Mohammad Arif, Munir (1994)

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Mohammad Arif, Munir; (1994) Systematics and biology of Phlebotomine sandflies of the Visceral
Leishmaniasis foci of Northern Pakistan. PhD thesis, London School of Hygiene & Tropical Medicine.
DOI: https://doi.org/10.17037/PUBS.00768489
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SYSTEMATICS
AND BIOLOGY OF PHLEBOTOMINE S., N, OF
-N-DFLIY-S
THE VISCERAL LEISHALANILASIS
FOCI OFNNORTHIERN PA. ýTAN.
Mohammad
Arif, Ntunir
MSc. (Punjab), MSc. (London)
Dissertation
to the
submitted
Faculty Science
of
LTNIWRSITY OF LONDON
in fulfilment
the
of requirements
for degree
the
of
DOCTOR OF PBEILOSOPHY
1994
Department Medical Parasitology
of
London School Hygiene Tropical Nledicine
of and
Keppel Street
LONDON NVC 1E 7HT
BIBL
LQNDON
us,
v
Dedicated to Sakieba Arif, My daughters Amna Arif Ayesha
my wife and
Arif Parents for
their
and my great patience and constant
throughout this
encouragement study.
ABSTRACT
leishmaniasis
The (s)
aim of this study was to incriminate the vector of visceral
Northern Pakistan. Two disease foci Azad Jammu &
in contrasting were studied-
Kashmir (AJK)
Northern Areas (NA)
and through monthly sampling.
Studies
defined
on the systematics morphologically variable species of the
Phlebolomus (Larrousslus) P. (Adlerius). Morphological
subgenera characters
and
belonging The
the
of all species to these subgenera were intensively studied. species
belonging Phlebotoinus (Larroussius) P.
to the
subgenus were identified as major,
Rkeshishiam, Rkandclakii burneyi P. belonging
those to
subgenus
and spA. and
Adlernis Rhinduslanicus P. Species belonging
as and salangensis. to other subgenera.
P (Phlebolonius) P (Pat-aphlebionius) P (Pat-alAleboloin
I)aI)a1asi, sergcntl and its)
alexandri were easily identified.
The longitudinal Bagh district (Rehra
entomological studies were carried out in
AJK Chilas district (Hudur 1200m Thor 1700m)
village) in and village, and village,
Northern Areas between April 1991 November 1991
the
in and and in same months
1992. Sampling done CDC-light
traps, traps
in was using sticky-paper and mouth
In higher
aspirators. addition, a general survey was also undertaken at altitudes in
Northern Areas AJK.
and
A 9656 Phlebotonnis (8797 during
total the
of sandflies were collected
longitudinal 859 during Nine Phlebolonlus
the
studies and general survey). species of
found, Phlebotonins (A) for first P.
the time
were salangensis and a new species
(Lai-i-ousslus) A. The differed
sl). species composition and relative abundance of species
between In Northern Areas P. (35.75' ) followed
the two A
within and areas. paj)atasl
by P. (19%) dominant lower Hudur but
the
sei-genn were at altitude of village
P. keshislnani (29.66%) higher Thor
the
was most abundant at altitude of village,
AJK, Rhinduslanicus (64.62%)
whereas in was predominant.
Species differed In Northern Areas P.
their
in seasonal abundance. papatasi and
P, June July P. keshishiam August. In AJK
scrgentl showed peak activity in and and in
Rhmdusiamcus June The
showed a clear peak in preceding the monsoon. activity was
found be Northern Areas
to positively correlated with temperature in and negatively
AJ-K-
correlated with rainfall in
iii
The dominant P. lower
anthropophilic species included papalasi at altitudes
(Hudur
Rkeshishianj higher (Thor Northern Areas
village), at altitudes village) in and
Rhindustanicus AJK. Most biting between -1200-2400
in occurred around midnight 1--
hours between 0400-0600 hours Northern Areas. None the
with a second peak in of
found biting human AJK. Blood-meal
sandflies were analysis revealed
volunteers in
dominant P. hinduslanicils
that the Rpaj)atasi, P. Rkeshishiani
species sergenti, and
have dog
hosts human, bovines dogs. Monthly
a range of mainly and sampling V"ith
baited traps also showed Rkeshishiani and P. hindustanictis as the dominant species
host (dog).
to the
attracted potential reservoir
Females Rkeshishiani (754), P. (36), P. (15)
of salangensis alcxandtl and
Rhindustanicus (301) dissected for Lelshmania
were natural infections with
blots by Lcishmania DNA
promastigotes and squash probed infantilln specific probe
(LUCA D2 200 BP). Only Rhindustanicus found be
was to naturally infected with
Leishinania (parasites identified by DNA hybridization) in AJK. This
infantuni, species
VL AJK
the the transmission
is principal vector involved in of in
.
From
that the transmission
ecological studies it is concluded of visceral
leishmaniasis higher Northern Areas P. keshishlam
takes that
place at altitudes in and
the
is vector.
IV
ACKNOWLEDGEMENTS
In Almighty Allah, beneficent
the the the
name of most and merciful. who
bestowed
the to
me strength and courage achieve my goal.
First foremost I like deep
to
and would extend my very appreciation, gratitude
Dr Richard P. Lane
and sincere thanks to who as my supervisor was alwaý, s there to
I him. His
assist me whenever needed approachability, sound professional guidance,
inspiring
the this
and ever encouragement played a vital role in accomplishment of
study.
I like Dr Janet Hemingway, for
to thanks to
would express my assistance in
Thanks due Drs Chris Dye Clive
the to
performing enzyme assays. are also and
Davies for Dr Brian Southgate for help
their the
constructive criticism and in making
links for M. Sc led P. hD.
to this
initial which on
I Dr Paul D. Ready, British Museum (Natural History)
to the
am grateful of
for his DNA from Pakistan. My
support and guidance with probes of sandfly material
Thanks due Entomology department, for
to the their
are also my colleagues in all
during Museum, Dr Rod
the to
cooperation and assistance my stay in especially
Dillon, Miss Theresa Howard, Mrs Carolyn Lowry, Miss Zoe Adams, Dr Megda
Charalambous, Dr Martin Hall, Dr Brian Pitkin, Dr Tony Shelley.
and
I like Professor R Kill
to thanks to
would express my special ick-Kendrick and
Mrs R. Kill for hospitality, during field
their training the
i ck-Kendri ck, especially in
France, for for for
the
south of providing me sandfly material enzyme assays, and
dissections. My due
thanks to
professional assistance on spermathecal special are also
Professor N. Leger for her for hospitality
taxonomy the
guidance on sandfly and she
has during Paris.
extended my stay in
Among friends London I Dr Adrian All Seyed, Dr Atta-
to
my in am grateful
Ul-Haq, Mr Kandan Illango, Professor Llanos Cuentas Mr Khalld Mahmood for
and
kindness help friends Lilian Penson Hall
their to
and encouragements and all my at
RaJko Reljic Subash Bhat for
their
especially and company and encouragement.
At home Pakistan, I like
in would to express my profound thanks and gratitude
Major General (Retd. ) NU. Burney
to
who always supported and encouraged me when
I him. I like full
to
ever needed would acknowledge the support in this project of the
former Executive Director the National Institute Health, Islamabad, late Dr
of the
of
V
Abdul Ghafoor
(May Allah his
Ameen) I
rest soul in eternal peace, wish to extend
deep
my thanks to the Chairman and the Executive Director of the Pakistan INIedical
Research Council for help. Special
their due
administrative support and thanks are also
to Dr Ather Saeed Dil, Chief Public Health Division, NIH Dr Javed Hamid,
and
Pakistan Medical Research Council for
consultant, their
assistance.
At NIH, I
Mr Sher
to
am most grateful all my colleagues especially
Mohammad Solangi, for his help during field Dr Mohammad Abdur
my work, and
Rab for field for his friendly
the
sharing with me experience and guidance and support
during
I Dr
the to thanks to
entire period of my study. also wish extend my special
BirJees Mazhar Kazi, Mr Mubashar Ahmed Khan, Dr Jamshiad Iqbal, Dr Hamayun
Asghar, Mr Sohad Zaidi, Dr Osman Yusuf, Dr Shahida Yusuf, Dr Arshad Mumtaz
and
Dr Shahid Abass for Thanks Laboratory
their to
encouragements and support. also my
Mr Mohammad Ramzan Mr Mohammad Yousaf for
their the
staff and assistance in
field drivers, Mr Mohammad Pervez Mr Mohammad TaJ for
to
work and our and
driving difificult Northern Areas AR for
throug the
efificlently us roads of and
hours.
endless
I like Col Zulfiqar, Major Shauket
to thanks to
would extend my special and
field Ambulance Bagh, AJK for hospitality
the the their
all officers and staff of in and
help during field I health both
to the
work. am also grateful provincial authorities of
AJK Northern Areas for during field
and their coordination and support the work.
Special due District Health Officers Chilas Bagh for
thanks are also to of and their
help field Thanks
to the
special assistance in providing man power carry out work.
health Mr Bughdar Khan, Mr Mohammad Sharif, Mr
to the
also provincial workers
Zia-ul-Haq Mr Bashir for field
and mohammad assisting me in the work and to the
AJK Northern Areas for
their
people of and cooperation.
In U. K. I Mr C. G. Farooq
to
am extremely grateful my cousin and my uncle
Mr Abdul Hamid Cokar families for kindness
their their
and and generosity and the
hospitality have family during
they extended to me and my our stay with them in
london.
The kind has long from home
this
study of which meant periods away can only
be by family. Therefore I like
accomplished the support of one's would to extend my
Sakieba, daughters
thanks to
very special my parents, my wife my -\mna -Arif and
. .
vi
Ayesha Arif, brother Mohammad Asif Munir, Aunty Mrs
my my sisters and my
Munawar Haleem for during
their tolerance, patience and constant support the entire
I
phase of this study. am also grateful to all my relations especially my uncle Mr
Abdul Azim Khan, help
target.
who's inspirations were a great in achieving my
My due friends Mr Abdus Sattar Khan, Mr Nlohammad
thanks to
are also my
Yusuf Khan, Mr Seyed Ghufran, Mr All Akbar Shah for
their
and support and
encouragements.
I late father law Mr Abdul
to to
also wish extend my acknowledgements my in
Haleem Cockar, highest level
to the
who always inspired me attain of education and
to the late Mr Mohammad Mr Ahmed Shaft
my uncles shaft and who always
family. May Allah
encouraged and supported education in the rest their souls in
Ameen.
eternal peace,
Last but least I like
to thanks to
not would extend my very special
UNDP/World BankMHO Special Programme for Research Training Tropical
and in
Disease for financial
the this
assistance in carrying out project.
Vil
TABLE OF CONTENTS
TITLE PAGE
..........................
..................... ...........
DEDICATIONS
...........................................................
ABSTRACT
............................................................
ACKNOWLEDGEMENTS
.............. ....... ..............................
TABLE OF CONTENTS
vIIi
....................................................
LIST OF TABLES
X1
................................ ........................
LIST OF FIGURES
xill
.......................................................
CHAPTER 1. INTRODUCTION
1.1. Leishmaniases I
..........................................................
I. I. I. Disease 2
incidence
.....................................................
1.1.2. Geographical distribution 11
.................................................
1.1,3. Reservoirs 4
...........................................................
1.1.4. Vectors 4
.............................................................
1.1.4.1. Vector Incrimination 5
...................................................
1.1.5. Life Leishmania hosts 6
the
cycle of in sandfly and vertebrate
.........................
1.2. Systematics biology 10
and of phlebotomine sandflies
...............................
1.2. L Brief histoi), 10
of sandfly systematics
.........................................
1.2.2. Biology 12
of phlebolominc sandflies
.........................................
1.2.2.1 Sonic key biolog-. 13
aspects of sandfly N .......................................
1.2.2.2. Essential biology disease
to
aspects of sandfly in relation
17
epjdcmlologý .............................................................
1.3. Methods 2 ',
of sandfly control
...............................................
1.3.1. Insecticides. 23
.... ý............ I.. I................................ 1
1.3.2. Ecological 25
control
.....................................................
1.3.3. Personal 26
protection
...................................
1.3.4. Biological Genetic 27
and control
.......................................
1.4. Leishmaniasis in Islamic Republic Pakistan
the
of and
27
neighbouring countries
.....................................................
1.4.1. Leishmaniasis in the Islamic Republic Pakistan 27
of
..............................
1.4.1.1. Visceral lcishnianiasis 28
.................................................
1.4.1.2. Cutaneous leishiiianiasis ', 2
..............................................
1.4.1.3. Sandflics Pakistan 33
studies in
............................................
1.4.2. Visceral leishmamasis in Pakistan 34
countries around
............................
1.4.2.1. China .
14
...........................................................
1.4.2.2. Islamic Republic Iran 39
of
...............................................
1.4.2.3. Jammu Kashmir (India) 42
...............................................
1.4 2.4. Afghanistan 43
........................................................
CHAPTER 2. OBJECTIVES 45
...........................................
CHAPTER 3. DESCRIPTION OF STUDY AREAS 46
................................
General description 4o
1.1.
. ....................................................
3.1. I. Northern Areas 46
of pakistan
. .............................................
\1 III
3.1.2. Azad Jammu & Kashmir
50
. ...............................................
3.2. Wild life
of northern pakistan
............................
..............
3,3. Local languages & kashmir
in northern areas and az-ad Jammu
......................
3.4.13escription for longitudinal
of villages selected entomological
Azad Jammu & Kashmir 54
studies in northern areas and
................................
3 4.1. Northern Areas
54
......................................................
3.4.1.1. Chilas district
54
. ......................................................
3.4.2. Azad Jammu & Kashmir
. ............................................ I. -58
3.4.2.1 Bagh District.
................................... ................
3.5. Descnption for
62
of vafious sites selected general surveý .............
................
CHAPTER 4. MATERIALS AND METHODS 69
....................................
4.1. Study 69
area
...........................................................
4.2. Sampling 69
regime of phlebotomine sandflies
.................... ................
4.2.1. General 70
suReý .......................................................
4.2.2. Longitudinal 70
entomological studies
.........................................
4.3. Sampling 71
methods
.....................................................
4.3.1. CDC light-traps 71
................................................... I.
4.3.2. Sticky 72
traps
paper
.................... I..............................
4.3.3. Human biting 7 ',
catches
..................................................
4.3,4, Dog-bait 74
catches.
,,................................................
4.4. Meteorological 74
records
...................................................
4.5. Dc-olling 75
and mounting methods
...........................................
4.6. Sandf1v 76
identification
...................................................
4.7. Dissection 76
of phlebotomine sandflies
.............................. I.........
4.9. Isolation Leishmania from 77
of sandflics
.......................................
4.9. Squash-prcparations Hybond
to the
of sandflN guts on nylon
for DNA h0ndization 78
membrane
............................................
4.9.1. DNA Hvbndization 78
....................................................
4.10. Blood 81
mcal analysis
...................................................
CHAPTER 5. SYSTEMATICS OF PHLEBOTOMINE SANDFLIES FROM VISCERAL
LEISHMANIASIS FOCI OF AZAD JAMMU & KASHMIR AND NORTHERN PAKISTAN 83
....
5.1. Introduction 83
..........................................................
5.2 The fauna from 84
of phlebotornine sandflics neighbouring countnes
.....................
5.3 Matenals 90
and methods
...................................................
5.3.1. Laboratory for 91
methods morphometi-ic measurements
.............................
5.3.2. Morphometeric Characters 91
studied
..........................................
5.4 Results discussions 94
and
...................................................
S. 4.1. General 94
surveý ........................................................
5.4.2. Systematics 96
.......... I..............................................
CHAPTER 6. BIOLOGY OF PHLLEBOTOMINE SANDFLIES IN RELATION TO VISCERAL
LEISHMANIASIS TRANSMISSION IN NORTHERN PAKISTAN 1,50
....... ..............
15()
6.1. INTRODUCTION
. ...................................................
6.2. MATERIALS AND METHODS 151
. ..........................................
152
6',. RESULTS
..........................................................
6-3.1. Spccics
composition.
... ý.............................................
152
6.3.1.1 Northem Areas
....................................................
1ý7
',. 1.2. Azad Jammu & Kashmir
o.
. ............................................
ix