying, with Special Reference to the Serological Findings

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