Animal Pharm Ecology of Malaria Vectors

  • ID: 4533550
  • Report
  • Region: Global
  • 241 pages
  • Animal Pharm
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The eradication of malaria is a global issue requiring professionals to fully understand the ecology of the disease vectors. The authors of this unique report have 40 years' experience across 5 continents and have produced a comprehensive overview of the biology, behaviour, and impact of mosquitoes.

The 19 chapters extent from an introduction to insects and mosquito systematics through to the development of novel control techniques and incorporate case histories of the vectors and their relationship to malaria in a variety of settings.

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Executive Summary


Chapter 1: Classification and Systematics
1.1 Insects are also nutritious
1.2 Diptera
1.3 Taxonomy
1.4 What is a species?
1.5 Mosquitoes (Culicidae)
1.6 Anopheles, Culex and Aedes
1.7 The ecological niche
1.8 Species complexes
1.9 The Anopheles gambiae complex. How many angels can dance on the head of a pin?

Chapter 2: Mosquito Life Histories
2.1 Eggs and larvae
2.2 Emergence and mating

Chapter 3: The Search for the Host
3.1 Biting cycles
3.2 Age and biting time
3.3 Blood feeding

Chapter 4: Dispersal
4.1 Some World records
4.2 Dispersal of males
4.3 Indoor/Outdoor mixing

Chapter 5: Population Dynamics

Chapter 6: Dry Season Ecology

Chapter 7: Mapping

Chapter 8: Vectorial Capacity

Chapter 9: Oviposition (gonotrophic) Cycle Duration

Chapter 10: Mosquito Survival Determined by Dissection

Chapter 11: Sporozoite Determination

Chapter 12: Vector Control
12.1 Insecticides
12.2 Insecticide Resistance
12.3 Alternative Methods of Control

Chapter 13: Surveillance and Sampling

Chapter 14: Sampling
14.1 Indoor resting (House) catches
14.2 Outside resting catches
14.3 Night catches
14.4 Sporozoite rate determination
14.5 Blood meal ELISA
14.6 Susceptibility tests
14.7 Larval surveys
14.8 Bioassay tests

Chapter 15: Epidemics
15.1 Classification of Epidemic types
15.2 How to measure Epidemic Thresholds
15.3 Indicators

Chapter 16: Malaria and Dengue
16.1 Malaria
16.2 Filariasis
16.3 Dengue and its vectors
16.4 Collection methods
16.5 Woolbachia for the control of Aedes aegypti
16.6 Release of Insects carrying Dominant Lethals (RIDL)

Chapter 17: Sampling Techniques
17.1 The Furvela tent-trap
17.2 The Suna Trap
17.3 Some comments on light-traps
17.4 Exit collections from houses
17.5 Resting collections
17.6 Experimental huts
17.7 Mosquito mounting and preservation
17.8 Collection of immature stages
17.9 Laboratory studies
17.10 Near Infra-Red - a Silver Bullet?
17.11 Enzyme Linked Immunosorbent Assay (ELISA) for circumsporozoite detection
17.12 gSG6 ELISA
17.13 The Polymerase Chain Reaction

Chapter 18: Some Case Histories
18.1 Furvela
18.2 Linga Linga
18.3 São Tomé and Príncipe

Chapter 19: Glossary

Chapter 20: References
List of Figures
Figure 1: ‘Senene’ are a delicacy in the Kagera region of Tanzania. Fried they remain good to eat (and they are delicious) for a year - until the next short season of abundance
Figure 2: Hierarchical classification (from species to general) of A. Anopheles freeborni, B. Anopheles minimus C. Anopheles albimanus A. Anopheles freeborni, Freeborni Subgroup, Maculipennis Group, Anopheles Series, Angusticom Section, Subgenus Anopheles; B. Anopheles minimus, Minimus Complex, Minimus Subgroup, Funestus Group, Myzomyia Series, Subgenus Cellia; C. Anopheles albimanus, Albimanus Series, Albimanus Section, Subgenus Nyssorhynchus (from Harbach, 2013)
Figure 3: The evolutionary and systematic relationships between the different arthropod groups that are pests of man and animals (from Black & Kondratieff, 2005)
Figure 4: The main morphological features of an adult female Anopheles mosquito. Note the banding on the palps and the dark and light areas on the wing - these are often important for taxonomic purposes
Figure 5: Classification of the Culicidae based on evolutionary relationships. Yellow highlights indicate species confined to the New World and Green to those restricted to the Australasian region
Figure 6: Distinguishing features of the different mosquito genera (after Marshall, 1938)
Figure 7: Morphological differences in the wings of the A. nili complex A: A. nili and A. somalicus B: A. carnevale C: A. ovengenisis (from Antonio-Nkondjio & Simard, 2013)
Figure 8: Larva of Anopheles showing the main characteristics used in identification
Figure 9: Anal papillae of a) the freshwater species Aedes aegypti and b) the saltwater species Aedes taeniorhynchus showing the differences in size of the anal papillae (APP) (from Darsie & Ward, 1981)
Figure 10: The shape of a typical Culex (A) and Anopheles (B) scutellum (Stm) as seen with a scanning electron microscope (from Harbach, 2013)
Figure 11: Eggs of the Anopheles maculipennis complex. A) sacharovi, B) melanoon, C) atroparvus, D) subalpinus, E) labranchaie, F) messeae, G) maculipennis, H) beklemishevi. (from Becker et al., 2010)
Figure 12: Distribution of the main members of the A. gambiae complex (the distribution of A. gambiae and A. coluzzii are considered together in this figure (from Lanzanro & Lee, 2013)
Figure 13: Ovarian polytene chromosomes of A. gambiae showing the light and dark bands used to distinguish chromosomal forms (from Lanzaro & Lee, 2013)
Figure 14: Distribution of the chromosomal forms of A. gambiae in West Africa and habitat ecotype (from Lanzaro &Lee 2013, after Coluzzi et al., 1974)
Figure 15: Distribution of A. coluzzii (M form) and A. gambiae (S form) in Africa (from Lanzaro & Lee, 2013)
Figure 16: Relative distribution of A. coluzzi and A. gambiae in Ghana according to A) elevation, B) mean daily rainfall and c) mean daily temperature (from de Souza et al., 2010)
Figure 17: A schema showing the effect of increasing temperatures on developmental velocity (in red) and mean generation time (in blue) with air temperature
Figure 18: Wing length (a proxy for adult size and mass) of A. funestus and mean temperature from Furvela village in southern Mozambique (from Charlwood & Bragança. 2012)
Figure 19: Numbers of A. gambiae collected in light-traps Furvela village, Mozambique, and temperature
Figure 20: Numbers of A. funestus and A. gambiae s.l. females caught in light traps relative to ambient temperature, Furvela, Mozambique (from Charlwood, 2017)
Figure 21: A) Wing lengths of A. funestus (from Mozambique) and B) A. coluzzii (from São Tomé). In both species males are smaller than females
Figure 22: Flight activity of virgin and mated female A. gambiae in the laboratory compared to biting activity in nature (from Jones, 1979)
Figure 23: The proportion of A. coluzzii (formerly M form A. gambiae) females from São Tomé that took a blood meal before mating according to their wing length (from Charlwood et al., 2003)
Figure 24:Proportion of female A. coluzzii with mating plugs (indicative of mating the previous night) by date of collection Okyereko Ghana. Black square windy night filled triangle following night (from Charlwood et al., 2011)
Figure 25: Swarm site of A. melas in the salt-flats close to the village of Keneba, The Gambia (from Charlwood & Jones, 1980)
Figure 26: Swarming sites used by A. funestus in Furvela Village Mozambique. The sites occur in sandy areas cleared around houses (from Charlwood et al., 2003)
Figure 27: Two vertical elevations of representative ‘swarming’ flight paths (each c. 2 seconds duration) by male A. gambiae over a 55x 11cm marker strip on the floor of a 1.2m cube cage. Bars represent the range in accuracy of measurement of the same flight traced ten times on a TV screen from an infra-red video recording. A. two flights seen in elevation parallel to axis of marker (drawn approximately in scale perspective view); B. two other flights seen with the marker moved through 90o relative to the cage and TV camera. In each case the shaded area represents the limits within which four males flew in 1 min. Three-pronged lines indicate approximate perspective position of cage corner (from Charlwood & Jones, 1979)
Figure 28: A swarm of A. pharoensis in Mozambique - note the erect antennae of the males
Figure 29: A) Female and B) male A. funestus. the plumose hairs on the antenna and clubbed end of the palps in the male
Figure 30: The base of a fibrillae on the male antenna showing the annulus which swells with a change in pH (from Nijhout & Sheffield, 1979)
Figure 31: Cyclical erection of the antennae of male A. gambiae continues when they are kept in constant dark (from Charlwood & Jones 1979)
Figure 32: Time of collection of mosquitoes leaving houses relative to sunset A Anopheles funestus B A. gambiae s.l. (from Charlwood, 2011)
Figure 33: The mating sequence in A. gambiae. a) males attach to the female using their complex claw on the front leg b) using the momentum of their initial attachment the male positions himself underneath the female c) within a second or two the terminalia (claspers) of the male attach to the female d) the male releases his hold on the females’ legs and the pair assume the end to end position. Note the erect antennal fibrillae of the males’ antennae (from Charlwood & Jones, 1979)
Figure 34: A) Response times of different members of the A. gambiae complex to female flight tones following light-off in the insectary. a) A. gambiae, b) A. arabiensis, c) A. melas and d) A. merus. B) Number of mating pairs of A. coluzzii leaving three swarms in São Tomé relative to the start of swarming C) Number of mating pairs of A. funestus leaving swarms relative to the start of swarming, Furvela, Mozambique. (from Charlwood & Jones, 1979 and Charlwood et al., 2003)
Figure 35: Time of the first pair of A. funestus seen in copula leaving a swarm relative to the total number of pairs subsequently seen during the whole swarming period. (from Charlwood et al., 2003)
Figure 36: A) Wing length of male A. funestus collected swarming (filled triangles) in copula (filled diamonds) and resting (open triangles) and B) A. coluzzii swarming (open squares), in copula (filled diamonds) and resting (open triangles). For both species mean sizes of each group were similar and approximated a normal distribution (from Charlwood et al., 2003, 2002)
Figure 37: Biting activity of Aedes albopictus from the Ou Chra woods, Mondolkiri, Cambodia. Bars indicate 95% confidence intervals. Blue control collections, red with a pyrethroid repellent in use. (from Charlwood et al., 2014)
Figure 38: Biting cycles of African Anopheles Vectors A- A. gambiae s.l.; B- A. funestus; C- A. nili; Non-vectors D- A. coustani; E- A. pharoensis; F- A. wellcomei; G- A. squamosus; H- A. flavicosta; I- A. brohieri (from Hamon 1964)
Figure 39: The biting cycles of A. coluzzii. a) overall cycles for the islands of São Tomé (filled square) and Príncipe (open square) and a composite figure from b) the cycles for virgin (open diamond), with mating plug (filled diamond) and mature (open circles) on the island of São Tomé and c) Principe (from Charlwood et al., 2003)
Figure 40: Biting of A. darlingi from three different areas of Brazil. The peak of activity observed in Aripuana in the early morning was largely due to young nulliparous insects (from Charlwood & Hayes,1978)
Figure 41: Age of A. darlingi females during the early part of the night from Aripuanã, Mato Grosso, Brasil. Note the preponderance of nulliparous females during the early evening peak of biting (from Charlwood & Wilkes 1979)
Figure 42: A) Biting activity of A. darlingi at Aripuanã on one night when rainstorms occurred at 18:05-18:10 and 18:35-18:47 h; B) Mean biting activity during the remainder of the week when no rain fell. The time of sunset has been adjusted to 18:00h (from Charlwood, 1980)
Figure 43: Numbers of A. farauti in landing collections (at different months) according to moon phase, Maraga, Madang, Papua New Guinea
Figure 44: The biting cycle of A. farauti collected in Maraga, Madang Province, Papua New Guinea, according to moon phase. The figure is the Williams’ mean of four collections A, B, D and six for C. The shaded portion of the figure represents the parous fractions and the graphs have been adjusted to a uniform height. A = no moon, B = Waxing moon, C = full moon, D = waning moon. (from Charlwood et al., 1986)
Figure 45: Proportion of the nights catch of Anopheles funestus from tent-trap collections according to phase of the moon, Furvela, Mozambique (from Kampango et al., 2011)
Figure 46: Biting activity of A. farauti from Madang Papua New Guinea. Note that Nulliparous insects had a similar biting cycle to parous insects but that among the latter the proportion of insects with ovariolar sacs changed with time of night (from Charlwood et al., 1988)
Figure 47: Numbers of A. gambiae s.l. collected in a tent-trap by period of the night Okyreko, Ghana
Figure 48: Proportion of the A. gambiae s.l. that were parous from tent-traps by time of the night, Okyreko, Ghana
Figure 49: Scanning electonmicrograph of a typical sensilla on the antenna of a female mosquito (from Klowden & Zwiebel. 2005)
Figure 50: Olfactory sensillum. Schematic longitudinal section through a sensillum of the single walled type. The pore region is enlarged to the left (from Cribb & Merritt, 2013)
Figure 51: Schematic figure of the odour plume coming from a village and the tracking behaviour of mosquitoes coming from a focal breeding site (in this case the drying river close to the hillside village of Adi Bosco in Eritrea). The yellow arrow denotes the wind direction. (after Gillies, 1989)
Figure 52: Representation of the odour plume coming from a house. Odours travel further than carbon dioxide (which when pulsed acts as an attractant). Once inside convection currents from the body will also provide cues for the mosquito. On coming to the wall of the house non-vectors turn aside but vectors go upwards
Figure 53: Average landing density (dm-2) of Aedes albopictus on body regions, Okyerko, Cambodia. The head was the most attacked part of the body (from Charlwood et al.,2014)
Figure 54: Mouthparts of a female mosquito (from Matheson, 1944)
Figure 55: Feeding of a Culex mosquito
Figure 56: ‘Spit’ and ‘Suck’ changes recorded during the feeding by individual females of Aedes aegypti on a mouse. Mosquito and mouse formed part of an electric circuit which was closed when the mosquito’s mouthparts penetrated the skin. Downward displacement of the trace indicates increases in current. Upward displacements indicate decreases in current. (after Kashin 1966)
Figure 57: The internal anatomy of a blood feeding insect. (after Jobling, courtesy of the Wellcome Museum)63 Figure 58: Epithelial cells lining the gut wall before and shortly after a blood meal (from Devenport & Jacobs- Lorena. 2005)
Figure 59: Effects of Anopheles saliva on hemostatic, inflammatory and immune reactions of the human to the bites of the vector (from Drame et al., 2013)
Figure 60: gSG6 levels and levels of parasitemia before and after Insecticide Treated Net distribution (from Drame et al., 2013)
Figure 61: gSG6 levels in control and intervention villages (using a spatial repellents) from Mondolkiri, Cambodia (from Charlwood et al., 2017)
Figure 62: Factors resulting in the inhibition of host-seeking behaviour in blood fed mosquitoes (from Klowden & Zwiebel, 2005)
Figure 63: Relative feeding success by mosquito density from Namawala, Tanzania. a A. gambiae s.l. b A. funestus (from Charlwood et al., 1995)
Figure 64: Map of recapture areas in Maraga Village. The circles represent the number of engorged females of Anopheles farauti analysed, the shaded portion being the proportion of buffalo fed mosquitoes in each area. The star denotes the position of the buffalo (from Charlwood et al., 1985)
Figure 65: Appearance of a female mosquito’s abdomen A unfed B recently engorged C semi-gravid D gravid. - ready to lay Semi-gravid insects are commonly seen during the cooler months of the year when gonotrophic development takes three instead of two days
Figure 66: Proprtion of A. funestus and A. gambiae semi-gravid and gravid in resting collection and temperature, Furvela, Mozambique (from Charlwood, 2017)
Figure 67: Numbers of A. arabiensis (thick line) and A. funestus (thin line) collected at different distances from the edge of the Kilombero Valley where breeding was taking place. Note the log scale. Thus, in the locations furthest from the Valley maximum numbers of A. arabiensis were <100 a night whilst closer to the Valley edge they were > 3,000 a night. Dispersal of Anopheles gambiae was nonrandom, but related primarily to the distribution and numbers of houses (from Charlwood et al., 1995)
Figure 68: Distribution of A. darlingi solid histogram) and other Anopheles (clear histogram) collected by human landing catch from the breeding site, Rondonia, Brazil (from Charlwood & Alecrim 1989)
Figure 69: Male Anopheles funestus marked with yellow fluorescent powder on their release, Furvela, Mozambique
Figure 70: Two recaptured anophelines marked with red fluouraescent powder are visible in this picture illuminated with a uv light (from Benedict et al., 2018)
Figure 71: Pattern of release and recapture data from Muheza in Tanzania. The dots represent recaptured mosquitoes and the open circles represent houses (from Gillies, 1961)
Figure 72: A) Dispersal and B) female survival data of A. gambiae from the recapture data of Gillies (1961). The solid line represents males and the broken line females. p is the probability of survival through one day
Figure 73: Movement of A. funestus and A. gambiae in Kikulukutu Namawala Tanzania. Solid arrows mosquitoes released in Area 1, Broken arrows mosquitoes released in Area 3 (from Takken et al., 1998)
Figure 74: Release pattern of A. punctulatus from the Sepik, Papua New Guinea (from Charlwood & Bryan, 1987)
Figure 75: Recapture rates of Anopheles funestus males collected exiting houses, Furvela, Mozambique (from Charlwood, 2011)
Figure 76: Map of the villages in which studies were performed in Papua New Guinea. Note that Maraga and Agan are separated by the estuary of the Gogol River. The village of Butelgut is located 25km to the north of Yagaum (from Charlwood et al., 1988)
Figure 77: Population cycles with and without controlling factors: A no external mortality factor - the population oscillates around the carrying capacity of the environment, B growth with density dependence below the carrying capacity, C Growth with a single density dependent factor, D population with density dependent and density independent mortality factors (from Hemingway 2005)
Figure 78: Risks associated with different patterns of vector numbers (from Billingsley et al., 2003)
Figure 79: ‘Boom and bust’ in A. arabiensis following rain in Tanzania. A) Rainfall, and B) numbers of A. funestus and C) numbers of A. arabiensis collected in Kikulukutu at the edge of the Kilombero Valley. The red histograms represent the proportion of the population that was parous (from Takken et al., 1998)
Figure 80: Two-week period variation in entomological and meteorological data. Top, mean mosquito densities. The values plotted are the expected numbers caught in light-traps adjusted to the mean for the sampled neighbourhoods …… Anopheles funestus A. gambiae. Bottom histogram = daily rainfall, = daily maximum temperature …. = daily minimum temperature (from Charlwood et al., 1998)
Figure 81: Numbers of male Anopheles funestus and A. gambiae s.l. in exit collections from Furvela, Mozambique and mean air temperature (from Charlwood, 2011)
Figure 82: Numbers of A. coluzzii and Cx. quinquefasciatus collected in a sentinel light-trap and mean daily temperature, São Tomé (from Charlwood et al., 2003)
Figure 83: Proportion of newly emerged Anopheles funestus with mating plugs and parous females with sacs on the four days before and after a rainstorm (from Charlwood & Braganca, 2012)
Figure 84: Distribution of malaria vectors during the dry season in the Kilombero Valley, Tanzania (from Charlwood et al., 1999)
Figure 85: The distribution of A. gambiae (in black) and A. arabiensis in and around Benin City. The stippled area shows the limit of urbanization (from Coluzzi et al., 1974)
Figure 86: Map of Namawala. The filled circles represent sampled houses and the open circles other houses in the village. The inset shows the hamlet Kikulukutu close to the Kilombero Valley
Figure 87: Density maps of a) A. gambiae s.l. and b) A. funestus from Namawala, Tanzania (from Smith et al., 1995)
Figure 88: Density maps of mosquitoes from light-trap collections, Massavasse, Mozambique. The colours show an increasing density from green to red (from Charlwood et al., 2013)
Figure 89: Map of mosquito densities from Massavasse, Mozambique obtained using tent-trap collections. The colours show an increasing density from green to red. Note that densities were, in general, greatest towards the edge of the village. (A A. funestus, B A. arabiensis, C A. tenebrosus, D Cx. quinquefasciatus, E Cx. tritaeniorhynchus, F Ms. africana) (from Charlwood et al., 2013)
Figure 90: Distribution of larvae of A. gambiae (blue) and A. arabiensis (orange), determined by PCR, close to the town of Ifakara, Tanzania (from Charlwood & Edoh, 1996)
Figure 91: Sensitivity of R0 to changes in mosquito density, biting rate, and mosquito survival calculated for the Ross-Macdonald model (based on Koella 1991). Macdonald’s formula for R0 is: ?? = ? - ? where the different parameters are m = the number of female mosquitoes per human host, a = the number of bites per mosquito per day, b = the probability of transmitting infection from an infectious mosquito to a human (per bite), c = the probability of transmission of infection from an infectious human to a mosquito (per bite), ? = the rate of recovery of humans from infectiousness, p = the daily survival of adult mosquitoes, and ? = the duration of the extrinsic cycle (the time required for the development of sporozoites from infection of the mosquito). Changes in parameter values are represented as the efficacy of shown factors relating to the original setting (e.g., an efficacy of 50% corresponds to a multiplication of m, or 1/? by 0.5; m or 1/? for the basic reproductive number linearly); therefore, this efficacy corresponds to a 50% decrease in reproductive number. Biting rate, a, enters the reproductive number quadratically, so that an efficacy of 50% in reducing this leads to reduction in R0 to 0.52 = 0.25 times its original value. Efficacy in adulticiding of 50% corresponds to a 50% reduction in survival per unit time. This enters the formula for R0 as a power function so decreases in this lead to the largest changes in R0. (figue kindly supplied by Tom Smith)
Figure 92: Oviposition cycle lengths, estimated by dissection, of Anopheles from Cambodia (from Charlwood et al., 2016)
Figure 93: A generalised schema of a female mosquito’s life history after emergence (after Gillies)
Figure 94: Ovaries of A) Anopheles and B) Culex (from Foster & Wlaker, 2002)
Figure 95: Ovariole structure (from Detinova, 1963)
Figure 96: Stages (from I to V) in the maturation and laying of an anopheline egg (from the WHO, 1975)
Figure 97: Dried ovaries of A) a nulliparous Culex quinquefasciatus B) a parous Cx. quinquefasciatus, C) a nulliparous A. arabiensis and D) a parous A. arabiensis. Note the coiled tracheoles in the nulliparous specimen
Figure 98: Large ovariolar sacs seen in an Armigeres milnensis and shrinkage of sacs seen in mosquitoes in the 24hrs following oviposition (from Charlwood & Gagal, 1985, Wilkes & Charlwood 1979)
Figure 99: A generalized schema of the information obtained by dissection of the female anophelines ovaries 99 Figure 100: A seven parous A. farauti from Papua New Guinea as identified by the dilatations on a dwarf ovariole (note the difference in size of the ovariole from a standard ovariole)
Figure 101: Possible appearance of individual follicles in a three-parous mosquito A with a sac, B a sac and a single dilatation C a sac and two dilatations and D three dilatations (from Hoq & Charlwood, 1990)
Figure 102: Photomicrograph of a two parous Ochlerotatus cantans, one ovariole having a sac and a dilatation and another having just a single sac
Figure 103: Age distribution of A. farauti from Papua New Guinea determined by dissection (from Charlwood et al., 1985)
Figure 104: Age distribution of A. farauti from three villages (Bilbil, Umuin and Maraga) from Papua New Guinea. Note the higher age specific mortality rate from Maraga
Figure 105: Survival of A. gambiae from Muheza, Tanzania follows a Gompertz distribution with an increasing force of mortality as the insects get older (from Clements and Paterson, 1981)
Figure 106: The decline in A. arabiensis and increase in sporozoite rates observed following an absence of rain in Namawala, Tanzania. The daily survival rate estimate was derived from the regression of numbers caught with days of collection (from Charlwood et al., 1995)
Figure 107: Proportion of parous Anopheles coluzzii without large ovariolar sacs from tent and light-traps (dotted line) and mean temperature, Okyereko, Ghana
Figure 108: Sac stages of Anopheles arabiensis that had died before dissection (blue histogram) and those that were alive before dissection (red histogram), Muleba, Tanzania
Figure 109: Mean number of Anopheles coluzzii collected in light-traps by house, Riboque, São Tomé (from Charlwood et al., 2003)
Figure 110: Sporozoite rates determined from light-trap collections by house from Furvela, Mozambique. The upper line is the corrected estimate according to pool size
Figure 111: The spatial distribution of the estimated basic reproductive number of P. falciparum malaria at present levels of control (RC) (from Smith et al., 2009)

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