View Article - Biodiversity Heritage Library

1999
Journal of the American Mosquito Control Association, l5(2):ll7-127,
Copyright O 1999 by the American Mosquito Control Association, Inc.
A HISTORICAL REVIEW OF THE F-l STRAIN OF ANOPHELES
FREEBORNI AS A HOST AND VECTOR FOR STUDIES OF MALARIA
WILLIAM
E. COLLINS
AND GEOFFR-EY M. JEFFERY
Divisktn of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention,
Public Health Service, U.S. Department of Health and Humnn Services, Atlanta, GA 30341
ABSTRACT. A reveiw was made of the use of a specific strain of Anopheles freeborni from California
(F-1) that has been used extensively in experimental investigations ofmalaria for more than 50 years. The
F-l strain of An. freeborni has been shown to be a suitable experimental host and vector for different
species of Plasmodium that cause malaria in humans and nonhuman primates for biologic, immunologic,
and chemotherapeutic studies. Eleven species of Plasmodium ftlly completed sporogonic development;
development of sporozoites within mature oocysts occurred in an additional 7 species. Transmission through
An. .freeborni from human to human, monkey to human, or monkey to monkey has been demonstrated for
9 species of Plasmodium.
KEY
WORDS
Anopheles freeborni, Plasmodium, malaria, mosquitoes
INTRODUCTION
Over the last half century, several species of
anopheline mosquitoes have served as laboratory
hosts for experimental studies on malaria. Among
these are Anopheles quadrimaculatus Say, An.
atroparvus Thiel, An stephensi Liston, An. albimanus Wiedemann, and An. freeborni Aitken.
Here we summarize some of the studies that have
established An. freeborni as one of the most useful and suitable hosts for a variety of investigations of malaria.
The F-l strain of An. (An.) freeborni Aiken
was established from eggs laid by wild-caught females collected near Marysville, CA, on March
3, 1943. The colony was supplemented by an additional 800 wild-caught females on March 15
and 25O to 400 females collected from the same
location on April 30, 1943. On August 21, 1944,
eggs were shipped from the U.S. Public Health
Service laboratory at Letterman General Hospital, San Francisco, CA, to the U.S. Public Health
Service laboratory in Columbia, SC. This was
part of the wartime "Imported Malaria Studies"
effort to determine the potential of native anophelines to transmit malaria parasites from infected
returning servicemen. Since its establishment,
this strain of An. freeborni l;.as been maintained
continuously in various laboratories where it has
served as the standard host and vector for comparative studies with many species of Plasmodium causing human and nonhuman malaria.
A suitable experimental host and vector should
be able to be reared in relatively large numbers
using standard insectary techniques, should readily feed on animal or human hosts, should support sporogonic development to the production of
infectious sporozoites, and should be capable of
transmitting the infection by feeding on a susceptible host. Preferably, a laboratory vector will be
susceptible to infection with and be capable of
transmitting
a number of different species of
Plasmodium. A review of the use of this mosquito for studies with human and nonhuman primate malaria parasites indicates that this is a remarkably usefi.rl vector for biologic, immunologic,
and chemotherapeutic studies.
HUMAN
MALARIA
PARASITES
The earliest studies with the F-l strain involved the feeding of colony-reared mosquitoes
on Plasmodium vivax-infected soldiers returning
from the South Pacific and the Mediterranean
during World War II. Young et al. (1945) reported
that 1,358 of 2,581 mosquitoes that fed on these
patients became infected; several infections with
P. vivax originating from the Pacific were experimentally transmitted by An. freeborni. Moore et
al. (1945) reported on the feeding of 64 lots of
An. freeborni on relapsing P. vivax infections in
soldiers. Mosquitoes became infected and 8 infections were transmitted to other patients by this
vector. Oocyst counts as high as 8OOper gut were
found, although the usual oocyst counts ranged
from 1 to 24. Hardman (L947) summarized the
procedures being used at that time for the laboratory rearing of these mosquitoes. These early
studies indicated that An. freeborni had high potential for more extensive investigations. Of early
interest was the relative efficiency of different
laboratory-reared anopheline vectors in transmitting different species and strains of human malaria parasites. Using simultaneous feedings,
Young and Burgess (1948) reported on the comparative susceptibility of An. quadrimaculatus
from the southeastern United States and An. freeborni from California to foreign vivax malaria;
their studies indicated that the latter was more
susceptible (more oocysts per gut and higher percentage of infection). Young et al. (1948) reported the infection of An. freeborni witln P. vivax
from different geographic origins, including the
Il]]]
u8
Table 1.
JounNnLon rne AvnnrcaN Mosqurro CoNrnol AssocrATroN
Studies on the infection and transmission of Plasmodium vivax, P. falciparum,
by Anophe les freeborni.
Species of
Plasmodium
Strains (geographic origin)
Primate hosts
P. vivax
South Pacific and Mediteranean, Sal I and Sal II (El
Salvador), Chesson (New
Guinea), West Pakistan
(Pakistan), ONG and
NAM (Indonesia), St,
Elizabeth (U.S.A.), NICA
(Nicaragua), Panama
(Panama), Vietnam I-IV
(Vietnam), Vietnam Palo
Alto (Vietnam), Brazll U
CDC (Brazil), Mauritania
VCDC (Mauritania), New
Guinea (New Guinea),
North Korean (Korea),
India VII (India), and
others
Humans, night monkeys,
squirrel monkeys, chimpanzees
P. falciparum
Mclendon (U.S.A.), Panama II (Panama), Santa
Lucia (El Salvador), Malayan IV (Malaysia),
Cambodian I (Cambodia).
West Africa I (Nigeria),
NF-54 and 3D7 (Netherlands). and Indochina I
(Thailand-Cambodia),
Burma Thau. (Burma),
Montagnard (Vietnam),
Colombia (Colombia),
Thailand (Thailand), El
Limon (Panama), and
others
Humans, night monkeys,
squirrel monkeys, chimpanzees
Solomon Islands, New Guinea, New Britain, the
Mediterranean, Burma, and the Carribean. Burgess and Young (1950) reported on a comparative
study on the susceptibility of An. quadrimaculatus and An. freeborni to the St. Elizabeth strain
of P. vivax. Here again, An. freeborni was more
Vor-. 15, No. 2
p. malariae,
and.p. ovale
References
Moore et al. 1945; Young
et al. 1945, 1948; Young
and Burgess 1948; Burgess and Young 195O;
Collins and Roberts
1991: Collins et al.
1969c, 1972b, 1973c,
1973d, 1974c, 1976a,
1976b, 1977a, 1979a,
1979d, 1980a, 1980b.
1980c. 1983a. 1985b.
1985c, 1985e,1986a,
1986c, 1987b, 1987d,
1988, 1992b, 1994a,
1998a, 1998b; Coatney et
al. 1971t Singal et al.
1977; Warren and Collins
1981; Krotoski et al.
1982; Campbell et al.
1983: Wirtz et al. 1985:
Hollingdale et al. 1985,
1986; Millet et al. 1989;
Porter and Collins 1990;
Barr et al. l99l; Charenov i t e t a l l 9 9 l ; S u l l i v a ne t
al. 1996; Nayar et al. 1997
Beier et al. 19921,Burgess
and Young 1946; Burkot
et al. 1984; Campbell et
al. 1980a, 1980b, 1982,
1986; Chege et al. 1996;
Collins et al.1963,
1964a, 1968b, 1972,
1973e, 1973f, 19'77a,
1977b, 1978, r979a,
1979c, 1979d, 1981a,
1982a,1982b, 1983b,
1986d, 1991, 1996a,
1996b. 1997b: Contacos
and Collins 1968; Sodeman et al. 1969; Coatney
et al. 1971; Chin and
Collins 1980;Collins and
Contacos 1980; Ponnudurai et al. 1982; Mazier et
al. 1984; Techlehaimanot
et al. 1987; Graves et al.
1988: Renia et al. 1988:
Do Rosario et al. 1989:
Millet et al. 1991a; Shahabuddin et al. 1993;
Vaughn et al. 1994a,
1994b; Noden et aI.
1995; Vaidya et al. 1995;
Gozar et al. 1998
susceptible than was An. quadrimaculatus. This
strain, of probable U.S. origin, was frequently
used for the induction of malariotherapy of patients with neurosyphilis, a standard treatment at
that time. With the cessation of the use of malaria
studies on
for the treatment of neurosyphilis,
JUNE 1999
HISToRICAL
REvIEw
Table 1.
Species of
Plasmodium
ll9
oF ANoPHELES FREEBORNI
Strains (geographicorigin)
Continued.
Primate hosts
References
P. malariae
USPHS (U.S.A.), Philippines, Nigeria, Uganda,
China I/CDC
Humans, night monkeys,
squirrel monkeys, chimDanzees
P. ovale
Donaldson (South Pacific),
West Africa, Nigerian
Humans, chimpanzees
transmission to humans ceased. With the subsequent establishment of P. vivax in New World
monkeys, a large number of different isolates and
strains of P. vivax were now available for studv
it An. freebornl (Table 1).
Burgess and Young (1946) were the lst to report the experimental transmission by An. freeborni of Plasmodium falciparum
(Mclendon
strain) to 2 patients; prepatent periods were 15
and 29 days. Anopheles freeborni then became
one of the standard hosts and vectors for transmission studies with this parasite. Jeffery et al.
(1963) reported on studies with a multidrug-resistant strain of P. falciparum from Thailand in
which 6 patients were infected via the bites of
An. freeborni.
In a comparative susceptibility
study based on oocyst densities, Collins et al.
(L964a) demonstrated that, with a strain of P.
falciparum from Panama, An. freeborni was more
heavily infected than was An. quadrimaculatus or
even a coindigenous strain of An. albimanus.
However, the adaptation of various strains of P.
falciparum to New World monkeys opened up a
new field of study where An. freeborni was exposed to isolates and strains of the parasite from
distant geographic areas (Table 1).
Plasmodium malariae was first shown to be
transmissible by An- freeborni
by Young and
Burgess (1947). Little further success in the
transmission of this parasite was obtained until
Contacos and Collins (1969) reported the transmission of P. malariae from an infected night
monkey (Aotus sp.) to humans. Although subsequent studies indicated monkeys and chimpanzees would support the development of p. malariae gametocytes infective to An. freeborni,
transmission via sporozoites to other monkeys
and chimpanzees was not successful.
Chin et al. (1966) reported the transmission of
a West African strain of Plasmodium ovale from
human to human using An. freeborni. Successful
Young and Burgess 1961;
Collins and Contacos
1969: Contacos and Collins 1969; Coatney et al.
1971; Collins et al.
1973a, 1975a, 1984a,
1989a, r989b, l99Od,
1994b. 1997a:.Millet et
al. 1988a: Nagasawa et
al. 1988
Chin et al- 1966: Collins et
a1. I969c. 1987c: Coatney et al. l97l; Mazier
et al. 1987; Nagasawa et
al. 1987; Millet et al.
1994; Morris et al. 1996
experimental studies with P. ovale and An. freeborni have also been conducted in chimpanzees.
Different strains of this parasite readily infect An.
(liver stages) of
freeborni, and exoerythrocytic
the parasite have been demonstrated in squirrel
monkeys (Saimiri spp.). However, no erythrocytic-stage infections have been established in New
World monkeys.
The ready infectivity of many different strains
of human malaria parasites from diverse geographic areas to An. freeborni suggested that this
mosquito could serve as a universal host for a
variety of chemotherapeutic
and immunologic
studies. In fact, this has become the case in several laboratories in the United States.
NONHUMAN
PRIMATE
PARASITES
MALARIA
Monkeys have long been used a models for
chemotherapeutic and immunologic studies with
malaria parasites, and both Old World and New
World monkeys have been infected with various
species of Plasmodium. For almost 40 years, we
have usedAn. freeborni as a laboratory vector for
a variety of studies on malaria in nonhuman primates (Table 2). It early became apparent that,
although in most instances An. freeborni
was
highly susceptible to the development of the oocyst stage, some species of Plasmodium failed to
develop to the point of sporozoites being present
in the salivary glands. With all but a few species,
oocyst densities in An. freeborni were high; oocyst counts could be used as an indicator of gametocyte infectivity.
However, transmission via
sporozoites could only be obtained if oocysts
containing mature sporozoites were crushed and
then injected into the primate. Plasmodium cynomolgi, P. gonderi, P. simium, P. fragite, and
P. brasilianum, parasites of monkeys, developed
fully, including the presence of sporozoites in the
120
Table 2.
Species of
Plasmodium
JounNnl on tHe AlvrnnrclNMosqurro Corqrnol AssocterroN
Studies on the infection and transmission of nonhuman primate-infecting
Anopheles freeborni.
Strains (geographic origin)
Primate hosts
P. brasilianum
S (Colombia), AT (Panama) Peruvian I-III
Night monkeys, squirrel
monkeys, spider monkeys, humans
P. coatneyi
Hackeri (Malaysia)
Macaques
P. crynomolgi
B, Berok, M, Gombak
(Malaysia), ceylonensis
(Sri Lanka), RO (Assam-Burma), Celebes
(Philippines), Cambodian
Macaques, night monkeys,
squirrel monkeys
P. fieldi
Macaques
P. fragile
Hackeri, N-3, ABI, Malaysian
Sri Lanka, Nilgiri (India)
P. gonderi
Mandrill
P. hylobati
WAK
P. inui
Taiwanland2(Taiwan),
N-34, Perlis, Perak, I-eaf
Monkey I and II, kucosphyrus, Mulligan,
and others (Malaysia),
OS (India)
Malaysian
Macaques, night monkeys,
squirrel monkeys
P. knowlesi
H, Malaysian, Hackeri
(Malaysia)
P, reichenowi
Chimpanzee (West Africa)
Macaques, humans, night
monkeys, squirrel monkeys
Chimpanzees
P. schwetzi
Chimpanzee (West Africa)
Chimpanzees, humans
P. simiovale
Sri Lanka
Macaques
P. simium
Howler (Brazil)
Night monkeys, squirrel
monkeys
P. jefferyi
(West Africa)
(Indonesia)
salivary glands of An. freeborni. Plasmodium
schwetzi and P. reichenowi, parasites of chimpanzees and gorillas, and P. hylobati, a parasite
of gibbons, also developed to maturity in this
vector.
Some parasites failed to develop beyond the
presence of mature sporozoites in oocysts and
Macaques, Night monkeys,
squirrel monkeys
Macaques
Gibbons
Gibbons
Vor-. 15, No. 2
species of Plasmodium by
References
Collins et al. 1969b,
1985d, 1990b, 1993; Sodeman et al. 1969; Coatney et al. l97l
Held and Contacos 1967;
Coatney et al. l97l;'
Coffins et al.1992a
Coatney et al. 1971; Collins et al. 1972c, l9'15b,
1985a, 1998; Krotoski et
al. 1973: Omar and Collins 1973; Omar et al.
1973, 1974:' Atkinson et
al. 1989; Millet et al.
1989,1990
Coatney et al. 1971; Collins et al. 1984b,1992a
Collins et al. 1967, 1974b,
1975c, l990a, 1992a;
Coatney et al. 19'71
Collins et al. 1964b,
1992a; Coatney et aI.
1971; Collins and Contacos 1980
Coatney et al. l97l; Collins et al. 1972d
Collins et al. 1968a,
198lb; Held et al. 1968;
Coatney et al. l97l:'
Nguyen-Dinh et al.
1980; Collins and Warren 1998
Collins and Orihel 1969;
Coatney et al. 1971; Rodenberg 1985; Millet et
al.1988b
Coatney et al. 19'71
Coatney et al. 1971; Collins et al. 1986b
Collins et al. 1969c; Contacos et al. 1970; Coatney et al. t97l
Coatney et al. l97l; Collins et al. 1972a,1992a;
Collins and Contacos
1979
Collins et al.1969a,
1973b, 1974a, 1979b,
1987a; Coatney et al.
197 |
transmission could be obtained only through the
injection of mechanically harvested sporozoites.
Those parasites requiring mechanical harvesting
included Plasmodium knowlesi, P. simiovale, P.
coatneyi, P. fieldi, and P. inui.
Anopheles freeborni has been shown to support
the complete sporogonic development of many
Juxe 1999
HISToRICAL
70
Rgvrsw
oF ANoPHELES FREEBoRNI
SPOROZOIIESIN SALIVARYGLANDS
sPoRozotTEs
tNoocYsTs
'15 17 17
11 ?? 12 11 12 13 12 14
12r 12' 14' 14' 13* 161 16r
a
260
o
E
Qso
e
cr40
UJ
-
lil
=3 0
o20
z
uJ .^
0
inui
cynomolgi gondei lalcipmm simium reichenowimaliliae knowl$i simiovale ietleN
lngile
schweai viw
Nah brcilimm
coatneyi tieldi
Wobati
SPECIESOF PIASMODIUM
Q a o e v s ! r o o r v s f f i r z o r v sf f i r + o n v s
Fig. l.
Mean oocyst diameter at 8, 10, 12, and 14 days and days when sporozoites are present in salivary glands
or mature oocysts inAnophelesfreeborni
mosqtoitoes infected with 18 species of Plasmodium when incubated at 25
+ 1"C.
different species of Plasmodium, but fails to do
so for other parasites (Fig. 1). This mosquito
readily supports full development, to the presence of sporozoites in the salivary glands, of P.
vivax and P. ovale and the related nonhunman
tertian parasites P. cynomolgi, P. gonderi, P.
schwetfi, and P. simium; P. falciparum and the
related parasite P. reichenowi; P. malariae and
the related quartan parasite P. brasilianum:
and
the tertian parasite P. hylobati. Anopheles freeborni supports to a lesser extent the sporogonic
development of the tertian parasites P. fragile, P.
Table 3.
Transmission
j"ff"ryi,
P. fieldi, P. simiovale, and P. coatneyi;
the quartan parasite P. inui; and the quotidian
parasite P. knowlesi. In these latter species, infective sporozoites are present in mature oocysts,
but are rarely found in the salivary glands. Infectivity of these sporozoites has been demonstrated
by the injection of susceptible hosts with sporozoites mechanically released from mature oocysts. In our studies with monkeys (Table 3),
transmission via bite or the injection of sporozoites dissected from An. freeborni has been
demonstrated with 9 species of Plasmodium. Be-
of 9 species of Plasmodium from monkey to monkey by Anopheles freeborni
mosquitoes.
Transmissions
Species of
Plasmodium
Donor
P. brasilianum
Recipient
P. coatneyi
P. cynomolgi
Saimiri
Ateles
Macaca mulatta
M. mulatta
Saimiri
Ateles
M. mulatta
M. mulatta
P. falciparum
Aotus
Aotus
Aotus
Aotus
P.
P.
P.
P.
P.
M. mulatta
M. mulatta
M. mulatta
M. mulntta
Aotus
M. mulatta
M. mulatta
M. mulatta
M. mulatta
Aotus
Aotus
Samiri
Saimiri
Saimiri
Bite
Injectionr
9
3
0
32
0
0
6
a1
fieldi
gonderi
inui
knowlesi
vivax
3
0
44
0
1
0
8
3
0
o
0
37
2
3
l
0
0
l
a
'Intravenous
or intrahepatic injection of sporozoites dissected from omysts or infected salivry
glands.
Prepatentperiod(days)
Range
t8-42
t8-43
14-15
8-36
8-24
l5-19
10-69
t6-69
l8-30
t2-17
t2-15
5-6
14-55
1417
39
28
Median
34.O
36.0
15.0
I1.0
9.0
18.0
23.O
22.O
18.0
13.0
13.5
6.0
2t.o
20.s
39.0
28.0
122
JounNll
oF THE AMERlc,rN Mosquno
cause of the invariable success in all species tested, there is no reason to believe that sporozoites
from salivary glands or mature oocysts of the
other species of human and nonhuman primate
malaria parasites produced in An. freeborni could
not also be infective to susceptible primate hosts.
Ano p he I es fre eb o rni, after long-term establishment in the laboratory, has been shown to be
highly susceptible to many species of Plasmodium from widely separated geographic areas. In
addition, the susceptibility
to many different
strains of the parasites from widely separated
geographic areas allows us to use this mosquito
as a standard for all studies with human malaria
parasites and most of the nonhuman-infecting
species.
Many questions remain concerning the relationship between this mosquito host and the different species of human and nonhuman primate
malaria parasites. The reasons why one species
of Plasmodiun develops completely, whereas another does not, deserves investigation. Why are
oocyst densities higher in An. freeborni than rn
other mosquitoes when simultaneously fed on
certain strains of Plasmodium? Why is the reverse true with other species and strains of parasites when different species of anophelines simultaneously
feed on the same animal? The
extensive data available from studies on the F-l
strain of An. freebornl generate more questions
than answers on the vector-parasite relationships
for this extremely important group of human
pathogens.
REFERENCES CITED
CoNrnol
AssocrATloN
V o l . 1 5 ,N o . 2
of cultured Plasmodium falciparum. Trans. R. Soc.
Trop. Med. Hy g. 74:668-669.
Campbell, C. C., W. E. Collins, J. M. Roberts and A.
Armstead. 1986. Adaptation of the Indochina VCDC
stratn of Plasmodium falciparum to the squirrel monkey
(Saimiri sciureus). Am. J. Trop. Med. Hyg. 35:472-475.
Campbell, C. C., H. C. Spencer, W. Chin and W. E. Cotlins. 1980b. Adaption of cultured Plasmodiumfalciparum to the intact squirrel monkey (Saimiri sciureus).
Trans. R. Soc. Trop. Med. Hyg. 74:548-549.
Campbell, C. C., W. Chin, W. E. Collins, S. M. Teitsch
and D. M. Moss. 1979. Chloroquine-resistant Plasmodium falciparum from East Africa. Lancet 1:11511t54.
Campbell, C. C., W. E. Collins, W. Chin, J. M. Roberts
and J. R. Broderson. 1983. Studies on the Sal I strain
of Plasmodium vivrtx in the squirrel monkey (Saimiri
sciureus). J. Parasitol. 69:598-601.
Campbell, C. C., W. E. Collins, P Nguyen-Dinh, A. Barber and J. R. Broderson. 1982. Plasmodiumfalciparum
gametocytes from in vitro culture develop to sporozoites which are infectious to primates. Science 217:
1048-1050.
Charoenvit, Y., W. E. Collins, T, R. Jones, P. Millet, L.
Yuan, G. H. Campbell, R. L. Beaudoin, J. R. Broderson
and S. L. Hoffman. 1991. Inability of malaria vaccine
to induce antibodies to a protective epitope within its
sequence. Science 251:668-67 l.
Chege, G. M., C. B. Pumpuni and J. C. Beier. 1996. Proteolytic enzyme activity and Plasmodium falciparum
sporogonic development in three species of Anopheles
mosquitoes. J. Parasitol. 82: I 1-16Chin, W. and W. E. Collins. 1980. Comparative studies on
two strains of Plasmodium falciparum isolated by the
culture method of Trager and Jenson. Am. J. Tiop. Med.
Hyg. 29:1143-1146.
Chin. W.. P. G. Contacos and J. N. Buxbaum. 1966. The
transmission of a West African strain of Plasmodium
ovale by Anopheles freeborni and Anopheles maculatus.
Am. J. Trop. Med. Hyg. 15:690-693.
Coatney, G. R., W. E. Collins, McW Warren and P G.
Contacos. 1971. The primate malarias. U.S. Government Printing Office, Washington, DC.
Collins, W. E. and P G. Contacos. 1969. Infectivity of
Plasmodium malariae in the Aotus trivirgatus monkey
to Anopheles freeborni mosquitoes. J. Parasitol. 55:
1253-1257.
Collins, W. E. and P G. Contacos. 1972. Transmission of
from monkey to monkey by the
Plasmodiumfalciparum
bite of infected Anopheles freeborni mosquitoes. Tlans.
R. Soc. Trop. Med. Hyg.66:371-372.
Collins. W. E. and P G. Contacos. 1979. Infection and
transmission studies with Plasmodium simiovale in the
Macaca mulatta monkey. J. Parasitol. 65:6O9-612.
Collins, W. E. and P G. Contacos. 1980. Infection and
transmission of Plasmodium gondei inthe Macaca mulatta monkey. J. Parasitol. 66:998-1002.
Collins, W. E. and T. C. Orihel. 1969. The sporogonic cyle
of P Ia smodium j effe ry i. J. Parasitol. 55 : l24O -1246.
Atkinson, C. T,, P Millet, W. E. Collins and M. Aikawa.
1989.Localizationof the circumsporozoiteantigenin
exoerythrocytic schizonts of Plasmodium cynomolgi.
Am. J. Trop.Med. Hyg. 40:13l-140.
Barr, P J., K. M. Green, H. L. Gibson, I. C. Bathurst, I.
A. Quakyi and D. C. Kaslow. 1991.RecombinantPfs25
protein of Plasmodium falciparum elicits malaria transmission-blocking immunity in experimentalanimals. J.
Exp. Med. l7 5:1203-12O8.
Beier,J. C., M. S. Beier,J. A. Vaughn,C. B. Pumpuni,J.
R. Davis and B. H. Noden. 1992. Sporozoitetransmission by Anophelesfreeborni and Anopheles gambiae
experimentallyinfected with Plasmodiumfalc iparum. J.
Am. Mosq. Control Assoc. 8:404-408.
Burgess, R. W. and M. D. Young. 1946. Experimental
transmissionof P. falciparumby Anophelesmaculipennis freeborni. J. Natl. Malar. Soc. 57:150-151.
Burgess,R. W. and M. D. Young. 1950.The comparative
susceptibility of Anopheles quadrimaculatus and
Anophelesfreeborni to infection by Plasmodium vivax Collins, W. E. and J. M. Roberts. 1991. Anopheles Satnbiae as a host for geographic isolates of Plasmodium
(St. Elizabeth strain). J. Natl. Malar. Soc.9:218221.
vivttx. L Am. Mosq. Control Assoc. 7:569-573.
Burkot, T. R., J. L. Williams and I. Schneider.1984. InCollins, W. E. and McW. Warren. 1998. Studies on infecfectivity to mosquitoes of Plasmodium falciparum
tions with two strains of Plasmodium inui from Taiwan
clones grown in vitro from the same isolate. Trans. R.
in rhesus monkeys and different anopheline mosquitoes.
Soc. Trop. Med. Hyg. 78:.339-341.
J. Parasitol. 84:547-551.
Campbell,C. C., W. Chin, W. E. Collins and D. M. Moss.
1980a.Infection of Anophelesfreeborni by gametocytes Collins. W. 8.. P G. Contacos and W. Chin. 1973a. Ex-
JuttB 1999
HISToRICAL
REVIEW OF ANOPHELES FREEBORN]
perimental infection in man with Plasmodium malariae.
Am. J. Trop. Med. Hyg. 22:685-692.
Collins, W. E., P. G. Contacos and E. G' Guinn. 1969a.
Observations on the sporogonic cycle and transmission
of Plasmodium simum Da Fonseca. J. Parasitol. 55:
814-816.
Collins, W. E., P G. Contacos and J. R. Jumper. 1972a.
Studies on the exoerythrocytic stages of simian malaria
Ylll. Plasmodium simiovale. J. Parasitol. 58:135-141.
Collins, WWE,., P G. Contacos and J. R. Jtmper. 1974a.
Studies on the exoerythrocytic stages of simian malaria.
IX. Plasmodium simium. J. Parasitol. 60:674-676.
Collins. W. E'.. P. G. Contacos and B. B. Richardson.
1975a. Studies on human malaria in Aotus monkeys.
VI. Infectivity of Plasmodium malariae to different
anophelines. J. Parasitol. 61 :941-943.
Collins, W. E., G. M. Jeffery and R. W Burgess. 1963.
Comparative infectivity of two strains of Plasmodtum
falciparum to Anopheles quadrimaculatus Say, Anopheles freeborni Aitken, and Anopheles albimanus
(Wied.). Mosq. News 23:702-104.
Collins, W. E., J. C. Skinner and P Mehaffey. 1985a. Infection of Aotus azarae boliviensis monkeys with the
RO strain of Plasmodium cynomolgi. J. Parasitol. 7l:
848-849.
Collins, W. E., P G. Contacos, E. G. Guinn and J. R. Held.
1967. Studies on the transmission of simian malaria. III.
Infection and transmission of Plasmodium coatneyi
with Anopheles.freeborni and A. balabacensis balabacensis mosquitoes. J. Parasitol. 53 : I I 30-1 134.
Collins, W. E'., P. G. Contacos, E. G. Guinn and J. R. Held.
1968a. Some observations on the transmission of P/csmodium inui. I. Parasitol. 54:846-847.
Collins, W. E., P G. Contacos, E. G. Guinn and J. R. Held.
1969b. Infectivity of Plasmodium brasilianun for six
species of Anopheles. J. Parasitol. 55 :685-686.
Collins, W. E'., P G. Contacos, E. G. Guinn and J. C.
Skinner. 1973b. Plasmodium simium in the Aotus trivirgatus monkey. J. Parasitol. 59:49-51.
Collins, W. E., P G. Contacos, W A. Krotoski and W. A.
Howard. 1972b. Transmission of four Central American
strains of Plasmodium vivax from monkey to man. J.
Parasitol. 58 :332-335.
Collins, W. E., P G. Contacos, B. B. Richardson and J.
C. Skinner. 1976a. Development of different strains of
Plasmodium vivax in two species of Anopheles. Arr:^.J.
Trop. Med. Hyg. 25:372-37 5.
Collins, W. E'., P G. Contacos, J. C. Skinner and E. G.
Guinn. 1972c. Studies on the transmission of simran
malaria. V. Infection and transmission of the B strain
of Plasmodium cynomolgi. J. Parasitol. 58:653-659.
Collins, W. E., P G. Contacos, P S. Stanfill and B. B.
Richardson. 1973c. Studies on human malaria in Aotus
monkeys. I. Sporozoite transmission of Plasmodium vivax from El Salvador. J. Parasitol. 59:606-608.
Collins, W E., G. M. Jeffery, J. C. Skinner and A. J.
Harrison. 1964a. Comparative susceptibilty of a strain
of Plasmodium falciparum
from Panama to thee species of Anopheles as studied by membrane feeding.
Mosq. News 24:28-31.
Collins, W. E., E E. Jones, C. G. Dobrovolny and H.
Akins. 1964b. Studies on the comparative susceptibility
of Anopheles freeborni Aitken, A. quadrimaculatus
Say, A. labranchiae atroparvus Thiel, and A. sundaicus
Rodenwaldt to Plasmodium gonderi with a report of
transmission by A. freeborni. Mosq. News 24:365-369.
Collins, W. E., P Nguyen-Dinh, J. C. Skinner and B. B.
t23
Sutton. 1981a. Infectivity of a strain of Plasmodrum
falciparum from Hainan, People's Republic of China,
to different anophelines. Am. J. Trop. Med. Hyg. 30:
538*540.
Collins. W. E.. I. K. Schwartz, J. C. Skinner and J. R.
Broderson. 1984a. Studies on the Uganda VCDC strain
of Plasmodium malariae in Bolivian Aotzs monkeys
and different anophelines. J. Parasitol. 7O:677-681.
Collins, W. E'., J. C. Skinner, B. B. Richardson and A' Y'
Huong. 198Ib. Development of Plasmodium inui inthe
Aotus trivirgatus monkey. J. Parasitol. 67:222-225.
Collins. W. E.. J. C. Skinner, B. B. Richardson and P S.
Stanfill. 1975b. Tiansmission of Plasrnodium cynomolgi
to Aotus trivirgatus monkeys. J. Parasitol. 6l:146-148.
Collins, W. 8., J. C. Skinner, B. B. Richardson and P S.
Stanfill. 1975c. Studies on the transmission of simian
malaria. VI. Mosquito infection and sporozoite transmission of Plasmodium fragile. J. Parasitol. 6l:718721.
Collins, W. 8., J. C. Skinner, P S. Stanfill and B. B. Richardson. 1978. Studies on the Burma (Thau.) strain of
Plasmodium falciparum in Aotus trivirgatus monkeys.
J. Parasitol. 64:497 -5OO.
Collins, W. 8., J. C. Skinner, McW. Warren and B. B.
Richardson. 1976b. Studies on human malaria in Aotus
monkeys. VII. Comparative infectivity of two strains of
Plasmodium vivax lo Anopheles freeborni, A. maculatus
and four strains of A. albimanus. J. Parasitol. 62:19O194.
Collins, W. 8., P S. Stanfill, B. B. Richardson and C. S.
Smith. 1974b. Transmission of Plasmodium fragile to
Aotus trivirgatus monkeys. J. Parasitol. 6O:.7I9-72O.
Collins, W. 8., McW. Warren, B. B. Richardson and J. C.
Skinner. 1979a. Selected pupal phenotypes of Anopheles freeborni and their susceptibility to Plasmodiumfalciparum and P. vivax. Mosq. News 39:466-472.
Collins, W. E., McW. Warren, J. C. Skinner and B. B.
Richardson. 1980a. Studies on the West Pakistan strain
of Plasmodium vivax in Aolus monkeys and anopheline
mosquitoes. J. Parasitol. 66:7 8O-7 85.
Collins, W. E., McW. Warren, J. C. Skinner and B. B.
Sutton. 1985b. Infectivity of two strains of Plasmodium
vivttx to Anopheles albitarsis mosquitoes from Colombia. J. Parasitol. 7 1:77 l-773.
Collins, W. E., P G. Contacos, W. Chin, M. H. Jeter and
P E. Briesch. 1980b. Transmission of Plasmodium vivax from Vietnam by four different anophelines. Am.
J. Trop. Med. Hyg. 29:473-375.
Collins, W. E., P G. Contacos, P. C. C. Garnham, McW.
Warren and J. C. Skinner. l9'72d. Plasmodium hylobati;
a malaria parasite of the gibbon. J. Parasitol. 58:123124.
Collins. W. E'.. P G. Contacos. E. G. Guinn. M. H. Jeter
and T. M. Sodeman. 1968b. Monkey to man transmission of Plasmodium falciparum by Anopheles freeborni
mosquitoes. J. Parasitol. 54:1166-1170.
Collins, W. E., P. G. Contacos, J. R. Jumper, C. S. Smith
and J. C. Skinner. 1973d. Studies on human malaria in
Aotus morkeys. III. Exoerythrocytic stages of the Salvador II strain of Plasmodium vivax. J. Parasitol. 59:
859-866.
Collins, W. E., P G. Contacos, J. C. Skinner, A. Y. Huong
and W. Chin. 1982a. Studies on the Cambodian I strain
of Plasmodium .falciparum in Aotus monkeys. J. Parasitol. 68:877-883.
Collins, W. 8., G. G. Galland, J. S. Sullivan. C. L. Morris
and B. B. Richardson. 1996a. The Santa Lucia strain of
124
Jounnel op mB AvenrceN Mosqurro CoNtr.ol AssocnrroN
Plasmodium falciparum as a model for vaccine studies.
II. Development of Aotus vociferans as a model for testing transmission-blocking vaccines. Am. J. Trop. Med.
Hyg. 54:380-385.
Collins, W. E'., H. M. McClure, R. B. Swenson, P. Mehaffey and J. C. Skinner. 1986a. Infection of mosquitoes
with Plasmodium vivax from chimpanzees using membrane feeding. Am. J. Trop. Med. Hyg. 35:56-60.
Collins, W E'., C. L. Morris, B. B. Richardson, J. S. Sullivan and G. G. Galland. 1994a. Further studies on the
sporozoite transmission of the Salvador I strain of P/asmodium vivcrx. l. Parasitol. 80:512-517.
Collins, W. E'., F A. Neva, E. Chaves-Carballo, P S. Stanfill and B. B. Richardson. 1973e. Studies on human
malaria in Aotus monkeys II. Establishment of a strain
of Plasmodium falciparum from Panama. J. Parasitol.
59:6O9-612.
Collins, W. E., T, C. Orihel, P G. Contacos, M. H. Jeter
and L. S. Gell. 1969c. Some observations on the sporogonic cycle of Plasmodium schwetzi, P. vivax, and P.
ovale in five species of Anopheles. J. Protozool. 16:
589-596.
Collins, W. E., B. B. Richardson, C. L. Morris, J. S. Sullivan and G. G. Galland. 1998a. Salvador II strain of
Plasmodium vivax in Aolzs monkeys for transmissionblocking vaccine trials. Am. J. Trop. Med. Hyg. 59:29)+Collins, W. E., B. B. Richardson, J. S. Sullivan, C. L.
Morris and G. G. Galland. 1997a. Infection of Anopheles freeborni mosquitoes on New World monkeys infected with the Uganda VCDC strain of Plasmodium
mnlariae. J. Parasitol. 83: 1099-1 103.
Collins, W E., J. C. Skinner, J. R. Broderson, P Mehaffey
and B. B. Sutton. 1985c. Infection of Aotus azarae boliviensis with different strains of Plasmodium vivax. J.
Parasitol. 7 I :239 -243.
Collins. W. E.. J. C. Skinner. J. R. Broderson. B. B. Richardson and P S. Stanfill. 1989a. The Uganda VCDC
strain of Plasmodium malariae in Saimiri sciureus boliviensis. J. Parasitol. 75:3 10-313.
Collins, W. E., J. C. Skinner, M. Pappaioanou, J. R. Broderson and P Mehaffey. 1986b. The sporogonic cycle of
P la smodium re ic henow i. J. Parasitol. 7 2:292298.
Collins, W. 8., J. C. Skinner, B. B. Richardson, P S. Stanfill and P G. Contacos. 1974c. Studies on human malaria in Aolas monkeys V. Blood-induced infections
with Plasmodium vivax. J. Parasitol. 60:393-398.
Collins. W. E.. J. C. Skinner. P. S. Stanfill. B. B. Sutton
and A. Y. Huong. 1984b. Infection and transmission
studies with the N-3 strain of Plasmodium fieldi in the
Macaca mulatta monkey. J. Parasitol. 70:422-427.
Collins, W. E., McW. Warren, P. G. Contacos, J. C. Skinner and B. B. Richardson. 1979b. Infectivity of Plasmodium simium to Aotus trivirgatas monkeys and different anophelines. J. Parasitol. 65 :87 O-87 4.
Collins. W. E.. McW. Warren. J. C. Skinner. W. Chin and
B. B. Richardson. 1977a. Studies on the Santa Lucia
(EI Salvador) slrrain of P lasmodium falciparum tn Aotus
trivirgatus monkeys. J. Parasitol. 63:52-56.
Collins, W. E., McW. Warren, J. C. Skinner, A. Y. Huong
and P Nguyen-Dinh. 1983a. Observations on the infectivity of two strains of Plasmodium vivax from Vietn:unese refugees to Aotus monkeys and anopheline
mosquitoes. J. Parasitol. 69:689-695.
Collins. W. E.. McW. Warren. J. C. Skinner. B. B. Richardson and W. Chin. 1979c. Studies on the West African
1 5 ,N o . 2
I strain of Plasmodium falciparum in Aotus trivirgatus
monkeys. J. Parasitol. 65:827 -829.
Collins, W. E., McW. Warren, J. C. Skinner, B. B. Richardson and T. S. Kearse. 1977b. Infectivity of the Santa
Lucia (E1 Salvador) strain of Plasmodium falciparum to
different anophelines. J. Parasitol. 63 :57 -61.
Collins, W. E., McW. Warren, J. C. Skinneq B. B. Richardson and T. S. Kearse. 1979d. Effect of sequential
infection with Plasmodium vivax and P. falciparurn in
the Aotus trivirgatus monkey. J. Parasitol. 65:605-608.
Collins, W.E'., C. C. Campbell, J. C. Skinner, W. Chin, P
Nguyen-Dinh and A. Y. Huong. 1983b. Studies on the
Indochina VCDC strain of Plasmodium falciparum
in
Colombian and Bolivian Aotus monkeys and different
anophelines. J. Parasitol. 69: 186-190.
Collins, W. E., W. Chin, McW. Warren, A. Y. Huong, G.
M. Jeffery and J. C. Skinner. 1982b. Observations on
two strains of Plasmodium falciparum from Haiti in
Aorns monkeys. J. Parasitol. 68:657-667.
Collins, W. E'., G. G. Galland, J. S. Sulivan, C. L. Morris,
B. B. Richardson and J. M. Roberts. 1996b. The Santa
Lucia strain of Plasmodium falciparum as a model for
vaccine studies. I. Development in Aotus lemurinus
griseimembra monkeys. Am. J. Tiop. Med. Hyg. 54:
372-379.
Collins, W. E., L. H. Miller, R. H. Glew, P G. Contacos,
W. A. Howard and D. J. Wyler. 1973f. Transmission of
three strains of Plasmodium falciparum
from monkey
to man. J. Parasitol. 59:855-858.
Collins, W E'., J. C. Skinner, J. R. Broderson, B. B. Richardson, N. S.-E Ma and P S. Stanfill. 1991. Infection
of Aotus vociferans monkeys with different strains of
P lasmodium falciparum. J. Parasitol. 77 :562-567 .
Collins, W. E'., J. C. Skinner, V. K. Filipski, J. R. Broderson, P S. Stanfill and C. L. Morris. 1990b. Transmission of Plasmodium fragile to Saimiri monkeys. J. Parasitol. 76i73O-732.
Collins, W. E'., J. C. Skinner, A. Y. Huong, J. R. Broderson, B. B. Sutton and P Mehaffey. 1985d. Studies on
a newly isolated strain of Plasmodium brasilianum in
Aotus and Saimiri monkeys and different anophelines.
J. Parasitol. 7 l:767-770.
Collins, W. E., J. S. Sullivan, C. L. Morris, G. G. Galland,
B. B. Richardson and S. Nesby. 1998b. Adaptation of
a strain of Plasmodium vivax ftom Mauritania to New
World monkeys and anopheline mosquitoes. J. Parasitol. 84:619-627.
Collins, W E., J. S. Sullivan, C. L. Morris, G. G. Galland,
B. B. Richardson and J. M. Roberts. 1997b. The Malayan IV strain of Plasmodium falciparum in Aotus
monkeys. Am. J. Trop. Med. Hyg. 56:49-56.
Collins, W. E., McW. Warren, P. G. Contacos, J. C. Skinner, B. B. Richardson and Thomas S. Kearse. 1980c.
The Chesson strain of Plasmodium vivax in Aotus monkeys and anopheline rnosquitoes. J. Parasitol. 66:48849'7.
Collins, W. E'., McW. Warren, A. Y. Huong, J. C. Skinner,
B. B. Sutton and P S. Stanfill. 1986c. Studies on the
comparative infectivity of fifteen strains of Plasmodium
vivax to laboratory-reared Anopheles with special reference to Anopheles culicifacies. J. Parasitol. 72:527524.
Collins, W. 8., T. K. Ruebush II, J. C. Skinner, V. K.
Filipski, J. R- Broderson, P S. Stanfill and Carla L.
Morris. 1990c. The Peruvian III strain of Plasmodiam
brasilianum in Saimiri sciureus boliviensis monkevs. J.
Parasitol. 7 6:67 6-68O.
JuNs 1999
Hts.tonlcer- Rrvrew
op ANopnetes pnersonNt
Collins, W. E'., J. C. Skinner, J. R. Broderson, V- K. Filipski. C. M. Morris. P S. Stanfill and McW. Warren.
1992a. Susceptibility of Macaca fascicularis monkeys
from Mauritius to different species of Plasmodium. J.
Parasitol. 78:505-5 I 1.
Collins. W. E.. J. C. Skinner. J. R. Broderson. A. Y.
Huong, P C. Mehaffey, P S. Stanfill and B. B. Sutton.
1986d. Infection of Aotus azarae holiviensis monkeys
with different strains of P/a^srzodiumfalciparum. J.Parasttol. 72:525-53O.
Collins, W. E'., J. C. Skinner, M. Pappaioanou, J. R. Broderson, N. S.-E Ma, P S. Stanfill and V. Filipski. 7987a.
Transmission of Plasmodium simium to Aotus nancymai, A. vociferans, A. azarae boliviensis, and Saimiri
.sciureus boliviensis monkeys. J. Parasitol. 73:653-655.
Collins, W. E., J. C. Skinner, M. Pappaioanou, N. S.-E
Ma. J. R. Broderson. B. B. Sutton and P S. Stanfill.
1987b. Infection of Aotus vociferans (karyotype V)
monkeys with different strains of P/asmodium vivax. J.
Parasitol. 7 3:536-54O.
Collins, W. E., K. K. Grady, P Millet, J. S. Sullivan, C.
L. Morris, G. G. Galland, B. B. Richardson and C.
Yang. 1997c. Adaptation of a strain of Plasmodiumfalciparum from a Montagnard refugee to Aotus monkeys.
J. Parasitol. 83: l I7 4-1177.
Collins, W E., H. M. McClure, E. Strobert, V. K. Filipski,
J. C. Skinner, P S. Stanfill, B. B. Richardson and C.
Morris. 1990d. Infection of chimpanzees with the
Uganda VCDC strain of Plasmodium malarine. Am. J.
Trop. Med. Hyg. 42:99-1O3.
Collins, W. E'., J. C. Skinner, W. A. Krotoski, E B. Cogswell, R. W. Gwadz, J- R. Broderson, N. S.-E Ma, P
Mehaffey and B. B. Sutton. 1985e. Studies on the North
Korean strain of Plctsmodium vivax in Aolas monkeys
and different anophelines. J. Parasitol. 7I:2O-27.
Collins, W' E., H. McClure, E. Strobert, J. C. Skinner, B.
B. Richardson, J. M. Roberts, G. G. Galland, J. Sullivan, C. L. Morris and S. R. Adams. 1993- Experimental
infection of Anopheles gambiae s.s. with Plasmodium
mnlariae and P. brasilianum. J. Am. Mosq. Control Assoc.9:68-71.
Collins, W. E., M. Pappaioanou, H. M. McClure, R- B.
Swenson, E. Strobert, J. C. Skinner, V. Filipski, P S.
Stanfill, F H. Collins and C. C. Campbell. 1987c. Infection of chimpanzees with the Nigerian I strain of
Plasmodium ovale. Am. J. Trop. Med. Hyg. 37:455459.
Collins, W. E'., J. C. Skinner, J. R. Broderson, M. Pappaioanou, V. Filipski, B. B. Sutton, P. S. Stanfill, A. Y.
Huong, J. Roberts and C. Wilson. 1989b. The Uganda
VCDC strain of Plasmodium malariae in Aotus lemurinus griseimemDra monkeys. J. Parasitol. 75:.61-65.
Collins, W. E., J. C. Skinner, P Millet, V. K. Filipski, C.
L. Morris, P M. Wilkins, G. H. Campbell, P S. Stanfill,
B. B. Richardson andJ. Sullivan. 1992b. Reinforcement
of immunity in monkeys following immunization with
irradiated sporozoites of Plnsmodium vivax. Arn- J.
Trop. Med. Hyg. 46:327-334.
Collins, W. E'., J. C. Skinner, M. Pappaioanou, J- R. Broderson, H. M. McClure, E. Strob€rt, B. B. Sutton, P S.
Stanfill, V. Filipski and C. C. Campbell. 1987d. Chesson strain Plasmodium vivax in Saimiri sciureus bolivlensrs monkeys. J. Parasitol. 73:929-934Collins, W' 8., J. C. Skinner, M. Pappaioanou, J. R. Broderson, V. K. Filipski, H. M. McClure, E. Strobert, B. B.
Sutton, P S. Stanfill and A. Y. Huong. 1988. Sporozoite-induced infections of the Salvador I strain of plas-
125
modium vivax in Saimiri sciureus boliviensis monkeys.
J. Parasitol. 74:582-585.
Collins, W. E., H. O. Lobel, H. McClure, E. Strobert, G.
G. Galland, E Taylor, A. L. Baretto, R. R. Roberto, J.
C. Skinner. S. Adams. C. L. Morris and J. Sullivan.
1994b. The China VCDC strain of Plasmodium mnlariae in Aotus monkeys and chimpanzees. Am. J. Trop.
Med. Hyg. 50:28-32.
Contacos, P G. and W. E. Collins. 1968. Falciparum malaria transmissible from monkey to man by mosquito
bite. Science 16l:56.
Contacos, P G. and W. E. Collins. 1969. Plasmodium maIariae: transmission from monkey to man by mosquito
bite. Science 165:918-919.
Contacos, P. G., G. R. Coatney, T. C. Orihel, W. E. Collins,
W. Chin and M. H. Jeter. 1970. Tiansmission of Plasmodium schwetzi from the chimpanzee to man by mosquito bite. Am. J. Trop. Med. Hyg. 19:190-195.
Do Rosario, V. E'., J. A. Vaughn and R. E. Coleman. 1989.
Analysis of the sporogonic development of Plasmodium
and, Plasmodium berghei in anopheline
falciparum
mosquitoes. Parasitologia 31:l0l-l I l.
Gozar. M. M.. V. L. Price and D. C. Kaslow. 1998. Sacchnromyces cerevisiae-secreted fusion proteins Pfs25
and Pfs28 elicit potent Plasmodium falciparum transmission-blocking antibodies in mice. Infect. Immun.66:
59-64.
Graves, P M., R. Carter, T. R. Burkot, I. A. Quakyi and
N. Kumar. 1988. Antibodies to Plasmodiumfalciparum
gamete surface antigens in Papua New Guinea sera.
Parasite Immunol. lO:2O9--218.
Hardman, N. E 1947. Studies on imported malarias. 3.
Laboratory rearing of western anophelines. J. Natl. Malar. Soc. 6:165-172.
Held, J. R. and P G. Contacos. 1967. Studies on the exoerythrocytic stages of simian malaria.ll.
Plasmodium
coatneyi. J. Parasitol. 53:910-918.
Held, J. R., P G. Contacos, J. R. Jumper and C. S. Smith.
1968. Studies on the exoerythrocytic stages of simian
malaria. Ill. Plasmodium inui. J. Parasitol. 54:249--254.
Hollingdale, M. R., W. E. Collins and C. C. Campbell.
I 986. In vitro culture of exoerythrocytic parasites of the
North Korean strain of Plasmodium vivax in hepatoma
cells. Am. J. Trop. Med. Hyg. 35:275-276.
Hollingdale, M. R., W. E. Collins, C. C. Campbell and A.
L. Schwartz. 1985. In vitro culture of two populations
(mitotically active and non-active) of exoerythrocytic
parasites of Plasmodium vivax. Am. J. Trop. Med. Hyg.
34:216-223.
Jeffery, G. M., W' E. Collins and J. C. Skinner. 1963.
Antimalarial drug trials on a multiresistant strain of
Plasmodium falciparum. Am. J. Trop. Med. Hyg. 12:
844-850.
Kaslow, D. C. 1993. Transmission-blocking
immunity
against malaria and other vector-borne diseases. Curr.
Opin. Immunol. 5:557-565.
Kaslow, D. C. and J. Shiloach. 1994. Production, purification and immunogenicity of a malaria transmissionblocking vaccine candidate: TBV25H
expressed in
yeast and purified using nickel-NTA agarose. Biotech-
nology12:494-499.
Kaslow, D. C., I. C. Bathurst, T. Lensen, T Ponnudurai,
P J. Barr and D. B. Keister. 1994. Saccharomyces cerevisiae recombinant Pfs25 adsorbed to alum elicits antibodies that block transmission of Plasmodium falciparum. lnfect. Immun. 62:557 6-558O.
Kaslow, D. C., I. C. Bathurst, D. B. Keister, G. H. Camp-
r26
JounNlr- or rHt AvsnrceN Moseurro CoNrnol AssocranoN
bell, S. Adams, C. L. Morris, J. S. Sullivan, p J. Ban
and W. E. Collins. 1993. Safety, immunogenicity and
in vitro efficacy of a muramyl-tripeptide-based malaria
transmission-blocking vaccines in an Aotus nancymai
monkey model. Vaccine Res. 2:95-103.
Keister, D. B. and D. C. Kaslow. 1994. Cryopreservation
of Plasmodium falciparum gametocytes. Exp. Parasitol.
78:I l8-1 19.
Kocken, C. H., R. L. Milek, T H. Lensen, D. C. Kaslow,
J. G. Shoemmakers and R. N. Konings. 1995. Minimal
variation in the transmission-blocking vaccine candidate Pfs48/45 of the human malaria parasite Plasmodiumfalciparum. Mol. Biochem. Parasitol. 69: I15-I18.
Krotoski, W. A., w' E. Collins and J. R. Jumper. 1973.
Detection of early exoerythrocytic schizonts of Plasmodium cynomolgi by immunofluorescence. Am. J.
Tiop. Med. Hyg. 22:443-451.
Krotoski, W. A., W. E. Collins, R. S. Bray, p C. C. Garnham, E B. Cogswell, R. W. Gwadz, R. Killick-Kendrick, R. Wolf, R. Sinden, L- C. Koontz and P. S. StanfiIl.
1982. Demonstration
of
hypnozoites
in
sporozoite-transmitted
P lasmodium vivax infection.
Am. J. Trop. Med. Hyg. 3l:1291-1293.
Mazier, D., W E. Collins, S. Mellock, P. M. Andrysiak,
N. Berbiguier, G. H. Campbell, E Miltgen, R. Bertolotti,
P. Langlois and M. Gentilini. 1987. Plasmodium ovale:
in vitro development of hepatic stages. Exp. Parasitol.
64:393-4OO.
Mazier, D., R. L. Beaudoin. S. Mellouk. P Druile. B. Texier, J. Tiosper, E Miltgen, I. Landau, C. Paul, O. Brandicourt, et. al. 1984. Obtention in vitro des stades hepatiques de Plasmodium falciparum. Ann. Parasitol.
Hum. Comp. 59:525-526.
Millet, P and W. E. Collins. 1990. Enhancement of in vitro
infectivity of simian malaria sporozoites to hepatocytes
by centrifugation. J. Parasitol. 7 5:232-234.
Millet, P, W. E. Collins, T. L. Fisk and P. Nguyen-Dinh.
1988a. In vitro cultivation of exoerythrocytic stages of
the human malaria parasite Plasmodium malariae. Am.
J. Tiop. Med. Hyg. 38:470-473.
Millet, P., W. E. Collins, L. Herman and P Nguyen-Dinh.
1989. Plasmodium vivax: in vitro development of exoerythrocytic stages in Saimiri hepatocytes and inhibition by an anti-P. cynomologi monoclonal antibody.
Exp. Parasitol. 69:91-93.
Millet, P., C. T Atkinson, M. Aikawa, M. R. Hollingdale
and W. E. Collins. 1991a. Strain specificity and ultrastructural study of the in vitro development of the liver
stage of Plasmodium falciparum in New World monkeys. Am. J. Tiop. Med. Hyg. 45:126-242.
Millet, P, W E. Collins, M. Aikawa, A. Cochrane and P.
Nguyen-Dinh. 1990a. Use of non-human primate hepatocytes for in vitro study of the pre-erythrocytic stages of malaria parasites. Bull. WHO 68(Suppl.):80-85.
Millet, P., T. L. Fisk, W. E. Collins, J. R. Broderson and
P. Nguyen-Dinh. 1988b. In vitro cultivation of the simian malaria parasites Plasmodium cynomolgi, P. knowlesi, P. coatneyi, and P. rnui in rhesus monkey hepatocytes. Am. J. Tiop. Med. Hyg. 39:533-538.
Millet, P., K. K. Kamboj, A. H. Cochrane, W. E. Collins,
J. R. Broderson, B. G. Brown and P Nguyen-Dinh.
l99ob. In vitro exoerythrocytic development of Plasmodium cynomolgi bastianellii: inhibitory activity of
monoclonal antibodies against sporozoites of different
P. cynomolgi strains and P. knowlesi. Parasite Immunol.
ll:223-230.
Millet, P., C. Nelson, G. G. Galland, J. S. Sullivan, C. L.
Vor-. 15, No. 2
Morris, B. B. Richardson and W E. Collins. 1994. Plasmodium ovale: observations on the parasite development in Saimiri monkey hepatocytes in vivo and in vitro, in contrast with its ability to induce parasitemia.
Exp. Parasitol.'7 8:394-399.
Millet, P, W. E. Collins, C. T. Atkinson, G. H. Campbell,
J. R. Broderson, B. G. Brown, V. Filipski, M. Aikawa
and P. Nguyen-Dinh. l99lb. Plasmodium cynomolgi:
immunization of a rhesus monkey with exoerythrocytic
stages cultured in autologous hepatocytes. Exp. Parasitol.72:91-98.
Moore, J. A., M. D. Young, N. E Hardman and T H.
Stubbs. 1945. Studies on imported malarias. 2. Ability
of California anopheline mosquitoes to transmit malarias of foreign origin and other considerations. J. Natl.
Malar. Soc. 4:3O7-329.
Morris, C. L., J. S. Sullivan, H. M. McClure, E. Strobert,
B. B. Richardson, G. G. Galland, I. E Goldman and W.
E. Collins. 1996. The Nigerian UCDC strain of Plasmodium ovale in chimpanzees. J. Parasitol. 82:444448.
Nagasawa, H., M. Aikawa, P M. Procell, G. H. Campbell,
W. E. Collins and C. C. Campbell. 1988. Plasmodtum
malariae: distribution of circumsporozoite protein in
midgut oocysts and salivary gland sporozoites. Exp.
Parasitol. 66:27-34.
Nagasawa, H., P M. Procell, C. T. Atkinson, G. H. Campbell, W. E. Collins and M. Aikawa. 1987. Localization
of circumsporozoite protein of Plasmodium ovale in
midgut oocysts. Infect. Immun. 55:2928-2932.
Nayar, J. K., R. H. Baker, J. W. Knight, J. S. Sullivan, C.
L. Morris, B. B. Richardson, G. G. Galland and W. E.
Collins. 1997. Studies on a primaquine-tolerant strain
of Plasmodium vivax from Brazil in Aotus and Saimiri
monkeys. J. Parasitol. 83:739-7 45.
Nguyen-Dinh, P, C. C. Campbell and W. E. Collins. 1980.
Cultivation in vitro of the quartan malaria parasite Pla.smodium inzi. Science 209:1249-125 l.
Noden, B. H., C. B. Pumpuni, J. A. Vaughn and J. C.
Beier. 1995. Noninfectious sporozoites in the salivary
glands of a minimally susceptible anopheline mosquito.
J. Parasitol. 8l:912-915.
Omar, M. S. and W. E. Collins. 1973. The antimalarial
activity of RCl2 against gametocytes and sporogony of
Plasmodium cynomolgi. Trans. R. Soc. Trop. Med. Hyg.
67:423-424.
Omar. M. S.. W. E. Collins and P G. Contacos. 1973.
Garnetocytocidal and sporontocidal effects of antimalarial drugs on malaria parasites. I. Effect of single and
multiple doses of primaquine on Plasmodium cynomolgi. Exp. Parasitol. 34:229-241.
Omar. M. S.. W. E. Collins and P G. Contacos. 1974.
Gametocytocidal and sporontocidal effects of antimalarial drugs on malaria parasites II. Action of the folic
reductase inhibitors, chlorguanide and pyrimethamine,
against Plasmodium cynomolgl. Exp. Parasitol. 36:167177.
Ponnudurai, T., J. H. Muwissen, A. D. I-eeuwenberg, J. P
Verhave and A. H. Lensen. 1982. The production of
mature gametocytes of Plasmodium falciparum in continuous culture of different isolates infective to mosquitoes. Trans. R. Soc. Trop. Med. Hyg. 76:242-25O.
Porter, C. H. and E H. Collins. 1990. Susceptibility of
Anopheles hertnsi to Plasmodium vivax. Am. J. Trop.
Med. Hyg. 42:414-416.
Porte! C. H. and E H. Collins. 1991. Species-diagnostic
differences in a ribosomal DNA internal transcribed
JuNe 1999
Hrsrozucer
REVIEw or Auopnotzs
spacer from the sibling species Anopheles freeborni and
Anopheles hermsi (Diptera: Culicidae). Am. J. Trop.
Med. Hyg. 45:271-279.
Renia, L., E Miltgen, Y. Charoenvit, T. Ponnundurai, J. P
Verhave, W. E. Collins and D. Mazier. 1988. Malaria
parasite penetratiol-a
new approach by double staining. J. Immunol. Methods 112:201-205.
Rosenberg, R. 1985. Inability of Plasmodium knowlesi
sporozoites to invade Anopheles freeborni salivary
glands. Am. J. Trop. Med. Hyg. 34:687-691.
Shahabuddin, M., T. Toyoshima, M. Aikawa and D. C.
Kaslow. 1993. Transmission-blocking activity of a chitenase inhibitor and activation of malarial parasite chitenase by mosquito protease. Proc. Natl. Acad. Sci.
USA 9O:4266-4270.
Singal, M., P K. Shaw, R. C. Lindsay and R. R. Roberto.
1977. An outbreak of introduced malaria in California
possibly involving secondary transmission. Am. J.
Trop. Med. Hyg.26:.l-9.
Sodeman, T, M., P G. Contacos, C. S. Smith, J. R. Jumper
and W. E. Collins. 1969a. The exo-erythrocytic stages
of Plasmodium falciparum in Aotus trivirgatus. J. Parasitol. 55:682-683.
Sodeman, T, M., J. R. Held, P G. Contacos, J. R. Jumper
and C. S. Smith. 1969b. Studies on the exoeryhrocytic
stages of simian malaria.lY. Plasmodium brasilianum.
J. Parasitol. 55:963-970
Sullivan, J. S., C. L. Morris, H. M. McClure, E. Strobert,
B. B. Richardson, G. G. Galland. I. F Goldman and W.
E. Collins. 7996. Plasmodium vivax infections in chimpanzees for sporozoite vaccine challenge studies in
monkeys. Am. J. Trop. Med. Hyg. 55:344-349.
Techlehaimanot, A., W. E. Collins, P Nguyen-Dinh, C. C.
Campbell and V. Bhasin. 1987. Characterization of
Plasmodiumfalciparum
cloned lines with respect to gametocyte production in vitro, infectivity to Anopheles
mosquitoes, and transmission to Aotus monkeys. Tians.
R. Soc. Tiop. Med. Hyg. 81:885-887.
Vaughn, J. A., L. Hensley and J. C. Beier. 1994a. Sporogonic development
of Plasmodium yoelii in five
anopheline species. J. Parasitol. 80:674-681.
Vaughn, J. A., D. Narum and A. E Azad. 1991. ptasmodium berghei ookinete densities in three anopheline
species. J. Parasitol. 77 :7 58-7 61.
rnnnaonNt
127
Vaughn, J. A., B. H. Noden and J. C. Beier. 1994b. Sporogonic development of cultured Plasmodium falciparum in six species of laoratory-reared Anopheles mosquitoes. Am. J. Tiop. Med. Hyg. 5l:233--243.
Vaidya, A. B., O. Muratova, E Guinet, D. Kister, T. E.
Wellems and D. C. Kaslow. 1995. A genetic locus on
Plasmodiumfalciparum
chromosome 12 linked to a defect in mosquito-infectivity
and male gametogenesis.
Mol. Biochem. Parasitol. 69:65J1.
Warren, McW. and W. E. Collins. 1981. Vector-parasite
interactions and the epidemiology
of malaria. Parasitological topics, a presentation volume to P C. C. Garnham, ER.S. on the occasion of his 80th birthday. Soc.
Protozool. Spec. Publ. l:266-274.
Williamson, K. C., D. B. Keister, O. Muratova and D. C.
Kaslow. 1995. Recombinant Pfs230, a Plasmodiumfalciparum gametocyte protein, induces antisera that reduce the infectivity of Plasmodiumfalciparum
to mosquitoes. Mol. Biochem. Parasitol.'15:33-42.
Wirtz, R. A., T, R. Burkot, R. G. Andre, R. Rosenberg,
W. E. Collins and D. R. Roberts. 1985. Identification
of Plasmodium vivax sporozoites in mosquitoes using
an enzyme-linked immunosorbent assay. Am. J. Trop.
Med. Hyg. 34:1O48-1O54.
Young, M. D. and R. W. Burgess. 1947. T\e transmission
of Plasmodium malariae by Anopheles maculipennis
freeborni. Am. J. Tiop. Med..27:39-4O.
Young, M. D. and R. W. Burgess. 1948. Studies on imported malarias 9. The comparative susceptibility of
Anophe le s q uadrimaculatus and Anophele s maculipe nnis freebomi
to foreign vivax malaria. J. Natl. Malar.
Soc. 7:134-137.
Young, M. D. and R. W. Burgess. 1961. The infectivity
to mosquitoes of Plasmodium malariae. Am. J. Hyg.
73:182-192.
Young, M. D., D. E. Eyles and R. W. Burgess. 1948. Studies on imported malarias. 10. An evatuation of the foreign malarias introduced into the United States by returning troops. J. Natl. Malar. Soc. 7:17l-185.
Young, M. D., T H. Stubbs, J. A. Moore, C, Ehrman, N.
F Hardman, J. M. Ellis and R. W. Burgess. 1945. Studies on imported malarias: l. Ability of domestic mosquitoes to transmit vivax malaia of foreign origin. J.
Nat1. Malar. Soc. 4:127-131.